Nf1-deficient mouse schwann cells are angiogenic and invasive and can be induced to hyperproliferate: Reversion of some phenotypes by an inhibitor of farnesyl protein transferase

Molecular and Cellular Biology

Volumn 17, Issue 2, 1997, Pages 862-872

  Kim, Haesun A ^a,b   Ling, Bo ^a   Ratner, Nancy ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; GROWTH FACTOR; NEUROFIBROMIN; PROTEIN FARNESYLTRANSFERASE; PROTEIN FARNESYLTRANSFERASE INHIBITOR;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL HYPERPLASIA; CELL INVASION; CELL SUBPOPULATION; NEUROFIBROMA; NEUROFIBROMATOSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHWANN CELL; SIGNAL TRANSDUCTION;

EID: 0031038519     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.2.862     Document Type: Article

References (74)

1. Arvidsson, U., H. Johnson, F. Piehl, S. Cullheim, T. Hokfelt, M. Risling, L. Terenius, and B. Ulfhake. 1990. Peripheral nerve section induces increased levels of calcitonin gene-related peptide (CGRP)-like immunoreactivity in axotomized motoneurons. Exp. Brain Res. 79:212-216.
2. Asprunk, K. H., D. R. Knighton, and J. Folkman. 1975. Vascularization of normal and neoplastic tissues grafted to the chick chorioallantois. Am. J. Pathol. 79:597-618.
3. Auerbach, W., and R. Auerbach. 1994. Angiogenesis inhibition: a review. Pharmacol. Ther. 63:265-311.
4. Ballester, R., D. Marchuk, M. Boguski, A. Saulino, R. Letcher, M. Wigler, and F. Collins. 1990. The NF1 locus encodes a protein functionally related to mammalian GAP and yeast IRA proteins. Cell 63:851-859.
5. Ballin, M., A. R. Mackay, J. L. Hartzler, A. Nason, M. D. Pelina, and U. P. Thorgeirsson. 1991. Ras levels and metalloproteinase activity in normal versus neoplastic rat mammary tissues. Clin. Exp. Metastasis 9:179-189.
6. Ballin, M., D. E. Gomez, C. C. Sinha, and U. P. Thorgeirsson. 1988. Ras oncogene mediated induction of a 92 kDa metalloproteinase: strong correlation with the malignant phenotype. Biochem. Biophys. Res. Commun. 154:832-838.
7. Basu, T. N., D. H. Gutmann, J. A. Fletcher, T. W. Glover, F. S. Collins, and J. Downward. 1992. Aberrant regulation of ras proteins in malignant tumour cells from type I neurofibromatosis patients. Nature 356:713-715.
8. Boghaert, E. R., J. F. Simpson, and S. G. Zimmer. 1992. Invasion of malignant hamster brain tumor cells is influenced by the numher of cells and the mode of malignant progression. Invasion Metastasis 12:12-23.
9. Brannan, C. I., A. S. Perkins, K. S. Vogel, M. Ratner, M. L. Nordlund, S. W. Reid, A. M. Buchberg, N. A. Jenkins, L. F. Parada, and N. G. Copeland. 1994. Targeted disruption of the neurofibromatosis type-1 gene leads to developmental abnormalities in heart and various neural crest-derived tissues. Genes Dev. 8:1019-1029. (Erratum, 8:2792.)
10. Cheng, L., M. Khan, and A. W. Mudge. 1995. Calcitonin gene-related peptide promotes Schwann cell proliferation. J. Cell Biol. 129:789-796.
11. Coffer, A., J. Fellows, S. Young, D. Pappin, and D. Rahman. 1991. Purification and characterization of biologically active scatter factor from ras-transformed NIH 3T3 conditioned medium. Biochem. J. 278:35-41.
12. Colman, S. D., C. A. Williams, and M. R. Wallace. 1995. Benign neurofibromas in type 1 neurofibromatosis (NF1) show somatic deletions of the NF1 gene. Nat. Genet. 11:90-92.
13. Cook, S. J., and F. McCormick. 1993. Inhibition by cAMP of Ras-dependent activation of Raf. Science 262:1069-1072.
14. Cox, A. D., A. M. Garcia, J. K. Westwick, J. J. Kowalczyk, M. D. Lewis, D. A. Brenner, and C. J. Der. 1994. The CAAX peptidomimetic compound B581 specifically blocks oncogenic ras signaling and transdormation. J. Biol. Chem. 269:19203-19206.
15. Crowe, C. A., W. J. Schull, and J. V. Neel. 1956. A clinical, pathological and genetic study of multiple neurofibromatosis. Charles C Thomas, Springfield, Ill.
16. DeClue, J. E., A. G. Papageorge, J. A. Fletcher, S. R. Diehl, N. Ratner, W. C. Vass, and D. R. Lowy. 1992. Abnormal regulation of mammalian p21ras contributes to malignant tumor growth in von Recklinghausen (type 1) neurofibromatosis. Cell 69:265-273.
17. Denko, N. C., A. J. Giaccia, J. R. Stringer, and P. J. Stambrook. 1994. The human Ha-ras oncogene induces genomic instability in murine fibroblasts within one cell cycle. Proc. Natl. Acad. Sci. USA 91:5124-5128.
18. Ducatman, B. S., B. W. Scheithauer, D. G. Piepgras, and H. M. Reiman. 1984. Malignant peripheral nerve sheath tumors in childhood. J. Neuro-Oncol. 2:241-248.
19. Glover, T. W., C. K. Stein, E. Legius, L. B. Andersen, A. Brereton, and S. Johnson. 1991. Molecular and cytogenetic analysis of tumors in von Recklinghausen neurofibromatosis. Genes Chromosomes Cancer 3:62-70.
20. Goldberg, G. I., S. M. Frisch, C. He, S. M. Wilhelm, R. Reich, and I. E. Collier. 1990. Secreted proteases. Regulation of their activity and their possible role in metastasis. Ann. N.Y. Acad. Sci. 580:375-384.
21. Golubic, M., M. Roudebush, S. Dobrowolski, A. Wolfman, and D. W. Stacey. 1992. Catalytic properties, tissue and intracellular distribution of neurofibromin. Oncogene 7:2151-2159.
22. Huson, S. M. 1994. Neurofibromatosis: historical perspective, classification and diagnostic criteria, p. 1-22. In S. M. Huson and R. A. Hughes (ed.). The neurofibromatoses. Chapman & Hall, London, England.
23. Iberg, N., S. Rogelj, P. Fanning, and M. Klagsbrun. 1989. Purification of 18-and 22-kDa forms of basic fibroblast growth factor from rat cells transformed by the ras oncogene. J. Biol. Chem. 264:19951-19955.
24. Ichikawa, T., N. Kyprianou, and J. T. Isaacs. 1990. Genetic instability and the acquisition of metastatic ability by rat mammary cancer cells following v-H-ras oncogene transfection. Cancer Res. 50:6349-6357.
25. Jacks, T., T. S. Shih, E. M. Schmitt, R. T. Bronson, A. Bernards, and R. A. Weinberg. 1994. Tumour predisposition in mice heterozygous for a targeted mutation in Nf1. Nat. Genet. 7:353-361.
26. James, G. L., J. L. Goldstein, M. S. Brown, I. E. Rawson, T. C. Somers, R. S. McDowell, C. W. Crowley, B. K. Lucas, A. D. Levinson, and J. C. Masters, Jr. 1993. Benzodiazepine peptidomimetrics: potent inhibitors of Ras farnesylation in animal cells. Science 260:1937-1942.
27. James, G. L., M. S. Brown, M. H. Cobb, and J. L. Goldstein. 1994. Benzodiazepine peptidomimetic BZA-5B interrupts the MAP kinase activation pathway in H-Ras-transformed rat-1 cells, but not in untransformed cells. J. Biol. Chem. 269:27705-27714.
28. Kamata, Y. 1978. On the ultrastructure and acetylcholinesterase activity in von Recklinghausen's neurofibromatosis. Acta Pathol. Jpn. 28:393-410.
29. Kim, H. A., T. Rosenbaum, M. A. Marchionni, N. Ratner, and J. E. DeClue. 1995. Schwann cells from neurofibromin deficient mice exhibit activation of p21ras, inhibition of cell proliferation and morphological changes. Oncogene 11:325-335.
30. Kim, J. H., F. E. Johansen, N. Robertson, J. J. Catino, R. Prywes, and C. C. Kumar. 1994. Suppression of Ras transformation by serum response factor. J. Biol. Chem. 269:13740-13743.
31. Kohl, N. E., C. A. Omer, M. W. Conner, N. J. Anthony, J. P. Davide, S. J. deSolms, E. A. Giuliani, R. P. Gomez, S. L. Graham, and K. Hamilton. 1995. Inhibition of farnesyltransferase induces regression of mammary and salivary carcinomas in ras transgenic mice. Nat. Med. 1:792-797.
32. Kohl, N. E., S. D. Mosser, S. J. deSolms, E. A. Giuliani, D. L. Pompliano, S. L. Graham, R. L. Smith, E. M. Scolnick, A. Oliff, and J. B. Gibbs. 1993. Selective inhibition of ras-dependent transformation by a farnesyltransferase inhibitor. Science 260:1934-1937.
33. Krasnoselsky, A., M. J. Massay, M. C. DeFrances, G. Michalopoulos, R. Zarnegar, and N. Ratner. 1994. Hepatocyte growth factor is a mitogen for Schwann cells and is present in neurofibromas. J. Neurosci. 14:7284-7290.
34. Krone, W., R. Mao, O. S. Muhleck, H. Kling, and T. Fink. 1986. Cell culture studies on neurofibromatosis (von Recklinghausen). Characterization of cells growing from neurofibromas. Ann. N.Y. Acad. Sci. 486:354-370.
35. Largaespada, D. A., C. I. Brannan, N. A. Jenkins, and N. G. Copeland. 1996. Nf1 deficiency causes Ras-mediated granulocyte/macrophage colony stimulating factor hypersensitivity and chronic myeloid leukaemia. Nat. Genet. 12:137-143.
36. Legius, E., D. A. Marchuk, F. S. Collins, and T. W. Glover. 1993. Somatic deletion of the neurofibromatosis type 1 gene in a neurofibrosarcoma supports a tumour suppressor gene hypothesis. Nat. Genet. 3:122-126.
37. Legius, E., H. Dierick, R. Wu, B. K. Hall, P. Marynen, J. J. Cassiman, and T. W. Glover. 1994. TP53 mutations are frequent in malignant NF1 tumors. Genes Chromosomes Cancer 10:250-255.
38. Liotta, L. A., U. Wewer, N. C. Rao, E. Schiffmann, M. Stracke, R. Guirguis, U. Thorgeirsson, R. Muschel, and M. Sobel. 1988. Biochemical mechanisms of tumor invasion and metastases. Prog. Clin. Biol. Res. 256:3-16.
39. LoSardo, J. E., B. S. Goggin, O. Bohoslawec, and A. Neri. 1995. Degradation of endothelial cell matrix collagen is correlated with induction of stromelysin by an activated ras oncogene. Clin. Exp. Metastasis 13:236-248.
40. Markwell, M. A., S. M. Haas, L. L. Bieber, and N. E. Tolbert. 1978. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal. Biochem. 82:206-210.
41. Martin, G. A., D. Viskochil, G. Bollag, P. C. McCabe, W. J. Crosier, H. Haubruck, L. Conroy, R. Clark, P. O'Connell, and R. M. Cawthon. 1990. The GAP-related domain of the neurofibromatosis type 1 gene product interacts with ras p21. Cell 63:843-849.
42. Menon, A. G., K. M. Anderson, V. M. Riccardi, R. Y. Chung, J. M. Whaley, D. W. Yandell, G. E. Farmer, R. N. Freiman, J. K. Lee, F. P. Li, et al. 1990. Chromosome 17p deletions and p53 gene mutations associated with the formation of malignant neurofibrosarcomas in von Recklinghausen neurofibromatosis. Proc. Natl. Acad. Sci. USA 87:5435-5439.
43. -) depends on growth inhibition. J. Cell Biol. 112:457-467.
44. Muir, D. 1995. Differences in proliferation and invasion by normal, transformed and NF1 Schwann cell cultures are influenced by matrix metalloproteinase expression. Clin. Exp. Metastasis 13:303-314.
45. Nagasu, T., K. Yoshimatsu, C. Rowell, M. D. Lewis, and A. M. Garcia. 1995. Inhibition of human tumor xenograft growth by treatment with the farnesyl transferase inhibitor B956. Cancer Res. 55:5310-5314.
46. Noguchi, K., E. Senba, Y. Morita, M. Sato, and M. Tohyama. 1990. Co-expression of alpha-CGRP and beta-CGRP mRNAs in the rat dorsal root ganglion cells. Neurosci. Lett. 108:1-5.
47. Nordlund, M., D. Hong, X. Fei, and N. Ratner. 1992. Schwann cells and cells in the oligodendrocyte lineage proliferate in response to a 50,000 dalton membrane-associated mitogen present in developing brain. Glia 5:182-192.
48. Ottini, L., D. L. Esposito, A. Richetta, M. Carlesimo, R. Palmirotta, M. C. Veri, P. Battista, L. Frati, F. G. Caramia, S. Calvieri, et al. 1995. Alterations of microsatellites in neurofibromas of von Recklinghausen's disease. Cancer Res. 55:5677-5680.
49. Peltonen, J., S. Jaakkola, M. Lebwohl, S. Renvall, L. Risteli, I. Virtanen, and J. Uitto. 1988. Cellular differentiation and expression of matrix genes in type 1 neurofibromatosis. Lab. Invest. 59:760-771.
50. Poirier, H., R. Escourolle, and P. Castaigne. 1968. Les neurofibromes de la maladie de Recklinghausen. Acta Neuropathol. 10:279-294.
51. Powell, P. P., and M. Klagsbrun. 1993. Regulation of basic fibroblast growth factor mRNA expression in rat C6 glioma cells. Exp. Cell Res. 209:224-230.
52. Prendergast, G. C., J. P. Davide, S. J. deSolms, E. A. Giuliani, S. L. Graham, J. B. Gibbs, A. Oliff, and N. E. Kohl. 1994. Farnesyltransferase inhibition causes morphological reversion of ras-transformed cells by a complex mechanism that involves regulation of the actin cytoskeleton. Mol. Cell. Biol. 14:4193-4202.
53. Rak, J., Y. Mitsubashi, L. Bayko, J. Filmus, S. Shirasawa, T. Sasazuki, and R. S. Kerbel. 1995. Mutant ras oncogenes upregulate VEGF/VPF expression: implications for induction and inhibition of tumor angiogenesis. Cancer Res. 55:4575-4580.
54. Ratner, N., A. Elbein, M. B. Bunge, S. Porter, R. P. Bunge, and L. Glaser. 1986. Specific asparagine-linked oligosaccharides are not required for certain neuron-neuron and neuron-Schwann cell interactions. J. Cell Biol. 103: 159-170.
55. Ratner, N., M. A. Lieberman, V. M. Riccardi, and D. M. Hong. 1990. Mitogen accumulation in von Recklinghausen neurofibromatosis. Ann. Neurol. 27:298-303.
56. Riccardi, V. M. 1991. Neurofibromatosis: past, present, and future. N. Engl. J. Med. 324:1283-1285. (Editorial.)
57. Ridley, A. J., H. F. Paterson, M. Noble, and H. Land. 1988. Ras-mediated cell cycle arrest is altered by nuclear oncogenes to induce Schwann cell transformation. EMBO J. 7:1635-1645.
58. Rosenbaum, T., H. A. Kim, B. Ling, and N. Ratner. Neurofibromin is required for appropriate P0 expression and myelination. Submitted for publication.
59. Rosenbaum, T., Y. L. Boissy, K. Kombrinck, C. Brannan, N. A. Jenkins, N. G. Copeland, and N. Ratner. 1995. Neurofibromin deficient fibroblasts fail to form perineurium in nitro. Development 121:3583-3592.
60. Sawada, S., S. Florell, S. M. Purandare, M. Ota, K. Stephens, and D. Viskochil. 1996. Identification of NF1 mutations in both alleles of a dermal neurofibroma. Nat. Genet. 14:110-112.
61. Schott, R. J., and L. A. Morrow. 1993. Growth factors and angiogenesis. Cardiovasc. Res. 27:1155-1161.
62. Seamon, K. B., and J. W. Daly. 1981. Forskolin: a unique diterpene activator of cyclic AMP-generating systems. J. Cyclic Nucleotide Res. 7:201-224.
63. Sheela, S., V. M. Riccardi, and N. Ratner. 1990. Angiogenic and invasive properties of neurofibroma Schwann cells. J. Cell Biol. 111:645-653.
64. Skuse, G. R., B. A. Kosciolek, and P. T. Rowley. 1989. Molecular genetic analysis of tumors in von Recklinghausen neurofibromatosis: loss of heterozygosity for chromosome 17. Genes Chromosomes Cancer 1:36-41.
65. Spinucci, C., S. Zucker, J. M. Wieman, R. M. Lysik, B. Imhof, N. Ramamurthy, L. A. Liotta, and H. Nagase. 1988. Purification of a gelatin-degrading type IV collagenase secreted by ras oncogene-transformed fibroblasts. J. Natl. Cancer Inst. 80:1416-1420.
66. Stenman, G., E. O. Delorme, C. C. Lau, and R. Sager. 1987. Transfection with plasmid pSV2gptEJ induces chromosome rearrangements in CHEF cells. Proc. Natl. Acad. Sci. USA 84:184-188.
67. Stewart, J. S., P. A. Eccleston, K. R. Jessen, and R. Mirsky. 1991. Interaction between cAMP elevation, identified growth factors, and serum components in regulating Schwann cell growth. J. Neurosci. Res. 30:346-352.
68. Vaalasti, A., H. Suomalainen, K. Kuokkanen, and L. Rechardt. 1990. Neuropeptides in cutaneous neurofibromas of von Recklinghausen's disease. J. Cutaneous Pathol. 17:371-373.
69. van den Berg, S., B. Kaina, H. J. Rahmsdorf, H. Ponta, and P. Herrlich. 1991. Involvement of fos in spontaneous and ultraviolet light-induced genetic changes. Mol. Carcinog. 4:460-466.
70. Vogel, K. S., C. I. Brannan, N. A. Jenkins, N. G. Copeland, and L. F. Parada. 1995. Loss of neurofibromin results in neurotrophin-independent survival of embryonic sensory and sympathetic neurons. Cell 82:733-742.
71. Wu, J., P. Dent, T. Jelinek, A. Wolfman, M. J. Weber, and T. W. Sturgill. 1993. Inhibition of the EGF-activated MAP kinase signaling pathway by adenosine 3′,5′-monophosphate. Science 262:1065-1069.
72. Xu, G. F., B. Lin, K. Tanaka, D. Dunn, D. Wood, R. Gesteland, R. White, R. Weiss, and F. Tamanoi. 1990. The catalytic domain of the neurofibromatosis type 1 gene product stimulates ras GTPase and complements ira mutants of S. cerevisiae. Cell 63:835-841.
73. Xu, G. F., P. O'Connell, D. Viskochil, R. Cawthon, M. Robertson, M. Culver, D. Dunn, J. Stevens, R. Gesteland, R. White, et al. 1990. The neurofibromatosis type 1 gene encodes a protein related to GAP. Cell 62:599-608.
74. Van, N., C. Ricca, J. Fletcher, T. Glover, B. R. Seizinger, and V. Manne. 1995. Farnesyltransferase inhibitors block the neurofibromatosis type I (NF1) malignant phenotype. Cancer Res. 55:3569-3575.