Bevacizumab-induced normalization of blood vessels in tumors hampers antibody uptake

Cancer Research

Volumn 73, Issue 11, 2013, Pages 3347-3355

  Arjaans, Marlous ^a   Munnink, Thijs H Oude ^a   Oosting, Sjoukje F ^a   Van Scheltinga, Anton G T Terwisscha ^a   Gietema, Jourik A ^a   Garbacik, Erik T ^b   Timmer Bosscha, Hetty ^a   Lub De Hooge, Marjolijn N ^a   Schröder, Carolina P ^a   De Vries, Elisabeth G E ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF TWENTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BEVACIZUMAB; BEVACIZUMAB ZR 89; IMMUNOGLOBULIN G ZR 89; RADIOPHARMACEUTICAL AGENT; TRASTUZUMAB ZR 89; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DETECTION; ANTIBODY LABELING; ARTICLE; CAPILLARY DENSITY; COMPUTED TOMOGRAPHY SCANNER; COMPUTER ASSISTED EMISSION TOMOGRAPHY; CONTROLLED STUDY; DRUG CLEARANCE; DRUG DISTRIBUTION; ESOPHAGUS CANCER; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMAGE PROCESSING; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROTEIN TRANSPORT; TUMOR GROWTH; TUMOR XENOGRAFT;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; DRUG INTERACTIONS; ESOPHAGEAL NEOPLASMS; FEMALE; HUMANS; IMMUNOGLOBULIN G; MALE; MICE; MICE, NUDE; NEOVASCULARIZATION, PATHOLOGIC; OVARIAN NEOPLASMS; POSITRON-EMISSION TOMOGRAPHY; RADIOISOTOPES; RADIOPHARMACEUTICALS; XENOGRAFT MODEL ANTITUMOR ASSAYS; ZIRCONIUM;

EID: 84878609062     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-3518     Document Type: Article

References (44)

1. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;11:646-74.
2. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003;9:669-76.
3. Carmeliet P, Jain RK. Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nat Rev Drug Discov 2011;10:417-27.
4. Goel S, Duda DG, Xu L, Munn LL, Boucher Y, Fukumura D, et al. Normalization of the vasculature for treatment of cancer and other diseases. Physiol Rev 2011;91:1071-121.
5. Ozerdem U, Stallcup WB. Early contribution of pericytes to angiogenic sprouting and tube formation. Angiogenesis 2003;6:241-49.
6. Yuan F, Chen Y, Dellian M, Safabakhsh N, Ferrara N, Jain RK. Timedependent 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 U S A 1996;93:14765-70.
7. Tong RT, Boucher Y, Kozin SV, Winkler F, Hicklin DJ, Jain RK. 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 2004;64: 3731-6.
8. Winkler F, Kozin SV, Tong RT, Chae SS, Booth MF, Garkavtsev I, 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;6:553-63.
9. Jain RK. Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy. Nat Med 2001;9:987-9.
10. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 2005;307:58-62.
11. Dickson PV, Hammer JB, Sims TL, Fraga CH, Ng CY, Rajasekeran S, et al. Bevacizumab-induced transient remodeling of the vasculature in neuroblastoma xenografts results in improved delivery and efficacy of systemically administered chemotherapy. Clin Cancer Res 2007;13: 3942-50.
12. Wildiers H, Guetens G, De Boeck G, Verbeken E, Landuyt B, Landuyt W, et al. Effect of antivascular endothelial growth factor treatment on the intratumoral uptake of CPT -11. Br J Cancer 2003;88:1979-86.
13. van der Veldt AA, Lubberink M, Bahce I, Walraven M, de Boer MP, Greuter HN, et al. Rapid decrease in delivery of chemotherapy to tumors after anti-VEGF therapy: implications for scheduling of antiangiogenic drugs. Cancer Cell 2012;21:82-91.
14. von Minckwitz G, Eidtmann H, Rezai M, Fasching PA, Tesch H, Eggemann H, et al. Neoadjuvant chemotherapy and bevacizumab for HER2-negative breast cancer. N Engl J Med 2012;366:299-309.
15. Bear HD, Tang G, Rastogi P, Geyer CE, Robidoux A, Atkins JN, et al. Bevacizumab added to neoadjuvant chemotherapy for breast cancer. N Engl J Med 2012;366:310-20.
16. Maeda H, Wu J, Sawa T, Matsumura Y, Hori K. Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review. J Control Release 2000;65:271-84.
17. Nakahara T, Norberg SM, Shalinsky DR, Hu-Lowe DD, McDonald DM. Effect of inhibition of vascular endothelial growth factor signaling on distribution of extravasated antibodies in tumors. Cancer Res 2006; 66:1434-45.
18. Tol J, Koopman M, Cats A, Rodenburg CJ, Creemers GJ, Schrama JG, et al. Chemotherapy, bevacizumab, and cetuximab in metastatic colorectal cancer. N Engl J Med 2009;360:563-72.
19. Hecht JR, Mitchell E, Chidiac T, Scroggin C, Hagenstad C, Spigel D, et al.Arandomized phase IIIB trial of chemotherapy, bevacizumab, and panitumumab compared with chemotherapy and bevacizumab alone for metastatic colorectal cancer. J Clin Oncol 2009;27:672-80.
20. Gianni L, Romieu G, Lichinitser M, Serrano S, Mansutti M, Pivot X, et al. First results of AVEREL, a randomized phase III trial to evaluate bevacizumab (BEV) in combination with trastuzumab (H) + docetaxel (DOC) as first-line therapy for HER2-positive locally recurrent/metastatic breast cancer (LR/mBC). SABCS 2011;71 (suppl). Abstract nr S4-8.
21. Arteaga CL, Mayer IA, O'Neill AM, Swaby RF, Alpaugh RK, Yang XJ, et al. A randomized phase III double-blinded placebo-controlled trial of first-line chemotherapy and trastuzumab with or without bevacizumab for patients with HER2/neu-overexpressing metastatic breast cancer (HER2+ MBC): A trials of the Eastern Cooperative Oncology Group (E1105). J Clin Oncol 2012;30 (suppl). Abstract nr 605.
22. Nagengast WB, de Vries EG, Hospers GA, Mulder NH, de Jong JR, Hollema H, et al. In vivo VEGF imaging with radiolabeled bevacizumab in a human ovarian tumor xenograft. J Nucl Med 2007;48:1313-9.
23. Dijkers EC, Oude Munnink TH, Kosterink JG, Brouwers AH, Jager PJ, de Jong J, et al. HER2 PET imaging with 89Zr-trastuzumab in metastatic breast cancer patients. Clin Pharmacol Ther 2010;87:586-92.
24. Dijkers ECF, Kosterink JG, Rademaker AP, Perk LR, Dongen van GA, Bart J, et al. Development and characterization of clinical-grade 89Zrtrastuzumab for HER2/neu immunoPET imaging. J Nucl Med 2009; 50:962-9.
25. Terwisscha van Scheltinga AG, van Dam GM, Nagengast WB, Ntziachristos V, Hollema H, Herek JL, et al. Intraoperative near-infrared fluorescence tumor imaging with vascular endothelial growth factor and human epidermal growth factor receptor 2 targeting antibodies. J Nucl Med 2011;52:1778-85.
26. Keyes KA, Mann L, Teicher B, Alvarez E. Site-dependent angiogenic cytokine production in human tumor xenografts. Cytokine 2003;21: 98-104.
27. Dahlberg PS, Jacobson BA, Dahal G, Fink JM, Kratzke RA, Maddaus MA, et al. ERBB2 amplifications in esophageal adenocarcinoma. Ann Thorac Surg 2004;78:1790-800.
28. Reddy N, Ong GL, Behr TM, Sharkey RM, Goldenberg DM, Mattes MJ. Rapid blood clearance of mouse IgG2a and human IgG1 in many nude and nu/+ mouse strains is due to low IgG2a serum concentrations. Cancer Immunol Immunother 1998;46:25-33.
29. Gerber HP, Ferrara N. Pharmacology and pharmacodynamics of bevacizumab as monotherapy or in combination with cytotoxic therapy in preclinical studies. Cancer Res 2005;65:671-80.
30. Oude Munnink TH, de Vries EG, Vedelaar SR, Timmer-Bosscha H, Schröder CP, Brouwers AH, et al. Lapatinib and 17AAG reduce 89Zrtrastuzumab-F(ab')2 uptake in SKBR3 tumor xenografts. Mol Pharm 2012;9:2995-3002.
31. Willett CG, Duda DG, di Tomaso E, Boucher Y, Ancukiewicz M, Sahani DV, et al. Efficacy, safety, and biomarkers of neoadjuvant bevacizumab, radiation therapy, and fluorouracil in rectal cancer: a multidisciplinary phase II study. J Clin Oncol 2009;27:3020-6.
32. Batchelor TT, Sorensen AG, di Tomaso E, Zhang WT, Duda DG, Cohen KS, et al. AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 2007;11:83-95.
33. Chauhan VP, Stylianopoulos T, Martin JD, Popovíc Z, Chen O, Kamoun WS, et al. Normalization of tumor blood vessels improves the delivery of nanomedicines in a size-dependent manner. Nat Nanotechnol 2012;7:383-8.
34. Pastuskovas CV, Mundo EE, Williams SP, Nayak TK, Ho J, Ulufatu S, et al. Effects of anti-VEGF on pharmacokinetics, biodistribution and tumor penetration of trastuzumab in a preclinical breast cancer model. Mol Cancer Ther 2012;11:752-62.
35. Le XF, Mao W, Lu C, Thornton A, Heymach JV, Sood AK, et al. Specific blockade of VEGF and HER2 pathways results in greater growth inhibition of breast cancer xenografts that overexpress HER2. Cell Cycle 2008;7:3747-58.
36. Traina TA, Higgins B, Theodoulou M, Dugan U, Kolinsky K, Zhang Y, et al. Preclinical testing of a novel regimen of capecitabine (C) in combination with bevacizumab (B) and trastuzumab (T) in a breast cancer xenograft model. J Clin Oncol 2007;25 (suppl). Abstract nr 1049.
37. Clynes RA, Towers TL, Presta LG, Ravetch JV. Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat Med 2000; 6:443-6.
38. zum Büschenfelde CM, Hermann C, Schmidt B, Peschel C, Bernhard H. Antihuman epidermal growth factor receptor 2 (HER2) monoclonal antibody trastuzumab enhances cytolytic activity of class I-restricted HER2-specific T lymphocytes against HER2-overexpressing tumor cells. Cancer Res 2002;62:2244-7.
39. Wolpoe ME, Lutz ER, Ercolini AM, Murata S, Ivie SE, Garrett ES, et al. HER-2/neu-specific monoclonal antibodies collaborate with HER-2/ neu-targeted granulocyte macrophage colony-stimulating factor secreting whole cell vaccination to augment CD8+ T cell effector function and tumor-free survival in Her-2/neu-transgenic mice. J Immunol 2003;171:2161-9.
40. Gennari R, Menard S, Fagnoni F, Ponchio L, Scelsi M, Tagliabue E, et al. Pilot study of the mechanism of action of preoperative trastuzumab in patients with primary operable breast tumors overexpressing HER2. Clin Cancer Res 2004;10:5650-5.
41. Jonker DJ, O'Callaghan CJ, Karapetis CS, Zalcberg JR, Tu D, Au HJ, et al. Cetuximab for the treatment of colorectal cancer. N Engl J Med 2007;357:2040-8.
42. Cunningham D, Humblet Y, Siena S, Khayat D, Bleiberg H, Santoro A, et al. Cetuximab monotherapy and cetuximab plus irinotecan in irinotecan refractory metastatic colorectal cancer. N Engl J Med 2004;351: 337-35.
43. Pander J, Heusinkveld M, van der Straaten T, Jordanova ES, Baak-Pablo R, Gelderblom H, et al. Activation of tumor-promoting type 2 macrophages by EGFR-targeting antibody cetuximab. Clin Cancer Res 2011;17:5668-73.
44. Oosting SF, Brouwers AH, Van Es SC, Nagengast WB, Oude Munnink TH, Lub-de Hooge MN, et al. 89Zr-bevacizumab PET imaging in metastatic renal cell carcinoma patients before and during antiangiogenic treatment. J Clin Oncol 2012;30 (suppl). Abstract nr 10581.