Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: Role of oxygenation, angiopoietin-1, and matrix metalloproteinases

Cancer Cell

Volumn 6, Issue 6, 2004, Pages 553-563

  Winkler, Frank ^a   Kozin, Sergey V ^a   Tong, Ricky T ^a   Chae, Sung Suk ^a   Booth, Michael F ^a   Garkavtsev, Igor ^a   Xu, Lei ^a   Hicklin, Daniel J ^b   Fukumura, Dai ^a   Di Tomaso, Emmanuelle ^a   Munn, Lance L ^a   Jain, Rakesh K ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b ELI LILLY AND COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN 1; MATRIX METALLOPROTEINASE; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANTIBODY SPECIFICITY; ARTICLE; BASEMENT MEMBRANE; BRAIN BLOOD VESSEL; BRAIN TUMOR; HUMAN; KINETICS; OXYGENATION; PERICYTE; PRIORITY JOURNAL; RADIATION RESPONSE; REDUCTION; TUMOR CELL; UPREGULATION;

EID: 19944422751     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2004.10.011     Document Type: Article

References (50)

1. Baluk P., Morikawa S., Haskell A., Mancuso M., McDonald D.M. Abnormalities of basement membrane on blood vessels and endothelial sprouts in tumors. Am. J. Pathol. 163:2003;1801-1815
2. Benjamin L.E., Golijanin D., Itin A., Pode D., Keshet E. Selective ablation of immature blood vessels in established human tumors follows vascular endothelial growth factor withdrawal. J. Clin. Invest. 103:1999;159-165
3. Bottaro D.P., Liotta L.A. Cancer. Out of air is not out of action Nature. 423:2003;593-595
4. Brown E.B., Campbell R.B., Tsuzuki Y., Xu L., Carmeliet P., Fukumura D., Jain R.K. In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy. Nat. Med. 7:2001;864-868
5. Carmeliet P., Jain R.K. Angiogenesis in cancer and other diseases. Nature. 407:2000;249-257
6. Cho C.H., Kammerer R.A., Lee H.J., Yasunaga K., Kim K.T., Choi H.H., Kim W., Kim S.H., Park S.K., Lee G.M., Koh G.Y. Designed angiopoietin-1 variant, COMP-Ang1, protects against radiation-induced endothelial cell apoptosis. Proc. Natl. Acad. Sci. USA. 101:2004;5553-5558
7. Dvorak H.F. Vascular permeability factor/vascular endothelial growth factor. A critical cytokine in tumor angiogenesis and a potential target for diagnosis and therapy J. Clin. Oncol. 20:2002;4368-4380
8. Farkas E., De Jong G.I., de Vos R.A., Jansen Steur E.N., Luiten P.G. Pathological features of cerebral cortical capillaries are doubled in Alzheimer's disease and Parkinson's disease. Acta Neuropathol. (Berl.). 100:2000;395-402
9. Ferrara N., Hillan K.J., Gerber H.P., Novotny W. Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nat. Rev. Drug Discov. 3:2004;391-400
10. Garcia-Barros M., Paris F., Cordon-Cardo C., Lyden D., Rafii S., Haimovitz-Friedman A., Fuks Z., Kolesnick R. Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science. 300:2003;1155-1159
11. 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., Weichselbaum R.R. Potentiation of the antitumor effect of ionizing radiation by brief concomitant exposures to angiostatin. Cancer Res. 58:1998;5686-5689
12. Hall E.J. The oxygen effect and reoxygenation. Hall E.J. Radiobiology for the Radiologist. 2000;91-111 JB Lippincott, Philadelphia
13. Hawighorst T., Skobe M., Streit M., Hong Y.K., Velasco P., Brown L.F., Riccardi L., Lange-Asschenfeldt B., Detmar M. Activation of the tie2 receptor by angiopoietin-1 enhances tumor vessel maturation and impairs squamous cell carcinoma growth. Am. J. Pathol. 160:2002;1381-1392
14. Hiratsuka S., Nakamura K., Iwai S., Murakami M., Itoh T., Kijima H., Shipley J.M., Senior R.M., Shibuya M. MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer Cell. 2:2002;289-300
15. Holash J., Maisonpierre P.C., Compton D., Boland P., Alexander C.R., Zagzag D., Yancopoulos G.D., Wiegand S.J. Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF. Science. 284:1999;1994-1998
16. Hurwitz H., Fehrenbacher L., Novotny W., Cartwright T., Hainsworth J., Heim W., Berlin J., Baron A., Griffing S., Holmgren E., et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N. Engl. J. Med. 350:2004;2335-2342
17. Inai T., Mancuso M., Hashizume H., Baffert F., Haskell A., Baluk P., Hu-Lowe D.D., Shalinsky D.R., Thurston G., Yancopoulos G.D., McDonald D.M. Inhibition of vascular endothelial growth factor (VEGF) signaling in cancer causes loss of endothelial fenestrations, regression of tumor vessels, and appearance of basement membrane ghosts. Am. J. Pathol. 165:2004;35-52
18. Jain R.K. Normalizing tumor vasculature with anti-angiogenic therapy. A new paradigm for combination therapy Nat. Med. 7:2001;987-989
19. Jain R.K. Molecular regulation of vessel maturation. Nat. Med. 9:2003;685-693
20. Jain R.K., Munn L.L. Leaky vessels? Call Ang. 1(Nat. Med. 6):2000;131-132
21. Kadambi A., Mouta C.C., Yun C.O., Padera T.P., Dolmans D.E., Carmeliet P., Fukumura D., Jain R.K. Vascular endothelial growth factor (VEGF)-C differentially affects tumor vascular function and leukocyte recruitment. Role of VEGF-receptor 2 and host VEGF-A Cancer Res. 61:2001;2404-2408
22. Kerbel R., Folkman J. Clinical translation of angiogenesis inhibitors. Nat. Rev. Cancer. 2:2002;727-739
23. Koga K., Todaka T., Morioka M., Hamada J., Kai Y., Yano S., Okamura A., Takakura N., Suda T., Ushio Y. Expression of angiopoietin-2 in human glioma cells and its role for angiogenesis. Cancer Res. 61:2001;6248-6254
24. Kozin S.V., Boucher Y., Hicklin D.J., Bohlen P., Jain R.K., Suit H.D. Vascular endothelial growth factor receptor-2-blocking antibody potentiates radiation-induced long-term control of human tumor xenografts. Cancer Res. 61:2001;39-44
25. Kwak H.J., Lee S.J., Lee Y.H., Ryu C.H., Koh K.N., Choi H.Y., Koh G.Y. Angiopoietin-1 inhibits irradiation- and mannitol-induced apoptosis in endothelial cells. Circulation. 101:2000;2317-2324
26. 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., Boucher Y. Anti-vascular endothelial growth factor treatment augments tumor radiation response under normoxic or hypoxic conditions. Cancer Res. 60:2000;5565-5570
27. Lee S.W., Kim W.J., Choi Y.K., Song H.S., Son M.J., Gelman I.H., Kim Y.J., Kim K.W. SSeCKS regulates angiogenesis and tight junction formation in blood-brain barrier. Nat. Med. 9:2003;900-906
28. Ma J., Pulfer S., Li S., Chu J., Reed K., Gallo J.M. Pharmacodynamic- mediated reduction of temozolomide tumor concentrations by the angiogenesis inhibitor TNP-470. Cancer Res. 61:2001;5491-5498
29. 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., et al. Combined effects of angiostatin and ionizing radiation in antitumour therapy. Nature. 394:1998;287-291
30. Millauer B., Shawver L.K., Plate K.H., Risau W., Ullrich A. Glioblastoma growth inhibited in vivo by a dominant-negative Flk-1 mutant. Nature. 367:1994;576-579
31. Murata R., Nishimura Y., Hiraoka M. An antiangiogenic agent (TNP-470) inhibited reoxygenation during fractionated radiotherapy of murine mammary carcinoma. Int. J. Radiat. Oncol. Biol. Phys. 37:1997;1107-1113
32. Plate K.H., Breier G., Weich H.A., Risau W. Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature. 359:1992;845-848
33. Rampling R., Cruickshank G., Lewis A.D., Fitzsimmons S.A., Workman P. Direct measurement of pO2 distribution and bioreductive enzymes in human malignant brain tumors. Int. J. Radiat. Oncol. Biol. Phys. 29:1994;427-431
34. Rofstad E.K., Henriksen K., Galappathi K., Mathiesen B. Antiangiogenic treatment with thrombospondin-1 enhances primary tumor radiation response and prevents growth of dormant pulmonary micrometastases after curative radiation therapy in human melanoma xenografts. Cancer Res. 63:2003;4055-4061
35. Song H.S., Son M.J., Lee Y.M., Kim W.J., Lee S.W., Kim C.W., Kim K.W. Oxygen tension regulates the maturation of the blood-brain barrier. Biochem. Biophys. Res. Commun. 290:2002;325-331
36. Stoeltzing O., Ahmad S.A., Liu W., McCarty M.F., Wey J.S., Parikh A.A., Fan F., Reinmuth N., Kawaguchi M., Bucana C.D., Ellis L.M. Angiopoietin-1 inhibits vascular permeability, angiogenesis, and growth of hepatic colon cancer tumors. Cancer Res. 63:2003;3370-3377
37. Stratmann A., Risau W., Plate K.H. Cell type-specific expression of angiopoietin-1 and angiopoietin-2 suggests a role in glioblastoma angiogenesis. Am. J. Pathol. 153:1998;1459-1466
38. Sweeney P., Karashima T., Kim S.J., Kedar D., Mian B., Huang S., Baker C., Fan Z., Hicklin D.J., Pettaway C.A., Dinney C.P. Anti-vascular endothelial growth factor receptor 2 antibody reduces tumorigenicity and metastasis in orthotopic prostate cancer xenografts via induction of endothelial cell apoptosis and reduction of endothelial cell matrix metalloproteinase type 9 production. Clin. Cancer Res. 8:2002;2714-2724
39. Teicher B.A., Holden S.A., Ara G., Dupuis N.P., Liu F., Yuan J., Ikebe M., Kakeji Y. Influence of an anti-angiogenic treatment on 9L gliosarcoma. Oxygenation and response to cytotoxic therapy Int. J. Cancer. 61:1995;732-737
40. Thurston G., Suri C., Smith K., McClain J., Sato T.N., Yancopoulos G.D., McDonald D.M. Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science. 286:1999;2511-2514
41. Thurston G., Rudge J.S., Ioffe E., Zhou H., Ross L., Croll S.D., Glazer N., Holash J., McDonald D.M., Yancopoulos G.D. Angiopoietin-1 protects the adult vasculature against plasma leakage. Nat. Med. 6:2000;460-463
42. Tong R.T., Boucher Y., Kozin S.V., Winkler F., Hicklin D.J., Jain R.K. Vascular normalization by vascular endothelial growth factor receptor 2 blockade induces a pressure gradient across the vasculature and improves drug penetration in tumors. Cancer Res. 64:2004;3731-3736
43. Tournaire R., Simon M.P., le Noble F., Eichmann A., England P., Pouyssegur J. A short synthetic peptide inhibits signal transduction, migration and angiogenesis mediated by Tie2 receptor. EMBO Rep. 5:2004;262-267
44. Tsilibary E.C. Microvascular basement membranes in diabetes mellitus. J. Pathol. 200:2003;537-546
45. Uemura A., Ogawa M., Hirashima M., Fujiwara T., Koyama S., Takagi H., Honda Y., Wiegand S.J., Yancopoulos G.D., Nishikawa S. Recombinant angiopoietin-1 restores higher-order architecture of growing blood vessels in mice in the absence of mural cells. J. Clin. Invest. 110:2002;1619-1628
46. Wachsberger P., Burd R., Dicker A.P. Tumor response to ionizing radiation combined with antiangiogenesis or vascular targeting agents. Exploring mechanisms of interaction Clin. Cancer Res. 9:2003;1957-1971
47. Willett C.G., Boucher Y., di Tomaso E., Duda D.G., Munn L.L., Tong R.T., Chung D.C., Sahani D.V., Kalva S.P., Kozin S.V., et al. Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nat. Med. 10:2004;145-147
48. Yuan F., Salehi H.A., Boucher Y., Vasthare U.S., Tuma R.F., Jain R.K. Vascular permeability and microcirculation of gliomas and mammary carcinomas transplanted in rat and mouse cranial windows. Cancer Res. 54:1994;4564-4568
49. Yuan F., Chen Y., Dellian M., Safabakhsh N., Ferrara N., Jain R.K. Time-dependent vascular regression and permeability changes in established human tumor xenografts induced by an anti-vascular endothelial growth factor/vascular permeability factor antibody. Proc. Natl. Acad. Sci. USA. 93:1996;14765-14770
50. Zips D., Krause M., Hessel F., Westphal J., Bruchner K., Eicheler W., Dorfler A., Grenman R., Petersen C., Haberey M., Baumann M. Experimental study on different combination schedules of VEGF-receptor inhibitor PTK787/ZK222584 and fractionated irradiation. Anticancer Res. 23:2003;3869-3876