Microvascular complications of diabetes

Endocrinology and Metabolism Clinics of North America

Volumn 33, Issue 1, 2004, Pages 215-238

  He, Zhiheng ^a   King, George L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KINASE C; REACTIVE OXYGEN METABOLITE;

DIABETIC RETINOPATHY; GLYCATION; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; KIDNEY DISEASE; MICROANGIOPATHY; NEUROPATHY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

ALDEHYDE REDUCTASE; ANIMALS; DIABETES MELLITUS, TYPE 1; DIABETIC ANGIOPATHIES; DIABETIC NEPHROPATHIES; DIABETIC NEUROPATHIES; DIABETIC RETINOPATHY; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; PROTEIN KINASE C;

EID: 1842526645     PISSN: 08898529     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ecl.2003.12.003     Document Type: Review

References (197)

1. 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. N Engl J Med. 329:1993;977-986.
2. The UK Prospective Diabetes Study (UKPDS) Group. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). Lancet. 352:1998;837-853.
3. Williamson J.R., Kilo C. Capillary basement membranes in diabetes. Diabetes. 32:(Suppl 2):1983;96-100.
4. Haneda M., Kikkawa R., Horide N., Togawa M., Koya D., Kajiwara N., et al. Glucose enhances type IV collagen production in cultured rat glomerular mesangial cells. Diabetologia. 34:1991;198-200.
5. Cai J., Boulton M. The pathogenesis of diabetic retinopathy: old concepts and new questions. Eye. 16:2002;242-260.
6. Yarom R., Zirkin H., Stammler G., Rose A.G. Human coronary microvessels in diabetes and ischaemia. Morphometric study of autopsy material. J Pathol. 166:1992;265-270.
7. Ferris F.L. III, Davis M.D., Aiello L.M. Treatment of diabetic retinopathy. N Engl J Med. 341:1999;667-678.
8. Engerman R.L. Pathogenesis of diabetic retinopathy. Diabetes. 38:1989;1203-1206.
9. Robison W.G. Jr., McCaleb M.L., Feld L.G., Michaelis O.E. IV, Laver N., Mercandetti M., et al. Degenerated intramural pericytes ('ghost cells') in the retinal capillaries of diabetic rats. Curr Eye Res. 10:1991;339-350.
10. Mizutani M., Kern T.S., Lorenzi M. Accelerated death of retinal microvascular cells in human and experimental diabetic retinopathy. J Clin Invest. 97:1996;2883-2890.
11. Friedman E.A. Renal syndromes in diabetes. Endocrinol Metab Clin North Am. 25:1996;293-324.
12. Ritz E., Orth S.R. Nephropathy in patients with type 2 diabetes mellitus. N Engl J Med. 341:1999;1127-1133.
13. Cooper M.E. Pathogenesis, prevention, and treatment of diabetic nephropathy. Lancet. 352:1998;213-219.
14. Kuroki T., Isshiki K., King G.L. Oxidative stress: the lead or supporting actor in the pathogenesis of diabetic complications. J Am Soc Nephrol. 14:(Suppl 3):2003;S216-S220.
15. Koya D., Jirousek M.R., Lin Y.W., Ishii H., Kuboki K., King G.L. Characterization of protein kinase C beta isoform activation on the gene expression of transforming growth factor-beta, extracellular matrix components, and prostanoids in the glomeruli of diabetic rats. J Clin Invest. 100:1997;115-126.
16. Koya D., Haneda M., Nakagawa H., Isshiki K., Sato H., Maeda S., et al. Amelioration of accelerated diabetic mesangial expansion by treatment with a PKC beta inhibitor in diabetic db/db mice, a rodent model for type 2 diabetes. FASEB J. 14:2000;439-447.
17. Harati Y. Diabetes and the nervous system. Endocrinol Metab Clin North Am. 25:1996;325-359.
18. Malik R.A., Tesfaye S., Thompson S.D., Veves A., Sharma A.K., Boulton A.J., et al. Endoneurial localisation of microvascular damage in human diabetic neuropathy. Diabetologia. 36:1993;454-459.
19. Sheetz M.J., King G.L. Molecular understanding of hyperglycemia's adverse effects for diabetic complications. JAMA. 288:2002;2579-2588.
20. Sugimoto K., Murakawa Y., Sima A.A. Diabetic neuropathy-a continuing enigma. Diabetes Metab Res Rev. 16:2000;408-433.
21. Schratzberger P., Walter D.H., Rittig K., Bahlmann F.H., Pola R., Curry C., et al. Reversal of experimental diabetic neuropathy by VEGF gene transfer. J Clin Invest. 107:2001;1083-1092.
22. Cameron N.E., Eaton S.E., Cotter M.A., Tesfaye S. Vascular factors and metabolic interactions in the pathogenesis of diabetic neuropathy. Diabetologia. 44:2001;1973-1988.
23. Kannel W.B., McGee D.L. Diabetes and glucose tolerance as risk factors for cardiovascular disease: the Framingham study. Diabetes Care. 2:1979;120-126.
24. Butler W.J., Ostrander L.D. Jr., Carman W.J., Lamphiear D.E. Mortality from coronary heart disease in the Tecumseh study. Long-term effect of diabetes mellitus, glucose tolerance and other risk factors. Am J Epidemiol. 121:1985;541-547.
25. Klein R. Hyperglycemia and microvascular and macrovascular disease in diabetes. Diabetes Care. 18:1995;258-268.
26. Kuller L.H., Velentgas P., Barzilay J., Beauchamp N.J., O'Leary D.H., Savage P.J. Diabetes mellitus: subclinical cardiovascular disease and risk of incident cardiovascular disease and all-cause mortality. Arterioscler Thromb Vasc Biol. 20:2000;823-829.
27. Howard B.V., Rodriguez B.L., Bennett P.H., Harris M.I., Hamman R., Kuller L.H., et al. Prevention Conference VI: diabetes and cardiovascular disease: writing group I: epidemiology. Circulation. 105:(18):2002;e132-e137.
28. Smith J.W., Marcus F.I., Serokman R. Prognosis of patients with diabetes mellitus after acute myocardial infarction. Am J Cardiol. 54:1984;718-721.
29. Abbott R.D., Donahue R.P., Kannel W.B., Wilson P.W. The impact of diabetes on survival following myocardial infarction in men vs women. The Framingham Study. JAMA. 260:1988;3456-3460.
30. Haffner S.M., Lehto S., Ronnemaa T., Pyorala K., Laakso M. Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N Engl J Med. 339:1998;229-234.
31. Marfella R., D'Amico M., Di Filippo C., Piegari E., Nappo F., Esposito K., et al. Myocardial infarction in diabetic rats: role of hyperglycaemia on infarct size and early expression of hypoxia-inducible factor 1. Diabetologia. 45:2002;1172-1181.
32. Abaci A., Oguzhan A., Kahraman S., Eryol N.K., Unal S., Arinc H., et al. Effect of diabetes mellitus on formation of coronary collateral vessels. Circulation. 99:1999;2239-2242.
33. McDonagh P.F., Hokama J.Y. Microvascular perfusion and transport in the diabetic heart. Microcirculation. 7:2000;163-181.
34. Thompson E.W. Quantitative analysis of myocardial structure in insulin-dependent diabetes mellitus: effects of immediate and delayed insulin replacement. Proc Soc Exp Biol Med. 205:1994;294-305.
35. Warley A., Powell J.M., Skepper J.N. Capillary surface area is reduced and tissue thickness from capillaries to myocytes is increased in the left ventricle of streptozotocin-diabetic rats. Diabetologia. 38:1995;413-421.
36. Chou E., Suzuma I., Way K.J., Opland D., Clermont A.C., Naruse K., et al. Decreased cardiac expression of vascular endothelial growth factor and its receptors in insulin-resistant and diabetic states: a possible explanation for impaired collateral formation in cardiac tissue. Circulation. 105:2002;373-379.
37. Giordano F.J., Gerber H.P., Williams S.P., VanBruggen N., Bunting S., Ruiz-Lozano P., et al. A cardiac myocyte vascular endothelial growth factor paracrine pathway is required to maintain cardiac function. Proc Natl Acad Sci USA. 98:2001;5780-5785.
38. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature. 414:2001;813-820.
39. Nishikawa T., Edelstein D., Du X.L., Yamagishi S., Matsumura T., Kaneda Y., et al. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature. 404:2000;787-790.
40. Du X.L., Edelstein D., Dimmeler S., Ju Q., Sui C., Brownlee M. Hyperglycemia inhibits endothelial nitric oxide synthase activity by posttranslational modification at the Akt site. J Clin Invest. 108:2001;1341-1348.
41. Wautier M.P., Chappey O., Corda S., Stern D.M., Schmidt A.M., Wautier J.L. Activation of NADPH oxidase by AGE links oxidant stress to altered gene expression via RAGE. Am J Physiol Endocrinol Metab. 280:2001;E685-E694.
42. Inoguchi T., Li P., Umeda F., Yu H.Y., Kakimoto M., Imamura M., et al. High glucose level and free fatty acid stimulate reactive oxygen species production through protein kinase C-dependent activation of NAD(P)H oxidase in cultured vascular cells. Diabetes. 49:2000;1939-1945.
43. Cosentino F., Hishikawa K., Katusic Z.S., Luscher T.F. High glucose increases nitric oxide synthase expression and superoxide anion generation in human aortic endothelial cells. Circulation. 96:1997;25-28.
44. Jain S.K., McVie R. Effect of glycemic control, race (white versus black), and duration of diabetes on reduced glutathione content in erythrocytes of diabetic patients. Metabolism. 43:1994;306-309.
45. Jennings P.E., Chirico S., Jones A.F., Lunec J., Barnett A.H. Vitamin C metabolites and microangiopathy in diabetes mellitus. Diabetes Res. 6:1987;151-154.
46. Karpen C.W., Cataland S., O'Dorisio T.M., Panganamala R.V. Production of 12-hydroxyeicosatetraenoic acid and vitamin E status in platelets from type I human diabetic subjects. Diabetes. 34:1985;526-531.
47. Will J.C., Ford E.S., Bowman B.A. Serum vitamin C concentrations and diabetes: findings from the Third National Health and Nutrition Examination Survey, 1988-1994. Am J Clin Nutr. 70:1999;49-52.
48. Campoy C., Baena R.M., Blanca E., Lopez-Sabater C., Fernandez-Garcia J.M., Miranda M.T., et al. Effects of metabolic control on vitamin E nutritional status in children with type 1 diabetes mellitus. Clin Nutr. 22:2003;81-86.
49. Dandona P., Thusu K., Cook S., Snyder B., Makowski J., Armstrong D., et al. Oxidative damage to DNA in diabetes mellitus. Lancet. 347:1996;444-445.
50. Suzuki S., Hinokio Y., Komatu K., Ohtomo M., Onoda M., Hirai S., et al. Oxidative damage to mitochondrial DNA and its relationship to diabetic complications. Diabetes Res Clin Pract. 45:1999;161-168.
51. Garcia Soriano F., Virag L., Jagtap P., Szabo E., Mabley J.G., Liaudet L., et al. Diabetic endothelial dysfunction: the role of poly(ADP-ribose) polymerase activation. Nat Med. 7:2001;108-113.
52. Kowluru R.A., Tang J., Kern T.S. Abnormalities of retinal metabolism in diabetes and experimental galactosemia VII. Effect of long-term administration of antioxidants on the development of retinopathy. Diabetes. 50:2001;1938-1942.
53. Kowluru R.A., Koppolu P. Diabetes-induced activation of caspase-3 in retina: effect of antioxidant therapy. Free Radic Res. 36:2002;993-999.
54. Cameron N.E., Cotter M.A., Archibald V., Dines K.C., Maxfield E.K. Anti-oxidant and pro-oxidant effects on nerve conduction velocity, endoneurial blood flow and oxygen tension in non-diabetic and streptozotocindiabetic rats. Diabetologia. 37:1994;449-459.
55. Nagamatsu M., Nickander K.K., Schmelzer J.D., Raya A., Wittrock D.A., Tritschler H., et al. Lipoic acid improves nerve blood flow, reduces oxidative stress, and improves distal nerve conduction in experimental diabetic neuropathy. Diabetes Care. 18:1995;1160-1167.
56. Lal M.A., Korner A., Matsuo Y., Zelenin S., Cheng S.X., Jaremko G., et al. Combined antioxidant and COMT inhibitor treatment reverses renal abnormalities in diabetic rats. Diabetes. 49:2000;1381-1389.
57. Gaede P., Poulsen H.E., Parving H.H., Pedersen O. Double-blind, randomised study of the effect of combined treatment with vitamin C and E on albuminuria in Type 2 diabetic patients. Diabet Med. 18:2001;756-760.
58. Bursell S.E., Clermont A.C., Aiello L.P., Aiello L.M., Schlossman D.K., Feener E.P., et al. High-dose vitamin E supplementation normalizes retinal blood flow and creatinine clearance in patients with type 1 diabetes. Diabetes Care. 22:1999;1245-1251.
59. Yusuf S., Dagenais G., Pogue J., Bosch J., Sleight P. Vitamin E supplementation and cardiovascular events in high-risk patients. The Heart Outcomes Prevention Evaluation Study Investigators. N Engl J Med. 342:2000;154-160.
60. Lonn E., Yusuf S., Hoogwerf B., Pogue J., Yi Q., Zinman B., et al. Effects of vitamin E on cardiovascular and microvascular outcomes in high-risk patients with diabetes: results of the HOPE study and MICRO-HOPE substudy. Diabetes Care. 25:2002;1919-1927.
61. Kunisaki M., Bursell S.E., Clermont A.C., Ishii H., Ballas L.M., Jirousek M.R., et al. Vitamin E prevents diabetes-induced abnormal retinal blood flow via the diacylglycerol-protein kinase C pathway. Am J Physiol. 269:1995;E239-E246.
62. Tesfamariam B. Free radicals in diabetic endothelial cell dysfunction. Free Radic Biol Med. 16:1994;383-391.
63. Robison W.G. Jr., Nagata M., Laver N., Hohman T.C., Kinoshita J.H. Diabetic-like retinopathy in rats prevented with an aldose reductase inhibitor. Invest Ophthalmol Vis Sci. 30:1989;2285-2292.
64. Kador P.F., Akagi Y., Takahashi Y., Ikebe H., Wyman M., Kinoshita J.H. Prevention of retinal vessel changes associated with diabetic retinopathy in galactose-fed dogs by aldose reductase inhibitors. Arch Ophthalmol. 108:1990;1301-1309.
65. Mauer S.M., Steffes M.W., Azar S., Brown D.M. Effects of sorbinil on glomerular structure and function in long-term- diabetic rats. Diabetes. 38:1989;839-846.
66. Yue D.K., Hanwell M.A., Satchell P.M., Turtle J.R. The effect of aldose reductase inhibition on motor nerve conduction velocity in diabetic rats. Diabetes. 31:1982;789-794.
67. Cameron N.E., Leonard M.B., Ross I.S., Whiting P.H. The effects of sorbinil on peripheral nerve conduction velocity, polyol concentrations and morphology in the streptozotocin-diabetic rat. Diabetologia. 29:1986;168-174.
68. Engerman R.L., Kern T.S., Larson M.E. Nerve conduction and aldose reductase inhibition during 5 years of diabetes or galactosaemia in dogs. Diabetologia. 37:1994;141-144.
69. Greene D.A., Arezzo J.C., Brown M.B. Effect of aldose reductase inhibition on nerve conduction and morphometry in diabetic neuropathy. Zenarestat Study Group. Neurology. 53:1999;580-591.
70. Wells-Knecht K.J., Zyzak D.V., Litchfield J.E., Thorpe S.R., Baynes J.W. Mechanism of autoxidative glycosylation: identification of glyoxal and arabinose as intermediates in the autoxidative modification of proteins by glucose. Biochemistry. 34:1995;3702-3709.
71. Thornalley P.J. The glyoxalase system: new developments towards functional characterization of a metabolic pathway fundamental to biological life. Biochem J. 269:1990;1-11.
72. Berg T.J., Bangstad H.J., Torjesen P.A., Osterby R., Bucala R., Hanssen K.F. Advanced glycation end products in serum predict changes in the kidney morphology of patients with insulin-dependent diabetes mellitus. Metabolism. 46:1997;661-665.
73. Suzuki D., Miyata T., Saotome N., Horie K., Inagi R., Yasuda Y., et al. Immunohistochemical evidence for an increased oxidative stress and carbonyl modification of proteins in diabetic glomerular lesions. J Am Soc Nephrol. 10:1999;822-832.
74. Gugliucci A., Bendayan M. Reaction of advanced glycation endproducts with renal tissue from normal and streptozotocin-induced diabetic rats: an ultrastructural study using colloidal gold cytochemistry. J Histochem Cytochem. 43:1995;591-600.
75. Makino H., Shikata K., Hironaka K., Kushiro M., Yamasaki Y., Sugimoto H., et al. Ultrastructure of nonenzymatically glycated mesangial matrix in diabetic nephropathy. Kidney Int. 48:1995;517-526.
76. Horie K., Miyata T., Maeda K., Miyata S., Sugiyama S., Sakai H., et al. Immunohistochemical colocalization of glycoxidation products and lipid peroxidation products in diabetic renal glomerular lesions. Implication for glycoxidative stress in the pathogenesis of diabetic nephropathy. J Clin Invest. 100:1997;2995-3004.
77. Tanji N., Markowitz G.S., Fu C., Kislinger T., Taguchi A., Pischetsrieder M., et al. Expression of advanced glycation end products and their cellular receptor RAGE in diabetic nephropathy and nondiabetic renal disease. J Am Soc Nephrol. 11:2000;1656-1666.
78. Stitt A.W., Li Y.M., Gardiner T.A., Bucala R., Archer D.B., Vlassara H. Advanced glycation end products (AGEs) co-localize with AGE receptors in the retinal vasculature of diabetic and of AGE-infused rats. Am J Pathol. 150:1997;523-531.
79. Hammes H.P., Wellensiek B., Kloting I., Sickel E., Bretzel R.G., Brownlee M. The relationship of glycaemic level to advanced glycation end-product (AGE) accumulation and retinal pathology in the spontaneous diabetic hamster. Diabetologia. 41:1998;165-170.
80. Yamagishi S., Hsu C.C., Taniguchi M., Harada S., Yamamoto Y., Ohsawa K., et al. Receptor-mediated toxicity to pericytes of advanced glycosylation end products: a possible mechanism of pericyte loss in diabetic microangiopathy. Biochem Biophys Res Commun. 213:1995;681-687.
81. Wautier J.L., Zoukourian C., Chappey O., Wautier M.P., Guillausseau P.J., Cao R., et al. Receptor-mediated endothelial cell dysfunction in diabetic vasculopathy. Soluble receptor for advanced glycation end products blocks hyperpermeability in diabetic rats. J Clin Invest. 97:1996;238-243.
82. Vlassara H., Fuh H., Makita Z., Krungkrai S., Cerami A., Bucala R. Exogenous advanced glycosylation end products induce complex vascular dysfunction in normal animals: a model for diabetic and aging complications. Proc Natl Acad Sci USA. 89:1992;12043-12047.
83. Soulis-Liparota T., Cooper M., Papazoglou D., Clarke B., Jerums G. Retardation by aminoguanidine of development of albuminuria, mesangial expansion, and tissue fluorescence in streptozocin-induced diabetic rat. Diabetes. 40:1991;1328-1334.
84. Nakamura S., Makita Z., Ishikawa S., Yasumura K., Fujii W., Yanagisawa K., et al. Progression of nephropathy in spontaneous diabetic rats is prevented by OPB-9195, a novel inhibitor of advanced glycation. Diabetes. 46:1997;895-899.
85. Hammes H.P., Martin S., Federlin K., Geisen K., Brownlee M. Aminoguanidine treatment inhibits the development of experimental diabetic retinopathy. Proc Natl Acad Sci USA. 88:1991;11555-11558.
86. Tanaka S., Avigad G., Brodsky B., Eikenberry E.F. Glycation induces expansion of the molecular packing of collagen. J Mol Biol. 203:1998;495-505.
87. Tsilibary E.C., Charonis A.S., Reger L.A., Wohlhueter R.M., Furcht L.T. The effect of nonenzymatic glucosylation on the binding of the main noncollagenous NC1 domain to type IV collagen. J Biol Chem. 263:1988;4302-4308.
88. Haitoglou C.S., Tsilibary E.C., Brownlee M., Charonis A.S. Altered cellular interactions between endothelial cells and nonenzymatically glucosylated laminin/type IV collagen. J Biol Chem. 267:1992;12404-12407.
89. Li Y.M., Mitsuhashi T., Wojciechowicz D., Shimizu N., Li J., Stitt A., et al. Molecular identity and cellular distribution of advanced glycation endproduct receptors: relationship of p60 to OST-48 and p90 to 80K-H membrane proteins. Proc Natl Acad Sci USA. 93:1996;11047-11052.
90. Smedsrod B., Melkko J., Araki N., Sano H., Horiuchi S. Advanced glycation end products are eliminated by scavenger-receptor-mediated endocytosis in hepatic sinusoidal Kupffer and endothelial cells. Biochem J. 322:(Pt 2):1997;567-573.
91. Vlassara H., Li Y.M., Imani F., Wojciechowicz D., Yang Z., Liu F.T., et al. Identification of galectin-3 as a high-affinity binding protein for advanced glycation end products (AGE): a new member of the AGE-receptor complex. Mol Med. 1:1995;634-646.
92. Neeper M., Schmidt A.M., Brett J., Yan S.D., Wang F., Pan Y.C., et al. Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins. J Biol Chem. 267:1992;14998-15004.
93. Schmidt A.M., Stern D.M. RAGE: a new target for the prevention and treatment of the vascular and inflammatory complications of diabetes. Trends Endocrinol Metab. 11:2000;368-375.
94. Vlassara H. The AGE-receptor in the pathogenesis of diabetic complications. Diabetes Metab Res Rev. 17:2001;436-443.
95. Yamamoto Y., Kato I., Doi T., Yonekura H., Ohashi S., Takeuchi M., et al. Development and prevention of advanced diabetic nephropathy in RAGE-overexpressing mice. J Clin Invest. 108:2001;261-268.
96. Yan S.D., Schmidt A.M., Anderson G.M., Zhang J., Brett J., Zou Y.S., et al. Enhanced cellular oxidant stress by the interaction of advanced glycation end products with their receptors/binding proteins. J Biol Chem. 269:1994;9889-9897.
97. Lander H.M., Tauras J.M., Ogiste J.S., Hori O., Moss R.A., Schmidt A.M. Activation of the receptor for advanced glycation end products triggers a p21(ras)-dependent mitogen-activated protein kinase pathway regulated by oxidant stress. J Biol Chem. 272:1997;17810-17814.
98. Huttunen H.J., Fages C., Rauvala H. Receptor for advanced glycation end products (RAGE)-mediated neurite outgrowth and activation of NFkappaB require the cytoplasmic domain of the receptor but different downstream signaling pathways. J Biol Chem. 274:1999;19919-19924.
99. Hofmann M.A., Drury S., Fu C., Qu W., Taguchi A., Lu Y., et al. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell. 97:1999;889-901.
100. Li J.H., Huang X.R., Zhu H.J., Oldfield M., Cooper M., Truong L.D., et al. Advanced glycation end products activate Smad signaling via TGF-beta-dependent and -independent mechanisms: implications for diabetic renal and vascular disease. FASEB J. 18:(1):2004;76-78.
101. Brownlee M., Vlassara H., Kooney A., Ulrich P., Cerami A. Aminoguanidine prevents diabetes-induced arterial wall protein cross-linking. Science. 232:1986;1629-1632.
102. Vasan S., Zhang X., Kapurniotu A., Bernhagen J., Teichberg S., Basgen J., et al. An agent cleaving glucose-derived protein crosslinks in vitro and in vivo. Nature. 382:1996;275-278.
103. Wolffenbuttel B.H., Boulanger C.M., Crijns F.R., Huijberts M.S., Poitevin P., Swennen G.N., et al. Breakers of advanced glycation end products restore large artery properties in experimental diabetes. Proc Natl Acad Sci USA. 95:1998;4630-4634.
104. Kass D.A., Shapiro E.P., Kawaguchi M., Capriotti A.R., Scuteri A., deGroof R.C., et al. Improved arterial compliance by a novel advanced glycation end-product crosslink breaker. Circulation. 104:2001;1464-1470.
105. Clements R.S. Jr., Robison W.G. Jr., Cohen M.P. Anti-glycated albumin therapy ameliorates early retinal microvascular pathology in db/db mice. J Diabetes Complications. 12:1998;28-33.
106. Park L., Raman K.G., Lee K.J., Lu Y., Ferran L.J. Jr., Chow W.S., et al. Suppression of accelerated diabetic atherosclerosis by the soluble receptor for advanced glycation endproducts. Nat Med. 4:1998;1025-1031.
107. Bonnardel-Phu E., Wautier J.L., Schmidt A.M., Avila C., Vicaut E. Acute modulation of albumin microvascular leakage by advanced glycation end products in microcirculation of diabetic rats in vivo. Diabetes. 48:1999;2052-2058.
108. Zheng F., Cai W., Mitsuhashi T., Vlassara H. Lysozyme enhances renal excretion of advanced glycation endproducts in vivo and suppresses adverse age-mediated cellular effects in vitro: a potential AGE sequestration therapy for diabetic nephropathy? Mol Med. 7:2001;737-747.
109. Federici M., Menghini R., Mauriello A., Hribal M.L., Ferrelli F., Lauro D., et al. Insulin-dependent activation of endothelial nitric oxide synthase is impaired by O-linked glycosylation modification of signaling proteins in human coronary endothelial cells. Circulation. 106:2002;466-472.
110. Du X., Edelstein D., Rossetti L., Fantus I., Goldberg H., Ziyadeh F., et al. Hyperglycemia-induced mitochondrial superoxide overproduction activates the hexosamine pathway and induces plasminogen activator inhibitor-1 expression by increasing Sp1 glycosylation. Proc Natl Acad Sci USA. 97:2000;12222-12226.
111. Wu G., Haynes T.E., Yan W., Meininger C.J. Presence of glutamine:fructose-6-phosphate amidotransferase for glucosamine-6-phosphate synthesis in endothelial cells: effects of hyperglycaemia and glutamine. Diabetologia. 44:2001;196-202.
112. Akimoto Y., Kreppel L.K., Hirano H., Hart G.W. Hyperglycemia and the O-GlcNAc transferase in rat aortic smooth muscle cells: elevated expression and altered patterns of O-GlcNAcylation. Arch Biochem Biophys. 389:2001;166-175.
113. Tannock L.R., Little P.J., Wight T.N., Chait A. Arterial smooth muscle cell proteoglycans synthesized in the presence of glucosamine demonstrate reduced binding to LDL. J Lipid Res. 43:2002;149-157.
114. Nerlich A.G., Sauer U., Kolm-Litty V., Wagner E., Koch M., Schleicher E.D. Expression of glutamine:fructose-6-phosphate amidotransferase in human tissues: evidence for high variability and distinct regulation in diabetes. Diabetes. 47:1998;170-178.
115. Fujii N., Kaji T., Yamamoto C., Fujiwara Y., Koizumi F. Phorbol 12-myristate 13-acetate stimulates the release of glycosaminoglycans from cultured vascular endothelial cells: possible involvement of protein kinase C activation. Thromb Res. 82:1996;379-387.
116. James L., Ingram A., Ly H., Thai K., Cai L., Scholey J. Angiotensin II activates the GFAT promoter in mesangial cells. Am J Physiol Renal Physiol. 281:2001;F151-F162.
117. Way K.J., Chou E., King G.L. Identification of PKC-isoform-specific biological actions using pharmacological approaches. Trends Pharmacol Sci. 21:2000;181-187.
118. Way K.J., Katai N., King G.L. Protein kinase C and the development of diabetic vascular complications. Diabet Med. 18:2001;945-959.
119. Inoguchi T., Battan R., Handler E., Sportsman J.R., Heath W., King G.L. Preferential elevation of protein kinase C isoform beta II and diacylglycerol levels in the aorta and heart of diabetic rats: differential reversibility to glycemic control by islet cell transplantation. Proc Natl Acad Sci USA. 89:1992;11059-11063.
120. Shiba T., Inoguchi T., Sportsman J.R., Heath W.F., Bursell S., King G.L. Correlation of diacylglycerol level and protein kinase C activity in rat retina to retinal circulation. Am J Physiol. 265:1993;E783-E793.
121. Xia P., Inoguchi T., Kern T.S., Engerman R.L., Oates P.J., King G.L. Characterization of the mechanism for the chronic activation of diacylglycerol-protein kinase C pathway in diabetes and hypergalactosemia. Diabetes. 43:1994;1122-1129.
122. Xia P., Aiello L.P., Ishii H., Jiang Z.Y., Park D.J., Robinson G.S., et al. Characterization of vascular endothelial growth factor's effect on the activation of protein kinase C, its isoforms, and endothelial cell growth. J Clin Invest. 98:1996;2018-2026.
123. Suzuma K., Takahara N., Suzuma I., Isshiki K., Ueki K., Leitges M., et al. Characterization of protein kinase C beta isoform's action on retinoblastoma protein phosphorylation, vascular endothelial growth factor-induced endothelial cell proliferation, and retinal neovascularization. Proc Natl Acad Sci USA. 99:2002;721-726.
124. Yu H.Y., Inoguchi T., Kakimoto M., Nakashima N., Imamura M., Hashimoto T., et al. Saturated non-esterified fatty acids stimulate de novo diacylglycerol synthesis and protein kinase c activity in cultured aortic smooth muscle cells. Diabetologia. 44:2001;614-620.
125. Taher M.M., Garcia J.G., Natarajan V. Hydroperoxide-induced diacylglycerol formation and protein kinase C activation in vascular endothelial cells. Arch Biochem Biophys. 303:1993;260-266.
126. Kim Y.S., Kim B.C., Song C.Y., Hong H.K., Moon K.C., Lee H.S. Advanced glycosylation end products stimulate collagen mRNA synthesis in mesangial cells mediated by protein kinase C and transforming growth factor-beta. J Lab Clin Med. 138:2001;59-68.
127. Ishii H., Jirousek M.R., Koya D., Takagi C., Xia P., Clermont A., et al. Amelioration of vascular dysfunctions in diabetic rats by an oral PKC beta inhibitor. Science. 272:1996;728-731.
128. Lynch J.J., Ferro T.J., Blumenstock F.A., Brockenauer A.M., Malik A.B. Increased endothelial albumin permeability mediated by protein kinase C activation. J Clin Invest. 85:1990;1991-1998.
129. Oliver J.A. Adenylate cyclase and protein kinase C mediate opposite actions on endothelial junctions. J Cell Physiol. 145:1990;536-542.
130. Stasek J.E. Jr., Patterson C.E., Garcia J.G. Protein kinase C phosphorylates caldesmon77 and vimentin and enhances albumin permeability across cultured bovine pulmonary artery endothelial cell monolayers. J Cell Physiol. 153:1992;62-75.
131. Studer R.K., Craven P.A., DeRubertis F.R. Role for protein kinase C in the mediation of increased fibronectin accumulation by mesangial cells grown in high-glucose medium. Diabetes. 42:1993;118-126.
132. Craven P.A., Studer R.K., DeRubertis F.R. Impaired nitric oxide-dependent cyclic guanosine monophosphate generation in glomeruli from diabetic rats. Evidence for protein kinase C-mediated suppression of the cholinergic response. J Clin Invest. 93:1994;311-320.
133. Ganz M.B., Seftel A. Glucose-induced changes in protein kinase C and nitric oxide are prevented by vitamin E. Am J Physiol Endocrinol Metab. 278:2000;E146-E152.
134. Kuboki K., Jiang Z.Y., Takahara N., Ha S.W., Igarashi M., Yamauchi T., et al. Regulation of endothelial constitutive nitric oxide synthase gene expression in endothelial cells and in vivo: a specific vascular action of insulin. Circulation. 101:2000;676-681.
135. Yokota T., Ma R.C., Park J.Y., Isshiki K., Sotiropoulos K.B., Rauniyar R.K., et al. Role of protein kinase C on the expression of platelet-derived growth factor and endothelin-1 in the retina of diabetic rats and cultured retinal capillary pericytes. Diabetes. 52:2003;838-845.
136. Williams B., Gallacher B., Patel H., Orme C. Glucose-induced protein kinase C activation regulates vascular permeability factor mRNA expression and peptide production by human vascular smooth muscle cells in vitro. Diabetes. 46:1997;1497-1503.
137. Way K.J., Isshiki K., Suzuma K., Yokota T., Zvagelsky D., Schoen F.J., et al. Expression of connective tissue growth factor is increased in injured myocardium associated with protein kinase C beta2 activation and diabetes. Diabetes. 51:2002;2709-2718.
138. Aiello L.P., Bursell S.E., Clermont A., Duh E., Ishii H., Takagi C., et al. Vascular endothelial growth factor-induced retinal permeability is mediated by protein kinase C in vivo and suppressed by an orally effective beta-isoform-selective inhibitor. Diabetes. 46:1997;1473-1480.
139. Kuroki T., Inoguchi T., Umeda F., Ueda F., Nawata H. High glucose induces alteration of gap junction permeability and phosphorylation of connexin-43 in cultured aortic smooth muscle cells. Diabetes. 47:1998;931-936.
140. Jirousek M.R., Gillig J.R., Gonzalez C.M., Heath W.F., McDonald J.H. III, Neel D.A., et al. (S)-13-[(dimethylamino)methyl]-10, 11,14, 15-tetrahydro-4, 9:16, 21-dimetheno-1H, 13H-dibenzo[e, k]pyrrolo[3, 4-h][1, 4,13] oxadiazacyclohexadecene-1, 3(2H)-d ione (LY333531) and related analogues: isozyme selective inhibitors of protein kinase C beta. J Med Chem. 39:1996;2664-2671.
141. Bursell S.E., Takagi C., Clermont A.C., Takagi H., Mori F., Ishii H., et al. Specific retinal diacylglycerol and protein kinase C beta isoform modulation mimics abnormal retinal hemodynamics in diabetic rats. Invest Ophthalmol Vis Sci. 38:1997;2711-2720.
142. Danis R.P., Bingaman D.P., Jirousek M., Yang Y. Inhibition of intraocular neovascularization caused by retinal ischemia in pigs by PKCbeta inhibition with LY333531. Invest Ophthalmol Vis Sci. 39:1998;171-179.
143. Nonaka A., Kiryu J., Tsujikawa A., Yamashiro K., Miyamoto K., Nishiwaki H., et al. PKC-beta inhibitor (LY333531) attenuates leukocyte entrapment in retinal microcirculation of diabetic rats. Invest Ophthalmol Vis Sci. 41:2000;2702-2706.
144. Aiello L.P. The potential role of PKC beta in diabetic retinopathy and macular edema. Surv Ophthalmol. 47:(Suppl 2):2002;S263-S269.
145. Kelly D.J., Zhang Y., Hepper C., Gow R.M., Jaworski K., Kemp B.E., et al. Protein kinase C beta inhibition attenuates the progression of experimental diabetic nephropathy in the presence of continued hypertension. Diabetes. 52:2003;512-518.
146. Nakamura J., Kato K., Hamada Y., Nakayama M., Chaya S., Nakashima E., et al. A protein kinase C-beta-selective inhibitor ameliorates neural dysfunction in streptozotocin-induced diabetic rats. Diabetes. 48:1999;2090-2095.
147. Cotter M.A., Jack A.M., Cameron N.E. Effects of the protein kinase C beta inhibitor LY333531 on neural and vascular function in rats with streptozotocin-induced diabetes. Clin Sci (Lond). 103:2002;311-321.
148. Cameron N.E., Cotter M.A. Effects of protein kinase C beta inhibition on neurovascular dysfunction in diabetic rats: interaction with oxidative stress and essential fatty acid dysmetabolism. Diabetes Metab Res Rev. 18:2002;315-323.
149. Beckman J.A., Goldfine A.B., Gordon M.B., Garrett L.A., Creager M.A. Inhibition of protein kinase C beta prevents impaired endothelium-dependent vasodilation caused by hyperglycemia in humans. Circ Res. 90:2002;107-111.
150. Bastyr E. III, Price K., Skljarevski V., Lledo A., Vignati L. Ruboxistaurin (RBX) mesylate treatment in patients with diabetic peripheral neuropathy (DPN) improves clinical global impression (CGI) and correlates with change in patient symptoms and signs. Diabetes. 52:2003;A191.
151. Aiello L.P., Avery R.L., Arrigg P.G., Keyt B.A., Jampel H.D., Shah S.T., et al. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med. 331:1994;1480-1487.
152. Hammes H.P., Lin J., Bretzel R.G., Brownlee M., Breier G. Upregulation of the vascular endothelial growth factor/vascular endothelial growth factor receptor system in experimental background diabetic retinopathy of the rat. Diabetes. 47:1998;401-406.
153. Boulton M., Foreman D., Williams G., McLeod D. VEGF localisation in diabetic retinopathy. Br J Ophthalmol. 82:1998;561-568.
154. Ishida S., Usui T., Yamashiro K., Kaji Y., Amano S., Ogura Y., et al. VEGF164-mediated inflammation is required for pathological, but not physiological, ischemia-induced retinal neovascularization. J Exp Med. 198:2003;483-489.
155. Cao R., Brakenhielm E., Pawliuk R., Wariaro D., Post M.J., Wahlberg E., et al. Angiogenic synergism, vascular stability and improvement of hind-limb ischemia by a combination of PDGF-BB and FGF-2. Nat Med. 9:2003;604-613.
156. Leveen P., Pekny M., Gebre-Medhin S., Swolin B., Larsson E., Betsholtz C. Mice deficient for PDGF B show renal, cardiovascular, and hematological abnormalities. Genes Dev. 8:1994;1875-1887.
157. Lindahl P., Johansson B.R., Leveen P., Betsholtz C. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science. 277:1997;242-245.
158. Lindblom P., Gerhardt H., Liebner S., Abramsson A., Enge M., Hellstrom M., et al. Endothelial PDGFB retention is required for proper investment of pericytes in the microvessel wall. Genes Dev. 17:2003;1835-1840.
159. Yamamoto T., Nakamura T., Noble N.A., Ruoslahti E., Border W.A. Expression of transforming growth factor beta is elevated in human and experimental diabetic nephropathy. Proc Natl Acad Sci USA. 90:1993;1814-1818.
160. Border W.A., Yamamoto T., Noble N.A. Transforming growth factor beta in diabetic nephropathy. Diabetes Metab Rev. 12:1996;309-339.
161. Sharma K., Ziyadeh F.N., Alzahabi B., McGowan T.A., Kapoor S., Kurnik B.R., et al. Increased renal production of transforming growth factor-beta1 in patients with type II diabetes. Diabetes. 46:1997;854-859.
162. Pankewycz O.G., Guan J.X., Bolton W.K., Gomez A., Benedict J.F. Renal TGF-beta regulation in spontaneously diabetic NOD mice with correlations in mesangial cells. Kidney Int. 46:1994;748-758.
163. Park I.S., Kiyomoto H., Abboud S.L., Abboud H.E. Expression of transforming growth factor-beta and type IV collagen in early streptozotocininduced diabetes. Diabetes. 46:1997;473-480.
164. Throckmorton D.C., Brogden A.P., Min B., Rasmussen H., Kashgarian M. PDGF and TGF-beta mediate collagen production by mesangial cells exposed to advanced glycosylation end products. Kidney Int. 48:1995;111-117.
165. Wong T.Y., Phillips A.O., Witowski J., Topley N. Glucose-mediated induction of TGF-beta 1 and MCP-1 in mesothelial cells in vitro is osmolality and polyol pathway dependent. Kidney Int. 63:2003;1404-1416.
166. Goldberg H.J., Scholey J., Fantus I.G. Glucosamine activates the plasminogen activator inhibitor 1 gene promoter through Sp1 DNA binding sites in glomerular mesangial cells. Diabetes. 49:2000;863-871.
167. Wolf G. Cell cycle regulation in diabetic nephropathy. Kidney Int Suppl. 77:2000;S59-S66.
168. Sharma K., Jin Y., Guo J., Ziyadeh F.N. Neutralization of TGF-beta by anti-TGF-beta antibody attenuates kidney hypertrophy and the enhanced extracellular matrix gene expression in STZ-induced diabetic mice. Diabetes. 45:1996;522-530.
169. Ziyadeh F.N., Hoffman B.B., Han D.C., Iglesias-De La Cruz M.C., Hong S.W., Isono M., et al. Long-term prevention of renal insufficiency, excess matrix gene expression, and glomerular mesangial matrix expansion by treatment with monoclonal antitransforming growth factor-beta antibody in db/db diabetic mice. Proc Natl Acad Sci USA. 97:2000;8015-8020.
170. Han D.C., Hoffman B.B., Hong S.W., Guo J., Ziyadeh F.N. Therapy with antisense TGF-beta1 oligodeoxynucleotides reduces kidney weight and matrix mRNAs in diabetic mice. Am J Physiol Renal Physiol. 278:2000;F628-F634.
171. Murphy M., Godson C., Cannon S., Kato S., Mackenzie H.S., Martin F., et al. Suppression subtractive hybridization identifies high glucose levels as a stimulus for expression of connective tissue growth factor and other genes in human mesangial cells. J Biol Chem. 274:1999;5830-5834.
172. Gupta S., Clarkson M.R., Duggan J., Brady H.R. Connective tissue growth factor: potential role in glomerulosclerosis and tubulointerstitial fibrosis. Kidney Int. 58:2000;1389-1399.
173. Riser B.L., Denichilo M., Cortes P., Baker C., Grondin J.M., Yee J., et al. Regulation of connective tissue growth factor activity in cultured rat mesangial cells and its expression in experimental diabetic glomerulosclerosis. J Am Soc Nephrol. 11:2000;25-38.
174. Weston B.S., Wahab N.A., Mason R.M. CTGF mediates TGF-beta-induced fibronectin matrix deposition by upregulating active alpha5beta1 integrin in human mesangial cells. J Am Soc Nephrol. 14:2003;601-610.
175. Riser B.L., Cortes P., DeNichilo M., Deshmukh P.V., Chahal P.S., Mohammed A.K., et al. Urinary CCN2 (CTGF) as a possible predictor of diabetic nephropathy: preliminary report. Kidney Int. 64:2003;451-458.
176. Twigg S.M., Cao Z., McLennan S.V., Burns W.C., Brammar G., Forbes J.M., et al. Renal connective tissue growth factor induction in experimental diabetes is prevented by aminoguanidine. Endocrinology. 143:2002;4907-4915.
177. Candido R., Forbes J.M., Thomas M.C., Thallas V., Dean R.G., Burns W.C., et al. A breaker of advanced glycation end products attenuates diabetes-induced myocardial structural changes. Circ Res. 92:2003;785-792.
178. Forbes J.M., Cooper M.E., Oldfield M.D., Thomas M.C. Role of advanced glycation end products in diabetic nephropathy. J Am Soc Nephrol. 14:2003;S254-S258.
179. Chen Y., Blom I.E., Sa S., Goldschmeding R., Abraham D.J., Leask A. CTGF expression in mesangial cells: involvement of SMADs, MAP kinase, and PKC. Kidney Int. 62:2002;1149-1159.
180. Suzuma K., Naruse K., Suzuma I., Takahara N., Ueki K., Aiello L.P., et al. Vascular endothelial growth factor induces expression of connective tissue growth factor via KDR, Flt1, and phosphatidylinositol 3-kinase-akt-dependent pathways in retinal vascular cells. J Biol Chem. 275:2000;40725-40731.
181. Abdel-Wahab N., Weston B.S., Roberts T., Mason R.M. Connective tissue growth factor and regulation of the mesangial cell cycle: role in cellular hypertrophy. J Am Soc Nephrol. 13:2002;2437-2445.
182. Feener E.P. The renin-angiotensin system in diabetic cardiovascular complications. Johnston M.T., Veves A. Diabetes and cardiovascular disease. 2001;103-121 Humana Press, Inc, Totowa (NJ).
183. Ardaillou R. Angiotensin II receptors. J Am Soc Nephrol. 10:(Suppl 11):1999;S30-S39.
184. Kagami S., Border W.A., Miller D.E., Noble N.A. Angiotensin II stimulates extracellular matrix protein synthesis through induction of transforming growth factor-beta expression in rat glomerular mesangial cells. J Clin Invest. 93:1994;2431-2437.
185. Chen H.C., Bouchie J.L., Perez A.S., Clermont A.C., Izumo S., Hampe J., et al. Role of the angiotensin AT(1) receptor in rat aortic and cardiac PAI-1 gene expression. Arterioscler Thromb Vasc Biol. 20:2000;2297-2302.
186. Pupilli C., Lasagni L., Romagnani P., Bellini F., Mannelli M., Misciglia N., et al. 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.
187. Hogeboom van Buggenum I.M., Polak B.C., Reichert-Thoen J.W., de Vries-Knoppert W.A., van Hinsbergh V.W., Tangelder G.J. Angiotensin converting enzyme inhibiting therapy is associated with lower vitreous vascular endothelial growth factor concentrations in patients with proliferative diabetic retinopathy. Diabetologia. 45:2002;203-209.
188. Chaturvedi N., Sjolie A.K., Stephenson J.M., Abrahamian H., Keipes M., Castellarin A., 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. 351:1998;28-31.
189. Lewis E.J., Hunsicker L.G., Bain R.P., Rohde R.D. The effect of angiotensin-converting-enzyme inhibition on diabetic nephropathy. The Collaborative Study Group. N Engl J Med. 329:1993;1456-1462.
190. Laffel L.M., McGill J.B., Gans D.J. The beneficial effect of angiotensin-converting enzyme inhibition with captopril on diabetic nephropathy in normotensive IDDM patients with microalbuminuria. North American Microalbuminuria Study Group. Am J Med. 99:1995;497-504.
191. The Microalbuminuria Study Group. Captopril reduces the risk of nephropathy in IDDM patients with microalbuminuria. The Microalbuminuria Captopril Study Group. Diabetologia. 39:1996;587-593.
192. The EUCLID Study Group. Randomised placebo-controlled trial of lisinopril in normotensive patients with insulin-dependent diabetes and normoalbuminuria or microalbuminuria. Lancet. 349:1997;1787-1792.
193. Ravid M., Brosh D., Levi Z., Bar-Dayan Y., Ravid D., Rachmani R. Use of enalapril to attenuate decline in renal function in normotensive, normoalbuminuric patients with type 2 diabetes mellitus. A randomized, controlled trial. Ann Intern Med. 128:1998;982-988.
194. Mathiesen E.R., Hommel E., Hansen H.P., Smidt U.M., Parving H.H. Randomised controlled trial of long term efficacy of captopril on preservation of kidney function in normotensive patients with insulin dependent diabetes and microalbuminuria. BMJ. 319:1999;24-25.
195. Heart Outcome Prevention Evaluation Study Investigators. Effects of ramipril on cardiovascular and microvascular outcomes in people with diabetes mellitus: results of the HOPE study and MICRO-HOPE substudy. Lancet. 355:2000;253-259.
196. Malik R.A., Williamson S., Abbott C., Carrington A.L., Iqbal J., Schady W., et al. Effect of angiotensin-converting-enzyme (ACE) inhibitor trandolapril on human diabetic neuropathy: randomised double-blind controlled trial. Lancet. 352:1998;1978-1981.
197. The UKPD Study Group. Tight blood pressure control and risk of macrovascular and microvascular complications in type 2 diabetes: UKPDS 38. UK Prospective Diabetes Study Group. BMJ. 317:1998;703-713.