From: Subject: Skin stem cells: rising to the surface -- Fuchs 180 (2): 273 -- The Journal of Cell Biology Date: Thu, 31 Jan 2008 09:05:59 +0100 MIME-Version: 1.0 Content-Type: multipart/related; type="text/html"; boundary="----=_NextPart_000_002D_01C863E8.7F5B46F0" X-MimeOLE: Produced By Microsoft MimeOLE V6.00.2900.3198 This is a multi-part message in MIME format. ------=_NextPart_000_002D_01C863E8.7F5B46F0 Content-Type: text/html; charset="Windows-1252" Content-Transfer-Encoding: quoted-printable Content-Location: http://www.jcb.org/cgi/content/full/180/2/273?ijkey=3751a3e8fb976f43e3775e18d1cf49167676bfba Skin stem cells: rising to the surface -- Fuchs 180 = (2): 273 -- The Journal of Cell Biology
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Published online 21 January=20 2008
doi:10.1083/jcb.200708185
The Journal of Cell = Biology, Vol.=20 180, No. 2, 273-284
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Mini-Review

Skin stem cells: = rising to=20 the surface

Elaine Fuchs =

Howard Hughes Medical = Institute,=20 Laboratory of Mammalian Cell Biology and Development, The Rockefeller=20 University, New York, NY 10065

Correspondence to Elaine Fuchs: = fuchslb{at}rockefeller.edu

The skin epidermis and its appendages provide = a=20 protective barrier that is impermeable to harmful microbes = and also=20 prevents dehydration. To perform their functions while being=20 confronted with the physicochemical traumas of the = environment, these=20 tissues undergo continual rejuvenation through homeostasis, = and, in=20 addition, they must be primed to undergo wound repair in = response to=20 injury. The skin's elixir for maintaining tissue homeostasis, = regenerating hair, and repairing the epidermis after injury = is its=20 stem cells, which reside in the adult hair follicle, = sebaceous gland,=20 and epidermis. Stem cells have the remarkable capacity to = both=20 self-perpetuate and also give rise to the differentiating = cells that=20 constitute one or more tissues. In recent years, scientists = have=20 begun to uncover the properties of skin stem cells and = unravel=20 the mysteries underlying their remarkable capacity to perform = these feats. In this paper, I outline the basic lineages of = the=20 skin epithelia and review some of the major findings about=20 mammalian skin epithelial stem cells that have emerged in the = past=20 five years.

Abbreviations used in=20 this paper: BMP, bone morphogenetic protein; BMPR, BMP = receptor; DP,=20 dermal papillae; E-cadherin, epithelial cadherin; EDA, = ectodysplasin;=20 EGFR, EGF receptor; EPU, epidermal proliferative unit; FA, = focal=20 adhesion; IRS, inner root sheath; ORS, outer root sheath; = RTK,=20 receptor tyrosine kinase; SG, sebaceous gland; Shh, Sonic = hedgehog;=20 TA, transit amplifying.

The=20 epidermis
I refer the reader to several fine reviews = on avian=20 skin epithelial stem cells (Chuong=20 et al., 2006) and other stem cells of the mammalian skin = (Nishikawa=20 and Osawa, 2006; Tiede=20 et al., 2007; Waters=20 et al., 2007; Fernandes=20 et al., 2008). The mammalian skin epidermis has been the = paradigm=20 for exploring homeostasis and injury repair in a stratified=20 epithelium. The epidermis maintains a single inner (basal) = layer of=20 proliferative cells that adhere to an underlying basement = membrane=20 rich in ECM and growth factors (Fig.=20 1). Basal cells express several characteristic markers, = including=20 keratins and transcription factors. Periodically, these cells = withdraw from the cell cycle, commit to differentiate = terminally,=20 move outward, and are eventually shed from the skin surface. = This=20 magnificent architecture allows the epidermis to generate a=20 self-perpetuating barrier that keeps harmful microbes out and = essential body fluids in.



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  		Figure 1.=20 Epidermal differentiation. The program of epidermal=20 differentiation is shown in this schematic, illustrating the = basement membrane at the base, the proliferative basal = layer, and=20 the three differentiation stages: spinous layer, granular = layer, and=20 outermost stratum corneum. At the right, key molecular = markers are=20 shown, which are described in the first section of this = paper. =

 
Upon=20 commitment to terminally differentiate, an epidermal keratinocyte=20 progresses through three distinct differentiation stages: = spinous,=20 granular, and stratum corneum (Fig.=20 1). Major changes in transcription, morphology, and = function=20 occur at the basal/spinous layer transition and again at the=20 granular/stratum corneum transition such that differentiated = cells=20 reaching the skin surface are enucleated cellular skeletons = that are=20 packed with cables of keratin filaments encased by a 3D{gamma}=20-glutamyl-3D{epsilon}=20-lysine cross-linked = cornified=20 envelope of proteins. An additional final step in the=20 differentiation process is the extrusion of a lipid bilayer = that=20 creates a saran wrap seal to the body surface (de=20 Guzman Strong et al., 2006; Elias,=20 2007). The process is in a dynamic flux so that surface = cells are=20 continually sloughed and replaced by inner cells differentiating = and=20 moving outward. In human epidermis, the self-renewing capacity = of=20 epidermal stem cells is enormous, and, within 4 wk, a basal = cell has=20 terminally differentiated and exited at the skin surface. In = mice,=20 the postnatal trunk epidermis becomes thinner, and = proliferation=20 slows substantially as the hair coat develops and becomes the = primary=20 line of protection.

Although researchers have known for years that stem cells exist=20 within the basal layer of adult epidermis, it is still not = clear=20 whether all cells within the basal layer are stem cells or = whether=20 only a small number of stem cells exist within this layer. = The=20 epidermal proliferative unit (EPU) has been architecturally=20 defined as a bed of 10 tightly packed basal cells yielding a=20 stack of increasingly larger and flatter cells that culminate = with a single hexagonal surface cell (Potten,=20 1974). This has led to the hypothesis that there is one=20 self-renewing stem cell per EPU and that the other basal = cells are=20 so-called transit-amplifying (TA) cells (i.e., committed = cells that=20 divide several times and then exit the basal layer and = terminally=20 differentiate; Potten,=20 1974; Mackenzie,=20 1997). In support of this notion are in vitro studies = that show=20 that human epidermal cells with the highest level of surface = β1=20 integrins give rise to the largest colonies (holoclones) that = can be=20 passaged long term, whereas cells with lower levels of = β1 integrins=20 produce smaller meroclones that do not survive passaging (Barrandon=20 and Green, 1987; Jones=20 et al., 1995). 3D{alpha}β1 Integrins are the transmembrane core = components of focal=20 adhesions (FAs), which are required for basement membrane = assembly,=20 cell substratum adhesion, and cell = survival/proliferation.=20

Based largely on in vitro observations, it has long been = surmised=20 that basal epidermal cells divide symmetrically and give rise = to equal daughter cells. In this scenario, a basal cell would = progressively reduce its adhesiveness to the underlying = basement=20 membrane, delaminate, and commit to terminally differentiate=20 (Fig.=20 2; Watt=20 et al., 1984; Watt=20 and Hogan, 2000). In vivo, regional variations within the = basement membrane and microenvironment have been described to = suggest=20 how distinct populations of integrin-rich stem cells and TA = cells=20 might arise within the basal layer (Lavker=20 and Sun, 1982; Jensen=20 et al., 1999). Recent studies suggest that basal epidermal = cells=20 can divide asymmetrically, affording a different view of how = one=20 basal stem cell and one committed cell might arise (Lechler=20 and Fuchs, 2005; Clayton=20 et al., 2007).



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  		Figure 2.=20 Models for the generation of a single innermost (basal) = layer of=20 cells with proliferative potential and multiple layers of = suprabasal=20 cells. Self-renewing stem cells (SCs) exist in the basal = layer=20 of the epidermis. Symmetrical divisions produce two stem = cells, a=20 process which can serve to replenish vacancies in the basal = layer.=20 In the three-step model, a transit-amplifying (TA) = intermediate=20 arises, which has been postulated to divide four to five = times=20 before delaminating (straight arrows) and entering into a = terminal=20 differentiation program. In the two-step model, a stem cell = divides=20 asymmetrically to preferentially partition = proliferation-associated=20 factors into the stem cell daughter while providing=20 differentiation-inducing components to the other daughter, = which is=20 fated to become a spinous cell (SP). Depending on the = orientation of=20 the spindle, the divisions could either result in detachment = of the=20 SP daughter from the basement membrane or, if lateral, would = then=20 necessitate subsequent delamination of the committed SP = daughter.=20 The spinous cells enter a program of terminal = differentiation as=20 they move outward and are eventually sloughed from the skin = surface=20 (see Fig.=20 1). Differentiating cells are continually replaced by a = flux of=20 inner cells committing to terminally differentiate and = moving=20 outward. =

 
In=20 the first study reporting asymmetrical divisions, at the = onset of=20 stratification, mouse embryonic basal cells were shown to = shift their=20 spindle orientation from a lateral to a more perpendicular=20 orientation to undergo asymmetrical divisions (Lechler=20 and Fuchs, 2005). Asymmetrical divisions soon accounted = for 70% of all = basal cell=20 mitoses, whereas 3D~30%=20 remained symmetric (Lechler=20 and Fuchs, 2005). Although the marked reduction in = postnatal=20 basal cell divisions posed technical difficulties in = measuring=20 asymmetrical divisions in most regions of adult mouse skin, = ear skin=20 as well as tongue displayed >60% asymmetrical divisions. = The=20 asymmetrical divisions observed provide a natural means of=20 maintaining one proliferative basal daughter cell rich in=20 growth-promoting receptor tyrosine kinases (RTKs) and integrins = and=20 one suprabasal daughter with reduced RTKs and integrin levels = (Fig.=20 2). Moreover, loss of function experiments demonstrated a = role=20 for 3D{alpha}β1 integrins=20 and also 3D{alpha}-catenin (a core member of cell=96cell adherens = junctions) in=20 setting up the cell polarity required for proper spindle pole = orientation and maintenance of homeostasis (Lechler=20 and Fuchs, 2005).

In a more recent study, lineage tracing experiments on adult = mouse=20 tail skin (another area diminished in hair follicles) also = provided=20 evidence that divisions in the basal layer are both = asymmetric and=20 symmetric, but, in this case, only 3D~=2030% occurred = at an=20 angle of >20=B0 relative to the basement membrane (Clayton=20 et al., 2007). In this case, it was proposed that asymmetrical=20 divisions might leave both daughters physically adhering to=20 their substratum but that the committed daughter cell = asymmetrically=20 inherits a stronger Notch signal (Clayton=20 et al., 2007), a key transcriptional determinant of the = spinous=20 cell fate (discussed in more detail later in this section; Rangarajan=20 et al., 2001; Pan=20 et al., 2004; Blanpain=20 et al., 2006; Nguyen=20 et al., 2006a; Lee=20 et al., 2007). In this model, the daughter inheriting the = Notch=20 signal would differentiate, detach from the underlying = basement=20 membrane, and enter the spinous layer, whereas the daughter = spared of=20 the Notch signal would remain a stem cell (Clayton=20 et al., 2007).

Although additional studies will be needed to resolve these=20 different models for basal cell divisions, they lead to = distinct=20 implications for the numbers of epidermal stem cells and the=20 location of the epidermal stem cell niche. The EPU model = implies=20 the existence of only a small number of basal stem cells, = suggesting=20 that within the basal layer, there should be spatially = organized=20 microenvironments that constitute a mini-niche for a single=20 stem cell. In contrast, the asymmetrical division models = suggest=20 that a single progenitor population within the basal layer = can=20 give rise to committed cells by differentially partitioning=20 proteins to the daughters. The lateral asymmetrical division=20 model implies that asymmetrical divisions are intrinsic to = the=20 epider-mal stem cell, alleviating the need for a = microenvironmental=20 change to trigger commitment. The perpendicular asymmetrical=20 division model suggests that the basement membrane itself may = constitute the epidermal stem cell niche, naturally placing = the=20 committed cell into the spinous layer. The lateral symmetric=20 divisions, which would yield two stem cells, might then = provide=20 a mechanism to replenish old or damaged basal stem cells (in=20 the case of perpendicular asymmetrical divisions) or spinous=20 cells (after delamination in the case of lateral asymmetrical = divisions). This perpendicular asymmetrical division model is = analogous to that of Drosophila melanogaster germ cell=20 development, in which preservation of contact with the niche=20 maintains stemness, whereas perpendicular asymmetrical = divisions=20 drive fate determination of the daughter cells that depart = the niche=20 (Fuller=20 and Spradling, 2007).

Irrespective of the orchestrator of epidermal cell fate, the=20 basement membrane demarcating the epidermis and dermis plays = a=20 critical role in governing the proliferative capacity of the=20 epidermis. Although its mechano-physical properties alone are = likely to impact the proliferative properties of basal cells=20 (Dobereiner=20 et al., 2005), the basement membrane is also composed of = a rich=20 array of ECM polymers and growth factors that provide a = complex=20 repertoire of stimuli for basal cells. Among them is laminin = 5, which=20 promotes anchorage and signaling/migration through its = respective=20 abilities to act as ligand for 3D{alpha}=206β4-rich=20 hemidesmosomes and 3D{alpha}3β1-rich FAs (Owens=20 and Watt, 2003; Raghavan=20 et al., 2003; Manohar=20 et al., 2004). Through downstream 3D{alpha}=203β1 integrin = activation of FAK,=20 integrin-linked kinase, and the RTK Src, integrin signaling = not only=20 stimulates the Ras=96MAPK pathway but also induces FA = adhesion=20 turnover and epidermal migration (Lorenz=20 et al., 2007; Schober=20 et al., 2007). Notably, transgenic suprabasal expression = of=20 integrins promotes tumorigenesis (Carroll=20 et al., 1995). Conversely, conditional loss of FAK in the = skin of=20 mice leads to an increased resistance to chemically induced = skin=20 tumorigenesis (McLean=20 et al., 2004), and, in vitro, FAK-deficient = keratinocytes=20 exhibit defects in cell migration and FA turnover under = conditions in=20 which apoptosis and proliferation are unaffected (Schober=20 et al., 2007). Such studies underscore the importance of=20 integrin/FAK signaling in balancing homeostasis, wound = repair, and=20 tumorigenesis in the skin.

The basement membrane is also rich in proteoglycans and other=20 proteins that act as molecular sinks for growth factors, such = as TGFβs, which restrict epidermal proliferation, and TGF3D{alpha}=20/EGFs and = insulin=20 growth factors, which promote it (for review see Fuchs,=20 2007). A recent study has shown that when TGFβ signaling = is=20 compromised through loss of the TβRII receptor, epidermal = homeostasis=20 is maintained, but the basal layer displays increased = proliferation=20 counterbalanced by increased apoptosis (Guasch=20 et al., 2007). Although homeostasis can be maintained, it = is=20 precarious: wounds heal faster, and with just one additional=20 oncogenic mutation, the tissue transforms quickly to squamous = cell=20 carcinoma of the skin. Interestingly, enhanced FAK/integrin = signaling=20 and accelerated migration are also seen when TGFβ = signaling=20 is compromised in the epidermis (Guasch=20 et al., 2007). Conversely, elevated integrin signaling = has been=20 shown to suppress TGFβ signaling (Owens=20 and Watt, 2003), suggesting that this molecular route may = be a=20 two-way street.

Although TGFβ signaling places the brake on epidermal = proliferation=20 and migration, EGF receptor (EGFR) signaling enhances = proliferation=20 and migration in the epidermis (Sibilia=20 et al., 2000). A recent study shows that Lrig1, an = inhibitory=20 ligand for EGFR signaling, is expressed within a less = proliferative,=20 β1-enriched subset of cells within the basal layer of = human epidermis=20 (Jensen=20 and Watt, 2006). Gene targeting has revealed that the = epidermis=20 of mice lacking Lrig1 hyperproliferates (Suzuki=20 et al., 2002), and human keratinocytes treated with = Lrig1=20 short hairpin RNA produce larger colonies than normal. These=20 observations have led to the hypothesis that Lrig1 plays a = role in=20 basal stem cell quiescence (Jensen=20 and Watt, 2006). Mitogen-inducible gene 6 is also a = suppressor of=20 EGFR signaling, and mice deficient in mitogen-inducible gene = 6 also=20 display epidermal hyperproliferation and increased tumor=20 susceptibility (Ferby=20 et al., 2006). Intriguingly, EGFR signaling promotes not = just=20 proliferation but also cell migration. One possible mechanism = is=20 through the ability of activated EGFR to phosphorylate = β4 integrin=20 and promote hemidesmosome disassembly (Wilhelmsen=20 et al., 2007).

Thus, through regulation of two opposing tyrosine kinase = receptor=20 pathways and two integrin structures, the basement membrane=20 plays an integral role in controlling the ability of basal = epidermal=20 stem cells to maintain homeostasis under normal and injury=20 conditions. When this regulation goes awry, there is an = increased=20 propensity to developing squamous cell carcinoma. As the = roles for=20 additional basement membrane constituents and their = associates are=20 uncovered, our understanding of the special features of the = epidermal=20 basement membrane and its ability to regulate epidermal stem = cell=20 biology should continue to unfold.

The extrinsic signals received by the microenvironment and = translated=20 through transmembrane receptors are likely to couple with the = intrinsic properties of the basal epidermal cells to define=20 their ability to self-renew and undergo homeostasis and wound = repair. One transcription factor that is likely to play a key = role in regulating the self-renewal and long-term = proliferative=20 capacity of the stem cell is p63, a member of the p53 family = of=20 protooncogenes. The 3D{Delta}N isoform of p63 is preferentially expressed in = basal=20 epidermal cells (Laurikkala=20 et al., 2006). Its importance in epidermal biology = surfaced when=20 two groups made the fortuitous discovery that mice lacking = p63 are=20 severely impaired in their ability to generate the epidermis = (Mills=20 et al., 1999; Yang=20 et al., 1999). The groups differed in whether the thin = epidermis=20 was caused by a defect in stem cell renewal (Yang=20 et al., 1999), an absence of lineage commitment, and/or = an early=20 block in epidermal differentiation (Mills=20 et al., 1999), and recent studies still leave this issue=20 unresolved.

Supporting a role for 3D{Delta}Np63 in stem cell self-renewal are clonal analyses = on=20 cultured thymic epithelial and epidermal cells, which suggest = that=20 when p63 mRNA is knocked down through small hairpin = RNAs, the=20 cells form smaller colonies with reduced proliferation rates = (Senoo=20 et al., 2007). Experiments on human epidermal raft = cultures=20 suggest that p63's function in basal cells is mediated by its = ability=20 to inhibit its relative p53, thereby promoting cell survival = and=20 longevity, whereas its effects on differentiation are p53 = independent=20 (Truong=20 and Khavari, 2007). Consistent with this notion, the p63=20 knockdown experiments of Senoo=20 et al. (2007) revealed the increased expression of = terminal=20 differentiation and apoptosis markers. In contrast, the = studies of Koster=20 et al. (2007) propose a role for p63 in triggering basal = cells to=20 switch from proliferation to terminal differentiation through = the=20 induction of I3D{kappa}B kinase-3D{alpha}, a putative regulator of differentiation (Hu=20 et al., 2001; Gareus=20 et al., 2007). Future studies will be needed to resolve = this=20 controversy.

Once cells become suprabasal, p63 is down-regulated by an = underlying=20 mechanism that is not yet clear. It has been reported that = suprabasal=20 signaling through Notch transmembrane receptors leads to = suprabasal=20 repression of p63 and inhibition of proliferation (Nguyen=20 et al., 2006a). Similarly, loss of function experiments = on the=20 basally expressed Notch ligand, Delta1, results in = hyperproliferation=20 as well as the repression of differentiation, suggesting that = Delta1 functions by repressing epidermal proliferation as = well as=20 promoting differentiation (Estrach=20 et al., 2007). That said, conditional ablation of all = canonical=20 Notch signaling in the embryonic epidermis results in basal = cell=20 hypoproliferation and repression of spinous layer = differentiation,=20 with no obvious suprabasal expression of p63 (Blanpain=20 et al., 2006). Recent studies by Lee=20 et al. (2007) suggest that the epidermal = hyperproliferation seen=20 when skin is partially compromised in Notch signaling may = arise from=20 noncell autonomous changes in the underlying dermis. Although = the=20 effects of Notch on proliferation appear to be complex, the=20 collective view emerging from the present studies is that = Notch=20 signaling plays a key role in the transition between basal = and=20 suprabasal cells in the epidermis, where it functions in = activating=20 the basal to suprabasal fate switch (Fig.=20 3).



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  		Figure 3.=20 Predicted roles of Notch signaling in the three different = lineages of the epidermis. (A) Model. In the skin, Notch = ligands=20 are often basal, whereas Notch receptors are typically = suprabasal=20 (Pan=20 et al., 2004; Blanpain=20 et al., 2006; Estrach=20 et al., 2006, 2007;=20 Nguyen=20 et al., 2006a). Notch signaling results in the release = of Notch=20 intracellular domain, which acts as a transcription cofactor = for the=20 DNA-binding protein RBPj (Pan=20 et al., 2004). Downstream targets of Notch intracellular = domain/RBPj include Hes1 and Hey1, which bind DNA and often = function=20 as transcriptional repressors (Hurlbut=20 et al., 2007). In the skin lineages, Notch signaling, as = indicated by either the expression of Notch intracellular = domain (Pan=20 et al., 2004), Notch target genes Hes1 and Hey1 (Blanpain=20 et al., 2006), or loss of function studies (Blanpain=20 et al., 2006; Estrach=20 et al., 2006, 2007),=20 is particularly prominent at the transition of fates from=20 proliferative to differentiating. The arrows denote = molecular steps=20 along the pathways for each of the three major epithelial = lineages=20 of the skin. Those marked in red indicate the steps at which = Notch=20 signaling acts. (B) Immunofluorescence. Immunofluorescence=20 microscopy was used on frozen mouse skin sections of E18.5=20 (epidermis) and postnatal day 28 (hair follicle bulb) to = illustrate=20 the localization of Notch3, Hes1, and Hey1. All samples were = counterstained with DAPI (blue) to mark the nuclei. Where = indicated,=20 antibodies against β4 integrin (Int) were used to mark = the=20 dermo-epidermal boundary, and keratin 14 (Ker14) was used to = denote=20 the basal layer of the ORS. The top two panels illustrate = the=20 coexpression of Notch3 and Hes1, which is particularly = strong at the=20 basal to suprabasal transition of the epidermis. The bottom = two=20 panels show that Hes1 is prominent in the differentiating = cells of=20 the IRS (left), whereas Hey1 is more broadly expressed in = both the=20 precortex and IRS (right). The inset in the image in the = bottom=20 right frame shows a close-up view of hair shaft precursor = cells that=20 have been labeled with antibodies against hair keratins in = green and=20 Hey1 in red to show that nuclear Hey1 colocalizes with cells = that=20 generate the hair shaft. Note that the highly proliferative = matrix=20 cells at the base of the hair bulb are negative for signs of = Notch=20 signaling. For further information and similar images = (courtesy of=20 C. Blanpain and W.E. Lowry), see Blanpain=20 et al. (2006). Bar, 45 mm. =

 
Overall,=20 the basal expression of Notch ligands such as Delta1 and the=20 suprabasal expression of Notch receptors and Notch downstream = target=20 genes such as Hes1 are consistent with a role for Notch = signaling in=20 controlling this switch. A role for Notch as the gatekeeper = of the=20 commitment of basal epidermal cells to terminally = differentiate is=20 particularly intriguing in light of a Notch inhibitor, Numb, = which=20 functions as an intrinsic cell fate determinant that is = segregated=20 into only one of the two daughter cells during neural = precursor=20 division in Drosophila neuroblasts (for review see Yu=20 et al., 2006). In flies, Numb localization is determined = by=20 opposing signals from the Par3=96atypical PKC complex, and = this=20 machinery is also present in basal epidermal cells and is = present at=20 the right time and place to control asymmetrical divisions = (Lechler=20 and Fuchs, 2005; Clayton=20 et al., 2007). Although much still remains to be learned = about=20 how basal epidermal cells become activated to withdraw from = the cell=20 cycle and commit to terminally differentiate, the action = appears to=20 converge at the base of the epidermis between the basal and = first=20 suprabasal layers.

The=20 hair follicle
One of the most remarkable features of = the=20 vertebrate epidermis is its extraordinary ability to generate = elaborate appendages. The scales of a fish, the horn of a=20 rhinocerous, the claws of an eagle, the mane of a lion, and = the sweat=20 (eccrine) and oil (sebaceous) glands of our skin are all = epidermal=20 appendages. Knowledge of how epidermal appendages develop has = been=20 gained by studying the embryonic skin at a stage when it = exists=20 as a single-layered epithelium.

Hair follicle morphogenesis begins early in embryonic = development=20 as dermal cells populate the skin, and signals from the = epithelium=20 induce the formation of dermal condensates. Dermal = condensates=20 are the precursors to the dermal papillae (DP), which are the = permanent mesenchymal component of the hair follicle. At=20 approximately embryonic day (E) 14.5 of mouse development,=20 mesenchymal=96epithelial interactions result in the formation = of the=20 first wave of hair placodes, which appear as small epidermal=20 invaginations into the dermis (Fig.=20 4). Once initiated, these placodes undergo marked = proliferation=20 and downgrowth to produce first the hair germs (3D~=20E15.5) and then hair = pegs (E16.5=9617.5). The=20 follicle cells at the leading front (matrix) remain highly=20 proliferative, and, through contact with the DP, they engage = in a=20 program of gene expression that is distinct from the root. = The outer=20 root sheath (ORS) maintains contact with the basement = membrane,=20 whereas the inner root sheath (IRS) provides the channel for = the=20 emerging hair (3D~E18.5). At birth, the most mature hairs begin to break = the=20 skin surface, and the sebaceous gland (SG) precursor cells = become=20 established in the upper segment of the root. Maturation = continues=20 through the first postnatal week (Fig.=20 4; for review see Schmidt-Ullrich=20 and Paus, 2005). There are four waves of follicle = morphogenesis,=20 with the large primary guard hairs forming first (E14.5) and = the bulk=20 of the hair coat follicles initiating within a few days after = this.



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  		Figure 4.=20 Embryonic stages of hair follicle morphogenesis. The = process=20 of follicle morphogenesis occurs relatively late in = embryonic=20 development. In the mouse, discrete waves of placodes are = seen=20 beginning at approximately E14.5 and ending near birth. Once = initiated, newly formed follicles continue to mature = postnatally=20 until approximately day 9, at which time matrix (TA) cells = at the=20 base of the follicle continue to rapidly proliferate and=20 differentiate, generating hair growth. For a comprehensive = analysis=20 of the regional, temporal, and strain-specific variations in = the=20 timing of hair follicle morphogenesis, see the reviews Muller-Rover=20 et al., 2001 andSchmidt-Ullrich=20 and Paus, 2005. =

 
One=20 dermal cue that appears to be critical is the bone morphogenetic=20 protein (BMP) inhibitory protein Noggin, whose absence = severely=20 impairs hair follicle morphogenesis (Botchkarev=20 et al., 1999). Ectodermal Wnt signals, which include = Wnt10b, are=20 thought to act in concert with dermal signals to instruct the = epidermal cells to grow downward (Botchkarev=20 et al., 1999; DasGupta=20 and Fuchs, 1999; Reddy=20 et al., 2001; Andl=20 et al., 2002). At the crux of this signaling cross talk = is the=20 bipartite transcription factor complex composed of LEF1 and=20 stabilized β-catenin, which is critical for hair = follicle=20 morphogenesis (van=20 Genderen et al., 1994; Zhou=20 et al., 1995; Gat=20 et al., 1998) and whose activity can be monitored by the = Wnt=20 reporter gene TOPGAL (DasGupta=20 and Fuchs, 1999; Millar,=20 2002). Inhibition of BMP signaling is permissive for LEF1 = expression and also promotes the stabilization of β-catenin = (Jamora=20 et al., 2003; Kobielak=20 et al., 2003; Andl=20 et al., 2004; Zhang=20 et al., 2006), whereas Wnts are well-established instigators = of=20 β-catenin stabilization (for review see Clevers,=20 2006). Interestingly, although this paradigm serves the = bulk of=20 follicle morphogenesis, the first wave of follicle = morphogenesis,=20 resulting in formation of the large primary guard hairs, = diverges=20 somewhat, particularly in the external cues guiding these = internal=20 regulatory processes. This first wave is uniquely dependent = on a=20 TNF-like ligand=96receptor complex composed of ectodysplasin = (EDA)=20 and EDA receptor, which, instead of inducing Noggin, induces=20 two different BMP inhibitors. EDA is a target of Wnt = signaling=20 (Laurikkala=20 et al., 2001), and signs of Wnt reporter gene activity = and=20 LEF1/β-catenin are present by E14.5, when the first wave = of follicle=20 morphogenesis occurs (DasGupta=20 and Fuchs, 1999; Pummila=20 et al., 2007; for review see Schmidt-Ullrich=20 and Paus, 2005).

Just how powerful is the stabilization of β-catenin to = promoting=20 hair follicle morphogenesis? Studies over the past decade = indicate=20 that it is indeed central to the decision-making process. = Thus, when=20 excess β-catenin is stabilized in the epidermis of = transgenic mice,=20 ectopic hair follicles appear within the interfollicular = epidermis,=20 generating super-furry mice (Gat=20 et al., 1998), and, when the Wnt inhibitor Dickoff 1 = (Dkk1) is=20 expressed ectopically or when β-catenin is conditionally = targeted for=20 ablation, hair follicle morphogenesis is blocked altogether = (Huelsken=20 and Birchmeier, 2001; Andl=20 et al., 2002). Recently, Ito=20 et al. (2007) showed that when the skin of mice is = severely=20 wounded, endogenous Wnt signaling is elevated in the skin, = and this=20 leads to the induction of hair follicle formation from = epidermal stem=20 cells. Collectively, these findings underscore the role for=20 stabilized β-catenin in governing the choice of whether = to become=20 epidermis or hair follicle.

Once the placode forms, signaling events downstream of Wnts/BMPs = drive the downgrowth and maturation of hair follicles. Sonic=20 hedgehog (Shh) is an early gene expressed downstream of = Wnt/BMP=20 receptor (BMPR) signaling (and EDA/EDA receptors in the case = of=20 guard hairs) and placode formation (Dahmane=20 et al., 1997; Oro=20 et al., 1997; Gat=20 et al., 1998; Morgan=20 et al., 1998; St-Jacques=20 et al., 1998). Shh plays a critical role in organizing = the dermal=20 cells into a condensate, or DP, which thereafter becomes a = permanent=20 component of the hair follicle (Hardy,=20 1992; St-Jacques=20 et al., 1998; Oro=20 and Higgins, 2003; Levy=20 et al., 2007). Overall, the formation of the hair bud = involves=20 many changes in gene expression as exemplified by the = differences=20 between the transcriptional profile of placode cells and = their=20 epidermal counterparts (Rhee=20 et al., 2006). Among the early steps is the activation of = additional key transcription factors (e.g., Lhx2 and=20 Sox9) whose absence results in a failure to maintain = follicle=20 stem cell behavior in mice (Vidal=20 et al., 2005; Rhee=20 et al., 2006). Additional changes involve down-regulation = of some=20 adhesion proteins (e.g., epithelial cadherin [E-cadherin]) = and=20 up-regulation of others (Jamora=20 et al., 2003). The field is still in the midst of = elucidating how=20 multiple signaling pathways converge on the ectoderm to = elicit=20 changes in transcription factors that then subsequently = change the=20 expression and dynamics of the extracellular matrix, = cytoskeleton,=20 and cell matrix and cell=96cell junctions that remodel the = epithelium=20 from its single layer to a hair bud. Once understood, this = process=20 is likely to be relevant to other morphogenetic processes=20 ranging from development of the mammary gland to that of the=20 tooth.

The hair cycle and hair follicle stem=20 cells
The hair follicle undergoes cycles of = degeneration and=20 regeneration throughout life. Matrix cells have been referred = to as=20 TA cells because they proliferate rapidly during the growth=20 (anagen) phase of the cycle but then suddenly undergo = apoptosis by=20 a mechanism that is still poorly understood. During this = 3=964-d=20 destructive phase (catagen), the hair bulb and root shrivel = to=20 an epithelial strand, which pulls the DP upward to rest at = the base=20 of the permanent, noncycling portion of the follicle. In = mice,=20 backskin follicles remain dormant for 1=962 d in the first = resting=20 phase (telogen) but then rest for >3 wk in the second = telogen. Old=20 hairs can remain in their socket through several bouts of = hair=20 cycling, rendering the hair coat impervious to this cyclic=20 behavior.

At the onset of each new anagen, the cycling portion of the=20 follicle regenerates, a process that necessitates a reservoir = of follicle stem cells. These stem cells reside in the lowest = permanent portion of the follicle, within the ORS, which = bulges=20 around the existing old hair pocket to enable the new hair to = emerge through the same orifice at the skin surface. The = cells=20 within the bulge of the ORS cycle less frequently than other=20 epithelial cells within the skin (Cotsarelis=20 et al., 1990). At the start of each new hair cycle, a = cluster of=20 stem cells at the base of the bulge become activated to = proliferate.=20 Grafting and lineage tracing experiments have shown that some = bulge=20 cells are stem cells and that offspring of a single bulge = stem=20 cell can form SGs and epidermis as well as new hair follicles = (Blanpain=20 et al., 2004; Morris=20 et al., 2004; Claudinot=20 et al., 2005). That said, although follicle stem cells = are=20 multipotent, unless the skin is wounded, follicle stem cells = only=20 function in hair follicle homeostasis and do not contribute = to=20 interfollicular epidermis (Ito=20 et al., 2005; Levy=20 et al., 2005, 2007).

To understand the special features of the bulge, researchers = have=20 conducted microarray profiling. Approximately 150 genes are=20 preferentially expressed in the bulge relative to the proliferating = basal cells of the epidermis (Blanpain=20 et al., 2004; Morris=20 et al., 2004; Tumbar=20 et al., 2004). The purification of bulge stem cells has = been=20 accomplished by FACS based on either (1) bulge cell surface = markers=20 3D{alpha}6 = and CD34=20 coupled with K14-GFP expression (Blanpain=20 et al., 2004), (2) K15-GFP expression (Morris=20 et al., 2004), or (3) a fluorescent histone pulse-chase=20 experiment in mice expressing a tetracycline-inducible=20 transcriptional regulatory repressor (Tetoff) under the = control of a K5 promoter and histone H2B-GFP under the = control of=20 a tetracycline regulatory element (Tumbar=20 et al., 2004). Although each of these different = procedures=20 purifies slightly different cell populations, the array data = are in=20 quite good agreement, enabling researchers to exploit this=20 information to learn more about follicle stem cells. =

Like the embryonic epidermis, bulge cells are Wnt responsive, = as=20 judged by their expression of two LEF1-related DNA-binding = proteins,=20 TCF3 and TCF4, and several Wnt receptor proteins (Fzds). = However, at=20 least in telogen, most bulge cells appear to be in a state of = Wnt=20 inhibition, as judged by the array data and by the lack of = detectable=20 nuclear β-catenin or TOPGAL activity (DasGupta=20 and Fuchs, 1999). These findings are consistent with a = recent=20 study showing that TCF3 can function as a repressor when = β-catenin is=20 absent or underrepresented and that TCF3 on its own functions = to=20 repress the differentiation of skin stem cells (Nguyen=20 et al., 2006b).

Although Wnt inhibition seems to be a feature of the dormant = stem=20 cell niche in the skin, stabilized β-catenin is a = feature of=20 activated stem cells. By transgenically elevating the levels = of=20 stabilized β-catenin, hair follicles precociously enter = anagen (Van=20 Mater et al., 2003; Lo=20 Celso et al., 2004). Conditional loss of BMPR1a in = telogen=20 follicles also results in the precocious entry of follicles = into=20 anagen and the stabilization of β-catenin, and, at least = in part,=20 this appears to be caused by the activation of PI3 kinase = signaling,=20 which, in turn, phosphorylates and inactivates GSK3β, = the kinase=20 that otherwise targets β-catenin for phosphorylation and = ubiquitin-mediated degradation (Zhang=20 et al., 2006; Kobielak=20 et al., 2007). These studies further clarify how the = inhibition=20 of BMP signaling and activation of Wnt signaling converge to = regulate=20 stem cell activation.

Once follicle stem cells are activated, Wnt3 signaling appears = to=20 be required for hair shaft differentiation, whereas BMP signaling = is=20 required for IRS and directly or indirectly is also required = for hair=20 shaft differentiation (Millar,=20 2002; Kobielak=20 et al., 2003; Andl=20 et al., 2004; Yuhki=20 et al., 2004). Thus, when β-catenin is conditionally = targeted for=20 depletion in adult skin when follicles are in telogen phase, = the=20 bulge stem cell compartment cannot be maintained, and the new = hair=20 cycle does not reinitiate (Lowry=20 et al., 2005); when stabilized β-catenin is = constitutively=20 activated, tumors develop that are composed of a center of = hair shaft=20 cells surrounded by matrix-like cells expressing nuclear=20 LEF1/β-catenin (Gat=20 et al., 1998).When the gene encoding BMPR1a is conditionally=20 targeted for depletion in adult follicles in telogen phase,=20 bulge stem cells become activated, as judged by their loss of = BrdU label retention and their entry into S phase (Andl=20 et al., 2004; Kobielak=20 et al., 2007). However, the cells cannot terminally=20 differentiate, and, within weeks, tumors develop that display = markers such as Lhx2, Sox4, Sox9, and Shh, which are features = of activated stem cells. Despite the fact that they are no = longer=20 slow cycling and do not express appreciable CD34, the = follicle=20 cells lacking BMPR1a are still able to repair epidermis in a=20 wound response, and they generate what appear to be = long-lived=20 tumors (Zhang=20 et al., 2006; Kobielak=20 et al., 2007). These studies are tantalizing in that they = suggest=20 that quiescence may not be an essential feature of follicle = stem=20 cells.

Overall, these data suggest that BMP signaling plays an = important=20 role in follicle stem cell quiescence. Consistent with this=20 view are immunofluorescence studies that detect = phosphorylated=20 Smad1, which is reflective of active BMP signaling, and the=20 behavior of cultured bulge cells exposed to BMP6, which = results=20 in their transient withdrawal from the cell cycle (Blanpain=20 et al., 2004; Kobielak=20 et al., 2007). TGFβ signaling also appears to be = up-regulated in=20 bulge cells (Tumbar=20 et al., 2004) and is known to dampen the cell cycle (Massague,=20 2007). However, conditional ablation of the TGFβ = receptor did not=20 appear to compromise the slow-cycling capability of the = follicle stem=20 cells in the bulge (Guasch=20 et al., 2007).

Although studies in recent years have led to major advances = in our=20 knowledge of bulge stem cells and the signaling pathways = involved in=20 their activation at the start of the hair cycle (for review = see Fuchs,=20 2007), the precise nature of the signals and where they = come from=20 are still poorly understood. Thus, despite the established = role for=20 β-catenin stabilization in follicle stem cell = activation,=20 documentation for the involvement of a specific Wnt is still = lacking.=20 Similarly, although the condensate of DP cells typically = rests at the=20 base of the bulge in telogen follicles and expresses several = BMP=20 inhibitory factors and Wnts that are candidates for follicle = stem=20 cell activation, it is not clear precisely what this = inductive signal=20 is. Further complicating the issue is that in the whisker = cycle of=20 rodents, the DP never reaches the bulge before the start of a = new=20 anagen. It has been proposed that stem cells from the bulge=20 therefore migrate along the ORS to the base of the follicle, = where=20 they become activated (Oshima=20 et al., 2001). Although further studies are required, = most=20 studies to date are consistent with the notion that this may = also=20 happen in backskin follicles. If so, it would imply that = Sox9, Tcf3,=20 and Lhx2 may be markers of follicle stem cells irrespective = of=20 whether they are quiescent or proliferative and that there = are likely=20 to be factors beyond DP signals that are required to activate = the=20 hair cycle.

SGs
Appendages of the hair = follicle,=20 SGs, are located above the bulge and just below the hair = shaft=20 orifice at the skin surface. The major role of the gland is = to=20 generate terminally differentiated sebocytes, which = degenerate to=20 release lipids and sebum and lubricate the skin surface. SG=20 homeostasis necessitates a population of progenitor cells = that gives=20 rise to a continual flux of proliferating and differentiating = cells=20 that are sloughed through the hair canal. Lineage tracing by=20 retroviral-mediated gene transfer suggests that a small = population of=20 cells near or at the base of the SG might be stem cells (Ghazizadeh=20 and Taichman, 2001).

Recently, the transcriptional repressor protein Blimp1 was = identified=20 in a genetic screen for hair follicle transcription factors,=20 and it was shown to mark a small population of cells at the = SG=20 base (Horsley=20 et al., 2006). These Blimp1-positive cells appeared to be = in=20 close association with the basement membrane surrounding the = gland=20 and are contiguous with the BM that demarcates the = dermal=96epidermal=20 border and surrounds the hair follicle. The Blimp1-positive = SG cells=20 also express K5/K14. Genetic lineage tracing experiments = reveal that=20 the Blimp1-positive SG cells can regenerate the entire gland, = including the sebocytes. When it was conditionally targeted = for=20 ablation, SGs got larger. The likely explanation stems from = Blimp1's=20 role in B lymphocytes, in which it transcriptionally = represses=20 c-myc (Chang=20 et al., 2000), a gene known to induce SG hyperplasia and = sebocyte=20 differentiation at the expense of hair follicle = differentiation (Arnold=20 and Watt, 2001; Waikel=20 et al., 2001). However, if Blimp1 truly marks the = progenitor/stem=20 cell population of the SG, why don't the enlarged glands = eventually=20 recede in Blimp1's absence even if hyperplasia is the initial = outcome?

Although further studies are needed, the underlying explanation=20 could be rooted in the ability of the bulge to become = mobilized=20 when the SG progenitor cell population is depleted. As judged = by BrdU pulse and pulse-chase experiments, Blimp1-negative = bulge=20 cells show signs of active cycling and reduced label = retention=20 in the absence of Blimp1 (Horsley=20 et al., 2006). In this regard, the behavior of bulge stem = cells=20 in response to a loss of Blimp1 in SG progenitors resembles = their=20 response to the epidermis lost upon injury in normal mice. = Such=20 precursor-product relation between the bulge and other skin = stem cell=20 populations has also been documented by engraftment = experiments with=20 isolated bulge stem cells (Blanpain=20 et al., 2004; Claudinot=20 et al., 2005).

Common themes in skin stem = cells
An=20 emerging view of skin stem cells is that there appears to be = at least=20 three distinct niches for skin stem cells: the follicle = bulge, the=20 base of the SG, and the basal layer of the epidermis. It is = not yet=20 resolved whether the basal layer contains a subset of stem = cells as=20 originally posited by Potten=20 (1974) or whether the basal compartment is composed of a = single=20 progenitor population, as more recently proposed by Clayton=20 et al. (2007).

Are there unifying features of keratinocyte stem cells and their = activation mechanisms that guide them along specific = lineages?=20 Although the answer to this question remains unknown, it = seems=20 reasonable to predict that certain features of keratinocyte=20 stem cells and stem cell activation must be similar given the = similarities in stem cell niches.

All three progenitor populations express K5, K14, and p63. = Although=20 p63 has also been implicated in differentiation, p63 remains=20 one of the best candidates to date for a gatekeeper of = proliferation=20 in epithelial stem cells (Truong=20 et al., 2006; Senoo=20 et al., 2007). Cells within all three progenitor pools = also=20 express E-cadherin and display elevated levels of adherens = junctions=20 and reduced levels of desmosomes. A reduction in E-cadherin = appears=20 to be an essential feature in mobilizing embryonic epidermal=20 cells to invaginate to form a hair follicle (Jamora=20 et al., 2003), and reductions in 3D{alpha}=20-catenin and = p120-catenin have=20 also been linked to epithelial cancers, a less organized form = of=20 invagination (Scott=20 and Yap, 2006; Reynolds,=20 2007). Such studies make it tempting to speculate that = the=20 mobilization of stem cells to exit their niches and either = form a=20 hair follicle or repair wounds may entail the remodeling of=20 intercellular junctions.

Additionally, the three progenitor compartments are typified = by=20 their proximity to an underlying basement membrane, and all = three=20 types of progenitors express integrins, including 3D{alpha}=206β4 = and 3β1, as well as their=20 associated proteins. The higher the integrin level, the = greater the=20 proliferative potential seems to be, as judged by the early = studies=20 of Jones=20 et al. (1995) on cultured epidermal stem cells. One = intriguing=20 aspect is the up-regulation of β6 integrin and the = presence of the=20 3D{alpha}vβ6=20 integrin ligand, tenascin C, in the bulge stem cells as they=20 transit from telogen to anagen (Tumbar=20 et al., 2004). Similar changes are seen in the epidermal = basal=20 layer in response to injury (Fassler=20 et al., 1996), leading to the speculation that these = changes=20 might be important in understanding how stem cells become = activated=20 to migrate from their niche and embark upon their specific=20 mission.

Thus, although none of these markers is exclusive to the three=20 progenitor populations, they do appear to be general features = of keratinocytes that maintain their proliferative potential, = whether sustained or transient. It is still formally possible = that expression of these markers empowers keratinocytes to = retain=20 or maintain their proliferative potential and their = stem-ness,=20 in which case down-regulation of these markers might define = a=20 point of no return along a stem cell lineage. As future studies = are=20 conducted, the extent to which this model is correct should = become=20 apparent.

The similarities in keratinocyte stem cell behavior may extend = to=20 shared principles and pathways, even if the precise players = may=20 differ. One example is Blimp1, which appears to mark SG = progenitors=20 and repress c-myc expression (Horsley=20 et al., 2006), whereas Miz1 seems to play a similar=20 c-myc=96repressive function in the epidermal basal layer (Gebhardt=20 et al., 2006). The outcome of c-myc expression is = keratinocyte=20 proliferation in both the SG and epidermis, leading to the = postulate=20 that c-myc might control the conversion of stem cells to=20 so-called TA (i.e., committed) cells (Waikel=20 et al., 2001; Frye=20 et al., 2003). In this regard, it is intriguing that = later in the=20 epidermal lineage, Ovol1, yet another transcriptional = repressor of=20 c-myc, is expressed suprabasally, where it may act to prevent = proliferation after TA cells commit to terminally = differentiate (Nair=20 et al., 2006).

Another signaling pathway likely to impact on more than one=20 keratinocyte stem cell niche is Notch, which controls = selective=20 cell fate determination through close-range interactions not=20 only in the epidermis but also in the hair follicle and the = SG=20 (Yamamoto=20 et al., 2003; Pan=20 et al., 2004; Vauclair=20 et al., 2005; Blanpain=20 et al., 2006; Estrach=20 et al., 2006; Nguyen=20 et al., 2006a). The studies to date support a role for = Notch in=20 activating the keratinocyte switch from the undifferentiated = to=20 differentiated fate (Fig.=20 3).

Although Notch signaling appears to affect the transition from=20 proliferation to differentiation throughout keratinocyte = populations=20 in the skin, other signaling pathways seem to have more = potent=20 effects on one lineage over another. Thus, in the follicle = bulge,=20 stem cells enter the new hair cycle when threshold levels of=20 stabilized β-catenin are reached (Gat=20 et al., 1998; Huelsken=20 et al., 2001; Van=20 Mater et al., 2003; Lo=20 Celso et al., 2004; Lowry=20 et al., 2005; Ito=20 et al., 2007). Conversely, a negative role for Wnt signaling = has=20 been proposed for SG fate determination because SG hyperplasia = occurs=20 when a truncated version of LEF1 is expressed that is unable = to=20 associate with β-catenin (Merrill=20 et al., 2001; Niemann=20 et al., 2002). Although epidermal stem cells are seemingly=20 unaffected by the loss of β-catenin (Huelsken=20 et al., 2001), they adopt a hair follicle cell fate when=20 β-catenin is stabilized through either genetic = manipulation or=20 wounding (Gat=20 et al., 1998; Ito=20 et al., 2007). As outlined in this paper, growth factor = receptor=20 signaling also appears to affect different keratinocyte stem = cell=20 populations in distinct ways.

When taken with the fact that cell fate signaling pathways are=20 often interdependent on one another, such differences can = have=20 a potent impact on lineage determination, as recently = demonstrated=20 by Estrach=20 et al. (2006). In the precortex of the hair follicle, = where Wnt=20 signaling is particularly high (DasGupta=20 and Fuchs, 1999), the Wnt target gene Jag1 is expressed, = leading=20 to active Notch signaling in these cells, promoting = proliferation and=20 differentiation to produce hair (Estrach=20 et al., 2006). Conversely, in the absence of Jag1, hair = follicles=20 fail to form, but the epidermis is spared. Thus, by = activating the=20 expression of other signaling genes, Wnt signaling can = accentuate its=20 effects on a particular lineage within the skin.

In closing, the existence of different skin stem cell = compartments=20 and the ability of these niches to respond differentially to=20 environmental cues has been an exciting new development in = the=20 field. Increasing knowledge about these stem cell populations = over the past 5 yr has begun to shed light on the = similarities=20 and differences among these niches. Important questions for = the=20 future are now raised. Are these different stem cell populations=20 multipotent, as recent experiments by Ito=20 et al. (2007) suggest? Is the multipotency of stem cells = in=20 response to wounding a reflection of mechanical disruption of = the=20 niche or a response to growth/differentiation factors = released in a=20 wound response? To what extent do the gene expression = programs of=20 other progenitor populations overlap with that of follicle = stem=20 cells, and do these similarities reflect their self-renewing, = undifferentiated features? When do these different = proliferative=20 epithelial compartments form during skin development, and to = what=20 extent are their differences in gene expression patterns = dependent on=20 their distinct in vivo microenvironments? What factors = control the=20 differences in the slow-cycling ability of different stem = cell=20 populations within the skin? The answers to these questions = will=20 bring us ever closer in the strife to understanding how stem = cells=20 are maintained in their undifferentiated, growth-restricted = state and=20 what prompts them to become activated, exit their niches, and = embark upon distinct lineages.


3D""    Acknowledgments=20
 
I am grateful to the Fuchs'=20 laboratory, past and present, for their enthusiasm, = dedication, and=20 contributions to the science and research that I have covered = here=20 along with those of many colleagues in the field. A special = thank you=20 goes to Jonathan Nowak, Dr. Valerie Horsley, and Dr. Michael = Rendl=20 for their helpful comments and constructive criticisms. I = also thank=20 Joe Alexander (Information Technology, The Rockefeller=20 University, New York NY) for his assistance in the = artwork.=20

E. Fuchs is an Investigator of the Howard Hughes Medical = Institute=20 and receives support for this research from the National = Institutes=20 of Health, in particular grant R01-AR050452.

Submitted: 28 August 2007

Accepted: 2 December 2007


3D""    References =
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Cross-Browser XMLHttpRequest v1.2=0A= =3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=3D=3D=3D=0A= =0A= Emulate Gecko 'XMLHttpRequest()' functionality in IE and Opera. Opera = requires=0A= the Sun Java Runtime Environment .=0A= =0A= by Andrew Gregory=0A= http://www.scss.com.au/family/andrew/webdesign/xmlhttprequest/=0A= =0A= This work is licensed under the Creative Commons Attribution License. To = view a=0A= copy of this license, visit = http://creativecommons.org/licenses/by-sa/2.5/ or=0A= send a letter to Creative Commons, 559 Nathan Abbott Way, Stanford, = California=0A= 94305, USA.=0A= =0A= Attribution: Leave my name and web address in this script intact.=0A= =0A= Not Supported in Opera=0A= ----------------------=0A= * user/password authentication=0A= * responseXML data member=0A= =0A= Not Fully Supported in Opera=0A= ----------------------------=0A= * async requests=0A= * abort()=0A= * getAllResponseHeaders(), getAllResponseHeader(header)=0A= =0A= */=0A= // IE support=0A= if (window.ActiveXObject && !window.XMLHttpRequest) {=0A= window.XMLHttpRequest =3D function() {=0A= var msxmls =3D new Array(=0A= 'Msxml2.XMLHTTP.5.0',=0A= 'Msxml2.XMLHTTP.4.0',=0A= 'Msxml2.XMLHTTP.3.0',=0A= 'Msxml2.XMLHTTP',=0A= 'Microsoft.XMLHTTP');=0A= for (var i =3D 0; i < msxmls.length; i++) {=0A= try {=0A= return new ActiveXObject(msxmls[i]);=0A= } catch (e) {=0A= }=0A= }=0A= return null;=0A= };=0A= }=0A= // Gecko support=0A= /* ;-) */=0A= // Opera support=0A= if (window.opera && !window.XMLHttpRequest) {=0A= window.XMLHttpRequest =3D function() {=0A= this.readyState =3D 0; // = 0=3Duninitialized,1=3Dloading,2=3Dloaded,3=3Dinteractive,4=3Dcomplete=0A= this.status =3D 0; // HTTP status codes=0A= this.statusText =3D '';=0A= this._headers =3D [];=0A= this._aborted =3D false;=0A= this._async =3D true;=0A= this._defaultCharset =3D 'ISO-8859-1';=0A= this._getCharset =3D function() {=0A= var charset =3D _defaultCharset;=0A= var contentType =3D = this.getResponseHeader('Content-type').toUpperCase();=0A= val =3D contentType.indexOf('CHARSET=3D');=0A= if (val !=3D -1) {=0A= charset =3D contentType.substring(val);=0A= }=0A= val =3D charset.indexOf(';');=0A= if (val !=3D -1) {=0A= charset =3D charset.substring(0, val);=0A= }=0A= val =3D charset.indexOf(',');=0A= if (val !=3D -1) {=0A= charset =3D charset.substring(0, val);=0A= }=0A= return charset;=0A= };=0A= this.abort =3D function() {=0A= this._aborted =3D true;=0A= };=0A= this.getAllResponseHeaders =3D function() {=0A= return this.getAllResponseHeader('*');=0A= };=0A= this.getAllResponseHeader =3D function(header) {=0A= var ret =3D '';=0A= for (var i =3D 0; i < this._headers.length; i++) {=0A= if (header =3D=3D '*' || this._headers[i].h =3D=3D header) {=0A= ret +=3D this._headers[i].h + ': ' + this._headers[i].v + '\n';=0A= }=0A= }=0A= return ret;=0A= };=0A= this.getResponseHeader =3D function(header) {=0A= var ret =3D getAllResponseHeader(header);=0A= var i =3D ret.indexOf('\n');=0A= if (i !=3D -1) {=0A= ret =3D ret.substring(0, i);=0A= }=0A= return ret;=0A= };=0A= this.setRequestHeader =3D function(header, value) {=0A= this._headers[this._headers.length] =3D {h:header, v:value};=0A= };=0A= this.open =3D function(method, url, async, user, password) {=0A= this.method =3D method;=0A= this.url =3D url;=0A= this._async =3D true;=0A= this._aborted =3D false;=0A= this._headers =3D [];=0A= if (arguments.length >=3D 3) {=0A= this._async =3D async;=0A= }=0A= if (arguments.length > 3) {=0A= opera.postError('XMLHttpRequest.open() - user/password not = supported');=0A= }=0A= this.readyState =3D 1;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= };=0A= this.send =3D function(data) {=0A= if (!navigator.javaEnabled()) {=0A= alert("XMLHttpRequest.send() - Java must be installed and = enabled.");=0A= return;=0A= }=0A= if (this._async) {=0A= setTimeout(this._sendasync, 0, this, data);=0A= // this is not really asynchronous and won't execute until the = current=0A= // execution context ends=0A= } else {=0A= this._sendsync(data);=0A= }=0A= }=0A= this._sendasync =3D function(req, data) {=0A= if (!req._aborted) {=0A= req._sendsync(data);=0A= }=0A= };=0A= this._sendsync =3D function(data) {=0A= this.readyState =3D 2;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= // open connection=0A= var url =3D new java.net.URL(new = java.net.URL(window.location.href), this.url);=0A= var conn =3D url.openConnection();=0A= for (var i =3D 0; i < this._headers.length; i++) {=0A= conn.setRequestProperty(this._headers[i].h, this._headers[i].v);=0A= }=0A= this._headers =3D [];=0A= if (this.method =3D=3D 'POST') {=0A= // POST data=0A= conn.setDoOutput(true);=0A= var wr =3D new = java.io.OutputStreamWriter(conn.getOutputStream(), this._getCharset());=0A= wr.write(data);=0A= wr.flush();=0A= wr.close();=0A= }=0A= // read response headers=0A= // NOTE: the getHeaderField() methods always return nulls for me :(=0A= var gotContentEncoding =3D false;=0A= var gotContentLength =3D false;=0A= var gotContentType =3D false;=0A= var gotDate =3D false;=0A= var gotExpiration =3D false;=0A= var gotLastModified =3D false;=0A= for (var i =3D 0; ; i++) {=0A= var hdrName =3D conn.getHeaderFieldKey(i);=0A= var hdrValue =3D conn.getHeaderField(i);=0A= if (hdrName =3D=3D null && hdrValue =3D=3D null) {=0A= break;=0A= }=0A= if (hdrName !=3D null) {=0A= this._headers[this._headers.length] =3D {h:hdrName, = v:hdrValue};=0A= switch (hdrName.toLowerCase()) {=0A= case 'content-encoding': gotContentEncoding =3D true; break;=0A= case 'content-length' : gotContentLength =3D true; break;=0A= case 'content-type' : gotContentType =3D true; break;=0A= case 'date' : gotDate =3D true; break;=0A= case 'expires' : gotExpiration =3D true; break;=0A= case 'last-modified' : gotLastModified =3D true; break;=0A= }=0A= }=0A= }=0A= // try to fill in any missing header information=0A= var val;=0A= val =3D conn.getContentEncoding();=0A= if (val !=3D null && !gotContentEncoding) = this._headers[this._headers.length] =3D {h:'Content-encoding', v:val};=0A= val =3D conn.getContentLength();=0A= if (val !=3D -1 && !gotContentLength) = this._headers[this._headers.length] =3D {h:'Content-length', v:val};=0A= val =3D conn.getContentType();=0A= if (val !=3D null && !gotContentType) = this._headers[this._headers.length] =3D {h:'Content-type', v:val};=0A= val =3D conn.getDate();=0A= if (val !=3D 0 && !gotDate) this._headers[this._headers.length] = =3D {h:'Date', v:(new Date(val)).toUTCString()};=0A= val =3D conn.getExpiration();=0A= if (val !=3D 0 && !gotExpiration) = this._headers[this._headers.length] =3D {h:'Expires', v:(new = Date(val)).toUTCString()};=0A= val =3D conn.getLastModified();=0A= if (val !=3D 0 && !gotLastModified) = this._headers[this._headers.length] =3D {h:'Last-modified', v:(new = Date(val)).toUTCString()};=0A= // read response data=0A= var reqdata =3D '';=0A= var stream =3D conn.getInputStream();=0A= if (stream) {=0A= var reader =3D new java.io.BufferedReader(new = java.io.InputStreamReader(stream, this._getCharset()));=0A= var line;=0A= while ((line =3D reader.readLine()) !=3D null) {=0A= if (this.readyState =3D=3D 2) {=0A= this.readyState =3D 3;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= }=0A= reqdata +=3D line + '\n';=0A= }=0A= reader.close();=0A= this.status =3D 200;=0A= this.statusText =3D 'OK';=0A= this.responseText =3D reqdata;=0A= this.readyState =3D 4;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= if (this.onload) {=0A= this.onload();=0A= }=0A= } else {=0A= // error=0A= this.status =3D 404;=0A= this.statusText =3D 'Not Found';=0A= this.responseText =3D '';=0A= this.readyState =3D 4;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= if (this.onerror) {=0A= this.onerror();=0A= }=0A= }=0A= };=0A= };=0A= }=0A= // ActiveXObject emulation=0A= if (!window.ActiveXObject && window.XMLHttpRequest) {=0A= window.ActiveXObject =3D function(type) {=0A= switch (type.toLowerCase()) {=0A= case 'microsoft.xmlhttp':=0A= case 'msxml2.xmlhttp':=0A= case 'msxml2.xmlhttp.3.0':=0A= case 'msxml2.xmlhttp.4.0':=0A= case 'msxml2.xmlhttp.5.0':=0A= return new XMLHttpRequest();=0A= }=0A= return null;=0A= };=0A= }=0A= ------=_NextPart_000_002D_01C863E8.7F5B46F0 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://www.jcb.org/javascript/ajax/utility.js /************************************************************************= *****=0A= * javascript/ajax/utility.js=0A= *=0A= * Utility functions for working with XMLHttpRequest data.=0A= *=0A= * Copyright 2006 Board of Trustees of the Leland Stanford Junior = University.=0A= = *************************************************************************= ***/=0A= =0A= /*=0A= * Copy XML nodes into an HTMLElement. This effectively=0A= * clones XML markup which uses XHTML naming conventions=0A= * into an HTML DOM.=0A= */=0A= function copy_xml_to_html(src, dst) {=0A= if (src.nodeType =3D=3D 1) { /* Node.ELEMENT_NODE */=0A= var e =3D document.createElement(src.nodeName);=0A= for (var i =3D 0; i < src.childNodes.length; i++) {=0A= copy_xml_to_html(src.childNodes[i], e);=0A= }=0A= for (var i =3D 0; i < src.attributes.length; i++) {=0A= var n =3D src.attributes[i].name;=0A= var v =3D unescape_xml_string(src.attributes[i].value); =0A= e.setAttribute(n, v);=0A= if (n =3D=3D "class") {=0A= e.className =3D v;=0A= }=0A= else if (n =3D=3D "style") {=0A= set_css_style(v, e, "");=0A= }=0A= }=0A= dst.appendChild(e);=0A= }=0A= else if (src.nodeType =3D=3D 3) { /* Node.TEXT_NODE */=0A= dst.appendChild(document.createTextNode(src.nodeValue));=0A= }=0A= }=0A= =0A= /* =0A= * It is unclear that this is the right thing to be calling=0A= * from copy_xml_to_html, but it appears that Safari decides=0A= * to convert & to the NCR #, and then encodes that=0A= * NCR to &%26%2338;. So, I'm going to treat the DOM Attr=0A= * value as a plain string, and run our XML string input=0A= * through the decoding routine below.=0A= */=0A= function unescape_xml_string(s) {=0A= return s.replace(/'/g, "'")=0A= .replace(/'/g, "'")=0A= .replace(/"/g, "\"")=0A= .replace(/"/g, "\"")=0A= .replace(/>/g, ">")=0A= .replace(/>/g, ">")=0A= .replace(/</g, "<")=0A= .replace(/</g, "<")=0A= .replace(/&/g, "&")=0A= .replace(/&/g, "&");=0A= }=0A= =0A= /*=0A= * Parse set of CSS rules and apply them to an element.=0A= * This is quite horrifying, but I'm unable to determine=0A= * how else to handle this with IE 6. FireFox and other=0A= * sane browsers let you simply set the style attribute=0A= * or use e.style.setProperty(rule, value, priority),=0A= * IE 6 appears to have neither of these capabilities..=0A= */=0A= function set_css_style(css, e, priority) {=0A= var rules =3D css.split(";");=0A= for (var i =3D 0; i < rules.length; i++) {=0A= var nvpair =3D rules[i].split(":");=0A= if (nvpair.length =3D=3D 2) {=0A= try {=0A= var name =3D nvpair[0]; /* style attribute */=0A= var value =3D nvpair[1]; /* attribute value */=0A= =0A= /*=0A= * For each possible style attribute, set the=0A= * appropriate style property in the element.=0A= */=0A= if (name =3D=3D "background") {=0A= e.style.background =3D value;=0A= }=0A= else if (name =3D=3D "background-attachment") {=0A= e.style.backgroundAttachment =3D value;=0A= }=0A= else if (name =3D=3D "background-color") {=0A= e.style.backgroundColor =3D value;=0A= }=0A= else if (name =3D=3D "background-image") {=0A= e.style.backgroundImage =3D value;=0A= }=0A= else if (name =3D=3D "background-position") {=0A= e.style.backgroundPosition =3D value;=0A= }=0A= else if (name =3D=3D "background-position-x") {=0A= e.style.backgroundPositionX =3D value;=0A= }=0A= else if (name =3D=3D "background-position-y") {=0A= e.style.backgroundPositionY =3D value;=0A= }=0A= else if (name =3D=3D "background-repeat") {=0A= e.style.backgroundRepeat =3D value;=0A= }=0A= else if (name =3D=3D "behavior") {=0A= e.style.behavior =3D value;=0A= }=0A= else if (name =3D=3D "border") {=0A= e.style.border =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom") {=0A= e.style.borderBottom =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-color") {=0A= e.style.borderBottomColor =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-style") {=0A= e.style.borderBottomStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-width") {=0A= e.style.borderBottomWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-collapse") {=0A= e.style.borderCollapse =3D value;=0A= }=0A= else if (name =3D=3D "border-color") {=0A= e.style.borderColor =3D value;=0A= }=0A= else if (name =3D=3D "border-left") {=0A= e.style.borderLeft =3D value;=0A= }=0A= else if (name =3D=3D "border-left-color") {=0A= e.style.borderLeftColor =3D value;=0A= }=0A= else if (name =3D=3D "border-left-style") {=0A= e.style.borderLeftStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-left-width") {=0A= e.style.borderLeftWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-right") {=0A= e.style.borderRight =3D value;=0A= }=0A= else if (name =3D=3D "border-right-color") {=0A= e.style.borderRightColor =3D value;=0A= }=0A= else if (name =3D=3D "border-right-style") {=0A= e.style.borderRightStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-right-width") {=0A= e.style.borderRightWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-style") {=0A= e.style.borderStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-top") {=0A= e.style.borderTop =3D value;=0A= }=0A= else if (name =3D=3D "border-top-color") {=0A= e.style.borderTopColor =3D value;=0A= }=0A= else if (name =3D=3D "border-top-style") {=0A= e.style.borderTopStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-top-width") {=0A= e.style.borderTopWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-width") {=0A= e.style.borderWidth =3D value;=0A= }=0A= else if (name =3D=3D "bottom") {=0A= e.style.bottom =3D value;=0A= }=0A= else if (name =3D=3D "clear") {=0A= e.style.clear =3D value;=0A= }=0A= else if (name =3D=3D "clip") {=0A= e.style.clip =3D value;=0A= }=0A= else if (name =3D=3D "color") {=0A= e.style.color =3D value;=0A= }=0A= else if (name =3D=3D "cssText") {=0A= e.style.Sets =3D value;=0A= }=0A= else if (name =3D=3D "cursor") {=0A= e.style.cursor =3D value;=0A= }=0A= else if (name =3D=3D "direction") {=0A= e.style.direction =3D value;=0A= }=0A= else if (name =3D=3D "display") {=0A= e.style.display =3D value;=0A= }=0A= else if (name =3D=3D "font") {=0A= e.style.font =3D value;=0A= }=0A= else if (name =3D=3D "font-family") {=0A= e.style.fontFamily =3D value;=0A= }=0A= else if (name =3D=3D "font-size") {=0A= e.style.fontSize =3D value;=0A= }=0A= else if (name =3D=3D "font-style") {=0A= e.style.fontStyle =3D value;=0A= }=0A= else if (name =3D=3D "font-variant") {=0A= e.style.fontVariant =3D value;=0A= }=0A= else if (name =3D=3D "font-weight") {=0A= e.style.fontWeight =3D value;=0A= }=0A= else if (name =3D=3D "height") {=0A= e.style.height =3D value;=0A= }=0A= else if (name =3D=3D "ime-mode") {=0A= e.style.imeMode =3D value;=0A= }=0A= else if (name =3D=3D "layout-flow") {=0A= e.style.layoutFlow =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid") {=0A= e.style.layoutGrid =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-char") {=0A= e.style.layoutGridChar =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-line") {=0A= e.style.layoutGridLine =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-mode") {=0A= e.style.layoutGridMode =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-type") {=0A= e.style.layoutGridType =3D value;=0A= }=0A= else if (name =3D=3D "left") {=0A= e.style.left =3D value;=0A= }=0A= else if (name =3D=3D "letter-spacing") {=0A= e.style.letterSpacing =3D value;=0A= }=0A= else if (name =3D=3D "line-break") {=0A= e.style.lineBreak =3D value;=0A= }=0A= else if (name =3D=3D "line-height") {=0A= e.style.lineHeight =3D value;=0A= }=0A= else if (name =3D=3D "list-style") {=0A= e.style.listStyle =3D value;=0A= }=0A= else if (name =3D=3D "list-style-image") {=0A= e.style.listStyleImage =3D value;=0A= }=0A= else if (name =3D=3D "list-style-position") {=0A= e.style.listStylePosition =3D value;=0A= }=0A= else if (name =3D=3D "list-style-type") {=0A= e.style.listStyleType =3D value;=0A= }=0A= else if (name =3D=3D "margin") {=0A= e.style.margin =3D value;=0A= }=0A= else if (name =3D=3D "margin-bottom") {=0A= e.style.marginBottom =3D value;=0A= }=0A= else if (name =3D=3D "margin-left") {=0A= e.style.marginLeft =3D value;=0A= }=0A= else if (name =3D=3D "margin-right") {=0A= e.style.marginRight =3D value;=0A= }=0A= else if (name =3D=3D "margin-top") {=0A= e.style.marginTop =3D value;=0A= }=0A= else if (name =3D=3D "min-height") {=0A= e.style.minHeight =3D value;=0A= }=0A= else if (name =3D=3D "overflow") {=0A= e.style.overflow =3D value;=0A= }=0A= else if (name =3D=3D "overflow-x") {=0A= e.style.overflowX =3D value;=0A= }=0A= else if (name =3D=3D "overflow-y") {=0A= e.style.overflowY =3D value;=0A= }=0A= else if (name =3D=3D "padding") {=0A= e.style.padding =3D value;=0A= }=0A= else if (name =3D=3D "padding-bottom") {=0A= e.style.paddingBottom =3D value;=0A= }=0A= else if (name =3D=3D "padding-left") {=0A= e.style.paddingLeft =3D value;=0A= }=0A= else if (name =3D=3D "padding-right") {=0A= e.style.paddingRight =3D value;=0A= }=0A= else if (name =3D=3D "padding-top") {=0A= e.style.paddingTop =3D value;=0A= }=0A= else if (name =3D=3D "page-break-after") {=0A= e.style.pageBreakAfter =3D value;=0A= }=0A= else if (name 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