Role of aldose reductase and oxidative damage in diabetes and the consequent potential for therapeutic options

Endocrine Reviews

Volumn 26, Issue 3, 2005, Pages 380-392

  Srivastava, Satish K ^a   Ramana, Kota V ^a   Bhatnagar, Aruni ^b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b University of Louisville School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; ALDEHYDE REDUCTASE; ALPHA TOCOPHEROL; ANTIOXIDANT; ASCORBIC ACID; BINDING PROTEIN; BUTYLATED HYDROXYANISOLE; BUTYLCRESOL; CYTOKINE; GLUCOSE; GROWTH FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN KINASE C; PYRUVIC ACID; SORBINIL; TOLRESTAT; TROLOX C;

ANTIOXIDANT ACTIVITY; APOPTOSIS; CARDIOVASCULAR DISEASE; CATALYSIS; CATARACT; CATARACTOGENESIS; CELL CULTURE; CELL GROWTH; CELL METABOLISM; DIABETES MELLITUS; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME INHIBITION; GLUCOSE METABOLISM; HEART INFARCTION PREVENTION; HUMAN; HYPERGLYCEMIA; LIPID PEROXIDATION; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; RESTENOSIS; RETINOPATHY; REVIEW; SIGNAL TRANSDUCTION; TISSUE INJURY; VASCULAR SMOOTH MUSCLE;

ALDEHYDE REDUCTASE; ANIMALS; CATARACT; DIABETES COMPLICATIONS; HUMANS; IMIDAZOLIDINES; MODELS, MOLECULAR; NAPHTHALENES; OXIDATION-REDUCTION; OXIDATIVE STRESS; SIGNAL TRANSDUCTION;

EID: 18844369302     PISSN: 0163769X     EISSN: None     Source Type: Journal    
DOI: 10.1210/er.2004-0028     Document Type: Review

References (142)

1. Hers HG 1956 The mechanism of the transformation of glucose in fructose in the seminal vesicles. Biochim Biophys Acta 22:202-203
2. van Heyningen R 1959 Formation of polyols by the lens of the rat with 'sugar' cataract. Nature 468:194-195
3. Kinoshita JH, Dvornik D, Kraml M, Gabbay KH 1968 The effect of an aldose reductase inhibitor on the galactose-exposed rabbit lens. Biochim Biophys Acta 158:472-475
4. Varma SD, Kinoshita JH 1976 Inhibition of lens aldose reductase by flavonoids - their possible role in the prevention of diabetic cataracts. Biochem Pharmacol 25:2505-2513
5. Varma SD, Mizuno A, Kinoshita JH 1977 Diabetic cataracts and flavonoids. Science 195:205-206
6. Kinoshita JH, Fukushi S, Kador P, Merola LO 1979 Aldose reductase in diabetic complications of the eye. Metabolism 28:462-469
7. Kinoshita JH, Kador P, Catiles M 1981 Aldose reductase in diabetic cataracts. JAMA 246:257-261
8. Kador PF, Robison Jr WG, Kinoshita JH 1985 The pharmacology of aldose reductase inhibitors. Annu Rev Pharmacol Toxicol 25:691-714
9. Dvornik D 1992 Aldose reductase inhibitors as pathobiochemical probes. J Diabetes Complications 6:25-34
10. Tsai SC, Burnakis TG 1993 Aldose reductase inhibitors: an update. Ann Pharmacother 27:751-754
11. Pfeifer MA, Schumer MP, Gelber DA 1997 Aldose reductase inhibitors: the end of an era or the need for different trial designs? Diabetes 46:S82-S89
12. Pitts NE, Gundersen K, Mehta DJ, Vreeland F, Shaw GL, Peterson MJ, Collier J 1986 Aldose reductase inhibitors in clinical practice. Preliminary studies on diabetic neuropathy and retinopathy. Drugs 32:30-35
13. Stribling D 1990 Clinical trials with aldose reductase inhibitors. Exp Eye Res 50:621-624
14. Hotta N, Kakuta H, Ando F, Sakamoto N 1990 Current progress in clinical trials of aldose reductase inhibitors in Japan. Exp Eye Res 50:625-628
15. Ranganathan S, Krempf M, Feraille E, Charbonnel B 1993 Short term effect of an aldose reductase inhibitor on urinary albumin excretion rate (UAER) and glomerular filtration rate (GFR) in type 1 diabetic patients with incipient nephropathy. Diabetes Metab 19:257-261
16. Passariello N, Sepe J, Marrazzo G, De Cicco A, Peluso A, Pisano MC, Sgambato S, Tesauro P, D'Onofrio F 1993 Effect of aldose reductase inhibitor (tolrestat) on urinary albumin excretion rate and glomerular filtration rate in IDDM subjects with nephropathy. Diabetes Care 16:789-795
17. Handelsman DJ, Turtle JR 1981 Clinical trial of an aldose reductase inhibitor in diabetic neuropathy. Diabetes 30:459-464
18. Jaspan J, Maselli R, Herold K, Bartkus C 1983 Treatment of severely painful diabetic neuropathy with an aldose reductase inhibitor: relief of pain and improved somatic and autonomic nerve function. Lancet 2:758-762
19. Jaspan JB, Towle VL, Maselli R, Herold K 1986 Clinical studies with an aldose reductase inhibitor in the autonomic and somatic neuropathies of diabetes. Metabolism 35:83-92
20. Srivastava SK, Petrash JM, Sadana IJ, Ansari NH, Partridge CA 1982 Susceptibility of aldehyde and aldose reductases of human tissues to aldose reductase inhibitors. Curr Eye Res 2:407-410
21. Srivastava SK, Ansari NH 1988 Prevention of sugar-induced cataractogenesis in rats by butylated hydroxytoluene. Diabetes 37:1505-1508
22. Ansari NH, Srivastava SK 1990 Allopurinol promotes and butylated hydroxy toluene prevents sugar-induced cataractogenesis. Biochem Biophys Res Commun 168:939-943
23. Ansari NH, Bhatnagar A, Fulep E, Khanna P, Srivastava SK 1994 Trolox protects hyperglycemia-induced cataractogenesis in cultured rat lens. Res Commun Chem Pathol Pharmacol 84:93-104
24. Bhatnagar A, Srivastava SK 1992 Aldose reductase: congenial and injurious profiles of an enigmatic enzyme. Biochem Med Metab Biol 48:91-121
25. Sheetz MJ, King GL 2002 Molecular understanding of hyperglycemia's adverse effects for diabetic complications. JAMA 288:2579-2588
26. Gonzalez RG, Barnett P, Aguayo J, Cheng HM, Chalack LT 1984 Direct measurement of polyol pathway activity in the ocular lens. Diabetes 33:196-199
27. Liu SQ, Bhatnagar A, Ansari NH, Srivastava SK Identification of the reactive cysteine residue in human placenta aldose reductase. Biochim Biophys Acta 1993 1164:268-272
28. Bhatnagar A, Liu SQ, Ueno N, Chakrabarti B, Srivastava SK 1994 Human placental aldose reductase: role of Cys-298 in substrate and inhibitor binding. Biochim Biophys Acta 1205:207-214
29. Srivastava SK, Hair GA, Das B 1985 Activated and unactivated forms of human erythrocyte aldose reductase. Proc Natl Acad Sci USA 82:7222-7226
30. Del Corso A, Barsacchi D, Camici M, Garland D, Mura U 1989 Bovine lens aldose reductase: identification of two enzyme forms. Arch Biochem Biophys 270:604-610
31. Grimshaw CE 1990 Chromatographic separation of activated and unactivated forms of aldose reductase. Arch Biochem Biophys 278:273-276
32. Lorenzi M, Toledo S, Boss GR, Lane MJ, Montisano DF 1987 The polyol pathway and glucose 6-phosphate in human endothelial cells cultured in high glucose concentrations. Diabetologia 30:222-227
33. Lee AY, Chung SK, Chung SS 1995 Demonstration that polyol accumulation is responsible for diabetic cataract by the use of transgenic mice expressing the aldose reductase gene in the lens. Proc Natl Acad Sci USA 92:2780-2784
34. Yagihashi S, Yamagishi S, Wada R, Sugimoto K, Baba M, Wong HG, Fujimoto J, Nishimura C, Kokai Y 1996 Galactosemic neuropathy in transgenic mice for human aldose reductase. Diabetes 45:56-59
35. Yagihashi S, Yamagishi SI, Wada Ri R, Baba M, Hohman TC, Yabe-Nishimura C, Kokai Y 2001 Neuropathy in diabetic mice overexpressing human aldose reductase and effects of aldose reductase inhibitor. Brain 124:2448-2458
36. Song Z, Fu DT, Chan YS, Leung S, Chung SS, Chung SK 2003 Transgenic mice overexpressing aldose reductase in Schwann cells show more severe nerve conduction velocity deficit and oxidative stress under hyperglycemic stress. Mol Cell Neurosci 23:638-647
37. Leto G, Pricci F, Amadio L, Iacobini C, Cordone S, Diaz-Horta O, Romeo G, Barsotti P, Rotella CM, di Mario U, Pugliese G 2001 Increased retinal endothelial cell monolayer permeability induced by the diabetic milieu: role of advanced non-enzymatic glycation and polyol pathway activation. Diabetes Metab Res Rev 17:448-458
38. Yan SF, Ramasamy R, Naka Y, Schmidt AM 2003 Glycation, inflammation, and RAGE: a scaffold for the macrovascular complications of diabetes and beyond. Circ Res 93:1159-1169
39. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, Brownlee M 2000 Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404:787-790
40. Williamson JR, Chang K, Frangos M, Hasan KS, Ido Y, Kawamura T, Nyengaard JR, van den Enden M, Kilo C, Tilton RG 1993 Hyperglycemic pseudohypoxia and diabetic complications. Diabetes 42:801-813
41. Ido Y, Williamson JR 1997 Hyperglycemic cytosolic reductive stress 'pseudohypoxia': implications for diabetic retinopathy. Invest Ophthalmol Vis Sci 38:1467-1470
42. Obrosova IG, Stevens MJ, Lang HJ 2001 Diabetes-induced changes in retinal NAD-redox status: pharmacological modulation and implications for pathogenesis of diabetic retinopathy. Pharmacology 62:172-180
43. Thomas TP, Porcellati F, Kato K, Stevens MJ, Sherman WR, Greene DA 1994 Effects of glucose on sorbitol pathway activation, cellular redox, and metabolism of myo-inositol, phosphoinositide, and diacylglycerol in cultured human retinal pigment epithelial cells. J Clin Invest 93:2718-2724
44. Derubertis FR, Craven PA 1994 Activation of protein kinase C in glomerular cells in diabetes. Mechanisms and potential links to the pathogenesis of diabetic glomerulopathy. Diabetes 43:1-8
45. Koya D, King GL Protein kinase C activation and the development of diabetic complications. Diabetes 47:859-866
46. Graier WF, Grubenthal I, Dittrich P, Wascher TC, Kostner GM 1995 Intracellular mechanism of high D-glucose-induced modulation of vascular cell proliferation. Eur J Pharmacol 294:221-229
47. Frank RN 2002 Potential new medical therapies for diabetic retinopathy: protein kinase C inhibitors. Am J Ophthalmol 133:693-698
48. Tuttle KR, Anderson PW 2003 A novel potential therapy for diabetic nephropathy and vascular complications: protein kinase C β inhibition. Am J Kidney Dis 42:456-465
49. Burg MB 1988 Role of aldose reductase and sorbitol in maintaining the medullary intracellular milieu. Kidney Int 33:635-641
50. Burg MB 1995 Molecular basis of osmotic regulation. Am J Physiol 268:F983-F996
51. Donohue PJ, Alberts GF, Hampton BS, Winkles JA 1994 A delayed-early gene activated by fibroblast growth factor-1 encodes a protein related to aldose reductase. J Biol Chem 269:8604-8609
52. Iwata T, Sato S, Jimenez J, McGowan M, Moroni M, Dey A, Ibaraki N, Reddy VN, Carper D 1999 Osmotic response element is required for the induction of aldose reductase by tumor necrosis factor-α. J Biol Chem 274:7993-8001
53. Ruef J, Liu SQ, Bode C, Tocchi M, Srivastava S, Runge MS, Bhatnagar A 2000 Involvement of aldose reductase in vascular smooth muscle cell growth and lesion formation after arterial injury. Arterioscler Thromb Vasc Biol 20:1745-1752
54. Spycher SE, Tabataba-Vakili S, O'Donnell VB, Palomba L, Azzi A 1997 Aldose reductase induction: a novel response to oxidative stress of smooth muscle cells. FASEB J 11:181-188
55. Tawata M, Ohtaka M, Hosaka Y, Onaya T 1992 Aldose reductase mRNA expression and its activity are induced by glucose in fetal rat aortic smooth muscle (A10) cells. Life Sci 51:719-726
56. Ramana KV, Chandra D, Srivastava S, Bhatnagar A, Srivastava SK 2003 Aldose reductase mediates the mitogenic signals of cytokines. Chem Biol Interact 143-144:587-596
57. Bhatnagar A, Ruef J, Liu S, Srivastava S, Srivastava SK 2001 Regulation of vascular smooth muscle cell growth by aldose reductase. Chem Biol Interact 130-132:627-636
58. Sibbitt Jr WL, Mills RG, Bigler CF, Eaton RP, Griffey RH, Vander Jagt DL 1989 Glucose inhibition of human fibroblast proliferation and response to growth factors is prevented by inhibitors of aldose reductase. Mech Ageing Dev 47:265-279
59. Derylo B, Babazono T, Glogowski E, Kapor-Drezgic J, Hohman T, Whiteside C 1998 High glucose-induced mesangial cell altered contractility: role of the polyol pathway. Diabetologia 41:507-515
60. Asnaghi V, Gerhardinger C, Hoehn T, Adeboje A, Lorenzi M 2003 A role for the polyol pathway in the early neuroretinal apoptosis and glial changes induced by diabetes in the rat. Diabetes 52:506-511
61. Price SA, Agthong S, Middlemas AB, Tomlinson DR 2004 Mitogen-activated protein kinase p38 mediates reduced nerve conduction velocity in experimental diabetic neuropathy: interactions with aldose reductase. Diabetes 53:1851-1856
62. Srivastava S, Watowich SJ, Petrash JM, Srivastava SK, Bhatnagar A 1999 Structural and kinetic determinants of aldehyde reduction by aldose reductase. Biochemistry 38:42-54
63. Srivastava S, Liu SQ, Conklin DJ, Zacarias A, Srivastava SK, Bhatnagar A 2001 Involvement of aldose reductase in the metabolism of atherogenic aldehydes. Chem Biol Interact 130-132:563-571
64. Srivastava S, Chandrasekar B, Bhatnagar A, Prabhu SD 2002 Lipid peroxidation-derived aldehydes and oxidative stress in the failing heart: role of aldose reductase. Am J Physiol Heart Circ Physiol 283:H2612-H2619
65. Ramana KV, Dixit BL, Srivastava S, Bhatnagar A, Balendiran GK, Watowich SJ, Petrash JM, Srivastava SK 2001 Characterization of the glutathione binding site of aldose reductase. Chem Biol Interact 130-132:537-548
66. Ramana KV, Dixit BL, Srivastava S, Balendiran GK, Srivastava SK, Bhatnagar A 2000 Selective recognition of glutathiolated aldehydes by aldose reductase. Biochemistry 39:12172-12180
67. Dixit BL, Balendiran GK, Watowich SJ, Srivastava S, Ramana KV, Petrash JM, Bhatnagar A, Srivastava SK 2000 Kinetic and structural characterization of the glutathione-binding site of aldose reductase. J Biol Chem 275:21587-21595
68. Srivastava S, Spite M, Trent JO, West MB, Ahmed Y, Bhatnagar A 2004 Aldose reductase-catalyzed reduction of aldehyde phospholipids. J Biol Chem 279:53395-53406
69. Bhatnagar A, Srivastava S, Wang LF, Chandra A, Ansari NH, Srivastava SK 1999 Cardiac metabolism of enals. Adv Exp Med Biol 463:223-229
70. Srivastava SK, Chandra A, Srivastava S, Petrash JM, Bhatnagar A 1999 Regulation of aldose reductase by aldehydes and nitric oxide. Adv Exp Med Biol 463:501-507
71. Nakano T, Petrash JM 1996 Kinetic and spectroscopic evidence for active site inhibition of human aldose reductase. Biochemistry 35:11196-11202
72. Schade SZ, Early SL, Williams TR, Kezdy FJ, Heinrikson RL, Grimshaw CE, Doughty CC 1990 Sequence analysis of bovine lens aldose reductase. J Biol Chem 265:3628-3635
73. Wilson DK, Bohren KM, Gabbay KH, Quiocho FA 1992 An unlikely sugar substrate site in the 1.65 A structure of the human aldose reductase holoenzyme implicated in diabetic complications. Science 257:81-84
74. Wilson DK, Tarle I, Petrash JM, Quiocho FA 1993 Refined 1.8 A structure of human aldose reductase complexed with the potent inhibitor zopolrestat. Proc Natl Acad Sci USA 90:9847-9851
75. Tarle I, Borhani DW, Wilson DK, Quiocho FA, Petrash JM 1993 Probing the active site of human aldose reductase. Site-directed mutagenesis of Asp-43, Tyr-48, Lys-77, and His-110. J Biol Chem 268:25687-25693
76. Petrash JM, Tarle I, Wilson DK, Quiocho FA 1994 Aldose reductase catalysis and crystallography. Insights from recent advances in enzyme structure and function. Diabetes 43:955-959
77. Borhani DW, Harter TM, Petrash JM 1992 The crystal structure of the aldose reductase. NADPH binary complex. J Biol Chem 267: 24841-24847
78. Srivastava S, Chandra A, Ansari NH, Srivastava SK, Bhatnagar A 1998 Identification of cardiac oxidoreductase(s) involved in the metabolism of the lipid peroxidation-derived aldehyde-4-hydroxynonenal. Biochem J 329:469-475
79. Srivastava S, Chandra A, Wang LF, Seifert Jr WE, DaGue BB, Ansari NH, Srivastava SK, Bhatnagar A 1998 Metabolism of the lipid peroxidation product, 4-hydroxy-trans-2-nonenal, in isolated perfused rat heart. J Biol Chem 273:10893-10900
80. Srivastava S, Dixit BL, Cai J, Sharma S, Hurst HE, Bhatnagar A, Srivastava SK 2000 Metabolism of lipid peroxidation product, 4-hydroxynonenal (HNE) in rat erythrocytes: role of aldose reductase. Free Radic Biol Med 29:642-651
81. Srivastava S, Conklin DJ, Liu SQ, Prakash N, Boor PJ, Srivastava SK, Bhatnagar A 2001 Identification of biochemical pathways for the metabolism of oxidized low-density lipoprotein derived aldehyde-4-hydroxy trans-2-nonenal in vascular smooth muscle cells. Atherosclerosis 158:339-350
82. Del Corso A, Dal Monte M, Vilardo PG, Cecconi I, Moschini R, Banditelli S, Cappiello M, Tsai L, Mura U 1998 Site-specific inactivation of aldose reductase by 4-hydroxynonenal. Arch Biochem Biophys 350:245-248
83. Cappiello M, Voltarelli M, Giannessi M, Cecconi I, Camici G, Manao G, Del Corso A, Mura U 1994 Glutathione dependent modification of bovine lens aldose reductase. Exp Eye Res 58:491-501
84. Cappiello M, Amodeo P, Mendez BL, Scaloni A, Vilardo PG, Cecconi I, Dal Monte M, Banditelli S, Talamo F, Micheli V, Giblin FJ, Corso AD, Mura U 2001 Modulation of aldose reductase activity through S-thiolation by physiological thiols. Chem Biol Interact 130-132:597-608
85. Cappiello M, Vilardo PG, Cecconi I, Leverenz V, Giblin FJ, Del Corso A, Mura U 1995 Occurrence of glutathione-modified aldose reductase in oxidatively stressed bovine lens. Biochem Biophys Res Commun 207:775-782
86. Cappiello M, Voltarelli M, Cecconi I, Vilardo PG, Dal Monte M, Marini I, Del Corso A, Wilson DK, Quiocho FA, Petrash JM, Mura U 1996 Specifically targeted modification of human aldose reductase by physiological disulfides. J Biol Chem 271:33539-33544
87. Del Corso A, Camici M, Mura U 1987 In vitro modification of bovine lens aldose reductase activity. Biochem Biophys Res Commun 148:369-375
88. Petrash JM, Harter TM, Devine CS, Olins PO, Bhatnagar A, Liu S, Srivastava SK 1992 Involvement of cysteine residues in catalysis and inhibition of human aldose reductase. Site-directed mutagenesis of Cys-80, -298, and -303. J Biol Chem 267:24833-24840
89. Cecconi I, Scaloni A, Rastelli G, Moroni M, Vilardo PG, Costantino L, Cappiello M, Garland D, Carper D, Petrash JM, Del Corso A, Mura U 2002 Oxidative modification of aldose reductase induced by copper ion. Definition of the metal-protein interaction mechanism. J Biol Chem 277:42017-42027
90. Halder AB, James M, Crabbe C 1985 Chemical modification studies on purified bovine lens aldose reductase. Ophthalmic Res 17:185-188
91. Cecconi I, Moroni M, Vilardo PG, Dal Monte M, Borella P, Rastelli G, Costantino L, Garland D, Carper D, Petrash JM, Del Corso A, Mura U 1998 Oxidative modification of aldose reductase induced by copper ion. Factors and conditions affecting the process. Biochemistry 37:14167-14174
92. Chandra A, Srivastava S, Petrash JM, Bhatnagar A, Srivastava SK 1997 Active site modification of aldose reductase by nitric oxide donors. Biochim Biophys Acta 1341:217-222
93. Dixit BL, Ramana KV, Chandra D, Jackson EB, Srivastava S, Bhatnagar A, Srivastava SK 2001 Metabolic regulation of aldose reductase activity by nitric oxide donors. Chem Biol Interact 130-132:573-581
94. Srivastava S, Dixit BL, Ramana KV, Chandra A, Chandra D, Zacarias A, Petrash JM, Bhatnagar A, Srivastava SK 2001 Structural and kinetic modifications of aldose reductase by S-nitrosothiols. Biochem J 358:111-118
95. Chandra D, Jackson EB, Ramana KV, Kelley R, Srivastava SK, Bhatnagar A 2002 Nitric oxide prevents aldose reductase activation and sorbitol accumulation during diabetes. Diabetes 51:3095-3101
96. Srivastava SK, Ramana KV, Chandra D, Srivastava S, Bhatnagar A 2003 Regulation of aldose reductase and the polyol pathway activity by nitric oxide. Chem Biol Interact 143-144:333-340
97. Ramana KV, Chandra D, Srivastava S, Bhatnagar A, Srivastava SK 2003 Nitric oxide regulates the polyol pathway of glucose metabolism in vascular smooth muscle cells. FASEB J 17:417-425
98. Barisani D, Meneveri R, Ginelli E, Cassani C, Conte D 2000 Iron overload and gene expression in HepG2 cells: analysis by differential display. FEBS Lett 469:208-212
99. O'connor T, Ireland LS, Harrison DJ, Hayes JD 1999 Major differences exist in the function and tissue-specific expression of human aflatoxin B1 aldehyde reductase and the principal human aldo-keto reductase AKR1 family members. Biochem J 343:487-504
100. Srivastava S, Chandrasekar B, Bhatnagar A, Prabhu SD 2002 Lipid peroxidation-derived aldehydes and oxidative stress in the failing heart: role of aldose reductase. Am J Physiol 283:H2612-H2619
101. Ramana KV, Friedrich B, Srivastava S, Bhatnagar A, Srivastava SK 2004 Activation of nuclear factor-κB by hyperglycemia in vascular smooth muscle cells is regulated by aldose reductase. Diabetes 53:2910-2920
102. Rittner HL, Hafner V, Klimiuk PA, Szweda LI, Goronzy JJ, Weyand CM 1999 Aldose reductase functions as a detoxification system for lipid peroxidation products in vasculitis. J Clin Invest 103:1007-1013
103. Shinmura K, Bolli R, Liu SQ, Tang XL, Kodani E, Xuan YT, Srivastava S, Bhatnagar A 2002 Aldose reductase is an obligatory mediator of the late phase of ischemic preconditioning. Circ Res 91:240-246
104. Hwang YC, Sato S, Tsai JY, Yan S, Bakr S, Zhang H, Oates PJ, Ramasamy R 2002 Aldose reductase activation is a key component of myocardial response to ischemia. FASEB J 16:243-245
105. Ramasamy R, Oates PJ, Schaefer S 1997 Aldose reductase inhibition protects diabetic and nondiabetic rat hearts from ischemic injury. Diabetes 46:292-300
106. Kaneko M, Ramasamy R 2004 Aldose reductase: a key player in myocardial ischemic injury. Exerc Sport Sci Rev 32:19-23
107. Hwang YC, Kaneko M, Bakr S, Liao H, Lu Y, Lewis ER, Yan S, Ii S, Itakura M, Rui L, Skopicki H, Homma S, Schmidt AM, Oates PJ, Szabolcs M, Ramasamy R 2004 Central role for aldose reductase pathway in myocardial ischemic injury. FASEB J 18:1192-1199
108. Horvath JJ, Witmer CM, Witz G 1992 Nephrotoxicity of the 1:1 acrolein-glutathione adduct in the rat. Toxicol Appl Pharmacol 117:200-207
109. Chakrabarti S, Malick MA 1991 In vivo nephrotoxic action of an isomeric mixture of S-(1-phenyl-2-hydroxyethyl)glutathione and S-(2-phenyl-2- hydroxyethyl)glutathione in Fischer-344 rats. Toxicology 67:15-27
110. Boon PJ, Marinho HS, Oosting R, Mulder GJ 1999 Glutathione conjugation of 4-hydroxy-trans-2,3-nonenal in the rat in vivo, the isolated perfused liver and erythrocytes. Toxicol Appl Pharmacol 159:214-223
111. Kicic E, Palmer TN 1996 Increased white cell aldose reductase mRNA levels in diabetic patients. Diabetes Res Clin Pract 33:31-36
112. Shimizu H, Ohtani KI, Tsuchiya T, Sato N, Tanaka Y, Takahashi H, Uehara Y, Inukai T, Mori M 2000 Aldose reductase mRNA expression is associated with rapid development of diabetic microangiopathy in Japanese type 2 diabetic (T2DM) patients. Diabetes Nutr Metab 13:75-79
113. Spallarossa P, Barsotti A, Cordera R, Ghigliotti G, Maggi D, Brunelli C 2004 Reduction of cardiovascular morbidity and mortality in type 2 diabetes. A rational approach to hypoglycemic therapy. J Endocrinol Invest 27:485-495
114. Moncada S, Palmer RM, Higgs EA 1991 Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 43:109-142
115. Wu SY, Leske MC 2000 Antioxidants and cataract formation: a summary review. Int Ophthalmol Clin 40:71-81
116. Richer S 2000 Antioxidants and the eye. Int Ophthalmol Clin 40:1-16
117. Kowluru RA, Kennedy A 2001 Therapeutic potential of anti-oxidants and diabetic retinopathy. Expert Opin Investig Drugs 10:1665-1676
118. Dickinson PJ, Carrington AL, Frost GS, Boulton AJ 2002 Neurovascular disease, antioxidants and glycation in diabetes. Diabetes Metab Res Rev 18:260-272
119. Vaziri ND 2004 Roles of oxidative stress and antioxidant therapy in chronic kidney disease and hypertension. Curr Opin Nephrol Hypertens 13:93-99
120. Ruhe RC, McDonald RB 2001 Use of antioxidant nutrients in the prevention and treatment of type 2 diabetes. J Am Coll Nutr 20:363S-369S
121. Basta G, Schmidt AM, De Caterina R 2004 Advanced glycation end products and vascular inflammation: implications for accelerated atherosclerosis in diabetes. Cardiovasc Res 63:582-592
122. Dandona P, Chaudhuri A, Aljada A 2004 Endothelial dysfunction and hypertension in diabetes mellitus. Med Clin North Am 88:911-931
123. Wilson Tang WH, Maroo A, Young JB 2004 Ischemic heart disease and congestive heart failure in diabetic patients. Med Clin North Am 88:1037-1061
124. Lim HS, Lip 2003 GY Diabetes, the renin-angiotensin system and heart disease. Curr Vasc Pharmacol 1:225-238
125. Lim HS, MacFadyen RJ, Lip GY 2004 Diabetes mellitus, the reninangiotensin-aldosterone system, and the heart. Arch Intern Med 164:1737-1748
126. Morgan KP, Kapur A, Beatt KJ 2004 Anatomy of coronary disease in diabetic patients: an explanation for poorer outcomes after percutaneous coronary intervention and potential target for intervention. Heart 90:732-738
127. Indolfi C, Mongiardo A, Curcio A, Torella D 2003 Molecular mechanisms of in-stent restenosis and approach to therapy with eluting stents. Trends Cardiovasc Med 3:142-148
128. Ramana KV, Chandra D, Srivastava S, Bhatnagar A, Aggarwal BB, Srivastava SK 2002 Aldose reductase mediates mitogenic signaling in vascular smooth muscle cells. J Biol Chem 277:32063-32070
129. Zhou Z, Lauer MA, Wang K, Forudi F, Zhou X, Song X, Solowski N, Kapadia SR, Nakada MT, Topol EJ, Lincoff AM 2002 Effect of anti-tumor necrosis factor-α polyclonal antibody on restenosis after balloon angioplasty in a rabbit atherosclerotic model. Atherosclerosis 161:153-159
130. Catley MC, Cambridge LM, Nasuhara Y, Ito K, Chivers JE, Beaton A, Holden NS, Bergmann MW, Barnes PJ, Newton R 2004 Inhibitors of protein kinase C (PKC) prevent activated transcription: role of events downstream of NF-κB DNA binding. J Biol Chem 279:18457-18466
131. Foey AD, Brennan FM 2004 Conventional protein kinase C and atypical protein kinase Cζ differentially regulate macrophage production of tumor necrosis factor-α and interleukin-10. Immunology 112:44-53
132. Satoh A, Gukovskaya AS, Nieto JM, Cheng JH, Gukovsky I, Reeve Jr JR, Shimosegawa T, Pandol SJ 2004 PKC-δ and -ε regulate NF-κB activation induced by cholecystokinin and TNF-α in pancreatic acinar cells. Am J Physiol Gastrointest Liver Physiol 287:G582-G591
133. Ramana KV, Friedrich B, Bhatnagar A, Srivastava SK 2003 Aldose reductase mediates cytotoxic signals of hyperglycemia and TNF-α in human lens epithelial cells. FASEB J 17:315-317
134. Ramana KV, Bhatnagar A, Srivastava SK 2004 Inhibition of aldose reductase attenuates TNF-α-induced expression of adhesion molecules in endothelial cells. FASEB J 18:1209-1218
135. Chandra D, Ramana KV, Friedrich B, Srivastava S, Bhatnagar A, Srivastava SK 2003 Role of aldose reductase in TNF-α-induced apoptosis of vascular endothelial cells. Chem Biol Interact 143-144:605-612
136. Ramana KV, Bhatnagar A, Srivastava SK 2004 Aldose reductase regulates TNF-α-induced cell signaling and apoptosis in vascular endothelial cells. FEBS Lett 570:189-194
137. Srivastava S, Ramana KV, Srivastana SK, D'Souza SE, Bhatnagar A 2004 Role of aldose reductase in the detoxification of oxidized phospholipids. ACS Symposium Series 865:49-64
138. Vander Jagt DL, Hassebrook RK, Hunsaker LA, Brown WM, Royer RE 2001 Metabolism of the 2-oxoaldehyde methylglyoxal by aldose reductase and by glyoxalase-I: roles for glutathione in both enzymes and implications for diabetic complications. Chem Biol Interact 130-132:549-562
139. Wermuth B, Monder C 1983 Aldose and aldehyde reductase exhibit isocorticosteroid reductase activity. Eur J Biochem 131:423-426
140. Matsuura K, Deyashiki Y, Bunai Y, Ohya I, Hara A 1996 Aldose reductase is a major reductase for isocaproaldehyde, a product of side-chain cleavage of cholesterol, in human and animal adrenal glands. Arch Biochem Biophys 328:265-271
141. Petrash JM, Harter TM, Murdock GL 1996 A potential role for aldose reductase in steroid metabolism. In: Weiner H, Lindahl R, Crabb DW, Flynn TG, eds. Enzymology and molecular biology of carbonyl metabolism. Vol 6. New York: Plenum Press; 465-473
142. Srivastava S, Liu SQ, Bhatnagar A 2003 Cellular metabolism of base propanols. FASEB J 17:A175-A176