Assessing the in vivo efficacy of biologic antiangiogenic therapies

Cancer Chemotherapy and Pharmacology

Volumn 71, Issue 1, 2013, Pages 1-12

  Wilson, Peter M ^a   Labonte, Melissa J ^b   Lenz, Heinz Josef ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b AZUSA PACIFIC UNIVERSITY   (United States)

Author keywords

Angiogenesis; Antiangiogenesis; Bevacizumab; Biomarkers; Review; Vascular endothelial growth factor (VEGF); Ziv aflibercept (VEGF Trap)

Indexed keywords

AFLIBERCEPT; ALPHA INTERFERON; ANGIOGENESIS INHIBITOR; ANTINEOPLASTIC AGENT; BEVACIZUMAB; BIOLOGICAL MARKER; CARBOPLATIN; CETUXIMAB; CYTOTOXIC AGENT; FLUOROURACIL; FOLINIC ACID; GEMCITABINE; IRINOTECAN; ISOPROTEIN; PACLITAXEL; PLACEBO; PLACENTAL GROWTH FACTOR; VASCULOTROPIN; VASCULOTROPIN A; VASCULOTROPIN B; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3;

ADVANCED CANCER; ANTIANGIOGENIC ACTIVITY; ANTIANGIOGENIC THERAPY; CANCER COMBINATION CHEMOTHERAPY; CANCER GROWTH; CANCER RADIOTHERAPY; CANCER RESISTANCE; CANCER SURVIVAL; CLINICAL EFFECTIVENESS; COLORECTAL CANCER; CONTRAST ENHANCEMENT; DRUG EFFICACY; DRUG HALF LIFE; DRUG MECHANISM; DRUG POTENCY; DRUG RESPONSE; DRUG SAFETY; ENDOTHELIUM CELL; GLIOBLASTOMA; HUMAN; HYPERTENSION; IN VIVO STUDY; KIDNEY METASTASIS; LIVER METASTASIS; LUNG CANCER; LUNG NON SMALL CELL CANCER; MALIGNANT NEOPLASTIC DISEASE; METASTASIS; MOLECULARLY TARGETED THERAPY; MULTIPLE CYCLE TREATMENT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PANCREAS CANCER; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEINURIA; REVIEW; SIGNAL TRANSDUCTION; TREATMENT DURATION; TREATMENT PLANNING; TUMOR VASCULARIZATION;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTINEOPLASTIC AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; NEOPLASM METASTASIS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PATIENT SELECTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84872354697     PISSN: 03445704     EISSN: 14320843     Source Type: Journal    
DOI: 10.1007/s00280-012-1978-8     Document Type: Review

References (61)

1. Fischer C, Mazzone M, Jonckx B, Carmeliet P (2008) FLT1 and its ligands VEGFB and PlGF: drug targets for anti-angiogenic therapy? Nat Rev Cancer 8:942-956
2. Ferrara N, Kerbel RS (2005) Angiogenesis as a therapeutic target. Nature 438:967-974
3. Folkman J, Merler E, Abernathy C, Williams G (1971) Isolation of a tumor factor responsible for angiogenesis. J Exp Med 133:275-288
4. Carmeliet P, Jain RK (2011) Molecular mechanisms and clinical applications of angiogenesis. Nature 473:298-307
5. Liu Y, Han ZP, Zhang SS, Jing YY, Bu XX, Wang CY, Sun K, Jiang GC, Zhao X, Li R, Gao L, Zhao QD, Wu MC, Wei LX (2011) Effects of inflammatory factors on mesenchymal stem cells and their role in the promotion of tumor angiogenesis in colon cancer. J Biol Chem 286:25007-25015
6. Gerber HP, Ferrara N (2005) Pharmacology and pharmacodynamics of bevacizumab as monotherapy or in combination with cytotoxic therapy in preclinical studies. Cancer Res 6:671-680
7. Jain RK (2005) Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307:58-62
8. Folkman J, Klagsbrun M (1987) Angiogenic factors. Science 235:442-447
9. Ferrara N (2004) Vascular endothelial growth factor as a target for anticancer therapy. Oncologist 9(Suppl 1):2-10
10. Harris AL (2002) Hypoxia-a key regulatory factor in tumour growth. Nat Rev Cancer 2:38-47
11. Bergers G, Hanahan D (2008) Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer 8:592-603
12. Gerger A, LaBonte M, Lenz HJ (2011) Molecular predictors of response to antiangiogenesis therapies. Cancer J 17:134-141
13. Murukesh N, Dive C, Jayson GC (2010) Biomarkers of angiogenesis and their role in the development of VEGF inhibitors. Br J Cancer 5:8-18
14. Kopetz S, Hoff PM, Morris JS, Wolff RA, Eng C, Glover KY, Adinin R, Overman MJ, Valero V, Wen S, Lieu C, Yan S, Tran HT, Ellis LM, Abbruzzese JL, Heymach JV (2010) Phase II trial of infusional fluorouracil, irinotecan, and bevacizumab for metastatic colorectal cancer: efficacy and circulating angiogenic biomarkers associated with therapeutic resistance. J Clin Oncol 28:453-459
15. Loupakis F, Cremolini C, Fioravanti A et al (2011) Pharmacodynamic and pharmacogenetic angiogenesis-related markers of first-line FOLFOXIRI plus bevacizumab schedule in metastatic colorectal cancer. Br J Cancer 104:1262-1269
16. Fischer C, Jonckx B, Mazzone M, Zacchigna S, Loges S, Pattarini L, Chorianopoulos E, Liesenborghs L, Koch M, De Mol M, Autiero M, Wyns S, Plaisance S, Moons L, van Rooijen N, Giacca M, Stassen JM, Dewerchin M, Collen D, Carmeliet P. Anti-PlGF inhibits growth of VEGF(R)-inhibitor-resistant tumors without affecting healthy vessels. Cell 131:463-475
17. Park JW, Kerbel RS, Kelloff GJ, Barrett JC, Chabner BA, Parkinson DR, Peck J, Ruddon RW, Sigman CC, Slamon DJ (2004) Rationale for biomarkers and surrogate en points in mechanism-driven oncology drug development. Clin Cancer Res 10:3885-3896
18. Hurwitz H, Fehrenbacher L, Novotny W, Cartwright T, Hainsworth J, Heim W, Berlin J, Baron A, Griffing S, Holmgren E, Ferrara N, Fyfe G, Rogers B, Ross R, Kabbinavar F (2004) Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med 350:2335-2342
19. Ferrara N, Hillan KJ, Novotny W (2005) Bevacizumab (Avastin), a humanized anti-VEGF monoclonal antibody for cancer therapy. Biochem Biophys Res Commun 333:328-335
20. Avastin [prescribing information] (2011) Roche, South San Francisco, CA
21. Veikkola T, Alitalo K (1999) VEGFs, receptors and angiogenesis. Semin Cancer Biol 9:211-220
22. Chu QS (2009) Ziv-aflibercept (AVE0005): an alternative strategy for inhibiting tumour angiogenesis by vascular endothelial growth factors. Expert Opin Biol Ther 9:263-271
23. Sweeney CJ, Miller KD, Sledge GW Jr (2003) Resistance in the anti-angiogenic era: nay-saying or a word of caution? Trends Mol Med 9:24-29
24. Martinez-Poveda B, Gomez V, Alcaide-German M, Perruca S, Vazquez S, Alba LE, Casanovas O, Garcia-Bermejo ML, Peso L, Jimenez B (2011) Non-invasive monitoring of hypoxia-inducible factor activation by optical imaging during antiangiogenic treatment in a xenograft model of ovarian carcinoma. Int J Oncol 39:543-552
25. Rudge JS, Holash J, Hylton D, Russell M, Jiang S, Leidich R, Papadopoulos N, Pyles EA, Torri A, Wiegand SJ, Thurston G, Stahl N, Yancopoulos GD (2007) VEGF Trap complex formation measures production rates of VEGF, providing a biomarker for predicting efficacious angiogenic blockade. Proc Natl Acad Sci USA 104:18363-18370
26. Ferrara N (2004) Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev 25:581-611
27. Bates RC, Goldsmith JD, Bachelder RE, Brown C, Shibuya M, Oettgen P, Mercurio AM (2003) Flt-1-dependent survival characterizes the epithelial-mesenchymal transition of colonic organoids. Curr Biol 13:1721-1727
28. Boscolo E, Mulliken JB, Bischoff J (2011) VEGFR-1 mediates endothelial differentiation and formation of blood vessels in a murine model of infantile hemangioma. Am J Pathol 179:2266-2277
29. Hilmi C, Guyot M, Pagès G (2012) VEGF spliced variants: possible role of anti-angiogenesis therapy. J Nucleic Acids 2012:162692
30. Nowak DG, Amin EM, Rennel ES, Hoareau-Aveilla C, Gammons M, Damodoran G, Hagiwara M, Harper SJ, Woolard J, Ladomery MR, Bates DO (2010) Regulation of vascular endothelial growth factor (VEGF) splicing from pro-angiogenic to anti-angiogenic isoforms: a novel therapeutic strategy for angiogenesis. J Biol Chem 285:5532-5540
31. Peiris-Pagès M, Harper SJ, Bates DO, Ramani P (2010) Balance of pro- versus anti-angiogenic splice isoforms of vascular endothelial growth factor as a regulator of neuroblastoma growth. J Pathol 222:138-147
32. Rennel ES, Varey AH, Churchill AJ, Wheatley ER, Stewart L, Mather S, Bates DO, Harper SJ (2009) VEGF(121)b, a new member of the VEGF(xxx)b family of VEGF-A splice isoforms, inhibits neovascularisation and tumour growth in vivo. Br J Cancer 101:1183-1193
33. Pritchard-Jones RO, Dunn DB, Qiu Y, Varey AH, Orlando A, Rigby H, Harper SJ, Bates DO (2007) Expression of VEGF(xxx)b, the inhibitory isoforms of VEGF, in malignant melanoma. Br J Cancer 97:223-230
34. Paule B, Bastien L, Deslandes E, Cussenot O, Podgorniak MP, Allory Y, Naïmi B, Porcher R, de La Taille A, Menashi S, Calvo F, Mourah S (2010) Soluble isoforms of vascular endothelial growth factor are predictors of response to sunitinib in metastatic renal cell carcinomas. PLoS One 5:e10715
35. Li X, Lee C, Tang Z, Zhang F, Arjunan P, Li Y, Hou X, Kumar A, Dong L (2009) VEGF-B: a survival, or an angiogenic factor? Cell Adh Migr 3:322-327
36. Olofsson B, Pajusola K, Kaipainen A, von Euler G, Joukov V, Saksela O, Orpana A, Pettersson RF, Alitalo K, Eriksson U (1996) Vascular endothelial growth factor B, a novel growth factor for endothelial cells. Proc Natl Acad Sci USA 93:2576-2581
37. Olofsson B, Pajusola K, von Euler G, Chilov D, Alitalo K, Eriksson U (1996) Genomic organization of the mouse and human genes for vascular endothelial growth factor B (VEGF-B) and characterization of a second splice isoform. J Biol Chem 271:19310-19317
38. Olofsson B, Korpelainen E, Pepper MS, Mandriota SJ, Aase K, Kumar V, Gunji Y, Jeltsch MM, Shibuya M, Alitalo K, Eriksson U (1998) Vascular endothelial growth factor B (VEGF-B) binds to VEGF receptor-1 and regulates plasminogen activator activity in endothelial cells. Proc Natl Acad Sci USA 95:11709-11714
39. Zhang F, Tang Z, Hou X, Lennartsson J, Li Y, Koch AW, Scotney P, Lee C, Arjunan P, Dong L, Kumar A, Rissanen TT, Wang B, Nagai N, Fons P, Fariss R, Zhang Y, Wawrousek E, Tansey G, Raber J, Fong GH, Ding H, Greenberg DA, Becker KG, Herbert JM, Nash A, Yla-Herttuala S, Cao Y, Watts RJ, Li X (2009) VEGF-B is dispensable for blood vessel growth but critical for their survival, and VEGF-B targeting inhibits pathological angiogenesis. Proc Natl Acad Sci USA 106:6152-6157
40. Carmeliet P, Moons L, Luttun A, Vincenti V, Compernolle V, De Mol M, Wu Y, Bono F, Devy L, Beck H, Scholz D, Acker T, DiPalma T, Dewerchin M, Noel A, Stalmans I, Barra A, Blacher S, Vandendriessche T, Ponten A, Eriksson U, Plate KH, Foidart JM, Schaper W, Charnock-Jones DS, Hicklin DJ, Herbert JM, Collen D, Persico MG (2001) Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med 7:575-583
41. Ribatti D (2008) The discovery of the placental growth factor and its role in angiogenesis: a historical review. Angiogenesis 11:215-221
42. Escudero-Esparza A, Martin TA, Davies ML, Jiang WG (2009) PGF isoforms, PlGF-1 and PlGF-2, in colorectal cancer and the prognostic significance. Cancer Genomics Proteomics 6:239-246
43. Hiratsuka S, Maru Y, Okada A, Seiki M, Noda T, Shibuya M (2001) Involvement of Flt-1 tyrosine kinase (vascular endothelial growth factor receptor-1) in pathological angiogenesis. Cancer Res 61:1207-1213
44. Bais C, Wu X, Yao J, Yang S, Crawford Y, McCutcheon K, Tan C, Kolumam G, Vernes JM, Eastham-Anderson J, Haughney P, Kowanetz M, Hagenbeek T, Kasman I, Reslan HB, Ross J, Van Bruggen N, Carano RA, Meng YJ, Hongo JA, Stephan JP, Shibuya M, Ferrara N (2010) PlGF blockade does not inhibit angiogenesis during primary tumor growth. Cell 141:166-177
45. Loges S, Schmidt T, Carmeliet P (2009) "Antimyeloangiogenic" therapy for cancer by inhibiting PlGF. Clin Cancer Res 15:3648-3653
46. Tew WP, Gordon M, Murren J, Dupont J, Pezzulli S, Aghajanian C, Sabbatini P, Mendelson D, Schwartz L, Gettinger S, Psyrri A, Cedarbaum JM, Spriggs DR (2010) Phase 1 study of ziv-aflibercept administered subcutaneously to patients with advanced solid tumors. Clin Cancer Res 16:358-366
47. Holash J, Davis S, Papadopoulos N, Croll SD, Ho L, Russell M, Boland P, Leidich R, Hylton D, Burova E, Ioffe E, Huang T, Radziejewski C, Bailey K, Fandl JP, Daly T, Wiegand SJ, Yancopoulos GD, Rudge JS (2002) VEGF-Trap: a VEGF blocker with potent antitumor effects. Proc Natl Acad Sci USA 99:11393-11398
48. Van Cutsem E, Tabernero J, Lakomy R, Prausova J, Ruff P, Van Hazel G, Moiseyenko V, Ferry D, McKendrick J, Tellier A, Castan R, Allegra C (2011) Intravenous (IV) ziv-aflibercept versus placebo in combination with irinotecan/5-FU (FOLFIRI) for second line treatment of metastatic colorectal cancer (mCRC): results of a multinational Phase III trial (EFC10262-VELOUR). Abstract O-0024
49. Sanofi-Aventis. Ziv-aflibercept versus placebo in combination with irinotecan and 5-FU in the treatment of patients with metastatic colorectal cancer after failure of an oxaliplatin based regimen (VELOUR). In: ClinicalTrials.gov [Internet]. National Library of Medicine (US), Bethesda 2000- [Jan 1 2012]. Available from: http://clinicaltrials.gov/ct2/show/NCT00561470 NLM Identifier:NCT00561470
50. Phase 3 trial of aflibercept in metastatic pancreatic cancer discontinued [press release]. Regeneron Pharmaceuticals, Inc. and sanofi-aventis, Paris and Tarrytown; 11 September 2009. http://newsroom.regeneron.com/releasedetail.cfm? releaseid=408744. Accessed 6 Aug 2012
51. Sanofi and Regeneron announce regulatory and clinical update for ZALTRAP® (aflibercept) [press release]. Regeneron Pharmaceuticals, Inc. and sanofi-aventis, Paris and Tarrytown; 5 Apr 2012. http://investor.regeneron.com/ releasedetail.cfm?releaseid=661995. Accessed 6 Aug 2012
52. Adams B (2011) Sanofi-Aventis' lung cancer drug aflibercept has failed to meet its primary endpoint in a phase III trial. InPharm. http://www.inpharm. com/news/150688/sanofi-regeneron-aflibercept-phase-iii. Accessed 6 Aug 2012
53. Meyer T, Robles-Carrillo L, Desai H, Hatfield M, Amaya M, Francis J, Amirkhosravi A (2010) Comparison of platelet activating potential of bevacizumab + VEGF and ziv-aflibercept + VEGF complexes. 53rd annual meeting of the American Society of Hematology, December 10-13, 2011, San Diego, CA, Abstract 3600
54. Norden-Zfoni A, Desai J, Manola J, Beaudry P, Force J, Maki R, Folkman J, Bello C, Baum C, DePrimo SE, Shalinsky DR, Demetri GD, Heymach JV (2007) Blood-based biomarkers of SU11248 activity and clinical outcome in patients with metastatic imatinib-resistant gastrointestinal stromal tumor. Clin Cancer Res 13:2643-2650
55. Scartozzi M, Galizia E, Chiorrini S, Giampieri R, Berardi R, Pierantoni C, Cascinu S (2009) Arterial hypertension correlates with clinical outcome in colorectal cancer patients treated with first-line bevacizumab. Ann Oncol 20:227-230
56. Motzer RJ, Michaelson MD, Redman BG, Hudes GR, Wilding G, Figlin RA, Ginsberg MS, Kim ST, Baum CM, DePrimo SE, Li JZ, Bello CL, Theuer CP, George DJ, Rini BI (2006) Activity of SU11248, a multitargeted inhibitor of vascular endothelial growth factor receptor and platelet-derived growth factor receptor, in patients with metastatic renal cell carcinoma. J Clin Oncol 24:16-24
57. Ebos JM, Lee CR, Christensen JG, Mutsaers AJ, Kerbel RS (2007) Multiple circulating proangiogenic factors induced by sunitinib malate are tumor-independent and correlate with antitumor efficacy. Proc Natl Acad Sci USA 104:17069-17074
58. Hirashima Y, Yamada Y, Tateishi U, Kato K, Miyake M, Horita Y, Akiyoshi K, Takashima A, Okita N, Takahari D, Nakajima T, Hamaguchi T, Shimada Y, Shirao K (2012) Pharmacokinetic parameters from 3-Tesla DCE-MRI as surrogate biomarkers of antitumor effects of bevacizumab plus FOLFIRI in colorectal cancer with liver metastasis. Int J Cancer 130:2359-2365
59. Vriens D, de Geus-Oei LF, Heerschap A, van Laarhoven HW, Oyen WJ (2011) Vascular and metabolic response to bevacizumab-containing regimens in two patients with colorectal liver metastases measured by dynamic contrast-enhanced MRI and dynamic 18F-FDG-PET. Clin Colorectal Cancer 10:E1-E5
60. Bhojani MS, Nyati MK, Zhao L, Normolle DP, Ross BD, Lawrence TS, Rehemtulla A (2011) Molecular imaging of akt enables early prediction of response to molecular targeted therapy. Transl Oncol 4:122-125
61. Beloueche-Babari M, Workman P, Leach MO (2011) Exploiting tumor metabolism for non-invasive imaging of the therapeutic activity of molecularly targeted anticancer agents. Cell Cycle 10:2883-2893