Bcl-2 overexpression and hypoxia synergistically act to modulate vascular endothelial growth factor expression and in vivo angiogenesis in a breast carcinoma line

FASEB Journal

Volumn 14, Issue 5, 2000, Pages 652-660

  Biroccio, Annamaria ^a   Candiloro, Antonio ^a   Mottolese, Marcella ^a   Sapora, Orazio ^b   Albini, Adriana ^c   Zupi, Gabriella ^a   Del Bufalo, Donatella ^a  

^a REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^c UNIVERSITY OF GENOA   (Italy)

Author keywords

In vivo matrigel assay; MCF7 ADR; Metastasis

Indexed keywords

PROTEIN BCL 2; VASCULOTROPIN;

ANGIOGENESIS; APOPTOSIS; ARTICLE; BREAST CARCINOGENESIS; BREAST CARCINOMA; CONTROLLED STUDY; DISEASE ASSOCIATION; HUMAN; HUMAN CELL; HYPOXIA; METASTASIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS REGULATION;

EID: 0034120314     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.14.5.652     Document Type: Article

References (47)

1. Adams, J. M., and Cory, S. (1998) The bcl-2 protein family: arbiters of cell survival. Science 281, 1322-1326
2. Kroemer, G. (1997) The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nature Med. 3, 614-620
3. 1 and sensitizes human testicular germ cell tumours to chemotherapy-induced apoptosis. Oncogene 18, 1457-1464
4. Cheng, E. H. Y., Kirsch, D. G., Clem, R. J., Ravi, R., Kastan, M. B., Bedi, A., Ueno, K., and Hardwick, J. M. (1997) Conversion of Bcl-2 to a Bax-like death effector by caspases. Science 278, 1966-1968
5. Uhlmann, E. J., Subramanian, T., Vater, C. A., Lutz, R., and Chinnadurai, G. (1998) A potent cell death activity associated with transient high level expression of BCL-2. J. Biol. Chem. 273, 17926-17932
6. Vaux, D. L., Cory, S., and Adams, J. M. (1988) Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature (London) 335, 440-442
7. Strasser, A., Harris, A. W., and Cory, S. (1993) E μ-bcl-2 transgene facilitates spontaneous transformation of early pre-B and immunoglobulin-secreting cells but not T cells. Oncogene 8, 1-9
8. Reed, J. C., Cuddy, M., Slabiaak, T., Croce, C. M., and Nowell, P. (1988) Oncogenic potential of bcl-2 demonstrated by gene transfer. Nature (London) 336, 259-261
9. Jager, R., Herzer, U., Schenkel, J., and Weiher, H. (1997) Overexpression of Bcl-2 inhibits alveolar cell apoptosis during involution and accelerates c-myc-induced tumorigenesis of the mammary gland in transgenic mice. Oncogene 15, 1787-1795
10. Uhlmann, E. J., D'Sa-Eipper, C., Subramanian, T., Wagner, A. J., Hay, N., and Chinnadurai, G. (1996) Deletion of a nonconserved region of Bcl-2 confers a novel gain of function: suppression of apoptosis with concomitant cell proliferation. Cancer Res. 56, 2506-2509
11. Basolo, F., Fiore, L., Fusco, A., Giannini, R., Albini, A., Merlo, G. R., Fontanini, G., Conaldi, P. G., and Toniolo, A. (1999) Potentiation of the malignant phenotype of the undifferentiated ARO thyroid cell line by insertion of the bcl-2 gene. Int. J. Cancer 81, 956-962
12. Takaoka, A., Adachi, M., Okuda, H., Sato, S., Yawata, A., Hinoda, Y., Takayama, S., Reed, J. C., and Imai, K. (1997) Anti-cell death activity promotes pulmonary metastasis of melanoma cells. Oncogene 14, 2971-2977
13. Del Bufalo, D., Biroccio, A., Leonetti, C., and Zupi, G. (1997) Bcl-2 overexpression enhances the metastatic potential of a human breast cancer line. FASEB J. 11, 947-953
14. Folkman, J. (1986) How is blood vessel growth regulated in normal and neoplastic tissue? G. H. A. Clowes Memorial Award lecture. Cancer Res. 46, 467-473
15. Gimbrone, M. A., Leapman, S. B., Cotran, R. S., and Folkman, J. (1972) Tumor dormancy in vivo by prevention of neovascularization. J. Exp. Med. 136, 261-276
16. Fidler, I. J., and Ellis, L. M. (1994) The implications of angiogenesis to the biology and therapy of cancer metastasis. Cell 79, 185-188
17. Ellis, L. M., and Fidler, I. J. (1996) Angiogenesis and metastasis. Eur. J. Cancer 32A:2451-2460
18. Liotta, L. A., Kleinerman, J., and Saidel, G. M. (1974) Quantitative relationships of intravascular tumor cells, tumor vessels, and pulmonary metastases following tumor implantation. Cancer Res. 34, 997-1003
19. Gasparini, G., Fox, S. B., Verderio, P., Bonoldi, E., Bevilacqua, P., Boracchi, P., Dante, S., Marubini, E., and Harris, A. L. (1996) Determination of angiogenesis adds information to estrogen receptor status in predicting the efficacy of adjuvant tamoxifen in node-positive breast cancer patients. Clin. Cancer Res. 2, 1191-1198
20. Horak, E. R., Leck, R., Klenk, N., LeJeune, S., Smith, K., Stuart, N., Greenall, M., Stepniewska, K., and Harris, A. L. (1992) Angiogenesis, assessed by platelet/endothelial cell adhesion molecule antibodies, as an indicator of node metastases and survival in breast cancer. Lancet 340, 1120-1124
21. Folkman, J., and Shing, Y. (1992) Angiogenesis. J. Biol. Chem. 267, 10931-10934
22. Folkman, J. (1995) Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1, 27-31
23. Risau, W., Drexler, H., Mironov, V., Smits, A., Siegbahn, A., Funa, K., and Heldin, C.-H. (1992) Platelet-derived growth factor is angiogenic in vivo. Growth Factors 7, 261-266
24. Mukhopadhyay, D., Tsiokas, L., Zhou, X., Foster, D., Brugge, J. S., and Sukhatme, V. P. (1995) Hypoxic induction of human vascular endothelial growth factor expression through c-Src activation. Nature (London) 375, 577-581
25. Grugel, S., Finkenzeller, G., Weindel, K., Barleon, B., and Marme, D. (1995) Both v-H-ras and v-raf stimulate expression of the vascular endothelial growth factor in NIH 3T3 cells. J. Biol. Chem. 270, 25915-25919
26. Kieser, A., Welch, H. A., Brandner, G., Marme, D., and Kolch, W. (1994) Mutant p53 potentiates protein kinase C induction of vascular endothelial growth factor expression. Oncogene 9, 963-969
27. Giaccia, A. J. (1996) Oncogenic transformation and hypoxia synergistically act to modulate vascular endothelial growth factor expression. Cancer Res. 56, 3436-3440
28. Plate, K. H., Breier, G., Weich, H. A., and Risau, W. (1992) Vascular endothelial growth factor is a potential tumor angiogenesis factor in human gliomas in vivo. Nature (London) 359, 845-848
29. Shweiki, D., Itin, A., Soffer, D., and Keshet, E. (1992) Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature (London) 359, 843-845
30. Graeber, T. G., Osmanian, C., Jacks, T., Housman, D. E., Koch, C. J., and Giaccia, A. J. (1996) Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature (London) 379, 88-91
31. Sapora, O., Barone, F., Belli, M., Maggi, A., Quintiliani, M., and Tabocchini, M. A. (1991) Relationship between cell killing, mutation induction and DNA damage in X-irradiated V79 cells: influence of oxygen and DMSO. Int. J. Radiat. Biol. 60, 467-482
32. Boocock, C. A., Charnock, D. S., Sharkey, A. M., McLaren, J., Barker, P. J., Wright, K. A., Twentyman, P. R., and Smith, S. K. (1995) Expression of vascular endothelial growth factor and its receptors flt and KDR in ovarian carcinoma. J. Natl. Cancer Inst. 87, 506-516
33. Viglietto, G., Maglione, D., Rambaldi, M., Cerutti, J., Romano, A., Trapasso, F., Fedele, M., Ippolito, P., Chiappetta, G., Botti, G., Fusco, A., and Pesico, G. (1995) Upregulation of vascular endothelial growth factor (VEGF) and downregulation of placenta growth factor (PIGF) associated with malignancy in human thyroid tumors and cell lines. Oncogene 11, 1569-1579
34. Leonetti, C., Biroccio, A., Candiloro, A., Citro, G., Fornari, C., Mottolese, M., Del Bufalo, D., and Zupi, G. (1999) Increase of cisplatin sensitivity by c-myc antisense oligodeoxynucleotides in a human metastatic melanoma inherently resistant to cisplatin. Clin. Cancer Res. 5, 2588-2595
35. Weidner, N., Semple J. P., Welch, W. R., and Folkman, J. (1991) Tumor angiogenesis and metastasis-correlation in invasive breast carcinoma. N. Engl. J. Med. 324, 1-8
36. Del Bufalo, D., Biroccio, A., Soddu, S., Laudonio, N., D'Angelo, C., Sacchi, A., and Zupi, G. (1996) Lonidamine induces apoptosis in drug-resistant cells independently of the p53 gene. J. Clin. Invest. 98, 1165-1173
37. Albini, A., Soldi, R., Giunciuglio, D., Giraudo, E., Benelli, R., Primo, L., Noonan, D., Salio, M., Camussi, G., Rockl, W., and Bussolino, F. (1996) The angiogenesis induced by HIV-1 tat protein is mediated by the Flk-1/KDR receptor on vascular endothelial cells. Nat. Med. 2, 1371-1375
38. Goldberg, M. A., and Schneider, T. J. (1994) Similarities between the oxygen-sensing mechanisms regulating the expression of vascular endothelial growth factor and erythropoietin. J. Biol. Chem. 269, 4355-4361
39. Harris, A. L., Zhang, H., Moghddam, A., Fox, S., Scott, P., Pattison, A., Gatter, K., Stratford, I., and Bicknell, R. (1996) Breast cancer angiogenesis-new approaches to therapy via antiangiogenesis, hypoxic activated drugs, and vascular targeting. Breast Cancer Res. Treat. 38, 97-108
40. Ryan, J. J., Prochownik, E., Gottlieb, C. A., Apel, I. J., Merino, R., Nunez, G., and Clarke, M. F. (1994) c-myc and bcl-2 modulate p53 function by altering p53 subcellular trafficking during the cell cycle. Proc. Natl. Acad. Sci. USA 91, 5878-5882
41. Riccioni, T., Cirielli, C., Wang, X., Passaniti, A., and Capogrossi, M. C. (1998) Adenovirus-mediated wild-type p53 overexpression inhibits endothelial cell differentiation in vitro and angiogenesis in vivo. Gene Ther. 5, 747-754
42. Bouvet, M., Ellis, L. M., Nishizaki, M., Fujiwara, T., Liu, W., Bucana, C. D., Fang, B., Lee, J. J., and Roth, J. A. (1998) Adenovirus-mediated wild-type p53 gene transfer down-regulates vascular endothelial growth factor expression and inhibits angiogenesis in human colon cancer. Cancer Res. 58, 2288-2292
43. Biroccio, A., Del Bufalo, D., Fanciulli, M., Bruno. T., Zupi, G., and Floridi, A. (1999) Bcl-2 inhibits mitochondrial metabolism and Ionidamine-induced apoptosis in adriamycin-resistant MCF7 cells. Int. J. Cancer 82, 125-130
44. Mandriota, S. J., Seghezzi, G., Vassalli, J.-D., Ferrara, N., Wasi, S., Mazzieri, R., Mignatti, P., and Pepper, M. S. (1990) Vascular endothelial growth factor increases urokinase receptor expression in vascular endothelial cells. J. Biol. Chem. 270, 9709-9716
45. Pepper, M. S., and Montesano, R. (1990) Proteolytic balance and capillary morphogenesis. Cell Differ. Dev. 32, 319-327
46. Wang, H., and Keiser, J. A. (1998) Vascular endothelial growth factor upregulates the expression of matrix metalloproteinases in vascular smooth muscle cells: role of flt-1. Circ. Res. 83, 832-840
47. Nör, J. E., Christensen, J., Mooney, D. J., and Polverini, P. J. (1999) Vascular endothelial growth factor (VEGF)-mediated angiogenesis is associated with enhanced endothelial cell survival and induction of bcl-2 expression. Am. J. Pathol. 154, 375-394