From: Subject: Cancerous stem cells can arise from pediatric brain tumors -- Hemmati et al. 100 (25): 15178 -- Proceedings of the National Academy of Sciences Date: Wed, 16 Jan 2008 19:28:24 +0100 MIME-Version: 1.0 Content-Type: multipart/related; type="text/html"; boundary="----=_NextPart_000_0000_01C85875.F651C0F0" X-MimeOLE: Produced By Microsoft MimeOLE V6.00.2900.3198 This is a multi-part message in MIME format. ------=_NextPart_000_0000_01C85875.F651C0F0 Content-Type: text/html; charset="Windows-1252" Content-Transfer-Encoding: quoted-printable Content-Location: http://www.pnas.org/cgi/content/full/100/25/15178 Cancerous stem cells can arise from pediatric brain = tumors -- Hemmati et al. 100 (25): 15178 -- Proceedings of the National = Academy of Sciences
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Published online before print November = 26, 2003,=20 10.1073/pnas.2036535100
PNAS | = December 9,=20 2003 | vol. 100 | no. 25 | 15178-15183


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Neuroscience
Cancerous stem=20 cells can arise from pediatric brain tumors

Houman D. Hemmati *, = Ichiro=20 Nakano 3D{dagger}, Jorge A. Lazareff 3D{ddagger}=20 3D=A7=20, = Michael=20 Masterman-Smith 3D{ddagger}=20, = Daniel=20 H. Geschwind =B6, Marianne=20 Bronner-Fraser *, and Harley I.=20 Kornblum 3D{dagger} 3D=A7 ||=20

*Division of Biology 139-74, California Institute of = Technology,=20 Pasadena, CA 91125; and 3D{dagger}=20Department = of Molecular=20 and Medical Pharmacology, 3D{ddagger}=20Division of = Neurosurgery, and Departments of 3D=A7=20Pediatrics = and=20 =B6Neurology, David Geffen School of Medicine, University of=20 California, Los Angeles, CA 90095=20

Communicated by Michael E. Phelps, University of California School of = Medicine, Los Angeles, CA, October 8, 2003 (received for review June 20, = 2003)


3D"   =20 Abstract
3D"Top
3D"Abstract
Materials and Methods
Results
Discussion
References
 
P= ediatric=20 brain tumors are significant causes of morbidity and = mortality. It=20 has been hypothesized that they derive from self-renewing = multipotent=20 neural stem cells. Here, we tested whether different = pediatric brain=20 tumors, including medulloblastomas and gliomas, contain cells = with=20 properties similar to neural stem cells. We find that = tumor-derived=20 progenitors form neurospheres that can be passaged at clonal = density=20 and are able to self-renew. Under conditions promoting=20 differentiation, individual cells are multipotent, giving = rise to=20 both neurons and glia, in proportions that reflect the tumor = of=20 origin. Unlike normal neural stem cells, however, = tumor-derived=20 progenitors have an unusual capacity to proliferate and = sometimes=20 differentiate into abnormal cells with multiple = differentiation=20 markers. Gene expression analysis reveals that both whole = tumors and=20 tumor-derived neurospheres express many genes characteristic = of=20 neural and other stem cells, including CD133, Sox2, = musashi-1,=20 bmi-1, maternal embryonic leucine zipper kinase, and=20 phosphoserine phosphatase, with variation from tumor to = tumor. After=20 grafting to neonatal rat brains, tumor-derived neurosphere = cells=20 migrate, produce neurons and glia, and continue to = proliferate for=20 more than 4 weeks. The results show that pediatric brain = tumors=20 contain neural stem-like cells with altered characteristics = that may=20 contribute to tumorigenesis. This finding may have important=20 implications for treatment by means of specific targeting of=20 stem-like cells within brain tumors.

Primary malignant central nervous system tumors are the most = frequent=20 form of solid malignancy in children (1). = A=20 heterogeneous group of tumors, some of the most common = histological=20 types are astrocytomas (52%), primitive neuroectodermal = tumors=20 (PNETs), including medulloblastoma (21%), and high-grade = gliomas=20 (19%) (2). = Despite=20 advances in therapy, morbidity and mortality remain high (3).=20

The cellular origin of pediatric brain tumors (PBTs) is unclear. = One possibility is that they arise by transformation of = proliferating=20 neural stem cells (NSCs) (4=96<= A=20 href=3D"http://www.pnas.org/cgi/content/full/100/25/15178#REF6">6), = cells with=20 the ability to self-renew and differentiate into neurons and = glia (7). = There=20 are several lines of indirect evidence in support of this = hypothesis.=20 First, PBTs often contain multiple cell types, suggestive of = an=20 origin from a cell with multilineage potential (8).=20 Second, many PBTs appear to arise from the ventricular zone, = the=20 location of NSCs (9=96<= A=20 href=3D"http://www.pnas.org/cgi/content/full/100/25/15178#REF11">11).= Third,=20 both PBTs and NSCs express nestin, an intermediate filament=20 characteristic of several progenitors (12=96= 14).= Fourth,=20 PBTs often express genes that regulate proliferation and = self-renewal=20 of normal NSCs (15=96= 17)<= SUP>=20 and mutations in genes that normally regulate neural stem = cell=20 proliferation are frequently found in PBTs. Finally, forced=20 expression of oncogenes in neural stem and progenitors cells = in=20 mice produces tumors that are similar to primary human tumors = (6).=20

If PBTs contain cells with stem cell properties, an important=20 question is whether these cells also have abnormal properties = that are responsible for the aberrant and persistent growth = of=20 the tumor (18).= In=20 models of breast cancer and acute myelogenous leukemia, = "cancer stem=20 cells" have been isolated and repassaged into experimental = animals to=20 form new tumors, providing strong evidence that these cells = are the=20 root cause of the tumor (19,<= SUP>=20 20).= =20 Such individual cells are capable of self-renewal, proliferation, = and=20 differentiation to create the complex heterogeneous tumor. It = is=20 unknown whether PBTs contain such cancer stem cells, and, if = so,=20 whether such cells are derived from neural stem cells.

In the current study, we asked whether PBTs contained progenitor = cells with characteristics similar to those of NSCs. We have=20 isolated and characterized multipotent, self-renewing cells=20 from tumor samples, here referred to as "tumor-derived = progenitors,"=20 which have both similarities to and differences from normal=20 NSCs (21).= Cells=20 derived from PBTs were able to produce proliferating = neurospheres=20 that could be passaged at clonal density and differentiated = into=20 cells with defining antigenic characteristics of neurons and = glia.=20 These neurospheres expressed many genes characteristic of = NSC-derived=20 spheres. Furthermore, like normal neurospheres, tumor-derived = spheres=20 migrated and continued to proliferate when transplanted into = neonatal=20 rat brain. Unlike NSCs, however, these tumor-derived = progenitors were=20 more long-lived and often gave rise to abnormal = dual-phenotype cells.=20 Our data suggest that PBTs arise from cells with many of the=20 characteristics of NSCs but with abnormal ability to = propagate and=20 differentiate. These studies also raise the possibility that = some=20 tumor-derived cells may be cancer stem cells with the ability = to=20 generate PBTs.


3D"   =20 Materials and Methods
3D"Top
3D"Abstract
3D"Materials and Methods
Results
Discussion
References
 
<= B>Tissue=20 Collection and Grading. PBT and nontumor human brain = specimens=20 from patients undergoing neocortical resections for = intractable=20 epilepsy were obtained within 30 min of surgical resection in = accordance with protocols approved by institutional review = boards at=20 University of California Los Angeles Medical Center and the=20 California Institute of Technology. The epilepsy surgery = tissue was=20 taken from the lateral ventricular surface and immediately = adjacent=20 tissues. Tumors were graded at the University of California = Los=20 Angeles Medical Center by the attending neuropathologist in=20 accordance with World Health Organization (WHO) established=20 guidelines (22).= =20

Neurosphere Culture. Tumor and neurosphere cultures were=20 performed as according to Svendsen et al. (23) = with some=20 modifications. A detailed protocol is found in Supporting=20 Methods, which is published as supporting information on = the PNAS=20 web site. Briefly, tissue was washed, minced, digested with = trypsin,=20 dissociated, and passed through a series of cell strainers. = Cells=20 were seeded in growth medium supplemented with basic = fibroblast=20 growth factor (20 ng/ml), epidermal growth factor (20 ng/ml), = and=20 leukemia inhibitory factor (20 ng/ml) at a density of 100,000 = cells=20 per ml. Clonal cultures were plated at a density of 1,000 = cells=20 per ml in mouse neurosphere-conditioned medium (24),= a=20 density that has been demonstrated to produce almost entirely = clonal neurospheres (25).= =20

Immunocytochemistry of Neurospheres. Immunocytochemistry = of=20 neurosphere cultures was performed as described (24).= =20 Differentiation of early passage (3D{approx}=204 weeks) spheres was = induced by=20 plating onto coverslips precoated with poly-L-lysine (Sigma) in Neurobasal medium=20 (GIBCO=96Invitrogen) supplemented with B-27 and in the = absence of added=20 basic fibroblast growth factor or epidermal growth factor. = After 7=20 days, the neurospheres were fixed in 4% paraformaldehyde and=20 immunostained with rabbit anti-nestin (1:200; Chemicon) or = rabbit=20 anti-musashi (1:200; Chemicon) for neural stem and progenitor = cells,=20 mouse anti-TuJ1 (1:500; Berkeley Antibodies) or anti-Hu = (1:300;=20 Molecular Probes) for neurons, rabbit anti-glial fibrillary = acidic=20 protein (GFAP; 1:500; DAKO) for astrocytes, and anti-O4 = (1:40;=20 Chemicon) for oligodendrocytes, followed by Alexa=20 fluorophore-conjugated secondary antibodies (1:2,000; = Molecular=20 Probes). In some cases, nuclei were counterstained with=20 4',6-diamidino-2-phenylindole (DAPI).

Statistical Analysis. Statistical analysis of cell counts = was=20 performed as described in Supporting Methods.

Immunohistochemistry of Whole Tumor Sections. = Formalin-fixed,=20 paraffin-embedded tissue specimens from tumors BT1, -2, -3, = and=20 -5 were sectioned at 8 =B5m, mounted on Superfrost Plus = slides=20 (Fisher), deparaffinized, and processed for antigen retrieval = by=20 microwave heating as described (26).= =20

BrdUrd-Labeling of Neurospheres. Neurospheres were = cultured=20 in proliferative medium containing 2 =B5M BrdUrd=20 (5-bromo-2'-deoxyuridine) for 14 h. The cells were fixed in = 4%=20 phosphate-buffered paraformaldehyde solution. Staining with=20 anti-BrdUrd antibody (Becton Dickinson) was performed = according to=20 the supplier's suggestions, and fluorescent secondary = antibody was=20 used.

Semiquantitative RT-PCR. Semiquantitative RT-PCR was = performed=20 with glyceraldehyde-3-phosphate dehydrogenase (GAPDH) as an=20 internal standard as described in Supporting Methods. =

Transplantation of Neurosphere Cells into Neonatal Rat = Brain.=20 Transplantation of 50,000 cells into the neostriata of = neonatal=20 rats was performed according to the methods of Uchida et = al.=20 (27) = with modifications as described in Supporting Methods. =

Immunohistochemical Analysis of Transplanted Rat Brain. = Four=20 weeks after transplantation, tissue was prepared for=20 immunocytochemical analysis as described in Supporting = Methods=20 and stained with antibodies directed against human nuclei, = neurons,=20 astrocytes, and Ki-67.


3D"   =20 Results
3D"Top
3D"Abstract
Materials and Methods
3D"Results
Discussion
References
 
T= wenty-two=20 PBTs were used in the current studies: 10 gliomas (including = 2=20 glioblastomas), 6 medulloblastomas, 5 primitive = neuroectodermal=20 tumors, and 1 ependymoma. For detailed analysis of cell fate = and gene=20 expression, we studied a subgroup of 6 tumors from 5 = pediatric=20 patients, aged 5 months to 6 years [designated tumors 1=965 = (BT1=96BT5);=20 Table = 1].=20 These were a midline anaplastic astrocytoma (World Health=20 Organization grade III astrocytic tumor; BT1), two cerebellar = medulloblastomas (BT2 and BT3), one glioblastoma multiforme = (World=20 Health Organization grade IV astrocytic tumor; BT4), and one=20 desmoplastic medulloblastoma (BT5), distinguished from=20 medulloblastoma by marked neuronal differentiation (22).= =20


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  		Table 1. = Tumor=20 and patient characteristics =

 = ;

Brain Tumor Cells Have the Ability to Form Neurospheres.=20 Dissociated tumor cells were assayed for their ability to = form=20 neurospheres by using the same methods as described = previously for=20 human NSCs (23, = 27).= All 22=20 primary brain tumors studied produced proliferating = neurospheres.=20 Large numbers of small spheres 3D{approx}=204=9610 = cells in diameter=20 were observed in culture flasks between 3 and 7 days after = seeding=20 the cells at 100,000 per ml. Within 2 weeks, most spheres had = increased their diameters 3D{approx}=205- to 10-fold = (Fig.=20 1A). Cells from a local recurrence of one tumor (BT4,=20 glioblastoma multiforme) also gave rise to spheres in = culture.=20 Neurospheres could be passaged multiple times by mechanical=20 dissociation of large spheres and reseeding in fresh = proliferative=20 medium every 2=963 weeks and could be maintained for 16 = weeks or=20 more.



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  		Fig. 1.=20 Tumor-derived progenitors form neurospheres in culture that = give=20 rise to both neuronal and glial cells. Neurospheres from one = tumor,=20 BT1, were cultured at medium (A=96D) and clonal = (E=96H)=20 densities. (A) A typical primary neurosphere. = (B and=20 C) Undifferentiated primary neurospheres expressed = high=20 levels of nestin protein (B, green) and low levels of = -III-tubulin (C, red) and GFAP (C, = green).=20 (D) Expression of 3D{beta}=20-III-tubulin and=20 GFAP, after 7 days of differentiation on substrate. = (E)=20 Nestin expression in undifferentiated clonal neurosphere = cells.=20 (F) Musashi-1 (green) expression in undifferentiated = clonal=20 neurospheres. (G) 3D{beta}=20-III-tubulin (red)=20 and GFAP (green) expression in a differentiated clonal = neurosphere.=20 Some cells (arrows) expressed both markers. (H) Hu = (green)=20 expression in a differentiated neurosphere. Some nuclei were = counterstained with DAPI (F and H, blue). = (Scale bar=20 in H =3D 30 =B5m in A, G, and H, 60 = =B5m in=20 B=96F.) =

=

We next asked whether tumor-derived progenitors maintained the=20 differentiative capacity of NSCs by examining the types of = molecular=20 markers expressed by neurospheres grown under both = proliferative=20 and differentiating conditions with immunocytochemistry. For=20 most tumors, undifferentiated tumor spheres in proliferation=20 medium contained many cells expressing the neural progenitor=20 marker nestin (28) = (Fig.=20 1B; except BT3) and relatively few cells = expressing the=20 neuronal marker 3D{beta}-III-tubulin and/or the astrocytic marker GFAP (Fig.=20 1C). These characteristics persisted even in = long-term=20 cultures (10=9616 weeks).

Under differentiating conditions, cell division in the spheres=20 slowed dramatically and attached cells migrated on the = substrate.=20 Immunocytochemstry revealed an increase in the proportion of=20 cells expressing 3D{beta}-III-tubulin and/or GFAP. Differentiated neurospheres=20 produced numerous cells resembling neurons and astrocytes, = with=20 many cells extending processes on the substrate (Fig.=20 1D).

Tumor-Derived Progenitors Can Be Serially Recloned. = Self-renewal=20 and multipotency are critical features of neural and other = stem=20 cells. We next tested whether individual cells derived from=20 these neurospheres had the ability to form new neurospheres=20 that subsequently differentiated into multiple cell types. = Primary=20 neurospheres were dissociated into single-cell suspensions = and=20 reseeded at clonal density in proliferative medium. After 1=20 day, only individual cells and no clusters could be observed, = verifying their clonal origin. In all cases, clonally derived = neurospheres were visible within 2=964 weeks after reseeding, = suggesting that neurospheres contain individual stem-like = cells=20 with the ability to self-renew and form neurosphere colonies. =

Immunocytochemistry was used to compare the molecular markers=20 expressed by clonal neurospheres grown under proliferation = and=20 differentiation conditions. Undifferentiated clonal spheres=20 from four of five tumors expressed nestin in a large = percentage=20 of their cells (>45%) with little variability between = clones=20 (Figs. 1E= and=20 2 = A, B,=20 D, and E). However, nestin protein expression = was=20 undetectable in BT3, a medulloblastoma (Fig.=20 2C). In addition, tumor-derived spheres expressed=20 musashi-1, another marker of NSCs (Fig.=20 1F) (29).= After=20 transfer to differentiating conditions for 7 days, the = proportion of=20 nestin-expressing cells declined in clonal spheres derived = from three=20 of the four tumors (Fig.= 2=20 A, B, and D); it remained unchanged only in BT5, a=20 desmoplastic medulloblastoma (Fig.=20 2E).



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  		Fig. 2.=20 Neurospheres derived from multiple types of tumors give rise = to=20 cells expressing neuronal and glial markers in various = proportions.=20 (Left) Average count of cells expressing nestin, TuJ1 = alone,=20 GFAP alone, or both markers in clonal neurospheres (NS) from = BT1=965=20 (A=96E) before (white) and after (black) = differentiation.=20 (Right) Fates of clonal neurospheres (NS) after=20 differentiation. Markers used are TuJ1 for neurons (N) and = GFAP for=20 astrocytes (A). =

=

We quantitatively compared the cell types produced by spheres=20 before and after differentiation by using cell type-specific=20 markers. Clonal neurospheres gave rise to cells with neuronal = and glial properties. Under differentiation conditions, the=20 majority of clones from each tumor gave rise to cells = resembling=20 both neurons and glia, with many cells per sphere expressing=20 3D{beta}-III-tubulin and/or GFAP (Fig.=20 1G). The percentage of 3D{beta}=20-III-tubulin+=20 cells in clonal spheres increased significantly after = transfer=20 to differentiation conditions in all tumors except BT5, a=20 desmoplastic medulloblastoma (Fig. = 2=20 Left). The percentage of GFAP+ cells in = clonal=20 spheres increased significantly after differentiation in all = tumors=20 except BT4, a glioblastoma multiforme (Fig. = 2=20 Left). Differentiated clonal spheres expressed the = neuronal=20 HuC/D antigen in proportions similar to their expression of=20 3D{beta}-III-tubulin (Fig.=20 1H). In contrast, the oligodendrocyte marker O4 = could not=20 be detected by immunocytochemistry in clonal or high-density=20 neurospheres. These results show that tumors contain = progenitor cells=20 that are multipotent, giving rise to cells with neuronal and = glial=20 characteristics.

Despite their all being multipotent, the percentage of = differentiated=20 cell types produced varied considerably from one tumor to = another=20 (Fig.=20 2 Right). BT5 produced only neurospheres that = differentiated=20 into both neurons and glia. The remaining tumors gave rise to = a=20 mixture of clones, some of which formed multiple cell types = and=20 others that formed only neuron-like cells.

Properties of Clonally Derived Spheres Recapitulate = Characteristics=20 of the Parental Tumors. To determine whether the above = findings=20 recapitulate the properties of the parental tumors, we = examined=20 nestin, GFAP, and TuJ1 staining of four tumors (Fig. = 3).=20 The staining patterns were broadly similar to those observed = in=20 tumor-derived spheres. For example, BT1 expressed high levels = of nestin within the tumor (Fig.=20 3A) as well as in neurospheres. Many cells in this = same=20 tumor expressed either TuJ1or or GFAP (Fig.=20 3E). BT2 (Fig. 3 = B=20 and F) also expressed all three markers but at = lower=20 levels than BT1, both in the parent tumor and in the = neurospheres.=20 BT3 had little nestin staining in the tumor (although nestin = is=20 obvious in the adjacent normal brain; Fig.= =20 3C); this low level of nestin parallels that observed = in=20 the neurospheres (compare Figs. 2C= and=20 3C= ).=20 With respect to TuJ1 and GFAP (Fig.=20 3G), BT3 had strong reactivity for both, as did = the=20 neurospheres (Fig.=20 2C). BT5 showed good correlation between the = amount of=20 TuJ1 and GFAP staining in both the tumors (Fig.= =20 3H) and neurospheres (Fig.=20 2E); in contrast, nestin expression did correlate = well=20 between tumor and neurosphere in this one particular case = (Figs. 3D= and=20 2E= ).=20 Taken together, these data indicate that the tumor-derived = spheres,=20 even after weeks in culture, differentiate similarly to the = original=20 tumors from which they were derived in the majority of = cases.=20



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  		Fig. 3.=20 Immunohistochemical characteristics of original tumor = samples.=20 Paraffin-embedded sections were labeled with antibodies to = nestin=20 (green; A=96D) or TuJ1 (red; E=96H) to = recognize neurons=20 or GFAP (green; E=96H) to recognize glia. Area = denoted by=20 asterisk in C and F delineates normal brain = tissue=20 adjacent to the tumor. (Scale bar in H =3D 60 =B5m in = A=96H.) =

=

Tumor-Derived Neurospheres Express NSC-Related Genes. We = used=20 semiquantitative RT-PCR analysis to determine whether = neurospheres=20 cultured from PBTs expressed multiple genes enriched in = neural=20 and other stem cells, and to compare expression among = proliferating=20 and differentiating tumor progenitors as well as the parent=20 tumor. Primers were designed for the following human genes:=20 CD133, a cell surface protein expressed on all fetal human = NSCs=20 (27);= =20 musashi-1 (msi1) (30);= Sox2, an=20 early transcription factor expressed in NSCs and the = developing=20 neural tube (31, = 32);= and=20 bmi-1, a Polycomb Group gene required for self-renewal and=20 proliferation of normal and leukemic hematopoietic stem cells = (33, = 34).= We=20 also examined the expression of two genes that we have = identified=20 from mouse neural progenitors by a subtractive microarray = screening=20 approach: melk, maternal embryonic leucine zipper kinase = and=20 PSP, phosphoserine phosphatase (24, = 35, = 36).= Both of=20 these genes are highly and selectively expressed in murine = central=20 nervous system germinal zones and are present in both neural=20 progenitors.

All tumors as well as cells derived from the ventricular zone = of=20 normal brain had detectable gene expression of CD133, Sox2, = melk,=20 PSP, and bmi-1 (Table = 2).=20 Those genes expressed in both tumor-derived and normal = neurospheres=20 were also expressed in their parental tissues, suggesting = that gene=20 expression observed in neurospheres is not an artifact of = cell=20 culture. Sox2, melk, and bmi-1 were expressed = in all=20 whole tumor, normal brain, and undifferentiated neurosphere = samples.=20 Expression of some genes, most noticeably PSP, was = reduced or=20 lost in spheres, as compared with whole tumor or ventricular=20 zone-containing tissue. This finding suggests either that = uncultured=20 tissues expressed these genes at higher levels than their=20 neurosphere-initiating cells and their progeny or that these = genes=20 were down-regulated as a consequence of cell culture. = Neurospheres=20 from BT1 and BT4, both glial tumors of different pathological = grades,=20 expressed nearly all stem cell-related genes, but BT3 and = BT5, both=20 medulloblastomas, had significantly lower or absent = detectable=20 expression of those genes, indicating that cells in glial = tumors=20 might have a closer molecular relation to NSCs. msi1=20 expression was variable but clearly present in spheres = derived from=20 two of the five tumors. In 11 instances, expression of = specific genes=20 in the tumor-derived spheres was reduced after growth factor=20 withdrawal, consistent with our prediction that tumor-derived = progenitors would produce differentiated cells at the expense = of=20 multipotent progenitor cells.


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  		Table 2. = Gene=20 expression analysis =

 = ;

All tumor-derived neurospheres maintained high bmi-1 = expression=20 both under proliferative and after differentiative = conditions.=20 In contrast, normal neurospheres had significantly less = bmi-1=20 expression, which further declined after differentiation. =

Tumor-Derived Neurospheres Incorporate into Rat Brain. To = test=20 whether tumor-derived progenitors possess the ability to = migrate=20 and differentiate after transplantation into rodent brain, = similar=20 to normal human progenitors (27, = 37),= 50,000=20 dissociated cells from neurospheres derived from BT4 at = passage 4=20 were injected into the neostriata of neonatal rats. The data = shown in=20 Fig. 5, which is published as supporting information on the = PNAS=20 web site, demonstrate that the transplanted cells incorporate = into the brain, have the characteristics of migrating neurons = (38),= =20 differentiate into neuronal and glial elements, and continue = to=20 divide as demonstrated by expression of Ki-67, a marker of = cycling=20 cells (39).= =20

Tumor-Derived Neurospheres Are Different from Normal=20 Neurospheres. We compared the properties of tumor-derived = neurospheres with those of normal neurospheres cultured from = the=20 brain tissue of pediatric epilepsy surgery patients. The data = suggest=20 that tumor-derived progenitors are not derived from=20 contaminating normal NSCs. Tumor-derived neurospheres could = be=20 maintained for at least 4 months with no obvious change in = their=20 proliferative properties, whereas normal neurospheres grown = under=20 identical conditions persisted no longer than 1 month in = culture.=20 Tumor-derived spheres demonstrated unusual proliferation even = in=20 apparently differentiated cells. We observed cells that = expressed=20 both 3D{beta}-III-tubulin and Ki-67, suggesting that cells with the = appearance=20 of differentiated neurons were dividing (BT4; Fig.=20 4A). Moreover, 3D{approx}=2050% of 3D{beta}=20-III-tubulin+ cells=20 derived from this tumor incorporated BrdUrd after a 14-h = pulse,=20 indicating that a significant proportion of tumor-derived = neurons=20 divided over a brief time (Fig.=20 4B).



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  		Fig. 4.=20 Tumor-derived neurospheres give rise to neurons that = proliferate=20 aberrantly. (A) Clonal neurosphere derived from the = BT4=20 tumor, double-labeled for 3D{beta}=20-III-tubulin (red)=20 and Ki-67 (green). Nuclei were counterstained with DAPI = (blue).=20 (B) Double-label for BrdUrd (green), visualized after = a 14-h=20 pulse and TuJ1 (red). (Scale bar in B =3D 15 =B5m in = A and=20 B.) =

=

Another distinctive feature of tumor-derived progenitors was = that=20 they gave rise not only to neurons and glia but also to cells = that=20 expressed both 3D{beta}-III-tubulin and GFAP (Fig. = 2).=20 Such dual-fate cells were common and represented a = significant=20 fraction of the population. 3D{beta}=20-III-tubulin+=20 GFAP+ cells were often larger than other cells in = the same=20 sphere (Fig.=20 1G, arrows). In two tumors, BT1 and BT5, the = percentage of=20 3D{beta}-III-tubulin+ GFAP+ cells = exceeded the=20 percentage of cells expressing 3D{beta}=20-III-tubulin = or GFAP=20 alone (Fig.=20 2). Previous studies have reported similar abnormal cells = derived=20 from adult brain tumors (40).= =20


3D"   =20 Discussion
3D"Top
3D"Abstract
Materials and Methods
Results
3D"Discussion
References
 
I= n the=20 present study, we asked whether pediatric brain tumors = contain neural=20 stem-like cells that may be responsible for their formation. = Our=20 results show that tumor-derived cells have the ability to = form=20 neurospheres and can be propagated for prolonged times in = culture.=20 This property is a general property of all of the 22 tumors = examined=20 in this study. We demonstrate that tumor-derived progenitors = and NSCs=20 express many of the same genes and proteins, and they share = some=20 common characteristics, including self-renewal and = multipotency.=20 However, the types of progeny arising from neurospheres vary = from=20 tumor to tumor and, to some extent, recapitulate the = properties of=20 their tumor of origin.

Among the characteristics in common between tumor-derived = spheres=20 and normal neural stem cells is the expression of specific = genes,=20 including CD133, musashi-1, Sox2, melk, PSP, bmi-1, = and=20 nestin. Only one of the tumors we studied, a medulloblastoma=20 (BT3), failed to express nestin in most cells in = undifferentiated=20 clonal neurospheres. Interestingly, BT3 was the least neural = stem=20 cell-like of all of the tumors we tested, giving rise to a = low=20 percentage of multipotent neurospheres that lacked expression = of most=20 known stem cell genes. Sox2, a gene known to play a = role in=20 maintenance of the neural progenitor state (41) = was=20 expressed by all tumors and neurospheres tested. In addition, = tumor-derived spheres express other markers that are = specifically=20 enriched in NSCs, such as maternal embryonic leucine zipper = kinase=20 and phosphoserine phosphatase (35, = 36).= =20

Although tumor-derived progenitors have many similarities to = NSCs=20 and to each other, it is important to note that differences = exist=20 between them and NSCs as well as between tumor-derived = progenitors=20 from different tumors. For example, unlike normal = neurospheres,=20 cancer-derived neurospheres undergo aberrant proliferation = and=20 differentiation. Clonally derived spheres from an individual = tumor=20 generally gave rise to similar percentages of neuron- and = glial-like=20 cells, suggesting that each tumor contained a fundamental = type of=20 stem cell. However, the degree of differentiation and types = of cells=20 produced differed from tumor to tumor, possibly reflecting a=20 fundamental difference in the progenitor cells of different=20 tumors.

One finding of our study is that the tumor-derived neurospheres=20 tend to differentiate into an array of progeny with the same=20 general profile as the parental tumor. Immunohistochemical = analysis=20 of the original tumor revealed striking similarities with the = corresponding neurospheres, suggesting that the presence of=20 diverse cell types in the tumors is not simply a result of = the=20 presence of "host" cells within the tumor mass, but rather is = a=20 property of the tumor itself.

Our finding that PBTs contain neural stem-like cells is = consistent=20 with the hypothesis that at least some PBTs are derived from=20 transformed NSCs in the central nervous system. It has = previously=20 been hypothesized that medulloblastomas and primitive = neuroectodermal=20 tumors (PNETs) are derived from multipotent progenitor cells=20 (8).=20 Our data suggest that these tumors are somewhat similar to = NSCs but=20 more strongly suggest that pediatric astrocytomas and = high-grade=20 gliomas are derived from either NSCs or progenitor cells. = Previous=20 studies have demonstrated that adult high-grade gliomas can = form=20 multiple differentiated cell types (42),= and=20 that some cells can form neurospheres with multiple = differentiated=20 cell types (40).= It is=20 unknown whether the originating cells of PNETs, = medulloblastomas and=20 gliomas, may be the same type of cell, such as a NSC, but = resulting=20 from different transformation events, or whether the glial = tumors=20 arise from a cell at a later stage of differentiation. In the = latter=20 case, a tumor may arise from a glial cell that is caused to=20 dedifferentiate by a transforming event or from a more = gliogenic, but=20 still multipotent, stem cell. In support of the latter = hypothesis is=20 the strong evidence to indicate that there is a lineage of = cells that=20 progresses from primitive cells within the neural tube to = radial glia=20 to GFAP-expressing "astrocytes" that all retain the = fundamental=20 properties of NSCs: self-renewal and multipotency (11, = 43).= =20 Additionally, it is possible that medulloblastomas arise not=20 from a true NSC, but rather from a different type of = progenitor,=20 such as a cerebellar granule cell. In any of the alternatives = presented above, the ultimate result would still be that the=20 tumors themselves contain multipotent self-renewing stem-like = cells.

The mechanism whereby normal NSCs may become malignant is not=20 clear. Our data demonstrate that normal and tumor-derived = spheres=20 express bmi-1, with sphere expression being maintained = even=20 after withdrawal of mitogen, in contrast to what was observed = in normal neural progenitors. This gene has been demonstrated = to be important for self-renewal of both leukemic and normal=20 hematopoietic stem cells (33, = 34).= It is=20 possible that the high level and persistent expression of=20 bmi-1 in tumor cells indicates a greater capacity for=20 self-renewing divisions.

Our data raise the possibility, but do not prove, that = tumor-derived=20 progenitors are cancer stem cells for PBTs. While we have = shown=20 that at least some tumor-derived progenitors, like normal = NSCs,=20 are able to migrate, proliferate, and differentiate when = transplanted=20 into developing rat brains, it is not yet known whether the=20 tumor-derived progenitors also have the ability to form = tumors=20 in an animal model.

Knowledge of the developmental origin of PBTs has important=20 implications for therapy. Our results demonstrate that these=20 tumors contain cells that are multipotent and self-renewing = and=20 are consistent with the hypothesis that these tumors are = derived from=20 progenitor cells with stem-cell like properties. These = observations=20 suggest that therapies for treating PBTs should include = methods for=20 targeting and elimination of the stem cell population. =

Note Added in Proof. After the final revision of this = manuscript=20 was submitted, another paper also demonstrating the presence = of=20 multipotent progenitors in brain tumors was published (44).= =20


3D"   =20 Acknowledgements
 
We are = grateful to=20 Simon Bababeygy, Benjamin Rafii, Miguel Minera, and Alexandra = Lowry=20 for laboratory assistance and patient recruitment, Keith = Tatsukawa=20 for performing animal surgeries, Lori Shoemaker for supplying = neurosphere-conditioned medium, Gary Mathern, Dennis Chute, = and Beth=20 Johnson for brain specimens, and Bud Saxton and Marcos Paiva = for=20 their guidance and support. We thank Drs. Jeffrey Twiss and = Paul=20 Mischel for helpful comments on the manuscript. This work was = supported by U.S. Public Health Service Grant NS42287 (to = M.B.-F.),=20 National Institute of Mental Health Grant MH65756 (to = H.I.K.), and=20 the Jonsson Comprehensive Cancer Center at the University of=20 California, Los Angeles. H.D.H. was supported by the McCallum = Fund at=20 California Institute of Technology, Medical Scientist = Training=20 Program Grant GM08042, and the Aesculapians Fund of the David = Geffen=20 School of Medicine at the University of California, Los = Angeles.=20


3D"   =20 Footnotes
 
Abbreviations: PBTs, pediatric brain tumors; = NSCs,=20 neural stem cells; GFAP, glial fibrillary acidic protein; = DAPI,=20 4',6-diamidino-2-phenylindole.

|| To whom correspondence = should be=20 addressed at: Room 1126 CIMI, 700 Westwood Plaza, Los Angeles, CA 90095. = E-mail:=20 hkornblum{at}mednet.ucla.edu .=20


3D"   =20 References
3D"Top
3D"Abstract
Materials and Methods
Results
Discussion
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 3D""=20 3D"Am.3D"Home
A.=20 Giangreco, K. R. Groot, and S. M. Janes
Lung Cancer and = Lung=20 Stem Cells: Strange Bedfellows?
Am. J. Respir. Crit. = Care=20 Med., March 15, 2007; 175(6): 547 - 553.
[Abstract]<= /A>=20 [Full = Text]=20 [PDF] =
=20 		3D""=20
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T.=20 Aguado, A. Carracedo, B. Julien, G. Velasco, G. Milman, R. = Mechoulam, L.=20 Alvarez, M. Guzman, and I. Galve-Roperh
Cannabinoids = Induce=20 Glioma Stem-like Cell Differentiation and Inhibit=20 Gliomagenesis
J. Biol. Chem., March 2, 2007; = 282(9):=20 6854 - 6862.
[Abstract]=20 [Full = Text]=20 [PDF] =
=20 		3D""=20
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 3D""=20 3D"Cancer3D"Home
C.=20 Li, D. G. Heidt, P. Dalerba, C. F. Burant, L. Zhang, V. Adsay, M. = Wicha,=20 M. F. Clarke, and D. M. Simeone
Identification of = Pancreatic=20 Cancer Stem Cells
Cancer Res., = February 1, 2007;=20 67(3): 1030 - 1037.
[Abstract]=20 [Fu= ll=20 Text] [PDF]=20
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M. E.=20 Prince, R. Sivanandan, A. Kaczorowski, G. T. Wolf, M. J. Kaplan, = P.=20 Dalerba, I. L. Weissman, M. F. Clarke, and L. E.=20 Ailles
Identification of a subpopulation of cells with = cancer=20 stem cell properties in head and neck squamous cell=20 carcinoma
PNAS, January 16, 2007; 104(3): = 973 - 978.=20
[Abstract]=20 [Full = Text]=20 [PDF] =
=20 		3D""=20
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 3D""=20 3D"Home
S.=20 Bruno, B. Bussolati, C. Grange, F. Collino, M. E. Graziano, U. = Ferrando,=20 and G. Camussi
CD133+ Renal Progenitor Cells Contribute = to=20 Tumor Angiogenesis
Am. J. Pathol., = December 1, 2006;=20 169(6): 2223 - 2235.
[Abstra= ct]=20 [Full=20 Text] [PDF] =
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 3D""=20 3D"Clin.3D"Home
K.=20 Tateishi, M. Ohta, F. Kanai, B. Guleng, Y. Tanaka, Y. Asaoka, M. = Tada, M.=20 Seto, A. Jazag, L. Lianjie, et = al.
Dysregulated=20 Expression of Stem Cell Factor Bmi1 in Precancerous Lesions of the = Gastrointestinal Tract
Clin. Cancer Res.,=20 December 1, 2006; 12(23): 6960 - 6966.
[Abstract]=20 [Full=20 Text] [PD= F]=20
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K.=20 Chaichana, G. Zamora-Berridi, J. Camara-Quintana, and A.=20 Quinones-Hinojosa
Neurosphere Assays: Growth Factors = and=20 Hormone Differences in Tumor and Nontumor Studies
Stem = Cells,=20 December 1, 2006; 24(12): 2851 - 2857.
[Abstract]=20 [= Full=20 Text] [PDF]<= /A>=20
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J. A.=20 Kruger, C. D. Kaplan, Y. Luo, H. Zhou, D. Markowitz, R. Xiang, and = R. A.=20 Reisfeld
Characterization of stem cell-like cancer = cells in=20 immune-competent mice
Blood, = December 1, 2006;=20 108(12): 3906 - 3912.
[Abstract]=20 [Full=20 Text] [PDF]=20
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F. J.=20 Sim, H. M. Keyoung, J. E. Goldman, D. K. Kim, H.-W. Jung, N. S. = Roy, and=20 S. A. Goldman
Neurocytoma Is a Tumor of Adult Neuronal=20 Progenitor Cells
J. Neurosci., = November 29, 2006;=20 26(48): 12544 - 12555.
[Abstr= act]=20 [Full=20 Text] [PDF] =
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S.=20 Horvath, B. Zhang, M. Carlson, K. V. Lu, S. Zhu, R. M. Felciano, = M. F.=20 Laurance, W. Zhao, S. Qi, Z. Chen, et = al.
Analysis of=20 oncogenic signaling networks in glioblastoma identifies ASPM as a=20 molecular target
PNAS, November 14, 2006; = 103(46):=20 17402 - 17407.
[Abstract]= =20 [Full=20 Text] [PDF]=20
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L.=20 Balenci, I. D. Clarke, P. B. Dirks, N. Assard, F. Ducray, A. = Jouvet, M.-F.=20 Belin, J. Honnorat, and J. Baudier
IQGAP1 Protein = Specifies=20 Amplifying Cancer Cells in Glioblastoma = Multiforme.
Cancer=20 Res., September 15, 2006; 66(18): 9074 - 9082.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
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C.-L.=20 Tso, P. Shintaku, J. Chen, Q. Liu, J. Liu, Z. Chen, K. Yoshimoto, = P. S.=20 Mischel, T. F. Cloughesy, L. M. Liau, et = al.
Primary=20 Glioblastomas Express Mesenchymal Stem-Like = Properties
Mol.=20 Cancer Res., September 1, 2006; 4(9): 607 - 619.
[Abstra= ct]=20 [Full=20 Text] [PDF] =
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T.=20 Okumura, S. Tsunoda, Y. Mori, T. Ito, K. Kikuchi, T. C. Wang, S. = Yasumoto,=20 and Y. Shimada
The Biological Role of the Low-Affinity = p75=20 Neurotrophin Receptor in Esophageal Squamous Cell=20 Carcinoma
Clin. Cancer Res., = September 1, 2006;=20 12(17): 5096 - 5103.
[Abstract]=20 [Full=20 Text] [PD= F]=20
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S.=20 Bao, Q. Wu, S. Sathornsumetee, Y. Hao, Z. Li, A. B. Hjelmeland, Q. = Shi, R.=20 E. McLendon, D. D. Bigner, and J. N. Rich
Stem = Cell-like Glioma=20 Cells Promote Tumor Angiogenesis through Vascular Endothelial = Growth=20 Factor
Cancer Res., August 15, 2006; 66(16): = 7843 -=20 7848.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
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A.=20 Erlandsson, K. Brannvall, S. Gustafsdottir, B. Westermark, and K.=20 Forsberg-Nilsson
Autocrine/Paracrine Platelet-Derived = Growth=20 Factor Regulates Proliferation of Neural Progenitor=20 Cells
Cancer Res., August 15, 2006; 66(16): = 8042 -=20 8048.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
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X.=20 Fan, W. Matsui, L. Khaki, D. Stearns, J. Chun, Y.-M. Li, and C. G. = Eberhart
Notch Pathway Inhibition Depletes Stem-like = Cells and=20 Blocks Engraftment in Embryonal Brain Tumors.
Cancer = Res.,=20 August 1, 2006; 66(15): 7445 - 7452.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
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M.=20 Dean
CANCER STEM CELLS: Redefining the Paradigm of = Cancer=20 Treatment Strategies
Mol. Interv., = June 1, 2006;=20 6(3): 140 - 148.
= [Abstract]=20 [Ful= l=20 Text] [PDF]= =20
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N.=20 Haraguchi, T. Utsunomiya, H. Inoue, F. Tanaka, K. Mimori, G. F. = Barnard,=20 and M. Mori
Characterization of a Side Population of = Cancer=20 Cells from Human Gastrointestinal System
Stem Cells,=20 March 1, 2006; 24(3): 506 - 513.
[Abstract]=20 [Fu= ll=20 Text] [PDF]=20
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C. A.=20 Huff, W. Matsui, B. D. Smith, and R. J. Jones
The = paradox of=20 response and survival in cancer therapeutics
Blood,=20 January 15, 2006; 107(2): 431 - 434.
[Abstract]=20 [Full=20 Text] = [PDF]=20
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M.=20 Groszer, R. Erickson, D. D. Scripture-Adams, J. D. Dougherty, J. = Le Belle,=20 J. A. Zack, D. H. Geschwind, X. Liu, H. I. Kornblum, and H.=20 Wu
PTEN negatively regulates neural stem cell = self-renewal by=20 modulating G0-G1 cell cycle entry
PNAS,=20 January 3, 2006; 103(1): 111 - 116.
[Abstract]=20 [Full = Text]=20 [PDF] =
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M.=20 Beullens, S. Vancauwenbergh, N. Morrice, R. Derua, H. Ceulemans, = E.=20 Waelkens, and M. Bollen
Substrate Specificity and = Activity=20 Regulation of Protein Kinase MELK
J. Biol. Chem.,=20 December 2, 2005; 280(48): 40003 - 40011.
[Abstract]<= /A>=20 [Full = Text]=20 [PDF] =
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J. D.=20 Dougherty, A. D. R. Garcia, I. Nakano, M. Livingstone, B. Norris, = R.=20 Polakiewicz, E. M. Wexler, M. V. Sofroniew, H. I. Kornblum, and D. = H.=20 Geschwind
PBK/TOPK, a Proliferating Neural = Progenitor-Specific=20 Mitogen-Activated Protein Kinase Kinase
J. Neurosci.,=20 November 16, 2005; 25(46): 10773 - 10785.
[Abstr= act]=20 [Full=20 Text] [PDF] =
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D.=20 Gray, A. M. Jubb, D. Hogue, P. Dowd, N. Kljavin, S. Yi, W. Bai, G. = Frantz,=20 Z. Zhang, H. Koeppen, et al.
Maternal = Embryonic=20 Leucine Zipper Kinase/Murine Protein Serine-Threonine Kinase 38 Is = a=20 Promising Therapeutic Target for Multiple = Cancers
Cancer Res.,=20 November 1, 2005; 65(21): 9751 - 9761.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
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N.=20 Sanai, A. Alvarez-Buylla, and M. S. Berger
Neural Stem = Cells=20 and the Origin of Gliomas
N. Engl. J. Med.,=20 August 25, 2005; 353(8): 811 - 822.
[Full = Text]=20 [PDF] =
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L.=20 Patrawala, T. Calhoun, R. Schneider-Broussard, J. Zhou, K. = Claypool, and=20 D. G. Tang
Side Population Is Enriched in Tumorigenic,=20 Stem-Like Cancer Cells, whereas ABCG2+ and ABCG2- Cancer Cells Are = Similarly Tumorigenic
Cancer Res., = July 15, 2005;=20 65(14): 6207 - 6219.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
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B. M.=20 Deasy, B. M. Gharaibeh, J. B. Pollett, M. M. Jones, M. A. Lucas, = Y. Kanda,=20 and J. Huard
Long-Term Self-Renewal of Postnatal = Muscle-derived=20 Stem Cells
Mol. Biol. Cell, July 1, 2005; = 16(7):=20 3323 - 3333.
[Abstr= act]=20 [Full=20 Text] [PDF] =
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B.=20 Dasgupta and D. H. Gutmann
Neurofibromin Regulates = Neural Stem=20 Cell Proliferation, Survival, and Astroglial Differentiation In = Vitro and=20 In Vivo
J. Neurosci., June 8, 2005; 25(23): = 5584 -=20 5594.
[Abstra= ct]=20 [Full=20 Text] [PDF] =
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T. G.=20 Oliver, T. A. Read, J. D. Kessler, A. Mehmeti, J. F. Wells, T. T. = T.=20 Huynh, S. M. Lin, and R. J. Wechsler-Reya
Loss of = patched and=20 disruption of granule cell development in a pre-neoplastic stage = of=20 medulloblastoma
Development, May 15, 2005; = 132(10):=20 2425 - 2439.
[Abst= ract]=20 [Full=20 Text] [PDF]=20
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 3D""=20 3DCarcinogenesis=203D"Home
F.=20 Behbod and J. M. Rosen
Will cancer stem cells provide = new=20 therapeutic targets?
Carcinogenesis, = April 1, 2005;=20 26(4): 703 - 711.
[= Abstract]=20 [Full= =20 Text] [PDF] =
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R.=20 Glass, M. Synowitz, G. Kronenberg, J.-H. Walzlein, D. S. Markovic, = L.-P.=20 Wang, D. Gast, J. Kiwit, G. Kempermann, and H.=20 Kettenmann
Glioblastoma-Induced Attraction of = Endogenous Neural=20 Precursor Cells Is Associated with Improved = Survival
J.=20 Neurosci., March 9, 2005; 25(10): 2637 - 2646.
[Abstra= ct]=20 [Full=20 Text] [PDF] =
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X.=20 Fan, I. Mikolaenko, I. Elhassan, X. Ni, Y. Wang, D. Ball, D. J. = Brat, A.=20 Perry, and C. G. Eberhart
Notch1 and Notch2 Have = Opposite=20 Effects on Embryonal Brain Tumor Growth
Cancer Res.,=20 November 1, 2004; 64(21): 7787 - 7793.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
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R.=20 Galli, E. Binda, U. Orfanelli, B. Cipelletti, A. Gritti, S. De = Vitis, R.=20 Fiocco, C. Foroni, F. Dimeco, and A. Vescovi
Isolation = and=20 Characterization of Tumorigenic, Stem-like Neural Precursors from = Human=20 Glioblastoma
Cancer Res., October 1, 2004; = 64(19):=20 7011 - 7021.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
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R. W.=20 Georgantas III, V. Tanadve, M. Malehorn, S. Heimfeld, C. Chen, L. = Carr, F.=20 Martinez-Murillo, G. Riggins, J. Kowalski, and C. I.=20 Civin
Microarray and Serial Analysis of Gene Expression = Analyses Identify Known and Novel Transcripts Overexpressed in=20 Hematopoietic Stem Cells
Cancer Res., = July 1, 2004;=20 64(13): 4434 - 4441.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
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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_0000_01C85875.F651C0F0 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://www.pnas.org/javascript/ajax/utility.js /************************************************************************= *****=0A= * javascript/ajax/utility.js=0A= *=0A= * Utility functions for working with XMLHttpRequest data.=0A= *=0A= * Copyright 2006 Board of Trustees of the Leland Stanford Junior = University.=0A= = *************************************************************************= ***/=0A= =0A= /*=0A= * Copy XML nodes into an HTMLElement. This effectively=0A= * clones XML markup which uses XHTML naming conventions=0A= * into an HTML DOM.=0A= */=0A= function copy_xml_to_html(src, dst) {=0A= if (src.nodeType =3D=3D 1) { /* Node.ELEMENT_NODE */=0A= var e =3D document.createElement(src.nodeName);=0A= for (var i =3D 0; i < src.childNodes.length; i++) {=0A= copy_xml_to_html(src.childNodes[i], e);=0A= }=0A= for (var i =3D 0; i < src.attributes.length; i++) {=0A= var n =3D src.attributes[i].name;=0A= var v =3D unescape_xml_string(src.attributes[i].value); =0A= e.setAttribute(n, v);=0A= if (n =3D=3D "class") {=0A= e.className =3D v;=0A= }=0A= else if (n =3D=3D "style") {=0A= set_css_style(v, e, "");=0A= }=0A= }=0A= dst.appendChild(e);=0A= }=0A= else if (src.nodeType =3D=3D 3) { /* Node.TEXT_NODE */=0A= dst.appendChild(document.createTextNode(src.nodeValue));=0A= }=0A= }=0A= =0A= /* =0A= * It is unclear that this is the right thing to be calling=0A= * from copy_xml_to_html, but it appears that Safari decides=0A= * to convert & to the NCR #, and then encodes that=0A= * NCR to &%26%2338;. So, I'm going to treat the DOM Attr=0A= * value as a plain string, and run our XML string input=0A= * through the decoding routine below.=0A= */=0A= function unescape_xml_string(s) {=0A= return s.replace(/'/g, "'")=0A= .replace(/'/g, "'")=0A= .replace(/"/g, "\"")=0A= .replace(/"/g, "\"")=0A= .replace(/>/g, ">")=0A= .replace(/>/g, ">")=0A= .replace(/</g, "<")=0A= .replace(/</g, "<")=0A= .replace(/&/g, "&")=0A= .replace(/&/g, "&");=0A= }=0A= =0A= /*=0A= * Parse set of CSS rules and apply them to an element.=0A= * This is quite horrifying, but I'm unable to determine=0A= * how else to handle this with IE 6. FireFox and other=0A= * sane browsers let you simply set the style attribute=0A= * or use e.style.setProperty(rule, value, priority),=0A= * IE 6 appears to have neither of these capabilities..=0A= */=0A= function set_css_style(css, e, priority) {=0A= var rules =3D css.split(";");=0A= for (var i =3D 0; i < rules.length; i++) {=0A= var nvpair =3D rules[i].split(":");=0A= if (nvpair.length =3D=3D 2) {=0A= try {=0A= var name =3D nvpair[0]; /* style attribute */=0A= var value =3D nvpair[1]; /* attribute value */=0A= =0A= /*=0A= * For each possible style attribute, set the=0A= * appropriate style property in the element.=0A= */=0A= if (name =3D=3D "background") {=0A= e.style.background =3D value;=0A= }=0A= else if (name =3D=3D "background-attachment") {=0A= e.style.backgroundAttachment =3D value;=0A= }=0A= else if (name =3D=3D "background-color") {=0A= e.style.backgroundColor =3D value;=0A= }=0A= else if (name =3D=3D "background-image") {=0A= e.style.backgroundImage =3D value;=0A= }=0A= else if (name =3D=3D "background-position") {=0A= e.style.backgroundPosition =3D value;=0A= }=0A= else if (name =3D=3D "background-position-x") {=0A= e.style.backgroundPositionX =3D value;=0A= }=0A= else if (name =3D=3D "background-position-y") {=0A= e.style.backgroundPositionY =3D value;=0A= }=0A= else if (name =3D=3D "background-repeat") {=0A= e.style.backgroundRepeat =3D value;=0A= }=0A= else if (name =3D=3D "behavior") {=0A= e.style.behavior =3D value;=0A= }=0A= else if (name =3D=3D "border") {=0A= e.style.border =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom") {=0A= e.style.borderBottom =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-color") {=0A= e.style.borderBottomColor =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-style") {=0A= e.style.borderBottomStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-width") {=0A= e.style.borderBottomWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-collapse") {=0A= e.style.borderCollapse =3D value;=0A= }=0A= else if (name =3D=3D "border-color") {=0A= e.style.borderColor =3D value;=0A= }=0A= else if (name =3D=3D "border-left") {=0A= e.style.borderLeft =3D value;=0A= }=0A= else if (name =3D=3D "border-left-color") {=0A= e.style.borderLeftColor =3D value;=0A= }=0A= else if (name =3D=3D "border-left-style") {=0A= e.style.borderLeftStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-left-width") {=0A= e.style.borderLeftWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-right") {=0A= e.style.borderRight =3D value;=0A= }=0A= else if (name =3D=3D "border-right-color") {=0A= e.style.borderRightColor =3D value;=0A= }=0A= else if (name =3D=3D "border-right-style") {=0A= e.style.borderRightStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-right-width") {=0A= e.style.borderRightWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-style") {=0A= e.style.borderStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-top") {=0A= e.style.borderTop =3D value;=0A= }=0A= else if (name =3D=3D "border-top-color") {=0A= e.style.borderTopColor =3D value;=0A= }=0A= else if (name =3D=3D "border-top-style") {=0A= e.style.borderTopStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-top-width") {=0A= e.style.borderTopWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-width") {=0A= e.style.borderWidth =3D value;=0A= }=0A= else if (name =3D=3D "bottom") {=0A= e.style.bottom =3D value;=0A= }=0A= else if (name =3D=3D "clear") {=0A= e.style.clear =3D value;=0A= }=0A= else if (name =3D=3D "clip") {=0A= e.style.clip =3D value;=0A= }=0A= else if (name =3D=3D "color") {=0A= e.style.color =3D value;=0A= }=0A= else if (name =3D=3D "cssText") {=0A= e.style.Sets =3D value;=0A= }=0A= else if (name =3D=3D "cursor") {=0A= e.style.cursor =3D value;=0A= }=0A= else if (name =3D=3D "direction") {=0A= e.style.direction =3D value;=0A= }=0A= else if (name =3D=3D "display") {=0A= e.style.display =3D value;=0A= }=0A= else if (name =3D=3D "font") {=0A= e.style.font =3D value;=0A= }=0A= else if (name =3D=3D "font-family") {=0A= e.style.fontFamily =3D value;=0A= }=0A= else if (name =3D=3D "font-size") {=0A= e.style.fontSize =3D value;=0A= }=0A= else if (name =3D=3D "font-style") {=0A= e.style.fontStyle =3D value;=0A= }=0A= else if (name =3D=3D "font-variant") {=0A= e.style.fontVariant =3D value;=0A= }=0A= else if (name =3D=3D "font-weight") {=0A= e.style.fontWeight =3D value;=0A= }=0A= else if (name =3D=3D "height") {=0A= e.style.height =3D value;=0A= }=0A= else if (name =3D=3D "ime-mode") {=0A= e.style.imeMode =3D value;=0A= }=0A= else if (name =3D=3D "layout-flow") {=0A= e.style.layoutFlow =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid") {=0A= e.style.layoutGrid =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-char") {=0A= e.style.layoutGridChar =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-line") {=0A= e.style.layoutGridLine =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-mode") {=0A= e.style.layoutGridMode =3D value;=0A= }=0A= else if (name 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