Radicals and oxidative stress in diabetes

Diabetic Medicine

Volumn 17, Issue 3, 2000, Pages 171-180

  West, Ian C ^a,b  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Ascorbic acid; Diabetes mellitus; Glutathione; Lipoate; Oxidative stress; Reactive oxygen species; Vitamin E

Indexed keywords

ALPHA TOCOPHEROL; ANTIOXIDANT; ASCORBIC ACID; GLUTATHIONE; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; THIOCTIC ACID;

DIABETES MELLITUS; DNA DAMAGE; GENETIC POLYMORPHISM; HUMAN; HYPERGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; REVIEW;

DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; FREE RADICALS; HUMANS; HYPERGLYCEMIA; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 0033994409     PISSN: 07423071     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1464-5491.2000.00259.x     Document Type: Review

References (103)

1. 1 Halliwell B, Gutteridge JMC. Free Radicals in Biology and Medicine, 2nd edn. Oxford: Oxford University Press, 1989.
2. 2 Baynes JW. Role of oxidative stress in development of complications in diabetes. Diabetes 1991; 40: 405-412.
3. 3 Grankvist K, Marklund S, Taljedal IB. Superoxide dismutase is a prophylactic against alloxan diabetes. Nature 1981; 294: 158-60.
4. 4 Asplund K, Grankvist K, Marklund S, Taljedal IB. Partial protection against streptozotocin-induced hyperglycaemia by superoxide dismutase linked to polyethylene glycol. Acta Endocrinol (Copenh) 1984; 107: 390-394.
5. 5 Kubisch HM, Wang J, Bray TM, Phillips JP. Targeted overexpression of Cu/Zn superoxide dismutase protects pancreatic beta-cells against oxidative stress. Diabetes 1997; 46: 1563-1566.
6. 6 Winter WE. Type 2 diabetes mellitus: the challenge of a metabolic epidemic. J Clin Ligand Assay 1998; 21: 293-308.
7. 7 Giugliano D, Ceriello A, Paolisso G. Oxidative stress and diabetic vascular complications. Diabetes Care 1996; 19: 257-267.
8. 8 Baynes JW, Thorpe SR. Role of oxidative stress in diabetic complications: a new perspective on an old paradigm. Diabetes 1999; 48: 1-9.
9. 9 Akkus I, Kalak S, Vural H, Caglayan O, Menekse E, Can G et al. Leukocyte lipid peroxidation, superoxide dismutase, glutathione peroxidase and serum and leukocyte vitamin C levels of patients with type II diabetes mellitus. Clin Chim Acta 1996; 244: 221-227.
10. 10 Laaksonen DE, Atalay M, Niskanen L, Uusitupa M, Hanninen O, Sen CK. Increased resting and exercise-induced oxidative stress in young IDDM men. Diabetes Care 1996; 19: 569-574.
11. 11 Skrha J, Hodinar A, Kvasnicka J, Hilgertova J. Relationship of oxidative stress and fibrinolysis in diabetes mellitus. Diabet Med 1996; 13: 800-805.
12. 12 Santini SA, Marra G, Giardina B, Cotroneo P, Mordente A, Martorana GE et al. Defective plasma antioxidant defenses and enhanced susceptibility to lipid peroxidation in uncomplicated IDDM. Diabetes 1997; 46: 1853-1858.
13. 13 Gopaul NK, Anggard EE, Mallet AI, Betteridge DJ, Wolff SP, Nourooz-Zadeh J. Plasma 8-epi-PGF2 alpha levels are elevated in individuals with non-insulin dependent diabetes mellitus. FEBS Lett 1995; 368: 225-229.
14. 14 Nourooz-Zadeh J, Rahimi A, Tajaddini-Sarmadi J, Tritschler H, Rosen P, Halliwell B et al. Relationships between plasma measures of oxidative stress and metabolic control in NIDDM. Diabetologia 1997; 40: 647-653.
15. 15 Oranje WA, Rondas-Colbers GJ, Swennen GN, Wolffenbuttel BH. Lipid peroxidation in type 2 diabetes: relationship with macrovascular disease? Neth J Med 1998; 53: 61-68.
16. 16 Leinonen J, Lehtimaki T, Toyokuni S, Okada K, Tanaka T, Hiai H et al. New biomarker evidence of oxidative DNA damage in patients with non-insulin-dependent diabetes mellitus. FEBS Lett 1997; 417: 150-152.
17. 17 Ahmed MU, Brinkmann FE, Degenhardt TP, Thorpe SR, Baynes JW. N-epsilon-(carboxyethyl) lysine, a product of the chemical modification of proteins by methylglyoxal, increases with age in human lens proteins. Biochem J 1997; 324: 565-570.
18. 18 Dean RT, Fu S, Stocker R, Davies MJ. Biochemistry and pathology of radical-mediated protein oxidation. Biochem J 1997; 324: 1-18.
19. 19 Altomare E, Grattagliano I, Vendemaile G, Micelli-Ferrari T, Signorile A, Cardia L. Oxidative protein damage in human diabetic-eye: evidence of a retinal participation. Eur J Clin Invest 1997; 27: 141-147.
20. 20 Schleicher ED, Wagner E., Nerlich AG. Increased accumulation of the glycoxidation product N (epsilon)-(carboxymerhyl) lysine in human tissues in diabetes and aging. J Clin Invest 1997; 99: 457-468.
21. 21 Wells-Knecht MC, Lyons TJ, McCance DR, Thorpe SR, Baynes JW. Age-dependent increase in ortho-tyrosine and methionine sulfoxide in human skin collagen is not accelerated in diabetes. Evidence against a generalized increase in oxidative stress in diabetes. J Clin Invest 1997; 100: 839-846.
22. 22 Atalay M, Laaksonen DE, Niskanen L, Uusitupa M, Hanninen O, Sen CK. Altered antioxidant enzyme defences in insulin-dependent diabetic men with increased resting and exercise-induced oxidative stress. Acta Physiol Scand 1997; 161: 195-201.
23. 23 Ceriello A, Bortolotti N, Falleti E, Taboga C, Tonutti L, Crescentini A et al. Total radical-trapping antioxidant parameter in NIDDM patients. Diabetes Care 1997; 20: 194-197.
24. 24 Vucic M, Gavella M, Bozikov V, Ashcroft SJ, Rocic B. Superoxide dismutase activity in lymphocytes and polymorphonuclear cells of diabetic patients. Eur J Clin Chem Clin Biochem 1997; 35: 517-521.
25. 25 Gale EA. Molecular mechanisms of beta-cell destruction in IDDM. The role of nicotinamide. Horm Res 1996; 45: 39-43.
26. 26 Holecek V, Racek J, Jerabek Z. Administration of multivitamin combinations and trace elements in diabetes [Czech], Cas Lek Cesk 1995; 134: 80-83.
27. 27 Mayer-Davis EJ, Bell RA, Reboussin BA, Rushing J, Marshall JA, Hamman RF. Antioxidant nutrient intake and diabetic retinopathy: the San Luis Valley Diabetes Study. Ophthalmology 1998; 105: 2264-2270.
28. 28 Hunt JV. Ascorbic acid and diabetes mellitus. Subcell Biochem 1996; 25: 369-405.
29. 29 Young IS, Tate S, Lightbody JH, McMaster D, Trimble ER. The effects of desferrioxamine and ascorbate on oxidative stress in the streptozorocin diabetic rat. Free Radic Biol Med 1995; 18: 833-840.
30. 30 Gazis A, White DJ, Page SR, Cockcroft JR. Effect of oral vitamin E (alpha-tocopherol) supplementation on vascular endothelial function in Type 2 diabetes mellitus. Diabet Med 1999; 16: 304-311.
31. 31 Keegan A, Cotter MA, Cameron NE. Effects of diabetes and treatment with the antioxidant alpha-lipoic acid on endothelial and neurogenic responses of corpus cavernosum in rats. Diabetologia 1999; 42: 343-350.
32. 32 Cameron NE, Cotter MA, Horrobin DH, Tritschler HJ. Effects of alpha-lipoic acid on neurovascular function in diabetic rats: interaction with essential fatty acids. Diabetologia 1998; 41: 390-399.
33. 33 Ziegler D, Gries FA. Alpha-lipoic acid in the treatment of diabetic peripheral and cardiac autonomic neuropathy. Diabetes 1997; 46: S62-S66.
34. 34 Kowluru RA, Kern TS, Engerman RL, Abnormalities of retinal metabolism in diabetes or experimental galactosemia. IV. Antioxidant defense system. Free Radic Biol Med 1997; 22: 587-592.
35. 35 Saito H. Biochemical changes in lens, aqueous humor and vitreous body and effects of aldolase reductase inhibitor (TAT) on rats with experimental diabetes [Japanese]. Nippon Ika Daigaku Zasshi 1995; 62: 339-50.
36. 36 Spycher SE, Tabataba-Vakili S, O'Donnell VB, Palomba L, Azzi A. Aldose reductase induction: a novel response to oxidative stress of smooth muscle cells. FASEB J 1997; 11: 181-188.
37. 37 Reddi AS, Bollineni JS. Renal cortical expression of mRNAs for antioxidant enzymes in normal and diabetic rats. Biochem Biophys Res Commun 1997; 235: 598-601.
38. 38 Ceriello A, dello Russo P, Amstad P, Cerutti P. High glucose induces antioxidant enzymes in human endothelial cells in culture. Evidence linking hyperglycemia and oxidative stress. Diabetes 1996; 45: 471-477.
39. 39 Blakytny R, Harding JJ. Glycation (non-enzymic glycosylation) inactivates glutathione reductase. Biochem J 1992; 288: 303-307.
40. 40 Stahlberg MR, Hietanen E. Glutathione and glutathione-metabolizing enzymes in the erythrocytes of healthy children and in children with insulin-dependent diabetes mellitus, juvenile rheumatoid arthritis, coeliac disease and acute lymphoblastic leukaemia. Scand J Clin Lab Invest 1991; 51: 125-130.
41. 41 Murakami K, Kondo T, Ohtsuka Y, Fujiwara Y, Shimada M, Kawakami Y. Impairment of glutathione metabolism in erythrocytes from patients with diabetes mellitus. Metabolism 1989; 38: 753-758.
42. 42 Yoshida K, Hirokawa J, Tagami S, Kawakami Y, Urata Y, Kondo T. Weakened cellular scavenging activity against oxidative stress in diabetes mellitus: regulation of glutathione synthesis and efflux. Diabetologia 1995; 38: 201-210.
43. 43 Burton K. Free energy data of biological Interest. Ergebn Physiol 1957; 49: 275-285.
44. 44 Elgawish A, Glomb M, Friedlander M, Monnier VM. Involvement of hydrogen peroxide in collagen cross-linking by high glucose in vitro and in vivo. J Biol Chem 1996; 271: 12964-12971.
45. 45 Khechai F, Ollivier V, Bridey F, Amar M, Hakim J, de Prost D. Effect of advanced glycation end product-modified albumin on tissue factor expression by monocytes. Role of oxidant stress and protein tyrosine kinase activation. Arterioscler Thromb Biol 1997; 17: 2885-2890.
46. 46 Lindsay RM, Smith W, Lee WK, Dominiczak MH, Baird JD. The effect of delta-gluconolactone, an oxidised analogue of glucose, on the nonenzymatic glycation of human and rat haemoglobin. Clin Chim Acta 1997; 263: 239-247.
47. 47 Schmidt AM, Weidman E, Lalla E, Yan SD, Hori O, Cao R et al. Advanced glycation endproducts (AGEs) induce oxidant stress in the gingiva: a potential mechanism underlying accelerated periodontal disease associated with diabetes. J Periodontal Res 1996; 31: 508-515.
48. 48 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 1997; 46: 895-899.
49. 49 Christopher MM, Broussard JD, Peterson ME. Heinz body formation associated with ketoacidosis in diabetic cats. J Vet Intern Med 1995; 9: 24-31.
50. 50 Stamler JS, Singel DJ, Loscalzo J. Biochemistry of nitric oxide and its redox-activated forms. Science 1992; 258: 1898-1902.
51. 51 Giugliano D, Ceriello A, Paolisso G. Diabetes mellitus, hypertension, and cardiovascular disease: which role for oxidative stress? Metabolism 1995; 44: 363-368.
52. 52 Mallozzi C, Di Stasi AM, Minetti M. Peroxynitrite modulates tyrosine-dependent signal transduction pathway of human erythrocyte band 3. FASEB J 1997; 11: 1281-1290.
53. 53 Ceriello A, Motz E, Cavarape A, Lizzio S, Russo A, Quatraro A et al. Hyperglycemia counterbalances the antihypertensive effect of glutathione in diabetic patients: evidence linking hypertension and glycemia through the oxidative stress in diabetes mellitus. J Diabetes Complic 1997; 11: 250-255.
54. 54 Romero-Alvira D, Roche E. High blood pressure, oxygen radicals and antioxidants: etiological relationships. Med Hypotheses 1996; 46: 414-420.
55. 55 Rattan V, Shen Y, Sultana C, Kumar D, Kalra VK. Diabetic RBC-induced oxidant stress leads to transendothelial migration of monocyte-like HL-60 cells. Am J Physiol 1997; 273 (2 Part 1): F369-F375.
56. 56 Zoukourian C, Wautier MP, Chappey O, Dosquet C, Rohban T, Schmidt AM et al. Endothelial cell dysfunction secondary to the adhesion of diabetic erythrocytes. Modulation by iloprost. Int Angiol 1996; 15: 195-200.
57. 57 Hori O, Yan SD, Ogawa S, Kuwabra K, Matsumoto M, Stern D et al. The receptor for advanced glycation end-products has a central role in mediating the effects of advanced glycation end-products on the development of vascular disease in diabetes mellitus. Nephrol Dial Transplant 1996; 11 (Suppl. 6): 13-26.
58. 58 Wolffenbuttel BH, Graal MB. New treatments for patients with type 2 diabetes mellitus. Postgrad Med J 1996; 72: 657-662.
59. 59 Wolffenbuttel BH, van Haeften TW. Prevention of complications in non-insulin-dependent diabetes mellitus (NIDDM). Drugs 1995; 50: 263-288.
60. 60 Salonen JT, Tuomainen TP, Nyyssonen K, Lakka HM, Punnonen K. Relation between iron stores and non-insulin dependent diabetes in men: case-control study. Br Med J 1998; 317: 727.
61. 61 Verge CF, Gianani R, Yu L, Pietropaola M, Smith T, Jackson RA et al. Late progression to diabetes and evidence for chronic beta-cell autoimmunity in identical twins of patients with type 1 diabetes. Diabetes 1995; 44: 1176-1179.
62. 62 Green A. The role of genetic factors in the development of insulin-dependent diabetes mellitus. Curr Top Microbiol Immunol 1990; 164: 3-16.
63. 63 Todd JA. The role of MHC class II genes in susceptibility to insulin-dependent diabetes mellitus. Curr Top Microbiol Immunol 1990; 164: 17-40.
64. 64 Petersen JS, Kyvik KO, Bingley PJ, Gale EA, Green A, Dyrberg T et al. Population based study of prevalence of islet cell autoantibodies in monozygotic and dizygotic Danish twin pairs with insulin dependent diabetes mellitus. Br Med J 1997; 314: 1575-1579.
65. 65 Hawa M, Rowe R, Lan MS, Notkins AL, Pozzilli P, Christie MR et al. Value of antibodies to islet protein tyrosine phosphatase-like molecule in predicting type 1 diabetes. Diabetes 1997; 48: 1270-1275.
66. 66 Karges W, Hammond-McKibben D, Cheung RK, Visconti M, Shibuya N, Kemp D et al. Immunological aspects of nutritional diabetes prevention in NOD mice: a pilot study for the cow's milk-based IDDM prevention trial. Diabetes 1997; 46: 557-564.
67. 67 Yoon JW. The role of viruses and environmental factors in the induction of diabetes. Curr Top Microbiol Immunol 1990; 164: 95-123.
68. 68 Welsh N, Margulis B, Borg LA, Wiklund HJ, Saldeen J, Flodstrom et al. Differences in the expression of heat-shock proteins and antioxidant enzymes between human and rodent pancreatic islets: implications for the pathogenesis of insulin-dependent diabetes mellitus. Mol Med 1995; 1: 806-220.
69. 69 Wilson GL, Leiter EH. Streptozotocin interactions with pancreatic beta cells and the induction of insulin-dependent diabetes. Curr Top Microbiol Immunol 1990; 156: 27-54.
70. 70 Degli Esposti M, Ngo A, Myers MA. Inhibition of mitochondrial complex I may account for IDDM induced by intoxication with the rodenticide Vacor. Diabetes 1996; 45: 1531-1534.
71. 71 Turrens JF, Alexandre A, Lehninger AL. Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch Biochem Biophysics 1985; 237: 408-414.
72. 72 Boveris A, Cadenas E, Stoppani AO. Role of ubiquinone in the mitochondrial generation of hydrogen peroxide. Biochem J 1976; 156: 435-444.
73. 73 Seaton TA, Cooper JM, Schapira AH. Free radical scavengers protect dopaminergic cell lines from apoptosis induced by complex I inhibitors. Brain Res 1997; 777: 110-118.
74. 74 Herrero A, Barja G. Sites and mechanisms responsible for the low rate of free radical production of heart mitochondria in the long-lived pigeon. Mech Ageing Dev 1997; 98: 95-111.
75. 75 Schon EA, Bonilla E, DiMauro S, Mitochondrial DNA mutations and pathogenesis. J Bioenerg Biomembr 1997; 29: 131-149.
76. 76 Like AA, Rossini AA. Streptozotocin-induced pancreatic insulitis: new model of diabetes mellitus. Science 1976; 193: 415-417.
77. 77 Yamamoto H, Uchigata Y, Okamoto H. Streptozotocin and alloxan induce DNA strand breaks and poly (ADP-ribose) synthetase in pancreatic islets. Nature 1981; 294: 284-286.
78. 78 LeDoux SP, Hall CR, Forbes PM, Patton NJ, Wilson GL. Mechanisms of nicotinamide and thymidine protection from alloxan and streptozocin toxicity. Diabetes 1988; 37: 1015-1019.
79. 2 as mediator for DNA fragmentation. Diabetes 1991; 40: 1141-1145.
80. 80 Bedoya FJ, Solano F, Lucas M. N-monomethyl-arginine and nicotinamide prevent streptozotocin-induced double strand DNA break formation in pancreatic rat islets. Experientia 1996; 52: 344-347.
81. 81 Hanafusa T, Tarui S. Immune pathogenesis of diabetes in the nonobese diabetic mouse: an overview. Curr Top Microbiol Immunol 1990; 156: 15-25.
82. 82 Greenbaum CJ, Kahn SE, Palmer JP. Nicotinamide's effects on glucose metabolism in subjects at risk for IDDM. Diabetes 1996; 45: 1631-1634.
83. 83 Enghofer M, Usadel KH, Beck O, Kusterer K. Superoxide dismutase reduces islet microvascular injury induced by Streptozotocin in the rat. Am J Physiol 1997; 273: E376-E382.
84. 84 Bellmann K, Hui L, Radons J, Burkart V, Kolb H. Low stress response enhances vulnerability of islet cells in diabetes-prone BB rats. Diabetes 1997; 46: 232-236.
85. 85 Elbein SC. The genetics of human noninsulin-dependent (type 2) diabetes mellitus. J Nutr 1997; 127: 1891S-1896S.
86. 86 Beck-Nielsen H, Henriksen JE, Vaag A, Hother-Nielsen O. Pathophysiology of non-insulin-dependent diabetes mellitus (NIDDM). Diabetes Res Clin Pract 1995; 28: S13-S25.
87. 87 Reaven GM. Pathophysiology of insulin resistance in human disease. Physiol Rev 1995; 75: 473-486.
88. 88 Davis TM, Pramukkul P, Suputtamongkol Y, Chaowagul W, Levy J. Glucose tolerance in rural diabetic Thais, first-degree relatives and non-diabetic controls. Diabetes Res Clin Pract 1995; 27: 171-180.
89. 89 Pimenta W, Korytkowski M, Mitrakou A et al. Pancreatic beta-cell dysfunction as the primary genetic lesion in NIDDM. Evidence from studies in normal glucose-tolerant individuals with a first-degree NIDDM relative. J Am Med A 1995; 273: 1855-1561.
90. 90 Velho G, Byrne MM, Clement K et al. Clinical phenotypes, insulin secretion, and insulin sensitivity in kindreds with maternally inherited diabetes and deafness due to mitochondrial tRNALeu (UUR) gene mutation. Diabetes 1996; 45: 478-487.
91. 91 Swinburn BA, Gianchandani R, Saad MF, Lillioja S. In vivo beta-cell function at the transition to early non-insulin-dependent diabetes mellitus. Metabolism 1995; 44: 757-764.
92. 92 Luo J, Quan J, Tsai J, Hobensack CK, Sullivan C, Hector R et al. Nongenetic mouse models of non-insulin-dependent diabetes mellitus. Metabolism 1998; 47: 663-668.
93. 93 Richards DM, Dean RT, Jessup W. Membrane proteins are critical targets in free radical mediated cytolysis. Biochimica Biophysica Acta 1988; 946: 281-288.
94. 94 Augustyniak K, Zavodnik I, Palecz D, Szosland K, Bryszewska M. The effect of oxidizing agents and diabetes mellitus on the human red blood cell membrane potential. Clin Biochem 1996; 29: 283-286.
95. 95 Yasutake M, Ibuki C, Hearse DJ, Avkiran M. Na+/H+ exchange and reperfusion arrhythmias: protection by intracoronary infusion of a novel inhibitor. Am J Physiol 1994; 267: H2430-H2440.
96. 96 Coetzee WA, Ichikawa H, Hearse DJ. Oxidant stress inhibits NaCa-exchange current in cardiac myocytes: mediation by sulfhydryl groups? Am J Physiol 1994; 266: H909-H919.
97. 97 Jones SC, Thomas TH, Marshall SC. Thiol group modulation of sodium-lithium countertransport kinetics in diabetic nephropathy. Diabetologia 1997; 40: 1079-1084.
98. 98 Wang Z, Gleichmann H. GLUT2 in pancreatic islets. Crucial target molecule in diabetes induced with multiple low doses of streptozotocin in mice. Diabetes 1998; 47: 50-56.
99. 99 Heesom AE, Millward A, Demaine AG. Susceptibility to diabetic neuropathy in patients with insulin dependent diabetes mellitus is associated with a polymorphism at the 5′ end of the aldose reductase gene. J Neurol Neurosurg Psychiatry 1998; 64: 213-216.
100. 100 Heesom AE, Hibberd ML, Millward A, Demaine AG. Polymorphism in the 5′-end of the aldose reductase gene is strongly associated with the development of diabetic nephropathy in type 1 diabetes. Diabetes 1997; 46: 287-291.
101. 101 Shah VO, Scavini M, Nikolic J et al. Z-2 microsatellite allele is linked to increased expression of the aldose reductase gene in diabetic nephropathy. J Clin Endocrinol Metab 1998; 83: 2886-2891.
102. 102 Shah VO, Dorin RI, Sun Y, Braun M, Zager PG. Aldose reductase gene expression is increased in diabetic nephropathy. J Clin Endocrinol Metab 1997; 82: 2294-2298.
103. 103 Loebstein R, Lehotay DC, Luo X, Bartfay W, Tyler B, Sher GD. Diabetic nephropathy in hypertransfused patients with beta-thalassemia. The role of oxidative stress. Diabetes Care 1998; 21: 1306-1309.