Is inflammation a common retinal-renal-nerve pathogenic link in diabetes?

Current Diabetes Reviews

Volumn 6, Issue 5, 2010, Pages 294-303

  Kaul, Kirti ^a   Hodgkinson, Andrea ^b   Tarr, Joanna M ^a   Kohner, Eva M ^a   Chibber, Rakesh ^a  

^a PLYMOUTH UNIVERSITY PENINSULA SCHOOLS OF MEDICINE AND DENTISTRY   (United Kingdom)

^b ITTC Building   (United Kingdom)

Author keywords

Adhesion molecules; Diabetes; Inflammation; Nephropathy; Neuropathy; Pro inflammatory cytokines; Retinopathy

Indexed keywords

ANTIINFLAMMATORY AGENT; C REACTIVE PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; TUMOR NECROSIS FACTOR; VASCULAR CELL ADHESION MOLECULE 1; BIOLOGICAL MARKER;

ARTICLE; DIABETIC NEPHROPATHY; DIABETIC NEUROPATHY; DIABETIC RETINOPATHY; DISEASE EXACERBATION; HUMAN; INFLAMMATION; INSULIN DEPENDENT DIABETES MELLITUS; KIDNEY NERVE; LEUKOCYTE; MICROANGIOPATHY; NERVE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RETINAL NERVE; ANIMAL; BIOLOGICAL MODEL; BLOOD; IMMUNOLOGY; INNERVATION; KIDNEY; METABOLISM; NEPHRITIS; PATHOLOGY; RETINA; RETINA NERVE CELL; RETINITIS; REVIEW;

ANIMALS; BIOLOGICAL MARKERS; DIABETIC NEPHROPATHIES; DIABETIC NEUROPATHIES; DIABETIC RETINOPATHY; HUMANS; INFLAMMATION; KIDNEY; MODELS, BIOLOGICAL; NEPHRITIS; RETINA; RETINAL NEURONS; RETINITIS;

EID: 79551482327     PISSN: 15733998     EISSN: 18756417     Source Type: Journal    
DOI: 10.2174/157339910793360851     Document Type: Article

References (153)

1. International Diabetes Federation. Diabetes Prevalence. Available at: http://www.idf.org/home/index.cfm?node=264
2. Department of Health UK. Diabetes. Available at: http://www.dh.gov.uk/en/Healthcare/Diabetes/index.htm
3. Centre for Chronic Disease. Diabetes. Available at: http://www.cdc.gov/diabetes/faq/research.htm
4. Porte D, Schwartz MW. Diabetes Complications-Why is glucose potentially toxic? Science 1996; 272: 699-700.
5. The Diabetes Control and Complications Trial Research Group: The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. New Engl J Med 1993; 329: 977-86.
6. Sowers JR, Epstein M. Diabetes mellitus and associated hyperten-sion,vascular disease, and nephropathy. Hypertension 1995; 26: 869-79.
7. Haneda M, Koya D, Kikkawa R. Cellular mechanisms in the development and progression of diabetic nephropathy: activation of the DAG-PKC-ERK pathway. Am J Kidney Dis 2001; 38: S178-81.
8. Klein R, Klein BE, Moss SE, et al. 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: 527-32.
9. Kohner EM, Porta M, Hyer SL. The pathogenesis of diabetic retinopathy and cataract. Textbook of Diabetes. Oxford, Blackwell, 1991.
10. Williams R, Aireyn M, Baxter H, et al. Epidemiology of diabetic retinopathy and macular edema: a systematic review. Eye 2004; 18: 963-83.
11. Cunha-Vaz JG. Pathophysiology of diabetic retinopathy. Br J Ophthalmol 1978; 62: 351-5.
12. Zeeuw D, Remuzzi G, Parving HH, et al. Albuminuria, a therapeutic target for cardiovascular protection in type 2 diabetic patients with nephropathy. Circulation 2004; 110: 921-7.
13. Dronovalli S, Burney BO, Bakris GO, et al. Glycemic control and cardiovascular disease in chronic kidney disease. Curr Diabetes Rep 2009; 9: 243-8.
14. Selby JB, Fitz-Simmons S, Newman JM. The natural history and epidemiology of diabetic nephropathy. J Am Med Assoc 1990; 263: 1954-60.
15. Lewko B, Stepinski J. Hyperglycemia and mechanical stress: targeting the renal podocytes. J Cell Physiol 2009; 221: 288-95.
16. Savage S, Estacio RO, Jeffers B, Schrier RW. Urinary albumin excretion as a predictor of diabetic retinopathy, neuropathy, and cardiovascular disease in NIDDM. Diabetes Care 1996; 19: 1243-8.
17. Marshall SM. Recent advances in diabetic nephropathy. Postgrad Med J 2004; 80: 624-33.
18. Andersen AR, Sandahl Christiansen JK, Andersen K, et al. Diabetic nephropathy in type (insulin dependent) diabetes: an epidemi-ological study. Diabetologia 1983; 25: 496-501.
19. Borch-Johnsen K, Andersen KP, Deckert T. The effect of proteinu-ria on relative mortality in type 1 (insulin dependent) diabetes mellitus. Diabetologia 1985; 28: 590-6.
20. Stephensen J, Fuller JH. Microvascular and acute complications in IDDM patients: the EURODIAB IDDM Complication Study. Diabetologia 1994; 37: 278-85.
21. Estudio Diamante Study Group. Renal involvement in type 1 (IDDM) diabetes in Spain. Diabetes Res Clin Pract 1997; 38: 129-37.
22. Forsblom CM, Groop PH, Groop LC. Predictive value of microalbuminuria in patients with insulin dependent diabetes of long duration. Br Med J 1992; 305: 1051-3.
23. Adler AI, Stevens RJ, Manley SE, et al. Development and progression of nephropathy in type 2 diabetes; the United Kingdom Prospective Diabetes Study (UKPDS). Kidney Int 2003; 63: 225-32.
24. Osterby R, Parving HH, Hommel E, et al. Glomerular structure and function in diabetic nephropathy. Diabetes 1990; 39:1057-63.
25. Gilbert RE, Cooper ME. The tubule-interstitium in progressive diabetic kidney disease: more than an aftermath of glomerular injury. Kidney Int 1999; 56: 1627-37.
26. Pavenstadt H, Kriz W, Kretzler M. Cell biology of the podocyte. Physiol Rev 1999; 56: 253-307.
27. White KE, Bilous RW, Marshall SM, et al. Podocyte number in normotensive type 1 diabetic patients with albuminuria. Diabetes 2002; 51: 3083-9.
28. Parving HH, Gall MA, Skott P, et al. Prevalence and causes of microalbuminuria in non-insulin dependent diabetic patients. Kidney Int 1991; 41: 758-62.
29. Gambara V, Mecca G, Remuzzi G, et al. Heterogeneous nature of renal lesions in type II diabetes. J Am Soc Nephol 1993; 3: 1458-66.
30. Llewelyn JG. The diabetic neuropathies: types, diagnosis and management. J Neurol Neurosurg Psychiatry 2003; 74: 15-19.
31. Boulton AJ, Vinik AI, Arezzo JC, et al. American Diabetes Association. Diabetic neuropathies: a statement by the American Diabetes Association. Diabetes Care 2005; 28: 956-62.
32. Hae Young Chung HY, Cesari M, Anton S. Molecular inflammation: underpinnings of aging and age-related diseases. Ageing Res Rev 2009; 8: 8-30.
33. Grimble, RF. Inflammatory status and insulin resistance. Current Opin Clin Nutr Metab Care 2002; 5: 551-9.
34. Pickup JC. Inflammation and activated innate immunity in the pathogenesis of type 2 diabetes. Diabetes Care 2004; 27: 813-23.
35. Malik S, Wong ND, Franklin S, Pio J, Fairchild C, Chen R. Cardiovascular disease in U.S. patients with metabolic syndrome, diabetes, and elevated C-reactive protein. Diabetes Care 2005; 28: 690-3.
36. Leinonen E, Hurt-Camejo E, Wiklund O, et al. Insulin resistance and adiposity correlate with acute-phase reaction and soluble cell adhesion molecules in type 2 diabetes. Atherosclerosis 2003; 166: 387-94.
37. Leeuwenberg JFM, Smeets EF, Neefjes JJ, et al. E-selectin and intercellular adhesion molecule-1 are released by activated human endothelial cells in vitro. Immunology 1992; 77: 543-49.
38. Rizzoni D, Porteri E, Guelfi D, et al. Endothelial dysfunction in small resistance arteries of patients with non-insulin-dependent diabetes mellitus. J Hyperten 2001; 19: 913-19.
39. Powell EDU, Field RA. Diabetic retinopathy in rheumatoid arthritis. Lancet 1964; 2: 17-8.
40. Boudoin C, Passa P, Sharp P, et al. The DAMAD Study Group. The effect of aspirin alone and aspirin plus dipyridamole in early diabetic retinopathy. A multicentre randomised controlled clinical trial. Diabetes 1989; 38: 491-8.
41. Early Treatment of Diabetic Retinopathy Study Group. Effect of aspirin on diabetic retinopathy. ETDRS report no 8. Ophthalmology 1991; 98: S757-65.
42. Kohner EM. Aspirin for Diabetic retinopathy: The evidence of a beneficial effect is from basic science, not clinical trials. Br Med J 2003; 327: 1060-61.
43. Bergthoff K, Clar C, Richter B. Aspirin in diabetic retinopathy. A systematic review. Endocrinol Metab Clin North Am 2002; 31: 779-83.
44. Navarro JF, Milena F, Mora C, et al. Renal pro-inflammatory cytokine gene expression in diabetic nephropathy: effect of angiotensin-converting enzyme inhibition and pentoxifylline administration. Am J Nephrol 2006; 26: 562-70.
45. Cryer B, Feldman M. Cyclooxygenase-1 and cyclooxygenase-2 selectivity of widely used nonsteroidal anti-inflammatory drugs. Am J Med 1998; 104: 413-21.
46. Kuwano T, Nakao S, Yamamoto H, et al. Cyclooxygenase 2 is a key enzyme for inflammatory cytokine-induced angiogenesis. FASEB J 2004; 18: 300-10.
47. Sheu ML, Ho FM, Yang RS, et al. High glucose induces human endothelial cell apoptosis through a phosphoinositide 3-kinase-regulated cyclooxygenase-2 pathway. Arterioscler Thromb Vasc Biol 2005; 25: 539-45.
48. 2 in non-insulin-dependent diabetes. Relationship to vascular complications. Eur J Clin Invest 1984; 14: 83-6.
49. Kojima S, Yamada T, Tamai M. Quantitative analysis of interleukin-6 in vitreous from patients with proliferative vitreoretinal diseases. Jpn J Ophthalmol 2001; 45: 40-5.
50. Abu el Asrar AM, Maimone D, Morse PH, et al. Cytokines in the vitreous of patients with proliferative diabetic retinopathy. Am J Ophthalmol 1992; 114: 731-6.
51. Zorena K, Mysliwska J, Mysliwiec M, et al. Serum TNF-alpha level predicts nonproliferative diabetic retinopathy in children. Mediat Inflamm 2007; 2007: 92196.
52. Yuuki T, Kanda T, Kimura Y, et al. Inflammatory cytokines in vitreous fluid and serum of patients with diabetic vitreoretinopathy. J Diabetes Complicat 2001; 15: 257-9.
53. Cicik E, Tekin H, Akar S, et al. Interleukin-8, nitric oxide, and glutathione status in proliferative vitreoretinopathy and proliferative diabetic retinopathy. Ophthalmol Res 2003; 35: 251-5.
54. Limb GA, Webster H, Soomro S, et al. Platelet expression of tumour necrosis factor-alpha (TNF-), TNF receptors and intercellular adhesion molecule-1 (ICAM-1) in patients with proliferative diabetic retinopathy. Clin Exp Immunol 1999; 118: 213-8.
55. Ben-Mahmud BM, Chan WH, Abdulahad RM, et al. Clinical validation of a link between TNF-alpha and the glycosylation enzyme core 2 GlcNAc-T and the relationship of this link to diabetic retinopathy. Diabetologia 2006; 49: 2185-91.
56. Demircan N, Safran BG, Soylu M, et al. Determination of vitreous interleukin-1 (IL-1) and tumour necrosis factor (TNF) levels in proliferative diabetic retinopathy Eye 2006; 20: 1366-9.
57. Bagi Z, Erdei N, Papp Z, et al. Up-regulation of vascular cyclooxygenase-2 in diabetes mellitus. Pharmacol Rep 2006; 58: 52-6S.
58. Yunpeng Du, 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-R41.
59. Sennlaub F, Valamanesh F, Vazquez-Tello A, et al. Cyclooxygenase-2 in human and experimental ischemic proliferative retinopathy. Circulation 2003; 108: 198-204.
60. Trifan OC, Hla T. Cyclooxygenase-2 modulates cellular growth and promotes tumorigenesis. J Cell Mol Med 2007; 7: 207-22.
61. Dohadwala M, Luo J, Zhu L, et al. Non-small cell lung cancer cyclooxygenase-2-dependent invasion is mediated by CD44. J Biol Chem 2001; 276: 20809-12.
62. Sun Y, Ming Tang X, Half E, et al. Cyclooxygenase-2 overexpres-sion reduces apoptotic susceptibility by inhibiting the cytochrome c-dependent apoptotic pathway in human colon cancer cells. Cancer Res 2002; 62: 6323-8.
63. Choudhary N, Ahlawat RS. Interleukin-6 and c-reactive protein in pathogenesis of diabetic nephropathy-new evidence linking inflammation, glycemic control, and microalbuminuria. Iran J Kidney Dis 2008; 2: 72-9.
64. Vestra MD, Mussap M, Gallina P, et al. Acute-phase markers of inflammation and glomerular structure in patients with type 2 diabetes. J Am Soc Nephrol 2005; 16: 78-82.
65. Roubicek T, Bartlova M, Krajickova J, et al. Increased production of proinflammatory cytokines in adipose tissue of patients with end-stage renal disease. Nutrition 2009; 25: 762-8.
66. Lechleitner M, Koch T, Herold M, et al. Tumour necrosis factor-alpha plasma level in patients with type 1 diabetes mellitus and its association with glycaemic control and cardiovascular risk factors. J Intern Med 2000; 248: 67-76.
67. Foss MC, Foss NT, Paccola GM, et al. Serum levels of tumor necrosis factor in insulin-dependent diabetic patients. Braz J Med Biol Res 1992; 25: 239-42.
68. Min D, Lyons JG, Bonner J, et al. Mesangial cell-derived factors alter monocyte activation and function through inflammatory pathway: possible pathogenic role in diabetic nephropathy. Am J Physiol Renal Physiol 2009; 297(5): F1229-37.
69. Navarro-González JF, Mora-Fernández C. The role of inflammatory cytokines in diabetic nephropathy. J Am Soc Nephrol 2008; 19: 433-42.
70. Hirano T, Akira S, Taga T, et al. Biological and clinical aspect of interleukin 6. Immunol Today 1990; 11: 443-9.
71. Hasegawa G, Nakano K, Sawada M, et al. Possible role of tumor necrosis factor and interleukin-1 in the development of diabetic nephropathy. Kidney Int 1991; 40: 1007-12.
72. Saraheimo M, Teppo AM, Forsblom C, et al. Diabetic nephropathy is associated with low-grade inflammation in Type 1 diabetic patients. Diabetologia 2003; 46: 1402-7.
73. Kiritoshi S. Reactive oxygen species from mitochondria induce cyclooxygenase-2 gene expression in human mesangial cells-potential role in diabetic nephropathy. Hypertension 2004; 43: 573.
74. Izhar M, Alausa T, Folker A, et al. Effects of COX inhibition on blood pressure and kidney function in ace inhibitor-treated blacks and hispanics. Hypertension 2004; 3: 573-7.
75. Doupis J, Lyons TE, Wu S, et al. Microvascular reactivity and inflammatory cytokines in painful and painless peripheral diabetic neuropathy. J Clin Metab Endocrinol 2008; 94: 2157-63.
76. Skundric DD and Lisak RP. Role of neuropoietic cytokines in development and progression of diabetic polyneuropathy: from glucose metabolism to neurodegeneration. Exp Diabetes Res 2003; 4: 303-12.
77. Empl M, Renaud S, Erne B, et al. TNF-alpha expression in painful and nonpainful neuropathies. Neurology 2001; 56: 1371-7.
78. �[78] Herder C, Lankisch M, Ziegler D, et al. http://care.diabetesjournals. org/content/32/4/680.long-aff-6#aff-6 Subclinical inflammation and diabetic polyneuropathy MONICA/KORA survey F3 (Augsburg, Germany). Diabetes Care 2009; 32: 680-2.
79. Yu LN, Yang XS, Hua Z, et al. Serum levels of pro-inflammatory cytokines in diabetic patients with peripheral neuropathic pain and the correlation among them. Zhonghua Yi Xue Za Zhi 2009; 89: 469-71.
80. Padi SS, Kulkarni SK. Minocycline prevents the development of neuropathic pain, but not acute pain: possible anti-inflammatory and antioxidant mechanisms. Eur J Pharmacol 2008; 601: 79-87.
81. Freshwater JD, Svensson CI, Malmberg AB, et al. Elevated spinal cyclooxygenase and prostaglandin release during hyperalgesia in diabetic rats. Diabetes 2002; 51: 2249-55.
82. Blüher M, Unger R, Rassoul F, Reppucci VS, Schiff VM, Schmidt SM. Relation between glycaemic control, hyperinsulinaemia and plasma concentrations of soluble adhesion molecules in patients with impaired glucose tolerance or type II diabetes. Diabetologia 2002; 45: 210-16.
83. Fasching P, Veitl M, Rohac M, et al. Elevated concentrations of circulating adhesion molecules and their association with microvascular complications in insulin-dependent diabetes mellitus. J Clin Endocrinol Metab 1996; 81: 4313-7.
84. McLeod DS, Lefer DJ, Merges C, et al. Enhanced expression of intercellular adhesion molecule-1 and p-selectin in the diabetic human retina and choroid. Am J Pathol 1995; 147: 642-53.
85. Morigi M, Angioletti S, Imberti B, et al. Leukocyte-endothelial interaction is augmented by high glucose concentrations and hy-perglycaemia in a NF-kB-dependent fashion. J Clin Invest 1998; 101: 1905-15.
86. Schmidt AM, Crandall J, Hori O, Cao R, et al. Elevated plasma levels of vascular cell adhesion molecule-1 (VCAM-1) in diabetic patients with microalbuminuria: a marker of vascular dysfunction and progressive vascular disease. Br J Haematol 1996; 92: 747-50.
87. Meleth AD, Agron E, Chan CC, et al. Serum inflammatory markers in diabetic retinopathy. Invest Ophthalmol Vis Sci 2005; 46: 4295-301.
88. Van Hecke MV, Dekker JM, Nijpels G, et al. Inflammation and endothelial dysfunction are associated with retinopathy: the Hoorn Study. Diabetologia 2005; 48: 1300-6.
89. Gustavsson C, Agardh CD, Per H, Agardg E. Markers in nondia-betic and diabetic rat retinas exposed to ischemia followed by reperfusion. Retina 2008; 28: 645-52.
90. Matsumoto K, Sera Y, Ueki Y, et al. Comparison of serum concentrations of soluble adhesion molecules in diabetic microangiopathy and macroangiopathy. Diabetes Med 2002; 19: 822-6.
91. Olson JA, Whitelaw CM, McHardy KC, et al. Soluble leucocyte adhesion molecules in diabetic retinopathy stimulate retinal capillary endothelial cell migration. Diabetologia 1997; 40: 1166-71.
92. Refaat GA, Abdel Rasol HA, Baligh MA. A study of soluble adhesion molecules in patients with diabetic retinopathy. Ophthalmic Res 2001; 33: S1.
93. �[93] Nowak M, Wielkoszyaski T, Marek B, et al. Blood serum levels of vascular cell adhesion molecule (sVCAM-1), intercellular adhesion molecule (sICAM-1) and endothelial leucocyte adhesion molecule-1(ELAM-1) in diabetic retinopathy. Clin Exp Med 2008; 8: 159-64.
94. Adamiec J, O Ficjalska-Mlynezak. Contribution of selected cellular adhesion molecules and proinflammatory cytokines in the patho-patho- genesis of proliferative diabetic retinopathy. Przegl lek 2007; 64: 389-92. genesis
95. Adamiec-Mroczek J, Oficjalska-Myczak J. Assessment of selected adhesion molecule and proinflammatory cytokine levels in the vitreous body of patients with type 2 diabetes--role of the in-flammatory-immune process in the pathogenesis of proliferative diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol 2008; 246: 1665-70.
96. Hernández C, Burgos R, Cantón A, et al. Vitreous levels of vascular cell adhesion molecule and vascular endothelial growth factor in patients with proliferative diabetic retinopathy: a case-control study. Diabetes Care 2001; 24: 516-21.
97. Koch AE, Halloran MM, Haskell CJ, et al. Angiogenesis mediated by soluble forms of E-selectin and vascular cell adhesion molecule-1. Nature 1995; 376: 517-9.
98. Chen, W, Esselman WJ, Jump DB, Busik et al. Anti-inflammatory effect of docosahexaenoic acid on cytokine-induced adhesion molecule expression in human retinal vascular endothelial cells. Invest Ophthalmol Vis Sci 2005; 46: 4342-7.
99. Adamis AP. Is diabetic retinopathy an inflammatory disease? Br J Ophthalmol 2002; 86: 363-5.
100. Adamiec-Mroczek J, Oficjalska-Mayaczak J. Assessment of selected adhesion molecule and proinflammatory cytokine levels in the vitreous body of patients with type 2 diabetes--role of the in-flammatory-immune process in the pathogenesis of proliferative diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol 2008; 246: 1665-70.
101. 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: 642-53.
102. Hirata F, Yoshida M, Ogura Y. High glucose exacerbates neutrophil adhesion to human retinal endothelial cells. Exp Eye Res 2006; 82: 179-182.
103. Stehouwer CD, Gall MA, Twisk JW, et al. Increased urinary albumin excretion, endothelial dysfunction, and chronic low-grade inflammation in type 2 diabetes: progressive, interrelated, and independently associated with risk of death. Diabetes 2002; 51: 1157-65.
104. Bavbek N, Kargili A, Kaftan O, et al. Elevated concentrations of soluble adhesion molecules and large platelets in diabetic patients: are they markers of vascular disease and diabetic nephropathy? Clin Appl Thromb Hemost 2007; 13: 391-7.
105. Clausen P, Jacobsen P, Rossing K, et al. Plasma concentrations of VCAM-1 and ICAM-1 are elevated in patients with Type 1 diabetes mellitus with microalbuminuria and overt nephropathy. Diabet Med 2000; 17: 644-9.
106. Koga M, Otsuki M, Kubo M, et al. Relationship between circulating vascular cell adhesion molecule-1 and microvascular complications in type 2 diabetes mellitus. Diabet Med 1998; 15: 661-7.
107. Chow FY, Nikolic-Paterson DJ, Ozols E, Atkins RC, Tesch GH. Intracellular adhesion molecule-1 deficiency is protective against nephropathy in type 2 diabetic db/db mice. J Am Soc Nephrol 2005; 16: 1711-22.
108. Jude EB, Abbott CA, Young MJ, et al. The potential role of cell adhesion molecules in the pathogenesis of diabetic neuropathy. Diabetologia 1998; 41: 330-6.
109. Liu ZG. Molecular mechanism of TNF signalling and beyond. Cell Res 2005; 15: 24-7.
110. Hussain MJ, Peakman M, Gallati H, et al. Elevated plasma levels of macrophage-derived cytokines precede and accompany the onset of IDDM. Diabetologia 1996; 39: 60-9.
111. Chibber R, Ben-Mahmud BM, Chibber S, Kohner EM. Leukocytes in diabetic retinopathy. Curr Diabetes Rev 2007; 3: 3-14.
112. Barouch FC, Miyamoto K, Allport JR, et al. Integrin-mediated neutrophil adhesion and retinal leukostasis in diabetes. Invest Ophthalmol Vis Sci 2000; 41: 1153-8.
113. Nowak M, Wielkoszyaski T, Marek B, et al. Blood serum levels of vascular cell adhesion molecule (sVCAM-1), intercellular adhesion molecule (sICAM-1) and endothelial leucocyte adhesion molecule-1 (ELAM-1) in diabetic retinopathy. Clin Exp Med 2008; 8: 159-64.
114. Avery RL, Pearlman J, Pieramici DJ, et al. Intravitreal bevacizu-mab (avastin) in the treatment of proliferative diabetic retinopathy. Opthamology 2006; 113: 1695-705.
115. Leal EC, Manivannan A, Hosoya K, 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.
116. Al-Shabrawey M, Rojas M, Sanders T, et al. Role of NADPH oxidase in retinal vascular inflammation. Invest Ophthalmol Vis Sci 2008; 49: 3239-44.
117. Joussen M, Poulaki V, Le ML, et al. A central role for inflammation in the pathogenesis of diabetic retinopathy. FASEB J 2004; 18: 1450-2.
118. Ceriello A, Falleti E, Motz E, et al. Hyperglycemia-induced circulating ICAM-1 increase in diabetes mellitus: the possible role of oxidative stress. Horm Metab Res 1998; 30(3): 146-9.
119. Haraldsen G, Kvale D, Lien B, Farstad IN, Brandtzaeg P. Cyto-kine-regulated expression of E-selectin, intercellular adhesion molecule-1 (ICAM-1), and vascular cell adhesion molecule-1 (VCAM-1) in human microvascular endothelial cells. J Immunol 1996; 156: 2558-65.
120. Xu Q, Qaum T, Adamis AP. Sensitive blood-retinal barrier breakdown quantitation using Evans blue. Invest Ophthalmol Vis Sci 2001; 42: 789-94.
121. Kim SY, Johnson MA, McLeod DS, et al. Neutrophils are associated with capillary closure in spontaneously diabetic monkey retinas. Diabetes 2005; 54: 1534-42.
122. 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. Nat Acad Sci 1999; 96: 10836-41.
123. Greiber S, Müller B, Daemisch P and Pavenstädt H. Reactive oxygen species alter gene expression in podocytes: induction of granu-locyte macrophage-colony-stimulating factor. J Am Soc Nephrol 2002; 13: 86-95.
124. Segerer S, Nelson, PJ, Schloendorf D. Chemokines, chemokine receptors, and renal disease: from basic science to pathophysiologic and therapeutic studies. J Am Soc Nephrol 2000; 11: 152-76.
125. Huber TB, Reinhardt HC, Exner M, et al. Expression of functional CCR and CXCR chemokine receptors in podocytes. J Immunol 2002; 168: 6244-52.
126. Navarro-Gonzalez JF, Fernandez CM. The role of inflammatory cytokines in diabetic nephropathy. J Am Soc Nephrol 2008; 19: 433-42.
127. Nishikawa T, Araki E. Impact of mitochondrial ROS production in the pathogenesis of diabetes mellitus and its complications. Anti-oxid Redox Signal 2007; 9: 343-53.
128. Østerby R, Parving HH, Nyberg G, et al. A strong correlation between glomerular filtration rate and filtration surface in diabetic nephropathy. Diabetologia 1988; 31: 265-70.
129. Galkina E, Ley K. Leukocyte recruitment and vascular injury in diabetic nephropathy. J Am Soc Nephrol 2006; 17: 368-77.
130. Okada S, Shikata K, Matsuda M, et al. Intercellular adhesion mole-cule-1-deficient mice are resistant against renal injury after induction of diabetes. Diabetes 2003; 52: 2586-93.
131. Yamamoto Y, Maeshima Y, Kitayama H, et al. Tumstatin peptide, an inhibitor of angiogenesis, prevents glomerular hypertrophy in the early stage of diabetic nephropathy. Diabetes 2004; 53: 1831-40.
132. Satoh J, Yagihashi S, Toyota T. The possible role of tumor necrosis factor-alpha in diabetic polyneuropathy. Exp Diabesity Res 2003; 4: 65-71.
133. Dyck PJ, Hansen S, Karnes J, et al. Capillary number and percentage closed in human diabetic sural nerve. Proc Natl Acad Sci USA 1985; 82: 2513-7.
134. Malik RA, Newrick PG, Sharma AK, et al. Microangiopathy in human diabetic neuropathy: relationship between capillary abnor-abnor- malities and the severity of neuropathy. Diabetologia 1989; 32: 92-102. malities
135. Dyck PJ, Davies JL, Wilson DM, Service FJ, Melton LJ, O'Brien PC. Risk factors for severity of diabetic polyneuropathy: intensive longitudinal assessment of the Rochester Diabetic Neuropathy Study cohort. Diabetes Care 1999; 22: 1479-86.
136. Dyck PJ, Karnes J, O'Brien P, Nukada H, Lais A, Low P. Spatial pattern of nerve fiber abnormality indicative of pathologic mechanism. Am J Pathol 1984; 117: 225-38.
137. Malik RA, Tesfaye S, Thompson SD, et al. Transperineurial capillary abnormalities in the sural nerve of patients with diabetic neuropathy. Microvasc Res 1994; 48: 236-45.
138. Ward JD. Abnormal microvasculature in diabetic neuropathy. Eye 1993; 7: 223-6.
139. Malik RA, Masson EA, Sharma AK, et al. Hypoxic neuropathy: relevance to human diabetic neuropathy. Diabetologia 1990; 33: 311-18.
140. Joussen A, Poulaki V, Mitsiades N, et al. Nonsteroidal anti-inflammatory drugs prevent early diabetic retinopathy via TNF- suppression. FASEB J 2002; 16: 438-40.
141. Zheng L, Howell SJ, Hatala D, Huang K, Kern TS. Salicylate-based anti-inflammatory drugs inhibit the early lesion of diabetic retinopathy. Diabetes 2007; 56: 337-45.
142. Joussen AM, Poulaki V, Le ML, et al. A central role for inflammation in the pathogenesis of diabetic retinopathy. FASEB J 2004; 18: 1450-52.
143. Carmo A, Cunha-Vaz JG, Carvalho AP, Lopes MC: Effect of cy-closporin-A on the blood–retinal barrier permeability in streptozotocin-induced diabetes. Mediators Inflamm 2000; 9: 243-8.
144. Kern TS and Engerman EL. Pharmacological inhibition of diabetic retinopathy aminoguanidine and aspirin. Diabetes 2001; 50: 1636-42.
145. Kellogg AP, Wiggin TD, Larkin DD, Hayes JM, Stevens MJ, Pop-Busui R. Protective effects of cyclooxygenase-2 gene inactivation against peripheral nerve dysfunction and intraepidermal nerve fiber loss in experimental diabetes. Diabetes 2007; 56: 2997-3005.
146. Gillies MC, Sutter FKP, Simpson JM, Larsson J, Ali H, Zhu M. Intravitreal triamcinolone for refractory diabetic macular edema: two-year results of a double-masked, placebo-controlled, randomized clinical trial. Ophthalmology 2006; 113: 1533-8.
147. Cohen KL, Harris S. Efficacy and safety of nonsteroidal anti-inflammatory drugs in the therapy of diabetic neuropathy. Arch Intern Med 1987; 147: 1442-4.
148. Krendel DA, Costigan DA, Hopkins LC. Successful treatment of neuropathies in patients with diabetes mellitus. Arch Neurol 1995; 52: 1053-61.
149. Wang JJ, Zhang SX, Mott R, et al. Anti-inflammatory effects of pigment epithelium-derived factor in diabetic nephropathy. Am J Physiol Renal Physiol 2008; 294: F1166-73.
150. Han SY, Kim CH, Kim HS, et al. Spironolactone prevents diabetic nephropathy through an anti-inflammatory mechanism in type 2 diabetic rats. J Am Soc Nephrol 2006; 17: 1362-72.
151. Utimura R, Fujihara CK, Mattar AL, et al. Mycophenolate mofetil prevents the development of glomerular injury in experimental diabetes. Kidney Int 2003; 63: 209-16.
152. Cheng HF, Harris RC. Renal effects of non-steroidal anti-inflammatory drugs and selective cyclooxygenase-2 inhibitors. Curr Pharm Des 2005; 11: 1795-1804.
153. Blackshear JL, Davidman M, Stillman MT. Identification of risk for renal insufficiency from nonsteroidal anti-inflammatory drugs. Arch Intern Med 1983; 143: 1130-4.