Suppression of diabetes-induced retinal inflammation by blocking the angiotensin II type 1 receptor or its downstream nuclear factor-κB pathway

Investigative Ophthalmology and Visual Science

Volumn 48, Issue 9, 2007, Pages 4342-4350

  Nagai, Norihiro ^a   Izumi Nagai, Kanako ^a   Oike, Yuichi ^a   Koto, Takashi ^a   Satofuka, Shingo ^a   Ozawa, Yoko ^a   Yamashiro, Kenji ^b   Inoue, Makoto ^a   Tsubota, Kazuo ^a   Umezawa, Kazuo ^c   Ishida, Susumu ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b KOBE CITY MEDICAL CENTER GENERAL HOSPITAL   (Japan)

^c KEIO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

1 (4 DIMETHYLAMINO 3 METHYLBENZYL) 5 DIPHENYLACETYL 4,5,6,7 TETRAHYDRO 1H IMIDAZO[4,5 C]PYRIDINE 6 CARBOXYLIC ACID; ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN 2 RECEPTOR; ANGIOTENSIN II; CONCANAVALIN A; DEHYDROXYMETHYLEPOXYQUINOMICIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; LECTIN; MONOCYTE CHEMOTACTIC PROTEIN 1; SYNAPTOTAGMIN I; TELMISARTAN; VALSARTAN; VASCULOTROPIN; ANGIOTENSIN RECEPTOR ANTAGONIST; BENZAMIDE DERIVATIVE; CCL2 PROTEIN, MOUSE; CYCLOHEXANONE DERIVATIVE; DRUG DERIVATIVE; ICAM1 PROTEIN, MOUSE; IMIDAZOLE DERIVATIVE; MESSENGER RNA; PYRIDINE DERIVATIVE; TELMESTEINE; TETRAZOLE DERIVATIVE; THIAZOLIDINE DERIVATIVE; UNCLASSIFIED DRUG; VALINE; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CAPILLARY ENDOTHELIUM; CONTROLLED STUDY; DIABETIC RETINOPATHY; DRUG MECHANISM; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; LEUKOCYTE ADHERENCE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; RETINA BLOOD VESSEL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STREPTOZOCIN DIABETES; UPREGULATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL ADHESION; DRUG ANTAGONISM; EXPERIMENTAL DIABETES MELLITUS; LEUKOCYTE; METABOLISM; PHYSIOLOGY; RETINITIS;

ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; BENZAMIDES; BLOTTING, WESTERN; CELL ADHESION; CHEMOKINE CCL2; CYCLOHEXANONES; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; ENZYME-LINKED IMMUNOSORBENT ASSAY; IMIDAZOLES; INTERCELLULAR ADHESION MOLECULE-1; LEUKOCYTES; MALE; MICE; MICE, INBRED C57BL; NF-KAPPA B; PYRIDINES; RECEPTOR, ANGIOTENSIN, TYPE 1; RECEPTOR, ANGIOTENSIN, TYPE 2; RENIN-ANGIOTENSIN SYSTEM; RETINITIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TETRAZOLES; THIAZOLIDINES; VALINE; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 35148898712     PISSN: 01460404     EISSN: None     Source Type: Journal    
DOI: 10.1167/iovs.06-1473     Document Type: Article

References (60)

1. Frank RN. Diabetic retinopathy. N Engl J Med. 2004;50:48-58.
2. Ishida S, Usui T, Yamashiro K, et al. VEGF164-mediated inflammation is required for pathological, but not physiological, ischemia-induced retinal neovascularization. J Exp Med. 2003;198:483-489.
3. Ishida S, Usui T, Yamashiro K, et al. VEGF164 is proinflammatory in the diabetic retina. Invest Ophthalmol Vis Sci. 2003;44:2155-2162.
4. Ishida S, Yamashiro K, Usui T, et al. Leukocytes mediate retinal vascular remodeling during development and vaso-obliteration in disease. Nat Med. 2003;9:781-788.
5. Miyamoto K, Khosrof S, Bursell SE, et al. Prevention of leukostasis and vascular leakage in streptozotocin-induced diabetic retinopathy via intercellular adhesion molecule-1 inhibition. Proc Natl Acad Sci USA. 1999;96:10836-10841.
6. Joussen AM, Poulaki V, Le ML, et al. A central role for inflammation in the pathogenesis of diabetic retinopathy. FASEB J. 2004;18:1450-1452.
7. Joussen AM, Poulaki V, Qin W, et al. Retinal vascular endothelial growth factor Induces intercellular adhesion molecule-1 and endothelial nitric oxide synthase expression and initiates early diabetic retinal leukocyte adhesion in vivo. Am J Pathol. 2002;160:501-509.
8. Miyamoto K, Hiroshiba N, Tsujikawa A, Ogura Y. In vivo demonstration of increased leukocyte entrapment in retinal microcirculation of diabetic rats. Invest Ophthalmol Vis Sci. 1998;39:2190-2194.
9. Bolton SJ, Anthony DC, Perry VH. Loss of the tight junction proteins occludin and zonula occludens-1 from cerebral vascular endothelium during neutrophil-induced blood-brain barrier breakdown in vivo. Neuroscience. 1998;86:1245-1257.
10. Aiello LP, Avery RL, Arrigg PG, et al. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med. 1994;331:1480-1487.
11. Mitamura Y, Takeuchi S, Matsuda A, Tagawa Y, Mizue Y, Nishihira J. Monocyte chemotactic protein-1 in the vitreous of patients with proliferative diabetic retinopathy. Ophthalmologica. 2001;215:415-418.
12. McLeod DS, Lefer DJ, Merges C, Lutty GA. Enhanced expression of intracellular adhesion molecule-1 and P-selectin in the diabetic human retina and choroid. Am J Pathol. 1995;147:642-653.
13. de Gasparo M, Catt KJ, Inagami T, Wright JW, Unger T. International union of pharmacology. XXIII. The angiotensin II receptors. Pharmacol Rev. 2000;52:415-472.
14. Moravski CJ, Kelly DJ, Cooper ME, et al. Retinal neovascularization is prevented by blockade of the renin-angiotensin system. Hypertension. 2000;36:1099-1104.
15. Egami K, Murohara T, Shimada T, et al. Role of host angiotensin II type 1 receptor in tumor angiogenesis and growth. J Clin Invest. 2003;112:67-75.
16. Candido R, Allen TJ, Lassila M, et al. Irbesartan but not amlodipine suppresses diabetes-associated atherosclerosis. Circulation. 2004;109:1536-1542.
17. Nagai N, Noda K, Urano T, et al. Selective suppression of pathological, but not physiological, retinal neovascularization by blocking angiotensin II type 1 receptor. Invest Ophthalmol Vis Sci. 2005;46:1078-1084.
18. Nagai N, Oike Y, Noda K, et al. Suppression of ocular inflammation in endotoxin-induced uveitis by blocking angiotensin II type 1 receptor. Invest Ophthalmol Vis Sci. 2005;46:2925-2931.
19. Nagai N, Oike Y, Izumi-Nagai K, et al. Angiotensin II Type 1 receptor-mediated inflammation is required for choroidal neovascularization. Arterioscler Thromb Vasc Biol. 2006;26:2252-2259.
20. Baldwin AS Jr. The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu Rev Immunol. 1996;14:649-683.
21. Suzuki Y, Ruiz-Ortega M, Lorenzo O, Ruperez M, Esteban V, Egido J. Inflammation and angiotensin II. Int J Biochem Cell Biol. 2003;35:881-900.
22. Kowluru RA, Koppolu P, Chakrabarti S, Chen S. Diabetes-induced activation of nuclear transcriptional factor in the retina, and its inhibition by antioxidants. Free Radic Res. 2003;37:1169-1180.
23. Chaturvedi N, Sjolie AK, Stephenson JM, et al. Effect of lisinopril on progression of retinopathy in normotensive people with type 1 diabetes. The EUCLID Study Group. EURODIAB Controlled Trial of Lisinopril in Insulin-Dependent Diabetes Mellitus. Lancet. 1998;351:28-31.
24. Gilbert RE, Kelly DJ, Cox AJ, et al. Angiotensin converting enzyme inhibition reduces retinal overexpression of vascular endothelial growth factor and hyperpermeability in experimental diabetes. Diabetologia. 2000;43:1360-1367.
25. Horio N, Clermont AC, Abiko A, et al. Angiotensin AT(1) receptor antagonism normalizes retinal blood flow and acetylcholine-induced vasodilatation in normotensive diabetic rats. Diabetologia. 2003;47:113-123.
26. Zhang X, Lassila M, Cooper ME, Cao Z. Retinal expression of vascular endothelial growth factor is mediated by angiotensin type 1 and type 2 receptors. Hypertension. 2004;43:276-281.
27. Umezawa K, Chaicharoenpong C. Molecular design and biological activities of NF-kappaB inhibitors. Mol Cell. 2002;14:163-167.
28. Suzuki Y, Sugiyama C, Ohno O, Umezawa K. Preparation and biological activities of optically active dehydroxymethylepoxyquinomicin, a novel NF-κB inhibitor. Tetrahedron. 2004;60:7061-7066.
29. Kurihara T, Ozawa Y, Shinoda K, et al. Neuroprotective effects of angiotensin II type 1 receptor (AT1R) blocker, telmisartan, via modulating AT1R and AT2R signaling in retinal inflammation. Invest Ophthalmol Vis Sci. 2006;47:5545-5552.
30. Kobori H, Ozawa Y, Suzaki Y, Nishiyama A. Enhanced intrarenal angiotensinogen contributes to early renal injury in spontaneously hypertensive rats. J Am Soc Nephrol. 2005;16:2073-2080.
31. Sarlos S, Rizkalla B, Moravski CJ, Cao Z, Cooper ME, Wilkinson-Berka JL. Retinal angiogenesis is mediated by an interaction between the angiotensin type 2 receptor, VEGF, and angiopoietin. Am J Pathol. 2003;163:879-887.
32. Satofuka S, Ichihara A, Nagai N, et al. Suppression of ocular inflammation in endotoxin-induced uveitis by inhibiting nonproteolytic activation of prorenin. Invest Ophthalmol Vis Sci. 2006;47:2686-2692.
33. Satofuka S, Ichihara A, Nagai N, et al. Role of nonproteolytically activated prorenin in pathologic, but not physiologic, retinal neovascularization. Invest Ophthalmol Vis Sci. 2007;48:422-429.
34. Rincon-Choles H, Kasinath BS, Gorin Y, Abboud HE. Angiotensin II and growth factors in the pathogenesis of diabetic nephropathy. Kidney Int Suppl. 2002;82:8-11.
35. Tikellis C, Wookey PJ, Candido R, Andrikopoulos S, Thomas MC, Cooper ME. Improved islet morphology after blockade of the renin- angiotensin system in the ZDF rat. Diabetes. 2004;53:989-997.
36. Zhang SL, Filep JG, Hohman TC, Tang SS, Ingelfinger JR, Chan JS. Molecular mechanisms of glucose action on angiotensinogen gene expression in rat proximal tubular cells. Kidney Int. 1999;55:454-464.
37. Funatsu H, Yamashita H, Nakanishi Y, Hori S. Angiotensin II and vascular endothelial growth factor in the vitreous fluid of patients with proliferative diabetic retinopathy. Br J Ophthalmol. 2002;86:311-315.
38. Funatsu H, Yamashita H, Ikeda T, Nakanishi Y, Kitano S, Hori S. Angiotensin II and vascular endothelial growth factor in the vitreous fluid of patients with diabetic macular edema and other retinal disorders. Am J Ophthalmol. 2002;133:537-543.
39. Miyahara S, Kiryu J, Miyamoto K, et al. In vivo three-dimensional evaluation of leukocyte behavior in retinal microcirculation of mice. Invest Ophthalmol Vis Sci. 2004;45:4197-4201.
40. Mori F, Hikichi T, Nagaoka T, Takahashi J, Kitaya N, Yoshida A. Inhibitory effect of losartan, an AT1 angiotensin II receptor antagonist, on increased leucocyte entrapment in retinal microcirculation of diabetic rats. Br J Ophthalmol. 2002;86:1172-1174.
41. Smith CW, Marlin SD, Rothlein R, Toman C, Anderson DC. Cooperative interactions of LFA-1 and Mac-1 with intercellular adhesion molecule-1 in facilitating adherence and transendothelial migration of human neutrophils in vitro. J Clin Invest. 1989;83:2008-2017.
42. Adamis AP, Miller JW, Bernal MT, et al. Increased vascular endothelial growth factor levels in the vitreous of eyes with proliferative diabetic retinopathy. Am J Ophthalmol. 1994;118:445-450.
43. Aiello LP, Avery RL, Arrigg PG, et al. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med. 1994;331:1480-1487.
44. Tanaka Y, Katoh S, Hori S, Miura M, Yamashita H. Vascular endothelial growth factor in diabetic retinopathy. Lancet. 1997;349:1520.
45. Cunningham ET Jr, Adamis AP, Altaweel M, et al. Macugen Diabetic Retinopathy Study Group. A phase II randomized double-masked trial of pegaptanib, an anti-vascular endothelial growth factor aptamer, for diabetic macular edema. Ophthalmology. 2005;112:1747-1757.
46. Ruiz-Ortega M, Esteban V, Ruperez M, et al. Renal and vascular hypertension-induced inflammation: role of angiotensin II. Curr Opin Nephrol Hypertens. 2006;15:159-166.
47. Otani A, Takagi H, Suzuma K, Honda Y. Angiotensin II potentiates vascular endothelial growth factor-induced angiogenic activity in retinal microcapillary endothelial cells. Circ Res. 1998;82:619-628.
48. Ohta K, Nakayama K, Kurokawa T, Kikuchi T, Yoshimura N. Inhibitory effects of pyrrolidine dithiocarbamate on endotoxin-induced uveitis in Lewis rats. Invest Ophthalmol Vis Sci. 2002;43:744-750.
49. Matsumoto G, Namekawa J, Muta M, et al. Targeting of nuclear factor kappaB pathways by dehydroxymethylepoxyquinomicin, a novel inhibitor of breast carcinomas: antitumor and antiangiogenic potential in vivo. Clin Cancer Res. 2005;11:1287-1293.
50. Poma P, Notarbartolo M, Labbozzetta M, et al. Antitumor effects of the novel NF-kappaB inhibitor dehydroxymethyl-epoxyquinomicin on human hepatic cancer cells: analysis of synergy with cisplatin and of possible correlation with inhibition of pro-survival genes and IL-6 production. Int J Oncol. 2006;28:923-930.
51. Yoshida A, Yoshida S, Ishibashi T, Kuwano M, Inomata H. Suppression of retinal neovascularization by the NF-kappaB inhibitor pyrrolidine dithiocarbamate in mice. Invest Ophthalmol Vis Sci. 1999;40:1624-1629.
52. Ruderman NB, Williamson JR, Brownlee M. Glucose and diabetic vascular disease. FASEB J. 1992;6:2905-2914.
53. Morigi M, Angioletti S, Imberti B, et al. Leukocyte-endothelial interaction is augmented by high glucose concentrations and hyperglycemia in a NF-κB-dependent fashion. J Clin Invest. 1998;101:1905-1915.
54. Dragomir E, Tircol M, Manduteanu I, Voinea M, Simionescu M. Aspirin and PPAR-alpha activators inhibit monocyte chemoattractant protein-1 expression induced by high glucose concentration in human endothelial cells. Vasc Pharmacol. 2006;44:440-449.
55. Harada C, Okumura A, Namekata K, et al. Role of monocyte chemotactic protein-1 and nuclear factor kappa B in the pathogenesis of proliferative diabetic retinopathy. Diabetes Res Clin Prac. 2006;74:249-256.
56. Ding C, He Q, Li PA. Diabetes increases expression of ICAM after a brief period of cerebral ischemia. J Neuroimmunol. 2005;161:61-67.
57. Jariyapongskul A, Patumraj S, Yamaguchi S, Niimi H. The effect of long-term supplementation of vitamin C on leukocyte adhesion to the cerebral endothelium in STZ-induced diabetic rats. Clin Hemorheol Microcirc. 2002;27:67-76.
58. Brasier AR, Li J. Mechanisms for inducible control of angiotensinogen gene transcription. Hypertension. 1996;27:465-475.
59. Cowling RT, Gurantz D, Peng J, Dillmann WH, Greenberg BH. Transcription factor NF-kappa B is necessary for up-regulation of type 1 angiotensin II receptor mRNA in rat cardiac fibroblasts treated with tumor necrosis factor-alpha or interleukin-1 beta. J Biol Chem. 2002;277:5719-5724.
60. UK Prospective Diabetes Study Group. Tight blood pressure control and risk of macrovascular and microvascular complications in type 2 diabetes (UKPDS 38). BMJ. 1998;317:703-713.