Alternative pathways in the development of diabetic retinopathy: The renin-angiotensin and kallikrein-kinin systems

Clinical and Experimental Optometry

Volumn 95, Issue 3, 2012, Pages 282-289

  Phipps, Joanna A ^a   Jobling, Andrew I ^a   Greferath, Ursula ^a   Fletcher, Erica L ^a   Vessey, Kirstan A ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Angiotensin; Diabetes; Kallikrein kinin; Retina; Retinopathy

Indexed keywords

ANIMAL; CLINICAL TRIAL (TOPIC); DIABETIC RETINOPATHY; HUMAN; KALLIKREIN KININ SYSTEM; PATHOPHYSIOLOGY; PHYSIOLOGY; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CLINICAL TRIALS AS TOPIC; DIABETIC RETINOPATHY; HUMANS; KALLIKREIN-KININ SYSTEM; RENIN-ANGIOTENSIN SYSTEM; SIGNAL TRANSDUCTION;

EID: 84861211421     PISSN: 08164622     EISSN: 14440938     Source Type: Journal    
DOI: 10.1111/j.1444-0938.2012.00747.x     Document Type: Review

References (99)

1. Mohamed Q, Gillies MC, Wong TY. Management of diabetic retinopathy: a systematic review. JAMA 2007; 298: 902-916.
2. Klein R, Klein BE, Moss SE, Davis MD, DeMets DL. The Wisconsin Epidemiologic Study of Diabetic Retinopathy. II. Prevalence and risk of diabetic retinopathy when age at diagnosis is less than 30years. Arch Ophthalmol 1984; 102: 520-526.
3. Klein R, Klein BE, Moss SE, Cruickshanks KJ. The Wisconsin Epidemiologic Study of Diabetic Retinopathy: XVII. The 14-year incidence and progression of diabetic retinopathy and associated risk factors in type 1 diabetes. Ophthalmology 1998; 105: 1801-1815.
4. Klein R, Klein BE, Moss SE, Davis MD, DeMets DL. The Wisconsin Epidemiologic Study of Diabetic Retinopathy. III. Prevalence and risk of diabetic retinopathy when age at diagnosis is 30 or more years. Arch Ophthalmol 1984; 102: 527-532.
5. Cheung N, Mitchell P, Wong TY. Diabetic retinopathy. Lancet 2010; 376: 124-136.
6. Barber AJ, Lieth E, Khin SA, Antonetti DA, Buchanan AG, Gardner TW. Neural apoptosis in the retina during experimental and human diabetes. Early onset and effect of insulin. J Clin Invest 1998; 102: 783-791.
7. Phipps JA, Fletcher EL, Vingrys AJ. Paired-flash identification of rod and cone dysfunction in the diabetic rat. Invest Ophthalmol Vis Sci 2004; 45: 4592-4600.
8. Li Q, Zemel E, Miller B, Perlman I. Early retinal damage in experimental diabetes: electroretinographical and morphological observations. Exp Eye Res 2002; 74: 615-625.
9. Hancock HA, Kraft TW. Oscillatory potential analysis and ERGs of normal and diabetic rats. Invest Ophthalmol Vis Sci 2004; 45: 1002-1008.
10. Grading diabetic retinopathy from stereoscopic color fundus photographs-an extension of the modified Airlie House classification. ETDRS report number 10. Early Treatment Diabetic Retinopathy Study Research Group. Ophthalmology 1991; 98: 786-806.
11. Sivaprasad S, Elagouz M, McHugh D, Shona O, Dorin G. Micropulsed diode laser therapy: evolution and clinical applications. Surv Ophthalmol 2010; 55: 516-530.
12. Diabetic Clinical Research Network, Elman MJ, Aiello LP, Beck RW, Bressler NM, Bressler SB, Edwards AR etal. Randomized trial evaluating ranibizumab plus prompt or deferred laser or triamcinolone plus prompt laser for diabetic macular edema. Ophthalmology 2010; 117: 1064-1077.e35.
13. Simo R, Carrasco E, Garcia-Ramirez M, Hernandez C. Angiogenic and antiangiogenic factors in proliferative diabetic retinopathy. Curr Diabetes Rev 2006; 2: 71-98.
14. Aiello LP, Avery RL, Arrigg PG, Keyt BA, Jampel HD, Shah ST, Pasquale LR etal. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med 1994; 331: 1480-1487.
15. van Wijngaarden P, Coster DJ, Williams KA. Inhibitors of ocular neovascularization: promises and potential problems. JAMA 2005; 293: 1509-1513.
16. D'Amico DJ, Masonson HN, Patel M, Adamis AP, Cunningham ET Jr, Guyer DR, Katz B. Pegaptanib sodium for neovascular age-related macular degeneration: two-year safety results of the two prospective, multicenter, controlled clinical trials. Ophthalmology 2006; 113: 992-1001.
17. Brown DM, Kaiser PK, Michels M, Soubrane G, Heier JS, Kim RY, Sy JP. Ranibizumab versus verteporfin for neovascular age-related macular degeneration. N Engl J Med 2006; 355: 1432-1444.
18. Gao BB, Chen X, Timothy N, Aiello LP, Feener EP. Characterization of the vitreous proteome in diabetes without diabetic retinopathy and diabetes with proliferative diabetic retinopathy. J Proteome Res 2008; 7: 2516-2525.
19. Gao BB, Clermont A, Rook S, Fonda SJ, Srinivasan VJ, Wojtkowski M, Fujimoto JG etal. Extracellular carbonic anhydrase mediates hemorrhagic retinal and cerebral vascular permeability through prekallikrein activation. Nat Med 2007; 13: 181-188.
20. Schmaier AH. The plasma kallikrein-kinin system counterbalances the renin-angiotensin system. J Clin Invest 2002; 109: 1007-1009.
21. Schmaier AH. The kallikrein-kinin and the renin-angiotensin systems have a multilayered interaction. Am J Physiol Regul Integr Comp Physiol 2003; 285: R1-R13.
22. Paul M, Poyan Mehr A, Kreutz R. Physiology of local renin-angiotensin systems. Physiol Rev 2006; 86: 747-803.
23. Kawamura H, Kobayashi M, Li Q, Yamanishi S, Katsumura K, Minami M, Wu DM etal. Effects of angiotensin II on the pericyte-containing microvasculature of the rat retina. J Physiol 2004; 561: 671-683.
24. Timmermans PB, Benfield P, Chiu AT, Herblin WF, Wong PC, Smith RD. Angiotensin II receptors and functional correlates. Am J Hypertens 1992; 5: 221S-235S.
25. 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.
26. Moravski CJ, Kelly DJ, Cooper ME, Gilbert RE, Bertram JF, Shahinfar S, Skinner SL etal. Retinal neovascularization is prevented by blockade of the renin-angiotensin system. Hypertension 2000; 36: 1099-1104.
27. Downie LE, Pianta MJ, Vingrys AJ, Wilkinson-Berka JL, Fletcher EL. AT1 receptor inhibition prevents astrocyte degeneration and restores vascular growth in oxygen-induced retinopathy. Glia 2008; 56: 1076-1090.
28. Grosso A, Cheung N, Veglio F, Wong TY. Similarities and differences in early retinal phenotypes in hypertension and diabetes. J Hypertens 2011; 29: 1667-1675.
29. Nagai N, Oike Y, Izumi-Nagai K, Urano T, Kubota Y, Noda K, Ozawa Y etal. Angiotensin II type 1 receptor-mediated inflammation is required for choroidal neovascularization. Arterioscler Thromb Vasc Biol 2006; 26: 2252-2259.
30. Hirooka K, Baba T, Fujimura T, Shiraga F. Prevention of visual field defect progression with angiotensin-converting enzyme inhibitor in eyes with normal-tension glaucoma. Am J Ophthalmol 2006; 142: 523-525.
31. Berka JL, Stubbs AJ, Wang DZ, DiNicolantonio R, Alcorn D, Campbell DJ, Skinner SL. Renin-containing Muller cells of the retina display endocrine features. Invest Ophthalmol Vis Sci 1995; 36: 1450-1458.
32. Danser AH, Derkx FH, Admiraal PJ, Deinum J, de Jong PT, Schalekamp MA. Angiotensin levels in the eye. Invest Ophthalmol Vis Sci 1994; 35: 1008-1018.
33. Danser AH, van den Dorpel MA, Deinum J, Derkx FH, Franken AA, Peperkamp E, de Jong PT etal. Renin, prorenin, and immunoreactive renin in vitreous fluid from eyes with and without diabetic retinopathy. J Clin Endocrinol Metab 1989; 68: 160-167.
34. Kohler K, Wheeler-Schilling T, Jurklies B, Guenther E, Zrenner E. Angiotensin II in the rabbit retina. Vis Neurosci 1997; 14: 63-71.
35. Wheeler-Schilling TH, Sautter M, Guenther E, Kohler K. Expression of angiotensin-converting enzyme (ACE) in the developing chicken retina. Exp Eye Res 2001; 72: 173-182.
36. Gerhardinger C, Costa MB, Coulombe MC, Toth I, Hoehn T, Grosu P. Expression of acute-phase response proteins in retinal Muller cells in diabetes. Invest Ophthalmol Vis Sci 2005; 46: 349-357.
37. Senanayake P, Drazba J, Shadrach K, Milsted A, Rungger-Brandle E, Nishiyama K, Miura S etal. Angiotensin II and its receptor subtypes in the human retina. Invest Ophthalmol Vis Sci 2007; 48: 3301-3311.
38. Datum KH, Zrenner E. Angiotensin-like immunoreactive cells in the chicken retina. Exp Eye Res 1991; 53: 157-165.
39. Downie LE, Vessey K, Miller A, Ward MM, Pianta MJ, Vingrys AJ, Wilkinson-Berka JL etal. Neuronal and glial cell expression of angiotensin II type 1 (AT1) and type 2 (AT2) receptors in the rat retina. Neuroscience 2009; 161: 195-213.
40. Funatsu H, Yamashita H, Ikeda T, Mimura T, Shimizu E, Hori S. Relation of diabetic macular edema to cytokines and posterior vitreous detachment. Am J Ophthalmol 2003; 135: 321-327.
41. Alpers CE, Hudkins KL. Mouse models of diabetic nephropathy. Curr Opin Nephrol Hypertens 2011; 20: 278-284.
42. Clermont AC, Brittis M, Shiba T, McGovern T, King GL, Bursell SE. Normalization of retinal blood flow in diabetic rats with primary intervention using insulin pumps. Invest Ophthalmol Vis Sci 1994; 35: 981-990.
43. Bursell SE, Clermont AC, Shiba T, King GL. Evaluating retinal circulation using video fluorescein angiography in control and diabetic rats. Curr Eye Res 1992; 11: 287-295.
44. Horio N, Clermont AC, Abiko A, Abiko T, Shoelson BD, Bursell SE, Feener EP. Angiotensin AT(1) receptor antagonism normalizes retinal blood flow and acetylcholine-induced vasodilatation in normotensive diabetic rats. Diabetologia 2004; 47: 113-123.
45. Clermont A, Chilcote TJ, Kita T, Liu J, Riva P, Sinha S, Feener EP. Plasma kallikrein mediates retinal vascular dysfunction and induces retinal thickening in diabetic rats. Diabetes 2011; 60: 1590-1598.
46. Frank RN. Diabetic retinopathy. N Engl J Med 2004; 350: 48-58.
47. Phipps JA, Clermont AC, Sinha S, Chilcote TJ, Bursell SE, Feener EP. Plasma kallikrein mediates angiotensin II type 1 receptor-stimulated retinal vascular permeability. Hypertension 2009; 53: 175-181.
48. Gilbert RE, Kelly DJ, Cox AJ, Wilkinson-Berka JL, Rumble JR, Osicka T, Panagiotopoulos S etal. Angiotensin converting enzyme inhibition reduces retinal overexpression of vascular endothelial growth factor and hyperpermeability in experimental diabetes. Diabetologia 2000; 43: 1360-1367.
49. Kim JH, Kim JH, Yu YS, Cho CS, Kim KW. Blockade of angiotensin II attenuates VEGF-mediated blood-retinal barrier breakdown in diabetic retinopathy. J Cereb Blood Flow Metab 2009; 29: 621-628.
50. Zheng Z, Chen H, Ke G, Fan Y, Zou H, Sun X, Gy Q etal. Protective effect of perindopril on diabetic retinopathy is associated with decreased vascular endothelial growth factor-to-pigment epithelium-derived factor ratio: involvement of a mitochondria-reactive oxygen species pathway. Diabetes 2009; 58: 954-964.
51. Zheng Z, Chen H, Xu X, Li C, Gu Q. Effects of angiotensin-converting enzyme inhibitors and beta-adrenergic blockers on retinal vascular endothelial growth factor expression in rat diabetic retinopathy. Exp Eye Res 2007; 84: 745-752.
52. Chen P, Scicli GM, Guo M, Fenstermacher JD, Dahl D, Edwards PA, Scicli AG. Role of angiotensin II in retinal leukostasis in the diabetic rat. Exp Eye Res 2006; 83: 1041-1051.
53. Miller AG, Tan G, Binger KJ, Pickering RJ, Thomas MC, Nagaraj RH, Cooper ME etal. Candesartan attenuates diabetic retinal vascular pathology by restoring glyoxalase-I function. Diabetes 2010; 59: 3208-3215.
54. Raab S, Beck H, Gaumann A, Yuce A, Gerber HP, Plate K, Hammes HP etal. Impaired brain angiogenesis and neuronal apoptosis induced by conditional homozygous inactivation of vascular endothelial growth factor. Thromb Haemost 2004; 91: 595-605.
55. Qaum T, Xu Q, Joussen AM, Clemens MW, Qin W, Miyamoto K, Hassessian H etal. VEGF-initiated blood-retinal barrier breakdown in early diabetes. Invest Ophthalmol Vis Sci 2001; 42: 2408-2413.
56. Satofuka S, Ichihara A, Nagai N, Noda K, Ozawa Y, Fukamizu A, Tsubota K etal. (Pro)renin receptor-mediated signal transduction and tissue renin-angiotensin system contribute to diabetes-induced retinal inflammation. Diabetes 2009; 58: 1625-1633.
57. Nagai N, Izumi-Nagai K, Oike Y, Koto T, Satofuka S, Ozawa Y, Yamashiro K etal. Suppression of diabetes-induced retinal inflammation by blocking the angiotensin II type 1 receptor or its downstream nuclear factor-kappaB pathway. Invest Ophthalmol Vis Sci 2007; 48: 4342-4350.
58. Ly A, Yee P, Vessey KA, Phipps JA, Jobling AI, Fletcher EL. Early inner retinal astrocyte dysfunction during diabetes and development of hypoxia, retinal stress and neuronal functional loss. Invest Ophthalmol Vis Sci 2011; 52: 9315-9326.
59. Hardy KJ, Lipton J, Scase MO, Foster DH, Scarpello JH. Detection of colour vision abnormalities in uncomplicated type 1 diabetic patients with angiographically normal retinas. Br J Ophthalmol 1992; 76: 461-464.
60. Bui BV, Armitage JA, Tolcos M, Cooper ME, Vingrys AJ. ACE inhibition salvages the visual loss caused by diabetes. Diabetologia 2003; 46: 401-408.
61. Phipps JA, Wilkinson-Berka JL, Fletcher EL. Retinal dysfunction in diabetic ren-2 rats is ameliorated by treatment with valsartan but not atenolol. Invest Ophthalmol Vis Sci 2007; 48: 927-934.
62. Kurihara T, Ozawa Y, Nagai N, Shinoda K, Noda K, Imamura Y, Tsubota K etal. Angiotensin II type 1 receptor signaling contributes to synaptophysin degradation and neuronal dysfunction in the diabetic retina. Diabetes 2008; 57: 2191-2198.
63. Sharma AM, Weir MR. The role of angiotensin receptor blockers in diabetic nephropathy. Postgrad Med 123: 109-121.
64. Burgess E. Reviewing the benefits of angiotensin-converting enzyme inhibitors and angiotensin receptor blockers in diabetic nephropathy-are they drug specific or class specific? Can J Cardiol 2010; 26 (Suppl E): 15E-19E.
65. Mauer M, Zinman B, Gardiner R, Suissa S, Sinaiko A, Strand T, Drummond K etal. Renal and retinal effects of enalapril and losartan in type 1 diabetes. N Engl J Med 2009; 361: 40-51.
66. Chaturvedi N, Porta M, Klein R, Orchard T, Fuller J, Parving HH, Bilous R etal. Effect of candesartan on prevention (DIRECT-Prevent 1) and progression (DIRECT-Protect 1) of retinopathy in type 1 diabetes: randomised, placebo-controlled trials. Lancet 2008; 372: 1394-1402.
67. Sjølie AK, Klein R, Porta M, Orchard T, Fuller J, Parving HH, Bilous R etal. Effect of candesartan on progression and regression of retinopathy in type 2 diabetes (DIRECT-Protect 2): a randomised placebo-controlled trial. Lancet 2008; 372: 1385-1393.
68. Efficacy of atenolol and captopril in reducing risk of macrovascular and microvascular complications in type 2 diabetes: UKPDS 39. UK Prospective Diabetes Study Group. BMJ 1998; 317: 713-720.
69. Tight blood pressure control and risk of macrovascular and microvascular complications in type 2 diabetes: UKPDS 38. UK Prospective Diabetes Study Group. BMJ 1998; 317: 703-713.
70. Knowler WC, Bennett PH, Ballintine EJ. Increased incidence of retinopathy in diabetics with elevated blood pressure. A six-year follow-up study in Pima Indians. N Engl J Med 1980; 302: 645-650.
71. Grosso A. Detection and management of vascular hypertension. Compr Ophthalmol Update 2007; 8: 145-151; discussion 153-144.
72. Venkatramani J, Mitchell P. Ocular and systemic causes of retinopathy in patients without diabetes mellitus. BMJ 2004; 328: 625-629.
73. McLeod D. Why cotton wool spots should not be regarded as retinal nerve fibre layer infarcts. Br J Ophthalmol 2005; 89: 229-237.
74. Estacio RO, Jeffers BW, Gifford N, Schrier RW. Effect of blood pressure control on diabetic microvascular complications in patients with hypertension and type 2 diabetes. Diabetes Care 2000; 23 (Suppl 2): B54-B64.
75. Schrier RW, Estacio RO, Esler A, Mehler P. Effects of aggressive blood pressure control in normotensive type 2 diabetic patients on albuminuria, retinopathy and strokes. Kidney Int 2002; 61: 1086-1097.
76. Chaturvedi N, Sjølie AK, Stephenson JM, Abrahamian H, Keipes M, Castellarin A, Rogulja-Pepeonik Z etal. 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.
77. Bhoola KD, Figueroa CD, Worthy K. Bioregulation of kinins: kallikreins, kininogens and kininases. Pharmacol Rev 1992; 44: 1-80.
78. Borges DR, Webster ME, Guimaraes JA, Prado JL. Synthesis of prekallikrein and metabolism of plasma kallikrein by perfused rat liver. Biochem Pharmacol 1981; 30: 1065-1069.
79. Sabourin T, Morissette G, Bouthillier J, Levesque L, Marceau F. Expression of kinin B(1) receptor in fresh or cultured rabbit aortic smooth muscle: role of NF-kappa B. Am J Physiol Heart Circ Physiol 2002; 283: H227-H237.
80. Hulstrom D, Svensjo E. Intravital and electron microscopic study of bradykinin-induced vascular permeability changes using FITC-dextran as a tracer. J Pathol 1979; 129: 125-133.
81. Maurer M, Bader M, Bas M, Bossi F, Cicardi M, Cugno M, Howarth P etal. New topics in bradykinin research. Allergy 2011; 66: 1397-1406.
82. Selvarajan S, Lund LR, Takeuchi T, Craik CS, Werb Z. A plasma kallikrein-dependent plasminogen cascade required for adipocyte differentiation. Nat Cell Biol 2001; 3: 267-275.
83. Liu J, Gao BB, Clermont AC, Blair P, Chilcote TJ, Sinha S, Flaumenhaft R etal. Hyperglycemia-induced cerebral hematoma expansion is mediated by plasma kallikrein. Nat Med 2011; 17: 206-210.
84. Abdallah RT, Keum JS, El-Shewy HM, Lee MH, Wang B, Gooz M, Luttrell LM etal. Plasma kallikrein promotes epidermal growth factor receptor transactivation and signaling in vascular smooth muscle through direct activation of protease-activated receptors. J Biol Chem 2010; 285: 35206-35215.
85. Ma JX, Song Q, Hatcher HC, Crouch RK, Chao L, Chao J. Expression and cellular localization of the kallikrein-kinin system in human ocular tissues. Exp Eye Res 1996; 63: 19-26.
86. Abdouh M, Khanjari A, Abdelazziz N, Ongali B, Couture R, Hassessian HM. Early upregulation of kinin B1 receptors in retinal microvessels of the streptozotocin-diabetic rat. Br J Pharmacol 2003; 140: 33-40.
87. Kedzierska K, Ciechanowski K, Golembiewska E, Safranow K, Ciechanowicz A, Domanski L, Myslak M etal. Plasma prekallikrein as a risk factor for diabetic retinopathy. Arch Med Res 2005; 36: 539-543.
88. Pinna A, Emanueli C, Dore S, Salvo M, Madeddu P, Carta F. Levels of human tissue kallikrein in the vitreous fluid of patients with severe proliferative diabetic retinopathy. Ophthalmologica 2004; 218: 260-263.
89. Abdouh M, Talbot S, Couture R, Hassessian HM. Retinal plasma extravasation in streptozotocin-diabetic rats mediated by kinin B(1) and B(2) receptors. Br J Pharmacol 2008; 154: 136-143.
90. Pouliot M, Hetu S, Lahjouji K, Couture R, Vaucher E. Modulation of retinal blood flow by kinin B receptor in Streptozotocin-diabetic rats. Exp Eye Res 2011; 92: 482-489.
91. Lawson SR, Gabra BH, Guerin B, Neugebauer W, Nantel F, Battistini B, Sirois P. Enhanced dermal and retinal vascular permeability in streptozotocin-induced type 1 diabetes in Wistar rats: blockade with a selective bradykinin B1 receptor antagonist. Regul Pept 2005; 124: 221-224.
92. Simard B, Gabra BH, Sirois P. Inhibitory effect of a novel bradykinin B1 receptor antagonist, R-954, on enhanced vascular permeability in type 1 diabetic mice. Can J Physiol Pharmacol 2002; 80: 1203-1207.
93. Kang SW, Park CY, Ham DI. The correlation between fluorescein angiographic and optical coherence tomographic features in clinically significant diabetic macular edema. Am J Ophthalmol 2004; 137: 313-322.
94. Scholl S, Augustin A, Loewenstein A, Rizzo S, Kupperman B. General pathophysiology of macular edema. Eur J Ophthalmol 2010; 21: 10-19.
95. Katsuda I, Maruyama F, Ezaki K, Sawamura T, Ichihara Y. A new type of plasma prekallikrein deficiency associated with homozygosity for Gly104Arg and Asn124Ser in apple domain 2 of the heavy-chain region. Eur J Haematol 2007; 79: 59-68.
96. Nussberger J, Cugno M, Amstutz C, Cicardi M, Pellacani A, Agostoni A. Plasma bradykinin in angio-oedema. Lancet 1998; 351: 1693-1697.
97. Morand-Contant M, Anand-Srivastava MB, Couture R. Kinin B1 receptor upregulation by angiotensin II and endothelin-1 in rat vascular smooth muscle cells: receptors and mechanisms. Am J Physiol Heart Circ Physiol 2010; 299: H1625-1632.
98. Lewis EJ, Hunsicker LG, Bain RP, Rohde RD. The effect of angiotensin-converting-enzyme inhibition on diabetic nephropathy. The Collaborative Study Group. N Engl J Med 1993; 329: 1456-1462.
99. Kakoki M, Sullivan KA, Backus C, Hayes JM, Oh SS, Hua K, Sasim AM etal. Lack of both bradykinin B1 and B2 receptors enhances nephropathy, neuropathy, and bone mineral loss in Akita diabetic mice. Proc Natl Acad Sci U S A 2010; 107: 10190-10195.