Angiogenesis and tumor microenvironment: bevacizumab in the breast cancer model

Targeted Oncology

Volumn 10, Issue 2, 2015, Pages 189-198

  Trédan, Olivier ^a   Lacroix Triki, Magali ^b   Guiu, Séverine ^c   Mouret Reynier, Marie Ange ^d   Barrière, Jérôme ^e   Bidard, François Clément ^f   Braccini, Antoine Laurent ^g   Mir, Olivier ^h   Villanueva, Christian ⁱ   Barthélémy, Philippe ^j  

^a CENTRE LÉON BÉRARD   (France)

^b INSTITUT CLAUDIUS REGAUD   (France)

^c CENTRE GEORGES FRANÇOIS LECLERC   (France)

^d CENTRE JEAN PERRIN   (France)

^e CENTRE ANTOINE LACASSAGNE   (France)

^f INSTITUT CURIE   (France)

^g CENTRE VAL D AURELLE   (France)

^h Institut Cochin   (France)

ⁱ UNIVERSITY HOSPITAL JEAN MINJOZ   (France)

^j HÔPITAL DE HAUTEPIERRE   (France)

more..

Author keywords

Angiogenesis; Bevacizumab; Breast cancer; Tumor microenvironment

Indexed keywords

BEVACIZUMAB; CAPECITABINE; DOCETAXEL; PACLITAXEL; TRASTUZUMAB; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; ANGIOGENESIS INHIBITOR; TUMOR MARKER; VASCULOTROPIN A;

BREAST METASTASIS; CANCER SURVIVAL; CELL KILLING; DISEASE FREE INTERVAL; DRUG EFFICACY; DRUG MECHANISM; DRUG TARGETING; ENDOTHELIUM CELL; HUMAN; OVERALL SURVIVAL; PATIENT SELECTION; PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; REVIEW; TREATMENT RESPONSE; TREATMENT WITHDRAWAL; TUMOR CELL; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BREAST NEOPLASMS; DRUG EFFECTS; DRUG RESISTANCE; FEMALE; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PREDICTIVE VALUE; SIGNAL TRANSDUCTION; VASCULARIZATION;

ANGIOGENESIS INHIBITORS; ANIMALS; BEVACIZUMAB; BIOMARKERS, TUMOR; BREAST NEOPLASMS; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; NEOVASCULARIZATION, PATHOLOGIC; PATIENT SELECTION; PREDICTIVE VALUE OF TESTS; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84930665395     PISSN: 17762596     EISSN: 1776260X     Source Type: Journal    
DOI: 10.1007/s11523-014-0334-9     Document Type: Review

References (75)

1. Jain RK (1988) Determinants of tumor blood flow: a review. Cancer Res 48:2641–2658
2. Shannon AM, Bouchier-Hayes DJ, Condron CM, Toomey D (2003) Tumour hypoxia, chemotherapeutic resistance and hypoxia-related therapies. Cancer Treat Rev 29:297–307
3. Pouysségur J, Dayan F, Mazure NM (2006) Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441:437–443
4. Tannock IF, Rotin D (1989) Acid pH in tumors and its potential for therapeutic exploitation. Cancer Res 49:4373–4384
5. Kroemer G, Pouyssegur J (2008) Tumor cell metabolism: cancer’s Achilles’ heel. Cancer Cell 13:472–482
6. Hobbs SK, Monsky WL, Yuan F, Roberts WG, Griffith L, Torchilin VP, Jain RK (1998) Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment. Proc Natl Acad Sci U S A 95:4607–4612
7. Hashizume H, Baluk P, Morikawa S et al (2000) Openings between defective endothelial cells explain tumor vessel leakiness. Am J Pathol 156:1363–1380
8. Semenza GL (2010) Oxygen homeostasis. Wiley Interdiscip Rev Syst Biol Med 2:336–361
9. Folkman J (1971) Tumor angiogenesis: therapeutic implications. N Engl J Med 285:1182–1186
10. Dvorak HF (2002) Vascular permeability factor/vascular endothelial growth factor: a critical cytokine in tumor angiogenesis and a potential target for diagnosis and therapy. J Clin Oncol 20:4368–4380
11. Carmeliet P (2005) Angiogenesis in life, disease and medicine. Nature 438:932–936
12. Rafii S, Lyden D, Benezra R, Hattori K, Heissig B (2002) Vascular and haematopoietic stem cells: novel targets for anti-angiogenesis therapy? Nat Rev Cancer 2:826–835
13. Trédan O, Galmarini CM, Patel K, Tannock IF (2007) Drug resistance and the solid tumor microenvironment. J Natl Cancer Inst 99:1441–1454
14. Goel S, Duda DG, Xu L, Munn LL, Boucher Y, Fukumura D, Jain RK (2011) Normalization of the vasculature for treatment of cancer and other diseases. Physiol Rev 91:1071–1121
15. Willett CG, Boucher Y, di Tomaso E et al (2004) Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nat Med 10:145–147
16. Yanagisawa M, Yorozu K, Kurasawa M et al (2010) Bevacizumab improves the delivery and efficacy of paclitaxel. Anticancer Drugs 21:687–694
17. Jain RK (2001) Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy. Nat Med 7:987–989
18. Abramsson A, Lindblom P, Betsholtz C (2003) Endothelial and nonendothelial sources of PDGF-B regulate pericyte recruitment and influence vascular pattern formation in tumors. J Clin Invest 112:1142–1151
19. Inai T, Mancuso M, Hashizume H et al (2004) 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 165:35–52
20. Tong RT, Boucher Y, Kozin SV, Winkler F, Hicklin DJ, Jain RK (2004) 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 64:3731–3736
21. Greenberg JI, Shields DJ, Barillas SG et al (2008) A role for VEGF as a negative regulator of pericyte function and vessel maturation. Nature 456:809–813
22. Winkler F, Kozin SV, Tong RT et al (2004) Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: role of oxygenation, angiopoietin-1, and matrix metalloproteinases. Cancer Cell 6:553–563
23. Kamoun WS, Chae SS, Lacorre DA et al (2010) Simultaneous measurement of RBC velocity, flux, hematocrit and shear rate in vascular networks. Nat Methods 7:655–660
24. Jain RK (2005) Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307:58–62
25. Boucher Y, Jain RK (1992) Microvascular pressure is the principal driving force for interstitial hypertension in solid tumors: implications for vascular collapse. Cancer Res 52:5110–5114
26. Roh HD, Boucher Y, Kalnicki S, Buchsbaum R, Bloomer WD, Jain RK (1991) Interstitial hypertension in carcinoma of uterine cervix in patients: possible correlation with tumor oxygenation and radiation response. Cancer Res 51:6695–6698
27. Less JR, Posner MC, Boucher Y, Borochovitz D, Wolmark N, Jain RK (1992) Interstitial hypertension in human breast and colorectal tumors. Cancer Res 52:6371–6374
28. Leunig M, Goetz AE, Dellian M, Zetterer G, Gamarra F, Jain RK, Messmer K (1992) Interstitial fluid pressure in solid tumors following hyperthermia: possible correlation with therapeutic response. Cancer Res 52:487–490
29. Padera TP, Stoll BR, Tooredman JB, Capen D, di Tomaso E, Jain RK (2004) Pathology: cancer cells compress intratumour vessels. Nature 427:695
30. Teicher BA, Holden SA, Ara G, Korbut T, Menon K (1996) Comparison of several antiangiogenic regimens alone and with cytotoxic therapies in the Lewis lung carcinoma. Cancer Chemother Pharmacol 38:169–177
31. Bottsford-Miller JN, Coleman RL, Sood AK (2012) Resistance and escape from antiangiogenesis therapy: clinical implications and future strategies. J Clin Oncol 30:4026–4034
32. Uzzan B, Nicolas P, Cucherat M, Perret GY (2004) Microvessel density as a prognostic factor in women with breast cancer: a systematic review of the literature and meta-analysis. Cancer Res 64:2941–2955
33. Rau KM, Huang CC, Chiu TJ et al (2012) Neovascularization evaluated by CD105 correlates well with prognostic factors in breast cancers. Exp Ther Med 4:231–236
34. Tanaka F, Otake Y, Yanagihara K et al (2001) Evaluation of angiogenesis in non-small cell lung cancer: comparison between anti-CD34 antibody and anti-CD105 antibody. Clin Cancer Res 7:3410–3415
35. Fonsatti E, Del Vecchio L, Altomonte M et al (2001) Endoglin: an accessory component of the TGF-beta-binding receptor-complex with diagnostic, prognostic, and bioimmunotherapeutic potential in human malignancies. J Cell Physiol 188:1–7
36. Kumar S, Ghellal A, Li C, Byrne G, Haboubi N, Wang JM, Bundred N (1999) Breast carcinoma: vascular density determined using CD105 antibody correlates with tumor prognosis. Cancer Res 59:856–861
37. Weidner N, Semple JP, Welch WR, Folkman J (1991) Tumor angiogenesis and metastasis—correlation in invasive breast carcinoma. N Engl J Med 324:1–8
38. Weidner N, Folkman J, Pozza F et al (1992) Tumor angiogenesis: a new significant and independent prognostic indicator in early-stage breast carcinoma. J Natl Cancer Inst 84:1875–1887
39. Gasparini G, Toi M, Gion M et al (1997) Prognostic significance of vascular endothelial growth factor protein in node-negative breast carcinoma. J Natl Cancer Inst 89:139–147
40. Hansen S, Grabau DA, Sørensen FB, Bak M, Vach W, Rose C (2000) The prognostic value of angiogenesis by Chalkley counting in a confirmatory study design on 836 breast cancer patients. Clin Cancer Res 6:139–146
41. Kostopoulos I, Arapantoni-Dadioti P, Gogas H et al (2006) Evaluation of the prognostic value of HER-2 and VEGF in breast cancer patients participating in a randomized study with dose-dense sequential adjuvant chemotherapy. Breast Cancer Res Treat 96:251–261
42. Manders P, Beex LV, Tjan-Heijnen VC, Geurts-Moespot J, Van Tienoven TH, Foekens JA, Sweep CG (2002) The prognostic value of vascular endothelial growth factor in 574 node-negative breast cancer patients who did not receive adjuvant systemic therapy. Br J Cancer 87:772–778
43. Linderholm B, Bergqvist J, Hellborg H (2009) Shorter survival-times following adjuvant endocrine therapy in oestrogen- and progesterone-receptor positive breast cancer overexpressing HER2 and/or with an increased expression of vascular endothelial growth factor. Med Oncol 26:480–490
44. Bando H, Weich HA, Brokelmann M, Horiguchi S, Funata N, Ogawa T, Toi M (2005) Association between intratumoral free and total VEGF, soluble VEGFR-1, VEGFR-2 and prognosis in breast cancer. Br J Cancer 92:553–561
45. Ribeiro-Silva A, Ribeiro do Vale F, Zucoloto S (2006) Vascular endothelial growth factor expression in the basal subtype of breast carcinoma. Am J Clin Pathol 125:512–518
46. Liu Y, Tamimi RM, Collins LC, Schnitt SJ, Gilmore HL, Connolly JL, Colditz GA (2011) The association between vascular endothelial growth factor expression in invasive breast cancer and survival varies with intrinsic subtypes and use of adjuvant systemic therapy: results from the nurses’ health study. Breast Cancer Res Treat 129:175–184
47. Nalwoga H, Arnes JB, Stefansson IM, Wabinga H, Foulkes WD, Akslen LA (2011) Vascular proliferation is increased in basal-like breast cancer. Breast Cancer Res Treat 130:1063–1071
48. Linderholm BK, Hellborg H, Johansson U, Elmberger G, Skoog L, Lehtiö J, Lewensohn R (2009) Significantly higher levels of vascular endothelial growth factor (VEGF) and shorter survival times for patients with primary operable triple-negative breast cancer. Ann Oncol 20:1639–1646
49. Miller K, Wang M, Gralow J et al (2007) Paclitaxel plus bevacizumab versus paclitaxel alone for metastatic breast cancer. N Engl J Med 357:2666–2676
50. Miles DW, Chan A, Dirix LY et al (2010) Phase III study of bevacizumab plus docetaxel compared with placebo plus docetaxel for the first-line treatment of human epidermal growth factor receptor 2-negative metastatic breast cancer. J Clin Oncol 28:3239–3247
51. Robert NJ, Diéras V, Glaspy J et al (2011) RIBBON-1: randomized, double-blind placebo-controlled, phase III trial of chemotherapy with or without bevacizumab for first-line treatment of human epidermal growth factor receptor 2-negative, locally recurrent or metastatic breast cancer. J Clin Oncol 29:1252–1260
52. Rossari JR, Metzger-Filho O, Paesmans M, Saini KS, Gennari A, de Azambuja E, Piccart-Gebhart M (2012) Bevacizumab and breast cancer: a meta-analysis of first-line phase III studies and a critical reappraisal of available evidence. J Oncol 2012:417673
53. Griffon-Etienne G, Boucher Y, Brekken C, Suit HD, Jain RK (1999) Taxane-induced apoptosis decompresses blood vessels and lowers interstitial fluid pressure in solid tumors: clinical implications. Cancer Res 59:3776–3782
54. Lang I, Brodowicz T, Ryvo L et al (2013) Bevacizumab plus paclitaxel versus bevacizumab plus capecitabine as first-line treatment for HER2-negative metastatic breast cancer: interim efficacy results of the randomised, open-label, non-inferiority, phase 3 TURANDOT trial. Lancet Oncol 14:125–133
55. Gianni L, Romieu GH, Lichinitser M et al (2013) AVEREL: a randomized phase III Trial evaluating bevacizumab in combination with docetaxel and trastuzumab as first-line therapy for HER2-positive locally recurrent/metastatic breast cancer. J Clin Oncol 31:1719–1725
56. Miller KD, Chap LI, Holmes FA et al (2005) Randomized phase III trial of capecitabine compared with bevacizumab plus capecitabine in patients with previously treated metastatic breast cancer. J Clin Oncol 23:792–799
57. Brufsky AM, Hurvitz S, Perez E, Swamy R, Valero V, O’Neill V, Rugo HS (2011) RIBBON-2: a randomized, double-blind, placebo-controlled, phase III trial evaluating the efficacy and safety of bevacizumab in combination with chemotherapy for second-line treatment of human epidermal growth factor receptor 2-negative metastatic breast cancer. J Clin Oncol 29:4286–4293
58. Pàez-Ribes M, Allen E, Hudock J et al (2009) Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 15:220–231
59. Miles D, Harbeck N, Escudier B et al (2011) Disease course patterns after discontinuation of bevacizumab: pooled analysis of randomized phase III trials. J Clin Oncol 29:83–88
60. Lim E, Vaillant F, Wu D et al (2009) Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat Med 15:907–913
61. Charafe-Jauffret E, Monville F, Bertucci F et al (2007) Moesin expression is a marker of basal breast carcinomas. Int J Cancer 121:1779–1785
62. Foulkes WD, Brunet JS, Stefansson IM et al (2004) The prognostic implication of the basal-like (cyclin E high/p27 low/p53+/glomeruloid-microvascular-proliferation+) phenotype of BRCA1-related breast cancer. Cancer Res 64:830–835
63. O’Shaughnessy J. Dieras V. Glaspy J et al. (2009) Comparison of subgroup analyses of PFS from three phase III studies of bevacizumab in combination with chemotherapy in patients with HER2-negative metastatic breast cancer (MBC). San Antonio Breast Cancer Symposium: abstract 207
64. Thomssen C, Pierga JY, Pritchard KI et al (2012) First-line bevacizumab-containing therapy for triple-negative breast cancer: analysis of 585 patients treated in the ATHENA study. Oncology 82:218–227
65. von Minckwitz G, Eidtmann H, Rezai M et al (2012) Neoadjuvant chemotherapy and bevacizumab for HER2-negative breast cancer. N Engl J Med 366:299–309
66. Bear HD, Tang G, Rastogi P et al (2012) Bevacizumab added to neoadjuvant chemotherapy for breast cancer. N Engl J Med 366:310–320
67. Pierga JY, Petit T, Delozier T et al (2012) Neoadjuvant bevacizumab, trastuzumab, and chemotherapy for primary inflammatory HER2-positive breast cancer (BEVERLY-2): an open-label, single-arm phase 2 study. Lancet Oncol 13:375–384
68. Thukral A, Thomasson DM, Chow CK et al (2007) Inflammatory breast cancer: dynamic contrast-enhanced MR in patients receiving bevacizumab—initial experience. Radiology 244:727–735
69. Yang SX, Steinberg SM, Nguyen D, Wu TD, Modrusan Z, Swain SM (2008) Gene expression profile and angiogenic marker correlates with response to neoadjuvant bevacizumab followed by bevacizumab plus chemotherapy in breast cancer. Clin Cancer Res 14:5893–5899
70. Cameron D. Brown J. Dent R et al. (2014) Adjuvant bevacizumab-containing therapy in triple-negative breast cancer (BEATRICE): primary results of a randomised, phase 3 trial. Lancet Oncol (in press)
71. Van der Veldt AA, Lubberink M, Bahce I et al (2012) Rapid decrease in delivery of chemotherapy to tumors after anti-VEGF therapy: implications for scheduling of anti-angiogenic drugs. Cancer Cell 21:82–91
72. Heskamp S, Boerman OC, Molkenboer-Kuenen JD, Oyen WJ, van der Graaf WT, van Laarhoven HW (2013) Bevacizumab reduces tumor targeting of antiepidermal growth factor and anti-insulin-like growth factor 1 receptor antibodies. Int J Cancer 133:307–314
73. Allegra CJ, Yothers G, O’Connell MJ et al (2011) Phase III trial assessing bevacizumab in stages II and III carcinoma of the colon: results of NSABP protocol C-08. J Clin Oncol 29:11–16
74. de Gramont A, Van Cutsem E, Schmoll HJ et al (2012) Bevacizumab plus oxaliplatin-based chemotherapy as adjuvant treatment for colon cancer (AVANT): a phase 3 randomised controlled trial. Lancet Oncol 13:1225–1233
75. Jain RK (2013) Normalizing tumor microenvironment to treat cancer: bench to bedside to biomarkers. J Clin Oncol 31:2205–2218