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Stem Cells and the Origin and Propagation of Brain Tumors
Brian A. Emmenegger, BA
Department of Pharmacology and Cancer Biology, Duke University Medical Center, Durham, North Carolina
Robert J. Wechsler-Reya, PhD
Department of Pharmacology and Cancer Biology, Duke University Medical Center, Durham, North Carolina, rw.reya{at}duke.edu
In recent years there has been a flood of interest in the relationship between brain tumors and stem cells. Some investigators have focused on the sensitivity of normal stem cells to transformation, others have described phenotypic or functional similarities between tumor cells and stem cells, and still others have suggested that tumors contain a subpopulation of ``cancer stem cells'' that is crucial for tumor maintenance or propagation. Although all these concepts are interesting and provide insight into the origins and properties of brain tumors, the use of similar terms to describe them has led to confusion. The goal of this review is to sort out some of that confusion and highlight what we know and what we have yet to learn.
Key Words: cell of origin cancer stem cells brain tumor glioma medulloblastoma mouse model
References
- Behin A., Hoang-Xuan K., Carpentier AF, Delattre JY Primary brain tumours in adults. Lancet. 2003;361:323-331.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Crawford JR, MacDonald TJ, Packer RJ Medulloblastoma in childhood: new biological advances. Lancet Neurol. 2007;6: 1073-1085.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Bao S., Wu Q., McLendon RE, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756-760.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Bao S., Wu Q., Sathornsumetee S., et al. Stem Cell-like Glioma Cells Promote Tumor Angiogenesis through Vascular Endothelial Growth Factor. Cancer Res. 2006;66:7843-7848.[Abstract/Free Full Text]
- Liu G., Yuan X., Zeng Z., et al. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer. 2006;5:67.[CrossRef][Medline]
[Order article via Infotrieve]
- Reya T., Morrison SJ, Clarke MF, Weissman IL Stem cells, cancer, and cancer stem cells. Nature. 2001;414:105-111.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Temple S. The development of neural stem cells. Nature. 2001;414:112-117.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Lee A., Kessler JD, Read TA, et al. Isolation of neural stem cells from the postnatal cerebellum. Nat Neurosci. 2005;8:723-729.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Shetty AK, Turner DA In vitro survival and differentiation of neurons derived from epidermal growth factor-responsive postnatal hippocampal stem cells: inducing effects of brain-derived neurotrophic factor. J Neurobiol. 1998;35:395-425.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Emsley JG, Mitchell BD, Kempermann G., Macklis JD Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells. Prog Neurobiol. 2005;75:321-341.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Liu Y., Rao MS Glial progenitors in the CNS and possible lineage relationships among them. Biol Cell. 2004;96:279-290.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Alder J., Cho NK, Hatten ME Embryonic precursor cells from the rhombic lip are specified to a cerebellar granule neuron identity. Neuron. 1996;17:389-399.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Mayer-Proschel M., Kalyani AJ, Mujtaba T., Rao MS Isolation of lineage-restricted neuronal precursors from multipotent neuroepithelial stem cells. Neuron. 1997;19:773-785.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Gregori N., Proschel C., Noble M., Mayer-Proschel M. The tripotential glial-restricted precursor (GRP) cell and glial development in the spinal cord: generation of bipotential oligodendrocyte-type-2 astrocyte progenitor cells and dorsal-ventral differences in GRP cell function. J Neurosci. 2002;22: 248-256.[Abstract/Free Full Text]
- Espinosa de los Monteros A., Zhang M., De Vellis J. 02A progenitor cells transplanted into the neonatal rat brain develop into oligodendrocytes but not astrocytes. Proc Natl Acad Sci USA. 1993;90:50-54.[Abstract/Free Full Text]
- Wechsler-Reya RJ, Scott MP Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog [see comments]. Neuron. 1999;22:103-114.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Altman J., Bayer SA Development of the Cerebellar System: In Relation to Its Evolution, Structure and Functions. Boca Raton, FL: CRC Press; 1997.
- Abraham H., Tornoczky T., Kosztolanyi G., Seress L. Cell formation in the cortical layers of the developing human cerebellum. Int J Dev Neurosci. 2001;19:53-62.[Web of Science][Medline]
[Order article via Infotrieve]
- Tohyama T., Lee VM, Rorke LB, et al. Nestin expression in embryonic human neuroepithelium and in human neuroepithelial tumor cells. Lab Invest. 1992;66:303-313.[Web of Science][Medline]
[Order article via Infotrieve]
- Dahlstrand J., Lardelli M., Lendahl U. Nestin mRNA expression correlates with the central nervous system progenitor cell state in many, but not all, regions of developing central nervous system. Brain Res Dev Brain Res. 1995;84:109-129.[Medline]
[Order article via Infotrieve]
- Graham V., Khudyakov J., Ellis P., Pevny L. SOX2 functions to maintain neural progenitor identity. Neuron. 2003;39:749-765.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Uchida N., Buck DW, He D., et al. Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci USA. 2000;97:14720-14725.[Abstract/Free Full Text]
- Corti S., Nizzardo M., Nardini M., et al. Isolation and characterization of murine neural stem/progenitor cells based on Prominin-1 expression. Exp Neurol. 2007;205:547-562.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Capela A., Temple S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron. 2002;35:865-875.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Sotelo C., Alvarado-Mallart RM, Frain M., Vernet M. Molecular plasticity of adult Bergmann fibers is associated with radial migration of grafted Purkinje cells. J Neurosci. 1994;14: 124-133.[Abstract]
- Pfenninger CV, Roschupkina T., Hertwig F., et al. CD133 is not present on neurogenic astrocytes in the adult subventricular zone, but on embryonic neural stem cells, ependymal cells, and glioblastoma cells. Cancer Res. 2007;67:5727-5736.[Abstract/Free Full Text]
- Doetsch F., Caille I., Lim DA, et al. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell. 1999;97:703-716.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Imura T., Kornblum HI, Sofroniew MV The predominant neural stem cell isolated from postnatal and adult forebrain but not early embryonic forebrain expresses GFAP. J Neurosci. 2003;23:2824-2832.[Abstract/Free Full Text]
- Reynolds BA, Rietze RL Neural stem cells and neurospheres- re-evaluating the relationship. Nat Methods. 2005;2:333-336.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Singec I., Knoth R., Meyer RP, et al. Defining the actual sensitivity and specificity of the neurosphere assay in stem cell biology. Nat Methods. 2006;3:801-806.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Gabay L., Lowell S., Rubin LL, Anderson DJ Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron. 2003;40: 485-499.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Ahn S., Joyner AL In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature. 2005;437:894-897.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- McCarthy M., Turnbull DH, Walsh CA, Fishell G. Telencephalic neural progenitors appear to be restricted to regional and glial fates before the onset of neurogenesis. J Neurosci. 2001;21:6772-6781.[Abstract/Free Full Text]
- Bogler O., Wren D., Barnett SC, et al. Cooperation between two growth factors promotes extended self-renewal and inhibits differentiation of oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells. Proc Natl Acad Sci USA. 1990;87:6368-6372.[Abstract/Free Full Text]
- Leung C., Lingbeek M., Shakhova O., et al. Bmi1 is essential for cerebellar development and is overexpressed in human medulloblastomas. Nature. 2004;428:337-341.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Molofsky AV, Pardal R., Iwashita T., et al. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature. 2003;425:962-967.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Roessmann U., Velasco ME, Gambetti P., Autilio-Gambetti L. Neuronal and astrocytic differentiation in human neuroepithelial neoplasms. An immunohistochemical study. J Neuropathol Exp Neurol. 1983;42:113-121.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Yang HY, Lieska N., Shao D., et al. Proteins of the intermediate filament cytoskeleton as markers for astrocytes and human astrocytomas. Mol Chem Neuropathol. 1994;21:155-176.[Web of Science][Medline]
[Order article via Infotrieve]
- Valtz NL, Hayes TE, Norregaard T., et al. An embryonic origin for medulloblastoma. New Biol. 1991;3:364-371.[Web of Science][Medline]
[Order article via Infotrieve]
- Zhu Y., Guignard F., Zhao D., et al. Early inactivation of p53 tumor suppressor gene cooperating with NF1 loss induces malignant astrocytoma. Cancer Cell. 2005;8:119-130.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Dai C., Celestino JC, Okada Y., et al. PDGF autocrine stimulation dedifferentiates cultured astrocytes and induces oligodendrogliomas and oligoastrocytomas from neural progenitors and astrocytes in vivo. Genes Dev. 2001;15:1913-1925.[Abstract/Free Full Text]
- Assanah M., Lochhead R., Ogden A., et al. Glial progenitors in adult white matter are driven to form malignant gliomas by platelet-derived growth factor-expressing retroviruses. J Neurosci. 2006;26:6781-6790.[Abstract/Free Full Text]
- Yang ZJ, Ellis T., Markant SL, et al. Medulloblastoma can be initiated by deletion of patched in lineage-restricted progenitors or stem cells. Cancer Cell. 2008;14:135-145.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Cozzio A., Passegue E., Ayton PM, et al. Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes Dev. 2003;17: 3029-3035.[Abstract/Free Full Text]
- Oliver TG, Read TA, Kessler JD, et al. Loss of patched and disruption of granule cell development in a pre-neoplastic stage of medulloblastoma. Development. 2005;132:2425-2439.[Abstract/Free Full Text]
- Singh SK, Hawkins C., Clarke ID, et al. Identification of human brain tumour initiating cells. Nature. 2004;432:396-401.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Wang JC, Dick JE Cancer stem cells: lessons from leukemia. Trends Cell Biol. 2005;15:494-501.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Bonnet D., Dick JE Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 1997;3:730-737.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Al-Hajj M., Wicha MS, Benito-Hernandez A., et al. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA. 2003;100:3983-3988.[Abstract/Free Full Text]
- Xin L., Lawson DA, Witte ON The Sca-1 cell surface marker enriches for a prostate-regenerating cell subpopulation that can initiate prostate tumorigenesis. Proc Natl Acad Sci USA. 2005;102:6942-6947.[Abstract/Free Full Text]
- Fang D., Nguyen TK, Leishear K., et al. A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res. 2005;65:9328-9337.[Abstract/Free Full Text]
- O'Brien CA, Pollett A., Gallinger S., Dick JE A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 2007;445:106-110.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Li C., Heidt DG, Dalerba P., et al. Identification of pancreatic cancer stem cells. Cancer Res. 2007;67:1030-1037.[Abstract/Free Full Text]
- Singh SK, Clarke ID, Terasaki M., et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003;63:5821-5828.[Abstract/Free Full Text]
- Krivtsov AV, Twomey D., Feng Z., et al. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature. 2006;442:818-822.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Matsui W., Huff CA, Wang Q., et al. Characterization of clonogenic multiple myeloma cells. Blood. 2004;103:2332-2336.[Abstract/Free Full Text]
- Wang J., Sakariassen PO, Tsinkalovsky O., et al. CD133 negative glioma cells form tumors in nude rats and give rise to CD133 positive cells. Int J Cancer. 2008;122:761-768.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Beier D., Hau P., Proescholdt M., et al. CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res. 2007;67: 4010-4015.[Abstract/Free Full Text]
- Kondo T., Setoguchi T., Taga T. Persistence of a small subpopulation of cancer stem-like cells in the C6 glioma cell line. Proc Natl Acad Sci USA. 2004;101:781-786.[Abstract/Free Full Text]
- Ghods AJ, Irvin D., Liu G., et al. Spheres isolated from 9L gliosarcoma rat cell line possess chemoresistant and aggressive cancer stem-like cells. Stem Cells. 2007;25:1645-1653.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Bar EE, Chaudhry A., Lin A., et al. Cyclopamine-mediated hedgehog pathway inhibition depletes stem-like cancer cells in glioblastoma. Stem Cells. 2007;25:2524-2533.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Piccirillo SG, Reynolds BA, Zanetti N., et al. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature. 2006;444:761-765.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Fan X., Matsui W., Khaki L., et al. Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res. 2006;66:7445-7452.[Abstract/Free Full Text]
- Calabrese C., Poppleton H., Kocak M., et al. A perivascular niche for brain tumor stem cells. Cancer Cell. 2007;11:69-82.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Fogarty MP, Kessler JD, Wechsler-Reya RJ Morphing into cancer: the role of developmental signaling pathways in brain tumor formation. J Neurobiol. 2005;64:458-475.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Zurawel RH, Chiappa SA, Allen C., Raffel C. Sporadic medulloblastomas contain oncogenic beta-catenin mutations. Cancer Res. 1998;58:896-899.[Abstract/Free Full Text]
- Pietsch T., Waha A., Koch A., et al. Medulloblastomas of the desmoplastic variant carry mutations of the human homologue of Drosophila patched. Cancer Res. 1997;57:2085-2088.[Abstract/Free Full Text]
- Taylor MD, Liu L., Raffel C., et al. Mutations in SUFU predispose to medulloblastoma. Nat Genet. 2002;31:306-310.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Molofsky AV, He S., Bydon M., et al. Bmi-1 promotes neural stem cell self-renewal and neural development but not mouse growth and survival by repressing the p16Ink4a and p19Arf senescence pathways. Genes Dev. 2005;19:1432-1437.[Abstract/Free Full Text]
- Bruggeman SW, Hulsman D., Tanger E., et al. Bmi1 controls tumor development in an Ink4a/Arf-independent manner in a mouse model for glioma. Cancer Cell. 2007;12:328-341.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
- Chow LM, Baker SJ PTEN function in normal and neoplastic growth. Cancer Lett. 2006;241:184-196.[CrossRef][Web of Science][Medline]
[Order article via Infotrieve]
Journal of Child Neurology, Vol. 23, No. 10,
1172-1178 (2008)
DOI: 10.1177/0883073808321062

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R. A. Brumback
Child Neurologists Should Be Interested In Brain Tumors!
J Child Neurol,
November 1, 2009;
24(11):
1338 - 1340.
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