Systemic VEGF inhibition accelerates experimental atherosclerosis and disrupts endothelial homeostasis - Implications for cardiovascular safety

International Journal of Cardiology

Volumn 168, Issue 3, 2013, Pages 2453-2461

  Winnik, Stephan ^a,b   Lohmann, Christine ^b   Siciliani, Giovanni ^b   Von Lukowicz, Tobias ^c   Kuschnerus, Kira ^b   Kraenkel, Nicolle ^b   Brokopp, Chad E ^b,d   Enseleit, Frank ^a   Michels, Stephan ^d   Ruschitzka, Frank ^a,b   Lüscher, Thomas F ^a,b   Matter, Christian M ^a,b  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF LÜBECK   (Germany)

^d TRIEMLI HOSPITAL   (Switzerland)

Author keywords

Adverse effects; Angiogenesis inhibitors; Cardiovascular diseases; Patient safety

Indexed keywords

APOLIPOPROTEIN E; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; NITRIC OXIDE; PLACEBO; SUPEROXIDE; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; VATALANIB; ANGIOGENESIS INHIBITOR; PHTHALAZINE DERIVATIVE; PYRIDINE DERIVATIVE; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA; AORTA ARCH; ARTICLE; ATHEROSCLEROSIS; BREAST METASTASIS; CELL PROLIFERATION; CHOLESTEROL DIET; CONTROLLED STUDY; DRUG SAFETY; ENDOTHELIUM CELL; HOMEOSTASIS; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; KNOCKOUT MOUSE; LEUKOCYTE; LYMPHOCYTE; MALE; MONOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CHEMICALLY INDUCED; DRUG EFFECTS; PATHOPHYSIOLOGY; VASCULAR ENDOTHELIUM;

ANGIOGENESIS INHIBITORS; ANIMALS; ATHEROSCLEROSIS; ENDOTHELIUM, VASCULAR; HOMEOSTASIS; MALE; MICE; MICE, INBRED C57BL; PHTHALAZINES; PYRIDINES; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84885622575     PISSN: 01675273     EISSN: 18741754     Source Type: Journal    
DOI: 10.1016/j.ijcard.2013.03.010     Document Type: Article

References (47)

1. P. Carmeliet, and R.K. Jain Molecular mechanisms and clinical applications of angiogenesis Nature 473 7347 2011 298 307
2. L.S. Lim, P. Mitchell, J.M. Seddon, F.G. Holz, and T.Y. Wong Age-related macular degeneration Lancet 379 9827 2012 1728 1738
3. M. Potente, H. Gerhardt, and P. Carmeliet Basic and therapeutic aspects of angiogenesis Cell 146 6 2011 873 887
4. K. Miller, M. Wang, and J. Gralow Paclitaxel plus bevacizumab versus paclitaxel alone for metastatic breast cancer N Engl J Med 357 26 2007 2666 2676
5. H. Hurwitz, L. Fehrenbacher, and W. Novotny Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer N Engl J Med 350 23 2004 2335 2342
6. A. Sandler, R. Gray, and M.C. Perry Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer N Engl J Med 355 24 2006 2542 2550
7. D.M. Brown, P.K. Kaiser, and M. Michels Ranibizumab versus verteporfin for neovascular age-related macular degeneration N Engl J Med 355 14 2006 1432 1444
8. P. Rosenfeld, D. Brown, and J. Heier Ranibizumab for neovascular age-related macular degeneration N Engl J Med. 355 14 2006 1419 1431
9. U. Chakravarthy, S.P. Harding, and C.A. Rogers Ranibizumab versus bevacizumab to treat neovascular age-related macular degeneration Ophthalmology 119 7 2012 1399 1411
10. D.F. Martin, M.G. Maguire, and S.L. Fine Ranibizumab and bevacizumab for treatment of neovascular age-related macular degeneration Ophthalmology 119 7 2012 1388 1398
11. D.M. Brown, P.A. Campochiaro, and R.P. Singh Ranibizumab for macular edema following central retinal vein occlusion Ophthalmology 117 6 2010 [1124-1133.e1]
12. M.J. Elman, N.M. Bressler, and H. Qin Expanded 2-year follow-up of ranibizumab plus prompt or deferred laser or triamcinolone plus prompt laser for diabetic macular edema Ophthalmology 118 4 2011 609 614
13. C. Cao, J. Wang, H. Bunjhoo, Y. Xu, and H. Fang Risk profile of bevacizumab in patients with non-small cell lung cancer: a meta-analysis of randomized controlled trials Acta Oncol 51 2 2012 151 156
14. T.K. Choueiri, F.A.B. Schutz, Y. Je, J.E. Rosenberg, and J. Bellmunt Risk of arterial thromboembolic events with sunitinib and sorafenib: a systematic review and meta-analysis of clinical trials J Clin Oncol 28 13 2010 2280 2285
15. V. Ranpura, S. Hapani, J. Chuang, and S. Wu Risk of cardiac ischemia and arterial thromboembolic events with the angiogenesis inhibitor bevacizumab in cancer patients: a meta-analysis of randomized controlled trials Acta Oncol 49 3 2010 287 297
16. F.A. Scappaticci, J.R. Skillings, and S.N. Holden Arterial thromboembolic events in patients with metastatic carcinoma treated with chemotherapy and bevacizumab J Natl Cancer Inst 99 16 2007 1232 1239
17. M.A. Hamburg Proposal to Withdraw Approval for the Breast Cancer Indication for AVASTIN (Bevacizumab) [Internet] 2011 Nov Department of Health and Human Services - Food and Drug Administration [Available from: http://www.fda.gov/downloads/NewsEvents/%20Newsroom/UCM280546.pdf ]
18. L.S. Lim, C.M.G. Cheung, P. Mitchell, and T.Y. Wong Emerging evidence concerning systemic safety of anti-VEGF agents-should ophthalmologists be concerned? Am J Ophthalmol 152 3 2011 329 331
19. S. Michels Is intravitreal bevacizumab (Avastin) safe? Br J Ophthalmol 90 11 2006 1333 1334
20. S.J. Bakri, M.R. Snyder, J.M. Reid, J.S. Pulido, and R.J. Singh Pharmacokinetics of intravitreal bevacizumab (Avastin) Ophthalmology 114 5 2007 855 859
21. J. Gaudreault Preclinical pharmacokinetics of ranibizumab (rhuFabV2) after a single intravitreal administration Invest Ophthalmol Vis Sci 46 2 2005 726 733
22. F. Girardi, E. Franceschi, and A.A. Brandes Cardiovascular safety of VEGF-targeting therapies: current evidence and handling strategies Oncologist 15 7 2010 683 694
23. S. Ylä-Herttuala, T.T. Rissanen, I. Vajanto, and J. Hartikainen Vascular endothelial growth factors J Am Coll Cardiol 49 10 2007 1015 1026
24. T. Asahara, C. Bauters, and C. Pastore Local delivery of vascular endothelial growth factor accelerates reendothelialization and attenuates intimal hyperplasia in balloon-injured rat carotid artery Circulation 91 11 1995 2793 2801
25. M.O. Hiltunen, M. Laitinen, and M.P. Turunen Intravascular adenovirus-mediated VEGF-C gene transfer reduces neointima formation in balloon-denuded rabbit aorta Circulation 102 18 2000 2262 2268
26. M. Laitinen, I. Zachary, and G. Breier VEGF gene transfer reduces intimal thickening via increased production of nitric oxide in carotid arteries Hum Gene Ther 8 15 1997 1737 1744
27. P. Leppänen, S. Koota, and I. Kholová Gene transfers of vascular endothelial growth factor-A, vascular endothelial growth factor-B, vascular endothelial growth factor-C, and vascular endothelial growth factor-D have no effects on atherosclerosis in hypercholesterolemic low-density lipoprotein-receptor/apolipoprotein B48-deficient mice Circulation 112 9 2005 1347 1352
28. F.L. Celletti, J.M. Waugh, P.G. Amabile, A. Brendolan, P.R. Hilfiker, and M.D. Dake Vascular endothelial growth factor enhances atherosclerotic plaque progression Nat Med 7 4 2001 425 429
29. F.D. Kolodgie, H.K. Gold, and A.P. Burke Intraplaque hemorrhage and progression of coronary atheroma N Engl J Med 349 24 2003 2316 2325
30. K.S. Moulton, K. Vakili, and D. Zurakowski Inhibition of plaque neovascularization reduces macrophage accumulation and progression of advanced atherosclerosis Proc Natl Acad Sci U S A 100 8 2003 4736 4741
31. J. Kastrup, E. Jørgensen, and A. Rück Direct intramyocardial plasmid vascular endothelial growth factor-A165 gene therapy in patients with stable severe angina pectoris. A randomized double-blind placebo-controlled study: The Euroinject One trial J Am Coll Cardiol 45 7 2005 982 988
32. T.D. Henry The VIVA trial: vascular endothelial growth factor in ischemia for vascular angiogenesis Circulation 107 10 2003 1359 1365
33. K. Makinen Increased vascularity detected by digital subtraction angiography after VEGF gene transfer to human lower limb artery: a randomized, placebo-controlled, double-blinded phase II study Mol Ther 6 1 2002 127 133
34. W.M. Howell VEGF polymorphisms and severity of atherosclerosis J Med Genet 42 6 2005 485 490
35. J.M. Wood, G. Bold, and E. Buchdunger PTK787/ZK 222584, a novel and potent inhibitor of vascular endothelial growth factor receptor tyrosine kinases, impairs vascular endothelial growth factor-induced responses and tumor growth after oral administration Cancer Res 60 8 2000 2178 2189
36. R. Ricci, G. Sumara, and I. Sumara Requirement of JNK2 for scavenger receptor a - mediated foam cell formation in atherogenesis Science 306 5701 2004 1558 1561
37. S. Winnik, C. Lohmann, and E.K. Richter Dietary α-linolenic acid diminishes experimental atherogenesis and restricts T cell-driven inflammation Eur Heart J 32 20 2011 2573 2584
38. T. von Lukowicz, P.O. Hassa, and C. Lohmann PARP1 is required for adhesion molecule expression in atherogenesis Cardiovasc Res 78 1 2008 158 166
39. E. Lutgens, L. Gorelik, and M.J. Daemen Requirement for CD154 in the progression of atherosclerosis Nat Med 5 11 1999 1313 1316
40. S. Stein, N. Schaefer, and A. Breitenstein SIRT1 reduces endothelial activation without affecting vascular function in ApoE-/-mice Aging (Albany NY) 2 6 2010 353
41. M.I. van der Reis, E.C. La Heij, Y. De Jong-Hesse, P.J. Ringens, F. Hendrikse, and J.S.A.G. Schouten A systematic review of the adverse events of intravitreal anti-vascular endothelial growth factor injections Retina 31 8 2011 1449 1469
42. L.R. de Brito, M.A. Batey, and Y. Zhao Comparative pre-clinical evaluation of receptor tyrosine kinase inhibitors for the treatment of multiple myeloma Leuk Res 35 9 2011 1233 1240
43. T. Murohara, J.R. Horowitz, and M. Silver Vascular endothelial growth factor/vascular permeability factor enhances vascular permeability via nitric oxide and prostacyclin Circulation 97 1 1998 99 107
44. R.L. Stone, A.K. Sood, and R.L. Coleman Collateral damage: toxic effects of targeted antiangiogenic therapies in ovarian cancer Lancet Oncol 11 5 2010 465 475
45. S. Ylä-Herttuala, J.E. Markkanen, and T.T. Rissanen Gene therapy for ischemic cardiovascular diseases: some lessons learned from the first clinical trials Trends Cardiovasc Med 14 8 2004 295 300
46. A. Daugherty Mouse models of atherosclerosis Am J Med Sci 323 1 2002 3 10
47. K. Kinnunen, and S. Ylä-Herttuala Gene therapy in age related macular degeneration and hereditary macular disorders Front Biosci (Elite Ed) 44 1 2012 2546 2557