Role of inflammation in the pathogenesis of diabetic retinopathy

Middle East African Journal of Ophthalmology

Volumn 19, Issue 1, 2012, Pages 70-74

  El Asrar, Ahmed M Abu ^a  

^a KING SAUD UNIVERSITY   (Saudi Arabia)

Author keywords

Angiogenesis; diabetic retinopathy; inflammation

Indexed keywords

ADVANCED GLYCATION END PRODUCT; BETA INTEGRIN; CD18 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; CYCLOOXYGENASE 2; CYTOKINE; GELATINASE A; GELATINASE B; HIGH MOBILITY GROUP B1 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; POLYOL; PROSTAGLANDIN E2; PROTEIN KINASE C; STROMAL CELL DERIVED FACTOR 1; THROMBOXANE A2; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR SP1;

CELL MIGRATION; CELL PROLIFERATION; CYTOKINE PRODUCTION; DIABETIC RETINOPATHY; HUMAN; HYPERGLYCEMIA; INFLAMMATION; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM;

EID: 84856404530     PISSN: 09749233     EISSN: 09751599     Source Type: Journal    
DOI: 10.4103/0974-9233.92118     Document Type: Review

References (63)

1. Fong DS, Aiello L, Gardner TW, King GL, Blankenship G, Cavallerano JD, et al. American Diabetes Association. Diabetic retinopathy. Diabetes Care 2003;26:226-9. (Pubitemid 36934461)
2. van Beijnum JR, Buurman WA, Griffioen AW. Convergence and amplification of toll-like receptor (TLR) and receptor for advanced glycation end products (RAGE) signaling pathways via high mobility group B1 (HMGB1). Angiogenesis 2008;11:91-9.
3. Joussen AM, Poulaki V, Le ML, Koizumi K, Esser C, Janicki H, et al. A central role for inflammation in the pathogenesis of diabetic retinopathy. FASEB J 2004;18:1450-2. (Pubitemid 39561611)
4. Adamis AP, Berman AJ. Immunological mechanisms in the pathogenesis of diabetic retinopathy. Semin Immunopathol 2008;30:65-84.
5. Kern TS. Contributions of inflammatory processes to the development of the early stages of diabetic retinopathy. Exp Diabetes Res 2007;2007:95103.
6. Demircan N, Safran BG, Soylu M, Ozcan AA, Sizmaz S. Determination of vitreous interleukin-1 (IL-1) and tumour necrosis factor (TNF) levels in proliferative diabetic retinopathy. Eye 2006;20:1366-9. (Pubitemid 44921137)
7. Doganay S, Evereklioglu C, Er H, Türköz Y, Sevinç A, Mehmet N, et al. Comparison of serum NO, TNF-alpha, IL-1beta, sIL-2R, IL-6 and IL-8 levels with grades of retinopathy in patients with diabetes mellitus. Eye 2002;16:163-70. (Pubitemid 34537693)
8. Abu El-Asrar AM, Missotten L, Geboes K. Expression of advanced glycation end products and related molecules in diabetic fibrovascular epiretinal membranes. Clin Experiment Ophthalmol 2010;38:57-64.
9. Joussen AM, Poulaki V, Mitsiades N, Kirchhof B, Koizumi K, Döhmen S, et al. Nonsteroidal anti-inflammatory drugs prevent early diabetic retinopathy via TNF-alpha suppression. FASEB J 2002;16:438-40.
10. Makino N, Maeda T, Sugano M, Satoh S, Watanabe R, Abe N. High serum TNF-alpha level in Type 2 diabetic patients with microangiopathy is associated with eNOS down-regulation and apoptosis in endothelial cells. J Diabetes Complications 2005;19:347-55. (Pubitemid 41563018)
11. Ben-Mahmud BM, Mann GE, Datti A, Orlacchio A, Kohner EM, Chibber R. Tumor necrosis factor-alpha in diabetic plasma increases the activity of core 2 GlcNAc-T and adherence of human leukocytes to retinal endothelial cells: significance of core 2 GlcNAc-T in diabetic retinopathy. Diabetes 2004;53:2968-76. (Pubitemid 39425923)
12. Gao X, Belmadani S, Picchi A, Xu X, Potter BJ, Tewari-Singh N, et al. Tumor necrosis factor-alpha induces endothelial dysfunction in Lepr(db) mice. Circulation 2007;115:245-54. (Pubitemid 46105724)
13. Gao X, Zhang H, Schmidt AM, Zhang C. AGE/RAGE produces endothelial dysfunction in coronary arterioles in type 2 diabetic mice. Am J Physiol Heart Circ Physiol 2008;295:H491-8.
14. Sainson RC, Johnston DA, Chu HC, Holderfield MT, Nakatsu MN, Crampton SP, et al. TNF primes endothelial cells for angiogenic sprouting by inducing a tip cell phenotype. Blood 2008;111:4997-5007.
15. Clauss M, Sunderkötter C, Sveinbjörnsson B, Hippenstiel S, Willuweit A, Marino M, et al. A permissive role for tumor necrosis factor in vascular endothelial growth factor-induced vascular permeability. Blood 2001;97:1321-9. (Pubitemid 32183755)
16. Vincent JA, Mohr S. Inhibition of caspase-1/interleukin-1beta signaling prevents degeneration of retinal capillaries in diabetes and galactosemia. Diabetes 2007;56:224-30.
17. Abu El-Asrar AM, Maimone D, Morse PH, Gregory S, Reder AT. Cytokines in the vitreous of patients with proliferative diabetic retinopathy. Am J Ophthalmol 1992;114:731-6.
18. Abu El-Asrar AM, Van Damme J, Put W, Veckeneer M, Dralands L, Billiau A, et al. Monocyte chemotactic protein-1 in proliferative vitreoretinal disorders. Am J Ophthalmol 1997;123:599-606. (Pubitemid 27203280)
19. Funatsu H, Noma H, Mimura T, Eguchi S, Hori S. Association of vitreous inflammatory factors with diabetic macular edema. Ophthalmology 2009;116:73-9.
20. Abu El-Asrar AM, Struyf S, Kangave D, Geboes K, Van Damme J. Chemokines in proliferative diabetic retinopathy and proliferative vitreoretinopathy. Eur Cytokine Netw 2006;17:155-65.
21. Maier R, Weger M, Haller-Schober EM, EL-Shabrawi Y, Wedrich A, Theisl A, et al. Multiplex bead analysis of vitreous and serum concentrations of inflammatory and proangiogenic factors in diabetic patients. Mol Vis 2008;14:637-43 . (Pubitemid 351486723)
22. Elner SG, Elner VM, Jaffe GJ, Stuart A, Kunkel SL, Strieter RM. Cytokines in proliferative diabetic retinopathy and proliferative vitreoretinopathy. Curr Eye Res 1995;14:1045-53.
23. Wada T, Furuichi K, Sakai N, Iwata Y, Kitagawa K, Ishida Y, et al. Gene therapy via blockade of monocyte chemoattractant protein-1 for renal fibrosis. J Am Soc Nephrol 2004;15:940-8. (Pubitemid 38375313)
24. Low QE, Drugea IA, Duffner LA, Quinn DG, Cook DN, Rollins BJ, et al. Wound healing in MIP-1alpha(-/-) and MCP-1 (-/-) mice. Am J Pathol 2001;159:457-63. (Pubitemid 32751076)
25. Hong KH, Ryu J, Han KH. Monocyte chemoattractant protein-1-induced angiogenesis is mediated by vascular endothelial growth factor-A. Blood 2005;105:1405-7. (Pubitemid 40223654)
26. Tager AM, Kradin RL, LaCamera P, Bercury SD, Campanella GS, Leary CP, et al. Inhibition of pulmonary fibrosis by the chemokine IP-10/CXCL10. Am J Respir Cell Mol Biol 2004;31:395-404. (Pubitemid 39330949)
27. Keane MP, Belperio JA, Arenberg DA, Burdick MD, Xu ZJ, Xue YY, et al. IFN-gamma-inducible protein-10 attenuates bleomycin-induced pulmonary fibrosis via inhibition of angiogenesis. J Immunol 1999;163:5686-92.
28. Bulter JM, Guthrie SM, Koc M, Afzal A, Caballero S, Brooks HL, et al. SDF-1 is both necessary and sufficient to promote proliferative retinopathy. J Clin Invest 2005;115:86-93. (Pubitemid 40385508)
29. Abu El-Asrar AM, Struyf S, Verbeke H, Van Damme J, Geboes K. Circulating bone marrow-derived enedothelial precursor cells contribute to neovascularization in diabetic epiretinal membranes. Acta Ophthalmol 2011;89:222-8.
30. Stellos K, Langer H, Daub K, Schoenberger T, Gauss A, Geisler T, et al. Platelet-derived stromal cell-derived factor-1 regulates adhesion and promotes differentiation of human CD34+ cells to endothelial progenitor cells. Circulation 2008;117:206-15.
31. Reddy K, Zhou Z, Jia SF, Lee TH, Morales-Arias J, Cao Y, et al. Stromal cell-derived factor-1 stimulates vasculogenesis and enhances Ewing's sarcoma tumor growth in the absence of vascular endothelial growth factor. Int J Cancer 2008;123:831-7. (Pubitemid 352032409)
32. De Falco E, Porcelli D, Torella AR, Straino S, Iachininoto MG, Orlandi A, et al. SDF-1 involvement in endothelial phenotype and ischemia-induced recruitment of bone marrow progenitor cells. Blood 2004;104:3472-82. (Pubitemid 39564415)
33. Petrovic MG, Korosec P, Kosnik M, Hawlina M. Vitreous levels of interleukin-8 in patients with proliferative diabetic retinopathy. Am J Ophthalmol 2007;143:175-6. (Pubitemid 44917800)
34. Kuwano T, Nakao S, Yamamoto H, Tsuneyoshi M, Yamamoto T, Kuwano M, et al. Cyclooxygenase 2 is a key enzyme for inflammatory cytokine-induced angiogenesis. FASEB J 2004;18:300-10. (Pubitemid 38186249)
35. Bagi Z, Erdei N, Papp Z, Edes I, Koller A. Up-regulation of vascular cyclooxygenase-2 in diabetes mellitus. Pharmacol Rep 2006;58 Suppl:52-6.
36. Abu El-Asrar AM, Missotten L, Geboes K. Expression of cyclooxygenase-2 and downstream enzymes in diabetic fibrovascular epiretinal membranes. Br J Ophthalmol 2008;92:1534-9.
37. Cook-Johnson RJ, Demasi M, Cleland LG, Gamble JR, Saint DA, James MJ. Endothelial cell COX-2 expression and activity in hypoxia. Biochim Biophys Acta 2006;1761:1443-9. (Pubitemid 44821907)
38. Du Y, Sarthy VP, Kern TS. Interaction between NO and COX pathways in retinal cells exposed to elevated glucose and retina of diabetic rats. Am J Physiol Regul Integr Comp Physiol 2004;287:R735-41.
39. Ayalasomayajula SP, Amrite AC, Kompella UB. Inhibition of cyclooxygenase-2, but not cyclooxygenase-1, reduces prostaglandin E2 secretion from diabetic rat retinas. Eur J Pharmacol 2004;498:275-8. (Pubitemid 39208089)
40. Tamura K, Sakurai T, Kogo H. Relationship between prostaglandin E2 and vascular endothelial growth factor (VEGF) in angiogenesis in human vascular endothelial cells. Vascul Pharmacol 2006;44:411-6. (Pubitemid 43766677)
41. Abu El-Asrar AM, Desmet S, Meersschaert A, Dralands L, Missotten L, Geboes K. Expression of the inducible isoform of nitric oxide synthase in the retinas of human subjects with diabetes mellitus. Am J Ophthalmol 2001;132:551-6. (Pubitemid 32904579)
42. Abu El-Asrar AM, Meersschaert A, Dralands L, Missotten L, Geboes K. Inducible nitric oxide synthase and vascular endothelial growth factor are colocalized in the retinas of human subjects with diabetes. Eye 2004;18:306-13. (Pubitemid 38455902)
43. Leal EC, Manivannan A, Hosoya K, Terasaki T, Cunha-Vaz J, Ambrósio AF, et al. Inducible nitric oxide synthase isoform is a key mediator of leukostasis and blood-retinal barrier breakdown in diabetic retinopathy. Invest Ophthalmol Vis Sci 2007;48:5257-65.
44. Zheng L, Du Y, Miller C, Gubitosi-Klug RA, Ball S, Berkowitz BA, et al. Critical role of inducible nitric oxide synthase in degeneration of retinal capillaries in mice with streptozotocininduced diabetes. Diabetologia 2007;50:1987-96.
45. Chan PS, Kanwar M, Kowluru RA. Resistance of retinal inflammatory mediators to suppress after reinstitution of good glycemic control: Novel mechanism for metabolic memory. J Diabetes Complications 2010;24:55-63.
46. Treutiger CJ, Mullins GE, Johansson AS, Rouhiainen A, Rauvala HM, Eriandsson-Harris H, et al. High mobility group 1B-box mediates activation of human endothelium. J Intern Med 2003;254:375-85. (Pubitemid 37211261)
47. Fiuza C, Bustin M, Talwar S, Tropea M, Gerstenberger E, Shelhamer JH, et al. Inflammation-promoting activity of HMGB1 on human microvascular endothelial cells. Blood 2003;101:2652-60. (Pubitemid 36857626)
48. Luan ZG, Zhang H, Yang PT, Ma XC, Zhang C, Guo RX. HMGB1 activates nuclear factor-κB signaling by RAGE and increases the production of TNF-α in human umbilical vein endothelial cells. Immunobiology 2010;215:956-62.
49. Mitola S, Belleri M, Urbinati C, Coltrini D, Sparatore B, Pedrazzi M, et al. Cutting edge: Extracellular high mobility group box-1 protein is a proangiogenic cytokine. J Immunol 2006;176:12-5. (Pubitemid 43023243)
50. Schlueter C, Weber H, Meyer B, Rogalla P, Röser K, Hauke S, et al. Angiogenetic signaling through hypoxia. HMGB1: An angiogenic switch molecule. Am J Pathol 2005;166:1259-63. (Pubitemid 40524448)
51. Chavakis E, Hain A, Vinci M, Carmona G, Bianchi ME, Vajkoczy P, et al. High-mobility group box 1 activates integrin-dependent homing of endothelial progenitor cells. Circ Res 2007;100: 204-12. (Pubitemid 46208720)
52. van Beijnum JR, Dings RP, van der Linden E, Zwaans BM, Ramaekers FC, Mayo KH, et al. Gene expression of tumor angiogenesis dissected: Specific targeting of colon cancer angiogenic vasculature. Blood 2006;108:2339-48. (Pubitemid 44497518)
53. Hamada N, Maeyama T, Kawaguchi T, Yoshimi M, Fukumoto J, Yamada M, et al. The role of high mobility group box 1 in pulmonary fibrosis. Am J Respir Cell Mol Biol 2008;39:440-7.
54. Yoshizaki A, Komura K, Iwata Y, Ogawa F, Hara T, Muroi E, et al. Clinical significance of serum HMGB-1 and sRAGE levels in systemic sclerosis: Association with disease severity. J Clin Immunol 2009;29:180-9.
55. Ranzato E, Patrone M, Pedrazzi M, Burlando B. Hmgb1 promotes wound healing of 3T3 mouse fibroblasts via RAGE-dependent ERK1/2 activation. Cell Biochem Biophys 2010;57:9-17.
56. Abu El-Asrar AM, Missotten L, Geboes K. Expression of high-mobility group box-1/receptor for advanced glycation end products/osteopontin/early growth response-1 pathway in proliferative vitreoretinal epiretinal membranes. Mol Vis 2011;17:508-18.
57. El-Asrar AM, Nawaz MI, Kangave D, Geboes K, Ola MS, Ahmad S, et al. High-mobility group box-1 and biomarkers of inflammation in the vitreous from patients with proliferative diabetic retinopathy. Mol Vis 2011;17:1829-38.
58. Giebel SJ, Menicucci G, McGuire PG, Das A. Matrix metalloproteinases in early diabetic retinopathy and their role in alteration of the blood-retinal barrier. Lab Invest 2005;85: 597-607. (Pubitemid 40675441)
59. Abu El-Asrar AM, Van den Steen PE, Al-Amro SA, Missotten L, Opdenakker G, Geboes K. Expression of angiogenic and fibrogenic factors in proliferative vitreoretinal disorders. Int Ophthalmol 2007;27:11-22. (Pubitemid 46672141)
60. Noda K, Ishida S, Inoue M, Obata K, Oguchi Y, Okada Y, et al. Production and activation of matrix metalloproteinase-2 in proliferative diabetic retinopathy. Invest Ophthalmol Vis Sci 2003;44:2163-70. (Pubitemid 36520313)
61. Jin M, Kashiwagi K, Izuka Y, Tanaka Y, Imai M, Tsukahara S. Matrix metalloproteinases in human diabetic and nondiabetic vitreous. Retina 2001;21:28-33. (Pubitemid 32151759)
62. Abu El-Asrar AM, Dralands L, Veckeneer M, Geboes K, Missotten L, Van Aelst I, et al. Gelatinase B in proliferative vitreoretinal disorders. Am J Ophthalmol 1998;125:844-51. (Pubitemid 28283745)
63. Descamps FJ, Martens E, Kangave D, Struyf S, Geboes K, Van Damme J, et al. The activated form of gelatinase B/matrix metalloproteinase-9 is associated with diabetic vitreous hemorrhage. Exp Eye Res 2006;83:401-7. (Pubitemid 43850955)