Molecular pathology of oxidative stress in diabetic angiopathy: Role of mitochondrial and cellular pathways

Diabetes Research and Clinical Practice

Volumn 87, Issue 3, 2010, Pages 313-321

  Mokini, Zhirajr ^a   Marcovecchio, M Loredana ^a   Chiarelli, Francesco ^a  

^a UNIVERSITY OF CHIETI   (Italy)

Author keywords

Angiopathy; Diabetes mellitus; Hyperglycaemia; Mitochondria; Oxidative stress

Indexed keywords

2 [[4 [2,6 BIS(1 PYRROLIDINYL) 4 PYRIMIDINYL] 1 PIPERAZINYL]METHYL] 3,4 DIHYDRO 2,5,7,8 TETRAMETHYL 2H 1 BENZOPYRAN 6 OL; ALPHA TOCOPHEROL; ASCORBIC ACID; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUTATHIONE; GLUTATHIONE REDUCTASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RETINOL; SUPEROXIDE DISMUTASE; THIOCTIC ACID; THIOREDOXIN REDUCTASE; TRANSCRIPTION FACTOR AP 1; UBIDECARENONE; UNCOUPLING PROTEIN 1; UNCOUPLING PROTEIN 2; UNCOUPLING PROTEIN 3;

ANTIOXIDANT ACTIVITY; APOPTOSIS; DIABETES MELLITUS; DIABETIC ANGIOPATHY; ENDOTHELIAL DYSFUNCTION; HUMAN; HYPERGLYCEMIA; INFLAMMATION; MITOCHONDRION; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PATHOGENESIS; PROTEIN DETERMINATION; PROTEIN FUNCTION; REVIEW; VASCULAR DISEASE;

DIABETIC ANGIOPATHIES; HUMANS; HYPERGLYCEMIA; ION CHANNELS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; OXIDATIVE STRESS;

EID: 77649189371     PISSN: 01688227     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.diabres.2009.11.018     Document Type: Review

References (68)

1. Mokini Z., and Chiarelli F. The molecular basis of diabetic microangiopathy. Pediatr. Endocrinol. Rev. 4 (2006) 138-152
2. Wild S., Roglic G., Green A., Sicree R., and King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27 (2004) 1047-1053
3. Zimmet P., Alberti K.G., and Shaw J. Global and societal implications of the diabetes epidemic. Nature 414 (2001) 782-787
4. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 414 (2001) 813-820
5. Giugliano D., Ceriello A., and Paolisso G. Oxidative stress and diabetic vascular complications. Diabetes Care 19 (1996) 257-267
6. Taniyama Y., and Griendling K.K. Reactive oxygen species in the vasculature: molecular and cellular mechanisms. Hypertension 42 (2003) 1075-1081
7. Johansen J.S., Harris A.K., Rychly D.J., and Ergul A. Oxidative stress and the use of antioxidants in diabetes: linking basic science to clinical practice. Cardiovasc. Diabetol. 4 (2005) 5
8. Vincent A.M., Russell J.W., Low P., and Feldman E.L. Oxidative stress in the pathogenesis of diabetic neuropathy. Endocr. Rev. 25 (2004) 612-628
9. Evans J.L., Goldfine I.D., Maddux B.A., and Grodsky G.M. Are oxidative stress-activated signaling pathways mediators of insulin resistance and beta-cell dysfunction?. Diabetes 52 (2003) 1-8
10. Ceriello A. Oxidative stress and glycemic regulation. Metabolism 49 (2000) 27-29
11. Mezzetti A., Cipollone F., and Cuccurullo F. Oxidative stress and cardiovascular complications in diabetes: isoprostanes as new markers on an old paradigm. Cardiovasc. Res. 47 (2000) 475-488
12. Son S.M. Role of vascular reactive oxygen species in development of vascular abnormalities in diabetes. Diabetes Res. Clin. Pract. 77 Suppl. 1 (2007) S65-70
13. Griendling K.K., and FitzGerald G.A. Oxidative stress and cardiovascular injury. Part I. Basic mechanisms and in vivo monitoring of ROS. Circulation 108 (2003) 1912-1916
14. De Vriese A.S., Verbeuren T.J., Van de Voorde J., Lameire N.H., and Vanhoutte P.M. Endothelial dysfunction in diabetes. Br. J. Pharmacol. 130 (2000) 963-974
15. Jay D., Hitomi H., and Griendling K.K. Oxidative stress and diabetic cardiovascular complications. Free Radic. Biol. Med. 40 (2006) 183-192
16. Balestrieri M.L., Rienzo M., Felice F., Rossiello R., Grimaldi V., Milone L., et al. High glucose downregulates endothelial progenitor cell number via SIRT1. Biochim. Biophys. Acta 1784 (2008) 936-945
17. Singh D.K., Winocour P., and Farrington K. Mechanisms of disease: the hypoxic tubular hypothesis of diabetic nephropathy. Nat. Clin. Pract. Nephrol. 4 (2008) 216-226
18. Kiritoshi S., Nishikawa T., Sonoda K., Kukidome D., Senokuchi T., Matsuo T., et al. Reactive oxygen species from mitochondria induce cyclooxygenase-2 gene expression in human mesangial cells: potential role in diabetic nephropathy. Diabetes 52 (2003) 2570-2577
19. Cameron N.E., Cotter M.A., Archibald V., Dines K.C., and Maxfield E.K. Anti-oxidant and pro-oxidant effects on nerve conduction velocity, endoneurial blood flow and oxygen tension in non-diabetic and streptozotocin-diabetic rats. Diabetologia 37 (1994) 449-459
20. Chiarelli F., Cipollone F., Mohn A., Marini M., Iezzi A., Fazia M., et al. Circulating monocyte chemoattractant protein-1 and early development of nephropathy in type 1 diabetes. Diabetes Care 25 (2002) 1829-1834
21. Chiarelli F., Santilli F., Sabatino G., Blasetti A., Tumini S., Cipollone F., et al. Effects of vitamin E supplementation on intracellular antioxidant enzyme production in adolescents with type 1 diabetes and early microangiopathy. Pediatr. Res. 56 (2004) 720-725
22. Davi G., Chiarelli F., Santilli F., Pomilio M., Vigneri S., Falco A., et al. Enhanced lipid peroxidation and platelet activation in the early phase of type 1 diabetes mellitus: role of interleukin-6 and disease duration. Circulation 107 (2003) 3199-3203
23. Burkle A. Physiology and pathophysiology of poly(ADP-ribosyl)ation. Bioessays 23 (2001) 795-806
24. Herceg Z., and Wang Z.Q. Functions of poly(ADP-ribose) polymerase (PARP) in DNA repair, genomic integrity and cell death. Mutat. Res. 477 (2001) 97-110
25. Du X., Matsumura T., Edelstein D., Rossetti L., Zsengeller Z., Szabo C., et al. Inhibition of GAPDH activity by poly(ADP-ribose) polymerase activates three major pathways of hyperglycemic damage in endothelial cells. J. Clin. Invest. 112 (2003) 1049-1057
26. Balaban R.S., Nemoto S., and Finkel T. Mitochondria, oxidants, and aging. Cell 120 (2005) 483-495
27. Bouche C., Serdy S., Kahn C.R., and Goldfine A.B. The cellular fate of glucose and its relevance in type 2 diabetes. Endocr. Rev. 25 (2004) 807-830
28. Miwa S., St-Pierre J., Partridge L., and Brand M.D. Superoxide and hydrogen peroxide production by drosophila mitochondria. Free Radic. Biol. Med. 35 (2003) 938-948
29. Green K., Brand M.D., and Murphy M.P. Prevention of mitochondrial oxidative damage as a therapeutic strategy in diabetes. Diabetes 53 Suppl. 1 (2004) S110-118
30. Votyakova T.V., and Reynolds I.J. DeltaPsi(m)-dependent and -independent production of reactive oxygen species by rat brain mitochondria. J. Neurochem. 79 (2001) 266-277
31. Brand M.D., Affourtit C., Esteves T.C., Green K., Lambert A.J., Miwa S., et al. Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins. Free Radic. Biol. Med. 37 (2004) 755-767
32. Erecinska M., Bryla J., Michalik M., Meglasson M.D., and Nelson D. Energy metabolism in islets of Langerhans. Biochim. Biophys. Acta 1101 (1992) 273-295
33. Du X.L., Edelstein D., Dimmeler S., Ju Q., Sui C., and Brownlee M. Hyperglycemia inhibits endothelial nitric oxide synthase activity by posttranslational modification at the Akt site. J. Clin. Invest. 108 (2001) 1341-1348
34. Ihnat M.A., Thorpe J.E., Kamat C.D., Szabo C., Green D.E., Warnke L.A., et al. Reactive oxygen species mediate a cellular 'memory' of high glucose stress signalling. Diabetologia 50 (2007) 1523-1531
35. Boss O., Hagen T., and Lowell B.B. Uncoupling proteins 2 and 3: potential regulators of mitochondrial energy metabolism. Diabetes 49 (2000) 143-156
36. Rousset S., Alves-Guerra M.C., Mozo J., Miroux B., Cassard-Doulcier A.M., Bouillaud F., et al. The biology of mitochondrial uncoupling proteins. Diabetes 53 Suppl. 1 (2004) S130-135
37. Echtay K.S., Winkler E., Frischmuth K., and Klingenberg M. Uncoupling proteins 2 and 3 are highly active H(+) transporters and highly nucleotide sensitive when activated by coenzyme Q (ubiquinone). Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 1416-1421
38. Echtay K.S., and Brand M.D. Coenzyme Q induces GDP-sensitive proton conductance in kidney mitochondria. Biochem. Soc. Trans. 29 (2001) 763-768
39. Krauss S., Zhang C.Y., and Lowell B.B. The mitochondrial uncoupling-protein homologues. Nat. Rev. Mol. Cell. Biol. 6 (2005) 248-261
40. Mattson M.P., and Liu D. Mitochondrial potassium channels and uncoupling proteins in synaptic plasticity and neuronal cell death. Biochem. Biophys. Res. Commun. 304 (2003) 539-549
41. Puigserver P., Wu Z., Park C.W., Graves R., Wright M., and Spiegelman B.M. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92 (1998) 829-839
42. Hsu Y.H., Niu T., Song Y., Tinker L., Kuller L.H., and Liu S. Genetic variants in the ucp2-ucp3 gene cluster and risk of diabetes in the Women's Health Initiative Observational Study. Diabetes 57 (2008) 1101-1107
43. Cui Y., Xu X., Bi H., Zhu Q., Wu J., Xia X.Q., et al. Expression modification of uncoupling proteins and MnSOD in retinal endothelial cells and pericytes induced by high glucose: the role of reactive oxygen species in diabetic retinopathy. Exp. Eye Res. 83 (2006) 807-816
44. Vincent A.M., Olzmann J.A., Brownlee M., Sivitz W.I., and Russell J.W. Uncoupling proteins prevent glucose-induced neuronal oxidative stress and programmed cell death. Diabetes 53 (2004) 726-734
45. Rudofsky Jr. G., Schroedter A., Schlotterer A., Voron'ko O.E., Schlimme M., Tafel J.I., et al. Functional polymorphisms of ucp2 and ucp3 are associated with a reduced prevalence of diabetic neuropathy in patients with type 1 diabetes. Diabetes Care 29 (2006) 89-94
46. Yamasaki H., Sasaki H., Ogawa K., Shono T., Tamura S., Doi A., et al. Uncoupling protein 2 promoter polymorphism -866G/A affects peripheral nerve dysfunction in Japanese type 2 diabetic patients. Diabetes Care 29 (2006) 888-894
47. Gustafsson H., Soderdahl T., Jonsson G., Bratteng J.O., and Forsby A. Insulin-like growth factor type 1 prevents hyperglycemia-induced uncoupling protein 3 down-regulation and oxidative stress. J. Neurosci. Res. 77 (2004) 285-291
48. Cave A.C., Brewer A.C., Narayanapanicker A., Ray R., Grieve D.J., Walker S., et al. NADPH oxidases in cardiovascular health and disease. Antioxid. Redox Signal. 8 (2006) 691-728
49. Lambeth J.D. Nox enzymes, ROS, and chronic disease: an example of antagonistic pleiotropy. Free Radic. Biol. Med. 43 (2007) 332-347
50. Rosen P., Nawroth P.P., King G., Moller W., Tritschler H.J., and Packer L. The role of oxidative stress in the onset and progression of diabetes and its complications: a summary of a Congress Series sponsored by UNESCO-MCBN, the American Diabetes Association and the German Diabetes Society. Diabetes Metab. Res. Rev. 17 (2001) 189-212
51. Guzik T.J., Mussa S., Gastaldi D., Sadowski J., Ratnatunga C., Pillai R., et al. Mechanisms of increased vascular superoxide production in human diabetes mellitus: role of NAD(P)H oxidase and endothelial nitric oxide synthase. Circulation 105 (2002) 1656-1662
52. Laursen J.B., Somers M., Kurz S., McCann L., Warnholtz A., Freeman B.A., et al. Endothelial regulation of vasomotion in ApoE-deficient mice: implications for interactions between peroxynitrite and tetrahydrobiopterin. Circulation 103 (2001) 1282-1288
53. Du X., Edelstein D., Obici S., Higham N., Zou M.H., and Brownlee M. Insulin resistance reduces arterial prostacyclin synthase and eNOS activities by increasing endothelial fatty acid oxidation. J. Clin. Invest. 116 (2006) 1071-1080
54. Srinivasan S., Hatley M.E., Bolick D.T., Palmer L.A., Edelstein D., Brownlee M., et al. Hyperglycaemia-induced superoxide production decreases eNOS expression via AP-1 activation in aortic endothelial cells. Diabetologia 47 (2004) 1727-1734
55. Wu K.K. Regulation of endothelial nitric oxide synthase activity and gene expression. Ann. NY Acad. Sci. 962 (2002) 122-130
56. 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
57. Lastra G., and Manrique C. The expanding role of oxidative stress, renin angiotensin system, and beta-cell dysfunction in the cardiometabolic syndrome and type 2 diabetes mellitus. Antioxid. Redox Signal. 9 (2007) 943-954
58. Hensley K., Robinson K.A., Gabbita S.P., Salsman S., and Floyd R.A. Reactive oxygen species, cell signaling, and cell injury. Free Radic. Biol. Med. 28 (2000) 1456-1462
59. Beckman J.A., Goldfine A.B., Gordon M.B., Garrett L.A., Keaney Jr. J.F., and Creager M.A. Oral antioxidant therapy improves endothelial function in type 1 but not type 2 diabetes mellitus. Am. J. Physiol. Heart Circ. Physiol. 285 (2003) H2392-2398
60. Heller R., Werner-Felmayer G., and Werner E.R. Alpha-tocopherol and endothelial nitric oxide synthesis. Ann. NY Acad. Sci. 1031 (2004) 74-85
61. Skyrme-Jones R.A., O'Brien R.C., Berry K.L., and Meredith I.T. Vitamin E supplementation improves endothelial function in type I diabetes mellitus: a randomized, placebo-controlled study. J. Am. Coll. Cardiol. 36 (2000) 94-102
62. Yusuf S., Dagenais G., Pogue J., Bosch J., and 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
63. Packer L., Kraemer K., and Rimbach G. Molecular aspects of lipoic acid in the prevention of diabetes complications. Nutrition 17 (2001) 888-895
64. van Dam P.S. Oxidative stress and diabetic neuropathy: pathophysiological mechanisms and treatment perspectives. Diabetes Metab. Res. Rev. 18 (2002) 176-184
65. Nascimento N.R., Lessa L.M., Kerntopf M.R., Sousa C.M., Alves R.S., Queiroz M.G., et al. Inositols prevent and reverse endothelial dysfunction in diabetic rat and rabbit vasculature metabolically and by scavenging superoxide. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 218-223
66. Szewczyk A., and Wojtczak L. Mitochondria as a pharmacological target. Pharmacol. Rev. 54 (2002) 101-127
67. Schnackenberg C.G. Oxygen radicals in cardiovascular-renal disease. Curr. Opin. Pharmacol. 2 (2002) 121-125
68. Sotiropoulos K.B., Clermont A., Yasuda Y., Rask-Madsen C., Mastumoto M., Takahashi J., et al. Adipose-specific effect of rosiglitazone on vascular permeability and protein kinase C activation: novel mechanism for ppargamma agonist's effects on edema and weight gain. FASEB J. 20 (2006) 1203-1205