The 43,000 growth-associated protein functions as a negative growth regulator in glioma

Cancer Research

Volumn 63, Issue 11, 2003, Pages 2933-2939

  Huang, Zhi yong ^a   Wu, YanLi ^a   Burke, Stephen P ^a   Gutmann, David H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH ASSOCIATED PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NEUROMODULIN; PROTEIN KINASE B; RNA; AKT1 PROTEIN, RAT; GROWTH INHIBITOR; ONCOPROTEIN; PROTEIN SERINE THREONINE KINASE; RAP1 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOMA; CANCER CELL CULTURE; CANCER INHIBITION; CARCINOGENESIS; CELL AGGREGATION; CELL CLONE; CELL MOTILITY; CLONOGENIC ASSAY; CONTROLLED STUDY; ENZYME ACTIVATION; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GLIOMA; GLIOMA CELL; GROWTH INHIBITION; GROWTH REGULATION; MALE; MITOGENICITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; TUMOR GROWTH; TUMOR MODEL; ANIMAL; BIOSYNTHESIS; CELL CULTURE; CELL DIVISION; CELL MOTION; CHICKEN; GENETIC TRANSFECTION; GENETICS; METABOLISM; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY;

ANIMALS; CELL DIVISION; CELL MOVEMENT; CHICKENS; GAP-43 PROTEIN; GLIOMA; GROWTH INHIBITORS; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, NUDE; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RAP1 GTP-BINDING PROTEINS; RATS; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 0037905619     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (60)

1. Kleihues, P., and Cavenee, W. K. Tumours of the nervous system. In: World Health Organization Classification of Tumours. Lyon: IARC Press, 2000.
2. Feldkamp, M. M., Lala, P., Lau, N., Roncari, L., and Guha, A. Expression of activated epidermal growth factor receptors. Ras-guanosine triphosphate, and mitogen-activated protein kinase in human glioblastoma multiforme specimens. Neurosurgery, 45: 1442-1453, 1999.
3. Simmons, M. L., Lamborn, K. R., Takahashi, M., Chen, P., Israel, M. A., Berger, M. S., Godfrey, T., Nigro, J., Prados, M., Chang, S., Barker, F. G., II, and Aldape, K. Analysis of complex relationships between age, p53, epidermal growth factor receptor, and survival in glioblastoma patients. Cancer Res., 61: 1122-1128, 2001.
4. Shamah, S. M., Stiles, C. D., and Guha, A. Dominant-negative mutants of platelet-derived growth factor revert the transformed phenotype of human astrocytoma cells. Mol. Cell. Biol., 13: 7203-7212, 1993.
5. Labuhn, M., Jones, G., Speel, E. J., Maier, D., Zweifel, C., Gratzl, O., Van Meir, E. G., Hegi, M. E., and Merlo, A. Quantitative real-time PCR does not show selective targeting of p14(ARF) but concomitant inactivation of both p16(INK4A) and pl4(ARF) in 105 human primary gliomas. Oncogene, 20: 1103-1109, 2001.
6. Guha, A., Feldkamp, M. M., Lau, N., Boss, G., and Pawson, A. Proliferation of human malignant astrocytomas is dependent on Ras activation. Oncogene, 15: 2755-2765, 1997.
7. Feldkamp, M. M., Lau, N., Roncari, L., and Guha, A. Isotype-specific Ras. GTP-levels predict the efficacy of farnesyl transferase inhibitors against human astrocytomas regardless of Ras mutational status. Cancer Res., 61: 4425-4431, 2001.
8. Lau, N., Feldkamp, M. M., Roncari, L., Loehr, A. H., Shannon, P., Gutmann, D. H., and Guha, A. Loss of neurofibromin is associated with activation of RAS/MAPK and PI 3-K/AKT signaling in a neurofibromatosis 1 astrocytoma. J. Neuropathol. Exp. Neurol., 59: 759-767, 2000.
9. Ding, H., Roncari, L. Shannon, P., Wu, X., Lau, N., Karaskova, J., Gutmann, D. H., Squire, J. A., Nagy, A., and Guha, A. Astrocyte-specific expression of activated p21-ras results in malignant astrocytoma formation in a transgenic mouse model of human gliomas. Cancer Res., 61: 3826-3836, 2001.
10. Gutmann, D. H., Huang, Z. Y., Hedrick, N. M., Ding, H., Guha, A., and Watson, M. A. Mouse glioma gene expression profiling identifies novel human glioma-associated genes. Ann. Neurol., 51: 393-405, 2002.
11. Kalil, K., and Skene, J. H. Elevated synthesis of an axonally transported protein correlates with axon outgrowth in normal and injured pyramidal tracts. J. Neurosci., 6: 2563-2570, 1986.
12. Goslin, K., Schreyer, D. J., Skene, J. H., and Banker, G. Development of neuronal polarity: GAP-43 distinguishes axonal from dendritic growth cones. Nature (Lond.), 336: 672-674, 1988.
13. Goslin, K., Schreyer, D. J., Skene, J. H., and Banker, G. Changes in the distribution of GAP-43 during the development of neuronal polarity. J. Neurosci., 10: 588-602, 1990.
14. Aigner, L., Arber, S., Kapfhammer, J. P., Laux, T., Schneider, C., Botteri, F., Brenner, H. R., and Caroni, P. Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell, 83: 269-278, 1995.
15. Caroni, P., Aigner, L., and Schneider, C. Intrinsic neuronal determinants locally regulate extrasynaptic and synaptic growth at the adult neuromuscular junction. J. Cell Biol., 136: 679-692, 1997.
16. Laux, T., Fukami, K., Thelen, M., Golub, T., Frey, D., and Caroni, P. GAP43. MARCKS, and CAP23 modulate PI(4, 5)P(2) at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism. J. Cell Biol., 149: 1455-1472, 2000.
17. Frey, D., Laux, T., Xu, L., Schneider, C., and Caroni, P. Shared and unique roles of CAP23 and GAP43 in actin regulation, neurite outgrowth, and anatomical plasticity. J. Cell Biol., 149: 1443-1454, 2000.
18. Caroni, P. New EMBO member's review: actin cytoskeleton regulation through modulation of PI (4, 5) P (2) rafts. EMBO J., 20: 4332-4336, 2001.
19. Maier, D. L., Mani, S., Donovan, S. L., Soppet, D., Tessarollo, L., McCasland, J. S., and Meiri, K. F. Disrupted cortical map and absence of cortical barrels in growth-associated protein (GAP)-43 knockout mice. Proc. Natl. Acad. Sci. USA, 96: 9397-9402, 1999.
20. Meiri, K. F., Saffell, J. L., Walsh, F. S., and Doherty, P. Neurite outgrowth stimulated by neural cell adhesion molecules requires growth-associated protein-43 (GAP-43) function and is associated with GAP-43 phosphorylation in growth cones. J. Neurosci., 18: 10429-10437, 1998.
21. Widmer, F., and Caroni, P. Phosphorylation-site mutagenesis of the growth-associated protein GAP-43 modulates its effects on cell spreading and morphology. J. Cell Biol., 120: 503-512, 1993.
22. Moretto, G., Xu, R. Y., Monaco, S., Rizzuto, N., and Kim, S. U. Expression and distribution of GAP-43 in human astrocytes in culture. Neuropathol. Appl. Neurobiol., 21: 362-367, 1995.
23. Vitkovic, L., Steisslinger, H. W., Aloyo, V. J., and Mersel, M. The 43-kDa neuronal growth-associated protein (GAP-43) is present in plasma membranes of rat astrocytes. Proc. Natl. Acad. Sci. USA, 85: 8296-8300, 1988.
24. Yamada, K., Goto, S., Oyama, T., Inoue, N., Nagahiro, S., and Ushio, Y. In vivo induction of the growth associated protein GAP43/B-50 in rat astrocytes following transient middle cerebral artery occlusion. Acta Neuropathol. (Berl.), 88: 553-557, 1994.
25. Deloulme, J. C., Laeng, P., Janet, T., Sensenbrenner, M., and Baudier, J. Expression of neuromodulin (GAP-43) and its regulation by basic fibroblast growth factor during the differentiation of O-2A progenitor cells. J. Neurosci. Res., 36: 147-162, 1993.
26. Curtis, R., Hardy, R., Reynolds, R., Spruce, B. A., and Wilkin, G. P. Down-regulation of GAP-43 during oligodendrocyte development and lack of expression by astrocytes in vivo: implications for macroglial differentiation. Eur. J. Neurosci., 3: 876-886, 1991.
27. Deloulme, J. C., Janet, T., Au, D., Storm, D. R., Sensenbrenner, M., and Baudier, J. Neuromodulin (GAP43): a neuronal protein kinase C substrate is also present in 0-2A glial cell lineage. Characterization of neuromodulin in secondary cultures of oligodendrocytes and comparison with the neuronal antigen. J. Cell Biol., 111: 1559-1569, 1990.
28. o. Proc. Natl. Acad. Sci. USA, 90: 2945-2949, 1993.
29. Wolfman, A., Wingrove, T. G., Blackshear, P. J., and Macara, I. G. Down-regulation of protein kinase C and of an endogenous 80-kDa substrate in transformed fibroblasts. J. Biol. Chem., 262: 16546-16552. 1987.
30. Simek, S. L., Kligman, D., Patel, J., and Calburn, N. H. Differential expression of an 80-kDa protein kinase C substrate in preneoplastic and neoplastic mouse JB6 cells. Proc. Natl. Acad. Sci. USA, 86: 7410-7414, 1989.
31. Otsuka, M., and Yang, H. C. Decreased expression of the myristoylated alanine-rich C kinase substrate in transformed BALB/C 3T3 mouse fibroblasts. Biochem. Biophys. Res. Commun., 178: 494-500, 1991.
32. Joseph, C. K., Qureshi, S. A., Wallace, D. J., and Foster, D. A. MARCKS protein is transcriptionally down-regulated in v-Src-transformed BALB/c 3T3 cells. J. Biol. Chem., 267: 1327-1330, 1992.
33. Rose, S. D., Cook, H. W., Palmer, F. B., Ridgway, N. D., and Byers, D. M. Differential expression of MARCKS and other calmodulin-binding protein kinase C substrates in cultured neuroblastoma and glioma cells. J. Neurochem., 63: 2314-2323, 1994.
34. Manenti, S., Malecaze, F., Chap, H., and Darbon, J. M. Overexpression of the myristoylated alanine-rich C kinase substrate in human choroidal melanoma cells affects cell proliferation. Cancer Res., 58: 1429-1434, 1998.
35. Gutmann, D. H., Hirbe, A. C., Huang, Z. H., and Haipek, C. A. The protein 4.1 tumor suppressor, DAL-1, impairs cell motility, but regulates proliferation in a cell-type-specific fashion. Neurobiol. Dis., 8: 266-278, 2001.
36. Li, J., Perry, A., James, C. D., and Gutmann, D. H. Cancer-related gene expression profiles in neurofibromatosis (NF1)-associated pilocytic astrocytomas. Neurology, 56: 885-890, 2001.
37. Zhang, Y., Zhao, W., Zhang, H. J., Domann, F. E., and Oberley, L. W. Overexpression of copper zinc superoxide dismutase suppresses human glioma cell growth. Cancer Res., 62: 1205-1212. 2002.
38. Zhong, W., Oberley, L. W., Oberley, T. D., Yan, T., Domann, F. E., and St. Clair, D. K. Inhibition of cell growth and sensitization to oxidative damage by overexpression of manganese superoxide dismutase in rat glioma cells. Cell Growth Differ., 7: 1175-1186 1996.
39. Zhong, W., Oberley, L. W., Oberley, T. D., and St. Clair, D. K. Suppression of the malignant phenotype of human glioma cells by overexpression of manganese superoxide dismutase. Oncogene, 14: 481-490, 1997.
40. Reuveni, H., Geiger, T., Geiger, B., and Levitzki, A. Reversal of the Ras-induced transformed phenotype by HR12, a novel ras famesylation inhibitor, is mediated by the Mek/Erk pathway. J. Cell Biol., 151: 1179-1192, 2000.
41. Schulze, A., Lehmann, K., Jefferies, H. B., McMahon, M., and Downward, J. Analysis of the transcriptional program induced by Raf in epithelial cells. Genes Dev., 15: 981-994, 2001.
42. Claes, P., Grobben, B., Van Kolen, K., Roymans, D., and Slegers, H. P2Y (AC) (-)-receptor agonists enhance the proliferation of rat C6 glioma cells through activation of the p42/44 mitogen-activated protein kinase. Br. J. Pharmacol., 134: 402-408, 2001.
43. Glass, T. L., Liu, T. J., and Yung, W. K. Inhibition of cell growth in human glioblastoma cell lines by farnesyltransferase inhibitor SCH66336. Neuro-oncol., 2: 151-158, 2000.
44. Xiao, A., Wu, H., Pandolfi, P. P., Louis, D. N., and Van Dyke, T. Astrocyte inactivation of the pRb pathway predisposes mice to malignant astrocytoma development that is accelerated by PTEN mutation. Cancer Cell, 1: 157-168, 2002.
45. Uhrbom, L., Dai, C., Celestino, J. C., Rosenblum, M. K., Fuller, G. N., and Holland, E. C. Ink4a-Arf loss cooperates with KRas activation in astrocytes and neural progenitors to generate glioblastomas of various morphologies depending on activated AKT. Cancer Res., 62: 5551-5558, 2002.
46. Scanga, S. E., Ruel, L., Binari, R. C., Snow, B., Stambolic, V., Bouchard, D., Peters, M., Calvieri, B., Mak, T. W., Woodgett, J. R., and Manoukian, A. S. The conserved PI3′K/PTEN/Akt signaling pathway regulates both cell size and survival in Drosophila. Oncogene, 19: 3971-3977, 2000.
47. Maier, D., Jones, G., Li, X., Schonthal, A. H., Gratzl, O., Van Meir, E. G., and Merlo, A. The PTEN lipid phosphatase domain is not required to inhibit invasion of glioma cells. Cancer Res., 59: 5479-5482, 1999.
48. Senger, D. L., Tudan, C., Guiot, M. C., Mazzoni, I. E., Molenkamp, G., Leblanc, R., Antel, J., Olivier, A., Snipes, G. J., and Kaplan, D. R. Suppression of Rac activity induces apoptosis of human glioma cells but not normal human astrocytes. Cancer Res., 62: 2131-2140, 2002.
49. Guizzetti, M., and Costa, L. G. Effect of ethanol on protein kinase Cζ and p70S6 kinase activation by carbachol: a possible mechanism for ethanol-induced inhibition of glial cell proliferation. J. Neurochem., 82: 38-46, 2002.
50. Maidment, S. L. The cytoskeleton and brain tumour cell migration. Anticancer Res., 17: 4145-4149, 1997.
51. Gorgels, T. G., Van Lookeren Campagne, M., Oestreicher, A. B., Gribnau, A. A., and Gispen, W. H. B-50/GAP43 is localized at the cytoplasmic side of the plasma membrane in developing and adult rat pyramidal tract. J. Neurosci., 9: 3861-3869, 1989.
52. Jacobson, R. D., Virag, I., and Skene, J. H. A protein associated with axon growth, GAP-43, is widely distributed and developmentally regulated in rat CNS. J. Neurosci., 6: 1843-1855, 1986.
53. Warn, R., Brown, D., Dowrick, P., Prescott, A., and Warn, A. Cytoskeletal changes associated with cell motility. Symp. Soc. Exp. Biol., 47: 325-338, 1993.
54. Nolte, C., Moller, T., Walter, T., and Kettenmann, H. Complement 5a controls motility of murine cells in vitro via activation of an inhibitory G-protein and the rearrangement of the actin cytoskeleton. Neuroscience, 73: 1091-1107, 1996.
55. Krushel, L. A., Tai, M. H., Cunningham, B. A., Edelman, G. M., Crossin, and K. L. Neural cell adhesion molecule (N-cam) domains and intracellular signaling pathway involved in the inhibition of astrocyte proliferation. Proc. Natl. Acad. Sci. USA, 95: 2592-2596. 1998.
56. Mariani, L., Beaudry, C., McDonough, W. S., Hoelzinger, D. B., Demuth, T., Ross, K. R., Berens, T., Coons, S. W., Watts, G., Trent, J. M., Wei, J. S., Giese, A., and Berens, M. E. Glioma cell motility is associated with reduced transcription of proapoptotic and proliferation genes: a cDNA microarray analysis. J. Neuro-oncol., 53: 161-176, 2001.
57. Rossino, P., Volpe, G., Negro, A., Callegaro, L., Altruda, F., Tarone, G., and Silengo, L. Ciliary neurotrophic factor-induced gene expression in human neuroblastoma cell lines. Neurochem. Res., 20: 675-680, 1995.
58. Bjelfman, C., Meyerson, G., Cartwright, C. A., Mellstrom, K., Hammerling, U., and Pahlman, S. Early activation of endogenous pp60src kinase activity during neuronal differentiation of cultured human neuroblastoma cells. Mol. Cell. Biol., 10: 361-370, 1990.
59. Turco, A., Scarpa, S., Coppa, A., Baccheschi, G., Palumbo, C., Leonetti, C., Zupi, G., and Colletta, G. Increased TGF β type II receptor expression suppresses the malignant phenotype and induces differentiation of human neuroblastoma cells. Exp. Cell Res., 255: 77-85, 2000.
60. Neuman, K., Soosaar, A., Nomes, H. O., and Neuman, T. Orphan receptor COUP-TF I antagonizes retinoic acid-induced neuronal differentiation. J. Neurosci. Res., 41: 39-48, 1995.