Oncogenes and tumor angiogenesis: Differential modes of vascular endothelial growth factor up-regulation in ras-transformed epithelial cells and fibroblasts

Cancer Research

Volumn 60, Issue 2, 2000, Pages 490-498

  Rak, Janusz ^a   Mitsuhashi, Yoshihiro ^a   Sheehan, Cap ^a   Tamir, Ami ^a   Viloria Petit, Alicia ^a   Filmus, Jorge ^a   Mansour, Sam J ^b   Ahn, Natalie G ^b   Kerbel, Robert S ^a,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF COLORADO   (United States)

^c SUNNYBROOK RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; DIMETHYL SULFOXIDE; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CARCINOGENICITY; CELL DENSITY; CELL TRANSFORMATION; CONTROLLED STUDY; EPITHELIUM CELL; FIBROBLAST; GENE EXPRESSION; GENETIC TRANSFECTION; MITOGENESIS; MOUSE; NONHUMAN; ONCOGENE RAS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM;

3T3 CELLS; ANIMALS; CELL DIVISION; CELL LINE; CELL TRANSFORMATION, NEOPLASTIC; CHROMONES; ENDOTHELIAL GROWTH FACTORS; ENZYME INHIBITORS; EPITHELIAL CELLS; FIBROBLASTS; FLAVONOIDS; GENE EXPRESSION REGULATION; GENES, RAS; INTESTINAL MUCOSA; KINETICS; LYMPHOKINES; MICE; MICE, NUDE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MORPHOLINES; NEOPLASMS, EXPERIMENTAL; NEOVASCULARIZATION, PATHOLOGIC; RATS; SIGNAL TRANSDUCTION; THROMBOSPONDIN 1; TRANSFECTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 0034650744     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (71)

1. Rak, J., Mitsuhashi, Y., Bayko, L., Filmus, J., Sasazuki, T., and Kerbel, R. S. Mutant ras oncogenes up-regulate VEGF/VPF expression: implications for induction and inhibition of tumor angiogenesis. Cancer Res., 55: 4575-4580, 1995.
2. Grugel, S., Finkenzeller, G., Weindel, K., Barleon, B., and Marme, D. Both v-Ha-ras and v-raf stimulate expression of the vascular endothelial growth factor in NIH 3T3 cells. J. Biol. Chem., 270: 25915-25919, 1995.
3. Dvorak, H. F., Brown, L. F., Detmar, M., and Dvorak, A. M. Review: vascular permeability factor/vascular endothelial growth factor, microvascular hyperperme-ability, and angiogenesis. Am. J. Pathol., 146: 1029-1039, 1995.
4. Shirasawa, S., Furuse, M., Yokoyama, N., and Sasazuki, T. Altered growth of human colon cancer cell lines disrupted at activated Ki-ras. Science (Washington DC), 260: 85-88, 1993.
5. Okada, F., Rak, J., St. Croix, B., Lieubeau, B., Kaya, M., Roncari, L., Sasazuki, S., and Kerbel, R. S. Impact of oncogenes on tumor angiogenesis: mutant K-ras up-regulation of VEGF/VPF is necessary but not sufficient for tumorigenicity of human colorectal carcinoma cells. Proc. Natl. Acad. Sci. USA, 95: 3609-3614, 1998.
6. Ferrara, N., Carver-Moore, K., Chen, H., Dowd, M., Lu, L., O'Shea, K. S., Powell-Braxton, L., Hillan, K. J., and Moore, M. W. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature (Lond.), 380: 439-442, 1996.
7. Shi, Y. P., and Ferrara, N. Oncogenic ras fails to restore an in vivo tumorigenic phenotype in embryonic stem cells lacking vascular endothelial growth factor (VEGF). Biochem. Biophys. Res. Commun., 254: 480-483, 1999.
8. Grunstein, J., Roberts, W. G., Mathieu-Costello, O., Hanahan, D., and Johnson, R. S. Tumor-derived expression of vascular endothelial growth factor is a critical factor in tumor expansion and vascular function. Cancer Res., 59: 1592-1598, 1999.
9. Rak, J., Mitsuhashi, Y., Sheehan, C., Krestow, J. K., Florenes, V. A., Filmus, J., and Kerbel, R. S. Collateral expression of proangiogenic and tumorigenic properties in intestinal epithelial cell variants selected for resistance to anoikis. Neoplasia, 1: 23-30, 1999.
10. Chin, L., Tam, A., Pomerantz, J., Wong, M., Holash, J., Bardeesy, N., Shen, Q., O'Hagan, R., Pantginis, J., Zhou, H., Homer, J. W., Cordon-Cardo, C., Yancopoulos, G. D., and DePinho, R. A. Essential role for oncogenic Ras in tumour maintenance. Nature (Lond.), 400: 468-472, 1999.
11. Charvat, S., Duchesne, M., Parvaz, P., Chignol, M. C., Schmitt, D., and Serres, M. The up-regulation of vascular endothelial growth factor in mutated Ha-ras HaCaT cell lines is reduced by a farnesyl transferase inhibitor. Anticancer Res., 19: 557-561, 1999.
12. Kerbel, R. S., Viloria-Petit, A. M., Okada, F., and Rak, J. W. Establishing a link between oncogenes and tumor angiogenesis. Mol. Med., 4: 286-295, 1998.
13. Viloria-Petit, A. M., Rak, J., Hung, M-C., Rockwell, P., Goldstein, N., and Kerbel, R. S. Neutralizing antibodies against EGF and ErbB-2/neu receptor tyrosine kinases down-regulate VEGF production by tumor cells in vitro and in vivo: angiogenic implications for signal transduction therapy of solid tumors. Am. J. Pathol., 157: 1523-1530, 1997.
14. Mansour, S. J., Matten, W. T., Hermann, A. S., Candia, J. M., Rong, S., Fukasawa, K., Woude, G. F. V., and Ahn, N. G. Transformation of mammalian cells by constitutively active MAP kinase kinase. Science (Washington DC), 265: 966-970, 1994.
15. Khosravi-Far, R., Campbell, S., Rossman, K. L., and Der, C. J. Increasing complexity of Ras signal transduction: involvement of Rho family proteins. Adv. Cancer Res., 72: 57-107, 1998.
16. Irani, K., Xia, Y., Zweier, J. L., Sollott, S. J., Der, C. J., Fearon, E. R., Sundaresan, M., Finkel, T., and Goldschmidt-Clermont, P. J. Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science (Washington DC), 275: 1649-1652, 1997.
17. Rodriguez-Viciana, P., Warne, P. H., Dhand, R., Vanhaesebroeck, B., Gout, I., Fry, M. J., Waterfield, M. D., and Downward, J. Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature (Lond.), 370: 527-532, 1994.
18. Rodriguez-Viciana, P., Warne, P. H., Khwaja, A., Marte, B. M., Pappin, D., Das, P., Waterfield, M. D., Ridley, A., and Downward, J. Role of phosphoinositide 3-OH kinase in cell transformation and control of the actin cytoskeleton by Ras. Cell, 89: 457-467, 1997.
19. Oldham, S. M., Clark, G. J., Gangarosa, L. M., Coffey, R. J., Jr., and Der, C. J. Activation of the RaM-1/MAP kinase cascade is not sufficient for Ras transformation of RIE-I epithelial cells. Proc. Natl. Acad. Sci. USA, 93: 6924-6928, 1996.
20. McKay, I. A., Malone, P., Marshall, C. J., and Hall, A. Malignant transformation of murine fibroblasts by a human c-Ha-ras-1 oncogene does not require a functional epidermal growth factor receptor. Mol. Cell. Biol., 6: 3382-3387, 1986.
21. Filmus, J., Shi, W., and Spencer, T. Role of transforming growth factor α (TGF-α) in the transformation of ras-transfected rat intestinal epithelial cells. Oncogene, 8: 1017-1022, 1993.
22. Gangarosa, L. M., Sizemore, N., Graves-Deal, R., Oldham, S. M., Der, C. J., and Coffey, R. J. A raf-independent epidermal growth factor receptor autocrine loop is necessary for Ras transformation of rat intestinal epithelial cells. J. Biol. Chem., 272: 18926-18931, 1997.
23. Goldman, C. K., Kim, J., Wong, W. L. King, V., Brock, T., and Gillespie, G. Y. Epidermal growth factor stimulates vascular endothelial growth factor production by human malignant glionia cells: a model of glioblastoma multiforme pathophysiology. Mol. Biol. Cell, 4: 121-133, 1993.
24. Ciardiello, F., Damiano, V., Bianco, R., Bianco, C., Fontanini, G., De Laurentiis, M., De Placido, S., Mendelsohn, J., Bianco, A. R., and Tortora, G. Antitumor activity of combined blockade of epidermal growth factor receptor and protein kinase A. J. Natl. Cancer Inst., 88: 1770-1776, 1996.
25. Gille, J., Swerlick, R. A., and Caughman, S. W. Transforming growth factor-α-induced transcriptional activation of the vascular permeability factor (VPF/VEGF) gene requires AP-2-dependent DNA binding and transactivation. EMBO J., 16: 750-759, 1997.
26. Tischer, E., Mitchell, R., Hartman, T., Silva, M., Gospodarowicz, D., and Fiddes, J. C. The human gene for vascular endothelial growth factor. J. Biol. Chem., 266: 11947-11954, 1991.
27. Shima, D. T., Kuroki, M., Deutsch, U., Ng, Y. S., Adamis, A. P., and D'Amore, P. A. The mouse gene for vascular endothelial growth factor. Genomic structure, definition of the transcriptional unit, and characterization of transcriptional and posl-transcriptional regulatory sequences. J. Biol. Chem., 271: 3877-3883, 1996.
28. Forsythe, J. A., Jiang, B. H., Iyer, N. V., Agani, F., Leung, S. W., Koos, R. D., and Semenza, G. L. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol., 16: 4604-4613, 1996.
29. Mazure, N. M., Chen, E. Y., Laderoute, K. R., and Giaccia, A. J. Induction of vascular endothelial growth factor by hypoxia is modulated by a phosphatidylinositol 3-kinase/ Akt signaling pathway in Ha-ras-transformed cells through a hypoxia inducible factor-1 transcriptional element. Blood, 90: 3322-3331, 1997.
30. Levy, A. P., Levy, N. S., and Goldberg, M. A. Post-transcriptional regulation of vascular endothelial growth factor by hypoxia. J. Biol. Chem., 271: 2746-2753, 1996.
31. Stein, I., Neeman, M., Shweiki, D., Itin, A., and Keshet, E. Stabilization of vascular endothelial growth factor mRN A by hypoxia and hypoglycemia and coregulation with other ischemia-induced genes. Mol. Cell. Biol., 15: 5363-5368, 1995.
32. Levy, A. P., Levy, N. S., Iliopoulos, O., Jiang, C., Kaplin, W. G., Jr., and Goldberg, M. A. Regulation of vascular endothelial growth factor by hypoxia and its modulation by the von Hippel-Lindau tumor suppressor gene. Kidney Int., 51: 575-578, 1997.
33. Dibbens, J. A., Miller, D. L., Damert, A., Risau, W., Vadas, M. A., and Goodall, G. J. Hypoxic regulation of vascular endothelial growth factor mRNA stability requires the cooperation of multiple RNA elements. Mol. Biol. Cell, 10: 907-919, 1999.
34. Kevil, C. G., De Benedetti, A., Payne, D. K., Coe, L. L., Laroux, F. S., and Alexander, J. S. Translational regulation of vascular permeability factor by eukaryotic initiation factor 4E: implications for tumor angiogenesis. Int. J. Cancer, 65: 785-790, 1996.
35. Stein, I., Itin, A., Einat, P., Skaliter, R., Grossman, Z., and Keshet, E. Translation of vascular endothelial growth factor mRNA by internal ribosome entry: implications for translation under hypoxia. Mol. Cell. Biol., 18: .3112-3119, 1998.
36. Akiri, G., Nahari, D., Finkelstein, Y., Le, S. Y., Elroy-Stein, O., and Levi, B. Z. Regulation of vascular endothelial growth factor (VEGF) expression is mediated by internal initiation of translation and alternative initiation of transcription. Oncogene, 17: 227-236, 1998.
37. Scott, P. A., Smith, K., Poulsom, R., De Benedetti, A., Bicknell, R., and Harris, A. L. Differential expression of vascular endothelial growth factor mRNA versus protein isoform expression in human breast cancer and relationship to eIF-4E. Br. J. Cancer, 77: 2120-2128, 1998.
38. Ferrara, N., and Davis-Smyth, T. The biology of vascular endothelial growth factor. Endocr. Rev., 18: 4-25, 1997.
39. Dudley, D. T., Pang, L., Decker, S. J., Bridges, A. J., and Saltiel, A. R. A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci, USA, 92: 7686-7689, 1995.
40. Alessi, D. R., Cuenda, A., Cohen, P., Dudley, D. T., and Saltiel, A. R. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J. Biol. Chem., 270: 27489-27494, 1995.
41. Buick, R. N., Filmus, J., and Quaroni, A. Activated H-ras transforms rat intestinal epithelial cells with expression of α-TGF. Exp. Cell Res., 170: 300-309, 1987.
42. Bouck, N., Stellmach, V., and Hsu, S. C. How tumors become angiogenic. Adv. Cancer Res., 69: 135-174, 1996.
43. Hanahan, D., and Folkman, J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell, 86: 353-364, 1996.
44. Jamal, H., Cano-Gauci, D. F., Buick, R. N., and Filmus, J. Activated ras and src induce CD44 overexpression in rat intestinal epithelial cells. Oncogene, 9: 417-423, 1994.
45. Mukhopadhyay, D., Tsiokas, L., Zhou, X-M., Foster, D., Brugge, J. S., and Sukhatme, V. P. Hypoxic induction of human vascular endothelial growth factor expression through c-Src activation. Nature (Lond.), 375: 577-581, 1995.
46. Ellis, L. M., Staley, C. A., Liu, W., Fleming, R. Y., Parikh, N. U., Bucana, C. D., and Gallick, G. E. Down-regulation of vascular endothelial growth factor in a human colon carcinoma cell line transfected with an antisense expression vector specific for c-src. J. Biol. Chem., 273: 1052-1057, 1998.
47. Jiang, B. H., Agani, F., Passaniti, A., and Semenza, G. L. V-SRC induces expression of hypoxia-inducible factor 1 (HlF-I) and transcription of genes encoding vascular endothelial growth factor and enolase 1: involvement of HIF-I in tumor progression. Cancer Res., 57: 5328-5335, 1997.
48. Dameron, K. M., Volpert, O. V., Tainsky, M. A., and Bouck, N. Control of angiogenesis in fibroblasts by p53 regulation of thrombospondin-1. Science (Washington DC), 265: 1582-1584, 1994.
49. Volpert, O. V., Dameron, K. M., and Bouck, N. Sequential development of an angiogenic phenotype by human fibroblasts progressing to tumorigenicity. Oncogene, 14: 1495-1502, 1997.
50. Koura, A. N., Liu, W., Kitadai, Y., Singh, R. K., Radinsky, R., and Ellis, L. M. Regulation of vascular endothelial growth factor expression in human colon carcinoma cells by cell density. Cancer Res., 56: 3891-3894, 1996.
51. Cowley, S., Paterson, H., Kemp, P., and Marshall, C. J. Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH 3T3 cells. Cell, 77: 841-852, 1994.
52. Leevers, S. J., Paterson, H. F., and Marshall, C. J. Requirement for ras in raf activation is overcome by targeting raf to the plasma membrane. Nature (Lond.), 369: 411-414, 1994.
53. Stokoe, D., Macdonald, S. G., Cadwallader, K., Symons, M., and Hancock, J. F. Activation of Raf as a result of recruitment to the plasma membrane. Science (Washington DC), 264: 1463-1467, 1994.
54. Brunet, A., Pages, G., and Pouyssegur, J. Constitutively active mutants of MAP kinase kinase (MEK1) induce growth factor-relaxation and oncogenicity when expressed in fibroblasts. Oncogene. 9: 3379-3387, 1994.
55. Rosen, K., Rak, J., Jin, J., Kerbel, R. S., Newman, M. J., and Filmus, J. Down-regulation of Bak plays a critical role in the growth of the ras-induced malignant phenotype in intestinal epithelial cells. Curr. Biol., 8: 1331-1334, 1998.
56. Vlahos, C. J., Matter, W. F., Hui, K. Y., and Brown, R. F. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem., 269: 5241-5248, 1994.
57. Pennisi, E. Superoxides relay Ras protein's oncogenic message. Science (Washington DC), 275: 1567-1568, 1997.
58. Kuroki, M., Voest, E. E., Amano, S., Beerepoot, L. V., Takashima, S., Tolentino, M., Kim, R. Y., Rohan, R. M., Colby, K. A., Yeo, K. T., and Adamis, A. P. Reactive oxygen intermediates increase vascular endothelial growth factor expression in vitro and in vivo. J. Clin. Investig., 98: 1667-1675, 1996.
59. Milanini, J., Vinals, F., Pouyssegur, J., and Pages, G. p42/p44 MAP kinase module plays a key role in the transcriptional regulation of the vascular endothelial growth factor gene in fibroblasls. J. Biol. Chem., 273: 18165-18172, 1998.
60. Rakb J.b Filmus, J., Finkenzeller, G., Grugel, S., Manne, D., and Kerbel, R. S. Oncogenes as inducers of tumor angiogenesis. Cancer Metastasis Rev., 14: 263-277, 1995.
61. Enholm, B., Paavonen, K., Ristimaki, A., Kumar, V., Gunji, Y., Klefstrom, J., Kivinen, L., Laiho, M., Olofsson, B., Joukov, V., Eriksson, U., and Alitalo, K. Comparison of VEGF, VEGF-B, VEGF-C and Ang-1 mRNA regulation by serum, growth factors, oncoproteins and hypoxia. Oncogene, 14: 2475-2483, 1997.
62. Ogiso, Y., Hwang, Y. W., Shih, T. Y., and Kuzumaki, N. Biological activity of a K-ras mutant that contains the 12R/59T/116Y mutations. Cancer Lett., 75: 19-26, 1993.
63. Larcher, F., Robles, A. I., Duran, H., Murillas, R., Quintanilla, M., Cano, A., Conti, C. J., and Jorcano, J. L. Up-regulation of vascular endothelial growth factor/vascular permeability factor in mouse skin carcinogenesis correlates with malignant progression state and activated H-ras expression levels. Cancer Res., 56: 5391-5396, 1996.
64. Arbiser, J. L., Moses, M. A., Fernandez, C. A., Ghiso, N., Cao, Y., Klauber, N., Frank, D., Brownlee, M., Flynn, E., Parangi, S., Byers, H. R., and Folkman, J. Oncogenic H-ras stimulates tumor angiogenesis by two distinct pathways. Proc. Natl. Acad. Sci. USA. 94: 861-866, 1997.
65. Mazure, N. M., Chen, E. Y., Yeh, P., Laderoute, K. R., and Giaccia, A. J. Oncogenic transformation and hypoxia synergistically act to modulate vascular endothelial growth factor expression. Cancer Res., 56: 3436-3440, 1996.
66. Feldkamp, M. M., Lau, N., Rak, J., Kerbel, R. S., and Guha, A. Normoxic and hypoxic regulation of vascular endothelial growth factor (VEGF) by astrocytoma cells is mediated by Ras. Int. J. Cancer, 81: 118-124, 1999.
67. Kelly, G. S. Clinical applications of N-acetylcysteine. Altern. Med. Rev., 3: 114-127, 1998.
68. Hanahan, D. Signaling vascular morphogenesis and maintenance. Science (Washington DC), 277: 48-50, 1997.
69. Perrotte, P., Matsumolo, T., Inoue, K., Kuniyasu, H., Eve, B. Y., Hicklin, D. J., Radinsky, R., and Dinney, C. P. Anti-epidermal growth factor receptor antibody C225 inhibits angiogenesis in human transitional cell carcinoma growing orthotopically in nude mice. Clin. Cancer Res., 5: 257-265, 1999.
70. Zabrenetzky, V., Harris, C. C., Steeg, P. S., and Roberts, D. D. Expression of the extracellular matrix molecule thrombospondin inversely correlates with malignant progression in melanoma, lung and breast carcinoma cell lines. Int. J. Cancer, 59: 191-195, 1994.
71. Stack, J. L., and Bornstein, P. Transformation by v-src causes transient induction followed by repression of mouse thrombospondin-1. Cell Growth Differ., 5: 1373-1380, 1994.