Efficacy of cotargeting angiopoietin-2 and the VEGF pathway in the adjuvant postsurgical setting for early breast, colorectal, and renal cancers

Cancer Research

Volumn 76, Issue 23, 2016, Pages 6988-7000

  Wu, Florence T H ^a,b   Man, Shan ^b   Xu, Ping ^b   Chow, Annabelle ^b   Paez Ribes, Marta ^b   Lee, Christina R ^b   Pirie Shepherd, Steven R ^c   Emmenegger, Urban ^b   Kerbel, Robert S ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b Canada   (Canada)

^c PFIZER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; ANGIOPOIETIN 2; ANTINEOPLASTIC AGENT; CVX 060; CVX 241; REGORAFENIB; SUNITINIB; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLUMINESCENCE; BREAST CANCER; CANCER ADJUVANT THERAPY; CANCER GROWTH; CANCER SURVIVAL; COLORECTAL CANCER; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; DRUG POTENCY; EARLY CANCER; FEMALE; HUMAN; HUMAN CELL; KIDNEY CANCER; LIVER METASTASIS; LUNG METASTASIS; LYMPH NODE METASTASIS; MALE; METASTASIS INHIBITION; MOLECULARLY TARGETED THERAPY; MONOTHERAPY; MOUSE; NONHUMAN; OVERALL SURVIVAL; PRIORITY JOURNAL; TUMOR VOLUME; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BREAST NEOPLASMS; COLORECTAL NEOPLASMS; KIDNEY NEOPLASMS; TUMOR CELL LINE;

ANGIOGENESIS INHIBITORS; ANGIOPOIETIN-2; ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; FEMALE; HUMANS; KIDNEY NEOPLASMS; MICE; MICE, INBRED BALB C; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 85003028819     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-16-0888     Document Type: Article

References (49)

1. de Gramont A, Van Cutsem E, Schmoll HJ, Tabernero J, Clarke S, Moore MJ, et al. Bevacizumab plus oxaliplatin-based chemotherapy as adjuvant treatment for colon cancer (AVANT): a phase 3 randomised controlled trial. Lancet Oncol 2012;13:1225-33.
2. Allegra CJ, Yothers G, O'Connell MJ, Sharif S, Petrelli NJ, Lopa SH, et al. Bevacizumab in stage II-III colon cancer: 5-year update of the national surgical adjuvant breast and bowel project C-08 trial. J Clin Oncol 2013;31:359-64.
3. Haas NB, Manola J, Uzzo RG, Flaherty KT, Wood CG, Kane C, et al. Adjuvant sunitinib or sorafenib for high-risk, non-metastatic renal-cell carcinoma (ECOG-ACRIN E2805): a double-blind, placebo-controlled, randomised, phase 3 trial. Lancet 2016;387:2008-16.
4. Paez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Vinals F, et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009;15:220-31.
5. Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 2009;15:232-9.
6. Donnem T, Hu J, Ferguson M, Adighibe O, Snell C, Harris AL, et al. Vessel co-option in primary human tumors and metastases: an obstacle to effective anti-angiogenic treatment? Cancer Med 2013;2:427-36.
7. Pezzella F, Gatter K. Non-angiogenic tumours unveil a new chapter in cancer biology. J Pathol 2015;235:381-3.
8. Mina LA, Sledge GW Jr. Rethinking the metastatic cascade as a therapeutic target. Nat Rev Clin Oncol 2011;8:325-32.
9. Cooke VG, LeBleu VS, Keskin D, Khan Z, O'Connell JT, Teng Y, 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.
10. Chung AS, Kowanetz M, Wu X, Zhuang G, Ngu H, Finkle D, et al. Differential drug class-specific metastatic effects following treatment with a panel of angiogenesis inhibitors. J Pathol 2012;227:404-16.
11. Welti JC, Powles T, Foo S, Gourlaouen M, Preece N, Foster J, et al. Contrasting effects of sunitinib within in vivo models of metastasis. Angiogenesis 2012;15:623-41.
12. Huang H, Bhat A, Woodnutt G, Lappe R. Targeting the ANGPT-TIE2 pathway in malignancy. Nat Rev Cancer 2010;10:575-85.
13. Holash J, Maisonpierre PC, Compton D, Boland P, Alexander CR, Zagzag D, et al. Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF. Science 1999;284:1994-8.
14. Keskin D, Kim J, Cooke VG, Wu CC, Sugimoto H, Gu C, et al. Targeting vascular pericytes in hypoxic tumors increases lung metastasis via angiopoietin-2. Cell Rep 2015;10:1066-81.
15. Falcon BL, Hashizume H, Koumoutsakos P, Chou J, Bready JV, Coxon A, et al. Contrasting actions of selective inhibitors of angiopoietin-1 and angiopoietin-2 on the normalization of tumor blood vessels. Am J Pathol 2009;175:2159-70.
16. Holopainen T, Saharinen P, D'Amico G, Lampinen A, Eklund L, Sormunen R, et al. Effects of angiopoietin-2-blocking antibody on endothelial cell-cell junctions and lung metastasis. J Natl Cancer Inst 2012;104:461-75.
17. Wang X, Bullock AJ, Zhang L, Wei L, Yu D, Mahagaokar K, et al. The role of angiopoietins as potential therapeutic targets in renal cell carcinoma. Transl Oncol 2014;7:188-95.
18. Kopczynska E, Dancewicz M, Kowalewski J, Makarewicz R, Kardymowicz H, Kaczmarczyk A, et al. Time-dependent changes of plasma concentrations of angiopoietins, vascular endothelial growth factor, and soluble forms of their receptors in nonsmall cell lung cancer patients following surgical resection. ISRN Oncol 2012;2012:638352.
19. Kumara HM, Feingold D, Kalady M, Dujovny N, Senagore A, Hyman N, et al. Colorectal resection is associated with persistent proangiogenic plasma protein changes: postoperative plasma stimulates in vitro endothelial cell growth, migration, and invasion. Ann Surg 2009;249:973-7.
20. Huang H, Lai JY, Do J, Liu D, Li L, Del Rosario J, et al. Specifically targeting angiopoietin-2 inhibits angiogenesis, Tie2-expressing monocyte infiltration, and tumor growth. Clin Cancer Res 2011;17:1001-11.
21. Teicher BA, Herman TS, Holden SA, Wang YY, Pfeffer MR, Crawford JW, et al. Tumor resistance to alkylating agents conferred by mechanisms operative only in vivo. Science 1990;247:1457-61.
22. Munoz R, Man S, Shaked Y, Lee CR, Wong J, Francia G, et al. Highly efficacious nontoxic preclinical treatment for advanced metastatic breast cancer using combination oral UFT-cyclophosphamide metronomic chemotherapy. Cancer Res 2006;66:3386-91.
23. Man S, Munoz R, Kerbel RS. On the development of models in mice of advanced visceral metastatic disease for anti-cancer drug testing. Cancer Metastasis Rev 2007;26:737-47.
24. Hackl C, Man S, Francia G, Milsom C, Xu P, Kerbel RS. Metronomic oral topotecan prolongs survival and reduces liver metastasis in improved preclinical orthotopic and adjuvant therapy colon cancer models. Gut 2013;62:259-71.
25. Jedeszko C, Paez-Ribes M, Di Desidero T, Man S, Lee CR, Xu P, et al. Postsurgical adjuvant or metastatic renal cell carcinoma therapy models reveal potent anti-tumor activity of metronomic oral topotecan with pazopanib. Sci Transl Med 2015;7:282ra50.
26. Tait LR, Pauley RJ, Santner SJ, Heppner GH, Heng HH, Rak JW, et al. Dynamic stromal-epithelial interactions during progression of MCF10DCIS.com xenografts. Int J Cancer 2007;120:2127-34.
27. Wu FT, Lee CR, Bogdanovic E, Prodeus A, Gariepy J, Kerbel RS. Vasculotide reduces endothelial permeability and tumor cell extravasation in the absence of binding to or agonistic activation of Tie2. EMBO Mol Med 2015;7:770-87.
28. Caine GJ, Blann AD, Stonelake PS, Ryan P, Lip GY. Plasma angiopoietin-1, angiopoietin-2 and tie-2 in breast and prostate cancer: a comparison with VEGF and flt-1. Eur J Clin Invest 2003;33:883-90.
29. Li P, He Q, Luo C, Qian L. Diagnostic and prognostic potential of serum angiopoietin-2 expression in human breast cancer. Int J Clin Exp Pathol 2015;8:660-4.
30. Gerald D, Chintharlapalli S, Augustin HG, Benjamin LE. Angiopoietin-2: an attractive target for improved antiangiogenic tumor therapy. Cancer Res 2013;73:1649-57.
31. Doppalapudi VR, Huang J, Liu D, Jin P, Liu B, Li L, et al. Chemical generation of bispecific antibodies. Proc Natl Acad Sci U S A 2010;107:22611-6.
32. Murukesh N, Dive C, Jayson GC. Biomarkers of angiogenesis and their role in the development of VEGF inhibitors. Br J Cancer 2010;102:8-18.
33. Stubenrauch K, Wessels U, Essig U, Vogel R, Waltenberger H, Hansbauer A, et al. An immunodepletion procedure advances free angiopoietin-2 determination in human plasma samples during anti-cancer therapy with bispecific anti-Ang2/VEGF CrossMab. J Pharm Biomed Anal 2015;102:459-67.
34. Loupakis F, Falcone A, Masi G, Fioravanti A, Kerbel RS, Del Tacca M, et al. Vascular endothelial growth factor levels in immunodepleted plasma of cancer patients as a possible pharmacodynamic marker for bevacizumab activity. J Clin Oncol 2007;25:1816-8.
35. Abou-Elkacem L, Arns S, Brix G, Gremse F, Zopf D, Kiessling F, et al. Regorafenib inhibits growth, angiogenesis, and metastasis in a highly aggressive, orthotopic colon cancer model. Mol Cancer Ther 2013;12:1322-31.
36. Ahmed D, Eide PW, Eilertsen IA, Danielsen SA, Eknaes M, Hektoen M, et al. Epigenetic and genetic features of 24 colon cancer cell lines. Oncogenesis 2013;2:e71.
37. Yu JL, Rak JW, Coomber BL, Hicklin DJ, Kerbel RS. Effect of p53 status on tumor response to antiangiogenic therapy. Science 2002;295:1526-8.
38. Vermeulen PB, Colpaert C, Salgado R, Royers R, Hellemans H, Van Den Heuvel E, et al. Liver metastases from colorectal adenocarcinomas grow in three patterns with different angiogenesis and desmoplasia. J Pathol 2001;195:336-42.
39. Guerin E, Man S, Xu P, Kerbel RS. A model of postsurgical advanced metastatic breast cancer more accurately replicates the clinical efficacy of antiangiogenic drugs. Cancer Res 2013;73:2743-8.
40. Srivastava K, Hu J, Korn C, Savant S, Teichert M, Kapel SS, et al. Postsurgical adjuvant tumor therapy by combining anti-angiopoietin-2 and metronomic chemotherapy limits metastatic growth. Cancer Cell 2014;26:880-95.
41. Kerbel RS, Guerin E, Francia G, Xu P, Lee CR, Ebos JM, et al. Preclinical recapitulation of antiangiogenic drug clinical efficacies using models of early or late stage breast cancer metastatis. Breast 2013;22 Suppl 2:S57-65.
42. Sheridan C. Amgen's angiopoietin blocker fails in ovarian cancer. Nat Biotechnol 2015;33:5-6.
43. Brown JL, Cao ZA, Pinzon-Ortiz M, Kendrew J, Reimer C, Wen S, et al. A human monoclonal anti-ANG2 antibody leads to broad antitumor activity in combination with VEGF inhibitors and chemotherapy agents in preclinical models. Mol Cancer Ther 2010;9:145-56.
44. Eggermont AM, Chiarion-Sileni V, Grob JJ, Dummer R, Wolchok JD, Schmidt H, et al. Prolonged Survival in Stage III Melanoma with Ipilimumab Adjuvant Therapy. N Engl J Med 2016 Oct 7. DOI: 10.1056/NEJMoa1611299.
45. Coffelt SB, Chen YY, Muthana M, Welford AF, Tal AO, Scholz A, et al. Angiopoietin 2 stimulates TIE2-expressing monocytes to suppress T cell activation and to promote regulatory T cell expansion. J Immunol 2011;186:4183-90.
46. Ibberson M, Bron S, Guex N, Faes-van't Hull E, Ifticene-Treboux A, Henry L, et al. TIE-2 and VEGFR kinase activities drive immunosuppressive function of TIE-2-expressing monocytes in human breast tumors. Clin Cancer Res 2013;19:3439-49.
47. Faivre S, Demetri G, Sargent W, Raymond E. Molecular basis for sunitinib efficacy and future clinical development. Nat Rev Drug Discov 2007;6:734-45.
48. Andrae J, Gallini R, Betsholtz C. Role of platelet-derived growth factors in physiology and medicine. Genes Dev 2008;22:1276-312.
49. Cao Y. Erythropoietin in cancer: a dilemma in risk therapy. Trends Endocrinol Metab 2013;24:190-9.