Review

Stem = Cells and=20 Niches: Mechanisms That Promote Stem Cell Maintenance throughout = Life

Sean J. Morrison1, and Allan C. Spradling2,

1 Howard = Hughes Medical=20 Institute, Life Sciences Institute, and Center for Stem Cell Biology, = University=20 of Michigan, Ann Arbor, MI, 48109-2216, USA2 Howard = Hughes Medical=20 Institute and Department of Embryology, Carnegie Institution, Baltimore, = MD=20 21218, USA

Corresponding author
Sean J. Morrison
seanjm@med.umich.edu

Corresponding author
Allan C. Spradling
spradling@ciwemb.edu

Summary

Summary
Main=20 Text
References

Niches are local=20 tissue microenvironments that maintain and regulate stem cells. = Long-predicted=20 from mammalian studies, these structures have recently been = characterized within=20 several invertebrate tissues using methods that reliably identify = individual=20 stem cells and their functional requirements. Although similar = single-cell=20 resolution has usually not been achieved in mammalian tissues, = principles likely=20 to govern the behavior of niches in diverse organisms are emerging. = Considerable=20 progress has been made in elucidating how the microenvironment promotes = stem=20 cell maintenance. Mechanisms of stem cell maintenance are key to the = regulation=20 of homeostasis and likely contribute to aging and tumorigenesis when = altered=20 during adulthood.

Main Text

Introduction

Stem cells are emerging as one of the = fundamental=20 underpinnings of tissue biology. They allow blood, bone, gametes, = epithelia,=20 nervous system, muscle, and myriad other tissues to be replenished by = fresh=20 cells throughout life. Additional stem cells lie dormant, but can be = activated=20 at particular life cycle stages, or following injury. These potent = agents are=20 controlled within restricted tissue microenvironments known as = =E2=80=9Cniches.=E2=80=9D Until=20 recently, niches were a theoretical concept strongly supported by the=20 observation that transplanted stem cells survive and grow only in = particular=20 tissue locations. The number of such sites could be saturated, after = which=20 transferring additional stem cells provided little or no further = engraftment.=20 However, in recent years it has become possible to identify stem cells = and=20 niches with increasing precision. In this review we summarize progress = in=20 delineating stem cells and their niches, as well as in discovering the=20 mechanisms that control stem cell function. Finally, we examine how = niches=20 change with age and contribute to cancer and tissue aging.

Identifying Stem = Cells

Accurately identifying stem cells in vivo = remains the=20 biggest obstacle to progress in understanding stem cell biology. Normal = stem=20 cells and their neighboring cells within tissues can rarely be = pinpointed by=20 histological methods. Some properties that have been widely assumed to = mark stem=20 cells, such as preferential bromodeoxyuridine (BrdU) label retention = (caused by=20 an expected tendency of stem cells to divide more slowly than many of = their=20 progeny) have frequently proven to be unreliable where definitive = independent=20 markers are available (Barker et al., 2007,=20 Crittenden et al., 2006,=20 Kiel et al., 2007,=20 Margolis et al., 1995). Specific stem cell molecular markers have not been = found in most=20 tissues. However, within the relatively simple tissues of small = invertebrates=20 such as the fruit fly Drosophila, it has been possible to = genetically tag=20 individual stem cells and to document their ability to self-renew for a=20 prolonged period. Seven different types of stem cell have now been = identified=20 (Figure 1; = Table = 1).

Figure 1. Two Classes of Fly Stem Cell = Niche

(A) A stromal niche. The Drosophila male and female = germline=20 stem cells (GSCs) reside in a stromal niche. Nondividing stromal cells = (green)=20 hold the GSCs (dark pink) in place via adherens junctions (black boxes). = GSCs=20 contain a spectrosome (S) and a localized centrosome ()=20 that in the male is known to be the maternal centrosome. The GSC is = surrounded=20 by escort stem cells (ESCs) or cyst progenitor stem cells (CPCs) whose = daughters=20 (light blue) encyst the GSC daughter cell (pink).

(B) An epidermal niche. The Drosophila follicle cell stem = cell=20 (FSC) resides in an epidermal niche. The FSC is surrounded by FSC = daugher cells=20 (light blue) and also contacts the thin escort cells (light blue) that = surround=20 developing germline cysts (pink). The FSC does not contact any permanent = stromal=20 cells, but remains associated with a region of the basement membrane = (thick=20 brown line). The movement of cells is indicated by green = arrows.

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Table 1. Characterized Invertebrate Stem Cells and = Their=20 Niches

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In contrast to the ability to identify = invertebrate=20 stem cells and their niches with single-cell resolution, the relative = vastness=20 of mammalian tissues and the rarity of stem cells have conspired to make = it much=20 more difficult to confidently identify individual stem cells in vivo (Table 2). = Germline stem=20 cells lie within the basal cell layer of the seminiferous tubules (de = Rooij,=20 2001;=20 see Minireview by R.M. Cinalli et al., page 559 of this issue), = epithelial=20 stem cells reside within the bulge of hair follicles (Cotsarelis et al., = 1990,=20 Taylor et al., 2000,=20 Tumbar et al., 2004), neural stem cells reside within the lateral ventricle=20 subventricular zone of the central nervous system (Doetsch, 2003;=20 see Review by C. Zhao et al., page 645 of this issue), muscle stem = cells=20 reside among satellite cells under the basal lamina of myofibers = (Collins et=20 al., 2005,=20 Kuang et al., 2007;=20 see Review by D.J. Laird et al., page 612 of this issue), and = hematopoietic=20 stem cells (HSCs) reside within the bone marrow, close to endosteum = and/or=20 sinusoidal blood vessels (Adams et al., 2006,=20 Kiel et al., 2005;=20 see Review by S.H. Orkin and L. Zon, page 631 of this issue) (Figure 2). = In each=20 case these locations have been described as stem cell niches, and the = factors=20 that regulate the maintenance of these stem cells are beginning to be=20 identified. Yet we have little definitive information about exactly = which=20 supporting cells the stem cells interact with or which cells produce the = key=20 factors that regulate stem cell maintenance. Improvements in imaging = technology=20 and more extensive genetic analyses are needed to bring = the resolution of=20 invertebrate stem cell studies to mammalian systems.

Table 2. Examples of Well-Characterized Mouse Stem = Cell=20 Niches

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Figure 2. Hematopoietic Stem Cell Niches

(A and B) Adult hematopoietic stem cells (HSCs) reside primarily = within bone=20 marrow. Bone marrow is a complex organ containing many different = hematopoietic=20 and nonhematopoietic cells. Bony trabeculae are found throughout the = trabecular=20 zone of bone, such that many cells in this region are close to the bone = surface.=20 The interface of bone and bone marrow is known as the endosteum. = Arteries carry=20 oxygen, nutrients, and hematopoietic growth factors into the bone marrow = before=20 feeding into the venous circulation. Sinusoids are specialized venules = that form=20 a reticular network of fenestrated vessels that allow cells to pass in = and out=20 of the circulation. Shown in (B) is a magnified view of the bone marrow = showing=20 sinusoids (red), bone (gray), and hematopoietic areas (light red). = Sinusoids are=20 often associated with megakaryocytes (purple), reticular cells producing = the=20 chemokine CXCL12 (light green), and mesenchymal progenitors (white). The = bone=20 surface is covered by bone-resorbing osteoclasts (dark green) as well as = bone-lining cells that can differentiate into bone-forming osteoblasts. = HSCs=20 (blue) are found adjacent to sinusoidal blood vessels (arrows) as well = as at or=20 near the endosteum (arrowhead) (Adams et al., 2006,=20 Kiel et al., 2007,=20 Kiel et al., 2005,=20 Nilsson et al., 2001). Osteoblasts and osteoclasts elaborate factors that = regulate HSC=20 maintenance and localization (Adams et al., 2006,=20 Arai et al., 2004,=20 Calvi et al., 2003,=20 Kollet et al., 2006,=20 Zhang et al., 2003). Perivascular reticular cells and mesenchymal = progenitors have=20 also been proposed to elaborate factors that regulate HSC maintenance = (Sacchetti=20 et al., 2007,=20 Sugiyama et al., 2006).

(C and D) Low (C) and high (D) magnification views of a section = through mouse=20 bone marrow showing a CD150+CD48=E2=88=92CD41=E2=88=92Lineage=E2=88=92 HSC (white arrow = pointing to red=20 cell) adjacent to a sinusoid. This HSC is close to the endosteum (dotted = line),=20 but not detectably in contact with cells lining bone. (B, bone; V, blood = vessel;=20 orange cell, megakaryocyte; green cells, more differentiated = hematopoietic=20 cells).

(E=E2=80=93H) Four possible models of a stem cell niche (E) HSCs = (round, blue) may=20 reside in perivascular niches in which HSCs adhere to perivascular cells = but are=20 influenced by soluble factors released by nearby endosteal cells. HSCs = may=20 reside in endosteal niches, but frequently migrate through perivascular=20 environments, where the cells may be regulated by perivascular cells = (F). HSCs=20 may reside in spatially distinct endosteal and perivascular niches that = may or=20 may not be functionally equivalent (G). HSCs may reside in a single type = of=20 niche that is created by both endosteal and perivascular cells (H). = Photos=20 courtesy of Mark Kiel and Shenghui He.

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Stem Cell = Markers

Gene-expression markers have long been = sought that=20 would distinguish stem cells based on a unique underlying process. Such = markers=20 would free researchers from the experimental difficulties of identifying = stem=20 cells by lineage and simultaneously provide clues about regulatory = mechanisms.=20 Recent studies of invertebrate stem cells generally encourage this view = but=20 provide a cautionary perspective. Markers truly specific for one or = multiple=20 stem cells, as might be expected if stem cells constitute a distinctive = cell=20 =E2=80=9Ctype=E2=80=9D sharing stem cell-specific genes, have not been = found. At the level of=20 gene expression, stem cells resemble their own daughters and transit = cells more=20 than stem cells from a different lineage. However, two types of useful = makers=20 have been identified. First, stem cells sometimes contain distinctive = structures=20 related to their early state of differentiation, such as an aggregate of = endoplasmic reticulum-like vesicles (called the spectrosome) in=20 Drosophila germline stem cells (GSCs). Second, components of the=20 signaling pathways involved in stem cell maintenance and daughter cell=20 programming, for instance the proteins Dad (Kai et al., 2003)=20 or Socs36E (Bach et al., 2007)=20 in male and female GSCs, respectively, allow stem cell identification if = combined with anatomical information.

Studies of well-characterized stem cells = reveal why it=20 is difficult to use markers to initially identify unknown stem cells. = Markers of=20 primitive cells are often not fully specific for stem cells. For = example,=20 spectrosomes identical to those in GSCs also reside in primordial germ = cells,=20 and the spectrosome structure does not change fast enough during = differentiation=20 to distinguish GSCs from their initial daughters. However, spectrosome = content=20 and anatomical position together allow GSCs to be accurately identified. = Markers=20 reflecting stem cell signaling also must be supplemented with additional = information. Daughter cells may briefly retain markers of signal = reception such=20 as Dad (Kai et al., 2003). Moreover, stem cells do not simply exhibit constant = signaling=20 profiles, but rather these vary depending on the behavior of neighboring = cells=20 and their physiological environment. For example, the Notch ligand, = Delta,=20 preferentially labels most intestinal stem cells with high specificity = (Ohlstein=20 et al., 2007). However, despite the fact that a Delta-mediated signal = from the=20 intestinal stem cell to its daughter programs the daughter to = differentiate into=20 an enterocyte, Delta does not reliably mark all intestinal stem cells.=20 Intestinal stem cells are multipotent, and stem cells about to generate=20 enteroendocrine rather than enterocyte daughters lack cytoplasmic Delta. = Consequently, stem cells typically can be recognized using gene markers = only=20 after they have been identified by lineage or transplantation, and their = behavior under various conditions becomes understood.

Among mammalian tissues, the hematopoietic = system is=20 perhaps the most advanced in terms of HSC markers (see Reviews by D.J. = Laird=20 et al., page 612 and S.H. Orkin and L. Zon, page 631 of = this=20 issue). HSCs are defined based on the ability of single cells to = self-renew and=20 to provide long-term multilineage reconstitution of all major blood cell = lineages upon transplantation into irradiated mice. HSCs represent only = about 1=20 out of every 30,000 cells (0.003%) in the bone marrow (Figure 2). = Thus,=20 purifying these cells is no mean feat: even combinations of markers that = distinguish HSCs from 99.9% of other cells in the bone marrow yield = populations=20 that are only 3% pure. Nonetheless, 20 years of work has identified = combinations=20 of markers that yield cells by flow cytometry that are approximately 50% = pure=20 for HSCs (Kiel et al., 2005,=20 Matsuzaki et al., 2004,=20 Takano et al., 2004). The problem is that, until recently, these = combinations of=20 markers were too complex for the identification of HSCs by = immunofluorescence in=20 sections from hematopoietic tissues. As a result, the field usually made = inferences about the localization of HSCs in vivo using simplified = combinations=20 of markers that yielded poor or uncertain stem cell purity. This created = uncertainty about the precise location of bona fide HSCs.

Similar issues limit the characterization of = stem cell=20 niches in most mammalian tissues. Neural stem cells in the forebrain = have been=20 identified based on their ultrastructural characteristics by electron = microscopy=20 within the subventricular zone of the lateral ventricle (Doetsch et al., = 1999); however, this approach does not allow the purification = of live=20 stem cells for transplantation, and definitive markers for their = purification by=20 flow cytometry have yet to be identified (see Review by C. Zhao = et al.,=20 page 645 of this issue). Epithelial stem cells within the bulge of the = hair=20 follicle have been enriched based on expression of the glycoprotein CD34 = and=20 retention of a histone-green fluorescent protein (GFP) label (Blanpain = et al.,=20 2004)=20 (Figure 3). = However,=20 the purity of this epithelial stem cell population remains uncertain, = and these=20 markers do not work as well in certain contexts, such as after stem cell = activation (Kobielak et al., 2007). The identification of markers that permit the = purification of=20 live stem cells, irrespective of cell-cycle status, would make it = possible to=20 more fully explore the mechanisms that regulate the function of these=20 cells.

Figure 3. Niches for Epithelial Stem Cells

(A) Mouse hair follicle niche. After the first and all subsequent = hair=20 cycles, stem cells located within the bulge region of the hair follicle = give=20 rise to new matrix cells located at the base of the hair and adjacent to = the=20 dermal papilla that support hair growth. Bulge cells can also = reconstitute the=20 sebaceous gland. The same or other stem cells can migrate out of the = bulge and=20 participate in epidermal wound repair. The identity of individual stem = cells=20 within the bulge and the nature of their niches have not yet been=20 determined.

(B) Gut epithelial stem cell niche. Gut epithelial stem cells were = thought to=20 be the =E2=80=9C+4 cells=E2=80=9D (red) that reside near the base of the = crypts (Potten et al.,=20 1990). However, a recent study demonstrated that Lgr5+ crypt base columnar cells = (yellow)=20 are actually the stem cells that both self-renew and give rise to the=20 differentiated cells that constantly repopulate the villi (Barker et = al., 2007). Although the niche itself has not yet been = characterized, these=20 results imply that the region at the base of the crypt comprises a niche = for gut=20 epithelial stem cells. Potential niche components include the paneth = cells that=20 are also present at the base of the crypt as well as the mesenchymal, = vascular,=20 neural, and hematopoietic cells that surround the crypt.

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Identification of = Stem Cells=20 through Lineage Analysis

Recent advances in the application of = Cre-recombinase=20 fate mapping in mice have begun to provide insights into the nature of = mammalian=20 stem cells. Fate-mapping studies of muscle satellite cells (Kuang et = al., 2007), spermatogonial stem cells (Nakagawa et al., 2007), epidermal stem cells (Clayton et al., 2007), and intestinal stem cells (Barker et al., 2007)=20 have clarified the relationship between stem cells and their daughters, = as well=20 as some of the mechanisms that regulate tissue homeostasis. = Hair-follicle stem=20 cells have also been fate mapped, demonstrating that cells within the = bulge give=20 rise to all of the epithelial cells within the hair follicle (Morris et = al.,=20 2004)=20 (Figure 3A) = and can=20 even transiently contribute to wound repair in the epidermis (Ito et = al., 2005). Neural stem cells in the forebrain subventricular zone = have been=20 fate mapped using a variety of approaches that have demonstrated = regional=20 heterogeneity in the embryonic origin, developmental potential, and fate = of=20 these cells (Merkle et al., 2007,=20 Young et al., 2007). These studies have provided considerable new insights = into the=20 biology of mammalian stem cells, though with certain notable exceptions = (Barker=20 et al., 2007,=20 Kuang et al., 2007)=20 these approaches have usually not made it possible to image mammalian = stem cells=20 within their niches in a way that clearly distinguishes these cells from = their=20 progeny.

The recent identification of intestinal = epithelial=20 stem cells by Clevers and colleagues illustrates the power of both = single-cell=20 resolution and lineage marking for the identification of a mammalian = stem cell=20 niche in vivo (Barker et al., 2007)=20 (Figure 3B). = These=20 authors discovered that a Wnt target gene, Lgr5, was restricted = in=20 expression within the intestinal epithelium to columnar epithelial cells = at the=20 base of the crypts. Fate mapping of these cells with a Cre knockin = allele of=20 Lgr5 demonstrated that individual Lgr5-positive crypt base columnar = cells=20 self-renew in vivo as well as giving rise to all intestinal epithelial = lineages.=20 This represents a critical advance as studies of intestinal epithelial = stem=20 cells have long been hampered by a lack of markers and clear functional = assays.=20 Moreover, a large body of older literature had provisionally identified = the=20 intestinal epithelial stem cells (the so-called +4 cells) based on more = indirect=20 methods, such as BrdU label retention, in a different position just = above the=20 columnar cells in the crypts (Potten et al., 1990). Thus, this study clarifies the identity of intestinal = epithelial=20 stem cells and implicates a different microenvironment (lower in the = crypt) as=20 their niche.

Cell Culture = Assays

The difficulty associated with identifying = markers is=20 not the only factor limiting our ability to identify mammalian stem cell = niches.=20 In some tissues, the functional definition for what constitutes a stem = cell is=20 also uncertain. Central nervous system stem cells have generally been = identified=20 based on their ability to self-renew and to form multilineage colonies = in=20 culture. However, at least some restricted progenitors in the nervous = system can=20 be reprogrammed by relatively short periods of culture to acquire = multipotency;=20 some of the cells that undergo multilineage differentiation in culture = might not=20 be capable of multilineage differentiation in vivo (Gabay et al., 2003,=20 Kondo et al., 2000). Moreover, some neural stem cell populations that have = been=20 considered homogeneous based on experiments performed in culture are = quite=20 heterogeneous in terms of fate and even developmental potential in vivo = (Gabay=20 et al., 2003,=20 Merkle et al., 2007). Culture environments sometimes alter the patterning of = cells in=20 ways that modify their fates and even their developmental potentials = (Joseph et=20 al., 2005). Similar concerns apply to other mammalian stem cells = that have=20 been identified and studied primarily based upon their behavior in = culture or=20 after expansion in culture.

This problem has been addressed in neural = crest stem=20 cells that give rise to the peripheral nervous system in the developing = embryo=20 by using flow cytometry to prospectively identify and isolate the neural = crest=20 stem cells that are capable of forming multilineage colonies in culture = (Bixby=20 et al., 2002,=20 Morrison et al., 1999). Prospective identification means that the uncultured = stem cells=20 can be distinguished from other cells based on marker expression, making = it=20 possible to study these cells in vitro or in vivo. Prospective = identification=20 thus made it possible to inject uncultured rat neural crest stem cells = into the=20 neural crest migration pathway of developing chick embryos. The ability = of these=20 cells to migrate throughout the chick peripheral nervous system and to = give rise=20 to diverse types of rat neurons and glia demonstrated that this broad=20 developmental potential was not acquired in culture (Bixby et al., = 2002,=20 Morrison et al., 1999). This work demonstrates that it is possible to = prospectively=20 identify and isolate by flow cytometry highly purified, uncultured stem = cells=20 from solid mammalian tissues, making it possible to study the stem cells = as they=20 exist in vivo, rather than after they have changed their properties in=20 culture.

Identifying = Niches

A niche consists of a local tissue = microenvironment=20 capable of housing and maintaining one or more stem cells. However, use = of the=20 term niche continues to vary widely, and in some cases is applied so = broadly as=20 to be almost devoid of meaning. Perturbing a precisely identified stem = cell or=20 its surroundings allows the existence, size, and regulatory properties = of a=20 corresponding niche to be revealed. Ideally, a candidate niche should be = transiently depleted of its full complement of stem cells and then shown = to take=20 up and maintain a newly introduced stem cell. This provides evidence = that the=20 niche microenvironment is localized and not a general tissue property. = For=20 example, showing that GSCs are maintained at the gonad tips by local = signals=20 suggested the existence of a niche (Kiger et al., 2001,=20 Tulina et al., 2001,=20 Xie et al., 1998); but demonstrating that new stem cells can be = introduced and=20 maintained there provided the clearest evidence (Brawley et al., 2004,=20 Kai et al., 2004,=20 Xie et al., 2000). Although regulation by widely diffusible signals such = as insulin=20 is also critically important (Drummond-Barbosa et al., 2001), we suggest that the term niche be reserved for = the=20 specialized local microenvironments where stem cells reside and that = directly=20 promote the maintenance of stem cells. This distinction is highly = relevant to=20 mammalian tissues. For example, it remains uncertain whether endosteal = cells,=20 such as osteoblasts and osteoclasts, influence HSC numbers in the bone = marrow=20 (Calvi et al., 2003,=20 Zhang et al., 2003)=20 by promoting the maintenance of HSCs that reside in direct contact with = these=20 cells, or by secreting factors that act at a distance, directly or = indirectly=20 regulating HSCs that are localized to other nearby = microenvironments (Adams=20 et al., 2006,=20 Kiel et al., 2007).

Two basic types of niche have been = recognized. The=20 niches at the tips of adult Drosophila female and male gonads are = examples of =E2=80=9Cstromal cell=E2=80=9D niches (Figure 1A). = These=20 niches develop whether or not stem cells are present, and maintain their = morphology after stem cell loss. Distinct =E2=80=9Cstromal=E2=80=9D cell = types=E2=80=94cap cells and hub=20 cells, respectively=E2=80=94initially guide niche morphogenesis and = continue to directly=20 contact and signal to resident stem cells. In contrast, the stem cells = for=20 ovarian follicle cells (FSCs) reside in =E2=80=9Cepithelial=E2=80=9D = niches devoid of=20 specialized cells (Figure 1B). = Niche-resident FSCs contact only migratory developing cells, including = their own=20 progeny (Nystul et al., 2007). Yet, precisely two FSC niches exist within each = ovariole at=20 sites that remain constant despite this dynamic environment, possibly = due to=20 direct contact between the FSCs and a fixed region of basement membrane. = Both=20 types of niches depend on cell-cell junction molecules (Song et al., = 2002,=20 Song et al., 2002). Epithelial niches may also be limited by the presence = of=20 specific molecules within the extracellular matrix or on nearby tissue = cells,=20 but this remains to be proven.

Currently well-characterized niches vary in = size and=20 complexity (Table 1). The = FSC niche=20 contains a single stem cell of a single type (Nystul et al., 2007). In contrast, the niches at the tip of the ovariole and = testis=20 are larger and house two types of stem cell. Escort stem cells and cyst=20 progenitor cells are squamous epithelial stem cells that contact the = GSCs in the=20 female and male, respectively, and coordinate to produce cysts = containing=20 daughters of both stem cell types. The ovarian niche usually contains 2 = GSCs and=20 4=E2=80=938 escort stem cells (Decotto et al., 2005), whereas 10=E2=80=9315 GSCs and 20=E2=80=9330 cyst = progenitor cells can occupy=20 the testis niche (Gonczy et al., 1997,=20 Wallenfang et al., 2006). The GSC niche at the tip of the gonad in = hermaphrodites of the=20 worm Caenorhabditis elegans appears to be even larger and may = harbor as=20 many as 50 developmentally equivalent GSCs (Crittenden et al., 2006).

Facultative, = Distributed=20 Niches for Mammalian Stem Cells

The small numbers of stem cells in some = invertebrate=20 niches are similar to what has been observed in mammalian skeletal = muscle.=20 Muscle satellite cells, which include the stem cells of skeletal muscle, = are=20 scattered as individual cells under the basal laminas of different = muscle fibers=20 (Collins et al., 2005,=20 Kuang et al., 2007). This suggests that at least some mammalian stem cells = can reside=20 as individual cells within niches distributed throughout tissues. In = other=20 cases, multiple stem cells are clustered together within relatively = small=20 substructures within tissues, as in the bulge of hair follicles = (Cotsarelis et=20 al., 1990)=20 (see Figure 3A) = or in the=20 forebrain subventricular zone (Doetsch et al., 1999). However, the challenge associated with definitively=20 distinguishing the stem cells from their progeny in these tissues makes = it=20 difficult to assess the extent to which stem cells are clustered = together as=20 opposed to being interspersed among other cells.

GSCs in Drosophila and C. = elegans occupy=20 a single spatially invariant niche throughout adult life. This is also = seen in=20 some mammalian tissues, for example in the central nervous system where = neural=20 stem cells reside throughout postnatal life in the lateral ventricle=20 subventricular zone (Doetsch, 2003)=20 and dentate gyrus of the hippocampus (Palmer et al., 1997;=20 see Review by C. Zhao et al., page 645 of this issue). However, = other=20 mammalian tissues are much more dynamic with respect to the locations = where stem=20 cells are sustained. A good example is the hematopoietic system. Under=20 steady-state conditions, HSCs reside and undergo hematopoiesis in the = bone=20 marrow (Figure 2). = SLAM=20 family proteins have facilitated the purification of HSCs: simple = combinations=20 of these markers can be used to identify HSCs by immunofluorescence in = tissue=20 sections (Kiel et al., 2005). Staining of sections through adult hematopoietic = tissues using=20 these markers revealed the presence of individual HSCs around bone = marrow=20 sinusoids (specialized blood vessels that allow cells to pass in and out = of=20 circulation) as well as near the endosteum (the interface of bone and = marrow).=20 It remains uncertain whether both locations represent niches and, if so, = whether=20 they are spatially distinct niches or whether perivascular cells and = endosteal=20 cells collaborate to form a common niche (Figure 2).=20 Histological examination has not yet revealed anatomically specialized = regions=20 of sinusoids or endosteum that seem uniquely capable of hosting HSCs. = Rather,=20 individual HSCs appear to be able to occupy facultative niches scattered = over=20 the surface of many sinusoids or near much of the vast endosteal surface = of=20 trabecular bone (Arai et al., 2004,=20 Kiel et al., 2005,=20 Nilsson et al., 2001,=20 Sugiyama et al., 2006,=20 Zhang et al., 2003).

The existence of facultative niches in the=20 hematopoietic system may be critical to facilitate migration of HSCs = (see Review=20 by D.J. Laird, page 612 of this issue). HSCs appear to constantly = recirculate=20 from one bone marrow compartment to another (for example, from femur to = tibia)=20 (Wright et al., 2001). It would appear that these recirculating HSCs move = from one=20 facultative niche to another, stochastically selecting among a wide = variety of=20 locations that are capable of supporting their maintenance. Of course, = it=20 remains to be determined whether all of these endosteal and sinusoidal = locations=20 actively promote the maintenance of HSCs, or whether HSCs simply pass = through=20 some of these locations during their migration.

This ability to activate facultative niches = may=20 underlie the remarkable capacity of the hematopoietic system to = dramatically=20 expand stem cell numbers and hematopoiesis in response to stress. The = spleen and=20 liver contain few stem cells and little hematopoiesis under normal = conditions,=20 but stresses that induce increased hematopoiesis can activate high = levels of=20 extramedullary hematopoiesis in these organs. For example, hematopoietic = malignancies that displace bone marrow hematopoiesis often lead to the=20 relocation of most hematopoiesis to the spleen and liver. When this = occurs,=20 greatly expanded numbers of HSCs and other hematopoietic progenitors can = be=20 found within these organs. This demonstrates that these organs are able = to=20 activate facultative niches that can support the long-term maintenance = of HSCs=20 and hematopoiesis. The precise nature of these niches remains largely=20 uncharacterized, but as in bone marrow, HSCs within the hematopoietic = spleen are=20 observed primarily around sinusoids (Kiel et al., 2005), raising the possibility of a perivascular niche. = The=20 ability to activate facultative niches is not limited to the = hematopoietic=20 system as injury of adult skin can lead to the formation of new hair = follicles=20 that become colonized by stem cells (Ito et al., 2007). The ability to dynamically redistribute and activate = new niches=20 may be an important strategy underlying the regenerative capacity of=20 metazoans.

Niche Mechanisms: = Primary=20 Maintenance Signals

All three characterized GSC niches maintain = resident=20 stem cells in an undifferentiated state using a major short-range = intercellular=20 signal. Local signaling both constrains the total number of stem cells = that can=20 be maintained and in the Drosophila GSC niches ensures that one = of the=20 two daughters of each stem cell division will lie outside the niche and = will=20 differentiate (Figure 4A). = In the=20 testis, JAK/STAT signal reception is restricted primarily by the = localized=20 expression of the Unpaired ligand in hub cells (Kiger et al., 2001,=20 Tulina et al., 2001). Similarly, localized Unpaired expression in the = terminal=20 filament and cap cells appears to stimulate expression of the bone = morphogenetic=20 protein (BMP) ligand within somatic cells of the ovarian niche, leading = to a=20 restricted zone of high BMP-signaling capacity (L=C3=B3pez-Oneiva et = al., 2008). C. elegans GSCs require Notch signals from the = distal tip=20 cells to be maintained (Kimble et al., 2007). Given that the lag-2 ligand is produced in the distal = tip cell,=20 it is available only at the distal end of the gonad, which plausibly = accounts=20 for the size of the niche. It is not known if the length of the = cytoplasmic=20 processes of the distal tip cell that extend from the gonad tip are = responsible=20 for determining how far the niche extends (reviewed in Kimble et al., = 2007).

Figure 4. Two Types of Stem Cell Asymmetry

(A) The preprogrammed differentiation of the first class of stem = cell, which=20 includes Drosophila GSCs, = is only=20 repressed by a local signal (red arrow) generated by nearby stromal = cells.=20 Daughter cells become derepressed by becoming displaced from the = repressive=20 signal within the niche and they then differentiate. Mammalian GSCs may = use a=20 related mechanism, as they are preferentially found near (but not = attached to)=20 hormone-producing interstitial cells (Yoshida et al., 2007).

(B) A second class of stem cell, such as the Drosophila intestinal stem = cell,=20 requires signals to differentiate. Intestinal stem cells divide = asymmetrically=20 such that only one daughter cell receives a (Notch) signal that = specifies its=20 fate (Ohlstein et al., 2007). Asymmetric partitioning of Notch activity also = maintains neural=20 progenitors in the fly and the mouse (Lee et al., 2006,=20 Petersen et al., 2004).

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The identities of the key factors that = maintain=20 mammalian stem cells and the cell types that produce them are less well = known.=20 For example, Hedgehog signaling is required to maintain neural stem = cells in the=20 forebrain subventricular zone, but it is unclear exactly what cells are=20 producing Hedgehog, whether they are a specialized niche component, or = whether=20 expression is generalized throughout the subventricular zone (Ahn et = al., 2005,=20 Balordi et al., 2007). Complex models are often proposed to describe HSC = niches, but=20 most elements of these models have not been tested genetically. In = contrast,=20 there is strong genetic evidence for the critical roles played by Wnt = signaling=20 and BMP signaling in the regulation of epithelial stem cells in the hair = follicle, although the sources of Wnts and BMPs remain uncertain = (Blanpain et=20 al., 2006). One limitation is that the lack of single-cell = resolution in the=20 imaging of most mammalian stem cells in vivo creates uncertainty about = the=20 identity of the supporting cells with which stem cells interact. The = size and=20 complexity of mammalian tissues also makes it daunting to conditionally = delete=20 regulatory genes from each potential supporting cell to directly = determine the=20 source of critical signals.

The hematopoietic system poignantly = illustrates this=20 challenge as most or all of the factors that regulate HSC maintenance = are=20 expressed by multiple cell types in different regions of the bone = marrow. The=20 chemokine CXCL12 (SDF-1) is required for the maintenance of bone marrow = HSCs and=20 is expressed by both perivascular and endosteal cells (Kollet et al., = 2006,=20 Sacchetti et al., 2007,=20 Sugiyama et al., 2006). Are there multiple, redundant sources of CXCL12 in the = bone=20 marrow, or is one cell type the major source of CXCL12 for HSC = maintenance?=20 Angiopoietin-1, a factor proposed to regulate HSC quiescence (Arai et = al.,=20 2004), is another example. Angiopoietin-1 expression has been = attributed to both osteoblasts at the endosteum (Arai et al., 2004)=20 and to perivascular mesenchymal progenitors (Sacchetti et al., 2007). The complexity of the bone marrow means that it will = ultimately=20 be necessary to conditionally delete factors from a number of different = cell=20 types to determine which cells play major roles in regulating HSC = maintenance.=20 So far, none of the factors that are thought to regulate HSC maintenance = have=20 been conditionally deleted from particular cell types to determine which = cell is=20 the physiologically important source.

Niche Mechanisms: = Additional=20 Signals

In addition to a major primary signal that = acts=20 directly on stem cells to promote their maintenance, many niches and = stem cells=20 have been shown to depend on additional signals whose action is less = well=20 understood and that may function indirectly to maintain niche integrity. = For=20 example, besides a primary Hedgehog signal (Forbes et al., 1996), the FSC niche requires Wingless (Wg) and BMP signaling = (Kirilly=20 et al., 2005,=20 Song et al., 2003). The male GSC niche, in addition to JAK/STAT signaling, = requires=20 the BMP pathway (Kawase et al., 2004,=20 Shivdasani et al., 2003). Detailed studies of the Drosophila GSC niches = reveal=20 hierarchies among the multiple signals. JAK/STAT signaling lies at the = top and=20 is used by key niche cells to stimulate other niche cells to signal GSCs = via the=20 BMP pathway (Decotto et al., 2005,=20 L=C3=B3pez-Oneiva et al., 2008). In contrast, at least in the ovary, Notch-mediated = signals are=20 sent from GSCs to niche cells (Song et al., 2007,=20 Ward et al., 2006). Niches inherently involve multiple interacting cell = types; there=20 are several conversations going on simultaneously. The male and female = GSC=20 niches use the same two major signaling pathways, but in the male, = JAK/STAT=20 signaling acts directly on GSCs, whereas in females it acts only = indirectly=20 (Decotto et al., 2005,=20 L=C3=B3pez-Oneiva et al., 2008). This may represent an example of how niche circuitry = has adapted=20 to the different regulatory requirements of male versus female gamete=20 production. Finally, some niche signals function to program daughter = cells=20 rather than to regulate the stem cells themselves (Figure 4B).<= /P>

The regulation of secondary niche signals = may have=20 implications for the recovery of mammalian tissues from stress. In the=20 hematopoietic system, Notch signaling (Calvi et al., 2003)=20 and Wnt signaling are sufficient to promote adult HSC self-renewal in = culture=20 (Reya et al., 2003,=20 Willert et al., 2003). Yet, in vivo, conditional deletion of the relevant = Notch=20 receptor and ligand (Mancini et al., 2005)=20 or conditional deletion of =CE=B2-catenin and =CE=B3-catenin (Koch et = al., 2007)=20 does not affect adult HSC maintenance. One possibility is that redundant = signals=20 promote HSC self-renewal in vivo such that maintenance of the tissue = does not=20 depend upon any one signal. Along these lines, Notch and Wnt signaling = may be=20 physiologically necessary for recovery from certain stresses but not for = adult=20 HSC maintenance under steady state conditions. Distributing = responsibility for=20 HSC maintenance across multiple primary and secondary signals, each of = which is=20 more or less important under different conditions, would confer = flexibility and=20 robustness.

Niche Mechanisms: = Asymmetric=20 Division

Niches also share a requirement for a system = to ensure=20 that stem cells remain in the niche following stem cell division. In all = of the=20 characterized invertebrate niches except for the C. elegans = niche, stem=20 cell divisions are usually asymmetric: one daughter cell remains in the = niche=20 and one exits and differentiates (see Review by J.A. Knoblich, page 583 = of this=20 issue). Two basic mechanisms for ensuring asymmetry are known: daughter=20 derepression and daughter induction (Figure 4). = In=20 addition to maintaining stem cells during division, stem cell niches = must=20 prevent external cells from gaining entry and displacing the resident = stem cells=20 (Nystul et al., 2007). The molecular basis of this exclusion remains poorly = understood,=20 but the need to discharge daughters without admitting competitors may = have=20 contributed to the evolution of niche structure as well as=20 self-/nonself-recognition by the immune system (Laird et al., 2005).

It remains unclear whether mammalian stem = cells=20 sustain themselves by undergoing asymmetric divisions that leave one = stem cell=20 within the niche while a second daughter exits to differentiate. The = divisions=20 of fetal progenitors in the nervous system (Gotz et al., 2005)=20 and skin (Lechler et al., 2005)=20 have been analyzed, suggesting that these early progenitors undergo = symmetric=20 and asymmetric divisions during the course of organogenesis. However, it = remains=20 technically difficult to directly image the divisions of rare stem cells = within=20 adult niches. For example, in the hematopoietic system, stem cells = represent=20 only 0.003% of cells, and only 2% of these cells are actively dividing = at any=20 one time. Finding these cells is like looking for a needle in a = haystack.=20 Nonetheless, a recent fate-mapping study of muscle satellite cells = showed that a=20 subset of these cells are Pax7⁺Myf5^=E2=88=92 stem = cells that=20 undergo asymmetric self-renewing divisions on muscle fibers, giving rise = to a=20 basal Pax7⁺Myf5^=E2=88=92 stem cell daughter and an = apical=20 Pax7⁺Myf5⁺ satellite cell with a more restricted=20 proliferative potential (Kuang et al., 2007). Overall, the evidence suggests that mammalian stem = cells employ=20 both symmetric and asymmetric divisions to regulate their numbers and = tissue=20 homeostasis, and that neither mechanism is likely to be constitutively = used as a=20 way of sustaining the niche (Morrison et al., 2006).

Maintaining Stem = Cell=20 Vitality: Hierarchies, Immortal Strands, and Competition

A longstanding goal has been to identify = biological=20 processes that promote a stem cell's ability to self-renew over the long = lifespan of metazoans such as humans. DNA damage occurs each time the = genome is=20 replicated, and inactivation of DNA repair pathways frequently leads to=20 premature stem cell depletion, resembling premature aging (Ito et al., = 2004;=20 see Review by D. Rossi et al., page 681 of this issue). = Mammalian stem=20 cells have surveillance mechanisms that detect unresolved DNA damage and = that=20 eliminate the cells in which this occurs, possibly by activation of the = tumor=20 suppressor proteins p53 or Rb leading to senescence (Collado et al., = 2007). The increased incidence of cancer observed in response = to=20 mutations that inactivate these senescence mechanisms suggests that = senescence=20 is induced to avoid carcinogenesis (see Review by D. Rossi=20 et al.).

Organizing cell production into a stem cell = hierarchy=20 can greatly decrease the maximum number of cell divisions stem cells = must=20 undergo. For example, a set of reserve stem cells might only replicate=20 periodically, whereas their daughters are used to replenish a set of=20 transit-amplifying progenitors that function during the remainder of = each cycle.=20 Despite these theoretical advantages, systems that maintain a true = hierarchy=20 like that in the hair follicle appear uncommon. The crypt base columnar = cells in=20 the mouse intestine divide at about the same rate as downstream cells = and=20 continue to divide throughout life (Barker et al., 2007). Most, if not all, HSCs simultaneously contribute to=20 hematopoiesis (Harrison et al., 1987), although these cells give rise to at least two = populations of=20 more rapidly dividing multipotent progenitors with limited self-renewal=20 potential, creating a hierarchy of multipotent progenitors = (Morrison et=20 al., 1997;=20 see Review by S.H. Orkin and L. Zon). The model invertebrate stem cells = studied=20 to date also divide at about the same rate as cells farther down the=20 lineage.

Asymmetrically dividing stem cells have been = proposed=20 to slow their accumulation of mutations by selectively segregating newly = synthesized DNA strands to differentiating daughter cells, while = retaining older=20 DNA strands in the stem cell daughters (Cairns, 1975). Experimental evidence has been provided in support of = this=20 =E2=80=9Cimmortal strand hypothesis=E2=80=9D in a variety of systems = (reviewed in Rando, 2007), although these have tended to be systems in which it = is not yet=20 possible to definitively distinguish stem cells from other types of = progenitors.=20 Analyses of highly purified HSCs (Kiel et al., 2007)=20 and C. elegans germline stem cells (Kimble et al., 2007)=20 failed to detect any evidence of asymmetric segregation of older and = younger DNA=20 strands. These studies indicate that asymmetric strand segregation = cannot be a=20 general feature of stem cells, though it may occur in some systems. = Critical=20 questions are whether asymmetric strand segregation occurs in stem cells = or in=20 other progenitors from these systems and whether this process really = serves to=20 slow the accumulation of mutations or whether it serves a very different = purpose.

Stem cell replacement has recently been = suggested as a=20 mechanism by which damaged or prematurely differentiated stem cells are=20 selectively removed from their niches (Nystul et al., 2007). Some wild-type invertebrate stem cells are regularly = displaced=20 from their niches (Margolis et al., 1995); the ability to label mammalian stem cell lineages now = reveals=20 that certain mammalian stem cell types may undergo a similar fate = (Nakagawa et=20 al., 2007). The stem cell supplying the replacement may lie nearby = (Xie et=20 al., 2000,=20 Jin et al., 2008), or a daughter cell may migrate over a distance, = suggesting that=20 it can actively home to an appropriate niche (Nystul et al., 2007). Competence to serve as a replacement stem cell = persists in=20 daughter cells for at least three divisions downstream from male and = female=20 Drosophila GSCs (Brawley et al., 2004,=20 Kai et al., 2004). However, for stem cell replacement to serve as a=20 damage-reduction mechanism, it must be shown that wild-type daughter = cells=20 preferentially replace stem cells with recently acquired deleterious = mutations.=20 Differences in adhesion, and to a lesser extent cellular growth rate, = determine=20 the replacement hierarchy of GSCs (Jin et al., 2008). Given that adhesion declines following the onset of=20 differentiation, the system may ensure the replacement of stem cells = that have=20 begun to differentiate prematurely.

Molecular Asymmetry = during=20 Stem Cell Division

The dramatic divergence in the fates of a = stem cell's=20 two daughters has spurred many searches for molecular asymmetries at = mitosis=20 (reviewed in Morrison et al., 2006). Cells are capable of asymmetrically segregating = proteins, RNAs,=20 organelles, DNA, and damaged molecules. The existence of asymmetric = inheritance=20 during stem cell division is not sufficient to demonstrate function, = however.=20 The spectrosome is preferentially retained in the stem cell at division, = yet=20 genetic disruption of the spectrosome does not affect GSC maintenance or = division but does prevent progeny germ cells from differentiating = properly.=20 Consequently, the challenge has been to identify asymmetries at stem = cell=20 division and show that they are functionally important for the outcome = of=20 division. One good example is the asymmetric segregation of atypical = protein=20 kinase C among asymmetrically dividing Drosophila neuroblasts: = cells that=20 inherit atypical protein kinase C inherit stem cell identity (Lee et = al., 2006).

One of the best-established asymmetries of = stem cell=20 division with an important functional role is spindle orientation. = Regulated=20 spindle orientation during stem cell division ensures that daughters end = up in=20 different signaling environments, as is the case for Drosophila = GSCs.=20 Programmed changes in divisional orientation figure prominently during=20 neuroblast and sensory organ precursor development (reviewed in Rogers = et al.,=20 1994). The genetic basis for this orientation has been = extensively=20 studied (Siller et al., 2006)=20 and has been shown to play a role in cell-fate determination (Egger et = al.,=20 2007). In the Drosophila testis, the GSC normally = divides=20 perpendicular to the hub. This ensures that one cell will remain = attached to the=20 hub and will continue as a stem cell, while the other will receive less = Unpaired=20 signal from the hub and will differentiate into a gonialblast. When the = normal=20 spindle orientation in GSCs is disrupted, daughter cell fates are = frequently=20 altered (Yamashita et al., 2003).

Other stem cells regulate spindle = orientation using=20 different mechanisms. GSCs and escort stem cells in the = Drosophila ovary=20 divide away from the cap cells, either by a specific system of = divisional=20 orientation (Deng et al., 1997)=20 or according to the balance of mechanical and adhesive forces in the = vicinity of=20 the cap cells. Such an orientation ensures that the downstream daughter = (the=20 prospective cystoblast) receives a lower BMP signal than the cap = cell-associated=20 daughter (the prospective GSC) leading to the derepression of the = cystoblast=20 determinant bam. However, the gene products that function in = spindle=20 orientation in male GSCs such as APC2 are not observed in female GSCs = (reviewed=20 in Fuller et al., 2007). Intestinal stem cells in Drosophila divide in a = programmed direction with respect to the basement membrane (Ohlstein et = al.,=20 2007)=20 but orient their spindles about 30=C2=B0 =C2=B1 15=C2=B0 from parallel. = Neither the genetic=20 basis nor the significance of this directional control is currently = known. FSCs=20 also divide away from the basement membrane, and also at an angle less = than 90=C2=B0=20 (Nystul et al., 2007).

The Immortal = Centrosome=20 Hypothesis

Spindle orientation in Drosophila = depends on=20 epithelial or planar cell polarity, G protein signaling, and the actin=20 cytoskeleton. Specific proteins and RNAs can be segregated cortically to = positions where they will be inherited primarily by one daughter or the = other.=20 Differences associated with the centrosomes can also be brought into = play. In=20 principle, inherent structural differences between the maternal = centrosome and=20 daughter centrosomes render every cell division asymmetric. After the=20 contractile ring forms, cell abscission requires that extracellular = vesicles=20 generated in just one of the cells fuse to the midbody ring (Gromley et = al.,=20 2005). Centriolin anchors complexes required for this vesicle = fusion=20 and integrates fusion with abscission. It is easy to see how such = differences=20 might be amplified and utilized to differentially program daughter cell = fates.=20 For example, the recycling endosome segregates asymmetrically in = association=20 with one of the two centrosomes in sensory organ precursors, biasing = Notch=20 signal reception (Emery et al., 2005). Such a mechanism might explain the differential = stability of=20 Delta ligand in the daughters of dividing intestinal stem cells = (Ohlstein et=20 al., 2007).

The Drosophila male GSCs = preferentially inherit=20 and retain the maternal centrosome as long as they remain in the niche.=20 Meanwhile, the daughter centrosome migrates to the opposite pole of the = cell=20 during division and is inherited by the daughter cell fated to = differentiate=20 (Yamashita et al., 2007). During this period, the GSCs divide perpendicular to = the hub due=20 to the association of the mother centrosome with the APC protein = located at=20 the GSC-hub cell junction (Yamashita et al., 2003). Maternal centrosomes support a more robust microtubule = array=20 that facilitates the association of the GSCs with the hub during = interphase,=20 allowing daughter centrosomes to migrate to the opposite side of the = cell prior=20 to division. This ensures that one pole of the spindle is adjacent to = the hub,=20 and that the spindle orients perpendicular to the niche, such that one = daughter=20 cell remains within the niche and the other daughter cell is displaced = from the=20 niche (and therefore fated to differentiate). The discovery that male = GSCs=20 contain an =E2=80=9Cimmortal=E2=80=9D centrosome raises the possibility = that preferential=20 centrosome inheritance is a conserved stem cell mechanism. It remains = unclear,=20 however, whether other stem cells exhibit this same behavior or whether = maternal=20 centrosome retention by GSCs is part of the cause or simply an effect of = its=20 spindle orientation mechanism.

Niches in Disease: = Cancer Stem=20 Cell Niches

There is abundant evidence that the normal = cells that=20 surround and infiltrate tumors secrete factors that promote the growth = and=20 progression of cancer (Tlsty et al., 2006). In this regard, neoplastic cells do not fundamentally = differ=20 from normal progenitors in the sense that they remain partially = dependent upon=20 environmental factors that are synthesized by other cells. A striking = example of=20 this comes from neurofibromatosis in which tumors arise from Schwann = cells in=20 peripheral nerves that lack neurofibromin (Nf1). Tumor = formation=20 by Nf1-deficient Schwann cells is greatly facilitated by clonally = unrelated Nf1^+/=E2=88=92 heterozygous cells in the = environment, such=20 as fibroblasts and mast cells, that are recruited to the tumor (Yang et = al.,=20 2003,=20 Yang et al., 2006). Nf1-deficient Schwann cells are less = tumorigenic in=20 wild-type environments, apparently because wild-type fibroblasts and = mast cells=20 are not recruited as efficiently or are less able to secrete factors = that=20 promote tumor growth (Zhu et al., 2002). Similar phenomena are observed in the hematopoietic = system where=20 myeloproliferative disease can arise as a result of mutations that only = affect=20 the bone marrow microenvironment and not the hyperproliferative = hematopoietic=20 cells themselves (Walkley et al., 2007). Alternatively, myeloproliferative disease may arise = due to=20 mutations in both the hyperproliferative hematopoietic cells and in=20 nonhematopoietic cells in the environment (Walkley et al., 2007). Beyond affecting tumor growth, normal cells can also = regulate=20 metastasis: for example, mesenchymal cells in or around tumors can = increase the=20 metastasis of breast cancer cells (Karnoub et al., 2007). These studies demonstrate profound effects of = unrelated cells in=20 the environment on the behavior of cancer cells.

Over the past several years, it has become = clear that=20 the growth of at least some cancers is driven by cancer stem cells, = particularly=20 malignant cancer cells that are more tumorigenic than other cancer cells = (Pardal=20 et al., 2003,=20 Reya et al., 2001). This means that many cancers are organized = hierarchically, much=20 like normal tissues, with infrequent stem cells at the top of the = hierarchy that=20 both self-renew to form more cancer stem cells and undergo epigenetic = changes=20 (=E2=80=9Cdifferentiate=E2=80=9D) to form phenotypically diverse cancer = cells with limited=20 proliferative potential. The tumorigenic cancer stem cells often have = phenotypic=20 and functional characteristics similar to normal stem cells in the same = tissue=20 (Bonnet et al., 1997,=20 Lessard et al., 2003,=20 Singh et al., 2004). This raises the question of whether cancer stem cells = depend=20 upon specialized microenvironments for their maintenance, just like = normal stem=20 cells.

For the most part, it has not yet been = possible to=20 address this question carefully because we are still trying to identify = markers=20 that definitively distinguish cancer stem cells from normal cells and = other=20 cancer cells. However, there is some evidence that supports this = proposition in=20 the context of brain tumors. Endothelial cells secrete factors that = promote the=20 self-renewal of normal neural stem cells in culture (Shen et al., 2004), and dividing neural progenitors sometimes reside close = to blood=20 vessels in the brain (Palmer et al., 2000). Recent work on brain tumor stem cells suggests that = these cells=20 tend to reside closer to blood vessels than other brain tumor cells and = that=20 vascular cells promote the maintenance of brain tumor stem cells in = culture and=20 promote tumorigenesis in vivo (Calabrese et al., 2007). These results raise the possibility that anticancer = therapies=20 might be more effective by targeting the microenvironments in which = cancer stem=20 cells reside in addition to the cancer cells themselves. Given that = cancer cells=20 are characteristically less dependent upon survival factors and less = restrained=20 in their expansion than normal stem cells, they are unlikely to have an=20 obligatory dependence on niches. Nonetheless, it is conceivable that = supportive=20 niches contribute to resistance to anticancer therapies by supplying = growth=20 factors that enhance the survival of tumorigenic cancer cells during=20 treatment.

Niches in Disease: = Niche=20 Aging

A fundamental characteristic of aging is the = reduced=20 regenerative capacity of tissues, and this is at least partially = attributable to=20 changes in the niche with age. In the Drosophila testis = (Wallenfang et=20 al., 2006,=20 Boyle et al., 2007)=20 and ovary (Pan et al., 2007), the number of germline stem cells, their mitotic = activity, and=20 the number of progeny they generate all decline with age. In males, = these=20 changes are partially attributable to changes within the niche as hub = cells from=20 older animals express reduced levels of DE-cadherin and Unpaired, both = of which=20 are necessary for GSC maintenance (Boyle et al., 2007). Overexpression of Unpaired in the hub cells of older = males=20 rescues the age-related decline in GSC division frequency. In the ovary, = expression of E-cadherin and BMP within the niche also declines with = age, and=20 genetically restoring high levels of expression can enhance the function = and=20 lifetime of old stem cells (Pan et al., 2007). Additional work will be required to characterize the = effect of=20 aging on mammalian stem cell niches.

Perspectives

The environmental mechanisms that regulate = stem cell=20 function are steadily being elucidated in invertebrate systems where = stem cells=20 from a variety of tissues can be imaged and genetically modified. In = vertebrate=20 tissues, there has also been impressive progress. However, technical = advances=20 will be required in most vertebrate systems to improve imaging of stem = cells at=20 a single-cell resolution. This will be required to show with confidence = that=20 individual cells are indeed bona fide stem cells based on the markers = they=20 express, rather than just members of a population that is somewhat = enriched for=20 stem cell activity. It will also be important to systematically test = mechanisms=20 that are proposed to regulate stem cell maintenance using genetics: Are = proposed=20 mechanisms really necessary for stem cell maintenance under = physiological=20 conditions in vivo, and can niche cells be identified by conditionally = deleting=20 potential maintenance factors from specific cell types that reside near = the stem=20 cells? Until these questions are answered, models of vertebrate stem = cell niches=20 will remain somewhat speculative. By better understanding the = physiological=20 mechanisms that regulate stem cell maintenance, new strategies can be = developed=20 to promote tissue regeneration after injury, to maintain stem cell = activity=20 during aging, and to sensitize cancer stem cells to therapy. Clearly,=20 fundamental scientific and medical questions reside within the = niche.

Acknowledgments

This work was supported by the Howard Hughes = Medical=20 Institute. Thanks to M. Kiel and T. Nystul for assistance with=20 figures.

References

Summary
Main=20 Text
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Structure =

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WIDTH: 730px; PADDING-TOP: 0px; = BORDER-BOTTOM: 0px; BORDER-COLLAPSE: collapse } TD.content_spacer { WIDTH: 10px } TD.magazine_content_header { PADDING-LEFT: 4px; BORDER-LEFT: #89a367 1px solid; WIDTH: 290px; = BORDER-BOTTOM: #89a367 1px solid; BACKGROUND-COLOR: #89a367 } TD.magazine_content { BORDER-RIGHT: #cccccc 1px solid; PADDING-RIGHT: 4px; BORDER-TOP: = #cccccc 1px solid; PADDING-LEFT: 4px; FONT-SIZE: 11px; PADDING-BOTTOM: = 4px; VERTICAL-ALIGN: top; BORDER-LEFT: #cccccc 1px solid; WIDTH: 300px; = COLOR: #333333; PADDING-TOP: 4px; BORDER-BOTTOM: #cccccc 1px solid; = FONT-FAMILY: Arial,Helvetica,sans_serif } TD.research_content_header { PADDING-LEFT: 4px; BORDER-LEFT: #759db6 1px solid; WIDTH: 410px; = BORDER-BOTTOM: #759db6 1px solid; BACKGROUND-COLOR: #759db6 } TD.research_content { BORDER-RIGHT: #cccccc 1px solid; PADDING-RIGHT: 4px; BORDER-TOP: = #cccccc 1px solid; PADDING-LEFT: 4px; FONT-SIZE: 11px; PADDING-BOTTOM: = 4px; VERTICAL-ALIGN: top; BORDER-LEFT: #cccccc 1px solid; 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= 20px; PADDING-LEFT: 0px; MARGIN-BOTTOM: 0px; PADDING-BOTTOM: 0px; = MARGIN-LEFT: 10px; BORDER-LEFT: 0px; WIDTH: 730px; PADDING-TOP: 0px; = BORDER-BOTTOM: 0px; BORDER-COLLAPSE: collapse } .general_table_bottom { BORDER-RIGHT: 0px; PADDING-RIGHT: 0px; BORDER-TOP: 0px; MARGIN-TOP: = 0px; PADDING-LEFT: 0px; MARGIN-BOTTOM: 10px; PADDING-BOTTOM: 0px; = MARGIN-LEFT: 10px; BORDER-LEFT: 0px; WIDTH: 730px; PADDING-TOP: 0px; = BORDER-BOTTOM: 0px; BORDER-COLLAPSE: collapse } TD.cover_image { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; = VERTICAL-ALIGN: top; WIDTH: 96px; PADDING-TOP: 0px; TEXT-ALIGN: center } TD.descriptive_content { BORDER-RIGHT: 0px; BORDER-TOP: 0px; PADDING-LEFT: 4px; VERTICAL-ALIGN: = top; BORDER-LEFT: 0px; WIDTH: 730px; BORDER-BOTTOM: 0px } TD.cover_image_content { BORDER-RIGHT: 0px; BORDER-TOP: 0px; PADDING-LEFT: 4px; VERTICAL-ALIGN: = top; BORDER-LEFT: 0px; WIDTH: 414px; BORDER-BOTTOM: 0px } TD.cover_image_content_footer { BORDER-RIGHT: 0px; BORDER-TOP: 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0px; BORDER-BOTTOM: #cccccc 1px solid; BORDER-COLLAPSE: collapse } .cover_caption_header { PADDING-LEFT: 4px; WIDTH: 194px; BORDER-BOTTOM: #cccccc 1px solid; = HEIGHT: 16px; BACKGROUND-COLOR: #cccccc } .cover_caption_header_blank { PADDING-RIGHT: 4px; PADDING-LEFT: 4px; PADDING-BOTTOM: 4px; WIDTH: = 430px; PADDING-TOP: 4px; BORDER-BOTTOM: #cccccc 1px solid; HEIGHT: 16px; = BACKGROUND-COLOR: #ffffff } TD.descriptive_content { PADDING-RIGHT: 4px; PADDING-LEFT: 4px; FONT-SIZE: 11px; PADDING-BOTTOM: = 4px; COLOR: #333333; PADDING-TOP: 4px; FONT-FAMILY: = Arial,Helvetica,sans_serif } TD.cover_image_content { PADDING-RIGHT: 4px; PADDING-LEFT: 4px; FONT-SIZE: 11px; PADDING-BOTTOM: = 4px; COLOR: #333333; PADDING-TOP: 4px; FONT-FAMILY: = Arial,Helvetica,sans_serif } TD.cover_image_content_footer { PADDING-RIGHT: 4px; PADDING-LEFT: 4px; FONT-SIZE: 11px; PADDING-BOTTOM: = 4px; COLOR: #333333; PADDING-TOP: 4px; FONT-FAMILY: = Arial,Helvetica,sans_serif } TD.descriptive_content P { MARGIN-TOP: 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WIDTH: 730px; PADDING-TOP: 0px; = BORDER-BOTTOM: 0px; BORDER-COLLAPSE: collapse } H1.dochead_title { FONT-WEIGHT: bold; FONT-SIZE: 18px; COLOR: #000000; FONT-FAMILY: = Verdana, Arial, Helvetica, sans_serif } H2.authors { FONT-WEIGHT: bold; FONT-SIZE: 15px; COLOR: #333333; FONT-FAMILY: = Verdana, Arial, Helvetica, sans_serif } H4.content_header { MARGIN-TOP: 20px; FONT-WEIGHT: bold; FONT-SIZE: 14px; MARGIN-BOTTOM: = 4px; COLOR: #333333 } STRONG { FONT-WEIGHT: bold } A.correspondence { COLOR: #333333; TEXT-DECORATION: underline } TD.article_info { PADDING-RIGHT: 20px; PADDING-BOTTOM: 40px; VERTICAL-ALIGN: top; WIDTH: = 500px } TD.article_summary { VERTICAL-ALIGN: top; WIDTH: 720px } TD.article_summary_content { PADDING-RIGHT: 10px; VERTICAL-ALIGN: top; WIDTH: 720px } TD.article_content { PADDING-RIGHT: 10px; PADDING-BOTTOM: 30px; WIDTH: 760px } TD.article_info P { FONT-SIZE: 11px; COLOR: #333333; LINE-HEIGHT: 1.2em; FONT-FAMILY: = Verdana, Arial, Helvetica, sans_serif } TD.article_info 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= MARGIN-LEFT: 10px; BORDER-LEFT: 0px; WIDTH: 730px; PADDING-TOP: 0px; = BORDER-BOTTOM: 0px } TD.article_options_footer_cell1 { BORDER-RIGHT: #e5e5e5 1px solid; PADDING-RIGHT: 2px; BORDER-TOP: = #e5e5e5 1px solid; PADDING-LEFT: 2px; PADDING-BOTTOM: 2px; = VERTICAL-ALIGN: top; BORDER-LEFT: #e5e5e5 1px solid; WIDTH: 320px; = PADDING-TOP: 2px; BORDER-BOTTOM: #e5e5e5 1px solid } TD.article_options_footer_cell2 { BORDER-RIGHT: #e5e5e5 1px solid; PADDING-RIGHT: 2px; BORDER-TOP: = #e5e5e5 1px solid; PADDING-LEFT: 2px; PADDING-BOTTOM: 2px; = VERTICAL-ALIGN: top; BORDER-LEFT: #e5e5e5 1px solid; WIDTH: 200px; = PADDING-TOP: 2px; BORDER-BOTTOM: #e5e5e5 1px solid } TD.article_options_footer_cell3 { BORDER-RIGHT: #e5e5e5 1px solid; PADDING-RIGHT: 2px; BORDER-TOP: = #e5e5e5 1px solid; PADDING-LEFT: 2px; PADDING-BOTTOM: 2px; = VERTICAL-ALIGN: top; BORDER-LEFT: #e5e5e5 1px solid; WIDTH: 200px; = PADDING-TOP: 2px; BORDER-BOTTOM: #e5e5e5 1px solid } .article_options_title { PADDING-LEFT: 4px; 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INPUT.button { BORDER-RIGHT: #000 1px solid; PADDING-RIGHT: 3px! important; = BORDER-TOP: #000 1px solid; PADDING-LEFT: 3px! important; FONT-WEIGHT: = bold; FONT-SIZE: 11px; MARGIN-BOTTOM: 1px; PADDING-BOTTOM: 0px! = important; VERTICAL-ALIGN: bottom; BORDER-LEFT: #000 1px solid; WIDTH: = auto! important; PADDING-TOP: 1px! important; BORDER-BOTTOM: #000 1px = solid } INPUT.checkbox { BORDER-RIGHT: 0px; BORDER-TOP: 0px; BORDER-LEFT: 0px; WIDTH: auto! = important; BORDER-BOTTOM: 0px } INPUT.radio { BORDER-RIGHT: 0px; BORDER-TOP: 0px; BORDER-LEFT: 0px; WIDTH: auto! = important; BORDER-BOTTOM: 0px } #userpanel LABEL { FLOAT: left; WIDTH: 20px; MARGIN-RIGHT: 2px } #search_author { BORDER-RIGHT: #ccc 1px solid; PADDING-RIGHT: 10px; MARGIN-TOP: 0px; = PADDING-LEFT: 10px; PADDING-BOTTOM: 10px; PADDING-TOP: 10px } TABLE.search TR TD { PADDING-RIGHT: 7px; PADDING-BOTTOM: 7px } DIV.no_results { PADDING-RIGHT: 10px; PADDING-LEFT: 10px; PADDING-BOTTOM: 10px; MARGIN: = 10px; PADDING-TOP: 10px } DIV.no_results H3 { BACKGROUND: none transparent scroll repeat 0% 0%; WIDTH: auto! = important } #search_author INPUT { WIDTH: 200px } #search_checkboxes { FLOAT: left; WIDTH: 450px } #search_checkboxes INPUT.checkbox { CLEAR: both; VERTICAL-ALIGN: top } FIELDSET LABEL { FONT-SIZE: 11px } FIELDSET LABEL.strong { FLOAT: none } FIELDSET TABLE TBODY TR TD { FONT-SIZE: 11px } DIV.no_results { PADDING-RIGHT: 10px; PADDING-LEFT: 10px; PADDING-BOTTOM: 10px; MARGIN: = 10px; PADDING-TOP: 10px } DIV.no_results H3 { BACKGROUND: none transparent scroll repeat 0% 0%; WIDTH: auto! = important } .subscriptions#generic_container DIV.subscribe_text { MARGIN-TOP: -35px; FLOAT: left; WIDTH: 610px! important } .subscriptions#generic_container DIV.subscribe_text H3 { BACKGROUND: url(../images/h2bg.gif) #fff no-repeat right top; WIDTH: = 610px! important } DIV.subscribe_text H3 { FONT-SIZE: 110%; BACKGROUND: none transparent scroll repeat 0% 0%; = WIDTH: 646px; COLOR: #000066! important; BORDER-BOTTOM: #000066 2px = solid } TD INPUT.radio { MARGIN-LEFT: 3px; VERTICAL-ALIGN: middle; MARGIN-RIGHT: 3px } #main { FLOAT: left; MARGIN: 20px 0px 30px 60px; WIDTH: 1000px } #sign_up { FLOAT: left; MARGIN: 0px 30px 0px 10px; WIDTH: 350px; HEIGHT: 300px } #edit_alerts { FLOAT: left; WIDTH: 350px } .alert_content { BORDER-RIGHT: #000066 1px solid; PADDING-RIGHT: 15px; BORDER-TOP: = #000066 1px solid; PADDING-LEFT: 15px; PADDING-BOTTOM: 20px; = BORDER-LEFT: #000066 1px solid; PADDING-TOP: 20px; BORDER-BOTTOM: = #000066 1px solid; HEIGHT: 200px } .alert_content FORM { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; = PADDING-TOP: 10px } #content_alerts UL { MARGIN: 5px 0px 50px } .button { BORDER-RIGHT: #000 1px solid; PADDING-RIGHT: 3px! important; = BORDER-TOP: #000 1px solid; PADDING-LEFT: 3px! important; FONT-WEIGHT: = bold; FONT-SIZE: 11px; MARGIN-BOTTOM: 1px; PADDING-BOTTOM: 0px! = important; VERTICAL-ALIGN: bottom; BORDER-LEFT: #000 1px solid; WIDTH: = auto! important; COLOR: #000! important; PADDING-TOP: 1px! important; = BORDER-BOTTOM: #000 1px solid; BACKGROUND-COLOR: #ccc } A.button { TEXT-DECORATION: none } TABLE#alerts { BORDER-RIGHT: #000066 1px solid; BORDER-TOP: #000066 1px solid; MARGIN: = 20px; BORDER-LEFT: #000066 1px solid; WIDTH: 600px; BORDER-BOTTOM: = #000066 1px solid } TABLE#register { BORDER-RIGHT: #000066 1px solid; BORDER-TOP: #000066 1px solid; MARGIN: = 20px; BORDER-LEFT: #000066 1px solid; WIDTH: 600px; BORDER-BOTTOM: = #000066 1px solid } #alerts TH { PADDING-RIGHT: 5px; PADDING-LEFT: 5px; FONT-SIZE: 12px; PADDING-BOTTOM: = 5px; PADDING-TOP: 5px } #alerts TD { PADDING-RIGHT: 5px; PADDING-LEFT: 5px; FONT-SIZE: 12px; PADDING-BOTTOM: = 5px; PADDING-TOP: 5px } #register TD { PADDING-RIGHT: 5px; PADDING-LEFT: 5px; FONT-SIZE: 12px; PADDING-BOTTOM: = 5px; PADDING-TOP: 5px } #register TH { PADDING-RIGHT: 5px; PADDING-LEFT: 5px; FONT-SIZE: 12px; PADDING-BOTTOM: = 5px; PADDING-TOP: 5px } #alerts TH { TEXT-ALIGN: center } #alerts TD { TEXT-ALIGN: center } #register TD.desc { PADDING-LEFT: 20px; FONT-WEIGHT: normal; MARGIN-LEFT: 0px; WIDTH: = 180px; TEXT-ALIGN: left } #alerts TD.desc { PADDING-LEFT: 20px; FONT-WEIGHT: normal; MARGIN-LEFT: 0px; WIDTH: = 210px; TEXT-ALIGN: left } #content TABLE#register TD.desc { WIDTH: auto! important } #register LABEL { FONT-WEIGHT: bold } #alerts TD.span { PADDING-LEFT: 20px; TEXT-ALIGN: left } P.favorite { MARGIN-TOP: 30px; FONT-WEIGHT: bold } #popup_container { MARGIN-LEFT: 0px; WIDTH: 500px } #popup_container INPUT { MARGIN: 0px 7px; WIDTH: 300px } #popup_container LABEL { MARGIN-LEFT: 10px } DIV#edit_alerts LABEL.short { MIN-WIDTH: 60px; DISPLAY: block; FLOAT: left; WIDTH: 60px; LINE-HEIGHT: = 22px } DIV#edit_alerts INPUT { =09 } DIV#edit_alerts A.forgot { MARGIN-TOP: 40px; DISPLAY: block; FLOAT: left; WIDTH: 80px } DIV#edit_alerts FORM { FLOAT: left; WIDTH: 200px } TD.imp_note { PADDING-LEFT: 16px! important; FONT-SIZE: 9px! important; TEXT-ALIGN: = right } UL#benefits { 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} DIV.hr HR { DISPLAY: none } TABLE#nav TD { FONT-SIZE: 11px; COLOR: #888; FONT-FAMILY: arial, helvetica, = sans-serif; TEXT-ALIGN: left! important } TABLE#nav TD.selected { COLOR: #000 } #nav TD { PADDING-RIGHT: 2px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; WIDTH: 3px; PADDING-TOP: 0px } #nav TD.content { WIDTH: 20px! important } #popup_main INPUT { =09 } #popup_main LABEL { CLEAR: both; DISPLAY: block; FLOAT: left; WIDTH: 80px } #popup_main FORM.popup_login INPUT { FLOAT: left; MARGIN-BOTTOM: 1px; WIDTH: 120px } #popup_main INPUT { PADDING-RIGHT: 2px; PADDING-LEFT: 3px; FONT-SIZE: 100%; MARGIN-BOTTOM: = 1px; PADDING-BOTTOM: 2px; MARGIN-LEFT: 1px; WIDTH: 250px; PADDING-TOP: = 2px } A.forgotp { DISPLAY: block; FLOAT: left; MARGIN: 5px 0px 0px 5px; WIDTH: 140px } A.largebutton { BORDER-RIGHT: #000 1px solid; PADDING-RIGHT: 7px! important; = BORDER-TOP: #000 1px solid; PADDING-LEFT: 7px! important; FONT-WEIGHT: = bold; FONT-SIZE: 11px; MARGIN-BOTTOM: 0px; PADDING-BOTTOM: 4px! = important; VERTICAL-ALIGN: bottom; BORDER-LEFT: #000 1px solid; WIDTH: = auto! important; COLOR: #000! important; PADDING-TOP: 5px! important; = BORDER-BOTTOM: #000 1px solid; HEIGHT: 25px; BACKGROUND-COLOR: #ccc; = TEXT-DECORATION: none } #popup_main TH.wide { PADDING-RIGHT: 30px } #popup_main TH.wider { PADDING-RIGHT: 40px } #popup_main .indent { PADDING-RIGHT: 0px; MARGIN-TOP: 0px; PADDING-LEFT: 20px; MARGIN-BOTTOM: = 0px; PADDING-BOTTOM: 10px; PADDING-TOP: 0px } #popup_main P.right { PADDING-RIGHT: 59px; TEXT-ALIGN: right } #popup_container TD.group { MARGIN-TOP: 20px } P.small { MARGIN-BOTTOM: 6px } #popup_main TD.delete { LINE-HEIGHT: 20px; TEXT-ALIGN: right } P.alert { PADDING-LEFT: 20px; COLOR: #f00 } H1.reg_title { MARGIN-TOP: 15px } #extra_messages { MARGIN-TOP: 15px } #popup_main TH { FONT-SIZE: 70% } #popup_container H1 { PADDING-RIGHT: 0px; PADDING-LEFT: 7px; FONT-WEIGHT: normal; FONT-SIZE: = 18px; PADDING-BOTTOM: 10px; MARGIN: 0px; COLOR: #fff; PADDING-TOP: 10px } 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DIV.content_panel { BORDER-TOP: #006 1px solid } DIV.article_summary { BORDER-TOP: #006 1px solid } DIV.article_summary1 { BORDER-TOP: #006 1px solid } #search_left DIV.content_panel { BORDER-TOP: #006 1px solid } DIV.article_fulltext_link { BORDER-TOP: #006 1px solid; MARGIN-LEFT: 10px } #search_right DIV.content_search { BORDER-RIGHT: #ccc 1px solid; BORDER-TOP: #006 1px solid; HEIGHT: 360px } A { COLOR: #006 } #alerts TD A { COLOR: #006 } DIV.content_panel P A { COLOR: #006 } #navigation UL LI A:hover { BACKGROUND-COLOR: #000066 } #navigation UL LI A.selected { BACKGROUND-COLOR: #000066 } A:link { COLOR: #006 } A:link { COLOR: #006 } A:active { COLOR: #006 } A:visited { COLOR: #440088 } A:hover { COLOR: #333; TEXT-DECORATION: none } #content A { COLOR: #006 } #supplemental_detail A { COLOR: #006 } #sitemap_all A { COLOR: #006 } #content_abstract A { COLOR: #006 } #image_detail A { COLOR: #006 } #content UL LI { BACKGROUND: url(../images/cell/cell_bullet.gif) no-repeat left top } #content_abstract UL LI { BACKGROUND: url(../images/cell/cell_bullet.gif) no-repeat left top } P.comment { COLOR: #006; BACKGROUND-COLOR: #fff } H3.leading_edge { BACKGROUND: url(../images/h3bggreen.gif) #89a367 no-repeat right top } #leading_edge H2 { BACKGROUND: url(../images/h3bggreen.gif) #89a367 no-repeat right top } #research_articles H2 { BACKGROUND: url(../images/h2bgblue.gif) #759db6 no-repeat right top } #research_articles .content_panel { PADDING-RIGHT: 4px; PADDING-LEFT: 4px; BACKGROUND: = url(../images/research_articles_grad.gif) #fff repeat-y right top; = PADDING-BOTTOM: 4px; PADDING-TOP: 4px } #leading_edge .content_panel { PADDING-RIGHT: 4px; PADDING-LEFT: 4px; BACKGROUND: = url(../images/leading_edge_grad.gif) #fff repeat-y left top; = PADDING-BOTTOM: 4px; PADDING-TOP: 4px } H1.article_title { COLOR: #000066 } H1.search_title { COLOR: #000066 } H1.archive_title { COLOR: #000066 } DIV.generic_panel H3 { PADDING-BOTTOM: 3px; COLOR: #000066! important; BORDER-BOTTOM: #000066 = 2px solid } #supplemental_data TH { PADDING-BOTTOM: 3px; COLOR: #000066! important; BORDER-BOTTOM: #000066 = 2px solid } TABLE.personalize TR TH { PADDING-BOTTOM: 3px; COLOR: #000066! important; BORDER-BOTTOM: #000066 = 2px solid } DIV.subscribe_text H3 { BACKGROUND: none transparent scroll repeat 0% 0%; WIDTH: 610px! = important; COLOR: #000066! important; BORDER-BOTTOM: #000066 2px solid; = FONT-FAMILY: Verdana, Arial } STRONG.rates { BACKGROUND: #006; COLOR: #fff } SPAN.link { FONT-WEIGHT: bold; COLOR: #000066 } .forgotten { FONT-WEIGHT: bold; FONT-SIZE: 17px; COLOR: #000066; FONT-FAMILY: = Verdana, Arial } #authors P A { FONT-SIZE: 16px; COLOR: #000066; FONT-FAMILY: "times new roman" } DIV.no_results { BORDER-RIGHT: #006 2px solid; BORDER-TOP: #006 2px solid; BORDER-LEFT: = #006 2px solid; BORDER-BOTTOM: #006 2px solid } #main A { COLOR: #000066 } #select_journal P A { COLOR: #000066 } #popup_container A { COLOR: #000066 } #login_form A { COLOR: #000066 } #content_alerts DIV.content_panel { BORDER-TOP: #006 1px solid } A.largebutton:hover { BACKGROUND: #00309c; COLOR: #fff! important } TD.totalprice { BORDER-TOP: #006 2px solid; FONT-WEIGHT: bold; PADDING-TOP: 5px } A { COLOR: #006 } #alerts TD A { COLOR: #006 } DIV.content_panel P A { COLOR: #006 } TABLE#register H2 { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; FONT-SIZE: 16px; BACKGROUND: 0px = 50%; PADDING-BOTTOM: 0px; MARGIN: 15px 0px 0px; WIDTH: auto; COLOR: = #006; PADDING-TOP: 0px; TEXT-ALIGN: left } TABLE#alerts H2 { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; FONT-SIZE: 16px; BACKGROUND: 0px = 50%; PADDING-BOTTOM: 0px; MARGIN: 15px 0px 0px; WIDTH: auto; COLOR: = #006; PADDING-TOP: 0px; TEXT-ALIGN: left } P STRONG#login_unsucces { COLOR: #900 } DIV.hr { BACKGROUND: #00309c } #popup_container H1 { BACKGROUND-COLOR: #003399; important:=20 } #popup_footer { BACKGROUND-COLOR: #003399; important:=20 } ------=_NextPart_000_002F_01C87D11.8C441FD0 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://www.cell.com/webfiles/javascript/script.js function dropdown(list) { var item=3Dlist.options[list.selectedIndex].value; if (item !=3D "nowhere")=20 { top.location=3Ditem; } } =09 function openhelp() { window.open('/popup/help', 'helpwindow', = 'width=3D580,height=3D410,left=3D0,top=3D0,screenX=3D0,screenY=3D0,resiza= ble=3Dno,scrollbars=3Dyes'); self.name=3D"main"; } function opensearchhelp() { = window.open('/popup/help/Finding_Information.htm','helpwindow','width=3D5= 80,height=3D410,left=3D0,top=3D0,screenX=3D0,screenY=3D0,resizable=3Dno,s= crollbars=3Dyes'); self.name=3D"main"; } function statecodeselect(thisform, thislist, list1, list2, = countrycodefield, countrydescfield) { var theform =3D eval("document." + thisform); var thelist =3D eval("theform." + thislist); eval("theform." + list1 + ".selectedIndex=3D0"); eval("theform." + list2 + ".selectedIndex=3D0"); eval("theform.elements[\"" + countrycodefield + = "\"].value=3Dthelist.options[thelist.selectedIndex].text"); eval("theform.elements[\"" + countrydescfield + = "\"].value=3Dthelist.options[thelist.selectedIndex].text"); } function clearstates ( thisform, strControlNameRoot, strIdentifiers ) { eval ( "document." + thisform + "." + strControlNameRoot + = ".value=3D''" ); var colIdentifiers =3D strIdentifiers.split ( ";" ); for ( var iCounter =3D 0; iCounter < colIdentifiers.length; iCounter++ = ) eval ( "document." + thisform + "." + strControlNameRoot + "_" + = colIdentifiers[iCounter] + ".selectedIndex=3D0" ); } //function finalstate ( thisform, strControlNameRoot, strSelectRef, = strIdentifiers ) function final_state ( thisform, strSelectRef, strIdentifiers ) { var strCountryID =3D eval ( "document." + thisform + "." + strSelectRef = + ".options[document." + thisform + "." + strSelectRef + = ".selectedIndex].value" ); if ( strIdentifiers.indexOf ( strCountryID ) =3D=3D -1 || strCountryID = =3D=3D "0") return; //var strStateID =3D eval ( "document." + thisform + "." + = strControlNameRoot + "_" + strCountryID + ".options[document." + = thisform + "." + strControlNameRoot + "_" + strCountryID + = ".selectedIndex].value" ); //eval ( "document." + thisform + "." + strControlNameRoot ).value =3D = strStateID; } function finalstate ( thisform, strControlNameRoot, strSelectRef, = strIdentifiers ) //function finalstate ( thisform, strSelectRef, strIdentifiers ) { var strCountryID =3D eval ( "document." + thisform + "." + strSelectRef = + ".options[document." + thisform + "." + strSelectRef + = ".selectedIndex].value" ); if ( strIdentifiers.indexOf ( strCountryID ) =3D=3D -1 || strCountryID = =3D=3D "0") return; var strStateID =3D eval ( "document." + thisform + "." + = strControlNameRoot + "_" + strCountryID + ".options[document." + = thisform + "." + strControlNameRoot + "_" + strCountryID + = ".selectedIndex].value" ); eval ( "document." + thisform + "." + strControlNameRoot ).value =3D = strStateID; } function setstate ( thisform, strControlNameRoot, strIdentifier, = strSelectRef, strIdentifiers, evt ) { // The following line ensures that the event type can be picked up = across all IE and NN var eventType =3D evt.type || arguments.callee.caller.name || = window.event.type; if ( eventType.indexOf ( "on" ) !=3D 0 ) eventType =3D "on" + eventType; if ( strIdentifier !=3D "" ) { if ( eval ( "document." + thisform + "." + strSelectRef + = ".options[document." + thisform + "." + strSelectRef + = ".selectedIndex].value" ) !=3D strIdentifier ) { // This part will be hit if the user selects a drop down that isn't = the one that they should // The country has not been set, or is set to something other than = the state box that was selected // Need to do two things. Set the country to the relevant value and = clear the other boxes if ( eventType =3D=3D "onchange" ) { // First, clear the other drop downs' values var colIdentifiers =3D strIdentifiers.split ( ";" ); for ( var iCounter =3D 0; iCounter < colIdentifiers.length; = iCounter++ ) { if ( colIdentifiers[iCounter] !=3D strIdentifier ) eval ( "document." + thisform + "." + strControlNameRoot + "_" + = colIdentifiers[iCounter] + ".selectedIndex=3D0" ); } // Clear the text box eval ( "document." + thisform + "." + strControlNameRoot + = ".value=3D''" ); // Now set the country eval ( "document." + thisform + "." + strSelectRef + ".selectedIndex = =3D " + searchArray ( eval ( "document." + thisform + "." + strSelectRef = + ".options" ), strIdentifier ) ); } return; } return; } else { if ( ( eval ( "document." + thisform + "." + strSelectRef + = ".selectedIndex" ) =3D=3D 0 ) || ( eval ( "document." + thisform + "." + strSelectRef + = ".options[document." + thisform + "." + strSelectRef + = ".selectedIndex].value" ) =3D=3D 1224 ) || ( eval ( "document." + thisform + "." + strSelectRef + = ".options[document." + thisform + "." + strSelectRef + = ".selectedIndex].value" ) =3D=3D 1037 ) ) { // This part will be entered when the user selects the text box and = that doesn't match what's in the country box // What needs to be done is the country box is aligned and the other = state input boxes to be reset if ( eventType =3D=3D "onchange" ) { // First, clear the drop downs' values var colIdentifiers =3D strIdentifiers.split ( ";" ); for ( var iCounter =3D 0; iCounter < colIdentifiers.length; = iCounter++ ) eval ( "document." + thisform + "." + strControlNameRoot + "_" + = colIdentifiers[iCounter] + ".selectedIndex=3D0" ); // Now set the country // Should we set it to a country? Or should it be blank? Think it = should be set to blank. eval ( "document." + thisform + "." + strSelectRef + ".selectedIndex = =3D 0" ); } return; } return; } } // This function searches an array and returns the index at which the = search string occurs function searchArray ( arrToSearch, strSearchValue ) { for ( var iCounter =3D 0; iCounter < arrToSearch.length; iCounter++ ) if ( arrToSearch[iCounter].value =3D=3D strSearchValue ) return iCounter; return -1; } function sethidden(value,field,value2) { if(!value2) { if(field.options) value2=3Dfield.options[field.selectedIndex].value; else value2=3Dfield.value; } if(value2!=3D"") { field.form.elements[value].value=3Dvalue2; } } function setEcommerce2Hidden() { sethidden('titleid',orderdetails.addresstitleid); sethidden('firstname',orderdetails.addressfirstname); sethidden('lastname',orderdetails.addresslastname); sethidden('address1',orderdetails.addressstreet); sethidden('address2',orderdetails.addressstreet2); sethidden('city',orderdetails.addresscity); sethidden('state',orderdetails.addressstate); sethidden('countryid',orderdetails.addresscountry); sethidden('zip',orderdetails.addresspostcode); sethidden('telephone',orderdetails.addressphone); } // Logic for YOAS checkboxs function yoasValidate(ckb) { var cnt =3D document.journals.journal.length - 3; var bk =3D document.journals.backfile.length >=3D 3; =09 if (bk) { //alert("records " + cnt); for (j =3D cnt; j < (cnt+3); j++)=20 { if (eval("document.journals.journal[" + (j) + "].checked") =3D=3D = true)=20 { document.journals.journal[j].checked =3D false; if (j - cnt =3D=3D ckb - 1)=20 { document.journals.journal[j].checked =3D true; } } } } } function noCheckbox() { for (j =3D 0; j < checkbox_form.uid.length; j++) { =20 if (checkbox_form.uid[j].checked) {=20 return true;=20 } =20 } msg =3D "Please select at least one checkbox"; alert(msg); return (false); } function oneCheckbox() { for (j =3D 1; j < document.rangedate.TOC.length; j++) { =20 if (eval("document.rangedate.TOC[" + (j) + "].checked") = =3D=3D true) {=20 rangedate.TOC[0].checked =3D false =09 } if (document.rangedate.TOC[0].checked =3D=3D true) {=20 rangedate.TOC[j].checked =3D false =09 } } return; } function oneCheckbox1() { for (j =3D 1; j < document.rangedate.TOC.length; j++) { =20 if (document.rangedate.TOC[0].checked =3D=3D true) {=20 rangedate.TOC[j].checked =3D false =09 } } return; } function encode(string){ =20 return string; } function linkChange(linkRef){=09 var volIssue =3D document.all.volIssue.value; linkRef.href=3DlinkRef.href+"&volIssue=3D"+volIssue; return true; } function refreshParent() { window.opener.location.href =3D window.opener.location.href; if (window.opener.progressWindow) =09 { window.opener.progressWindow.close() } window.close(); } // This function displays the ad results. // It must be defined above the script that calls show_ads.js // to guarantee that it is defined when show_ads.js makes the = call-back. function google_ad_request_done(google_ads) { // Proceed only if we have ads to display! if (google_ads.length < 1 ) return; // Display ads in a table document.write("
"); // Print "Ads By Google" -- include link to Google feedback page if = available if (google_info.feedback_url) { document.write("Ads by Google"); } else { document.write("Ads By Google"); } =20 document.write("
"); // For text ads, display each ad in turn. // In this example, each ad goes in a new row in the table. if (google_ads[0].type =3D=3D 'text') { for(i =3D 0; i < google_ads.length; ++i) { =09 document.write("
" + "" + =20 google_ads[i].line1 + "
" + google_ads[i].line2 + " " + google_ads[i].line3 + "
" +=20 "" +=20 google_ads[i].visible_url + "
");=20 } } // For an image ad, display the image; there will be only one . if (google_ads[0].type =3D=3D 'image') { document.write("" + "" + ""); } // Finish up anything that needs finishing up document.write ("
"); } function loadFormValues() { //alert(document.getElementById("a2").value); document.getElementById("search_author2").value = =3Ddocument.getElementById("a2").value ; document.getElementById("search_author1").value = =3Ddocument.getElementById("a1").value ; document.getElementById("search_words_title").value = =3Ddocument.getElementById("title-abstract").value ; document.getElementById("search_yearfrom").value = =3Ddocument.getElementById("fromyear").value ; document.getElementById("search_yearto").value = =3Ddocument.getElementById("toyear").value ; if(document.getElementById("orand").value=3D=3D'or') { document.getElementById("or").checked=3Dtrue; } if(document.getElementById("keywordloc").value=3D=3D'anywhere') { document.getElementById("inanywhere").checked=3Dtrue; } if(document.getElementById("keywordoptions").value=3D=3D'any') { document.getElementById("kw_any").checked=3Dtrue; } if(document.getElementById("keywordoptions").value=3D=3D'exact') { document.getElementById("kw_exact").checked=3Dtrue; } if(document.getElementById("published").value=3D=3D'0') { document.getElementById("pub_week").checked=3Dtrue; } if(document.getElementById("published").value=3D=3D'1') { document.getElementById("pub_month").checked=3Dtrue; } if(document.getElementById("published").value=3D=3D'2') { document.getElementById("pub_6months").checked=3Dtrue; } if(document.getElementById("published").value=3D=3D'4') { document.getElementById("pub_all").checked=3Dtrue; } =20 if(document.getElementById("typearticle").value=3D=3D'research') { document.getElementById("search_research").checked=3Dtrue; } if(document.getElementById("typearticle").value=3D=3D'review') { document.getElementById("search_review").checked=3Dtrue; } if(document.getElementById("sortby").value=3D=3D'rank') { document.getElementById("search_rank").checked=3Dtrue; } =20 // For Journal Check boxes var journal=3Ddocument.getElementById("journal-name").value;=09 var length_cell=3Djournal.length; var = immuni=3Ddocument.getElementById("journal-name").value.match("Immunity");= var = neuron=3Ddocument.getElementById("journal-name").value.match("Neuron"); var = mcell=3Ddocument.getElementById("journal-name").value.match("Molecular");= var = struc=3Ddocument.getElementById("journal-name").value.match("Structure");= var = curbio=3Ddocument.getElementById("journal-name").value.match("Current"); var = dcell=3Ddocument.getElementById("journal-name").value.match("Developmenta= l"); var = ccell=3Ddocument.getElementById("journal-name").value.match("Cancer"); var = chbiol=3Ddocument.getElementById("journal-name").value.match("Chemistry")= ; var = cmet=3Ddocument.getElementById("journal-name").value.match("Metabolism");= var = chom=3Ddocument.getElementById("journal-name").value.match("Host"); var = stem=3Ddocument.getElementById("journal-name").value.match("Stem"); var cell =3D journal.substring(0,5); if(length_cell=3D=3D'4' || cell=3D=3D'Cell,'){ =09 document.getElementById("search_cell").checked =3D true; rangedate.TOC[0].checked =3D false; } if(immuni=3D=3D'Immunity'){ document.getElementById("search_immuni").checked =3D true; rangedate.TOC[0].checked =3D false; } if(neuron=3D=3D'Neuron'){ document.getElementById("search_neuron").checked =3D true; rangedate.TOC[0].checked =3D false; } =20 if(mcell=3D=3D'Molecular'){ document.getElementById("search_molcel").checked =3D true; rangedate.TOC[0].checked =3D false; } =20 if(struc=3D=3D'Structure'){ document.getElementById("search_foldes").checked =3D true; rangedate.TOC[0].checked =3D false; } =09 if(curbio=3D=3D'Current'){ document.getElementById("search_curbio").checked =3D true; rangedate.TOC[0].checked =3D false; } =09 if(dcell=3D=3D'Developmental'){ document.getElementById("search_dcell").checked =3D true; rangedate.TOC[0].checked =3D false; } =09 if(ccell=3D=3D'Cancer'){ document.getElementById("search_ccell").checked =3D true; rangedate.TOC[0].checked =3D false; } =09 if(chbiol=3D=3D'Chemistry'){ document.getElementById("search_chbiol").checked =3D true; rangedate.TOC[0].checked =3D false; } =09 if(cmet=3D=3D'Metabolism'){ document.getElementById("search_cmet").checked =3D true; rangedate.TOC[0].checked =3D false; } =20 if(chom=3D=3D'Host'){ document.getElementById("search_chom").checked =3D true; rangedate.TOC[0].checked =3D false; } =09 if(stem=3D=3D'Stem'){ document.getElementById("search_stem").checked =3D true; rangedate.TOC[0].checked =3D false; } =09 } ------=_NextPart_000_002F_01C87D11.8C441FD0 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: https://ad.uk.doubleclick.net/adj/cell.rbi/content/article/fulltext;abr=!webtv;sz=728x90;ord=46465? document.write('');=0A= ------=_NextPart_000_002F_01C87D11.8C441FD0--

Review

Stem = Cells and=20 Niches: Mechanisms That Promote Stem Cell Maintenance throughout = Life

Summary

Main Text

Introduction

Identifying Stem = Cells

Stem Cell = Markers

Identification of = Stem Cells=20 through Lineage Analysis

Cell Culture = Assays

Identifying = Niches

Facultative, = Distributed=20 Niches for Mammalian Stem Cells

Niche Mechanisms: = Primary=20 Maintenance Signals

Niche Mechanisms: = Additional=20 Signals

Niche Mechanisms: = Asymmetric=20 Division

Maintaining Stem = Cell=20 Vitality: Hierarchies, Immortal Strands, and Competition

Molecular Asymmetry = during=20 Stem Cell Division

The Immortal = Centrosome=20 Hypothesis

Niches in Disease: = Cancer Stem=20 Cell Niches

Niches in Disease: = Niche=20 Aging

Perspectives

Acknowledgments

References

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