Irradiation-induced angiogenesis through the up-regulation of the nitric oxide pathway: Implications for tumor radiotherapy

Cancer Research

Volumn 63, Issue 5, 2003, Pages 1012-1019

  Sonveaux, Pierre ^a   Brouet, Agnès ^a   Havaux, Xavier ^b   Grégoire, Vincent ^b   Dessy, Chantal ^a   Balligand, Jean Luc ^a   Feron, Olivier ^a,b  

^a Therapeutics Unit (FATH 5349)   (Belgium)

^b UNIVERSITY OF LOUVAIN MEDICAL SCHOOL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; NITRIC OXIDE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER ADJUVANT THERAPY; CANCER RADIOTHERAPY; CONTROLLED STUDY; ENDOTHELIUM CELL; HEAD AND NECK CARCINOMA; IONIZING RADIATION; LEWIS CARCINOMA; MALE; MOUSE; NONHUMAN; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; TARGET CELL; TUMOR RECURRENCE;

ANIMALS; CARCINOMA, LEWIS LUNG; CARCINOMA, SQUAMOUS CELL; CATTLE; CELL MOVEMENT; COMBINED MODALITY THERAPY; ENDOTHELIUM, VASCULAR; ENZYME ACTIVATION; HUMANS; MALE; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; RNA, MESSENGER; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 0037373834     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (41)

1. Siemann, D. W., Warrington, K. H., and Horsman, M. R. Targeting tumor blood vessels: an adjuvant strategy for radiation therapy. Radiother. Oncol., 57: 5-12, 2000.
2. Gorski, D. H., Beckett, M. A., Jaskowiak, N. T., Calvin, D. P., Mauceri, H. J., Salloum, R. M., Seetharam, S., Koons, A., Haf Hari, D. M., Kufe, D. W., and Weichselbaum, R. R. Blockade of the vascular endothelial growth factor stress response increases the antitumor effects of ionizing radiation. Cancer Res., 59: 3374-3378, 1999.
3. Lee, C. G., Heijn, M., di Tomaso, E., Griffon-Etienne, G., Ancukiewicz, M., Koike, C., Park, K. R., Ferrara, N., Jain, R. K., Suit, H. D., and Boucher, Y. Anti-vascular endothelial growth factor treatment augments tumor radiation response under normoxic or hypoxic conditions. Cancer Res., 60: 5565-5570, 2000.
4. Kozin, S. V., Boucher, Y., Hicklin, D. J., Bohlen, P., Jain, R. K., and Suit, H. D. Vascular endothelial growth factor receptor-2-blocking antibody potentiates radiation-induced long-term control of human tumor xenografts. Cancer Res., 61: 39-44, 2001.
5. Geng, L., Donnelly, E., McMahon, G., Lin, P. C., Sierra-Rivera, E., Oshinka, H., and Hallahan, D. E. Inhibition of vascular endothelial growth factor receptor signaling leads to reversal of tumor resistance to radiotherapy. Cancer Res., 61: 2413-2419, 2001.
6. Griffin, R. J., Williams, B. W., Wild, R., Cherrington, J. M., Park, H., and Song, C. W. Simultaneous inhibition of the receptor kinase activity of vascular endothelial, fibroblast, and platelet-derived growth factors suppresses tumor growth and enhances tumor radiation response. Cancer Res., 62: 1702-1706, 2002.
7. Hess, C., Vuong, V., Hegyi, I., Riesterer, O., Wood, J., Fabbro, D., Glanzmann, C., Bodis, S., and Pruschy, M. Effect of VEGF receptor inhibitor PTK787/ZK222584 [correction of ZK222548] combined with ionizing radiation on endothelial cells and tumour growth. Br. J. Cancer, 85: 2010-2016, 2001.
8. Huang, S. M., Li, J., Armstrong, E. A., and Harari, P. M. Modulation of radiation response and tumor-induced angiogenesis after epidermal growth factor receptor inhibition by ZD1839 (Iressa). Cancer Res., 62: 4300-4306, 2002.
9. Camphausen, K., and Menard, C. Angiogenesis inhibitors and radiotherapy of primary tumours. Expert Opin. Biol, Ther., 2: 477-481, 2002.
10. Gupta, V. K., Jaskowiak, N. T., Beckett, M. A., Mauceri, H. J., Grunstein, J., Johnson, R. S., Calvin, D. A., Nodzenski, E., Pejovic, M., Kufe, D. W., Posner, M. C., and Weichselbaum, R. R. Vascular endothelial growth factor enhances endothelial cell survival and tumor radioresistance. Cancer J., 8: 47-54, 2002.
11. Fukumura, D., Gohongi, T., Kadambi, A., Izumi, Y., Ang, J., Yun, Yuri, C. O., Buerk, D. G., Huang, P. L., and Jain, R. K. Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc. Natl. Acad. Sci. USA, 98: 2604-2609, 2001.
12. Lopez-Ongil, S., Hernandez-Perera, O., Navarro-Antolin, J., Perez, d. L., Rodriguez-Puyol, M., Lamas, S., and Rodriguez-Puyol, D. Role of reactive oxygen species in the signalling cascade of cyclosporine A-mediated up-regulation of eNOS in vascular endothelial cells. Br. J. Pharmacol., 124: 447-454, 1998.
13. Drummond, G. R., Cai, H., Davis, M. E., Ramasamy, S., and Harrison, D. G. Transcriptional and posttranscriptional regulation of endothelial nitric oxide synthase expression by hydrogen peroxide. Circ. Res., 86: 347-354, 2000.
14. Thomas, S. R., Chen, K., and Keaney, J. F., Jr. Hydrogen peroxide activates endothelial nitric-oxide synthase through coordinated phosphorylation and dephosphorylation via a phosphoinositide 3-kinase-dependent signaling pathway. J. Biol. Chem., 277: 6017-6024, 2002.
15. Cai, H., and Harrison, D. G. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ. Res., 87: 840-844, 2000.
16. Taper, H. S., Woolley, G. W., Teller, M. N., and Lardis, M. P. A new transplantable mouse liver tumor of spontaneous origin. Cancer Res., 26: 143-148, 1966.
17. Bertram, J. S., and Janik, P. Establishment of a cloned line of Lewis lung carcinoma cells adapted to cell culture. Cancer Lett., 11: 63-73, 1980.
18. Brouet, A., Sonveaux, P., Dessy, C., Moniotte, S., Balligand, J. L., and Feron, O. Hsp90 and caveolin are key targets for the proangiogenic nitric oxide-mediated effects of statins. Circ. Res., 89: 866-873, 2001.
19. 2+-dependent to the late phosphorylation-dependent activation of the endothelial nitric-oxide synthase in vascular endothelial growth factor-exposed endothelial cells. J. Biol. Chem., 276: 32663-32669, 2001.
20. Dimmeler, S., Dembach, E., and Zeiher, A. M. Phosphorylation of the endothelial nitric oxide synthase at Ser-1177 is required for VEGF-induced endothelial cell migration. FEBS Lett., 477: 258-262, 2000.
21. Navarro-Antolin, J., Rey-Campos, J., and Lamas, S. Transcriptional induction of endothelial nitric oxide gene by cyclosporine A. A role for activator protein-1. J. Biol. Chem., 275: 3075-3080, 2000.
22. Edwards, E., Geng, L., Tan, J., Onishko, H., Donnelly, E., and Hallahan, D. E. Phosphatidylinositol 3-kinase/akt signaling in the response of vascular endothelium to ionizing radiation. Cancer Res., 62: 4671-4677, 2002.
23. Paris, F., Fuks, Z., Kang, A., Capodieci, P., Juan, G., Ehleiter, D., Haimovitz-Friedman, A., Cordon-Cardo, C., and Kolesnick, R. Endothelial apoptosis as the primary lesion initiating intestinal radiation damage in mice. Science (Wash. DC), 293: 293-297, 2001.
24. Folkman, J., and Camphausen, K. Cancer. What does radiotherapy do to endothelial cells? Science (Wash. DC). 293: 227-228, 2001.
25. Lyden, D., Hattori, K., Dias, S., Costa, C., Blaikie, P., Butros, L., Chadbum, A., Heissig, B., Marks, W., Witte, L., Wu, Y., Hicklin, D., Zhu, Z., Hackett, N. R., Crystal, R. G., Moore, M. A., Hajjar, K. A., Manova, K., Benezra, R., and Rafii, S. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat. Med., 7: 1194-1201, 2001.
26. Goepfert, C., Sundberg, C., Sevigny, J., Enjyoji, K., Hoshi, T., Csizmadia, E., and Robson, S. Disordered cellular migration and angiogenesis in cd39-null mice. Circulation, 104: 3109-3115, 2001.
27. Teicher, B. A., Holden, S. A., Ara, G., Dupuis, N. P., Liu, F., Yuan, J., Ikebe, M., and Kakeji, Y. Influence of an anti-angiogenic treatment on 9L gliosarcoma: oxygenation and response to cytotoxic therapy. Int. J. Cancer, 61: 732-737, 1995.
28. Mauceri, H. J., Hanna, N. N., Beckett, M. A., Gorski, D. H., Staba, M. J., Stellato, K. A., Bigelow, K., Heimann, R., Gately, S., Dhanabal, M., Soff, G. A., Sukhatme, V. P., Kufe, D. W., and Weichselbaum, R. R. Combined effects of angiostatin and ionizing radiation in antitumour therapy. Nature (Lond.), 394: 287-291, 1998.
29. Gorski, D. H., Mauceri, H. J., Salloum, R, M., Gately, S., Hellman, S., Beckett, M. A., Sukhatme, V. P., Soff, G. A., Kufe, D. W., and Weichselbaum, R. R. Potentiation of the antitumor effect of ionizing radiation by brief concomitant exposures to angiostatin. Cancer Res., 58: 5686-5689, 1998.
30. Murata, R., Nishimura, Y., and Hiraoka, M. An antiangiogenic agent (TNP-470) inhibited reoxygenation during fractionated radiotherapy of murine mammary carcinoma. Int. J. Radiat. Oncol. Biol. Phys., 37: 1107-1113, 1997.
31. Griscelli, F., Li, H., Cheong, C., Opolon, P., Bennaceur-Griscelli, A., Vassal, G., Soria, J., Soria, C., Lu, H., Perricaudet, M., and Yeh, P. Combined effects of radiotherapy and angiostatin gene therapy in glioma tumor model. Proc. Natl. Acad. Sci. USA, 97: 6698-6703, 2000.
32. Salloum, R. M., Jaskowiak, N. T., Mauceri, H. J., Seetharam, S., Beckett, M. A., Koons, A. M., Hari, D. M., Gupta, V. K., Reimer, C., Kalluri, R., Posner, M. C., Hellman, S., Kufe, D. W., and Weichselbaum, R. R. NM-3, an isocoumarin, increases the antitumor effects of radiotherapy without toxicity. Cancer Res., 60: 6958-6963, 2000.
33. Dent, P., Reardon, D. B., Park, J. S., Bowers, G., Logsdon, C., Valerie, K., and Schmidt-Ullrich, R. Radiation-induced release of transforming growth factor α activates the epidermal growth factor receptor and mitogen-activated protein kinase pathway in carcinoma cells, leading to increased proliferation and protection from radiation-induced cell death. Mol. Biol. Cell, 10: 2493-2506, 1999.
34. Huang, S. M., Bock, J. M., and Harari, P. M. Epidermal growth factor receptor blockade with C225 modulates proliferation, apoptosis, and radiosensitivity in squamous cell carcinomas of the head and neck. Cancer Res., 59: 1935-1940, 1999.
35. Milas, L., Mason, K., Hunter, N., Petersen, S., Yamakawa, M., Ang, K., Mendelsohn, J., and Fan, Z. In vivo enhancement of tumor radioresponse by C225 antiepidermal growth factor receptor antibody. Clin. Cancer Res., 6: 701-708, 2000.
36. Ergun, E., Camphausen, K., and Wein, L. M. Optimal scheduling of radiotherapy and angiogenic inhibitors. Bull. Math. Biol., in press. 2003.
37. Sonveaux, P., Dessy, C., Brouet, A., Jordan, B. F., Gregoire, V., Gallez, B., Balligand, J. L., and Feron, O. Modulation of the tumor vasculature functionality by ionizing radiation accounts for tumor radiosensitization and promotes gene delivery. FASEB J., 16: 1979-1981, 2002.
38. Jordan, B. F., Gregoire, V., Demeure, R. J., Sonveaux, P., Feron, O., O'Hara, J., Vanhulle, V. P., Delzenne, N., and Gallez, B. Insulin increases the sensitivity of tumors to irradiation: involvement of an increase in tumor oxygenation mediated by a nitric oxide-dependent decrease of the tumor cells oxygen consumption. Cancer Res., 62: 3555-3561, 2002.
39. Gallez, B., Jordan, B. F., Baudelet, C., and Misson, P. D. Pharmacological modifications of the partial pressure of oxygen in murine tumors: evaluation using in vivo EPR oximetry. Magn. Reson. Med., 42: 627-630, 1999.
40. Teicher, B. A., Dupuis, N. P., Kuzumoto, T., Robinson, M. F., Liu, F., Menon, K., and Coleman, N. Anti-angiogenic agents can increase tumor oxygenation and response to tumor irradiation. Radiat. Oncol. Investig., 2: 269-276, 1995.
41. Jain, R. K. Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy. Nat. Med., 7: 987-989, 2001.