Malignant transformation of p53-deficient astrocytes is modulated by environmental cues in vitro

Cell Growth and Differentiation

Volumn 10, Issue 2, 1999, Pages 73-86

  Bögler, Oliver ^a,b   Nagane, Motoo ^a   Gillis, Jennifer ^b   Su Huang, H J ^a   Cavenee, Webster K ^a  

^a LUDWIG INSTITUTE FOR CANCER RESEARCH   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN P53; VASCULOTROPIN RECEPTOR;

ANIMAL CELL; ANTIGENICITY; ARTICLE; ASTROCYTE; ASTROCYTOMA; CHROMOSOME NUMBER; COLONY FORMATION; CONTACT INHIBITION; ENVIRONMENTAL FACTOR; GENE MUTATION; GROWTH INHIBITION; IN VITRO STUDY; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR GROWTH; TUMOR SUPPRESSOR GENE;

ANEUPLOIDY; ANIMALS; ASTROCYTES; BLOTTING, NORTHERN; BRAIN; BRAIN NEOPLASMS; CARCINOGENICITY TESTS; CELL CULTURE TECHNIQUES; CELL DIVISION; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; CULTURE MEDIA; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; GLIOMA; HUMANS; MICE; MICE, NUDE; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, PLATELET-DERIVED GROWTH FACTOR; TIME FACTORS; TUMOR STEM CELL ASSAY; TUMOR SUPPRESSOR PROTEIN P53;

ANIMALIA; MUS MUSCULUS;

EID: 0345434899     PISSN: 10449523     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (66)

1. Sidransky, D., Mikkelsen, T., Schwechheimer, K., Rosenblum, M. L., Cavenee, W. K., and Vogelstein, B. Clonal expansion of p53 mutant cells is associated with brain tumour progression. Nature (Lond.), 355: 846-847, 1992.
2. Bogler, O., Huang, H. J., Kleihues, P., and Cavenee, W. K. The p53 gene and its role in human brain tumors. Glia, 15: 308-327, 1995.
3. Reifenberger, G., Liu, L., Ichimura, K., Schmidt, E. E., and Collins, V. P. Amplification and overexpression of the MDM2 gene in a subset of human malignant gliomas without p53 mutations. Cancer Res., 53: 2736-2739, 1993.
4. Biernat, W., Kleihues, P., Yonekawa, Y., and Ohgaki, H. Amplification and overexpression of MDM2 in primary (de novo) glioblastomas. J. Neuropathol. Exp. Neurol., 56: 180-185, 1997.
5. Watanabe, K., Tachibana, O., Sata, K., Yonekawa, Y., Kleihues, P., and Ohgaki, H. Overexpression of the EGF receptor and p53 mutations are mutually exclusive in the evolution of primary and secondary glioblastomas. Brain Pathol., 6: 217-223, 1996.
6. Chung, R., Whaley, J., Kley, N., Anderson, K., Louis, D., Menon, A., Hettlich, C., Freiman, R., Hedley-Whyte, E. T., Martuza, R., and et al. TP53 gene mutations and 17p deletions in human astrocytomas. Genes Chromosomes Cancer, 3: 323-331, 1991.
7. Yahanda, A. M., Bruner, J. M., Donehower, L. A., and Morrison, R. S. Astrocytes derived from p53-deficient mice provide a multistep in vitro model for development of malignant gliomas. Mol. Cell. Biol., 15: 4249-4259, 1995.
8. Tang, P., Steck, P. A., and Yung, W. K. The autocrine loop of TGF-α/ EGFR and brain tumors. J. Neurooncol., 35: 303-314, 1997.
9. Moscatello, D. K., Montgomery, R. B., Sundareshan, P., McDanel, H., Wong, M. Y., and Wong, A. J. Transformational and altered signal transduction by a naturally occurring mutant EGF receptor. Oncogene, 13: 85-96, 1996.
10. Hunter, T. Oncoprotein networks. Cell, 88: 333-346, 1997.
11. Noble, M., and Mayer-Proschel, M. Growth factors, glia and gliomas. J. Neurooncol., 35: 193-209, 1997.
12. Bogler, O., Wren, D., Barnett, S. C., Land, H., and Noble, M. 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, 87: 6368-6372, 1990.
13. Hart, I. K., Richardson, W. D., Bolsover, S. R., and Raff, M. C. PDGF and intracellular signaling in the timing of oligodendrocyte differentiation. J. Cell Biol., 709: 3411-3417, 1989.
14. Mayer, M., Bogler, O., and Noble, M. The inhibition of oligodendrocytic differentiation of O-2A progenitors caused by basic fibroblast growth factor is overridden by astrocytes. Glia, 8: 12-19, 1993.
15. Noble, M., Murray, K., Stroobant, P., Waterfield, M. D., and Riddle, P. Platelet-derived growth factor promotes division and motility and inhibits premature differentiation of the oligodendrocyte/type-2 astrocyte progenitor cell. Nature (Lond.), 333: 560-562, 1988.
16. Vergeli, M., Mazzanti, B., Ballerini, C., Gran, B., Amaducci, L., and Massacesi, L. Transforming growth factor-β1 inhibits the proliferation of rat astrocytes induced by serum and growth factors. J. Neurosci. Res., 40: 127-133, 1995.
17. Gately, S., Soff, G. A., and Brem, S. The potential rote of basic fibroblast growth factor in the transformation of cultured primary human fetal astrocytes and the proliferation of human glioma (U-87) cells. Neurosurgery, 37: 723-730, 1995.
18. Bogler, O., Huang, H. J., and Cavenee, W. K. Loss of wild-type p53 bestows a growth advantage on primary cortical astrocytes and facilitates their in vitro transformation. Cancer Res., 55: 2746-2751, 1995.
19. Eisenbarth, G. S., Walsh, F. S., and Nirenberg, M. Monoclonal antibody to plasma membrane antigen of neurons. Proc. Natl. Acad. Sci. USA, 76: 4913-4917, 1979.
20. Miller, R. H., and Szigeti, V. Clonal analysis of astrocyte diversity in neonatal rat spinal cord cultures. Development (Camb.), 113: 353-362, 1991.
21. Raff, M. C., Miller, R. H., and Noble, M. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature (Lond.), 303: 390-396, 1983.
22. Fukasawa, K., Choi, T., Kuriyama, R., Rulong, S., and Vande, W. Abnormal centrosome amplification in the absence of p53. Science (Washington DC), 277: 1744-1747, 1996.
23. Agapova, L. S., Ilyinskaya, G. V., Turovets, N. A., Ivanov, A. V., Chumakov. P. M., and Kopnin, B. P. Chromosome changes caused by alterations of p53 expression. Mutat. Res., 354: 129-138, 1996.
24. Fields-Berry, S. C., Halliday, A. L., and Cepko, C. L. A recombinant retrovirus encoding alkaline phosphatase confirms clonal boundary assignment in lineage analysis of murine retina. Proc. Natl. Acad. Sci. USA, 89: 693-697, 1992.
25. Luetteke, N. C., Phillips, H. K., Qiu, T. H., Copeland, N. G., Earp, H. S., Jenkins, N. A., and Lee, D. C. The mouse waved-2 phenotype results from a point mutation in the EGF receptor tyrosine kinase. Genes Dev., 8: 399-413, 1994.
26. Shinbrot, E., Peters, K. G., and Williams, L. T. Expression of the platelet-derived growth factor β receptor during organogenesis and tissue differentiation in the mouse embryo. Dev. Dyn., 199: 169-175, 1994.
27. Stephenson, D. A., Mercola, M., Anderson, E., Wang, C., Stiles, C. D., Bowen-Pope, D. F., and Chapman, V. M. Platelet-derived growth factor receptor a-subunit gene (Pdgfra) is deleted in the mouse patch (Ph) mutation. Proc. Natl. Acad. Sci. USA, 88: 6-10, 1991.
28. Mischak, H., Bodenteich, A., Kolch, W., Goodnight, J., Hofer, F., and Mushinski, J. F. Mouse protein kinase C-δ, the major isoform expressed in mouse hemopoietic cells: sequence of the cDNA, expression patterns and characterization of the protein. Biochemistry, 30: 7925-7931, 1991.
29. Cheng, S. Y., Nagane, M., Huang, H. S., and Cavenee, W. K. Intracerebral tumor-associated hemorrhage caused by overexpression of the vascular endothelial growth factor isoforms VEGF121 and VEGF165 but not VEGF189. Proc. Natl. Acad. Sci. USA, 94: 12081-12087, 1997.
30. Bigner, S. H., Humphrey, P. A., Wong, A. J., Vogelstein, B., Mark, J., Friedman, H. S., and Bigner, D. D. Characterization of the epidermal growth factor receptor in human glioma cell lines and xenografts. Cancer Res., 50: 8017-8022, 1990.
31. Fleming, T. P., Saxena, A., Clark, W. C., Robertson, J. T., Oldfield, E. H., Aaronson, S. A., and Ali, I. U. Amplification and/or overexpression of platelet-derived growth factor receptors and epidermal growth factor receptor in human glial tumors. Cancer Res., 52: 4550-4553, 1992.
32. Hebert, J. M., Basilico, C., Goldfarb, M., Haub, O., and Martin, G. R. Isolation of cDNAs encoding four mouse FGF family members and characterization of their expression patterns during embryogenesis. Dev. Biol., 138: 454-463, 1990.
33. Iyer, A., Kmiecik, T. E., Park, M., Daar, I., Blair, D., Dunn, K. J., Sutrave, P., Ihle, J. N., Bodescot, M., and Vande, W. Structure, tissue-specific expression, and transforming activity of the mouse met protooncogene. Cell Growth Differ., 1: 87-95, 1990.
34. Lee, D. C., Rose, T. M., Webb, N. R., and Todaro, G. J. Cloning and sequence analysis of a cDNA for rat transforming growth factor-α. Nature (Lond.), 313: 489-491, 1985.
35. Rong, S., Donehower, L. A., Hansen, M. F., Strong, L., Tainsky, M., Jeffers, M., Resau, J. H., Hudson, E., Tsarfaty, I., and VandeWoude, G. Met proto-oncogene product is overexpressed in tumors of p53-deficient mice and tumors of Li-Fraumeni patients. Cancer Res., 55: 1963-1970, 1995.
36. Schlegel, U., Moots, P. L., Rosenblum, M. K., Thaler, H. T., and Furneaux, H. M. Expression of transforming growth factor α in human gliomas. Oncogene, 5: 1839-1842, 1990.
37. Stone, J. C., Crosby, J. L., Kozak, C. A., Schievella, A. R., Bernard, R., and Nadeau, J. H. The murine retinoblastoma homolog maps to chromosome 14 near Es-10. Genomics, 5: 70-75, 1989.
38. Quelle, D. E., Ashmun, R. A., Hannon, G. J., Rehberger, P. A., Trono, D., Richter, K. H., Walker, C., Beach, D., Sherr, C. J., and Serrano, M. Cloning and characterization of murine p16INK4a and p15INK4b genes. Oncogene, 11: 635-645, 1995.
39. Matsushime, H., Ewen, M. E., Strom, D. K., Kato, J. Y., Hanks, S. K., Roussel, M. F., and Sherr, C. J. Identification and properties of an atypical catalytic subunit (p34PSK-J3/cdk4) for mammalian D type G1 cyclins. Cell, 71: 323-334, 1992.
40. Oltvai, Z. N., Milliman, C. L., and Korsmeyer, S. J. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell, 74: 609-619, 1993.
41. Reid, H. H., Wilks, A. F., and Bernard, O. Two forms of the basic fibroblast growth factor receptor-like mRNA are expressed in the developing mouse brain. Proc. Natl. Acad. Sci. USA, 87: 1596-1600, 87: 1596-1600, 1990.
42. 1 a zinc finger transcriptional factor and oncogene, is expressed during normal mouse development. Dev. Dyn., 796: 91-102, 1993.
43. Ostman, A., Yang, Q., and Tonks, N. K. Expression of DEP-1, a receptor-like protein tyrosine-phosphatase, is enhanced with increasing cell density. Proc. Natl. Acad. Sci. USA, 91: 9680-9684, 1994.
44. Martinez, R., Mathey-Prevot, B., Bernards, A., and Baltimore, D. Neuronal pp60c-src contains a six-amino acid insertion relative to its non-neuronal counterpart. Science (Washington DC), 237: 411-415, 1987.
45. Huppi, K., Siwarski, D., Shaughnessy, J. D., Jr., and Mushinski, J. F. Co-amplification of c-myc/pvt-1 in immortalized mouse B-lymphocytic cell lines results in a novel pvt-1/AJ-1 transcript. Int. J. Cancer, 53: 493-498, 1993.
46. Mercola, M., Wang, C. Y., Kelly, J., Brownlee, C., Jackson-Grusby, L., Stiles, C., and Bowen-Pope, D. Selective expression of PDGF A and its receptor during early mouse embryogenesis. Dev. Biol., 138: 114-122, 1990.
47. Goodnight, J., Kazanietz, M. G., Blumberg, P., Mushinski, J. F., and Mischak, H. The cDNA sequence, expression pattern and protein characteristics of mouse protein kinase C-ζ Gene (Amst.), 122: 305-311, 1992.
48. Mischak, H., Goodnight, J., Henderson, D. W., Osada, S., Ohno, S., and Mushinski, J. F. Unique expression pattern of protein kinase C-θ: high mRNA levels in normal mouse testes and in T-lymphocytic cells and neoplasms. FEBS Lett., 326: 51-55, 1993.
49. McCarthy, K. D., and De Vellis, J. Preparation of separate astrocyte and oligodendrocyte cultures from rat cerebral tissue. J. Cell Biol., 85: 890-902, 1980.
50. Harvey, M., Sands, A. T., Weiss, R. S., Hegi, M. E., Wiseman, R. W., Pantazis, P., Giovanella, B. C., Tainsky, M. A., Bradley, A., and Donehower, L. A. In vitro growth characteristics of embryo fibroblasts isolated from p53-deficient mice. Oncogene, 8: 2457-2467, 1993.
51. Santarius, T., Kirsch, M., Rossi, M. L., and Black, P. M. Molecular aspects of neuro-oncology. Clin. Neurol. Neurosurg., 99: 184-195, 1997.
52. Bredel, M., and Pollack, I. F. The role of protein kinase C (PKC) in the evolution and proliferation of malignant gliomas, and the application of PKC inhibition as a novel approach to anti-glioma therapy. Acta Neurochir. (Wien.), 139: 1000-1013, 1997.
53. James, C. D., and Olson, J. J. Molecular genetics and molecular biology advances in brain tumors. Curr. Opin. Oncol., 8: 188-195, 1996.
54. Guha, A., Dashner, K., Black, P. M., and Wagner, J. A. S. C. D. Expression of PDGF and PDGF receptors in human astrocytoma operation specimens supports the existence of an autocrine loop. Int. J. Cancer, 60: 168-173, 1995.
55. Mauro, A., Bulfone, A., Turco, E., and Schiffer, D. Coexpression of platelet-derived growth factor (PDGF) B chain and PDGF B-type receptor in human gliomas. Childs Nerv. Syst., 7: 432-436, 1991.
56. Westermark, B., Heldin, C. H., and Nister, M. Platelet-derived growth factor in human glioma. Glia, 15: 257-263, 1995.
57. Hermanson, M., Funa, K., Koopman, J., Maintz, D., Waha, A., Westermark, B., Heldin, C. H., Wiestler, O. D., Louis, D. N., von Deimling, A., and Nister, M. Association of loss of heterozygosity on chromosome 17p with high platelet-derived growth factor α receptor expression in human malignant gliomas. Cancer Res., 56: 164-171, 1996.
58. Hermanson, M., Funa, K., Hartman, M., Claesson-Welsh, L., Heldin, C. H., Westermark, B., and Nister, M. Platelet-derived growth factor and its receptors in human glioma tissue: expression of messenger RNA and protein suggests the presence of autocrine and paracrine loops. Cancer Res., 52: 3213-3219, 1992.
59. Arap, W., Knudsen, E. S., Wang, J. Y., Cavenee, W. K., and Huang, H. J. Point mutations can inactivate in vitro and in vivo activities of p16(INK4a)/ CDKN2A in human glioma. Oncogene, 14: 603-609, 1997.
60. Lane, D. P. p53, guardian of the genome. Nature (Lond.), 358: 15-16, 1992.
61. Wilkin, G. P., Marriott, D. R., and Cholewinski, A. J. Astrocyte heterogeneity. Trends Neurosci., 13: 43-46, 1990.
62. Donehower, L. A., Harvey, M., Slagle, B. L., McArthur, M. J., Montgomery, C. A., Butel, J. S., and Bradley, A. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature (Lond.), 356: 215-221, 1992.
63. Noble, M., and Murray, K. Purified astrocytes promote the in vitro division of a bipotential glial progenitor cell. EMBO J., 3: 2243-2247, 1984.
64. Barch, M. J. The Association of Cytogenetic Technologists Cytogenetics Laboratory Manual, p. 275. New York: Raven Press, 1998.
65. Lee, W. H., Bister, K., Moscovici, C., and Duesberg, P. H. Temperature-sensitive mutants of Fujinami sarcoma virus: tumorigenicity and reversible phosphorylation of the transforming p140 protein. J. Virol., 38: 1064-1076, 1981.
66. Nagane, M., Coufal, F., Lin, H., Bogler, O., Cavenee, W. K., and Huang, H. J. A common mutant epidermal growth factor receptor confers enhanced tumorigenicity on human glioblastoma cells by increasing proliferation and reducing apoptosis. Cancer Res., 56: 5079-5086, 1996.