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(Circulation Research. 2003;92:598.)
=A9 2003 = American Heart=20 Association, Inc.

Review

Neural Stem Cells

An Overview

Rossella Galli, Angela=20 Gritti, Luca Bonfanti, Angelo Luigi = Vescovi=20

From the Stem Cell Research Institute (R.G., A.G., = A.L.V.),=20 DIBIT, Hospital San Raffaele, Milan, Italy; and the Department of = Veterinary=20 Morphophysiology (L.B.), Rita Levi Montalcini Center for Brain Repair,=20 University of Turin, Grugliasco, Italy.

Correspondence to Angelo Luigi Vescovi, Stem Cell = Research=20 Institute, DIBIT, Hospital San Raffaele, Via Olgettina 58, Milan, Italy, = 20132.=20 E-mail vescovi.angelo{at}hsr.it


3D*   =20 Abstract
Top
3D*Abstract
Introduction
The Forebrain Subventricular...
The Nature and Origin...
Ex Vivo Behavior of...
Plasticity of NSCs Within...
Plasticity of NSCs Outside...
Conclusions
References
 
T= his=20 review focuses on the nature and functional properties of = stem cells=20 of the adult mammalian central nervous system (CNS). It has = recently=20 been shown that cell turnover, including neurons, does occur = in the=20 mature CNS, thanks to the persistence of precursor cells that = possess=20 the functional characteristics of bona-fide neural stem cells = (NSCs)=20 within restricted brain areas. We discuss how the = subventricular zone=20 of the forebrain (SVZ) is the most active neurogenetic area = and the=20 richest source of NSCs. These NSCs ensure a life-long = contribution of=20 new neurons to the olfactory bulb and, when placed in = culture, can be=20 grown and extensively expanded for months, allowing the=20 generation of stem cell lines, which maintain stable and = constant=20 functional properties. A survey of the differentiation = potential of=20 these NSCs, both in vitro and in vivo, outlines their extreme = plasticity that seems to outstretch the brain boundaries, so = that=20 these neuroectodermal stem cells may give rise to cells that=20 derive from developmentally distinct tissues. A critical=20 discussion of the latest, controversial findings regarding = this=20 surprising phenomenon is provided.


Key Words: stem cells =95 transdifferentiation = =95=20 neurogenesis


3D*   =20 Introduction
Top
Abstract
3D*Introduction
The Forebrain Subventricular...
The Nature and Origin...
Ex Vivo Behavior of...
Plasticity of NSCs Within...
Plasticity of NSCs Outside...
Conclusions
References
 
T= he=20 nervous tissue, particularly that of the central nervous = system=20 (CNS), is endowed with several peculiar characteristics that = make it=20 unique among the other bodily tissues. Ultimately, these = properties=20 relate to the CNS heterogeneous cell composition that = underlies the=20 elaboration of an enormous amount of information into a = complex=20 output. Historically, this complexity has been seen = inextricably=20 linked to the lack of any cell turnover in the adult = brain.=20

The dogmatic view of an ever-immutable neural tissue in mammals = is=20 now been replaced by the notion that cell replacement occurs = within=20 specific brain regions throughout adulthood. This continuous=20 neurogenetic process is sustained by the life-long = persistence=20 of neural stem cells (NSCs) within restricted CNS areas. =

In the adult mammalian brain, the genesis of new neurons has = been=20 consistently documented in the subgranular layer of the = dentate gyrus=20 of the hippocampus1=20 and the subventricular zone (SVZ) of the lateral = ventricles.1=963=20 From=20 the SVZ, newly generated neurons reach their final = destination in the=20 olfactory bulb after long-distance migration through a = well-defined=20 path called the rostral migratory stream (RMS)2,3=20 (Fi= gure=20 1). The SVZ is the adult brain region with the highest=20 neurogenetic rate, from which NSCs have been firstly = isolated4=20 and characterized for their ability to give rise to = non-neural=20 cells.5=967=20 Thus,=20 in this review we shall focus our attention on SVZ-derived = NSCs.=20



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  		Figure 1. A, Global view = of the=20 adult rodent brain that depicts (in gray) the regions within = which=20 continuous neurogenesis occurs throughout adulthood, namely = the=20 olfactory bulb (OB) and the hippocampus (H). Areas that are = known to=20 contain NSCs are outlined in black: the subventricular zone = (SVZ)=20 with its rostral extension reaching the OB and the dentate = gyrus=20 (DG) of the hippocampus. B, Schematic sagittal section of = the adult=20 rodent brain through the SVZ-RE system; the dotted line = outlines the=20 contour of the lateral ventricle (LV). The SVZ is composed = of a=20 posterior part (dark gray) lining the lateral ventricle = (SVZ-LV) and=20 an anterior part (light gray) forming the rostral extension=20 (SVZ-RE). CC indicates corpus callosum; CX, cerebral cortex; = and OB,=20 olfactory bulb. C, Transverse sections of the SVZ at the = levels 1=20 and 2 as indicated in A and B; 1, SVZ-RE, 2, SVZ of the = lateral=20 ventricle (LV; see also Fi= gure=20 2A). Glial tubes are in black; CH, chains of neuronal=20 precursors; CC, corpus callosum; e, ependymal monolayer. D,=20 Schematic representation of the chains of migrating = neuroblasts=20 within the astroglial tubes (in black). Tubes are not = present in the=20 distal tip of the OB (gray shadowed area), within which the=20 neuroblasts depart from the terminal end of the tubes, leave = the=20 chains by detaching from each other, and migrate outwardly=20 (radially) as isolated cells (n) through the OB parenchyma. = T=20 indicates tangential chain migration; R, radial migration; = N,=20 differentiated neurons in the olfactory bulb; SC, area in = which the=20 stem cells are found; and MP, area containing migrating = precursors=20 but not NSCs (modified from Peretto P, Merighi A, Fasolo A, = Bonfanti=20 L. The subependymal layer in rodents: a site of structural=20 plasticity and cell migration in the adult mammalian brain. = Brain=20 Res Bull. 1999;49:221=96243). =



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  		Figure 2. Neural stem = cells of the=20 adult rodent brain. A, Transverse section through the=20 periventricular SVZ is shown. This section corresponds to = the plane=20 section 2 as shown in Fi= gure=20 1. V indicates ventricle; SVZ, subventricular zone. = Arrows point=20 to some of the proliferating cells in the SVZ that were = labeled=20 after intraperitoneal injection of the thymidine analogue,=20 5-bromodeoxyuridine. SVZ contains fast and slow = proliferating=20 precursor populations with a cell cycle time comprised = between 12=20 hours and 28 days. B through D, Stem cells isolated from the = SVZ are=20 shown in serum-free cultures in the presence of both EGF and = FGF2.=20 Under these conditions, stem cells undergo proliferation, = eventually=20 giving rise to neurospheres. One day (B), 4 days (C), 7 days = (D)=20 after plating. E, On removal of growth factors and plating = onto a=20 laminin-coated substrate, cells in the sphere differentiate = into=20 mature brain cells that express the typical markers of = neurons (red,=20 =DF-tubulin), astrocytes (green, glial fibrillary acidic = protein), and=20 oligodendrocytes (blue, O4). Bars: A=3D100 =B5m; B and = C=3D20 =B5m (bar in=20 B); E=3D30 =B5m. =

Lately, the "antidogmatic" nature of NSCs has emerged twice.=20 Although the scenario is gradually changing,8=9610=20 the=20 lack of specific markers has long hampered the univocal=20 identification and characterization of NSCs. However, the use = of=20 specific systems has permitted the isolation and impressive = expansion=20 of NSCs ex vivo=97quite a striking phenomenon for cells of = the=20 most quiescent bodily tissue. This has allowed the = establishment=20 of NSC lines from various species, including humans, that are = being used to explore novel therapeutic strategies to treat=20 neurological disorders (see reviews1,11,12=20 )=20 as well as trigged an impressive plethora of studies = investigating=20 the differentiation potential of NSCs, which may be broader = than=20 expected. In fact, an impressive example of the extreme = developmental=20 potential of NSCs may have been provided by studies in which = NSCs=20 appear to generate cell types that belong to developmentally=20 unrelated tissues=97a concept that may also apply to stem = cells=20 from the hemopoietic system and from other adult = tissues.


3D*    The=20 Forebrain Subventricular Zone as a Source of Adult NSCs: A "Brain = Marrow"=20 Case?
Top
Abstract
Introduction
3D*The Forebrain = Subventricular...
The Nature and Origin...
Ex Vivo Behavior of...
Plasticity of NSCs Within...
Plasticity of NSCs Outside...
Conclusions
References
 
I= n the=20 mammalian adult brain, the genesis of new neurons continues=20 throughout life within two 3-layered cortical regions, the=20 hippocampus and olfactory bulb (OB), where it is sustained by = endogenous stem cells. The most active NSC compartment is = found in=20 SVZ. This area represents a remnant of the embryonic germinal = neuroepithelium, which persists throughout life as an = actively=20 mitotic layer in the wall of the telencephalic lateral = ventricles and=20 along its rostral extension toward the olfactory bulb (Fi= gure=20 1). A complete turnover of the resident proliferating = cell=20 population occurs every 12 to 28 days in the SVZ,13=20 with about 30 000 new neuronal precursors (neuroblasts) being = produced every day and migrating to the OB3=20 (Fi= gure=20 1).

Two main cell types are found in the SVZ: migratory, = proliferating=20 neuroblasts and astrocytes (Fi= gure=20 1). The latter form a meshwork throughout the whole SVZ = and are=20 organized into channels that are oriented along the = anteroposterior=20 axis and are called glial tubes.14=9616=20 Within=20 these glial tubes, NSC-generated neuroblasts undergo = rostraward,=20 tangential migration as cells grouped into tightly packed = chains.14,17=20 Eventually,=20 neuroblasts reach the distal tip of the OB, separate from = each other=20 and leave the tubes, shifting their migration pattern from=20 tangential to radial. In this way, they reach the more = superficial OB=20 layers and terminally differentiate into granule and=20 periglomerular neurons. Importantly, tangential migration = toward the=20 OB has also been documented in the adult brain of primates18,19=20 and=20 even in the infant human brain.20=20 Also, the possible migration of cells from the SVZ to the = neocortex=20 has been proposed in mouse21,22=20 as=20 well as in adult macaque monkeys,23=9625=20 although=20 this view has recently been questioned.18=20

Glial tubes are composed of a special type of astroglia that=20 expresses the marker of mature CNS astrocytes, namely glial=20 fibrillary acidic protein (GFAP), but also contain the = cytoskeletal=20 proteins vimentin and nestin.16,17=20 The=20 presence in glial tubes of such molecules, known to abound in = those=20 immature and radial glial cells that guide young neurons = during CNS=20 development, suggested a role for glial tubes in influencing = the=20 migration/guidance of neuroblasts in the SVZ. However, the = actual=20 role of astroglial cells in this process remains unclear.26=20 They may simply act as a barrier to prevent neuroblasts from = escaping=20 the proper migratory route before they reach the OBs.17=20 Although the presence of astrocytes is not essential for = chain=20 migration,27=20 they do secrete factors that facilitate this process.28=20 Notably, astroglial tubes and NSCs do not coexist solely = within the=20 periventricular aspect of the SVZ but also within the rostral = migratory stream that extends into the OB,29=20 with the former perhaps contributing to create an appropriate = stem=20 cell "niche" for the maintenance of NSCs all along the = pathway.=20

In an appealing functional/structural parallelism with the = hemopoietic=20 system, it has been proposed to use terms like "neuropoiesis" = to portray the persistence of neurogenesis in adulthood, and=20 "brain marrow" to describe the anatomical regions that = contain=20 the NSCs supporting neurogenesis.30,31=20 Thus,=20 whereas hematopoiesis takes place within the boundaries of = the marrow=20 in the deep adult bone, adult neurogenesis is a spatially = confined=20 process, constrained within the boundaries of the brain-deep = SVZ.=20 In both "marrows", we can find (1) proliferating = stem/progenitor=20 cells, (2) cell types, which can carry out stromal = function(s),=20 and (3) extracellular matrix that can modulate cell = proliferation,=20 adhesion, and migration. Stromal cells of the bone marrow are = known to act as an interface between peripheral blood and the = stem/progenitor pool, thus modulating the fate of = hematopoietic=20 stem cells (HSCs). In a similar fashion, astrocytes and = ependymal=20 cells of the SVZ may act as "stromal" elements of the CNS by=20 producing molecules as bone morphogenetic proteins that = affect=20 the neuronal versus glial fate of the stem/progenitor cells.32=20 Furthermore, the extracellular matrix of both the SVZ and = bone=20 marrow contains tenascin and proteoglycans, molecules that = are=20 important in the formation of developmental compartments and = in=20 the control of cell adhesion, migration and differentiation.15,30,31,33=20 Finally,=20 similarly to the bone marrow, the proximity of the SVZ with = the=20 cerebrospinal fluid, the enlarged intercellular spaces, the = reduced=20 cell-cell contacts,15,16,19=20 and=20 the presence of molecules linked to water cotransport34,35=20 contribute=20 to create in the SVZ a cytoarchitectural/biochemical niche,=20 which is very different from the environment of the mature = CNS=20 parenchyma.


3D*    The=20 Nature and Origin of the Adult Neural Stem Cell In Vivo=20
Top
Abstract
Introduction
The Forebrain Subventricular...
3D*=20The Nature and = Origin...
Ex Vivo Behavior of...
Plasticity of NSCs Within...
Plasticity of NSCs Outside...
Conclusions
References
 
A= series=20 of observations indicate that a specific subtype of SVZ = astroglial=20 cells is the actual NSC36=20 (see review26).=20 In fact, after the killing of all the proliferating SVZ=20 neuroblasts by administration of subdural, cytotoxic doses of = antimitotic drugs, only astroglial cells were left, which=20 surprisingly, were shown to be able to regenerate the entire = SVZ cell=20 system. According to this view, some of the SVZ astrocytes = (named=20 type B cells) are thought to represent relatively quiescent = stem=20 cells that normally proliferate at a low rate and generate = the=20 neuronal precursors (type A cells), through the generation of = a=20 third, intermediate cell type: the C cell (or D cell in the=20 hippocampus37),=20 which has the characteristics of the classic, = fast-proliferating,=20 transit-amplifying progenitor cells found in many = self-renewing=20 tissues.36,38,39=20 Taking=20 into account the immature features of SVZ astrocytes16,17,36=20 and=20 the fact that radial glia of the developing cerebral cortex = can act=20 as a bipotent stem cell,40=20 it is most likely that NSCs originate from type B cells that = retain=20 radial glia-like features within specific regions of the = adult brain=20 (see review38).=20

It should be emphasized, however, that NSCs can also be isolated = and grown in vitro from nonneurogenic periventricular = regions,=20 in which the mature parenchyma is directly in contact with = the=20 ependymal monolayer, such as the fourth ventricle or the = spinal=20 cord.41=20 These findings may indicate that cells endowed with some = extent of=20 stem-like potential may exist throughout the whole adult CNS = tissue.=20 However, only those NSCs that occur within adult brain areas = that=20 retain a brain marrow-like environment, as the SVZ, take up = an actual=20 stem-cell behavior, self-renew, and generate a mature progeny = in=20 vivo, whereas those residing within nonneurogenetic regions = may=20 remain dormant.42=9644=20


3D*    Ex=20 Vivo Behavior of NSCs
Top
Abstract
Introduction
The Forebrain Subventricular...
The Nature and Origin...
3D*Ex Vivo Behavior = of...
Plasticity of NSCs Within...
Plasticity of NSCs Outside...
Conclusions
References
 
T= o carry=20 out the vital function of maintaining cell homeostasis and = integrity=20 throughout life, stem cells are endowed with peculiar = functional=20 characteristics that provide suitable criteria to identify = and=20 classify them. In fact, stem cells are highly undifferentiated = cells=20 possessing a significant proliferation potential, a broad=20 developmental fate, and most and foremost, an intrinsic = capacity=20 for self-perpetuation=97better defined as self-maintenance = or=20 self-renewal=97throughout adulthood.39=20

Historically, hemopoietic stem cells (HSCs) have been the first = to=20 provide a useful prototypic functional model in order to = devise=20 conceptual and practical strategies to tackle investigations = on other=20 stem cell types.45=20 When comparing HSCs and NSCs with regard to their functions, = the two=20 systems appear to sit at opposite sides of the functional = spectrum.=20 Because enormous amounts of new blood cells are generated = every day=20 from stem cells of the hemopoietic tissue(s), it has been = possible=20 to develop an in vivo functional assay by which bona fide = stem=20 cells (even a single candidate cell46)=20 have been identified for their capacity to reconstitute the=20 hemopoietic stem compartment after its deadly experimental = ablation.=20 Moreover, a reliable antigenic fingerprint based on the = expression of=20 multiple, lineage-specific markers is now available to = distinguish=20 various hemopoietic precursors. However, one of the most = significant=20 hurdles in the field of HSCs is their resilience to undergo = extensive=20 proliferation in culture.

Fascinatingly, a mirror-like situation has emerged in the field = of=20 NSCs. Given the relative overall quiescence and=20 structural/cytoarchitectural "rigidity" of the brain = parenchyma, the=20 classical hemopoietic experimental paradigms of = reconstitution of=20 ablated stem cell compartments are rarely used to investigate = and=20 characterize NSCs. Thus, the study of NSCs received much of = its=20 initial impulse from in vitro findings that firstly = demonstrated and=20 exploited the amazing proliferation capacity that NSCs = display in=20 culture.

Under appropriate conditions and in the presence of mitogens=20 (epidermal growth factor (EGF) and/or fibroblast growth = factor=20 2 [FGF2]), it is possible to induce the proliferation of = rapidly=20 dividing precursors from the SVZ. At least in vitro, these = precursors=20 fulfill most of the criteria of bona fide stem cells.47=9649=20 Lately,=20 these cultured NSCs have been suggested to derive from the C = type=20 cells of the SVZ.50=20 Since in vivo type C cells represent transit-amplifying = progenitors=20 rather than bona fide stem cells, the concept has been put = forth for=20 the possibility that tissue culturing and/or mitogens can = re-awake a=20 latent stem cell program in what can be considered "potential = stem cells."39=20 On removal of the mitogens, the progeny of NSCs promptly=20 differentiate into the three main cell types of the CNS = (astrocytes,=20 oligodendrocytes, and neurons) (Fi= gure=20 2).36,42,51=9654=20 It=20 should be noted that similar results could be obtained with = adult=20 hippocampal cells.55=20

The most important concept regarding this method is that it=20 represents a selective system by which, in a heterogeneous = primary=20 culture, the more committed progenitors and/or differentiated = mature cells rapidly die and thus are eliminated, whereas the = undifferentiated NSCs are positively selected and forced to=20 access a state of active proliferation.12=20 NSCs start proliferating initially as adherent cells and = attach to=20 each other, eventually giving rise to spherical clusters that = float=20 in suspension and form the so-called "neurospheres." In = giving rise=20 to neurospheres, NSCs undergo multiple symmetric cell = divisions by=20 which two new NSCs are generated at each cycle (Fi= gure=20 3). It should be noted that not all the NSC progeny found = in a=20 neurosphere are stem cells. Indeed, only 10% to 50% of these = progeny=20 retain stem cell features, whereas the remainders are cells = that=20 undergo spontaneous differentiation. Consequently, a = neurosphere=20 is a mixture of NSCs, differentiating progenitors, and even=20 differentiated neurons and glia, depending on the neurosphere = size=20 and time in culture. This is the reason why neurospheres are=20 subcultured by harvesting, followed by mechanical = dissociation and by=20 re-plating under the same growth conditions. As in the = primary=20 culture, differentiating/differentiated cells rapidly die = while the=20 NSCs continue to proliferate, giving rise to many secondary=20 spheres and exponential growth in vitro. In this way, stable = NSCs=20 cell lines can be obtained.12=20



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  		Figure 3. Schematic = outline of how=20 stem cell expansion is achieved in cultured neural stem = cells. A,=20 Under serum-free conditions and in the sustained presence of = mitogens such as EGF and/or FGF2, NSCs (red, S) are thought = to=20 undergo symmetric divisions in which either (i) two more=20 differentiated cells (likely transient amplifying = precursors, green,=20 T) (symmetric differentiative divisions) or (ii) two NSCs = are=20 generated (symmetric proliferative divisions); (iii) = asymmetric=20 cycles giving rise to one NSC and to one more differentiated = (not=20 shown) or apoptotic cell (yellow) can also take place at the = same=20 time. If within a NSC population the frequency of = proliferative=20 cycles equals that of differentiative divisions, the overall = number=20 of NSCs within the pool is maintained at a steady level39;=20 (iv) under the conditions used for NSCs expansion, the = number of=20 proliferative divisions normally exceeds that of = differentiative=20 cycles, so that an increasing number of NSCs is generated = within the=20 stem cell pool at each cell generation. B, Starting from a = single=20 NSC (red) all the types of cell division described in A = concur to=20 the formation a clonal cluster of cells called neurosphere.=20 Therefore, each neurosphere contains a mixture of many NSCs, = as well=20 as transient amplifying precursors (green) and dead/dying = cells=20 (yellow). When neurospheres are dissociated, all but the = stem cells=20 die (light blue shadowed area), due to the stringent culture = conditions, whereas NSCs continue to proliferate, giving = rise to=20 more, secondary neurospheres. This procedure can be repeated = sequentially over many months, resulting in an exponential = increase=20 in the overall number of NSCs and in the establishment of = NSC stable=20 cell lines. =

Due to these properties, it has been possible to establish = continuous=20 mouse transgenic/genetically modified56=20 or human NSC lines57,58=20 that=20 expand merely by growth factor stimulation and under completely=20 chemically defined conditions. In particular, human NSC lines = represent a renewable source of normal nervous cells that = might=20 facilitate basic studies on human neurogenesis and drug = discovery=20 and, remarkably, may virtually eliminate the need of fetal = human=20 tissue for therapeutic neural transplantation. It is well = known=20 that some CNS disorders may require grafting of specific = neuronal=20 subtypes. Notably, human NSCs, which are available in huge = amount=20 as compared with fetal tissues, can be easily induced to=20 differentiate into specific cell types and/or = neurotransmitter=20 phenotypes by simply modifying the culture medium. For = example,=20 NSC-derived GABAergic neurons could be used to replace = GABAergic=20 spiny neurons lost in Huntington=92s disease. Similarly, we = have=20 been able to induce a significant fraction of the progeny of=20 various human NSC lines to express catecholaminergic neuronal = features59=20 that may prove useful for cell replacement therapy in = Parkinson=92s=20 disease. Very recently, human NSCs have been shown to = efficiently=20 integrate in the adult rat brain where they differentiated = acquiring=20 a cholinergic phenotype.60=20 Thus, in addition to markedly reducing the use of human fetal = brain=20 tissue, stem cell lines may eventually eliminate the need for = tissue=20 exclusively from selected embryonic regions.

The issues discussed so far prompt some final remarks as to = the=20 classification of NSCs with respect to their ex vivo behavior.=20 Recently, the identification of putative NSC markers as = AC133,=20 PNAlow/HSAlow, and LeX/ssea-18=9610=20 has=20 provided researchers with a valuable tool for identifying and = enriching bona fide NSCs. This antigenic characterization = will=20 eventually help to resolve the state of confusion in the NSC = area in=20 which classification based on functional approaches presents = severe=20 limitations due to the different techniques, the variety of = the brain=20 regions investigated, and the variable ages of the donors = yielding=20 the isolation of different precursor cell types that all=20 promiscuously go by the name of NSCs.

Once again, it is tempting to borrow from the hemopoietic field, = in which a lineage of stem cells endowed with progressively=20 narrowing self-renewal capacities has clearly been defined.61=20 Although limited to the in vitro studies and mainly for = practical=20 purposes, we speculate that a similar criterion of = classification=20 may be initially assumed for NSCs, thus identifying them as=20 long-term or short-term self-renewing NSCs based on the = extent=20 of their self-maintenance ability in culture. At this point, = we=20 ought to remember that (1) challenging a cell in vitro only = unveils=20 its developmental potential and not its actual in vivo fate, = and (2)=20 the extent by which a cell can self-renew in vitro may depend = on the=20 culture conditions adopted. Nevertheless, it has also emerged = that=20 some NSCs from distinct regions display clearly distinct = self-renewal=20 capacities under identical culture conditions, thus lending = to the=20 attempt to classify cultured NSCs based on the self-renewal = capacity=20 that they display in vitro.62,63=20


3D*   =20 Plasticity of NSCs Within the CNS =
Top
Abstract
Introduction
The Forebrain Subventricular...
The Nature and Origin...
Ex Vivo Behavior of...
3D*Plasticity of NSCs = Within...
Plasticity of NSCs Outside...
Conclusions
References
 
A= lthough=20 in vivo NSCs appear to generate almost exclusively neuronal = cells,=20 their actual developmental potential as observed ex vivo is = much=20 broader than expected. In fact, cultured NSCs do give rise to = neurons, astrocytes, and oligodendrocytes and are therefore = normally=20 classified as being multipotent in nature. The concept of NSC = plasticity and of their dependence on environmental cues is=20 strengthened by transplantation and manipulation/recruitment = studies=20 in vivo. For example, intrahippocampus transplantation of = hippocampal=20 stem cells results in the generation of the neuronal types = normally=20 found within this region.55=20 However, if the same hippocampal stem cells are transplanted=20 heterotopically, that is into the SVZ, they produce cell = types that=20 are normally found in the latter, rather than hippocampal = ones.55=20 Further, when transplanted in adult brain regions in which no = neurogenesis takes place, NSCs produce exclusively glial = cells. After=20 intracerebral administration of growth factors, namely EGF,64=20 FGF2,65=20 or transforming growth factor-3D{alpha}=20 = (TGF-),66=20 the proliferation of cells in the SVZ is dramatically = increased and=20 the fate of the progeny can change depending on the type of = factor(s)=20 used. In particular, EGF infusion results in an increased = production=20 of cells in the SVZ, in a diversion of their migration = pattern from=20 tangential to radial,65=20 and in the eventual generation of cells of the glial lineage = rather=20 than neurons.64,65=20 These=20 findings altogether re-emphasize the concept expressed = earlier in=20 this review that NSCs appear to possess a rather broad = developmental=20 potential and functional repertoire whose expression is = strongly=20 influenced by extracellular cues.


3D*   =20 Plasticity of NSCs Outside the CNS =
Top
Abstract
Introduction
The Forebrain Subventricular...
The Nature and Origin...
Ex Vivo Behavior of...
Plasticity of NSCs Within...
3D*Plasticity of NSCs = Outside...
Conclusions
References
 
S= ome=20 important considerations have emerged so far. First, the = nervous=20 tissue contains bona fide stem cells that support neuronal = cell=20 turnover throughout life. Second, despite their origin from = one of=20 the most quiescent tissues in the body, NSCs can undergo = effective=20 long-term culturing, proliferation and expansion while = retaining=20 stable functional characteristics. Third, when properly = challenged,=20 the overall developmental potential appears to be broader = than that=20 observed under physiological conditions in vivo.

This section reviews recent observations suggesting that this=20 plasticity may perhaps outstretch the brain boundaries, so = that=20 NSCs (neuroectodermal in origin) can give rise to cells that=20 normally derive from germ layers other than the = neuroectoderm.=20 This is discussed later, in the more general perspective that = many somatic stem cells may give rise to cells of an = embryonic=20 origin different from their own. One of the most intriguing=20 cases is the virtual pluripotency of bone marrow=96derived=20 cells67;=20 however, multiple examples of SCs giving rise to cells = normally found=20 in other tissues have become available. In some cases, both = the=20 original SCs and the cells to which they give rise derive = from the=20 same embryonic germ layer (intragerm layer conversion). For = instance,=20 intramesoderm conversion has been documented by showing the = genesis=20 of skeletal68=20 or cardiac muscle cells from bone marrow cells.69=20 Similarly, muscle precursors can give rise to hematopoietic = cells,70=9672=20 although=20 it has now been shown that the original muscle population = undergoing=20 conversion are Sca-1 and CD45-positive cells, which are = hemopoietic=20 in origin.71,73=20 Finally,=20 muscle satellite cells retain an osteogenic and adipogenic=20 differentiation potential that is normally retrieved in=20 mesoderm-derived stromal cells.74=20

More striking examples of transgerm layer conversion=97hereby = also=20 defined as transdifferentiation=97in which SCs and their = progeny belong=20 to developmentally unrelated cell lineages have been reported = (Ta= ble).=20 Thus, mesoderm-derived mesenchymal stem cells appear to = generate=20 astrocytes and neurons, both in vivo75=20 and in vitro,76,77=20 and=20 bone marrow SCs can give rise to endoderm-derived liver = cells.78,79=20 Of=20 note, Wagers et al80=20 have recently demonstrated that, in the absence of a = tissue-specific=20 lesion, there is not appreciable contribution of single = repopulating=20 hematopoietic stem cell to nonhemopoietic tissues, suggesting = that the production of nonhemopoietic cell types is not a=20 physiological function of HSCs. Nonetheless, in the presence = of=20 sustained damage as caused by lethal irradiation, adult bone = marrow=20 cells were found to integrate and differentiate within the = brain=20 tissue after systemic injection. In these mice, 0.2% to 0.3% = of=20 the total neurons in the olfactory bulbs appeared to derive = from=20 the bone marrow cells.81=20 In a similar study, bone marrow cells from wild-type male = mice were=20 injected intraperitoneally in PU.1-mutant, immunodeficient = females.82=20 In these animals, 0.2% to 2.3% of the male cells found within = the=20 brain parenchyma expressed neuronal markers.82,83=20 Nonetheless,=20 a recent report by Castro et al84=20 has questioned the "blood-into-brain" conversion. These = authors=20 failed in detecting side population or unfractionated donor = bone=20 marrow cells integration in the brain of lethally irradiated = mice=20 even after injury. Importantly, in the same experimental = model,=20 blood-into-muscle conversion appeared to take place. At = present, this=20 issue remains open for discussion, although it is perhaps = possible to=20 infer that we are dealing with a rather rare phenomenon that = takes=20 place only under specific conditions with a low frequency, = whose=20 detection may be elusive under certain circumstances, but = which seems=20 to be effective also in humans.85=20


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  		Table 1. Somatic Stem = Cells Give=20 Rise to Mature Progeny That May Belong to Other Tissues and = Organs,=20 Also of a Distinct Embryological Origin=20

A similar situation has arisen in a neighboring area that is = the=20 field of investigation in which the opposite phenomenon, ie,=20 brain-to-blood conversion, is studied. The initial discovery = that=20 transgerm layer differentiation can occur in adult mammals = came from=20 cells that were derived from the adult brain. In 1999, we = reported=20 that clonally derived adult NSCs could give rise to = hematopoietic=20 cells in vivo.5=20 In these experiments, the progeny of genetically tagged (ie,=20 constitutively expressing =DF-galactosidase, the product of = the=20 bacterial LacZ gene), single NSCs were injected into=20 sublethally irradiated mice. NSCs integrate into many of the = host=20 hematopoietic tissues, including spleen, thymus, and bone = marrow and=20 gave rise to various types of blood progenitors. These = progenitors=20 did eventually differentiate into a wide range of blood = cells,=20 including megacaryocytes, granulocytes, macrophages, and B- = and=20 T-lymphocytes; however, erythroid cells were not observed.=20 Furthermore, although not described in the initial study (R. = Rietze,=20 C.R. Bjornson, A.L. Vescovi, unpublished observations, 2002), = NSCs=20 increased viability in recipient animals, suggesting that = they may=20 partially reconstitute and, in fact, rescue lethally = irradiated=20 animals. It is worth noting that neurohemopoietic conversion = has now=20 been documented also by using human NSCs.7=20 These cells were transplanted into SCID-Hu mice, which carry=20 transplanted human fetal bone and thymic fragments, thus = providing=20 physiologically relevant human bone marrow and thymic=20 microenvironments. Under these conditions, human NSCs were = able to=20 establish long-term hemopoiesis, as shown by serial = reconstitution=20 experiments.7=20 In further support of brain into blood conversion, a recent=20 work has provided evidence that hematopoietic epigenetic = factors=20 can induce human fetal neural tissues to give rise to blood=20 cells in vitro and that this wider lineage potential is=20 characteristic of the AC133-positive fraction.86=20

Rather peculiar circumstances appear to be necessary for the=20 expression of the latent, broad developmental potential of = NSCs=20 that underlies neuromesodermal transdifferentiation. First, = it=20 appears that only bona fide stem cells can undergo = transdifferentiation.=20 As described in Galli et al,6=20 only SVZ cells, but not cells from regions that do not appear = to=20 contain actual stem cells, such as the striatum and the = cerebral=20 cortex, undergo neuromyogenic conversion. This was confirmed = by=20 Rietze et al,9=20 who enriched their cultures for NSCs by cell surface markers=20 (PNAlo/HSAlo) and showed how this = resulted in=20 an increased neuromyogenic conversion rate=97from 2.5%6=20 to 57% of the total cells. Furthermore, when the = differentiated=20 progeny of NSCs were exposed to the same cues that induce = myogenesis=20 in enriched NSC cultures, negligible conversion to skeletal = muscle,=20 if any, was observed.6=20

The fact that only NSCs, but not their differentiated neuronal = or=20 glial progeny, can give rise to nonneural cells6=20 highlights an important difference between this phenomenon = and=20 transdifferentiation as conceived in a classical view. In = fact,=20 transdifferentiation implies the ability of differentiated = cells to=20 acquire a new identity by turning off one set of = lineage-specific=20 genes and activating genes of another differentiated cell = type. The=20 two sets of antigens sometimes colocalize in cells undergoing = transdifferentiation. Conversely, transgerm layer = differentiation=20 seems to reflect the de novo expression of a broader = developmental=20 potential of NSCs that may become evident only under peculiar = conditions. Accordingly, no molecular and biochemical = overlapping of=20 specific neural and nonneural markers were ever observed in = either=20 NSCs or their nonneural progeny. Thus, markers of = hematopoietic=20 precursors were not detected in NSCs before they were = injected into=20 injured animals,5=20 and expression of muscle determination factors or other = muscle=20 differentiation markers such as MyoD, Myf5, myogenin, and = myosin was=20 never observed in NSCs before their exposure to myogenic=20 environments.6=20 Similarly, lack of expression of mesodermal and endodermal = antigens,=20 such as TROMA-1, was detected in NSCs before injection into = the=20 developing blastula,87=20 yet these cells can give rise to derivatives from both these=20 germ layers.

It can be speculated that, in order to undergo transgerm layer=20 differentiation, NSCs ought to be exposed to = microenvironments=20 that contain rather peculiar, as yet unidentified cues. CNS=20 stem cells have been shown to repopulate the injured = hemopoietic=20 system5=20 and muscles.6=20 Similarly, bone marrow cells regenerate the muscle and = liver68,78=20 only=20 in the presence of an injury.80=20 Hence, it can be argued that specific instructive cues may = become=20 available during the early and regenerative phases that = follow=20 an injury in a given adult tissue, which may resemble those=20 found in embryonic development. Importantly, recent data = suggest=20 that transgerm layer differentiation might be an integral = part=20 of tissue regeneration when happening in a physiological = context,=20 like the regenerating tail in amphibians.88=20 In this system, neuroectodermal radial glial cells, which = normally=20 regenerate the spinal cord after tail amputation, also = contribute to=20 mesoderm lineages such as cartilage and, more intriguingly, = muscle.=20 This study suggests that the existence of a blastema (ie,=20 undifferentiated proliferative cells) in a regenerative = milieu is=20 most likely accountable for this phenomenon, which resembles = or can=20 be considered neuromesodermal transdifferentiation. One = significant=20 hurdle in the identification of the cues involved in=20 neuromesodermal conversion depends on the fact that most of = the=20 models used rely on in vivo assays. Yet, in vitro models of=20 neuromesodermic conversion are now available that allow for = some=20 tentative hypotheses to be drawn.6=20 Using these systems, it has emerged that neuromesodermal = conversion=20 could only be observed when NSCs were cocultured with C2C12 = myogenic=20 cells or with primary myoblasts=97and never with other cell = types.=20 Furthermore, when NSCs underwent myogenic induction as = clustered=20 cells into neurospheres, the proportion of cells that = converted to=20 skeletal muscle dropped by almost 80% as compared with = dissociated=20 cells. Thus, when neural cells are grouped together, = neural-to-neural=20 signals override the myoblast-derived myogenic cues, blocking = neuromyogenic conversion. Hence, some type of "neuralizing"=20 signal(s), occurring between neighboring neural cells, = counteract the=20 induction of the muscle fate on NSCs. Thus, this phenomenon = might be=20 interpreted as a classical "community effect." In vivo, these = signals=20 can be found in the extracellular microenvironment that has = been=20 perturbed by an injury and may be elicited through a direct=20 cell-to-cell interaction between the host and the donor = cells.

Notably, conversion required direct cell-to-cell contact and = did=20 not take place when neural and myogenic cells were physically=20 separated by a porous membrane, nor when NSCs were exposed to = muscle cell=96conditioned medium. This requirement might = suggest=20 that spontaneous cell fusion between inducing and induced = cells might=20 account for neuromyogenic conversion in this system. Although = specific experiments based on cell selection with transgenic = markers=20 need to be undertaken to completely rule out this possibility, = the=20 presence of a significant number of mononucleated NSC-derived=20 myocytes in this culture (authors=92 unpublished = observations,=20 2003) clearly suggests that cell fusion alone may not justify = brain-into-muscle conversion in this system. In this context, = it is possible that, in the case of polynucleated NSC-derived = myotubes=97in which fusion of NSCs with C2C12 myoblasts = does=20 occur=97cell fusion might be responsible for the activation = of the=20 muscle-specific reporter gene in NSCs, without the latter = undergoing=20 an effective cell fate shift. Yet, we ought to emphasize that = the=20 expression of many other muscle-specific markers, such as = MyoD,=20 myosin heavy chain (MHC), together with ultrastructural = analysis,=20 have been associated with the neural-to-muscle transition in = this=20 coculture model.6=20 Based on these findings, we can infer that, at least in the = specific=20 case of neuromesodermal conversion, cell-to-cell contact is=20 required,6=20 underlining the necessity of a direct exchange of information = between=20 the "inducing" and the "induced" cells. This may imply the=20 interaction of cell surface receptors and ligands, the = formation of=20 gap junction structures, as well as the involvement of short=20 range=96acting molecules.

A fascinating extension of the these findings came from the=20 observation that NSCs could integrate into many different = tissues=20 derived from the three main germ layers on injection into the = mouse blastocyst,87=20 thus behaving as embryonic stem (ES) cells. Intriguingly, the = contribution of NSCs to some major mesodermal lineages, such = as blood=20 and the skeletal muscle, was never observed in this work. = Yet, it was=20 soon clear from additional studies that both human and mouse = NSCs do=20 possess the ability to differentiate into skeletal muscle, = both in=20 vivo and in vitro6=20 (Fi= gure=20 4), and more recent data demonstrated that, on injection = into=20 the blastocyst, the very first lineage that NSCs colonize is=20 indeed the hemopoietic one.89=20



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  		Figure 4. An example of = the=20 transdifferentiation capacity of NSCs. Generation of = skeletal muscle=20 from NSCs. A, NSCs that were derived from a strain of = transgenic=20 mice in which the promoter of the myosin light chain gene = drives the=20 expression of =DF-galactosidase in the nucleus of muscle = cells=20 activate the transgene when cocultured with C2C12 myocytes.=20 NSC-derived polynucleated myotubes are identified by the = nuclear=20 expression of =DF-galactosidase (X-gal reaction, blue). = Bar=3D40 =B5m. B,=20 Clonally derived NSCs from ROSA 26 = =DF-galactosidase=96expressing=20 transgenic mice cocultured with C2C12 cells differentiate = into=20 myotubes. NSCs expressing =DF-galactosidase immunoreactivity = are shown=20 in red (concave arrowhead). C2C12 cells labeled with the=20 antisarcomeric myosin heavy chain (MHC) antibody are shown = in green=20 (arrowhead). NSCs-derived polynucleated myotubes (blue, DAPI = nuclear=20 staining) appear as yellow cells due to the overlapping MHC = and=20 =DF-galactosidase staining (arrow). Bar=3D20 =B5m. =

The discrepancy between the various transdifferentiation = examples=20 described above and the initial study of NSCs injection into=20 blastocyst87=20 most likely lies in the fact that a number of inductive = factors=20 competitively act on NSCs cells in this system. The = prevalence of the=20 effect of a given set of instructive cues that acts on NSCs = will=20 ultimately depend on the initial, very variable site of=20 deposition/integration of the cells on their injection into = the=20 blastocyst, thus yielding rather variable results. =

Transdifferentiation of somatic stem cells is a hot, highly=20 debated issue. Particularly, despite the ability of NSCs to=20 give rise to blood cells has been reported in both human and=20 mouse cells by 4 independent groups, this phenomenon could = not=20 be detected in a recent study.90=20 This situation exemplifies the state of confusion that = plagues the=20 field of neural stem cells. Particularly, it emphasizes the = need for=20 standardization of the terminology adopted when it comes to = defining=20 NSCs or, at least, of the tissue culture systems used to grow = and=20 expand them. In fact, Morshead et al90=20 stated that they failed in reproducing brain-into-blood = conversion=20 when using the very same cells and system used by Bjornson et = al5=20 in their initial finding on neurohemopoietic conversion. As = it turns=20 out,91=20 the culture functional characteristics described by Morshead = et al=20 showed that the cells that they used were different from any = known=20 NSCs, particularly those used in previous = transdifferentiation=20 experiments.5,6=20 In=20 fact, Morshead=92s cultures consistently underwent = transformation.=20 This is not a property that was ever observed in studies from = many groups. In fact, neither human nor mouse NSCs undergo = consistent=20 transformation on subculturing. Over extensive time in = culture,=20 these cells exhibit strict growth factor dependency, = unchanged=20 growth kinetics and prompt differentiation on removal of = mitogens.56,58,92,93=20 Furthermore,=20 a clear difference emerged when comparing the content of NSCs = (ie,=20 clonogenic cells in culture) in Morshead et al cultures with = that of=20 other groups. It was evident that less than 1% of the cells = in=20 Morshead=92s system were NSCs, whereas Bjornson et al=92s = data agreed=20 with the literature=92s data pointing to a minimal standard = value of=20 20%.56,58,92,93=20 Bjornson=20 et al contended that the combination of low NSC number and=20 significant transformation found in the Morshead et al = cultures would=20 lead to the transplantation of a negligible number of NSCs = and to the=20 negative outcome of these experiments.

Perhaps, the most knowledgeable conclusion to draw=97also = given the=20 constant state of flux of this novel field of investigation=97is = that=20 transdifferentiation is an uncommon phenomenon that takes = place only=20 under very peculiar circumstances. Because the capacity to = undergo=20 transdifferentiation is a characteristic of specific cell = types,=20 namely somatic stem cells, and because the latter normally = represent=20 a minor fraction of the overall cell population in vivo or a = pool=20 whose relative size fluctuates in vitro depending on culture=20 conditions, detection of transdifferentiation is rather = difficult,=20 and requires appropriately refined and sensitive = methodologies=20 concerning both cell culturing and fate assessment.

Recently, explanations that are alternative to = transdifferentiation=20 have been invoked to explain, at least in part, the findings=20 discussed so far. Two distinct studies94,95=20 reported=20 that adult stem cells from the CNS and the bone marrow can = give rise=20 to cell types as a consequence of cell fusion with ES cells,=20 rather than by transdifferentiation. The first consideration = to=20 make in this context is that these results are limited to = cell=20 fusion between adult and embryonic stem cells and do not = impinge=20 on the interpretation of data in which adult somatic cells=20 undergo transdifferentiation in vivo in adult animals, or in = vitro=20 in adult cells.

Yet, it is possible that part of the transdifferentiation events = reported so far could be explained by cell fusion. = Nonetheless,=20 due to the very low frequency of hybrid formation (an average = frequency of 10-5 in the two reports), owing to the = fact=20 that ES cells might be more susceptible to cell fusion than=20 somatic cells and to the observation that the eventual = polyploid=20 fusion products are highly unstable, a main role of the sole = cell=20 fusion in the conversion of somatic stem cell into different = cell=20 types is unlikely.

In fact, as shown in these two studies and as argued by others,96=20 at least 30% of the bone marrow=96derived cells injected = in vivo=20 transdifferentiated81=20 and, similarly, 10% of NSCs cocultured with inducing = myoblasts gave=20 rise to muscle cells.6=20 These frequencies are orders of magnitude higher than the = fusion=20 efficiency between ES and somatic stem cells. Particularly,=20 concerning brain into muscle conversion, the possibility that = cell=20 fusion might be responsible for transdifferentiation seems = more=20 remote, due to the following facts: (1) proliferating C2 = myoblasts=20 are strongly resistant even to Sendai virus=96mediated cell = fusion;97=20 (2) myoblasts fuse with other myoblasts only when both are = committed=20 to differentiation and not when they are still proliferating98=20 as in our experimental paradigm;6=20 (3) myoblasts do not normally fuse with nonmyogenic cells98=20 and, on this rare event, the fusion of a myocyte with a = nonmyogenic=20 cells generally results in the extinction of muscle-specific=20 properties in the immediate fusion product,99=20 and (4) in our in vitro model, we observed high frequency of=20 mononucleated NSC-derived myocytes.6=20 Thus, the chances that cell fusion between NSCs and inducing=20 myoblasts might occur spontaneously are quite low. =

Whichever interpretation one may adopt, it is cogently clear = that=20 the field of transdifferentiation is in its infancy and that = this=20 phenomenon is far from being a widely accepted and = well-established=20 one. Many questions remain unanswered. The topic is open to = heated=20 discussion(s).


3D*   =20 Conclusions
Top
Abstract
Introduction
The Forebrain Subventricular...
The Nature and Origin...
Ex Vivo Behavior of...
Plasticity of NSCs Within...
Plasticity of NSCs Outside...
3D*Conclusions
References
 
T= he field=20 of neural stem cells is in a state of rapid growth. Every = month, new=20 pieces are added to the puzzle of the neurogenetic process in = adult=20 mammals. As expected for such a young field, stimulating new = findings=20 go hand in hand with the raising of new outstanding issues = that heat=20 the debate around these cells. This area is, therefore, in a = state of=20 rapid flux and will clearly benefit from the isolation of = specific=20 antigenic markers that allow for the univocal identification = of the=20 NSC and its derivatives.8,9,10=20 A=20 somewhat more conservative use of the term stem cell as = applied to=20 different types of brain precursors would also be beneficial. = In this=20 view, studies that aim at unraveling the relationship between = candidate stem cells as they are identified in vitro and in = vivo will=20 certainly provide more rigorous criteria for the = identification of=20 NSCs.

Nevertheless, these cells represent one of the most astonishing=20 discoveries of the last decade. It is intriguing that cells=20 isolated from what has long been viewed as the most quiescent = among the bodily tissues can display such an amazing degree = of=20 plasticity and, equally important, such a remarkable growth = capacity.=20 The latter properties will certainly provide the necessary = basis to=20 unravel the most intimate mechanisms underlining the genesis = of=20 neural cells and the process of development, degeneration, = and repair=20 in the CNS.

Finally, the availability of a renewable source of human neural=20 cells as provided by the establishment of NSC lines promises = to=20 open new, and as of yet, unpredictable therapeutic venues for = the=20 treatment of neurological disorders.


3D*   =20 Acknowledgments
 
We are = grateful to=20 the Fondazione Agarini for the continued support of our = research on=20 neural stem cells. We thank Sig. G. Zanutto for assistance = with=20 drawing.

Received March 4, 2002; revision received February 4, 2003; accepted = February=20 25, 2003.


3D*   =20 References
Top
Abstract
Introduction
The Forebrain Subventricular...
The Nature and Origin...
Ex Vivo Behavior of...
Plasticity of NSCs Within...
Plasticity of NSCs Outside...
Conclusions
3D*References
&nb= sp;

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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. 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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 =3D=3D "page-break-before") {=0A= e.style.pageBreakBefore =3D value;=0A= }=0A= else if (name =3D=3D "pixelBottom") {=0A= e.style.pixelBottom =3D value;=0A= }=0A= else if (name =3D=3D "pixelHeight") {=0A= e.style.pixelHeight =3D value;=0A= }=0A= else if (name =3D=3D "pixelLeft") {=0A= e.style.pixelLeft =3D value;=0A= }=0A= else if (name =3D=3D "pixelRight") {=0A= e.style.pixelRight =3D value;=0A= }=0A= else if (name =3D=3D "pixelTop") {=0A= e.style.pixelTop =3D value;=0A= }=0A= else if (name =3D=3D "pixelWidth") {=0A= e.style.pixelWidth =3D value;=0A= }=0A= else if (name =3D=3D "posBottom") {=0A= e.style.posBottom =3D value;=0A= }=0A= else if (name =3D=3D "posHeight") {=0A= e.style.posHeight =3D value;=0A= }=0A= else if (name =3D=3D "position") {=0A= e.style.position =3D value;=0A= }=0A= else if (name =3D=3D "posLeft") {=0A= e.style.posLeft =3D value;=0A= }=0A= else if (name =3D=3D "posRight") {=0A= e.style.posRight =3D value;=0A= }=0A= else if (name =3D=3D "posTop") {=0A= e.style.posTop =3D value;=0A= }=0A= else if (name =3D=3D "posWidth") {=0A= e.style.posWidth =3D value;=0A= }=0A= else if (name =3D=3D "right") {=0A= e.style.right =3D value;=0A= }=0A= else if (name =3D=3D "ruby-align") {=0A= e.style.rubyAlign =3D value;=0A= }=0A= else if (name =3D=3D "ruby-overhang") {=0A= e.style.rubyOverhang =3D value;=0A= }=0A= else if (name =3D=3D "ruby-position") {=0A= e.style.rubyPosition =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-3dlight-color") {=0A= e.style.scrollbar3dLightColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-arrow-color") {=0A= e.style.scrollbarArrowColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-base-color") {=0A= e.style.scrollbarBaseColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-darkshadow-color") {=0A= e.style.scrollbarDarkShadowColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-face-color") {=0A= e.style.scrollbarFaceColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-highlight-color") {=0A= e.style.scrollbarHighlightColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-shadow-color") {=0A= e.style.scrollbarShadowColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-track-color") {=0A= e.style.scrollbarTrackColor =3D value;=0A= }=0A= else if (name =3D=3D "float") {=0A= e.style.styleFloat =3D value;=0A= }=0A= else if (name =3D=3D "table-layout") {=0A= e.style.tableLayout =3D value;=0A= }=0A= else if (name =3D=3D "text-align") {=0A= e.style.textAlign =3D value;=0A= }=0A= else if (name =3D=3D "text-align-last") {=0A= e.style.textAlignLast =3D value;=0A= }=0A= else if (name =3D=3D "text-autospace") {=0A= e.style.textAutospace =3D value;=0A= }=0A= else if (name =3D=3D "text-decoration") {=0A= e.style.textDecoration =3D value;=0A= }=0A= else if (name =3D=3D "textDecorationBlink") {=0A= e.style.textDecorationBlink =3D value;=0A= }=0A= else if (name =3D=3D "textDecorationLineThrough") {=0A= e.style.textDecorationLineThrough =3D value;=0A= }=0A= else if (name =3D=3D "textDecorationNone") {=0A= e.style.textDecorationNone =3D value;=0A= }=0A= else if (name =3D=3D "textDecorationOverline") {=0A= e.style.textDecorationOverline =3D value;=0A= }=0A= else if (name =3D=3D "textDecorationUnderline") {=0A= e.style.textDecorationUnderline =3D value;=0A= }=0A= else if (name =3D=3D "text-indent") {=0A= e.style.textIndent =3D value;=0A= }=0A= else if (name =3D=3D "text-justify") {=0A= e.style.textJustify =3D value;=0A= }=0A= else if (name =3D=3D "text-kashida-space") {=0A= e.style.textKashidaSpace =3D value;=0A= }=0A= else if (name =3D=3D "text-overflow") {=0A= e.style.textOverflow =3D value;=0A= }=0A= else if (name =3D=3D "text-transform") {=0A= e.style.textTransform =3D value;=0A= }=0A= else if (name =3D=3D "text-underline-position") {=0A= e.style.textUnderlinePosition =3D value;=0A= }=0A= else if (name =3D=3D "top") {=0A= e.style.top =3D value;=0A= }=0A= else if (name =3D=3D "unicode-bidi") {=0A= e.style.unicodeBidi =3D value;=0A= }=0A= else if (name =3D=3D "vertical-align") {=0A= e.style.verticalAlign =3D value;=0A= }=0A= else if (name =3D=3D "visibility") {=0A= e.style.visibility =3D value;=0A= }=0A= else if (name =3D=3D "white-space") {=0A= e.style.whiteSpace =3D value;=0A= }=0A= else if (name =3D=3D "width") {=0A= e.style.width =3D value;=0A= }=0A= else if (name =3D=3D "word-break") {=0A= e.style.wordBreak =3D value;=0A= }=0A= else if (name =3D=3D "word-spacing") {=0A= e.style.wordSpacing =3D value;=0A= }=0A= else if (name =3D=3D "word-wrap") {=0A= e.style.wordWrap =3D value;=0A= }=0A= else if (name =3D=3D "writing-mode") {=0A= e.style.writingMode =3D value;=0A= }=0A= else if (name =3D=3D "z-index") {=0A= e.style.zIndex =3D value;=0A= }=0A= else if (name =3D=3D "zoom") {=0A= e.style.zoom =3D value;=0A= }=0A= }=0A= catch (e) {=0A= /* ignore error on attempt to set e.style.[property] */=0A= }=0A= }=0A= }=0A= }=0A= ------=_NextPart_000_0000_01C85938.DD0370D0 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://circres.ahajournals.org/javascript/entrez/callback.js /************************************************************************= *****=0A= * javascript/entrez/callback.js=0A= *=0A= * Entrez Linking callback to populate content box.=0A= *=0A= * Copyright 2006 Board of Trustees of the Leland Stanford Junior = University.=0A= = *************************************************************************= ***/=0A= =0A= /*=0A= * Execute callback to fill content box with Entrez Linking information.=0A= */=0A= function entrez_callback(pmid, callback_url) {=0A= /*=0A= * MSIE 5.5 and below have issues with the JavaScript=0A= * used for Entrez Linking. For now we have to disable=0A= * the callback until we can track down a proper fix=0A= * (or everybody sanely upgrades to version 6 or 7!).=0A= */=0A= if (navigator) {=0A= var appname =3D navigator.appName;=0A= if (appname =3D=3D "Microsoft Internet Explorer") {=0A= var userAgent =3D navigator["userAgent"];=0A= var s =3D "MSIE ";=0A= var n =3D -1; =0A= if ((n =3D userAgent.indexOf(s)) !=3D -1) {=0A= var v =3D parseFloat(userAgent.substring(n+s.length));=0A= if (v < 6) {=0A= return;=0A= }=0A= }=0A= }=0A= }=0A= =0A= /*=0A= * Acquire table row element to update, initiate callback=0A= * to update table with Entrez Links.=0A= */=0A= var tr =3D document.getElementById('entrez_callback_'+pmid);=0A= if (!tr) {=0A= return;=0A= }=0A= var req =3D new XMLHttpRequest();=0A= if (!req) {=0A= return;=0A= }=0A= req.onreadystatechange =3D function() {=0A= if (req.readyState =3D=3D 4 && (req.status =3D=3D 200 || req.status = =3D=3D 304)) {=0A= var src =3D req.responseXML.documentElement;=0A= var dst =3D document.createDocumentFragment();=0A= for (var i =3D 0; i < src.childNodes.length; i++) {=0A= copy_xml_to_html(src.childNodes[i], dst);=0A= }=0A= var tbl =3D tr.parentNode;=0A= tbl.replaceChild(dst, tr);=0A= }=0A= }=0A= req.open('GET', callback_url, true);=0A= req.send(null);=0A= }=0A= ------=_NextPart_000_0000_01C85938.DD0370D0 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://www.google-analytics.com/urchin.js //-- Google Analytics Urchin Module=0A= //-- Copyright 2007 Google, All Rights Reserved.=0A= =0A= //-- Urchin On Demand Settings ONLY=0A= var _uacct=3D""; // set up the Urchin Account=0A= var _userv=3D1; // service mode (0=3Dlocal,1=3Dremote,2=3Dboth)=0A= =0A= //-- UTM User Settings=0A= var _ufsc=3D1; // set client info flag (1=3Don|0=3Doff)=0A= var _udn=3D"auto"; // (auto|none|domain) set the domain name for cookies=0A= var _uhash=3D"on"; // (on|off) unique domain hash for cookies=0A= var _utimeout=3D"1800"; // set the inactive session timeout in seconds=0A= var _ugifpath=3D"/__utm.gif"; // set the web path to the __utm.gif file=0A= var _utsp=3D"|"; // transaction field separator=0A= var _uflash=3D1; // set flash version detect option (1=3Don|0=3Doff)=0A= var _utitle=3D1; // set the document title detect option = (1=3Don|0=3Doff)=0A= var _ulink=3D0; // enable linker functionality (1=3Don|0=3Doff)=0A= var _uanchor=3D0; // enable use of anchors for campaign = (1=3Don|0=3Doff)=0A= var _utcp=3D"/"; // the cookie path for tracking=0A= var _usample=3D100; // The sampling % of visitors to track (1-100).=0A= =0A= //-- UTM Campaign Tracking Settings=0A= var _uctm=3D1; // set campaign tracking module (1=3Don|0=3Doff)=0A= var _ucto=3D"15768000"; // set timeout in seconds (6 month default)=0A= var _uccn=3D"utm_campaign"; // name=0A= var _ucmd=3D"utm_medium"; // medium (cpc|cpm|link|email|organic)=0A= var _ucsr=3D"utm_source"; // source=0A= var _uctr=3D"utm_term"; // term/keyword=0A= var _ucct=3D"utm_content"; // content=0A= var _ucid=3D"utm_id"; // id number=0A= var _ucno=3D"utm_nooverride"; // don't override=0A= =0A= //-- Auto/Organic Sources and Keywords=0A= var _uOsr=3Dnew Array();=0A= var _uOkw=3Dnew Array();=0A= _uOsr[0]=3D"google"; _uOkw[0]=3D"q";=0A= _uOsr[1]=3D"yahoo"; _uOkw[1]=3D"p";=0A= _uOsr[2]=3D"msn"; _uOkw[2]=3D"q";=0A= _uOsr[3]=3D"aol"; _uOkw[3]=3D"query";=0A= _uOsr[4]=3D"aol"; _uOkw[4]=3D"encquery";=0A= _uOsr[5]=3D"lycos"; _uOkw[5]=3D"query";=0A= _uOsr[6]=3D"ask"; _uOkw[6]=3D"q";=0A= _uOsr[7]=3D"altavista"; _uOkw[7]=3D"q";=0A= _uOsr[8]=3D"netscape"; _uOkw[8]=3D"query";=0A= _uOsr[9]=3D"cnn"; _uOkw[9]=3D"query";=0A= _uOsr[10]=3D"looksmart"; _uOkw[10]=3D"qt";=0A= _uOsr[11]=3D"about"; _uOkw[11]=3D"terms";=0A= _uOsr[12]=3D"mamma"; _uOkw[12]=3D"query";=0A= _uOsr[13]=3D"alltheweb"; _uOkw[13]=3D"q";=0A= _uOsr[14]=3D"gigablast"; _uOkw[14]=3D"q";=0A= _uOsr[15]=3D"voila"; _uOkw[15]=3D"rdata";=0A= _uOsr[16]=3D"virgilio"; _uOkw[16]=3D"qs";=0A= _uOsr[17]=3D"live"; _uOkw[17]=3D"q";=0A= _uOsr[18]=3D"baidu"; _uOkw[18]=3D"wd";=0A= _uOsr[19]=3D"alice"; _uOkw[19]=3D"qs";=0A= _uOsr[20]=3D"yandex"; 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path=3D"+_utcp+";"+nx+_udo;=0A= _ubd.cookie=3D"__utmb=3D"+_udh+"; path=3D"+_utcp+";"+x+_udo;=0A= _ubd.cookie=3D"__utmc=3D"+_udh+"; path=3D"+_utcp+";"+_udo;=0A= _ufns=3D1;=0A= } else if (a>=3D0 && b>=3D0 && c>=3D0) {=0A= _ubd.cookie=3D"__utmb=3D"+_udh+"; path=3D"+_utcp+";"+x+_udo;=0A= } else {=0A= if (a>=3D0) a=3D_uFixA(_ubd.cookie,";",_ust);=0A= else a=3D_udh+"."+_uu+"."+_ust+"."+_ust+"."+_ust+".1";=0A= _ubd.cookie=3D"__utma=3D"+a+"; path=3D"+_utcp+";"+nx+_udo;=0A= _ubd.cookie=3D"__utmb=3D"+_udh+"; path=3D"+_utcp+";"+x+_udo;=0A= _ubd.cookie=3D"__utmc=3D"+_udh+"; path=3D"+_utcp+";"+_udo;=0A= _ufns=3D1;=0A= }=0A= if (_ulink && xx && xx!=3D"" && xx!=3D"-") {=0A= xx=3D_uUES(xx);=0A= if (xx.indexOf(";")=3D=3D-1) _ubd.cookie=3D"__utmx=3D"+xx+"; = path=3D"+_utcp+";"+nx+_udo;=0A= }=0A= if (_ulink && v && v!=3D"" && v!=3D"-") {=0A= v=3D_uUES(v);=0A= if (v.indexOf(";")=3D=3D-1) _ubd.cookie=3D"__utmv=3D"+v+"; = path=3D"+_utcp+";"+nx+_udo;=0A= }=0A= _uInfo(page);=0A= _ufns=3D0;=0A= _ufno=3D0;=0A= if (!page || page=3D=3D"") _uff=3D1;=0A= }=0A= function _uInfo(page) {=0A= var p,s=3D"",dm=3D"",pg=3D_udl.pathname+_udl.search;=0A= if (page && page!=3D"") pg=3D_uES(page,1);=0A= _ur=3D_ubd.referrer;=0A= if (!_ur || _ur=3D=3D"") { _ur=3D"-"; }=0A= else {=0A= dm=3D_ubd.domain;=0A= if(_utcp && _utcp!=3D"/") dm+=3D_utcp;=0A= p=3D_ur.indexOf(dm);=0A= if ((p>=3D0) && (p<=3D8)) { _ur=3D"0"; }=0A= if (_ur.indexOf("[")=3D=3D0 && = _ur.lastIndexOf("]")=3D=3D(_ur.length-1)) { _ur=3D"-"; }=0A= }=0A= s+=3D"&utmn=3D"+_uu;=0A= if (_ufsc) s+=3D_uBInfo();=0A= if (_uctm) s+=3D_uCInfo();=0A= if (_utitle && _ubd.title && _ubd.title!=3D"") = s+=3D"&utmdt=3D"+_uES(_ubd.title);=0A= if (_udl.hostname && _udl.hostname!=3D"") = s+=3D"&utmhn=3D"+_uES(_udl.hostname);=0A= s+=3D"&utmr=3D"+_ur;=0A= s+=3D"&utmp=3D"+pg;=0A= if ((_userv=3D=3D0 || _userv=3D=3D2) && _uSP()) {=0A= var i=3Dnew Image(1,1);=0A= i.src=3D_ugifpath+"?"+"utmwv=3D"+_uwv+s;=0A= i.onload=3Dfunction() {_uVoid();}=0A= }=0A= if ((_userv=3D=3D1 || _userv=3D=3D2) && _uSP()) {=0A= var i2=3Dnew Image(1,1);=0A= = i2.src=3D_ugifpath2+"?"+"utmwv=3D"+_uwv+s+"&utmac=3D"+_uacct+"&utmcc=3D"+= _uGCS();=0A= i2.onload=3Dfunction() { _uVoid(); }=0A= }=0A= return;=0A= }=0A= function _uVoid() { return; }=0A= function _uCInfo() {=0A= if (!_ucto || _ucto=3D=3D"") { _ucto=3D"15768000"; 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