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[Cancer Research 63, 5821-5828, September 15, = 2003]
=A9 2003=20 American=20 Association for Cancer Research

Regular Articles

Identification of a Cancer Stem Cell in Human Brain Tumors=20

Sheila K. Singh, Ian D. = Clarke,=20 Mizuhiko Terasaki, Victoria E. Bonn, = Cynthia=20 Hawkins, Jeremy Squire and Peter B. = Dirks=20

The Arthur and Sonia Labatt Brain Tumour Research = Centre, The=20 Hospital for Sick Children, Toronto, Ontario M5G 1X8, Canada [S. K. S., = I. D.=20 C., M. T., V. E. B., P. B. D.], and Program in Developmental Biology [S. = K. S.,=20 I. D. C., M. T., V. E. B., P. B. D.], Division of Neurosurgery [S. K. = S., P. B.=20 D.], Department of Pediatric Laboratory Medicine [C. H.], and Department = of=20 Laboratory Medicine and Pathobiology [J. S.], University of Toronto, = Toronto,=20 Ontario M5G 1X8 Canada


3D"   =20 ABSTRACT
Top
3D"ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
 
M= ost=20 current research on human brain tumors is focused on the = molecular=20 and cellular analysis of the bulk tumor mass. However, there = is=20 overwhelming evidence in some malignancies that the tumor = clone is=20 heterogeneous with respect to proliferation and = differentiation. In=20 human leukemia, the tumor clone is organized as a hierarchy = that=20 originates from rare leukemic stem cells that possess = extensive=20 proliferative and self-renewal potential, and are responsible = for=20 maintaining the tumor clone. We report here the = identification and=20 purification of a cancer stem cell from human brain tumors of = different phenotypes that possesses a marked capacity for=20 proliferation, self-renewal, and differentiation. The = increased=20 self-renewal capacity of the brain tumor stem cell (BTSC) was = highest=20 from the most aggressive clinical samples of medulloblastoma = compared=20 with low-grade gliomas. The BTSC was exclusively isolated = with the=20 cell fraction expressing the neural stem cell surface marker = CD133.=20 These CD133+ cells could differentiate in culture into tumor = cells=20 that phenotypically resembled the tumor from the patient. The = identification of a BTSC provides a powerful tool to = investigate the=20 tumorigenic process in the central nervous system and to = develop=20 therapies targeted to the BTSC.


3D"   =20 INTRODUCTION
Top
ABSTRACT
3D"INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
 
B= rain=20 tumors are the leading cause of cancer mortality in children = and=20 remain difficult to cure despite advances in surgery and = adjuvant=20 therapy. Most current brain tumor research is focused on the=20 molecular and cellular analysis of the bulk tumor mass. Brain = tumors=20 are typically comprised of morphologically diverse cells that = express=20 a variety of neural lineage markers. Study of the basic = morphology=20 and phenotype of brain tumors has only yielded a limited = amount of=20 knowledge of the clinical behavior of the tumor, as brain = tumors that=20 share similar morphology and phenotype can have a very = different=20 prognosis and response to treatment. We lack a functional = assay of=20 the brain tumor cells that could determine which of the=20 morphologically diverse tumor cells are capable of = maintaining the=20 growth of the tumor. Determination of key cells in the tumor=20 population that are able to maintain the tumor will give = insight into=20 the mechanism of brain tumorigenesis and will allow us to = trace back=20 to the cell of origin in the normal brain.

There is overwhelming evidence in other malignancies, such as=20 leukemia, that the clonal population of neoplastic cells = exhibits=20 marked heterogeneity with respect to proliferation and=20 differentiation (1=20 ,=20 2) . Rare stem cells within the leukemic population possess=20 extensive proliferation and self-renewal capacity that is not = found in the majority of the leukemic cells. The ability to=20 fractionate and functionally analyze leukemic stem cells led = to=20 the determination that they are necessary and sufficient to = maintain=20 the leukemia (1=20 ,=20 3) .

We have applied the techniques used to isolate normal neural = stem=20 cells in culture (as clonally derived neurospheres, each of = which=20 arise from a single stem cell; Ref. 4 )=20 to the analysis of human pediatric brain tumors. We used = assays of=20 neurosphere cells to functionally characterize the tumor cell = populations. We report the identification and purification of = a cell=20 from primary human brain tumors of different phenotypes that = has=20 marked capacity for proliferation, self-renewal, and = differentiation.=20 This cell represented a minority of the tumor cell population = and was identified by expression of the cell surface marker=20 CD133. This CD133+ cell, which we have termed the BTSC,3=20 lacked the expression of neural differentiation markers, and = was=20 necessary for the proliferation and self-renewal of the tumor = in=20 culture. This cell was also capable of differentiating in=20 vitro into cell phenotypes identical to the tumor in = situ.=20 The marker phenotype of the BTSC was similar to that of = normal neural=20 stem cells, in that it expressed CD133 and nestin, and was = the same=20 in patients with the same pathological type of tumor and in = patients=20 with different pathological subtypes. This suggests that = brain=20 tumors can be generated from BTSCs that share a very similar=20 phenotype. A better understanding of brain tumor biology will = come=20 from additional cellular and molecular studies of the BTSC.=20 Comparison of normal neural stem cells and BTSCs will aid in = finding=20 the normal brain cell that originates the tumor.


3D"   =20 MATERIALS AND METHODS
Top
ABSTRACT
INTRODUCTION
3D"MATERIALS AND = METHODS
RESULTS
DISCUSSION
REFERENCES
 
<= STRONG>Primary=20 Tumor Sphere Culture.
Tumor samples were obtained from = consenting=20 patients, as approved by the Research Ethics Board at The = Hospital=20 for Sick Children. Tumors were washed, acutely dissociated in = oxygenated artificial cerebrospinal fluid and subject to = enzymatic=20 dissociation as described previously (4)=20 . Tumor cells were then resuspended in TSM consisting of a = chemically=20 defined serum-free neural stem cell medium (4)=20 , human recombinant EGF (20 ng/ml; Sigma), bFGF (20 ng/ml; = Upstate),=20 leukemia inhibitory factor (10 ng/ml; Chemicon), Neuronal = Survival=20 Factor (NSF) (1x; Clonetics), and N-acetylcysteine (60 = =B5g/ml;=20 Sigma; Ref. 5 ),=20 and plated at a density of 3 x=20 106 live cells/60-mm plate. RBCs were removed = using=20 lympholyte-M (Cedarlane).

Limiting Dilution Assay and Primary Sphere Formation=20 Assay.
Limiting dilution assay was performed as described=20 previously (6=20 ,=20 7) . After primary sphere formation was noted, sphere cells = were=20 dissociated and plated in 96-well microwell plates in 0.2 ml = volumes=20 of TSM. Final cell dilutions ranged from 200 cells/well to 1=20 cell/well in 0.2-ml volumes. Cultures were fed 0.025 ml of = TSM every=20 2 days until day 7, when the percentage of wells not = containing=20 spheres for each cell plating density was calculated and = plotted=20 against the number of cells per well. Regression lines were = plotted=20 and x-intercept values calculated, which represent the number = of=20 cells required to form at least 1 tumor sphere in every well. = CD133-adherent tumor cells were trypsinized before collection = for=20 assays. For primary sphere formation assays, this analysis = was=20 performed on the entire acutely dissociated tumor cell = population on=20 day 0 to quantify stem cell frequency within the tumor. =

Cell Proliferation Assays.
Cells were plated in = 96-well=20 microwell plates in 0.1-ml volumes of SFM supplemented with = growth=20 factors, at a density of 1000 cells/well. Cell proliferation = assays=20 were performed on days 0, 3 5, and 7 postplating using the = Roche=20 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium = bromide-based=20 Colorimetric Assay Cell Proliferation kit 1. Quantification = of viable=20 cells through reading of UV absorption spectrums at 575 nm = was=20 performed on a Versamax microplate reader.

Differentiation Assay of Tumor Spheres.
Two days = after=20 primary culture, cells were plated onto glass coverslips = coated in=20 poly-L-ornithine (Sigma; Ref. 4 )=20 in medium with 10% FBS in individual wells of a 24-well = culture=20 plate. Cells were fed with FBS-supplemented medium every 2 = days,=20 and coverslips were processed 7 days after plating using=20 immunocytochemistry.

Immunocytochemical Staining of Tumor Stem=20 Cells.
Immunocytochemistry was performed as described = previously (7)=20 . Briefly, for immunostaining of undifferentiated tumor = spheres,=20 cells were plated onto poly-L-ornithine = coated glass=20 coverslips in SFM containing 10% FBS, for 4 h. Cells were = then fixed=20 with 4% paraformaldehyde and stained with antibodies against=20 CD133/1 (mouse monoclonal IgG1; Miltenyi Biotec), nestin = (rabbit=20 polyclonal; Chemicon), =DF-tubulin 3 (mouse monoclonal IgG1;=20 Chemicon), GFAP (rabbit polyclonal; DAKO), mitogen-activated = protein=20 2 (mouse monoclonal IgG1; Chemicon), and PDGFR 3D{alpha}=20 = (rabbit=20 polyclonal C20; Santa Cruz Biotechnology). Appropriate = secondary=20 antibodies (Texas Red donkey antirabbit; Jackson = Immunoresearch; and=20 Alexa 488 goat antimouse; Molecular Probes) were used. =

For immunostaining of differentiated tumor cells, = differentiation=20 assays were performed 2 days after primary tumor culture; 7=20 days after differentiation, immunocytochemistry was performed = as described above. Cells were additionally immunostained = with=20 4',6-diamidino-2-phenylindole (Sigma), to permit counting of=20 cell nuclei in at least 5 microscopic fields per specimen.=20 Quantification of cells stained with each antibody could then = be=20 averaged and estimated as a percentage of total nuclei = counted.=20

Magnetic Cell Sorting and Flow Cytometry.
Within = 3 days=20 of primary culture, cells were centrifuged at 800 x g for 5 min, triturated with a=20 fire-narrowed Pasteur pipette, and resuspended in 1x PBS with 0.5% BSA and 2 mM=20 EDTA. Magnetic labeling with 1 =B5l CD133/1 Microbeads/1 = million=20 cells was performed using the Miltenyi Biotec CD133 Cell=20 Isolation kit. Ten =B5l of CD133=962-phycoerythrin=20 (fluorochrome-conjugated mouse monoclonal IgG1; Miltenyi = Biotec) was=20 added for an additional 30 min to evaluate the efficiency of = magnetic=20 separation by flow cytometry. Magnetic separation was carried = out on=20 the autoMACS machine (Miltenyi Biotec). Positive and negative = fractions were eluted with a double-sensitive mode. Aliquots = of=20 CD133+ and CD133- sorted cells were evaluated for purity by = flow=20 cytometry with a FACSCalibur machine (BD Biosciences). CD133+ = and=20 CD133- sorted cell populations were resuspended in SFM with=20 growth hormones.

Spectral Karyotype Analysis of Tumor Sphere = Cells.
Tumor=20 spheres were gently aspirated to disaggregate and cultured in = TSM as=20 described above. The cultures were harvested within 3=965 = days with 0.1=20 =B5g/ml Colcemid (Life Technologies, Inc.) for 2=963 h, KCl = (0.075 M) -treated, and fixed in 3:1 methanol: = acetic acid.=20 SKY was performed on tumor metaphase cells according to the=20 manufacturer=92s instructions (ASI, Carlsbad, CA) and as = published=20 previously (8)=20 . Spectral images were acquired and analyzed with an SD 200 = Spectral=20 Bio-imaging System (ASI Ltd., MigdalHaemek, Israel) attached = to a=20 Zeiss Axioplan 2 microscope (Carl Zeiss, Toronto, Ontario,=20 Canada), and analyzed using SKYVIEW (ver. 1.2; ASI) = software.=20

Immunohistochemistry on Tumor = Sections.
Formalin-fixed,=20 paraffin-embedded tissue sections were mounted on positive = charged=20 microscope slides. Tissue sections were then baked overnight = at 60=B0C,=20 and treated with epitope retrieval techniques and blocked for = endogenous peroxidase and biotin before the application of = the=20 primary antibody. Incubation of antihuman CD133 at a 1:10 = dilution=20 was performed overnight at room temperature. Subsequent=20 immunodetection was performed using the Elite Vector Stain = ABC System=20 (Vector Laboratories, Burlingham, CA). Color visualization = was=20 performed using 3-3'-diaminobenzidine as the chromagen = substrate=20 (Sigma Chemical Company, St. Louis, MO).


3D"   =20 RESULTS
Top
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
3D"RESULTS
DISCUSSION
REFERENCES
 
<= STRONG>Primary=20 Brain Tumors of Different Phenotypes Form Neurosphere-like=20 Colonies.
One key determinant of stem cells is the capacity = for=20 extensive proliferation. To determine whether cells with = distinct=20 proliferative abilities were present in human brain tumors, = we=20 established cultures from 14 solid primary pediatric brain = tumors=20 (Table 1) , which were acutely dissociated into individual cells. = We=20 used culture conditions that favored stem cell growth, = established=20 previously for isolation of neural stem cells as neurospheres = (4)=20 . SFM allows for the maintenance of an undifferentiated stem = cell=20 state, and the addition of bFGF and EGF induced the = proliferation of=20 multipotent, self-renewing, and expandable neural stem cells = (9=20 ,=20 10) . Regardless of pathological subtype, within 24=9648 = h of=20 primary culture all of the brain tumors yielded a minority = fraction=20 of cells that demonstrated growth into clonally derived=20 neurosphere-like clusters, termed tumor spheres (Fig. 1) . The frequency of the stem cell population = within the=20 tumor was determined by primary sphere formation assays = performed on=20 6 tumors, yielding a stem cell frequency ranging from 0.3% to = 25.1%=20 (Table 2) . The remaining majority of tumor cells = exhibited=20 adherence, loss of proliferation, and subsequent = differentiation,=20 whereas tumor spheres remained nonadherent, continuing to = proliferate=20 and expand the tumor cell culture over time. Tumor spheres = generated=20 from all 14 of the specimens showed immunoreactivity for = nestin (an=20 intermediate filament protein found in undifferentiated = central=20 nervous system cells and a characteristic neural stem cell = marker;=20 Ref. 11=20 ) and for CD133, a novel putative neural stem cell marker = (Refs. 5 ,=20 12 ; Fig. 1, E=96L ). Furthermore, the tumor spheres did not = express=20 markers for differentiated neurons, astrocytes, or=20 oligodendrocytes.


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  		Table 1 Summary of patient = population =

 = ;


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  		Fig. 1. Primary brain tumors of = different=20 phenotypes form neurosphere-like colonies. Photomicrographs = of=20 cultured brain tumor cells (magnification x20) at 24=9648 h after = plating in TSM,=20 containing EGF and bFGF. Each tumor subtype yielded growth = of cells=20 in neurosphere-like clusters, termed tumor spheres. Tumor = spheres=20 are shown from a medulloblastoma (A), pilocytic = astrocytoma=20 (B), ependymoma (C), and ganglioglioma = (D).=20 Undifferentiated primary tumor spheres from a = medulloblastoma (E,=20 F, I, and J) and a pilocytic astrocytoma (G, = H, K,=20 and L) are immunostained at 4 h for characteristic = neural=20 stem cell marker nestin (E and G) and for = CD133=20 (F and H). Individual undifferentiated = medulloblastoma=20 sphere cells and astrocytoma sphere cells are also shown = stained for=20 nestin (I and K) and CD133 (J and = L). =

 = ;

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  		Table 2 Primary sphere formation = assay =

 = ;
Tumor=20 Sphere Cells Exhibit Increased Potential For = Self-Renewal.
Only a=20 small proportion (<1%) of cells composing individual = neurospheres=20 from a normal brain are stem cells with the ability to = self-renew and=20 generate all neural lineages (9=20 ,=20 13) . The remaining majority are progenitor cells with = more=20 restricted self-renewal capacity and lineage potential. Tumor = spheres=20 are defined as clonally derived nonadherent colonies of cells = derived from a single tumor stem cell. To build on the = analogy=20 between neurosphere and tumor sphere, we subjected tumor = spheres=20 to stem cell assays designed to test the self-renewal,=20 proliferation, and differentiation capacities of a putative=20 BTSC.

The self-renewing capacity of the tumor spheres was assayed = by=20 dissociation of primary tumor spheres, and plating of cells = at serial=20 dilutions down to 1 cell/well. All of the dissociated primary = tumor=20 spheres demonstrated the capacity to form secondary tumor = spheres,=20 exhibiting an ability to self-renew. When self-renewal = capacity was=20 compared among tumor subtypes at a plating density of 100 = cells/well,=20 medulloblastomas were found to generate a greater mean number = of=20 secondary tumor spheres (20.27 =B1 SE 5.24), compared with = pilocytic=20 astrocytomas (5.85 =B1 SE 1.96) and to control sphere forming = human=20 fetal neural stem cells (Clonetics; 2.88 =B1 SE 0.25; Fig. = 2A ).



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  		Fig. 2. Tumor sphere cells = exhibit=20 increased self-renewal potential compared with controls. = A,=20 when tumor cells were plated at a density of 100 cells/well, = medulloblastomas were found to generate a greater mean = number of=20 secondary tumor spheres (20.27 =B1 5.24) than pilocytic = astrocytomas=20 (5.85 =B1 1.96) or control human neural stem cells (2.88 =B1 = 0.25).=20 B, cells plated at limiting dilution in 200 =B5l = volumes of=20 medium showed that the frequency at which one tumor stem = cell=20 proliferates to form a secondary tumor sphere varied = according to=20 tumor pathology [representative samples of each tumor = subtype shown:=20 medulloblastoma, patient 14 (3D{blacktriangleup}=20),=20 pilocytic astrocytoma, patient 10 (3D{circ}=20), and=20 control fetal human neural stem cells (3D{bullet}=20)].=20 The mean x-intercept values calculated from limiting = dilution=20 analysis for each tumor subtype reveal that the number of = cells=20 required to form at least 1 tumor sphere/well was much lower = in=20 medulloblastomas (3D{circ}=20),=20 compared with gliomas (3D{blacktriangleup}=20) or=20 human controls (3D{bullet}=20;=20 Fig. 2B; Table 2 ). C, morphology of secondary tumor = spheres was=20 identical to that of primary tumor spheres (magnification = x200). D and E,=20 undifferentiated secondary tumor spheres (magnification = x100) retain expression of = neural stem=20 cell markers nestin (with rhodamine, in red; = D) and=20 CD133 (with FITC, in green; E). =

 = ;
If=20 a single tumor sphere results from the proliferation of a = single=20 BTSC, limiting dilution analysis allows for the determination = of the=20 minimal frequency of repopulating tumor sphere cells within = the cell=20 population (6=20 ,=20 7) . The number of cells required to generate at least 1 = tumor=20 sphere/well was calculated as 23.5 =B1 17.0 (SD) in the=20 medulloblastomas, 99.18 =B1 45.9 (SD) in the pilocytic = astrocytomas,=20 and 98.25 =B1 4.6 (SD) in the control human neural stem cells = (Table=20 3 ; Fig. 2B ). These data reveal that the frequency at = which 1=20 tumor sphere cell will proliferate to form a new tumor sphere = varied=20 according to tumor pathological subtype, with more aggressive = medulloblastomas exhibiting increased self-renewal capacity = compared=20 with pilocytic astrocytomas (P =3D 0.004) and human = neural stem=20 cell controls (P =3D 0.001). Morphology of secondary = tumor=20 spheres was identical to that of primary spheres (Fig. = 2C) , and secondary tumor spheres retain = expression of the=20 neural stem cell markers nestin (Fig. 2D) and CD133 (Fig. 2E) , whereas failing to express neural = differentiation=20 markers. Secondary spheres from two medulloblastomas (patient = 7 and=20 patient 14) were passaged to tertiary spheres, and quantified = by=20 limiting dilution at 12.5 cells/well and 20 cells/well, = respectively.=20 All of the tumors studied generated spheres with multiple = passages.=20 These data show that all of the brain tumors had a = subpopulation of=20 cells with a capacity to self-renew and that the self-renewal = ability=20 of the tumors correlated with the clinical aggressiveness of = the=20 different tumor phenotypes.


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  		Table 3 Self renewal capacity of = tumor=20 subtypes =

 = ;
To=20 evaluate proliferative capacity of tumor sphere cells, cells = were=20 plated at 1000 cells/well, and the number of viable cells was = quantified on days 0, 3, 5, and 7 after plating by the=20 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide=20 colorimetric assay. All of the tumor sphere cell populations = assayed=20 demonstrated increased proliferative capacity compared with = human=20 controls (Fig. 3A) . The histopathologic MIB-1 index is thought = to=20 correlate with tumor proliferation. The mean MIB-1 index of=20 medulloblastoma and pilocytic astrocytoma tumor specimens is = shown in=20 Fig. 3B . We suggest that the differing tumor stem = cell=20 proliferation rates are responsible for the MIB-1 indices = observed in=20 various tumor subtypes.



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  		Fig. 3. Tumor sphere cells = exhibit=20 increased proliferation consistent with histopathologic = tumor=20 mitotic indices. A, tumor stem cells from dissociated = medulloblastoma spheres (3D{circ}=20)=20 showed a greater degree of cell proliferation than pilocytic = astrocytoma spheres (3D{blacktriangleup}=20) or=20 control human neurospheres (3D{bullet}=20).=20 B, the higher degree of proliferation of the tumor = sphere=20 cell population is associated with an increased mitotic rate = of the=20 tumor as a whole, as reflected by mean MIB-1 values of each = tumor=20 subtype (medulloblastomas, 3D{circ}=20: mean=20 MIB-1 =3D 43.5% =B1 17.4, n =3D 7; pilocytic = astrocytoma, :=20 mean MIB-1 =3D 1.5% =B1 0.5, n =3D 3). =

 = ;
BTSCs=20 Differentiate to Produce a Phenotype Identical to the Tumor in=20 Situ.
We next applied conditions used for normal = neurosphere=20 differentiation to primary tumor spheres to determine whether = the=20 BTSC was capable of multilineage differentiation. After=20 differentiation with 10% FBS for 7 days, immunocytochemistry = was=20 performed on tumor stem cells using the following antibodies: = CD133,=20 nestin, =DF-tubulin 3 (=DF-tub-3; for neurons), GFAP (for = astrocytes),=20 and PDGFR-3D{alpha}=20 (for=20 oligodendrocytes). Immunocytochemistry was also performed on=20 undifferentiated primary tumor stem cells using the same = panel of=20 antibodies.

Undifferentiated tumor spheres from all of the tumor subtypes=20 exhibited immunoreactivity for CD133 and nestin, and lack of=20 immunoreactivity for markers of differentiated neural cell = types=20 such as GFAP for astrocytes and =DF-tubulin 3 for neurons = (Fig.=20 4, A=96D) . Strikingly, dissociated tumor spheres from = all of the=20 specimens grown adherently and in serum for 7 days = preferentially=20 differentiated down the lineage that characterized the = original tumor=20 phenotype of the patient (histopathology patient data not = shown).=20 Thus, the majority of differentiated cells from a primary=20 medulloblastoma sphere expressed =DF-tub-3 when = differentiated (81.9% =B1=20 SD 6.02), reflecting the neuronal marker expression commonly = seen in=20 medulloblastomas, whereas the majority of tumor stem cells = from=20 pilocytic astrocytomas expressed GFAP when differentiated = (77.9% =B1 SD=20 14.9), recapitulating the astrocytic lineage of the tumor = (Fig.=20 4, A=96D) . All of the tumor subtypes lost expression of = CD133=20 and nestin when subjected to differentiating conditions (Fig. = 4, A=96D) . Although a small minority of differentiated = cells=20 from each tumor subtype expressed other differentiated cell = markers,=20 the overwhelming majority of differentiated cells expressed = markers=20 that reflected the immunophenotype of the original tumor.=20 Interestingly, only medulloblastomas that expressed GFAP in = the=20 primary tumor (by immunohistochemistry) were able to express = GFAP=20 after tumor sphere differentiation in vitro, = illustrating the=20 striking in vitro recapitulation of tumor phenotype = within=20 tumors of the same histopathological subtype. In addition, 2=20 medulloblastoma specimens (Patients 2 and 4, 20.5% =B1 3.35)=20 demonstrated costaining for =DF-tub-3 and GFAP (Fig. 4 E, bottom panel), whereas the majority of=20 differentiated medulloblastoma tumor cells (60.3% =B1 SD = 3.55) in=20 these tumors stained for =DF-tub-3 alone (Fig. 4 E, top panel). Immunocytochemistry was = repeated=20 on these samples for another neuronal marker, = mitogen-activated=20 protein-2, and costaining with GFAP was again evident (data = not=20 shown). This differentiated tumor stem cell immunophenotype = may=20 represent a bipotential precursor cell, such as has been = identified=20 previously by Kilpatrick and Bartlett (14)=20 in normal neural precursor cells. These results show that the = BTSC=20 may re-establish the original tumor and demonstrate that = brain tumors=20 are heterogeneous and consist of a differentiating population = that=20 originates from a BTSC.



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  		Fig. 4. Tumor spheres = differentiate to=20 express immunophenotypes similar to the primary tumor.=20 Immunocytochemistry was performed on tumor stem cells using = CD133=20 (3D{square}=20),=20 nestin (), =DF-tubulin 3 (), GFAP (3D{blacksquare}=20),=20 and PDGFR-3D{alpha}=20 (). A=96D, all tumor spheres = lost expression=20 of CD133 and nestin when differentiated. Dissociated tumor = spheres=20 preferentially differentiated down the lineage that = characterized=20 the original tumor phenotype (A), pilocytic = astrocytoma=20 (specimen from Patient 9); (B), medulloblastoma = (specimen=20 from Patient 7). Tumor stem cells (77.9%) from pilocytic=20 astrocytomas expressed GFAP (A and C), whereas = 81.9%=20 of tumor stem cells from medulloblastomas expressed the = early=20 neuronal marker =DF-tubulin 3 (B and D) when=20 differentiated. E, whereas the majority of cells = within two=20 medulloblastoma cultures (patients 2 and 4) differentiated = into=20 cells with a neuronal immunophenotype (top panel,=20 magnification x200, = immunostaining=20 with =DF-tubulin-3), these cultures showed a small = population of cells=20 that costained for =DF-tubulin 3 and GFAP (bottom = panel,=20 magnification x400; GFAP = and=20 rhodamine in red, =DF-tubulin 3 and ALEXA 488 in = green). =

 = ;
CD133+=20 Tumor Cells Show Marked Stem Cell Activity.
To better define = the=20 BTSC, we needed a surface marker that would enable isolation. = CD133=20 is a novel 120 kDa five-transmembrane cell surface protein = originally=20 shown to be a hematopoietic stem cell marker, and found = recently to=20 be a marker of normal human neural stem cells (5=20 ,=20 12 ,=20 15) . We demonstrated CD133 expression by = immunohistochemistry in=20 brain tumors (Fig. 5 A, medulloblastoma, patient 1), = showing a plasma=20 membrane staining pattern also characterized in other = tissues. To=20 determine whether CD133 was present in tumor sphere cultures, = we=20 analyzed the expression of CD133 using flow cytometry, and we = sorted=20 for CD133 positive and negative cell populations using = magnetic=20 bead cell sorting.



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  		Fig. 5. CD133+ tumor cells show = marked=20 stem cell activity. A, immunohistochemistry for CD133 = shows a=20 plasma membrane staining pattern in scattered cells within a = medulloblastoma. BTSCs from both medulloblastomas and = pilocytic=20 astrocytomas were immunostained for CD133 and subjected to = flow=20 cytometry for quantification of CD133 expression (Table 3) , which varied widely in each tumor subtype. = B,=20 flow cytometry histogram in representative medulloblastoma = tumor=20 cells (from patient 6), with the first peak (gate M1) = representing=20 cells negative for CD133-phycoerythrin expression, and the = second=20 peak (gate M2) representing CD133 positive cells. Tumor = cells were=20 then sorted for CD133 expression by magnetic bead cell = sorting.=20 CD133+ and CD133- populations were collected, checked for = purity by=20 flow cytometry, and cultured separately in TSM for stem cell = assays.=20 Purity was found to range from 46.9 to 79.8% in CD133+ = populations,=20 and 92.6 to 97.3% in CD133- populations. C, CD133+ = tumor=20 cells proliferated in culture as nonadherent spheres, = whereas CD133-=20 tumor cells adhered to culture dishes, did not proliferate = and did=20 not form spheres. D, limiting dilution analysis = showed that=20 self-renewal capacity resides in the CD133+ tumor cell = population=20 (CD133+cells, 3D{blacktriangleup}=20;=20 unsorted tumor cells, 3D{bullet}=20;=20 CD133- cells, 3D{blacksquare}=20).=20 E, cell proliferation assays demonstrate that CD133+ = cells=20 (3D{blacktriangleup}=20)=20 possess marked proliferative capacity, whereas CD133- cells = do not=20 (3D{blacksquare}=20;=20 unsorted tumor cells, 3D{bullet}=20). =

 = ;
Flow=20 cytometric quantification of CD133 expression in brain tumor = cultures=20 ranged from 3.5% to 46.3% in both medulloblastomas and = pilocytic=20 astrocytomas (Table 4) . The lower-grade astrocytomas typically had = a lower=20 CD133 fraction compared with high-grade medulloblastomas. = When tumor=20 cell cultures were sorted for CD133 expression (Fig. = 5B) , CD133 positive and negative cell populations = were=20 collected and cultured separately, under the same conditions = as=20 unsorted BTSCs. Sorted CD133+ and CD133- aliquots from each = tumor=20 were checked by flow cytometry to evaluate the efficiency of = sorting:=20 purity of the CD133+ populations ranged from 46.9% to 79.8%, = and=20 purity of the CD133- populations ranged from 92.6% to 97.3%. = Over a=20 7-day culture period in SFM and growth factors, CD133+ tumor = cells=20 demonstrated growth as nonadherent tumor spheres, which = continued to=20 expand the cell population (Fig. 5 C, top panels). However, CD133- cells adhered to = the=20 culture dishes, did not proliferate, and did not form spheres = (Fig. 5 C, bottom panels).


View = this=20 table:
[in=20 this window]
[in a new window]
  		Table 4 CD133 expression of = brain tumor=20 stem cells =

 = ;
The=20 observed stem cell activity of CD133+ tumor cells was confirmed = when=20 CD133+ and CD133- tumor cells from 8 tumors (4 medulloblastomas, = 3=20 pilocytic astrocytomas, and 1 ganglioglioma) were plated at = limiting=20 dilutions (Fig. 5D) . These data show that the capacity for tumor = self-renewal resides in the CD133+ fraction, and that this = stem cell=20 property is absent in the CD133- tumor cell population. Cell=20 proliferation assays of tumor cells sorted for CD133 expression=20 demonstrate that CD133+ cells possess proliferative capacity, = whereas CD133- cells did not proliferate (Fig. 5E) . Thus, CD133 identifies an exclusive = subpopulation of=20 brain tumor cells that have neural stem cell activity. =

BTSC Cultures Exhibit Abnormal Karyotypes and Are Not = Migrating=20 Normal Neural Stem Cells.
Because normal stem cells can = migrate to=20 sites of injury, and brain tumor cultures may potentially be=20 contaminated with some normal neural stem cells, we conducted = appropriate cellular and genetic analyses to demonstrate that = the=20 BTSC we isolated was indeed transformed and are not normal = brain stem=20 cells.

Cellular analyses of medulloblastoma cultures sorted for CD133=20 expression reveal that neither CD133+ nor CD133- cell = differentiation=20 profiles resemble the differentiation profile of a normal = human=20 neural stem cell (Fig. 6, A and B) . Normal human neural stem cells demonstrate=20 multipotentiality by differentiating into characteristic = proportions=20 of astrocytes (50=9660%), neurons (20=9630%), and = oligodendrocytes=20 (5=9610%; Fig. 6C ). However, differentiated CD133+ cells that = harbor=20 stem cell activity and CD133- tumor cells sorted from a=20 medulloblastoma exhibit an abnormally high proportion of = cells=20 immunostaining for =DF-III tubulin (86.5% and 83.0%, = respectively),=20 resembling the original tumor rather than normal brain = phenotype=20 (Fig. 6, A and B) .



View = larger=20 version (51K):
[in=20 this window]
[in a new window]
  		Fig. 6. Unlike normal neural = stem cells,=20 the BTSC has undergone transformation. A, normal = human neural=20 stem cells differentiate into characteristic proportions of=20 astrocytes (GFAP, ), neurons (=DF-tubulin 3, 3D{blacksquare}=20) and=20 oligodendrocytes (PDGFR-3D{alpha}=20, ) reflecting the composition of normal = brain.=20 Immunostaining for CD133 (3D{square}=20)=20 and nestin () is characteristically lost after=20 differentiation. B and C, both differentiated = CD133+=20 (B) and CD133- (C) tumor cells sorted from a=20 medulloblastoma exhibit abnormally high proportions of cells = staining for =DF-tubulin 3 (3D{blacksquare}=20),=20 recapitulating the original tumor phenotype. Note that = CD133- cells=20 display minimal staining for undifferentiated cell markers = CD133=20 (3D{square}=20)=20 and nestin (). D, spectral karyotype = analysis performed=20 on tumor sphere cells isolated from a medulloblastoma shows = changes=20 typical of medulloblastoma, including loss of chromosomes 10 = and 16,=20 and gain of chromosome 18. =

 = ;
We=20 also performed cytogenetic analysis and SKY (8)=20 using metaphase preparations obtained directly from cultured = tumor=20 spheres from a medulloblastoma (Patient 7; Fig. 6D ). After dissociation of the primary tumor = and=20 formation of primary tumor spheres, medulloblastoma cells = were again=20 dissociated and metaphase spreads were prepared. Detailed SKY = analysis was possible in 8 metaphases, and all of the cells = had an=20 identical clonally abnormal karyotype. In all of the = metaphases the=20 consistent numerical alterations 45 XY, -10, -16, and +18 = were=20 present. Of these alterations, loss of chromosome 10 is one = of the=20 most characteristic findings in medulloblastoma (16=20 ,=20 17) . We also performed interphase fluorescent in = situ=20 hybridization on another medulloblastoma specimen (Patient = 14), from=20 which tumor cells underwent magnetic bead cell sorting for = CD133.=20 Unsorted tumor cells, CD133+ purified tumor stem cells, and = CD133-=20 cells were probed for centromere 17 and the p53 locus = on=20 chromosome 17p. All three cell populations (unsorted, CD133+, = and=20 CD133-) showed presence of isochromosome 17q (data not = shown). Taken=20 together, these cellular and genetic data demonstrate that = the=20 tumor-derived sphere cells possess an abnormal karyotype and = are not=20 contaminating normal neural stem cells. Rather, these cells = have=20 undergone a transformation event, incurring the enhanced = self-renewal=20 and proliferation properties we observed in = vitro.


3D"   =20 DISCUSSION
Top
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
3D"DISCUSSION
REFERENCES
 
S= tem cells=20 are functionally defined as self-renewing, multipotent cells = that=20 exhibit multilineage differentiation (18=20 ,=20 19) . Somatic stem cells are thought to self-renew to = generate=20 all of the mature cell types of a particular tissue through=20 differentiation, although rigorous identification and = isolation of=20 tissue-specific stem cells has been accomplished = prospectively in=20 only a few organ systems (2)=20 . The neurosphere assay has permitted rigorous in = vitro=20 characterization of the neural stem cell, but prospective = study of=20 this cell has been limited previously by lack of cell surface = markers=20 necessary for its isolation.

The potential that a neural stem cell may be transformed into = a=20 brain tumor has long been considered, but no prospective isolation = of=20 stem cells has been performed in brain tumors. Brain tumor = cells can=20 express the neural stem cell marker nestin (20=20 ,=20 21) , and brain tumors are comprised of cells expressing=20 phenotypes of more that one neural lineage. Microarray = analysis of=20 human medulloblastomas also suggests a similarity of gene=20 expression with normal developing brain cells (22)=20 . Recent experiments in mice also suggest that neural = progenitors may=20 be transformed into brain tumors. Mouse brain cells = expressing neural=20 progenitor markers are more receptive to oncogenic = transformation=20 than differentiated brain cells (23,=20 24,=20 25,=20 26)=20 . However, others suggest that a differentiated neural cell = is=20 equally permissive to transformation if it has a key genetic=20 alteration (27)=20 .

The concept of the cancer stem cell arose from the observation = of=20 striking similarities between the self-renewal mechanisms of = stem=20 cells and cancer cells (2)=20 . In malignancies such as leukemia (1)=20 , multiple myeloma (28)=20 , and most recently breast cancer (29)=20 , rare cells were isolated with a remarkable potential for=20 self-renewal, and these cells alone were found to drive the = formation=20 and growth of tumors. Because normal somatic stem cells must=20 self-renew and maintain a relative balance between = self-renewal and=20 differentiation, cancer can be contextualized as a disease of = unregulated self-renewal (2)=20 .

In this report, we have identified a new population of cancer = stem=20 cells in brain tumors of different phenotypes. These tumor = stem cells=20 represented a fraction of the total cells comprising the = tumor, and=20 they were identified by CD133 expression. There are three = pieces of=20 evidence that support that these cells are BTSCs: (a) = they=20 generate clusters of clonally derived cells resembling = neurospheres;=20 (b) they self-renew and proliferate; and (c) = they=20 differentiate to recapitulate the phenotype of the tumor from = which=20 they were derived.

The application of principles for study of normal neural stem=20 cells to brain tumor cell populations establishes a link = between=20 normal neurogenesis and brain tumorigenesis. Brain tumors are = not only phenotypically heterogeneous but are also = functionally=20 heterogeneous. Brain tumors exhibit phenotypic heterogeneity, = being composed of cells expressing both undifferentiated and=20 differentiated markers. Our data suggest that brain tumors = are=20 comprised of populations of proliferating tumor stem cells = that=20 are differentiating into the more mature cell types, which=20 characterize the tumor. Purification of CD133+ cells in brain = tumors=20 implies that a hierarchy may exist in the tumor cell = population,=20 because not all of the tumor cells were capable of = maintaining the=20 tumor in culture. This apparent hierarchy may be functionally = elucidated as more surface markers for neural stem cells = emerge and=20 additional tumor subpopulations are identified. The data = suggest that=20 the tumors originate from tumor cells that express CD133, as=20 this fraction exclusively had the ability to proliferate,=20 self-renew, and differentiate. Because normal neural stem = cells are=20 also found in the CD133 population of the normal human fetal=20 brain, it suggests that the cell of origin for a brain tumor = may=20 be a normal neural stem cell. Future investigations of the = BTSC=20 may lead to additional insight of this possibility, and may=20 clarify whether the BTSC sits at the top of a lineage = hierarchy,=20 or further down as a lineage-restricted progenitor.

We recall the principles that first defined the cellular = organization=20 of proliferative blast cells in leukemia to understand the=20 tumor-specific differentiation profile. Buick et al. = (30)=20 first proposed that malignant transformation might limit the=20 differentiation capacity of normal pluripotent stem cells and = cited=20 experimental support for this "blocked differentiation" model = in the=20 culture of bone marrow from leukemia patients. Moreover, if a = tumor=20 is viewed as an aberrant organ initiated by a cancer stem = cell (2)=20 , then the role of the tumor stem cell would be necessarily=20 lineage-restricted to generate only the mature cells that = comprise=20 the tumor. It is intriguing to speculate whether specific = growth=20 factors could force lineage-restricted tumor stem cells to=20 differentiate down a different pathway; for example, could a = neuronal=20 growth factor impose a neuronal fate on stem cells from a = pilocytic=20 astrocytoma? We do not believe that absence of multilineage=20 differentiation of the BTSC refutes that these cells are stem = cells,=20 because some cells differentiated into more than one lineage, = and=20 these cells uniquely had the ability to proliferate and=20 self-renew to generate differentiated progeny that comprise = the=20 tumor. The BTSCs from the different tumor phenotypes and = patient=20 samples demonstrated little variability in marker expression, = which was also expressed in normal neural stem cells. This=20 limited variation in marker phenotype for the BTSC for = different=20 tumors suggests that normal neural stem cells as opposed to=20 committed progenitors are the more likely targets of=20 transformation.

In this study, we provide new insight into the brain tumorigenic = process. With evidence of self-renewal, proliferation, and=20 lineage-restricted differentiation that recapitulates the = original=20 tumor phenotype, we define a class of BTSCs that can be = prospectively=20 isolated from many brain tumors. These cells grow as=20 neurosphere-like clusters and expressed neural stem cell = markers. We=20 also provide evidence to support the use of a novel stem cell = assay,=20 namely cell sorting for CD133 expression, for the = purification of=20 the BTSC from brain tumors. These findings support the=20 application of principles of leukemogenesis to solid tumors: = namely,=20 the principle that only a small subset of cancer stem cells = is=20 enriched for clonogenic capacity and that these cells alone = are=20 capable of tumor propagation.

The identification of the BTSC has important implications for=20 understanding the molecular mechanisms of brain = tumorigenesis,=20 as current molecular pathological analyses of global tumor = cell=20 populations (such as is performed in tumor microarray = experiments)=20 may not be sufficient to determine the key molecular = alterations=20 in rarer tumor stem cells. The presence of a BTSC will also=20 have important implications for understanding brain tumor=20 dissemination if these are the cells that migrate and = establish=20 central nervous system metastasis. The functional analysis of = the=20 BTSC may also provide a novel means for testing of new = treatment=20 strategies that focus on the eradication of the tumor = maintaining=20 BTSC. The fact that we are able to differentiate BTSCs into=20 cells that express more mature markers supports that = additional=20 exploration of the dynamic tumor differentiation process may = lead to=20 differentiation therapy. Finally, as it has been emerging = that normal=20 stem cells and cancer cells share similar phenotypic and = functional=20 properties, studies of stem cells found in brain tumors may = shed=20 additional light on the biology of normal neural stem = cells.=20


3D"   =20 ACKNOWLEDGMENTS
 
We = thank John Dick=20 for inspiration, mentorship, and guidance; Sean Egan for = invaluable=20 help and advice; Michael Ho, Gisele Knowles, Jane Bayani, and = Jana=20 Karaskova for expert technical assistance; and Todd Mainprize = and=20 Ajay Pandita for helpful discussions. We thank Dr. Wieland = Huttner=20 for antihuman prominin antibody. We also honor the late Larry = Becker=20 for his constant devotion to the principles of our work, and = his=20 inspired efforts on our behalf.


3D"   =20 FOOTNOTES
 
The costs of publication of this article were = defrayed=20 in part by the payment of page charges. This article must=20 therefore be hereby marked advertisement in accordance = with 18=20 U.S.C. Section 1734 solely to indicate this fact.

1 P. D. is supported by = National=20 Cancer Institute of Canada with funds from the Terry Fox Run, = the=20 Arthur and Sonia Labatt Brain Tumour Research Center, the = Hospital=20 for Sick Children Research Institute, and a gift from the = Baker=20 Family. S. S. is supported by a fellowship from the = Neurosurgery=20 Research and Education Foundation with Funds from the = American Brain=20 Tumour Association.

2 To whom requests for = reprints=20 should be addressed, at Hospital for Sick Children, 555 = University=20 Avenue, Toronto, Ontario, Canada, M5G 1X8. Phone: (416) = 813-6426;=20 Fax: (416) 813-4975; E-mail: peter.dirks{at}sickkids.ca

3 The abbreviations used = are: BTSC,=20 brain tumor stem cell; TSM, tumor sphere medium; EGF, = epidermal=20 growth factor; bFGF, basic fibroblast growth factor; FBS, = fetal=20 bovine serum; PDGFR, platelet-derived growth factor receptor; = SKY,=20 spectral karyotyping; SFM, serum-free medium; GFAP, glial = fibrillary=20 acidic protein.

Received 2/ 6/03. Revised 7/24/03. Accepted 7/29/03.


3D"   =20 REFERENCES
Top
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
3D"REFERENCES
&nb= sp;

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Side Population Cells = Isolated from=20 Mesenchymal Neoplasms Have Tumor Initiating = Potential
Cancer=20 Res., September 1, 2007; 67(17): 8216 - 8222.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
3D""=20=20 		3D""=20
3D""=20
 3D""=20 3D"Home
 3D""=20 3D"Stem3D"Home
U. Ganapati, H. T. Tan, M. Lynch, M. Dolezal, S. de Vos, = and J. C.=20 Gasson
Modeling Notch Signaling in Normal and = Neoplastic=20 Hematopoiesis: Global Gene Expression Profiling in Response to = Activated=20 Notch Expression
Stem Cells, August 1, 2007; = 25(8):=20 1872 - 1880.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
3D""=20=20 		3D""=20
3D""=20
 3D""=20 3D"Home
 3D""=20 3DGlycobiology=203D"Home
M. Yanagisawa and R. K Yu
The expression and = functions=20 of glycoconjugates in neural stem cells
Glycobiology,=20 July 1, 2007; 17(7): 57R - 74R.
[= Abstract]=20 [Full= =20 Text] [PDF] =
3D""=20=20 		3D""=20
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 3D""=20 3D"Stem3D"Home
A. J. Ghods, D. Irvin, G. Liu, X. Yuan, I. R. = Abdulkadir, P.=20 Tunici, B. Konda, S. Wachsmann-Hogiu, K. L. Black, and J. S.=20 Yu
Spheres Isolated from 9L Gliosarcoma Rat Cell Line = Possess=20 Chemoresistant and Aggressive Cancer Stem-Like = Cells
Stem=20 Cells, July 1, 2007; 25(7): 1645 - 1653.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
3D""=20=20 		3D""=20
3D""=20
 3D""=20 3D"Home
 3D""=20 3D"Cancer3D"Home
C. V. Pfenninger, T. Roschupkina, F. Hertwig, D. = Kottwitz, E.=20 Englund, J. Bengzon, S. E. Jacobsen, and U. A. = Nuber
CD133 Is=20 Not Present on Neurogenic Astrocytes in the Adult Subventricular = Zone, but=20 on Embryonic Neural Stem Cells, Ependymal Cells, and Glioblastoma=20 Cells
Cancer Res., June 15, 2007; 67(12): = 5727 -=20 5736.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Cancer3D"Home
D. Beier, P. Hau, M. Proescholdt, A. Lohmeier, J. = Wischhusen, P.=20 J. Oefner, L. Aigner, A. Brawanski, U. Bogdahn, and C. P.=20 Beier
CD133+ and CD133- Glioblastoma-Derived Cancer = Stem Cells=20 Show Differential Growth Characteristics and Molecular=20 Profiles
Cancer Res., May 1, 2007; 67(9): = 4010 -=20 4015.
[Abstract]=20 [Fu= ll=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Hum3D"Home
K. Kato, M. Yoshimoto, K. Kato, S. Adachi, A. Yamayoshi, = T. Arima,=20 K. Asanoma, S. Kyo, T. Nakahata, and N. = Wake
Characterization=20 of side-population cells in human normal = endometrium
Hum.=20 Reprod., May 1, 2007; 22(5): 1214 - 1223.
= [Abstract]=20 [Ful= l=20 Text] [PDF]= =20
3D""=20=20 		3D""=20
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 3D""=20 3D"Home
 3D""=20 3D"Cancer3D"Home
C. Folkins, S. Man, P. Xu, Y. Shaked, D. J. Hicklin, and = R. S.=20 Kerbel
Anticancer Therapies Combining Antiangiogenic = and Tumor=20 Cell Cytotoxic Effects Reduce the Tumor Stem-Like Cell Fraction in = Glioma=20 Xenograft Tumors
Cancer Res., = April 15, 2007; 67(8):=20 3560 - 3564.
[Abstract]=20 [Fu= ll=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Cancer3D"Home
X. Zheng, G. Shen, X. Yang, and W. Liu
Most = C6 Cells=20 Are Cancer Stem Cells: Evidence from Clonal and Population=20 Analyses
Cancer Res., April 15, 2007; 67(8): = 3691 -=20 3697.
[Abstract]=20 [Fu= ll=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Cancer3D"Home
J. Wang, L.-P. Guo, L.-Z. Chen, Y.-X. Zeng, and S. H.=20 Lu
Identification of Cancer Stem Cell-Like Side = Population=20 Cells in Human Nasopharyngeal Carcinoma Cell = Line
Cancer Res.,=20 April 15, 2007; 67(8): 3716 - 3724.
[Abstract]=20 [Fu= ll=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Cancer3D"Home
C. Foroni, R. Galli, B. Cipelletti, A. Caumo, S. = Alberti, R.=20 Fiocco, and A. Vescovi
Resilience to Transformation and = Inherent Genetic and Functional Stability of Adult Neural Stem = Cells Ex=20 vivo
Cancer Res., April 15, 2007; 67(8): = 3725 -=20 3733.
[Abstract]=20 [Fu= ll=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Home
D. Faury, A. Nantel, S. E. Dunn, M.-C. Guiot, T. Haque, = P. Hauser,=20 M. Garami, L. Bognar, Z. Hanzely, P. P. Liberski, et=20 al.
Molecular Profiling Identifies Prognostic = Subgroups of=20 Pediatric Glioblastoma and Shows Increased YB-1 Expression in=20 Tumors
J. Clin. Oncol., April 1, 2007; = 25(10): 1196=20 - 1208.
[Abstrac= t]=20 [Full=20 Text] [PDF] =
3D""=20
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 3D""=20 3DEndocrinology=203D"Home
N. Mitsutake, A. Iwao, K. Nagai, H. Namba, A. Ohtsuru, = V. Saenko,=20 and S. Yamashita
Characterization of Side Population in = Thyroid=20 Cancer Cell Lines: Cancer Stem-Like Cells Are Enriched Partly But = Not=20 Exclusively
Endocrinology, April 1, 2007; = 148(4):=20 1797 - 1803.
[Ab= stract]=20 [Full=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Am.3D"Home
A. Giangreco, K. R. Groot, and S. M. = Janes
Lung Cancer=20 and Lung Stem Cells: Strange Bedfellows?
Am. J. = Respir. Crit.=20 Care Med., March 15, 2007; 175(6): 547 - 553.
[Abstract]<= /A>=20 [Full = Text]=20 [PDF] =
3D""=20
3D""=20
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 3D""=20 3D"Home
T. Aguado, A. Carracedo, B. Julien, G. Velasco, G. = Milman, R.=20 Mechoulam, L. Alvarez, M. Guzman, and I.=20 Galve-Roperh
Cannabinoids Induce Glioma Stem-like Cell=20 Differentiation and Inhibit Gliomagenesis
J. Biol. = Chem.,=20 March 2, 2007; 282(9): 6854 - 6862.
[Abstract]=20 [Full = Text]=20 [PDF] =
3D""=20
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 3D""=20 3D"Stem3D"Home
F. F. Costa, K. Le Blanc, and B. = Brodin
Concise Review:=20 Cancer/Testis Antigens, Stem Cells, and Cancer
Stem = Cells,=20 March 1, 2007; 25(3): 707 - 711.
[Abstract]=20 [Fu= ll=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"The3D"Home
K. Ishikawa, A. Sasaki, N. Haraguchi, Y. Yoshikawa, and = M.=20 Mori
A Case of an {alpha}-Fetoprotein-Producing = Intrahepatic=20 Cholangiocarcinoma Suggests Probable Cancer Stem Cell=20 Origin
Oncologist, March 1, 2007; 12(3): 320 = - 324.=20
[Abstract]=20 [Full=20 Text] [PDF= ]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Cancer3D"Home
C. Li, D. G. Heidt, P. Dalerba, C. F. Burant, L. Zhang, = V. Adsay,=20 M. Wicha, M. F. Clarke, and D. M. = Simeone
Identification of=20 Pancreatic Cancer Stem Cells
Cancer Res.,=20 February 1, 2007; 67(3): 1030 - 1037.
[Abstract]=20 [Fu= ll=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Home
M. E. Prince, R. Sivanandan, A. Kaczorowski, G. T. Wolf, = M. J.=20 Kaplan, P. 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] =
3D""=20
3D""=20
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 3D""=20 3D"JNCI3D"Home
T. M. Phillips, W. H. McBride, and F. = Pajonk
The=20 Response of CD24-/low/CD44+ Breast Cancer-Initiating Cells to=20 Radiation
J Natl Cancer Inst, = December 20, 2006;=20 98(24): 1777 - 1785.
[= Abstract]=20 [Full= =20 Text] [PDF] =
3D""=20=20 		3D""=20
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 3D""=20 3D"Home
S. Bruno, B. Bussolati, C. Grange, F. Collino, M. E. = Graziano, U.=20 Ferrando, and G. Camussi
CD133+ Renal Progenitor Cells=20 Contribute to Tumor Angiogenesis
Am. J. Pathol.,=20 December 1, 2006; 169(6): 2223 - 2235.
[Abstra= ct]=20 [Full=20 Text] [PDF] =
3D""=20
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 3D""=20 3D"Clin.3D"Home
K. Tateishi, M. Ohta, F. Kanai, B. Guleng, Y. Tanaka, Y. = Asaoka,=20 M. Tada, M. Seto, A. Jazag, L. Lianjie, et=20 al.
Dysregulated Expression of Stem Cell Factor = Bmi1 in=20 Precancerous Lesions of the Gastrointestinal = Tract
Clin.=20 Cancer Res., December 1, 2006; 12(23): 6960 - 6966. =
[Abstract]=20 [Full=20 Text] [PD= F]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Stem3D"Home
K. 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
3D""=20=20 		3D""=20
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 3D""=20 3DBlood=203D"Home
J. A. Kruger, C. D. Kaplan, Y. Luo, H. Zhou, D. = Markowitz, R.=20 Xiang, and R. A. Reisfeld
Characterization of stem = cell-like=20 cancer cells in immune-competent mice
Blood,=20 December 1, 2006; 108(12): 3906 - 3912.
[Abstract]=20 [Full=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Home
F. J. Sim, H. M. Keyoung, J. E. Goldman, D. K. Kim, = H.-W. Jung, N.=20 S. Roy, and S. A. Goldman
Neurocytoma Is a Tumor of = Adult=20 Neuronal Progenitor Cells
J. Neurosci.,=20 November 29, 2006; 26(48): 12544 - 12555.
[Abstr= act]=20 [Full=20 Text] [PDF] =
3D""=20
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 3D""=20 3D"Home
S. Horvath, B. Zhang, M. Carlson, K. V. Lu, S. Zhu, R. = M.=20 Felciano, M. F. Laurance, W. Zhao, S. Qi, Z. Chen, et=20 al.
Analysis of oncogenic signaling networks in=20 glioblastoma identifies ASPM as a molecular = target
PNAS,=20 November 14, 2006; 103(46): 17402 - 17407.
[Abstract]= =20 [Full=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Ann3D"Home
C Massard, E Deutsch, and J-C Soria
Tumour = stem=20 cell-targeted treatment: elimination or = differentiation
Ann.=20 Onc., November 1, 2006; 17(11): 1620 - 1624.
[Abstract]=20 [Fu= ll=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Stem3D"Home
M. Mimeault and S. K. Batra
Concise Review: = Recent=20 Advances on the Significance of Stem Cells in Tissue Regeneration = and=20 Cancer Therapies
Stem Cells, = November 1, 2006;=20 24(11): 2319 - 2345.
[Abstract]=20 [= Full=20 Text] [PDF]<= /A>=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Home
P. O. Sakariassen, L. Prestegarden, J. Wang, K.-O. = Skaftnesmo, R.=20 Mahesparan, C. Molthoff, P. Sminia, E. Sundlisaeter, A. Misra, B. = B.=20 Tysnes, et al.
Angiogenesis-independent tumor = growth=20 mediated by stem-like cancer cells
PNAS,=20 October 31, 2006; 103(44): 16466 - 16471.
[Abstract]= =20 [Full=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Home
J. Pogoriler, K. Millen, M. Utset, and W. = Du
Loss of=20 cyclin D1 impairs cerebellar development and suppresses = medulloblastoma=20 formation
Development, October 1, 2006; = 133(19):=20 3929 - 3937.
[Abst= ract]=20 [Full=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Home
C. T. Jordan, M. L. Guzman, and M. = Noble
Cancer stem=20 cells.
N. Engl. J. Med., September 21, 2006; = 355(12): 1253 - 1261.
[Full=20 Text] [PDF] =
3D""=20
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 3D""=20 3D"Cancer3D"Home
L. Balenci, I. D. Clarke, P. B. Dirks, N. Assard, F. = Ducray, A.=20 Jouvet, M.-F. Belin, J. Honnorat, and J. Baudier
IQGAP1 = Protein=20 Specifies Amplifying Cancer Cells in Glioblastoma=20 Multiforme.
Cancer Res., September 15, 2006; = 66(18):=20 9074 - 9082.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Cancer3D"Home
S. Bao, Q. Wu, S. Sathornsumetee, Y. Hao, Z. Li, A. B. = Hjelmeland,=20 Q. Shi, R. E. McLendon, D. D. Bigner, and J. N. = Rich
Stem=20 Cell-like Glioma Cells Promote Tumor Angiogenesis through Vascular = Endothelial Growth Factor
Cancer Res.,=20 August 15, 2006; 66(16): 7843 - 7848.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Cancer3D"Home
A. Erlandsson, K. Brannvall, S. Gustafsdottir, B. = Westermark, and=20 K. 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
3D""=20=20 		3D""=20
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 3D""=20 3D"Clin.3D"Home
N. Mehra, M. Penning, J. Maas, L. V. Beerepoot, N. van = Daal, C. H.=20 van Gils, R. H. Giles, and E. E. Voest
Progenitor = Marker CD133=20 mRNA Is Elevated in Peripheral Blood of Cancer Patients with Bone=20 Metastases.
Clin. Cancer Res., = August 15, 2006;=20 12(16): 4859 - 4866.
[Abstract]=20 [Full=20 Text] [PD= F]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Cancer3D"Home
X. Fan, W. Matsui, L. Khaki, D. Stearns, J. Chun, Y.-M. = Li, and C.=20 G. Eberhart
Notch Pathway Inhibition Depletes Stem-like = Cells=20 and 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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 3D""=20 3D"Home
M. Assanah, R. Lochhead, A. Ogden, J. Bruce, J. Goldman, = and P.=20 Canoll
Glial progenitors in adult white matter are = driven to=20 form malignant gliomas by platelet-derived growth = factor-expressing=20 retroviruses.
J. Neurosci., June 21, 2006; = 26(25):=20 6781 - 6790.
[Abstra= ct]=20 [Full=20 Text] [PDF] =
3D""=20
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 3D""=20 3D"Cancer3D"Home
S. Liu, G. Dontu, I. D. Mantle, S. Patel, N.-s. Ahn, K. = W.=20 Jackson, P. Suri, and M. S. Wicha
Hedgehog Signaling = and Bmi-1=20 Regulate Self-renewal of Normal and Malignant Human Mammary Stem=20 Cells.
Cancer Res., June 15, 2006; 66(12): = 6063 -=20 6071.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Home
A. Y. Khakoo, S. Pati, S. A. Anderson, W. Reid, M. F. = Elshal, I.=20 I. Rovira, A. T. Nguyen, D. Malide, C. A. Combs, G. Hall, et=20 al.
Human mesenchymal stem cells exert potent=20 antitumorigenic effects in a model of Kaposi's = sarcoma
J. Exp.=20 Med., May 15, 2006; 203(5): 1235 - 1247.
[Abstract]=20 [Full = Text]=20 [PDF] =
3D""=20
3D""=20
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 3D""=20 3D"Stem3D"Home
M. Miura, Y. Miura, H. M. Padilla-Nash, A. A. Molinolo, = B. Fu, V.=20 Patel, B.-M. Seo, W. Sonoyama, J. J. Zheng, C. C. Baker, et=20 al.
Accumulated Chromosomal Instability in Murine = Bone=20 Marrow Mesenchymal Stem Cells Leads to Malignant=20 Transformation
Stem Cells, April 1, 2006; = 24(4):=20 1095 - 1103.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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D. A. Reardon, J. N. Rich, H. S. Friedman, and D. D.=20 Bigner
Recent Advances in the Treatment of Malignant=20 Astrocytoma
J. Clin. Oncol., March 10, 2006; = 24(8):=20 1253 - 1265.
[Abstract= ]=20 [Full=20 Text] [PDF] =
3D""=20
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 3D""=20 3D"Cancer3D"Home
H. B. Frieboes, X. Zheng, C.-H. Sun, B. Tromberg, R. = Gatenby, and=20 V. Cristini
An Integrated Computational/Experimental = Model of=20 Tumor Invasion
Cancer Res., = February 1, 2006; 66(3):=20 1597 - 1604.
[Abstract]=20 [Fu= ll=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3DBlood=203D"Home
C. A. Huff, W. Matsui, B. D. Smith, and R. J. = Jones
The=20 paradox of response and survival in cancer = therapeutics
Blood,=20 January 15, 2006; 107(2): 431 - 434.
[Abstract]=20 [Full=20 Text] = [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Home
 3D""=20 3D"Cancer3D"Home
A. T. Collins, P. A. Berry, C. Hyde, M. J. Stower, and = N. J.=20 Maitland
Prospective Identification of Tumorigenic = Prostate=20 Cancer Stem Cells
Cancer Res., = December 1, 2005;=20 65(23): 10946 - 10951.
[Abstract]=20 [= Full=20 Text] [PDF]<= /A>=20
3D""=20=20 		3D""=20
3D""=20
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 3D""=20 3D"Home
J. D. Dougherty, A. D. R. Garcia, I. Nakano, M. = Livingstone, B.=20 Norris, R. Polakiewicz, E. M. Wexler, M. V. Sofroniew, H. I. = Kornblum, and=20 D. H. Geschwind
PBK/TOPK, a Proliferating Neural=20 Progenitor-Specific Mitogen-Activated Protein Kinase = Kinase
J.=20 Neurosci., November 16, 2005; 25(46): 10773 - 10785. =
[Abstr= act]=20 [Full=20 Text] [PDF] =
3D""=20
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 3D""=20 3D"Cancer3D"Home
D. Fang, T. K. Nguyen, K. Leishear, R. Finko, A. N. = Kulp, S. Hotz,=20 P. A. Van Belle, X. Xu, D. E. Elder, and M. Herlyn
A=20 Tumorigenic Subpopulation with Stem Cell Properties in=20 Melanomas
Cancer Res., October 15, 2005; = 65(20):=20 9328 - 9337.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Cancer3D"Home
M. Locke, M. Heywood, S. Fawell, and I. C.=20 Mackenzie
Retention of Intrinsic Stem Cell Hierarchies = in=20 Carcinoma-Derived Cell Lines
Cancer Res.,=20 October 1, 2005; 65(19): 8944 - 8950.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Stem3D"Home
A. Toren, B. Bielorai, J. Jacob-Hirsch, T. Fisher, D. = Kreiser, O.=20 Moran, S. Zeligson, D. Givol, A. Yitzhaky, J. Itskovitz-Eldor, = et=20 al.
CD133-Positive Hematopoietic Stem Cell = "Stemness"=20 Genes Contain Many Genes Mutated or Abnormally Expressed in=20 Leukemia
Stem Cells, September 1, 2005; = 23(8): 1142=20 - 1153.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3DBlood=203D"Home
F. Rosenbauer, S. Koschmieder, U. Steidl, and D. G.=20 Tenen
Effect of transcription-factor concentrations on = leukemic=20 stem cells
Blood, September 1, 2005; 106(5): = 1519 -=20 1524.
[Abstract]=20 [Full=20 Text] [PDF]=20
3D""=20=20 		3D""=20
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 3D""=20 3D"Home
N. Sanai, A. Alvarez-Buylla, and M. S. = Berger
Neural=20 Stem Cells and the Origin of Gliomas
N. Engl. J. Med., = August 25, 2005; 353(8): 811 - 822.
[Full = Text]=20 [PDF] =
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 3D""=20 3D"Home
W. A. Woodward, M. S. Chen, F. Behbod, and J. M.=20 Rosen
On mammary stem cells
J. Cell Sci.,=20 August 15, 2005; 118(16): 3585 - 3594.
[Abst= ract]=20 [Full=20 Text] [PDF]=20
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 3D""=20 3D"Clin.3D"Home
S.-K. Kim, T. G. Cargioli, M. Machluf, W. Yang, Y. Sun, = R.=20 Al-Hashem, S. U. Kim, P. M. Black, and R. S.=20 Carroll
PEX-Producing Human Neural Stem Cells Inhibit = Tumor=20 Growth in a Mouse Glioma Model
Clin. Cancer Res.,=20 August 15, 2005; 11(16): 5965 - 5970.
[Abstract]=20 [Full=20 Text] [PD= F]=20
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L. Patrawala, T. Calhoun, R. Schneider-Broussard, J. = Zhou, K.=20 Claypool, and D. G. Tang
Side Population Is Enriched in = Tumorigenic, Stem-Like Cancer Cells, whereas ABCG2+ and ABCG2- = Cancer=20 Cells Are Similarly Tumorigenic
Cancer Res.,=20 July 15, 2005; 65(14): 6207 - 6219.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
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D. Ponti, A. Costa, N. Zaffaroni, G. Pratesi, G. = Petrangolini, D.=20 Coradini, S. Pilotti, M. A. Pierotti, and M. G.=20 Daidone
Isolation and In vitro Propagation of = Tumorigenic=20 Breast Cancer Cells with Stem/Progenitor Cell=20 Properties
Cancer Res., July 1, 2005; = 65(13): 5506 -=20 5511.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
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B. M. Deasy, B. M. Gharaibeh, J. B. Pollett, M. M. = Jones, M. A.=20 Lucas, Y. Kanda, and J. Huard
Long-Term Self-Renewal of = Postnatal Muscle-derived Stem Cells
Mol. Biol. Cell,=20 July 1, 2005; 16(7): 3323 - 3333.
[Abstr= act]=20 [Full=20 Text] [PDF] =
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B. Dasgupta and D. H. Gutmann
Neurofibromin = Regulates=20 Neural Stem Cell Proliferation, Survival, and Astroglial = Differentiation=20 In Vitro and In Vivo
J. Neurosci., = June 8, 2005;=20 25(23): 5584 - 5594.
[Abstra= ct]=20 [Full=20 Text] [PDF] =
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J. G. Toma, I. A. McKenzie, D. Bagli, and F. D.=20 Miller
Isolation and Characterization of Multipotent=20 Skin-Derived Precursors from Human Skin
Stem Cells,=20 June 1, 2005; 23(6): 727 - 737.
[Abstract]=20 [Fu= ll=20 Text] [PDF]=20
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T. G. Oliver, T. A. Read, J. D. Kessler, A. Mehmeti, J. = F. Wells,=20 T. T. T. Huynh, S. M. Lin, and R. J. Wechsler-Reya
Loss = of=20 patched and disruption of granule cell development in a = pre-neoplastic=20 stage of medulloblastoma
Development, = May 15, 2005;=20 132(10): 2425 - 2439.
[Abst= ract]=20 [Full=20 Text] [PDF]=20
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S. A. Bapat, A. M. Mali, C. B. Koppikar, and N. K.=20 Kurrey
Stem and Progenitor-Like Cells Contribute to the = Aggressive Behavior of Human Epithelial Ovarian = Cancer
Cancer=20 Res., April 15, 2005; 65(8): 3025 - 3029.
[Abstract]=20 [Fu= ll=20 Text] [PDF]=20
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 3D""=20 3DCarcinogenesis=203D"Home
F. Behbod and J. M. Rosen
Will cancer stem = cells=20 provide new therapeutic targets?
Carcinogenesis,=20 April 1, 2005; 26(4): 703 - 711.
[= Abstract]=20 [Full= =20 Text] [PDF] =
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G. Cronwright, K. Le Blanc, C. Gotherstrom, P. Darcy, M. = Ehnman,=20 and B. Brodin
Cancer/Testis Antigen Expression in Human = Mesenchymal Stem Cells: Down-regulation of SSX Impairs Cell = Migration and=20 Matrix Metalloproteinase 2 Expression
Cancer Res.,=20 March 15, 2005; 65(6): 2207 - 2215.
[Abstract]=20 [Fu= ll=20 Text] [PDF]=20
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R. Glass, M. Synowitz, G. Kronenberg, J.-H. Walzlein, D. = S.=20 Markovic, L.-P. 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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M.-H. Tai, C.-C. Chang, L.K. Olson, and J. E.=20 Trosko
Oct4 expression in adult human stem cells: = evidence in=20 support of the stem cell theory of=20 carcinogenesis
Carcinogenesis, = February 1, 2005;=20 26(2): 495 - 502.
[= Abstract]=20 [Full= =20 Text] [PDF] =
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 3D""=20 3D"Clin.3D"Home
B. K. Abraham, P. Fritz, M. McClellan, P. Hauptvogel, M. = Athelogou, and H. Brauch
Prevalence of CD44+/CD24-/low = Cells in=20 Breast Cancer May Not Be Associated with Clinical Outcome but May = Favor=20 Distant Metastasis
Clin. Cancer Res.,=20 February 1, 2005; 11(3): 1154 - 1159.
[Abstract]=20 [Full=20 Text] [PDF= ]=20
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X. Fan, I. Mikolaenko, I. Elhassan, X. Ni, Y. Wang, D. = Ball, D. J.=20 Brat, A. Perry, and C. G. Eberhart
Notch1 and Notch2 = Have=20 Opposite 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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 3D""=20 3D"Cancer3D"Home
R. Galli, E. Binda, U. Orfanelli, B. Cipelletti, A. = Gritti, S. De=20 Vitis, R. Fiocco, C. Foroni, F. Dimeco, and A.=20 Vescovi
Isolation and Characterization of Tumorigenic,=20 Stem-like Neural Precursors from Human = Glioblastoma
Cancer=20 Res., October 1, 2004; 64(19): 7011 - 7021.
[Abstract]=20 [F= ull=20 Text] [PDF]=20
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A. T. Kho, Q. Zhao, Z. Cai, A. J. Butte, J. Y.H. Kim, S. = L.=20 Pomeroy, D. H. Rowitch, and I. S. Kohane
Conserved = mechanisms=20 across development and tumorigenesis revealed by a mouse = development=20 perspective of human cancers
Genes & Dev.,=20 March 15, 2004; 18(6): 629 - 640.
[Abstract]= =20 [Full=20 Text] [PDF]=20
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L.-X. Wang, J. Kjaergaard, P. A. Cohen, S. Shu, and G. = E.=20 Plautz
Memory T Cells Originate from Adoptively = Transferred=20 Effectors and Reconstituting Host Cells after Sequential = Lymphodepletion=20 and Adoptive Immunotherapy
J. Immunol.,=20 March 15, 2004; 172(6): 3462 - 3468.
[Abstrac= t]=20 [Full=20 Text] [PDF] =
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H. D. Hemmati, I. Nakano, J. A. Lazareff, M. = Masterman-Smith, D.=20 H. Geschwind, M. Bronner-Fraser, and H. I. = Kornblum
Cancerous=20 stem cells can arise from pediatric brain tumors
PNAS, = December 9, 2003; 100(25): 15178 - 15183.
[Abstract]= =20 [Full=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; 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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_01C856A0.287EBDD0 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://cancerres.aacrjournals.org/javascript/ajax/utility.js /************************************************************************= *****=0A= * javascript/ajax/utility.js=0A= *=0A= * Utility functions for working with XMLHttpRequest data.=0A= *=0A= * Copyright 2006 Board of Trustees of the Leland Stanford Junior = University.=0A= = *************************************************************************= ***/=0A= =0A= /*=0A= * Copy XML nodes into an HTMLElement. This effectively=0A= * clones XML markup which uses XHTML naming conventions=0A= * into an HTML DOM.=0A= */=0A= function copy_xml_to_html(src, dst) {=0A= if (src.nodeType =3D=3D 1) { /* Node.ELEMENT_NODE */=0A= var e =3D document.createElement(src.nodeName);=0A= for (var i =3D 0; i < src.childNodes.length; i++) {=0A= copy_xml_to_html(src.childNodes[i], e);=0A= }=0A= for (var i =3D 0; i < src.attributes.length; i++) {=0A= var n =3D src.attributes[i].name;=0A= var v =3D unescape_xml_string(src.attributes[i].value); =0A= e.setAttribute(n, v);=0A= if (n =3D=3D "class") {=0A= e.className =3D v;=0A= }=0A= else if (n =3D=3D "style") {=0A= set_css_style(v, e, "");=0A= }=0A= }=0A= dst.appendChild(e);=0A= }=0A= else if (src.nodeType =3D=3D 3) { /* Node.TEXT_NODE */=0A= dst.appendChild(document.createTextNode(src.nodeValue));=0A= }=0A= }=0A= =0A= /* =0A= * It is unclear that this is the right thing to be calling=0A= * from copy_xml_to_html, but it appears that Safari decides=0A= * to convert & to the NCR #, and then encodes that=0A= * NCR to &%26%2338;. So, I'm going to treat the DOM Attr=0A= * value as a plain string, and run our XML string input=0A= * through the decoding routine below.=0A= */=0A= function unescape_xml_string(s) {=0A= return s.replace(/'/g, "'")=0A= .replace(/'/g, "'")=0A= .replace(/"/g, "\"")=0A= .replace(/"/g, "\"")=0A= .replace(/>/g, ">")=0A= .replace(/>/g, ">")=0A= .replace(/</g, "<")=0A= .replace(/</g, "<")=0A= .replace(/&/g, "&")=0A= .replace(/&/g, "&");=0A= }=0A= =0A= /*=0A= * Parse set of CSS rules and apply them to an element.=0A= * This is quite horrifying, but I'm unable to determine=0A= * how else to handle this with IE 6. FireFox and other=0A= * sane browsers let you simply set the style attribute=0A= * or use e.style.setProperty(rule, value, priority),=0A= * IE 6 appears to have neither of these capabilities..=0A= */=0A= function set_css_style(css, e, priority) {=0A= var rules =3D css.split(";");=0A= for (var i =3D 0; i < rules.length; i++) {=0A= var nvpair =3D rules[i].split(":");=0A= if (nvpair.length =3D=3D 2) {=0A= try {=0A= var name =3D nvpair[0]; /* style attribute */=0A= var value =3D nvpair[1]; /* attribute value */=0A= =0A= /*=0A= * For each possible style attribute, set the=0A= * appropriate style property in the element.=0A= */=0A= if (name =3D=3D "background") {=0A= e.style.background =3D value;=0A= }=0A= else if (name =3D=3D "background-attachment") {=0A= e.style.backgroundAttachment =3D value;=0A= }=0A= else if (name =3D=3D "background-color") {=0A= e.style.backgroundColor =3D value;=0A= }=0A= else if (name =3D=3D "background-image") {=0A= e.style.backgroundImage =3D value;=0A= }=0A= else if (name =3D=3D "background-position") {=0A= e.style.backgroundPosition =3D value;=0A= }=0A= else if (name =3D=3D "background-position-x") {=0A= e.style.backgroundPositionX =3D value;=0A= }=0A= else if (name =3D=3D "background-position-y") {=0A= e.style.backgroundPositionY =3D value;=0A= }=0A= else if (name =3D=3D "background-repeat") {=0A= e.style.backgroundRepeat =3D value;=0A= }=0A= else if (name =3D=3D "behavior") {=0A= e.style.behavior =3D value;=0A= }=0A= else if (name =3D=3D "border") {=0A= e.style.border =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom") {=0A= e.style.borderBottom =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-color") {=0A= e.style.borderBottomColor =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-style") {=0A= e.style.borderBottomStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-width") {=0A= e.style.borderBottomWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-collapse") {=0A= e.style.borderCollapse =3D value;=0A= }=0A= else if (name =3D=3D "border-color") {=0A= e.style.borderColor =3D value;=0A= }=0A= else if (name =3D=3D "border-left") {=0A= e.style.borderLeft =3D value;=0A= }=0A= else if (name =3D=3D "border-left-color") {=0A= e.style.borderLeftColor =3D value;=0A= }=0A= else if (name =3D=3D "border-left-style") {=0A= e.style.borderLeftStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-left-width") {=0A= e.style.borderLeftWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-right") {=0A= e.style.borderRight =3D value;=0A= }=0A= else if (name =3D=3D "border-right-color") {=0A= e.style.borderRightColor =3D value;=0A= }=0A= else if (name =3D=3D "border-right-style") {=0A= e.style.borderRightStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-right-width") {=0A= e.style.borderRightWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-style") {=0A= e.style.borderStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-top") {=0A= e.style.borderTop =3D value;=0A= }=0A= else if (name =3D=3D "border-top-color") {=0A= e.style.borderTopColor =3D value;=0A= }=0A= else if (name =3D=3D "border-top-style") {=0A= e.style.borderTopStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-top-width") {=0A= e.style.borderTopWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-width") {=0A= e.style.borderWidth =3D value;=0A= }=0A= else if (name =3D=3D "bottom") {=0A= e.style.bottom =3D value;=0A= }=0A= else if (name =3D=3D "clear") {=0A= e.style.clear =3D value;=0A= }=0A= else if (name =3D=3D "clip") {=0A= e.style.clip =3D value;=0A= }=0A= else if (name =3D=3D "color") {=0A= e.style.color =3D value;=0A= }=0A= else if (name =3D=3D "cssText") {=0A= e.style.Sets =3D value;=0A= }=0A= else if (name =3D=3D "cursor") {=0A= e.style.cursor =3D value;=0A= }=0A= else if (name =3D=3D "direction") {=0A= e.style.direction =3D value;=0A= }=0A= else if (name =3D=3D "display") {=0A= e.style.display =3D value;=0A= }=0A= else if (name =3D=3D "font") {=0A= e.style.font =3D value;=0A= }=0A= else if (name =3D=3D "font-family") {=0A= e.style.fontFamily =3D value;=0A= }=0A= else if (name =3D=3D "font-size") {=0A= e.style.fontSize =3D value;=0A= }=0A= else if (name =3D=3D "font-style") {=0A= e.style.fontStyle =3D value;=0A= }=0A= else if (name =3D=3D "font-variant") {=0A= e.style.fontVariant =3D value;=0A= }=0A= else if (name =3D=3D "font-weight") {=0A= e.style.fontWeight =3D value;=0A= }=0A= else if (name =3D=3D "height") {=0A= e.style.height =3D value;=0A= }=0A= else if (name =3D=3D "ime-mode") {=0A= e.style.imeMode =3D value;=0A= }=0A= else if (name =3D=3D "layout-flow") {=0A= e.style.layoutFlow =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid") {=0A= e.style.layoutGrid =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-char") {=0A= e.style.layoutGridChar =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-line") {=0A= e.style.layoutGridLine =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-mode") {=0A= e.style.layoutGridMode =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-type") {=0A= e.style.layoutGridType =3D value;=0A= }=0A= else if (name =3D=3D "left") {=0A= e.style.left =3D value;=0A= }=0A= else if (name =3D=3D "letter-spacing") {=0A= e.style.letterSpacing =3D value;=0A= }=0A= else if (name =3D=3D "line-break") {=0A= e.style.lineBreak =3D value;=0A= }=0A= else if (name =3D=3D "line-height") {=0A= e.style.lineHeight =3D value;=0A= }=0A= else if (name =3D=3D "list-style") {=0A= e.style.listStyle =3D value;=0A= }=0A= else if (name =3D=3D "list-style-image") {=0A= e.style.listStyleImage =3D value;=0A= }=0A= else if (name =3D=3D "list-style-position") {=0A= e.style.listStylePosition =3D value;=0A= }=0A= else if (name =3D=3D "list-style-type") {=0A= e.style.listStyleType =3D value;=0A= }=0A= else if (name =3D=3D "margin") {=0A= e.style.margin =3D value;=0A= }=0A= else if (name =3D=3D "margin-bottom") {=0A= e.style.marginBottom =3D value;=0A= }=0A= else if (name =3D=3D "margin-left") {=0A= e.style.marginLeft =3D value;=0A= }=0A= else 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