The Complexity of Translating Anti-angiogenesis Therapy from Basic Science to the Clinic

Developmental Cell

Volumn 37, Issue 2, 2016, Pages 114-125

  Ye, Weilan ^a  

^a GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; VASCULOTROPIN; VASCULOTROPIN A;

ANGIOGENESIS; ANTIANGIOGENIC THERAPY; CANCER CHEMOTHERAPY; CANCER SURVIVAL; HEALTH CARE QUALITY; HUMAN; METASTASIS; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; REVIEW; TUMOR GROWTH; ANIMAL; METABOLISM; NEOPLASM METASTASIS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PATHOLOGY; VASCULARIZATION;

ANGIOGENESIS INHIBITORS; ANIMALS; HUMANS; NEOPLASM METASTASIS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 84963607076     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2016.03.015     Document Type: Review

References (121)

1. Allegra C.J., Yothers G., O'Connell M.J., Sharif S., Petrelli N.J., Colangelo L.H., Atkins J.N., Seay T.E., Fehrenbacher L., Goldberg R.M., et al. Phase III trial assessing bevacizumab in stages II and III carcinoma of the colon: results of NSABP protocol C-08. J. Clin. Oncol. 2011, 29:11-16.
2. Baffert F., Thurston G., Rochon-Duck M., Le T., Brekken R., McDonald D.M. Age-related changes in vascular endothelial growth factor dependency and angiopoietin-1-induced plasticity of adult blood vessels. Circ. Res. 2004, 94:984-992.
3. Bagri A., Berry L., Gunter B., Singh M., Kasman I., Damico L.A., Xiang H., Schmidt M., Fuh G., Hollister B., et al. Effects of anti-VEGF treatment duration on tumor growth, tumor regrowth, and treatment efficacy. Clin. Cancer Res. 2010, 16:3887-3900.
4. Baluk P., Hashizume H., McDonald D.M. Cellular abnormalities of blood vessels as targets in cancer. Curr. Opin. Genet. Dev. 2005, 15:102-111.
5. Beck B., Driessens G., Goossens S., Youssef K.K., Kuchnio A., Caauwe A., Sotiropoulou P.A., Loges S., Lapouge G., Candi A., et al. A vascular niche and a VEGF-Nrp1 loop regulate the initiation and stemness of skin tumours. Nature 2011, 478:399-403.
6. Bellou S., Pentheroudakis G., Murphy C., Fotsis T. Anti-angiogenesis in cancer therapy: Hercules and Hydra. Cancer Lett. 2013, 338:219-228.
7. 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. 1999, 103:159-165.
8. Bennouna J., Sastre J., Arnold D., Osterlund P., Greil R., Van Cutsem E., von Moos R., Vieitez J.M., Bouche O., Borg C., et al. Continuation of bevacizumab after first progression in metastatic colorectal cancer (ML18147): a randomised phase 3 trial. Lancet Oncol. 2013, 14:29-37.
9. Bergers G., Hanahan D. Modes of resistance to anti-angiogenic therapy. Nat. Rev. Cancer 2008, 8:592-603.
10. Blagoev K.B., Wilkerson J., Stein W.D., Motzer R.J., Bates S.E., Fojo A.T. Sunitinib does not accelerate tumor growth in patients with metastatic renal cell carcinoma. Cell Rep. 2013, 3:277-281.
11. Blagoev K.B., Wilkerson J., Stein W.D., Yang J., Bates S.E., Fojo T. Therapies with diverse mechanisms of action kill cells by a similar exponential process in advanced cancers. Cancer Res. 2014, 74:4653-4662.
12. Bouma-ter Steege J.C., Baeten C.I., Thijssen V.L., Satijn S.A., Verhoeven I.C., Hillen H.F., Wagstaff J., Griffioen A.W. Angiogenic profile of breast carcinoma determines leukocyte infiltration. Clin. Cancer Res. 2004, 10:7171-7178.
13. Burger R.A., Brady M.F., Bookman M.A., Fleming G.F., Monk B.J., Huang H., Mannel R.S., Homesley H.D., Fowler J., Greer B.E., et al. Incorporation of bevacizumab in the primary treatment of ovarian cancer. N. Engl. J. Med. 2011, 365:2473-2483.
14. Burotto M., Wilkerson J., Stein W., Motzer R., Bates S., Fojo T. Continuing a cancer treatment despite tumor growth may be valuable: sunitinib in renal cell carcinoma as example. PLoS One 2014, 9:e96316.
15. Cacheux W., Boisserie T., Staudacher L., Vignaux O., Dousset B., Soubrane O., Terris B., Mateus C., Chaussade S., Goldwasser F. Reversible tumor growth acceleration following bevacizumab interruption in metastatic colorectal cancer patients scheduled for surgery. Ann. Oncol. 2008, 19:1659-1661.
16. Calabrese C., Poppleton H., Kocak M., Hogg T.L., Fuller C., Hamner B., Oh E.Y., Gaber M.W., Finklestein D., Allen M., et al. A perivascular niche for brain tumor stem cells. Cancer Cell 2007, 11:69-82.
17. Carmeliet P., Jain R.K. Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nat. Rev. Drug Discov. 2011, 10:417-427.
18. Carmeliet P., Ferreira V., Breier G., Pollefeyt S., Kieckens L., Gertsenstein M., Fahrig M., Vandenhoeck A., Harpal K., Eberhardt C., et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996, 380:435-439.
19. Chen H.X., Cleck J.N. Adverse effects of anticancer agents that target the VEGF pathway. Nat. Rev. Clin. Oncol. 2009, 6:465-477.
20. Chinchar E., Makey K.L., Gibson J., Chen F., Cole S.A., Megason G.C., Vijayakumar S., Miele L., Gu J.W. Sunitinib significantly suppresses the proliferation, migration, apoptosis resistance, tumor angiogenesis and growth of triple-negative breast cancers but increases breast cancer stem cells. Vasc. Cell 2014, 6:12.
21. Chinot O.L., Wick W., Mason W., Henriksson R., Saran F., Nishikawa R., Carpentier A.F., Hoang-Xuan K., Kavan P., Cernea D., et al. Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N. Engl. J. Med. 2014, 370:709-722.
22. Chung A.S., Ferrara N. Developmental and pathological angiogenesis. Annu. Rev. Cell Dev. Biol. 2011, 27:563-584.
23. Chung A.S., Kowanetz M., Wu X., Zhuang G., Ngu H., Finkle D., Komuves L., Peale F., Ferrara N. Differential drug class-specific metastatic effects following treatment with a panel of angiogenesis inhibitors. J. Pathol. 2012, 227:404-416.
24. Conley S.J., Gheordunescu E., Kakarala P., Newman B., Korkaya H., Heath A.N., Clouthier S.G., Wicha M.S. Antiangiogenic agents increase breast cancer stem cells via the generation of tumor hypoxia. Proc. Natl. Acad. Sci. USA 2012, 109:2784-2789.
25. Cooke V.G., LeBleu V.S., Keskin D., Khan Z., O'Connell J.T., Teng Y., Duncan M.B., Xie L., Maeda G., Vong S., et al. Pericyte depletion results in hypoxia-associated epithelial-to-mesenchymal transition and metastasis mediated by met signaling pathway. Cancer Cell 2012, 21:66-81.
26. Currier M.A., Eshun F.K., Sholl A., Chernoguz A., Crawford K., Divanovic S., Boon L., Goins W.F., Frischer J.S., Collins M.H., et al. VEGF blockade enables oncolytic cancer virotherapy in part by modulating intratumoral myeloid cells. Mol. Ther. 2013, 21:1014-1023.
27. de Gramont A., Van Cutsem E., Schmoll H.J., Tabernero J., Clarke S., Moore M.J., Cunningham D., Cartwright T.H., Hecht J.R., Rivera F., et al. Bevacizumab plus oxaliplatin-based chemotherapy as adjuvant treatment for colon cancer (AVANT): a phase 3 randomised controlled trial. Lancet Oncol. 2012, 13:1225-1233.
28. Dikov M.M., Ohm J.E., Ray N., Tchekneva E.E., Burlison J., Moghanaki D., Nadaf S., Carbone D.P. Differential roles of vascular endothelial growth factor receptors 1 and 2 in dendritic cell differentiation. J. Immunol. 2005, 174:215-222.
29. Du Four S., Maenhout S.K., De Pierre K., Renmans D., Niclou S.P., Thielemans K., Neyns B., Aerts J.L. Axitinib increases the infiltration of immune cells and reduces the suppressive capacity of monocytic MDSCs in an intracranial mouse melanoma model. Oncoimmunology 2015, 4:e998107.
30. Dvorak H.F., Brown L.F., Detmar M., Dvorak A.M. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am. J. Pathol. 1995, 146:1029-1039.
31. Eberhard A., Kahlert S., Goede V., Hemmerlein B., Plate K.H., Augustin H.G. Heterogeneity of angiogenesis and blood vessel maturation in human tumors: implications for antiangiogenic tumor therapies. Cancer Res. 2000, 60:1388-1393.
32. Ebos J.M., Kerbel R.S. Antiangiogenic therapy: impact on invasion, disease progression, and metastasis. Nat. Rev. Clin. Oncol. 2011, 8:210-221.
33. Ebos J.M., Lee C.R., Cruz-Munoz W., Bjarnason G.A., Christensen J.G., Kerbel R.S. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 2009, 15:232-239.
34. Eisenhauer E.A., Therasse P., Bogaerts J., Schwartz L.H., Sargent D., Ford R., Dancey J., Arbuck S., Gwyther S., Mooney M., et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur. J. Cancer 2009, 45:228-247.
35. Ellingson B.M., Cloughesy T.F., Lai A., Nghiemphu P.L., Lalezari S., Zaw T., Motevalibashinaeini K., Mischel P.S., Pope W.B. Quantification of edema reduction using differential quantitative T2 (DQT2) relaxometry mapping in recurrent glioblastoma treated with bevacizumab. J. Neurooncol. 2012, 106:111-119.
36. Ferrara N. Role of myeloid cells in vascular endothelial growth factor-independent tumor angiogenesis. Curr. Opin. Hematol. 2010, 17:219-224.
37. Ferrara N., Carver-Moore K., Chen H., Dowd M., Lu L., O'Shea K.S., Powell-Braxton L., Hillan K.J., Moore M.W. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 1996, 380:439-442.
38. Ferrara N., Gerber H.P., LeCouter J. The biology of VEGF and its receptors. Nat. Med. 2003, 9:669-676.
39. 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. 2004, 3:391-400.
40. Fiedler U., Augustin H.G. Angiopoietins: a link between angiogenesis and inflammation. Trends Immunol. 2006, 27:552-558.
41. Folkman J. Tumor angiogenesis: therapeutic implications. N. Engl. J. Med. 1971, 285:1182-1186.
42. Folkman J., Merler E., Abernathy C., Williams G. Isolation of a tumor factor responsible for angiogenesis. J. Exp. Med. 1971, 133:275-288.
43. Friedman H.S., Prados M.D., Wen P.Y., Mikkelsen T., Schiff D., Abrey L.E., Yung W.K., Paleologos N., Nicholas M.K., Jensen R., et al. Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J. Clin. Oncol. 2009, 27:4733-4740.
44. Gabrilovich D.I., Chen H.L., Girgis K.R., Cunningham H.T., Meny G.M., Nadaf S., Kavanaugh D., Carbone D.P. Production of vascular endothelial growth factor by human tumors inhibits the functional maturation of dendritic cells. Nat. Med. 1996, 2:1096-1103.
45. Gabrilovich D.I., Ishida T., Nadaf S., Ohm J.E., Carbone D.P. Antibodies to vascular endothelial growth factor enhance the efficacy of cancer immunotherapy by improving endogenous dendritic cell function. Clin. Cancer Res. 1999, 5:2963-2970.
46. Gabrusiewicz K., Liu D., Cortes-Santiago N., Hossain M.B., Conrad C.A., Aldape K.D., Fuller G.N., Marini F.C., Alonso M.M., Idoate M.A., et al. Anti-vascular endothelial growth factor therapy-induced glioma invasion is associated with accumulation of Tie2-expressing monocytes. Oncotarget 2014, 5:2208-2220.
47. Gerald D., Chintharlapalli S., Augustin H.G., Benjamin L.E. Angiopoietin-2: an attractive target for improved antiangiogenic tumor therapy. Cancer Res. 2013, 73:1649-1657.
48. Gerber H.P., Hillan K.J., Ryan A.M., Kowalski J., Keller G.A., Rangell L., Wright B.D., Radtke F., Aguet M., Ferrara N. VEGF is required for growth and survival in neonatal mice. Development 1999, 126:1149-1159.
49. Goldmann E. The growth of malignant disease in man and the lower animals. Lancet 1907, ii:1236-1240.
50. Gould S.E., Junttila M.R., de Sauvage F.J. Translational value of mouse models in oncology drug development. Nat. Med. 2015, 21:431-439.
51. Grothey A., Sugrue M.M., Purdie D.M., Dong W., Sargent D., Hedrick E., Kozloff M. Bevacizumab beyond first progression is associated with prolonged overall survival in metastatic colorectal cancer: results from a large observational cohort study (BRiTE). J. Clin. Oncol. 2008, 26:5326-5334.
52. Grun D., Adhikary G., Eckert R.L. VEGFA acts via neuropilin-1 to enhance epidermal cancer stem cell survival and formation of aggressive and highly vascularized tumors. Oncogene 2016, 10.1038/onc.2015.507.
53. Hegde P.S., Jubb A.M., Chen D., Li N.F., Meng Y.G., Bernaards C., Elliott R., Scherer S.J., Chen D.S. Predictive impact of circulating vascular endothelial growth factor in four phase III trials evaluating bevacizumab. Clin. Cancer Res. 2013, 19:929-937.
54. Hunter J. The Works of John Hunter 1787, Cambridge University Press.
55. 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. 2004, 350:2335-2342.
56. Ivy S.P., Wick J.Y., Kaufman B.M. An overview of small-molecule inhibitors of VEGFR signaling. Nat. Rev. Clin. Oncol. 2009, 6:569-579.
57. Jackson A., O'Connor J.P., Parker G.J., Jayson G.C. Imaging tumor vascular heterogeneity and angiogenesis using dynamic contrast-enhanced magnetic resonance imaging. Clin. Cancer Res. 2007, 13:3449-3459.
58. Jain R.K. Molecular regulation of vessel maturation. Nat. Med. 2003, 9:685-693.
59. Jain L., Vargo C.A., Danesi R., Sissung T.M., Price D.K., Venzon D., Venitz J., Figg W.D. The role of vascular endothelial growth factor SNPs as predictive and prognostic markers for major solid tumors. Mol. Cancer Ther. 2009, 8:2496-2508.
60. Jubb A.M., Harris A.L. Biomarkers to predict the clinical efficacy of bevacizumab in cancer. Lancet Oncol. 2010, 11:1172-1183.
61. Jubb A.M., Cesario A., Ferguson M., Congedo M.T., Gatter K.C., Lococo F., Mule A., Pezzella F. Vascular phenotypes in primary non-small cell lung carcinomas and matched brain metastases. Br. J. Cancer 2011, 104:1877-1881.
62. Kamba T., Tam B.Y., Hashizume H., Haskell A., Sennino B., Mancuso M.R., Norberg S.M., O'Brien S.M., Davis R.B., Gowen L.C., et al. VEGF-dependent plasticity of fenestrated capillaries in the normal adult microvasculature. Am. J. Physiol. Heart Circ. Physiol. 2006, 290:H560-H576.
63. Kim K.J., Li B., Winer J., Armanini M., Gillett N., Phillips H.S., Ferrara N. Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature 1993, 362:841-844.
64. Kozloff M., Yood M.U., Berlin J., Flynn P.J., Kabbinavar F.F., Purdie D.M., Ashby M.A., Dong W., Sugrue M.M., Grothey A., et al. Clinical outcomes associated with bevacizumab-containing treatment of metastatic colorectal cancer: the BRiTE observational cohort study. Oncologist 2009, 14:862-870.
65. Kreisl T.N., Kim L., Moore K., Duic P., Royce C., Stroud I., Garren N., Mackey M., Butman J.A., Camphausen K., et al. Phase II trial of single-agent bevacizumab followed by bevacizumab plus irinotecan at tumor progression in recurrent glioblastoma. J. Clin. Oncol. 2009, 27:740-745.
66. Kuhnert F., Kirshner J.R., Thurston G. Dll4-Notch signaling as a therapeutic target in tumor angiogenesis. Vasc. Cell 2011, 3:20.
67. Lambrechts D., Lenz H.J., de Haas S., Carmeliet P., Scherer S.J. Markers of response for the antiangiogenic agent bevacizumab. J. Clin. Oncol. 2013, 31:1219-1230.
68. Lederle W., Palmowski M., Kiessling F. Imaging in the age of molecular medicine: monitoring of anti-angiogenic treatments. Curr. Pharm. Biotechnol. 2012, 13:595-608.
69. Leung D.W., Cachianes G., Kuang W.J., Goeddel D.V., Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 1989, 246:1306-1309.
70. Mabuchi S., Terai Y., Morishige K., Tanabe-Kimura A., Sasaki H., Kanemura M., Tsunetoh S., Tanaka Y., Sakata M., Burger R.A., et al. Maintenance treatment with bevacizumab prolongs survival in an in vivo ovarian cancer model. Clin. Cancer Res. 2008, 14:7781-7789.
71. Madsen C.D., Pedersen J.T., Venning F.A., Singh L.B., Moeendarbary E., Charras G., Cox T.R., Sahai E., Erler J.T. Hypoxia and loss of PHD2 inactivate stromal fibroblasts to decrease tumour stiffness and metastasis. EMBO Rep. 2015, 16:1394-1408.
72. Malhotra V., Perry M.C. Classical chemotherapy: mechanisms, toxicities and the therapeutic window. Cancer Biol. Ther. 2003, 2:S2-S4.
73. Manning E.A., Ullman J.G., Leatherman J.M., Asquith J.M., Hansen T.R., Armstrong T.D., Hicklin D.J., Jaffee E.M., Emens L.A. A vascular endothelial growth factor receptor-2 inhibitor enhances antitumor immunity through an immune-based mechanism. Clin. Cancer Res. 2007, 13:3951-3959.
74. Miles D., Harbeck N., Escudier B., Hurwitz H., Saltz L., Van Cutsem E., Cassidy J., Mueller B., Sirzen F. Disease course patterns after discontinuation of bevacizumab: pooled analysis of randomized phase III trials. J. Clin. Oncol. 2011, 29:83-88.
75. Miller K.D., Wang J., Gralow J., Dickler M., Cobleigh M.A., Perez E.A., Shenkier T.N., Davidson N.E. A Randomized Phase III Trial of Paclitaxel versus Paclitaxel Plus Bevacizumab as First Line Therapy for Locally Recurrent Metastatic Breast Cancer. ASCO, Annual Meeting 2005, http://www.asco.org/portal/site/ASCO/menuitem.64cfbd0f85cb37b2eda2be0aee37a01d/?vgnextoid=09f8201eb61a7010VgnVCM100000ed730ad1RCRD&vmview=vm_session_presentations_view&index=y&confID=34&trackID=1&sessionID=934.
76. Mimura K., Kono K., Takahashi A., Kawaguchi Y., Fujii H. Vascular endothelial growth factor inhibits the function of human mature dendritic cells mediated by VEGF receptor-2. Cancer Immunol. Immunother. 2007, 56:761-770.
77. Moens S., Goveia J., Stapor P.C., Cantelmo A.R., Carmeliet P. The multifaceted activity of VEGF in angiogenesis-implications for therapy responses. Cytokine Growth Factor Rev. 2014, 25:473-482.
78. Monk B.J., Dalton H., Farley J.H., Chase D.M., Benjamin I. Antiangiogenic agents as a maintenance strategy for advanced epithelial ovarian cancer. Crit. Rev. Oncol. Hematol. 2013, 86:161-175.
79. Monk B.J., Minion L., Lambrechts S., Vergote I.B., Devoogdt N., Karlan B.Y. Incidence and management of edema associated with trebananib (AMG 386). Gynecol. Oncol. 2013, 130:636-641.
80. Monk B.J., Poveda A., Vergote I., Raspagliesi F., Fujiwara K., Bae D.S., Oaknin A., Ray-Coquard I., Provencher D.M., Karlan B.Y., et al. Anti-angiopoietin therapy with trebananib for recurrent ovarian cancer (TRINOVA-1): a randomised, multicentre, double-blind, placebo-controlled phase 3 trial. Lancet Oncol. 2014, 15:799-808.
81. Motz G.T., Coukos G. The parallel lives of angiogenesis and immunosuppression: cancer and other tales. Nat. Rev. Immunol. 2011, 11:702-711.
82. Motz G.T., Santoro S.P., Wang L.P., Garrabrant T., Lastra R.R., Hagemann I.S., Lal P., Feldman M.D., Benencia F., Coukos G. Tumor endothelium FasL establishes a selective immune barrier promoting tolerance in tumors. Nat. Med. 2014, 20:607-615.
83. Mulligan J.K., Rosenzweig S.A., Young M.R. Tumor secretion of VEGF induces endothelial cells to suppress T cell functions through the production of PGE2. J. Immunother. 2010, 33:126-135.
84. Nagy J.A., Dvorak H.F. Heterogeneity of the tumor vasculature: the need for new tumor blood vessel type-specific targets. Clin. Exp. Metastasis 2012, 29:657-662.
85. O'Connor J.P., Carano R.A., Clamp A.R., Ross J., Ho C.C., Jackson A., Parker G.J., Rose C.J., Peale F.V., Friesenhahn M., et al. Quantifying antivascular effects of monoclonal antibodies to vascular endothelial growth factor: insights from imaging. Clin. Cancer Res. 2009, 15:6674-6682.
86. Osada T., Chong G., Tansik R., Hong T., Spector N., Kumar R., Hurwitz H.I., Dev I., Nixon A.B., Lyerly H.K., et al. The effect of anti-VEGF therapy on immature myeloid cell and dendritic cells in cancer patients. Cancer Immunol. Immunother. 2008, 57:1115-1124.
87. Oyama T., Ran S., Ishida T., Nadaf S., Kerr L., Carbone D.P., Gabrilovich D.I. Vascular endothelial growth factor affects dendritic cell maturation through the inhibition of nuclear factor-kappa B activation in hemopoietic progenitor cells. J. Immunol. 1998, 160:1224-1232.
88. Paez-Ribes M., Allen E., Hudock J., Takeda T., Okuyama H., Vinals F., Inoue M., Bergers G., Hanahan D., Casanovas O. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009, 15:220-231.
89. Patel N., Harris A.L., Gleeson F.V., Vallis K.A. Clinical imaging of tumor angiogenesis. Future Oncol. 2012, 8:1443-1459.
90. Perren T.J., Swart A.M., Pfisterer J., Ledermann J.A., Pujade-Lauraine E., Kristensen G., Carey M.S., Beale P., Cervantes A., Kurzeder C., et al. A phase 3 trial of bevacizumab in ovarian cancer. N. Engl. J. Med. 2011, 365:2484-2496.
91. Phan V.T., Wu X., Cheng J.H., Sheng R.X., Chung A.S., Zhuang G., Tran C., Song Q., Kowanetz M., Sambrone A., et al. Oncogenic RAS pathway activation promotes resistance to anti-VEGF therapy through G-CSF-induced neutrophil recruitment. Proc. Natl. Acad. Sci. USA 2013, 110:6079-6084.
92. Piao Y., Liang J., Holmes L., Zurita A.J., Henry V., Heymach J.V., de Groot J.F. Glioblastoma resistance to anti-VEGF therapy is associated with myeloid cell infiltration, stem cell accumulation, and a mesenchymal phenotype. Neuro Oncol. 2012, 14:1379-1392.
93. Plouet J., Schilling J., Gospodarowicz D. Isolation and characterization of a newly identified endothelial cell mitogen produced by AtT-20 cells. Embo J. 1989, 8:3801-3806.
94. Radtke F., MacDonald H.R., Tacchini-Cottier F. Regulation of innate and adaptive immunity by Notch. Nat. Rev. Immunol. 2013, 13:427-437.
95. Ritchie K.E., Nor J.E. Perivascular stem cell niche in head and neck cancer. Cancer Lett. 2013, 338:41-46.
96. Roland C.L., Dineen S.P., Lynn K.D., Sullivan L.A., Dellinger M.T., Sadegh L., Sullivan J.P., Shames D.S., Brekken R.A. Inhibition of vascular endothelial growth factor reduces angiogenesis and modulates immune cell infiltration of orthotopic breast cancer xenografts. Mol. Cancer Ther. 2009, 8:1761-1771.
97. Roland C.L., Lynn K.D., Toombs J.E., Dineen S.P., Udugamasooriya D.G., Brekken R.A. Cytokine levels correlate with immune cell infiltration after anti-VEGF therapy in preclinical mouse models of breast cancer. PLoS One 2009, 4:e7669.
98. Sandler A., Gray R., Perry M.C., Brahmer J., Schiller J.H., Dowlati A., Lilenbaum R., Johnson D.H. Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N. Engl. J. Med. 2006, 355:2542-2550.
99. Sandmann T., Bourgon R., Garcia J., Li C., Cloughesy T., Chinot O.L., Wick W., Nishikawa R., Mason W., Henriksson R., et al. Patients with proneural glioblastoma may derive overall survival benefit from the addition of bevacizumab to first-line radiotherapy and temozolomide: retrospective analysis of the AVAglio trial. J. Clin. Oncol. 2015, 33:2735-2744.
100. Sardari Nia P., Hendriks J., Friedel G., Van Schil P., Van Marck E. Distinct angiogenic and non-angiogenic growth patterns of lung metastases from renal cell carcinoma. Histopathology 2007, 51:354-361.
101. Schneider B.P., Shen F., Miller K.D. Pharmacogenetic biomarkers for the prediction of response to antiangiogenic treatment. Lancet Oncol. 2012, 13:e427-e436.
102. Senger D.R., Galli S.J., Dvorak A.M., Perruzzi C.A., Harvey V.S., Dvorak H.F. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 1983, 219:983-985.
103. Shibuya M. Vascular endothelial growth factor and its receptor system: physiological functions in angiogenesis and pathological roles in various diseases. J. Biochem. 2013, 153:13-19.
104. Shing Y., Folkman J., Sullivan R., Butterfield C., Murray J., Klagsbrun M. Heparin affinity: purification of a tumor-derived capillary endothelial cell growth factor. Science 1984, 223:1296-1299.
105. Shojaei F., Wu X., Malik A.K., Zhong C., Baldwin M.E., Schanz S., Fuh G., Gerber H.P., Ferrara N. Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+ myeloid cells. Nat. Biotechnol. 2007, 25:911-920.
106. Shojaei F., Wu X., Zhong C., Yu L., Liang X.H., Yao J., Blanchard D., Bais C., Peale F.V., van Bruggen N., et al. Bv8 regulates myeloid-cell-dependent tumour angiogenesis. Nature 2007, 450:825-831.
107. Shrimali R.K., Yu Z., Theoret M.R., Chinnasamy D., Restifo N.P., Rosenberg S.A. Antiangiogenic agents can increase lymphocyte infiltration into tumor and enhance the effectiveness of adoptive immunotherapy of cancer. Cancer Res. 2010, 70:6171-6180.
108. Singh M., Lima A., Molina R., Hamilton P., Clermont A.C., Devasthali V., Thompson J.D., Cheng J.H., Bou Reslan H., Ho C.C., et al. Assessing therapeutic responses in Kras mutant cancers using genetically engineered mouse models. Nat. Biotechnol. 2010, 28:585-593.
109. Singh M., Couto S.S., Forrest W.F., Lima A., Cheng J.H., Molina R., Long J.E., Hamilton P., McNutt A., Kasman I., et al. Anti-VEGF antibody therapy does not promote metastasis in genetically engineered mouse tumour models. J. Pathol. 2012, 227:417-430.
110. Stein W.D., Yang J., Bates S.E., Fojo T. Bevacizumab reduces the growth rate constants of renal carcinomas: a novel algorithm suggests early discontinuation of bevacizumab resulted in a lack of survival advantage. Oncologist 2008, 13:1055-1062.
111. Sznol M., McDermott D., Jones S., Mier J., Waterkamp D., Rossi C., Wallin J., Funke R., Bendell J. Phase Ib evaluation of MPDL3280A (anti-PDL1) in combination with bevacizumab (bev) in patients (pts) with metastatic renal cell carcinoma (mRCC). J. Clin. Oncol. 2015, 33(Suppl 7). abstr 410.
112. Takano S., Kimu H., Tsuda K., Osuka S., Nakai K., Yamamoto T., Ishikawa E., Akutsu H., Matsuda M., Matsumura A. Decrease in the apparent diffusion coefficient in peritumoral edema for the assessment of recurrent glioblastoma treated by bevacizumab. Acta Neurochir Suppl. 2013, 118:185-189.
113. Tarallo V., De Falco S. The vascular endothelial growth factors and receptors family: up to now the only target for anti-angiogenesis therapy. Int. J. Biochem. Cell Biol. 2015, 64:185-189.
114. Tewari K.S., Sill M.W., Long H.J., Penson R.T., Huang H., Ramondetta L.M., Landrum L.M., Oaknin A., Reid T.J., Leitao M.M., et al. Improved survival with bevacizumab in advanced cervical cancer. N. Engl. J. Med. 2014, 370:734-743.
115. Van der Veldt A.A., Lubberink M., Bahce I., Walraven M., de Boer M.P., Greuter H.N., Hendrikse N.H., Eriksson J., Windhorst A.D., Postmus P.E., et al. Rapid decrease in delivery of chemotherapy to tumors after anti-VEGF therapy: implications for scheduling of anti-angiogenic drugs. Cancer Cell 2012, 21:82-91.
116. Vaziri S.A., Kim J., Ganapathi M.K., Ganapathi R. Vascular endothelial growth factor polymorphisms: role in response and toxicity of tyrosine kinase inhibitors. Curr. Oncol. Rep. 2010, 12:102-108.
117. Wehland M., Bauer J., Magnusson N.E., Infanger M., Grimm D. Biomarkers for anti-angiogenic therapy in cancer. Int. J. Mol. Sci. 2013, 14:9338-9364.
118. Weis S.M., Cheresh D.A. Tumor angiogenesis: molecular pathways and therapeutic targets. Nat. Med. 2011, 17:1359-1370.
119. Winkler F., Kozin S.V., Tong R.T., Chae S.S., Booth M.F., Garkavtsev I., Xu L., Hicklin D.J., Fukumura D., di Tomaso E., et al. Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: role of oxygenation, angiopoietin-1, and matrix metalloproteinases. Cancer Cell 2004, 6:553-563.
120. Yang J.C., Haworth L., Sherry R.M., Hwu P., Schwartzentruber D.J., Topalian S.L., Steinberg S.M., Chen H.X., Rosenberg S.A. A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N. Engl. J. Med. 2003, 349:427-434.
121. Zhang L., Conejo-Garcia J.R., Katsaros D., Gimotty P.A., Massobrio M., Regnani G., Makrigiannakis A., Gray H., Schlienger K., Liebman M.N., et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N. Engl. J. Med. 2003, 348:203-213.