Human cortical glial tumors contain neural stem-like cells expressing astroglial and neuronal markers in vitro

GLIA

Volumn 39, Issue 3, 2002, Pages 193-206

  Ignatova, Tatyana N ^a   Kukekov, Valery G ^a   Laywell, Eric D ^a   Suslov, Oleg N ^a   Vrionis, Frank D ^b   Steindler, Dennis A ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

Delta; Glial tumors; Jagged; Nestin; Neural cell diversity; Neural stem cell; Pleiotropic growth factors; Serum and anchorage withdrawal; Survivin

Indexed keywords

ASTROCYTES; BIOLOGICAL MARKERS; CEREBRAL CORTEX; CLONE CELLS; GLIOMA; HUMANS; MULTIPOTENT STEM CELLS; NEURONS; TUMOR CELLS, CULTURED;

EID: 0036737914     PISSN: 08941491     EISSN: None     Source Type: Journal    
DOI: 10.1002/glia.10094     Document Type: Article

References (66)

1. Adida C, Crotty P, McGraph J, Berrebi D, Diebold J, Altiery DC. 1998. Developmentally regulated expression of the novel cancer anti-apoptosis gene Survivin in human and mouse differentiation. Am J Pathol 152:43-49.
2. Ambrosini G, Adida C, Altiery DC. 1997. A novel anti-apoptosis gene, Survivin, expressed in cancer and lymphoma. Nature Med 3:917-921.
3. Barnett SC, Robertson L, Graham D, Allan D, Rampling R. 1998. Olygodendrocyte-type-2 astrocyte (O2A) progenitor cells transformed with c-myc and H-ras form high-grade glioma after stereotactic injection into the rat. Carcinogenesis 19:1529-1537.
4. Bordey A, Sontheimer H. 1998. Electrophysiological properties of human astrocytic tumor cells in situ: enigma of spiking glial cells. J Neurophysiol 79:2782-2793.
5. Bouterfa H, Darlapp AR, Klein E, Pietsch T, Roosen K, Tonn JC. 1999. Expression of different extracellular matrix components in human brain tumor and melanoma cells in respect to variant culture conditions. J Neurooncol 44:23-33.
6. Brazelton TR, Rossi FM, Keshet GI, Blau HM. 2000. From marrow to brain: expression of neuronal phenotypes in adult mice. Science 290:1775-1779.
7. Brodkey JA, Laywell ED, O'Brien TF, Faissner A, Stefansson K, Dorries U, Schachner M, Steindler DA. 1995. Focal brain injury and the upregulation of a developmentally-regulated extracellular matrix protein. J Neurosurg 82:106-112.
8. Brustle O, McKay RD. 1995. The neuroepithelial stem cell concept: implications for neuro-oncology. J Neurooncol 24:57-59.
9. Dahlstrand J, Collins VP, Lendahl U. 1992. Expression of the class VI intermediate filament nestin in human central nervous system tumors. Cancer Res 52:5334-5341.
10. Doetsch F, Caille I, Lim, DA, Garsia-Verdugo JM, Alvares-Buylla A. 1999. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703-716.
11. Eaves CJ. 1995. Assays of hemopoietic progenitor cells. In: Beutler E, Lichtman MA, Coller BS, Kipps TJ, editors. Hematology, 5th ed. New York: McGraw-Hill. p 122-126.
12. Faux CH, Turnley AM, Epa R, Cappai R, Bartlett PF. 2001. Interactions between fibroblast growth factors and Notch regulate neuronal differentiation. J Neurosci 21:5587-5596.
13. Furukawa Y, Nakamura M, Matsuda M. 2000. Transcriptional repressor E2F-6 regulates apoptosis in hematopoietic stem cells. Exp Hematol 28:1504-1505.
14. Gaidano G, Ballerini P, Gong JZ, Inghirami G, Neri A, Newcomb EW, Magrath IT, Knowles DM, Dalla-Favera R. 1991. p53 mutations in human lymphoid malignancies: association with Burkitt lymphoma and chronic lymphocytic leukemia. Proc Natl Acad Sci 88:5413-5417.
15. Galli R, Borello, U, Gritti A, Bjornson C, Coletta M, Mora M, De Angelis GC, Fiocco R, Cossu G, Vescovi AL. 2000. Skeletal myogenic potential of human and mouse neural stem cells. Nat Neurosci 3:986-991.
16. Galy B, Creancier L, Prado-Lourenco L, Prats AC, Prats H. 2001. p53 directs conformational change and translation initiation blockade of human fibroblast growth factor 2 mRNA. Oncogene 20:4613-4620.
17. Gates MA, Thomas LB, Howard E, Laywell ED, Sajin B, Faissner A, Silver J, Steindler DA. 1995. A cell and molecular analysis of the developing and adult mouse subependymal zone of the cerebral hemispheres. J Comp Neurol 361:249-266.
18. Gritti A, Frollchsthal-Schoeller P, Galli R, Parati EI, Cova L, Pagano SF, Bjornson CR, Vescovi AL. 1999. Epidermal and fibroblast growth factors behave as mitogenic regulators for a single multipotent stem cell-like population from the subventricular region of the adult mouse forebrain. J Neurosci 19:3287-3297.
19. Gritti A, Rosati B, Lecchi M, Vescovi AL, Wanke E. 2000. Excitable properties in astrocytes derived from human embryonic CNS stem cells. Eur J Neurosci 12:3549-3559.
20. Gussoni E, Soneoka Y, Strickland CD, Buzney EA., Khan MK, Flint AF, Kunkel LM, Mulligan RC. 1999. Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 401:390-394.
21. Hattori M, Sakamoto H, Satoh K, Yamamoto T. 2001. DNA demethylase is expressed in ovarian cancers and the expression correlates with demethylation of CpG sites in the promoter region of c-ErbB-2 and Survivin genes. Cancer Lett 169:155-164.
22. Holland EC, Celestino J, Dai C, Schaefer L, Sawaya RE, Fuller GN. 2000. Combined activation of Ras and Akt in neural progenitors induces glioblastoma formation in mice. Nat Genet 25:55-57.
23. Jackson KA, Mi T, Goodell MA. 1999. Hematopoietic potential of stem cells isolated from murine skeletal muscle. Proc Natl Acad Sci USA 96:14482-14486.
24. Kobayashi K, Hatano M, Otaki M, Ogasawara T, Tokuhisa T. 1999. Expression of murine homologue of the inhibitor of apoptosis protein is related to cell proliferation. Proc Natl Acad Sci USA 96:1457-1462.
25. Kopen GC, Prockop DJ, Phinney D. 1999. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc Natl Acad Sci USA 96:10711-10716.
26. Kukekov VG, Laywell ED, Thomas LB, Steindler DA. 1997. A nestin-negative precursor cell from the adult mouse brain gives rise to neurons and glia. Glia 21:399-407.
27. Kukekov VG, Laywell ED, Suslov O, Davies K, Scheffler B, Thomas LB, O'Brien TF, Kusakabe M, Steindler DA. 1999. Multipotent stem/progenitor cells with similar properties arise from two neurogenic regions of adult human brain. Exp Neurol 156:333-344.
28. Kurpad SN, Zhao XG, Wikstrand CJ, Batra SK, McLendon RE, Bigner DD. 1995. Tumor antigens in astrocytic gliomas. Glia 15:244-256.
29. Lagasse E, Connors H, Al-Dhalimy M, Reitsma M., Dohse M, Osborne L, Wang X, Finegold M, Weissman IL, Grompe M. 2000. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med 6:1229-1234.
30. Laywell ED, Kukekov VG, Steindler DA. 1999. Multipotent neurospheres can be derived from forebrain subependymal zone and spinal cord of adult mice after protracted post-mortem intervals. Exp Neurol 156:430-433.
31. Laywell ED, Rakic P, Kukekov VG, Holland E, Steindler DA. 2000. Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc Natl Acad Sci USA 97:13883-13888.
32. Lendahl U, Zimmerman LB, McKay RDG. 1990. CNS stem cells express a new class of intermediate filament protein. Cell 60:585-595.
33. Li F, Ambrosini G, Chu EY, Plescia J, Tognin S, Marchisio PC, Altieri DC. 1998. Control of apoptosis and mitotic spindle checkpoint by Survivin. Nature 396:580-584.
34. Lin RC, Matesic DF, Marvin M, McKay RDG, Brustle O. 1995. Reexpression of the intermediate filament nestin in reactive astrocytes. Neurobiol Dis 2:79-85.
35. Lindsell CE, Boulter J, diSibio G, Gossler A, Weinmaster G. 1996. Expression patterns of Jagged, Delta 1, Notch 1, Notch 2, and Notch 3 genes identify ligand-receptor pairs that may function in neural development. Mol Cell Neurosci 8:14-27.
36. Mahotka C, Wenzel M, Springer E, Gabbert HE, Gerharz CD. 1999. Survivin-AEx3 and survivin-2B: two novel splice variants of the apoptosis inhibitor survivin with different antiapoptotic properties. Cancer Res 59:6098-6102.
37. McKeon R, Schreiber J, Rudge JS, Silver J. 1991. Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J Neurosci 11:3398-3411.
38. Mezey E, Chandross KJ, Harta G, Maki RA, McKercher SR. 2000. Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science 290:1779-1782.
39. Miele L, Osborne B. 1999. Arbiter of differentiation and death: notch signaling meets apoptosis. J Cell Physiol 181:393-409.
40. Morrison SJ, White PM, Zock C, Anderson DJ. 1999. Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell 96:737-749.
41. Morse RP, Darras B, Ye Z, Wu JK. 1994. Clonal analysis of human astrocytomas. J Neurooncol 21:151-157.
42. Noble M, Mayer-Proschel M. 1997. Growth factors, glia and gliomas. J Neurooncol 35:193-209.
43. O'Kusky JR, Ye P, D'Ercole AJ. 2000. Insulin-like growth factor-I promotes neurogenesis and synaptogenesis in the hippocampal dentate gyrus during postnatal development. J Neurosci 20:8435-8442.
44. Palmer TD, Markakis EA, Willhoite AR, Safar F, Gage FH. 1999. Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J Neurosci 19:8487-8497.
45. Petersen BE, Bowen WC, Patrene KD, Mars WM, Sullivan AK, Murase N, Boggs SS, Greenberger JS, Goff JP. 1999. Bone marrow as a potential source of hepatic oval cells. Science 284:1168-1170.
46. Reynolds BA, Weiss S. 1992. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707-1710.
47. Sanchez-Ramos J, Song S, Cardoso-Pelaes F, Hazzi C, Stedford T, Willing A, Freeman TB, Saporta S, Janssen W, Patel N, Cooper, DR, Sanberg PR. 2000. Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp Neurol 164:247-256.
48. Scheffler B, Horn M, Bluemcke I, Laywell ED, Coomes D, Kukekov VG, Steindler DA. 1999. Marrow-mindedness: a perspective on neuropoiesis. Trends Neurosci 22:348-357.
49. Schmechel DE, Marangos PJ, Matin BM, Winfield S, Burhart DS, Roses AD, Ginnes EI. 1987. Localization of neuron-specific enolase (NSE) mRNA in human brain. Neurosci Lett 76:233-238.
50. Seri B, Garcia-Verdugo J, McEwen BS, Alvarez-Buylla A. 2001. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153-7160.
51. Sidransky D, Mikkelsen T, Schwechheimer K, Rosenblum ML, Cavanee W, Vogelstein B. 1992. Clonal expansion of p53 mutant cells is associated with brain tumor progression. Nature 355:846-847.
52. Silbergeld DL, Chicoine MR. 1997. Isolation and characterization of human malignant glioma cells from histologically nomral brain. J Neurosurg 86:484-485.
53. Steindler DA, Kadrie T, Fillmore H, Thomas LB. 1996. The subependymal zone of the adult brain: "brain marrow." Prog Brain Res 108:349-363.
54. Suslov ON, Kukekov VG, Laywell ED, Scheffler B, Steindler DA. 2000. RT-PCR amplification of mRNA from single brain neurospheres. J Neurosci Meth 96:57-61.
55. Temple S, Raff MC. 1985. Differentiation of a bipotential glial progenitor cell in a single cell microculture. Nature 313:223-225.
56. Thomas LB, Steindler DA. 1995. Glial boundaries and scars: Programs for normal development and wound healing in the brain. Neuroscientist 1:142-154.
57. Toda M, Iizuka Y, Yu W, Imai T, Ikeda E, Yoshida K, Kawase T, Kawakami Y, Okano H, Uyemura K. 2001. Expression of the neural RNA-binding protein Musashi1 in human gliomas. Glia 34:1-7.
58. Tropepe V, Sibilia M, Ciruna BG, Rossant J, Wagner EF, Van der Kooy D. 1999. Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon. Dev Biol 208:166-188.
59. Tsai RYL, McKay RDG. 2000. Cell contact regulates fate choice by cortical stem cells. J Neurosci 20:3725-3735.
60. Ueba T, Nosaka T, Takahashi JA, Shibata F, Florkiewicz RZ, Vogelstein B, Oda Y, Kikuchi H, Hatanaka M. 1994. Transcriptional regulation of basic fibroblast growth factor gene by p53 in human glioblastoma and hepatocellular carcinoma cells. Proc Natl Acad Sci USA 91:9009-9013.
61. Uhrbum L, Hesselager G, Nister M, Westermark B. 1998. Induction of brain tumors in mice using a recombinant platelet-derived growth factor B-chain retrovirus. Cancer Res 58:5275-5279.
62. Vescovi AL, Reynolds BA, Fraser DD, Weiss S. 1993. FGF-2 regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron 11: 951-966.
63. Vescovi AL, Parati E, Gritti A, Poulin P, Farrario M, Wanke E, Frolichsthal-Schoeller P, Cova L, Arcellana-Panlilio M, Colombo A, Galli R. 1999. Isolation and cloning of multipotential stem cells from the embryonic human CNS and establishment of transplantable human neural stem cell lines by epigenetic stimulation. Exp Neurol 156:71-83.
64. Weinmaster G. 2000. Notch signal transduction: a real rip and more. Curr Opin Genet Dev 10:363-369.
65. Woodbury D, Schwarz EJ, Prockop DJ, Black I. 2000. Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res 61:364-370.
66. Zhang T, Otevrel T, Gao Zhengiang, Gao Zhiping, Ehrlich SM, Fields JZ, Boman BM. 2001. Evidence that APC regulates survivin expression: a possible mechanism contributing to the stem cell origin of colon cancer. Cancer Res 62:8664-8667.