From: Subject: Cell biology of stem cells: an enigma of asymmetry and self-renewal -- Lin 180 (2): 257 -- The Journal of Cell Biology Date: Wed, 30 Jan 2008 18:00:28 +0100 MIME-Version: 1.0 Content-Type: multipart/related; type="text/html"; boundary="----=_NextPart_000_000A_01C86369.FF6F9DC0" X-MimeOLE: Produced By Microsoft MimeOLE V6.00.2900.3198 This is a multi-part message in MIME format. ------=_NextPart_000_000A_01C86369.FF6F9DC0 Content-Type: text/html; charset="iso-8859-1" Content-Transfer-Encoding: quoted-printable Content-Location: http://www.jcb.org/cgi/content/full/180/2/257 Cell biology of stem cells: an enigma of asymmetry = and self-renewal -- Lin 180 (2): 257 -- The Journal of Cell = Biology
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Published online 28 January=20 2008
doi:10.1083/jcb.200712159
The Journal of Cell = Biology, Vol.=20 180, No. 2, 257-260
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Cell biology of = stem cells:=20 an enigma of asymmetry and self-renewal

Haifan=20 Lin1,2

1 Yale Stem Cell = Center and=20 2 Department of Cell Biology, Yale University School of = Medicine, New=20 Haven, CT 06511

Correspondence to Haifan Lin: haifan.lin{at}yale.edu

Stem = cells present a=20 vast, new terrain of cell biology. A central question in stem = cell=20 research is how stem cells achieve asymmetric divisions to = replicate=20 themselves while producing differentiated daughter cells. = This=20 hallmark of stem cells is manifested either strictly during = each=20 mitosis or loosely among several divisions. Current research = has=20 revealed the crucial roles of niche signaling, intrinsic cell = polarity, subcellular localization mechanism, asymmetric = centrosomes=20 and spindles, as well as cell cycle regulators in = establishing=20 self-renewing asymmetry during stem cell division. Much of = this=20 progress has benefited from studies in model stem cell = systems such=20 as Drosophila melanogaster neuroblasts and germline = stem cells=20 and mammalian skin stem cells. Further investigations of = these=20 questions in diverse types of stem cells will significantly = advance=20 our knowledge of cell biology and allow us to effectively = harness=20 stem cells for therapeutic applications.

Introduction: cell biology of asymmetry for=20 self-renewal
Stem cells exist in early embryos and = individual=20 tissues. Embryonic stem cells have the ability to ultimately=20 differentiate into all types of cells in our bodies, whereas = tissue=20 stem cells (also known as adult stem cells) serve as = immediate=20 sources of cell supply to their resident tissues. Stem cell=20 research has offered the promise of effective cell-based = therapies=20 in treating many debilitating diseases such as diabetes,=20 neurodegenerative diseases, and cancer. The therapeutic = potential of=20 stem cells has inspired the imagination, intense interest, = and=20 targeted investment of scientists, clinicians, and the = general=20 public toward this fascinating area of biology. At present, = human=20 embryonic stem cell research is politically charged, with = biologists=20 engaging in ethical debates. Meanwhile, much of the research = effort=20 has been channeled to harnessing stem cells into desired cell = types for clinical applications. Such translational research = has=20 yielded some exciting results in tissue therapy by=20 transplantation. Excitement notwithstanding, there is still a = long=20 way to go in understanding the fundamental mechanisms of stem = cells=20 before new therapies will be effectively established. = However,=20 this aspect of stem cell research has not garnered as much=20 attention.

As evident from the three papers in this series of reviews, = stem=20 cell biology is, by and large, an integral part of cell = biology and=20 presents a vast new terrain of basic cell biology for = exploration.=20 The hallmark of a stem cell is its ability to self-renew = while=20 generating many daughter cells that are committed to = differentiation.=20 Intimately related to this ability are a host of fundamental=20 questions that await investigation: How can we definitively = identify=20 a stem cell? What defines a stem cell in molecular terms? = What=20 signaling events control stem cell proliferation and = differentiation?=20 How does a stem cell behave in its biological context? What = happens=20 to a differentiated cell when it is reprogrammed into a stem = cell or=20 vice versa? Solutions to these wide-ranging and perplexing = questions=20 of cell biology are all related to understanding the single=20 defining feature of stem cells=97their self-renewing ability. = The=20 self-renewing ability of stem cells is tightly related to = their=20 ability to undergo self-renewing asymmetric divisions. The = concept=20 of self-renewing asymmetry should be applicable, either = strictly=20 during each mitosis or loosely among several mitoses, to all=20 types of tissue stem cells and perhaps even to embryonic stem = cells to account for their self-renewal. A stereotypical = asymmetric=20 division gives rise to both a daughter stem cell and a = daughter=20 cell that has acquired a more differentiated fate. This = unique=20 asymmetry allows a stem cell to self-replicate while = producing=20 numerous differentiated progeny. It is distinct from another=20 form of asymmetric division that produces two daughter cells=20 that are different from each other as well as from the = mother,=20 as often seen for progenitor cells. For those stem cells that = undergo apparently symmetric divisions, the self-renewing = asymmetry=20 still exists among several divisions because, even = stochastically,=20 50% of the daughter cells need to acquire a more = differentiated=20 fate after the divisions. Therefore, how the self-renewing = asymmetry=20 is achieved is a central question in stem cell biology. =

The three reviews in this issue effectively summarize the latest = progress in our understanding of mechanisms that underlie=20 self-renewing asymmetric division of three of the = best-characterized=20 tissue stem cell systems=97Drosophila melanogaster=20 neuroblasts, Drosophila germline stem cells, and = mammalian=20 skin stem cells. Discoveries from these three model systems=20 complement one another, each revealing a unique aspect of the = asymmetric mechanism. Together, they present a comprehensive=20 landscape of molecular mechanisms underlying the = self-renewing=20 asymmetric division of stem cells. It is a pleasure to = comment on=20 these exciting discoveries from a more general = perspective.=20

The niche induces asymmetric=20 division
Self-renewing asymmetric division of a stem = cell is=20 controlled by both extrinsic signaling and intrinsic = mechanisms. Much=20 progress has been made in understanding intercellular = mechanisms,=20 especially the identification of niches for various types of = tissue=20 stem cells and elucidation of the role of the niche in=20 regulating asymmetric stem cell division. Perhaps the=20 best-illustrated role of the niche in regulating stem cell = division=20 comes from the study of germline stem cells in the = Drosophila=20 ovary and testis (see Yamashita and Fuller on p. 261 of = this issue;=20 for more detailed information, also see Lin, = 2002). In=20 female flies, somatic niche signaling requires the TGFβ = pathway and=20 another signaling pathway defined by the YB and PIWI = proteins,=20 which are required in niche cells for germline stem cell=20 maintenance. The TGFβ and YB=96PIWI pathways converge in = germline=20 stem cells to repress the expression of bag of marbles=20 (bam), a gene that is necessary and sufficient for = promoting=20 stem cell differentiation (Chen and = McKearin,=20 2005; Szakmary=20 et al., 2005). The niche function is also assisted by = Hedgehog=20 signaling and requires niche cell=96stem cell adhesion as = mediated=20 by epithelial cadherin (King et al., = 2001;=20 Song et = al.,=20 2002). The niche induces the attachment of one pole of = the stem=20 cell spindle to the niche cells (Deng and = Lin,=20 1997). Such attachment is mediated by a spectrin-rich = structure=20 called the spectrosome and a cytoplasmic dynein-mediated = mechanism=20 (Deng and = Lin,=20 1997; McGrail and = Hays,=20 1997).

Similarly, the Drosophila male germline stem cell system = contains=20 somatic niche cells (hub cells) that secrete the unpaired = ligand=20 for the JAK=96STAT (Janus kinase=96signal transducer = and activator=20 of transcription) signaling pathway to maintain germline stem = cells,=20 as reviewed by Yamashita = and Fuller=20 (2008). As a stem cell divides, one pole of its mitotic = spindle=20 is anchored to the niche cells, ensuring the asymmetric = division that=20 allows only one of the two daughter cells to maintain contact = with the niche cells and, as such, retains the stem cell = fate.=20 This attachment requires adherens complexes that contain=20 cadherin, β-catenin, and adenomatous polyposis coli 2 = (APC2)=20 protein, which is similar to the anchorage of mitotic spindle = in=20 Drosophila embryonic epithelial cells (for review see = Lin, = 2003).=20

Although the role of niche in the asymmetric division of = mammalian=20 stem cells has not been as clearly illustrated, Fuchs and = colleagues=20 have shown that embryonic basal epidermal cells use their = polarity=20 to divide asymmetrically with respect to the underlying basal = lamina, generating a committed suprabasal cell and a = proliferative=20 basal cell (Lechler and = Fuchs,=20 2005; see Fuchs on p. 273 = of=20 this issue). Because skin stem cells are a subpopulation of=20 mitotically active basal epidermal cells, it is conceivable=20 that these stem cells divide in an asymmetric fashion to = self-renew=20 and to produce differentiated keratinocytes. Moreover, = integrins=20 and cadherins in the basal lamina are essential for the = proper=20 localization of apical complexes containing atypical PKC = (aPKC),=20 the Par3=96LGN=96Inscuteable protein, and NuMA (nuclear = mitotic=20 apparatus protein)=96dynactin. This asymmetric localization = may be=20 functionally important because similar complexes in = Drosophila=20 neuroblasts are essential for asymmetric division, as = reviewed=20 in this issue (see Chia et al. on p. 267 of = this issue).=20 The requirement of integrins and cadherins suggests that the=20 extracellular matrix, such as basal lamina, can also serve as = a stem=20 cell niche or part of a niche. Such an acellular niche also=20 contains signaling molecules such as laminin 5, which is a = stable=20 ligand for integrin in hemidesmosomes and focal adhesions. In = addition, the basal lamina may serve as mechanical support to = the=20 stem cell system. Moreover, its resident proteoglycans and = other=20 proteins may function as molecular sinks for growth factors=20 that either promote or restrict the proliferation of = epidermal=20 cells, thus serving as a signaling source for these = molecules.

In addition to basal epidermal cells, mouse neuroepithelial = stem=20 cells and hematopoietic precursor cells undergo both asymmetric = and=20 symmetric divisions. In the mammalian central nervous system,=20 embryonic neuroepithelial cells first undergo symmetric = division=20 to expand their population and then switch to asymmetric = divisions=20 for neurogenesis. This switch involves a change in cleavage=20 plane orientation from perpendicular to parallel to the plane = of the apical lamina, leading to an asymmetric distribution = to=20 the daughter cells of the apical plasma membrane, which constitutes = only a minute fraction (1=962%) of the entire neuroepithelial = cell plasma membrane (Kosodo et = al.,=20 2004). Somewhat similarly, mouse hematopoietic progenitor = cells=20 are capable of both symmetric and asymmetric divisions in = cultures=20 supported by stromal cells (Wu et al., = 2007).=20 A prodifferentiation stromal cell line increased the = frequency of=20 asymmetric division, whereas a pro-proliferation stromal cell = line=20 promoted symmetric division. These observations indicate that = niche=20 signaling can also control the asymmetry of stem cell = division at a=20 populational level.

Inherited cell polarity determines asymmetric=20 division
Although niche induction accounts for = asymmetric=20 division in some types of stem cells, it may not play a role = in all=20 types of stem cells. For Drosophila neuroblasts, the = initial=20 cue for symmetry seems to depend solely on the cell itself, = as=20 reviewed by Chia et al.=20 (2008). The neuroblasts are derived from embryonic = epithelial=20 cells and inherit their polarity, with one end being apical = and the=20 other being basal. This allows molecules that determine cell = fate to=20 be segregated along the apical-basal axis. The mitotic = spindle is=20 also oriented along this axis such that the plane of division = is=20 perpendicular to the axis. This means that one daughter cell = inherits=20 the apical molecules and remains a neuroblast; the other = inherits the=20 basal components and becomes a ganglion mother cell. =

Studies on Drosophila neuroblasts in the past 15 years = have=20 identified a group of proteins localized to the apical cortex = that determine the asymmetry of stem cell division. These = proteins=20 are organized into two complexes linked by the Inscuteable = protein.=20 The first complex includes Bazooka=96Par3, aPKC, and Par6, = which=20 regulates the tumor suppressor Lethal (2) giant larva (LGL). = Such=20 regulation is likely via phosphorylation, which, in turn, = affects the=20 activity of LGL in the localization of basal complexes. = Conversely,=20 LGL inhibits the basal localization of aPKC, thereby = restricting aPKC=20 to the apical cortex (Lee et al.,=20 2006). Therefore, the regulation of LGL and aPKC is = likely to be=20 mutual inhibition. The second apical complex contains=20 heterotrimeric G protein signaling mechanism components: = Gi, = Partner of=20 Inscuteable (Pins), and Locomotion defect (Loco). These two = complexes=20 work in parallel to control the asymmetric localization of = cell=20 fate regulators, the apicobasal orientation of the mitotic=20 spindle, and the asymmetric structure of the spindle itself. = The=20 coordination of all of these aspects of asymmetry is = essential for=20 the asymmetric fates of the two daughter cells, as reviewed = by Chia et al.=20 (2008), and will be discussed in further detail in the = following=20 sections.

Interestingly, key components of the Par3 complex have also = been=20 found in the apical cortex of mammalian skin stem cells, as = reviewed=20 by Fuchs=20 (2008). The mouse Numb homologue is localized = asymmetrically=20 during hematopoietic precursor cell division, similar to the=20 asymmetric behavior of Numb in Drosophila neuroblasts = (Wu et al., = 2007).=20 These observations raise the possibility that the asymmetric=20 mechanism discovered in the Drosophila neuroblast is = conserved=20 during evolution.

Centrosomal asymmetry contributes to = asymmetric=20 division
A fundamental aspect of the asymmetric = division=20 mechanism is the asymmetric property of centrosomes during = stem cell=20 division. The mother and daughter centrosomes are known to = differ in=20 size, molecular composition, the ability to organize=20 microtubules, and even the ability to localize mRNAs or = possibly=20 other cell fate determinants, as systematically discussed by = Yamashita = and Fuller=20 (2008) and by Chia et al.=20 (2008). In both Drosophila male germline stem = cells and=20 neuroblasts, the large mother centrosome organizes a more = extensive=20 population of astral microtubules and is selectively retained = in the=20 daughter stem cell after stem cell division. This feature has = also=20 been found in mammalian cultured cells. Additionally, the two = centrosomes may differentially associate with cell fate = determinants,=20 which would be an effective mechanism for the asymmetric = segregation=20 of cell fate determinants. Finally, anchoring of the mother=20 centrosome to the niche is also important for the oriented = asymmetric=20 division.

The multifaceted difference between the mother and daughter=20 centrosomes may be a consequence of the structural difference = of their resident old and young centrioles, as discussed by = Yamashita = and Fuller=20 (2008). The exploration of asymmetric features in = centrosomal=20 biogenesis and function represents a new area of stem cell = research=20 with general implications in cell and cancer biology. =

Spindle asymmetry determines the size = difference of the=20 two daughter cells
An intriguing feature of asymmetry = as=20 revealed by the study of Drosophila neuroblast = division is the=20 asymmetric geometry of the mitotic spindle. Particularly, the = distance between the apical pole and equator of the spindle = is=20 greater than that between the basal pole and the equator. = This=20 results in an apically located larger daughter neuroblast and = a=20 basally located smaller differentiated cell (i.e., the = ganglion=20 mother cell). The spindle asymmetry is controlled by both = apical=20 complex I (Bazooka=96Par3 and aPKC=96Par6) and apical complex = II (Gi=96Pins=96Loco),=20 with either complex alone being sufficient to maintain the = geometric=20 asymmetry of the spindle (Cai et al., = 2003).=20 In addition, the apical localization of these complexes leads = to=20 displacement of the spindle toward the basal cortex, which = also=20 contributes to the size difference between the two daughter = cells.=20 Given that the components of these complexes are = evolutionally=20 conserved, this mechanism may be involved in the asymmetric = division=20 of other types of stem cells that generates two daughter = cells=20 of unequal size.

Cell cycle regulators have novel roles in = asymmetric=20 division
A particularly exciting development in basic = stem=20 cell research in the past few years is the discovery of novel = functions of cell cycle regulators in controlling the = asymmetry of=20 stem cell division, as timely reviewed by Chia et al.=20 (2008). For example, the CDC2/CDK1 level controls whether = a=20 neural or muscle progenitor undergoes symmetric or asymmetric = division. In neuroblasts, high levels of CDK1 during mitosis = are=20 required for the asymmetric localization of apical and basal = protein=20 complexes. In addition, Aurora and Polo kinases act as tumor=20 suppressors in neuroblasts by preventing excess self-renewal, = implicating the function of asymmetric division in = restricting=20 overproliferation. The mutations of these two kinase genes = affect the=20 asymmetric localization of aPKC, Numb, Partner of Numb, and = Notch,=20 causing symmetric division to generate two daughter = neuroblasts. In=20 addition, anaphase-promoting complex/cyclosome is also = required for=20 the localization of Miranda and its cargo proteins (Prospero, = Brain Tumor, and Staufen). More surprisingly, even cyclin E, = a=20 G1 cyclin, is involved in asymmetric neuroblast = division.

Multiple lines of evidence suggest that the asymmetric function = of=20 these cell cycle regulators is not via their conventional = function in=20 cell cycle control but rather by directly impinging on the = asymmetric=20 localization and segregation machineries in neuroblasts. = Mutants of=20 some of these cell cycle genes exhibit tumor phenotypes, = which is=20 similar to the phenotype of genes required for apicobasal = polarity in=20 Drosophila epithelia and neuroblasts. These = observations=20 highlight the importance of asymmetry in preventing = overproliferation=20 (Chia et = al.,=20 2008).

Asymmetric division and tissue maintenance: = skin as an=20 example
Just as it is important to understand the = asymmetric=20 mechanism of stem cells, it is imperative to comprehend the=20 biological impact of asymmetric stem cell division on the = development=20 and maintenance of tissues. In this regard, mammalian = epidermal=20 stem cells provide an unparalleled opportunity. As described = in=20 the review by Fuchs=20 (2008), stem cells for the epidermis and its appendages = (hair=20 follicles and sebaceous glands) have been relatively well = identified.=20 In the epidermis, different types of differentiating = keratinocytes=20 are organized in an orderly fashion along the baso-apical = axis. This=20 reflects a gradient of differentiation from basally located = stem=20 cells to the most differentiated cells, the stratum corneum = on the=20 apical surface. This organization pattern is readily = accessible for=20 investigating how the asymmetric division of epidermal stem = cells=20 with a defined orientation serves the need to replenish this = tissue.=20 Moreover, epidermal stem cells together with hair follicle = and=20 sebaceous gland stem cells contribute to the skin. The three = types=20 of stem cells behave similarly in their corresponding = lineage,=20 yet they can transiently contribute to another lineage during = the injury repair process. This provides excellent = opportunities=20 for studying the coordinated control of different stem cell=20 lineages within a tissue to ensure its development and = homeostasis.=20 For example, Wnt signaling plays a key role in promoting hair = follicle versus epidermal development. After formation of the = hair follicle primordial (placodes), Shh further promotes the = growth and maturation of hair buds by turning on specific=20 transcription factors. Fuchs = (2008)=20 elegantly addresses these issues.

Concluding remarks
Current = progress=20 in studying the self-renewing mechanisms of stem cells = demonstrates=20 how basic stem cell questions are characteristically cell = biological=20 questions and how these questions can be effectively = approached by=20 cell biological approaches. Current findings also reveal that = stem=20 cells use evolutionally conserved molecular pathways and = machineries=20 for their asymmetric division and self-renewal. Thus, the = unique=20 properties of stem cells are more a result of the unique = combination=20 of cell-general mechanisms than the existence and effect of = stem=20 cell=96specific molecules. The three reviews in this issue = each in its=20 own unique way cover this exciting progress as well as = present=20 challenging questions that await exploration. These = challenges and=20 progress invite cell biologists to the fascinating world of = basic=20 stem cell research.


Acknowledgments
I thank Valentina = Greco,=20 Travis Thomson, Li Liu, Xiao Huang, and Jianquan Wang for = critical=20 reading of this review.

The stem cell work in my laboratory is supported by the National = Institutes of Health (grants HD33760, HD42042, and = HD37760S1),=20 the Connecticut Stem Cell Research Fund, the G. Harold and = Leila=20 Mathers Award, and the Stem Cell Research Foundation.

Submitted: 27 December 2007

Accepted: 7 January 2008


References

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Chen, D., and D. McKearin. 2005. Gene circuitry controlling a stem = cell=20 niche. Curr. Biol. 15:179=96184.[CrossRef][Medline]

Chia, W., W.G. Somers, and H. Wang. 2008. Drosophila = neuroblast=20 asymmetric divisions: cell cycle regulators, asymmetric protein = localization,=20 and tumorigenesis. J. Cell Biol. 180:267=96272.[Abstract/Free Full Text]

Deng, W., and H. Lin. 1997. Spectrosomes and fusomes are essential = for=20 anchoring mitotic spindles during asymmetric germ cell divisions and for = the=20 microtubule-based RNA transport during oocyte specification in=20 Drosophila. Dev. Biol. 189:79=9694.[CrossRef][Medline]

Fuchs, E. 2008. Skin stem cells: rising to the surface. J. Cell = Biol.=20 180:273=96284.[Abstract/Free Full Text]

King, F.J., A. Szakmary, D.N. Cox, and H. Lin. 2001. Yb = modulates the=20 divisions of both germline and somatic stem cells through piwi- = and=20 hh-mediated mechanisms in the Drosophila ovary. Mol. = Cell.=20 7:497=96508.[CrossRef][Medline]

Kosodo, Y., K. Roper, W. Haubensak, A.M. Marzesco, D. Corbeil, and = W.B.=20 Huttner. 2004. Asymmetric distribution of the apical plasma membrane = during=20 neurogenic divisions of mammalian neuroepithelial cells. EMBO J.=20 23:2314=962324.[CrossRef][Medline]

Lechler, T., and E. Fuchs. 2005. Asymmetric cell divisions promote=20 stratification and differentiation of mammalian skin. Nature.=20 437:275=96280.[CrossRef][Medline]

Lee, C.Y., K.J. Robinson, and C.Q. Doe. 2006. Lgl, Pins and aPKC = regulate=20 neuroblast self-renewal versus differentiation. Nature. = 439:594=96598.[CrossRef][Medline]

Lin, H. 2002. The stem-cell niche theory: lessons from flies. Nat. = Rev.=20 Genet. 3:931=96940.[CrossRef][Medline]

Lin, H. 2003. To be and not to be. Nature. 425:353=96355.[CrossRef][Medline]

McGrail, M., and T.S. Hays. 1997. The microtubule motor cytoplasmic = dynein is=20 required for spindle orientation during germline cell divisions and = oocyte=20 differentiation in Drosophila. Development. = 124:2409=962419.[Abstract]

Song, X., C.H. Zhu, C. Doan, and T. Xie. 2002. Germline stem cells = anchored=20 by adherens junctions in the Drosophila ovary niches. = Science.=20 296:1855=961857.[Abstract/Free Full Text]

Szakmary, A., D.N. Cox, Z. Wang, and H. Lin. 2005. Regulatory = relationship=20 among piwi, pumilio, and bag-of-marbles in Drosophila germline = stem cell=20 self-renewal and differentiation. Curr. Biol. 15:171=96178.[CrossRef][Medline]

Wu, M., H.Y. Kwon, F. Rattis, J. Blum, C. Zhao, R. Ashkenazi, T.L. = Jackson,=20 N. Gaiano, T. Oliver, and T. Reya. 2007. Imaging hematopoietic precursor = division in real time. Cell Stem Cell. 1:541=96554.[CrossRef]

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quoted-printable Content-Location: http://www.jcb.org/javascript/ajax/xmlhttprequest.js /*=0A= =0A= 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_000A_01C86369.FF6F9DC0 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 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quoted-printable Content-Location: http://www.jcb.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. 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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_000A_01C86369.FF6F9DC0 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"; 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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"-"; 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