Candesartan, an angiotensin II type 1 receptor antagonist, inhibits pathological retinal neovascularization by downregulating VEGF receptor-2 expression

European Journal of Pharmacology

Volumn 685, Issue 1-3, 2012, Pages 8-14

  Nakamura, Shinsuke ^a   Tsuruma, Kazuhiro ^a   Shimazawa, Masamitsu ^a   Hara, Hideaki ^a  

^a GIFU PHARMACEUTICAL UNIVERSITY   (Japan)

Author keywords

Angiotensin II; Angiotensin II type 1 receptor; Candesartan; Retinal neovascularization; Vascular endothelial growth factor

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; CANDESARTAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; DOSE RESPONSE; DOWN REGULATION; DRUG DOSE COMPARISON; DRUG EFFECT; GENE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HYPOXIA INDUCIBLE FACTOR 1 ALPHA GENE; IN VITRO STUDY; IN VIVO STUDY; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; RETINA CELL; RETINA NEOVASCULARIZATION; RETINOPATHY; SIGNAL TRANSDUCTION; UPREGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A GENE; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR 1 GENE; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR 2 GENE;

ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; BENZIMIDAZOLES; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; HUMANS; MICE; MICE, INBRED C57BL; OXYGEN; POLYMERASE CHAIN REACTION; RETINAL DISEASES; RETINAL NEOVASCULARIZATION; TETRAZOLES; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84861343998     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2012.04.017     Document Type: Article

References (65)

1. L.P. Aiello Vascular endothelial growth factor and the eye: biochemical mechanisms of action and implications for novel therapies Ophthalmic Res. 29 1997 354 362
2. E. Banin, M.I. Dorrell, E. Aguilar, M.R. Ritter, C.M. Aderman, A.C. Smith, J. Friedlander, and M. Friedlander T2-TrpRS inhibits preretinal neovascularization and enhances physiological vascular regrowth in OIR as assessed by a new method of quantification Invest. Ophthalmol. Vis. Sci. 47 2006 2125 2134
3. S.J. Budd, H. Thompson, and M.E. Hartnett Association of retinal vascular endothelial growth factor with avascular retina in a rat model of retinopathy of prematurity Arch. Ophthalmol. 128 2010 1014 1021
4. G. Castoldi, C.R. Di Gioia, F. Pieruzzi, C. D'Orlando, W.M. Van De Greef, G. Busca, G. Sperti, and A. Stella ANG II increases TIMP-1 expression in rat aortic smooth muscle cells in vivo Am. J. Physiol. Heart Circ. Physiol. 284 2003 H635 H643
5. Y. Chikaraishi, M. Shimazawa, and H. Hara New quantitative analysis, using high-resolution images, of oxygen-induced retinal neovascularization in mice Exp. Eye Res. 84 2007 529 536
6. Y. Chikaraishi, N. Matsunaga, M. Shimazawa, and H. Hara Rifampicin inhibits the retinal neovascularization in vitro and in vivo Exp. Eye Res. 86 2008 131 137
7. C.C. Chua, R.C. Hamdy, and B.H. Chua Upregulation of vascular endothelial growth factor by angiotensin II in rat heart endothelial cells Biochim. Biophys. Acta 1401 1998 187 194
8. M.L. Corcoran, R.E. Hewitt, D.E. Kleiner Jr., and W.G. Stetler-Stevenson MMP-2: expression, activation and inhibition Enzyme Protein 49 1996 7 19
9. A.H. Danser, M.A. van den Dorpel, J. Deinum, F.H. Derkx, A.A. Franken, E. Peperkamp, P.T. de Jong, and M.A. Schalekamp Renin, prorenin, and immunoreactive renin in vitreous fluid from eyes with and without diabetic retinopathy J. Clin. Endocrinol. Metab. 68 1989 160 167
10. M. de Gasparo, K.J. Catt, T. Inagami, J.W. Wright, and T. Unger International union of pharmacology. XXIII. The angiotensin II receptors. Pharmacol. Rev. 52 2000 415 472
11. M. DeNiro, A. Al-Halafi, F.H. Al-Mohanna, O. Alsmadi, and F.A. Al-Mohanna Pleiotropic effects of YC-1 selectively inhibit pathological retinal neovascularization and promote physiological revascularization in a mouse model of oxygen-induced retinopathy Mol. Pharmacol. 77 2010 348 367
12. 1 receptor inhibition prevents astrocyte degeneration and restores vascular growth in oxygen-induced retinopathy Glia 56 2008 1076 1090
13. M.J. Eagleton, N. Ballard, E. Lynch, S.D. Srivastava, G.R. Upchurch Jr., and J.C. Stanley Early increased MT1-MMP expression and late MMP-2 and MMP-9 activity during angiotensin II induced aneurysm formation J. Surg. Res. 135 2006 345 351
14. K. Egami, T. Murohara, T. Shimada, K. Sasaki, S. Shintani, T. Sugaya, M. Ishii, T. Akagi, H. Ikeda, T. Matsuishi, and T. Imaizumi Role of host angiotensin II type 1 receptor in tumor angiogenesis and growth J. Clin. Invest. 112 2003 67 75
15. N. Ferrara Role of vascular endothelial growth factor in the regulation of angiogenesis Kidney Int. 56 1999 794 814
16. J.A. Forsythe, B.H. Jiang, N.V. Iyer, F. Agani, S.W. Leung, R.D. Koos, and G.L. Semenza Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1 Mol. Cell. Biol. 16 1996 4604 4613
17. M. Friedlander Fibrosis and diseases of the eye J. Clin. Invest. 117 2007 576 586
18. H. Fu, N. Hosomi, N. Pelisch, D. Nakano, G. Liu, M. Ueno, T. Miki, H. Masugata, Y. Sueda, T. Itano, M. Matsumoto, A. Nishiyama, and M. Kohno Therapeutic effects of postischemic treatment with hypotensive doses of an angiotensin II receptor blocker on transient focal cerebral ischemia J. Hypertens. 29 2011 2210 2219
19. H. Funatsu, H. Yamashita, T. Ikeda, Y. Nakanishi, S. Kitano, and S. Hori Angiotensin II and vascular endothelial growth factor in the vitreous fluid of patients with diabetic macular edema and other retinal disorders Am. J. Ophthalmol. 133 2002 537 543
20. R.F. Gariano, and T.W. Gardner Retinal angiogenesis in development and disease Nature 438 2005 960 966
21. S. Hiratsuka, Y. Maru, A. Okada, M. Seiki, T. Noda, and M. Shibuya Involvement of Flt-1 tyrosine kinase (vascular endothelial growth factor receptor-1) in pathological angiogenesis Cancer Res. 61 2001 1207 1213
22. N. Hosomi, A. Nishiyama, C.R. Ban, T. Naya, T. Takahashi, M. Kohno, and J.A. Koziol Angiotensin type 1 receptor blockage improves ischemic injury following transient focal cerebral ischemia Neuroscience 134 2005 225 231
23. W. Huang, L.F. Yu, J. Zhong, M.M. Qiao, F.X. Jiang, F. Du, X.L. Tian, and Y.L. Wu Angiotensin II type 1 receptor expression in human gastric cancer and induces MMP2 and MMP9 expression in MKN-28 cells Dig. Dis. Sci. 53 2008 163 168
24. E.R. Inwang, J.R. Puddefoot, C.L. Brown, A.W. Goode, S. Marsigliante, M.M. Ho, J.G. Payne, and G.P. Vinson Angiotensin II type 1 receptor expression in human breast tissues Br. J. Cancer 75 1997 1279 1283
25. N. Kociok, S. Radetzky, T.U. Krohne, C. Gavranic, and A.M. Joussen Pathological but not physiological retinal neovascularization is altered in TNF-Rp55-receptor-deficient mice Invest. Ophthalmol. Vis. Sci. 47 2006 5057 5065
26. M. Kosugi, A. Miyajima, E. Kikuchi, Y. Horiguchi, and M. Murai Angiotensin II type 1 receptor antagonist candesartan as an angiogenic inhibitor in a xenograft model of bladder cancer Clin. Cancer Res. 12 2006 2888 2893
27. L.E. Kotch, N.V. Iyer, E. Laughner, and G.L. Semenza Defective vascularization of HIF-1alpha-null embryos is not associated with VEGF deficiency but with mesenchymal cell death Dev. Biol. 209 1999 254 267
28. 1 receptor Nature 375 1995 247 250
29. N. Matsunaga, Y. Chikaraishi, H. Izuta, N. Ogata, M. Shimazawa, M. Matsumura, and H. Hara Role of soluble vascular endothelial growth factor receptor-1 in the vitreous in proliferative diabetic retinopathy Ophthalmology 115 2008 1916 1922
30. C.D. McWhinney, R.A. Hunt, K.M. Conrad, D.E. Dostal, and K.M. Baker The type I angiotensin II receptor couples to Stat1 and Stat3 activation through Jak2 kinase in neonatal rat cardiac myocytes J. Mol. Cell. Cardiol. 29 1997 2513 2524
31. F. Michel, J.S. Silvestre, L. Waeckel, S. Corda, T. Verbeuren, J.P. Vilaine, M. Clergue, M. Duriez, and B.I. Levy Thromboxane A2/prostaglandin H2 receptor activation mediates angiotensin II-induced postischemic neovascularization Arterioscler. Thromb. Vasc. Biol. 26 2006 488 493
32. J.W. Miller, A.P. Adamis, D.T. Shima, P.A. D'Amore, R.S. Moulton, M.S. O'Reilly, J. Folkman, H.F. Dvorak, L.F. Brown, and B. Berse Vascular endothelial growth factor/vascular permeability factor is temporally and spatially correlated with ocular angiogenesis in a primate model Am. J. Pathol. 145 1994 574 584
33. Y. Mizukami, K. Fujiki, E.M. Duerr, M. Gala, W.S. Jo, X. Zhang, and D.C. Chung Hypoxic regulation of vascular endothelial growth factor through the induction of phosphatidylinositol 3-kinase/Rho/ROCK and c-Myc J. Biol. Chem. 281 2006 13957 13963
34. C.J. Moravski, D.J. Kelly, M.E. Cooper, R.E. Gilbert, J.F. Bertram, S. Shahinfar, S.L. Skinner, and J.L. Wilkinson-Berka Retinal neovascularization is prevented by blockade of the renin-angiotensin system Hypertension 36 2000 1099 1104
35. T.J. Murphy, R.W. Alexander, K.K. Griendling, M.S. Runge, and K.E. Bernstein Isolation of a cDNA encoding the vascular type-1 angiotensin II receptor Nature 351 1991 233 236
36. J.A. Nadal, G.M. Scicli, L.A. Carbini, and A.G. Scicli Angiotensin II stimulates migration of retinal microvascular pericytes: involvement of TGF-beta and PDGF-BB Am. J. Physiol. Heart Circ. Physiol. 282 2002 H739 H748
37. N. Nagai, Y. Oike, K. Noda, T. Urano, Y. Kubota, Y. Ozawa, H. Shinoda, T. Koto, K. Shinoda, M. Inoue, K. Tsubota, K. Yamashiro, T. Suda, and S. Ishida Suppression of ocular inflammation in endotoxin-induced uveitis by blocking the angiotensin II type 1 receptor Invest. Ophthalmol. Vis. Sci. 46 2005 2925 2931
38. Y. Nagisa, A. Shintani, and S. Nakagawa The angiotensin II receptor antagonist candesartan cilexetil (TCV-116) ameliorates retinal disorders in rats Diabetologia 44 2001 883 888
39. H. Nakamura, T. Inoue, N. Arakawa, Y. Shimizu, Y. Yoshigae, I. Fujimori, E. Shimakawa, T. Toyoshi, and T. Yokoyama Pharmacological and pharmacokinetic study of olmesartan medoxomil in animal diabetic retinopathy models Eur. J. Pharmacol. 512 2005 239 246
40. H. Nakamura, M. Yamazaki, T. Ohyama, T. Inoue, N. Arakawa, Y. Domon, and T. Yokoyama Role of angiotensin II type 1 receptor on retinal vascular leakage in a rat oxygen-induced retinopathy model Ophthalmic Res. 41 2009 210 215
41. S. Nakamura, Y. Chikaraishi, K. Tsuruma, M. Shimazawa, and H. Hara Ruboxistaurin, a PKCbeta inhibitor, inhibits retinal neovascularization via suppression of phosphorylation of ERK1/2 and Akt Exp. Eye Res. 90 2010 137 145
42. S. Nakamura, K. Hayashi, H. Takizawa, T. Murase, K. Tsuruma, M. Shimazawa, H. Kakuta, H. Nagasawa, and H. Hara An arylidene-thiazolidinedione derivative, GPU-4, without PPARgamma activation, reduces retinal neovascularization Curr. Neurovasc. Res. 8 2011 25 34
43. S. Nakamura, N. Morimoto, K. Tsuruma, H. Izuta, Y. Yasuda, N. Kato, T. Ikeda, M. Shimazawa, and H. Hara Tissue kallikrein inhibits retinal neovascularization via the cleavage of vascular endothelial growth factor-165 Arterioscler. Thromb. Vasc. Biol. 31 2011 1041 1048
44. A. Okamura, H. Rakugi, M. Ohishi, Y. Yanagitani, S. Takiuchi, K. Moriguchi, P.A. Fennessy, J. Higaki, and T. Ogihara Upregulation of renin-angiotensin system during differentiation of monocytes to macrophages J. Hypertens. 17 1999 537 545
45. A. Otani, H. Takagi, H. Oh, S. Koyama, and Y. Honda Angiotensin II induces expression of the Tie2 receptor ligand, angiopoietin-2, in bovine retinal endothelial cells Diabetes 50 2001 867 875
46. H. Ozaki, A.Y. Yu, N. Della, K. Ozaki, J.D. Luna, H. Yamada, S.F. Hackett, N. Okamoto, D.J. Zack, G.L. Semenza, and P.A. Campochiaro Hypoxia inducible factor-1alpha is increased in ischemic retina: temporal and spatial correlation with VEGF expression Invest. Ophthalmol. Vis. Sci. 40 1999 182 189
47. H. Ozaki, M.S. Seo, K. Ozaki, H. Yamada, E. Yamada, N. Okamoto, F. Hofmann, J.M. Wood, and P.A. Campochiaro Blockade of vascular endothelial cell growth factor receptor signaling is sufficient to completely prevent retinal neovascularization Am. J. Pathol. 156 2000 697 707
48. P. Pan, H. Fu, L. Zhang, H. Huang, F. Luo, W. Wu, Y. Guo, and X. Liu Angiotensin II upregulates the expression of placental growth factor in human vascular endothelial cells and smooth muscle cells BMC Cell Biol. 11 2010 36
49. N. Pelisch, N. Hosomi, M. Ueno, H. Masugata, K. Murao, H. Hitomi, D. Nakano, H. Kobori, A. Nishiyama, and M. Kohno Systemic candesartan reduces brain angiotensin II via downregulation of brain renin-angiotensin system Hypertens. Res. 33 2010 161 164
50. E.A. Pierce, R.L. Avery, E.D. Foley, L.P. Aiello, and L.E. Smith Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization Proc. Natl. Acad. Sci. U. S. A. 92 1995 905 909
51. 1 receptor subtypes and extracellular matrix turnover in mouse retinal pigment epithelium Exp. Eye Res. 89 2009 109 118
52. C. Pupilli, L. Lasagni, P. Romagnani, F. Bellini, M. Mannelli, N. Misciglia, C. Mavilia, U. Vellei, D. Villari, and M. Serio Angiotensin II stimulates the synthesis and secretion of vascular permeability factor/vascular endothelial growth factor in human mesangial cells J. Am. Soc. Nephrol. 10 1999 245 255
53. K. Sagawa, K. Nagatani, Y. Komagata, and K. Yamamoto Angiotensin receptor blockers suppress antigen-specific T cell responses and ameliorate collagen-induced arthritis in mice Arthritis Rheum. 52 2005 1920 1928
54. M. Saint-Geniez, and P.A. D'Amore Development and pathology of the hyaloid, choroidal and retinal vasculature Int. J. Dev. Biol. 48 2004 1045 1058
55. H. Sano, K. Hosokawa, H. Kidoya, and N. Takakura Negative regulation of VEGF-induced vascular leakage by blockade of angiotensin II type 1 receptor Arterioscler. Thromb. Vasc. Biol. 26 2006 2673 2680
56. K. Sasaki, T. Murohara, H. Ikeda, T. Sugaya, T. Shimada, S. Shintani, and T. Imaizumi Evidence for the importance of angiotensin II type 1 receptor in ischemia-induced angiogenesis J. Clin. Invest. 109 2002 603 611
57. M. Shibuya Differential roles of vascular endothelial growth factor receptor-1 and receptor-2 in angiogenesis J. Biochem. Mol. Biol. 39 2006 469 478
58. A.K. Sjolie, R. Klein, M. Porta, T. Orchard, J. Fuller, H.H. Parving, R. Bilous, and N. Chaturvedi Effect of candesartan on progression and regression of retinopathy in type 2 diabetes (DIRECT-Protect 2): a randomised placebo-controlled trial Lancet 372 2008 1385 1393
59. L.E. Smith, E. Wesolowski, A. McLellan, S.K. Kostyk, R. D'Amato, R. Sullivan, and P.A. D'Amore Oxygen-induced retinopathy in the mouse Invest. Ophthalmol. Vis. Sci. 35 1994 101 111
60. C. Sunderkotter, K. Steinbrink, M. Goebeler, R. Bhardwaj, and C. Sorg Macrophages and angiogenesis J. Leukoc. Biol. 55 1994 410 422
61. D.J. Van Dyk, A. Erman, T. Erman, B. Chen-Gal, J. Sulkes, and G. Boner Increased serum angiotensin converting enzyme activity in type I insulin-dependent diabetes mellitus: its relation to metabolic control and diabetic complications Eur. J. Clin. Invest. 24 1994 463 467
62. M. Wang, J. Zhang, G. Spinetti, L.Q. Jiang, R. Monticone, D. Zhao, L. Cheng, M. Krawczyk, M. Talan, G. Pintus, and E.G. Lakatta Angiotensin II activates matrix metalloproteinase type II and mimics age-associated carotid arterial remodeling in young rats Am. J. Pathol. 167 2005 1429 1442
63. J. Wasa, H. Sugiura, E. Kozawa, K. Kohyama, K. Yamada, and O. Taguchi The tumor suppressive effect of angiotensin II type 1 receptor antagonist in a murine osteosarcoma model Anticancer. Res. 31 2011 123 127
64. B. Williams, A.Q. Baker, B. Gallacher, and D. Lodwick Angiotensin II increases vascular permeability factor gene expression by human vascular smooth muscle cells Hypertension 25 1995 913 917
65. H. Yoshiji, S. Kuriyama, and H. Fukui Angiotensin-I-converting enzyme inhibitors may be an alternative anti-angiogenic strategy in the treatment of liver fibrosis and hepatocellular carcinoma. Possible role of vascular endothelial growth factor Tumour Biol. 23 2002 348 356