MAIN MECHANISMS OF THE INITIATION AND DEVELOPMENT OF DIABETIC COMPLICATIONS: THE ROLE OF NITRATIVE STRESS

V. R. Drel


DOI: http://dx.doi.org/10.30970/sbi.0402.085

Abstract


In the review described the main mechanisms of the oxidative stress initiation in the mitochondria electron-transport chain under the hyperglycaemia condition. It is described the main metabolic and signal-transduction mechanisms, activation of which takes place under the chronic diabetic complications, and which leads to the increase of oxidative stress. It is analised in detail the role of nitric oxide in the biological systems and its properties under the condition of oxidative stress, especially under the diabetes mellitus. The results of the main biological targets for the peroxinitrite and the molecular markers of the diabetic complications were summarized.


Keywords


diabetes mellitus, glicosylation, peroxinitrite, oxidative-nitrative stress, poly-ADP-ribosylation

References


1. Akizuki E., Akaike T., Okamoto S. et al. Role of NO and superoxide in acute cardiac allograft rejection in rats. Proc. Soc. Exp. Biol. Med, 2000; 225(2): 151-159.
https://doi.org/10.1046/j.1525-1373.2000.22519.x
PMid:11044258

2. Atkins R.C., Zimmet P. Diabetic kidney disease: act now or pay later. Saudi. J. Kidney Dis. Transpl, 2010; 21(2): 217-221.
https://doi.org/10.1159/000280547
PMid:20213919

3. Baker P.R., Schopfer F.J., Sweeney S., Freeman B.A. Red cell membrane and plasma linoleic acid nitration products: synthesis, clinical identification, and quantitation. Proc. Natl. Acad. Sci. USA, 2004; 101 (32): 11577-11582.
https://doi.org/10.1073/pnas.0402587101
PMid:15273286 PMCid:PMC511023

4. Beckman J.S., Beckman T.W., Chen J. et al. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA, 1990; 87(4), 1620-1624.
https://doi.org/10.1073/pnas.87.4.1620
PMid:2154753 PMCid:PMC53527

5. Beckman J.S., Koppenol W.H. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am. J. Physiol, 1996; 271(5 Pt 1): C1424-1437.
https://doi.org/10.1152/ajpcell.1996.271.5.C1424
PMid:8944624

6. Bishop A., Anderson J.E. NO signaling in the CNS: from the physiological to the pathological. Toxicology, 2005; 208(2): 193-205.
https://doi.org/10.1016/j.tox.2004.11.034
PMid:15691584

7. Bonini M.G., Radi R., Ferrer-Sueta G. et al. Direct EPR detection of the carbonate radical anion produced from peroxynitrite and carbon dioxide. J. Biol. Chem, 1999; 274(16): 10802-10806.
https://doi.org/10.1074/jbc.274.16.10802
PMid:10196155

8. Boulares A.H., Yakovlev A.G., Ivanova V. et al. Role of poly(ADP-ribose) polymerase (PARP) cleavage in apoptosis. Caspase 3-resistant PARP mutant increases rates of apoptosis in transfected cells. J. Biol. Chem, 1999; 274(33): 22932-22940.
https://doi.org/10.1074/jbc.274.33.22932
PMid:10438458

9. Brennan M.L., Wu W., Fu X. et al. A tale of two controversies: defining both the role of peroxidases in nitrotyrosine formation in vivo using eosinophil peroxidase and myeloperoxidase-deficient mice, and the nature of peroxidase-generated reactive nitrogen species. J. Biol. Chem, 2002; 277(20): 17415-17427.
https://doi.org/10.1074/jbc.M112400200
PMid:11877405

10. Brito C., Naviliat M., Tiscornia A.C. et al.Peroxynitrite inhibits T lymphocyte activation and proliferation by promoting impairment of tyrosine phosphorylation and peroxynitrite-driven apoptotic death. J. Immunol, 1999; 162(6): 3356-3366.

11. Brown G.C. Nitric oxide and mitochondria. Front. Biosci, 2007; 12: 1024-1033.
https://doi.org/10.2741/2122
PMid:17127357

12. Brown G.C., Borutaite V. Inhibition of mitochondrial respiratory complex I by nitric oxide, peroxynitrite and S-nitrosothiols. Biochim. Biophys. Acta, 2004; 1658(1-2): 44-49.
https://doi.org/10.1016/j.bbabio.2004.03.016
PMid:15282173

13. Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes, 2005; 54(6): 1615-1625.
https://doi.org/10.2337/diabetes.54.6.1615
PMid:15919781

14. Bruckdorfer R. The basics about nitric oxide. Mol. Aspects Med, 2005; 26 (1-2): 3-31.
https://doi.org/10.1016/j.mam.2004.09.002
PMid:15722113

15. Brüne B., Zhou J. Nitric oxide and superoxide: interference with hypoxic signaling. Cardiovasc. Res, 2007; 75(2): 275-282.
https://doi.org/10.1016/j.cardiores.2007.03.005
PMid:17412315

16. Buchczyk D.P., Grune T., Sies H., Klotz L.O. Modifications of glyceraldehyde-3-phosphate dehydrogenase induced by increasing concentrations of peroxynitrite: early recognition by 20S proteasome. Biol. Chem, 2003; 384(2): 237-241.
https://doi.org/10.1515/BC.2003.026
PMid:12675516

17. Burney S., Caulfield J.L., Niles J.C. et al. The chemistry of DNA damage from nitric oxide and peroxynitrite. Mutat. Res, 1999; 424 (1-2): 37-49.
https://doi.org/10.1016/S0027-5107(99)00006-8

18. Chen Y.R., Chen C.L., Chen W. et al. Formation of protein tyrosine ortho-semiquinone radical and nitrotyrosine from cytochrome c-derived tyrosyl radical. J. Biol. Chem, 2004; 279(17): 18054-18062.
https://doi.org/10.1074/jbc.M307706200
PMid:14761966

19. Chi Q., Wang T., Huang K. Effect of insulin nitration by peroxynitrite on its biological activity. Biochem. Biophys. Res. Commun, 2005; 330(3): 791-796.
https://doi.org/10.1016/j.bbrc.2005.03.034
PMid:15809066

20. Cole A.R., Astell A., Green C., Sutherland C. Molecular connexions between dementia and diabetes. Neurosci. Biobehav, 2007; 31(7): 1046-1063.
https://doi.org/10.1016/j.neubiorev.2007.04.004
PMid:17544131

21. 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, 1997; 96(1): 25-28.
https://doi.org/10.1161/01.CIR.96.1.25
PMid:9236411

22. Crosswhite P., Sun Z. Nitric oxide, oxidative stress and inflammation in pulmonary arterial hypertension. J. Hypertens, 2010; 28(2): 201-212.
https://doi.org/10.1097/HJH.0b013e328332bcdb
PMid:20051913 PMCid:PMC2809140

23. Denicola A., Radi R. Peroxynitrite and drug-dependent toxicity. Toxicology, 2005; 208(2): 273-288.
https://doi.org/10.1016/j.tox.2004.11.023
PMid:15691591

24. Dicks A.P., Williams D.L. Generation of nitric oxide from S-nitrosothiols using protein-bound Cu2+ sources. Chem. Biol, 1996; 3(8): 655-659.
https://doi.org/10.1016/S1074-5521(96)90133-7

25. Drel V.R., Mashtalir N., Ilnytska O. et al. The leptin-deficient (ob/ob) mouse: a new animal model of peripheral neuropathy of type 2 diabetes and obesity. Diabetes, 2006; 55(12): 3335-3343.
https://doi.org/10.2337/db06-0885
PMid:17130477

26. Drel V.R., Pacher P., Vareniuk I. et al. Evaluation of the peroxynitrite decomposition catalyst Fe(III) tetra-mesitylporphyrin octasulfonate on peripheral neuropathy in a mouse model of type 1 diabetes. Int. J. Mol. Med, 2007; 20(6): 783-792.
https://doi.org/10.3892/ijmm.20.6.783
PMid:17982684 PMCid:PMC2527588

27. Drel V.R., Pacher P., Vareniuk I. et al. A peroxynitrite decomposition catalyst counteracts sensory neuropathy in streptozotocin-diabetic mice. Eur. J. Pharmacol, 2007; 569(1-2): 48-58.
https://doi.org/10.1016/j.ejphar.2007.05.055
PMid:17644085 PMCid:PMC2225472

28. Drel V.R., Xu W., Zhang J. et al. Poly(ADP-ribose)polymerase inhibition counteracts cataract formation and early retinal changes in streptozotocin-diabetic rats. Invest. Ophthalmol. Vis. Sci, 2009; 50(4): 1778-1790.
https://doi.org/10.1167/iovs.08-2191
PMid:19098320

29. Drel V.R., Xu W., Zhang J. et al. Poly(Adenosine 5′-diphosphate-ribose) polymerase inhibition counteracts multiple manifestations of experimental type 1 diabetic nephropathy. Endocrinology, 2009; 150(12): 5273-5283.
https://doi.org/10.1210/en.2009-0628
PMid:19854869 PMCid:PMC2795707

30. El-Remessy A.B., Bartoli M., Platt D.H. et al. Oxidative stress inactivates VEGF survival signaling in retinal endothelial cells via PI 3-kinase tyrosine nitration. J. Cell Sci, 2005; 118(Pt. 1): 243-252.
https://doi.org/10.1242/jcs.01612
PMid:15615788

31. Eu J.P., Liu L., Zeng M., Stamler, J.S. An apoptotic model for nitrosative stress. Biochemistry, 2000; 39(5): 1040-1047.
https://doi.org/10.1021/bi992046e
PMid:10653649

32. Ferrer-Sueta G., Quijano C., Alvarez B., Radi R. Reactions of manganese porphyrins and manganese- superoxide dismutase with peroxynitrite. Methods Enzymol, 2002; 349: 23-37.
https://doi.org/10.1016/S0076-6879(02)49318-4

33. Forsmark-Andree P., Persson B., Radi R. et al. Oxidative modification of nicotinamide nucleotide transhydrogenase in submitochondrial particles: effect of endogenous ubiquinol. Arch. Biochem. Biophys, 1996; 336(1): 113-120.
https://doi.org/10.1006/abbi.1996.0538
PMid:8951041

34. Geller D.A., Billiar T.R. Molecular biology of nitric oxide synthases. Cancer Metastasis Rev, 1998; 17(1): 7-23.
https://doi.org/10.1023/A:1005940202801

35. Goodwin D.C., Gunther M. R., Hsi L. C. et al. Nitric oxide trapping of tyrosyl radicals generated during prostaglandin endoperoxide synthase turnover. Detection of the radical derivative of tyrosine 385. J. Biol. Chem, 1998; 273(15): 8903-8909.
https://doi.org/10.1074/jbc.273.15.8903
PMid:9535872

36. Gorbunov N.V., Osipov A.N., Day B.W. et al. Reduction of ferrylmyoglobin and ferrylhemoglobin by nitric oxide: a protective mechanism against ferryl hemoprotein-induced oxidations. Biochemistry, 1995; 34(20): 6689-6699.
https://doi.org/10.1021/bi00020a014
PMid:7756300

37. Gorg B., Bidmon H.J., Keitel V. et al. Inflammatory cytokines induce protein tyrosine nitration in rat astrocytes. Arch. Biochem. Biophys, 2006; 449(1-2): 104-114.
https://doi.org/10.1016/j.abb.2006.02.012
PMid:16579953

38. Govers R., Coster A.C., James D.E. Insulin increases cell surface GLUT4 levels by dose dependently discharging GLUT4 into a cell surface recycling pathway. Mol. Cell. Biol, 2004; 24(14): 6456-6466.
https://doi.org/10.1128/MCB.24.14.6456-6466.2004
PMid:15226445 PMCid:PMC434240

39. Gow A., Duran D., Thom S.R. Ischiropoulos H. Carbon dioxide enhancement of peroxynitrite-mediated protein tyrosine nitration. Arch. Biochem. Biophys, 1996; 333(1): 42-48.
https://doi.org/10.1006/abbi.1996.0362
PMid:8806752

40. Greenacre S.A., Ischiropoulos H. Tyrosine nitration: localisation, quantification, consequences for protein function and signal transduction. Free Radic. Res, 2001; 34(6): 541-581.
https://doi.org/10.1080/10715760100300471
PMid:11697033

41. Guidarelli A., Fiorani M., Cantoni O. Enhancing effects of intracellular ascorbic acid on peroxynitrite-induced U937 cell death are mediated by mitochondrial events resulting in enhanced sensitivity to peroxynitrite-dependent inhibition of complex III and formation of hydrogen peroxide. Biochem. J, 2004; 378(Pt. 3): 959-966.
https://doi.org/10.1042/bj20031167
PMid:14627438 PMCid:PMC1223997

42. Ha H.C., Snyder S.H. Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc. Natl. Acad. Sci. USA, 1999; 96(24): 13978-13982.
https://doi.org/10.1073/pnas.96.24.13978
PMid:10570184 PMCid:PMC24176

43. Han D., Canali R., Garcia J. et al. Sites and mechanisms of aconitase inactivation by peroxynitrite: modulation by citrate and glutathione. Biochemistry, 2005; 44(36): 11986-11996.
https://doi.org/10.1021/bi0509393
PMid:16142896

44. Haqqani A.S., Kelly J.F., Birnboim H.C. Selective nitration of histone tyrosine residues in vivo in mutatect tumors. J. Biol. Chem, 2002; 277(5): 3614-3621.
https://doi.org/10.1074/jbc.M105730200
PMid:11723112

45. Hogg N., Kalyanaraman B. Nitric oxide and lipid peroxidation. Biochim. Biophys. Acta, 1999; 1411(2-3): 378-384.
https://doi.org/10.1016/S0005-2728(99)00027-4

46. Jang B., Han S. Biochemical properties of cytochrome c nitrated by peroxynitrite. Biochimie, 2006; 88(1): 53-58.
https://doi.org/10.1016/j.biochi.2005.06.016
PMid:16040185

47. Jansson E.A., Huang L., Malkey R. et al. A mammalian functional nitrate reductase that regulates nitrite and nitric oxide homeostasis. Nat. Chem. Biol, 2008; 4(7): 411-417.
https://doi.org/10.1038/nchembio.92
PMid:18516050

48. Kelm M., Feelisch M., Deussen A. et al. Release of endothelium derived nitric oxide in relation to pressure and flow. Cardiovasc. Res, 1991; 25(10): 831-836.
https://doi.org/10.1093/cvr/25.10.831
PMid:1747876

49. Kim P.K., Kwon Y.G., Chung H.T., Kim Y.M. Regulation of caspases by nitric oxide. Ann. N Y Acad. Sci, 2002; 962: 42-52.
https://doi.org/10.1111/j.1749-6632.2002.tb04054.x
PMid:12076961

50. King H., Aubert R.E., Herman W.H. Global burden of diabetes, 1995-2025: prevalence, numerical estimates, and projections. Diabetes Care, 1998; 21(9): 1414-1431.
https://doi.org/10.2337/diacare.21.9.1414
PMid:9727886

51. Klebanoff S.J. Reactive nitrogen intermediates and antimicrobial activity: role of nitrite. Free. Radic. Biol. Med, 1993; 14(4): 351-360.
https://doi.org/10.1016/0891-5849(93)90084-8

52. Klotz L.O., Schieke S.M., Sies H., Holbrook N.J. Peroxynitrite activates the phosphoinositide 3-kinase/Akt pathway in human skin primary fibroblasts. Biochem. J, 2000; 352(Pt. 1): 219-225.
https://doi.org/10.1042/bj3520219
PMid:11062076 PMCid:PMC1221450

53. Knight T.R., Kurtz A., Bajt M.L. et al. Vascular and hepatocellular peroxynitrite formation during acetaminophen toxicity: role of mitochondrial oxidant stress. Toxicol. Sci, 2001; 62(2): 212-220.
https://doi.org/10.1093/toxsci/62.2.212
PMid:11452133

54. Kosenko E., Llansola M., Montoliu C. et al. Glutamine synthetase activity and glutamine content in brain: modulation by NMDA receptors and nitric oxide. Neurochem. Int, 2003; 43(4-5): 493-499.
https://doi.org/10.1016/S0197-0186(03)00039-1

55. Lancaster J.R. Simulation of the diffusion and reaction of endogenously produced nitric oxide. Proc. Natl. Acad. Sci. USA, 1994; 91(17): 8137-8141.
https://doi.org/10.1073/pnas.91.17.8137
PMid:8058769 PMCid:PMC44560

56. Lee J.R., Kim J.K., Lee S.J., Kim K.P. Role of protein tyrosine nitration in neurodegenerative diseases and atherosclerosis. Arch. Pharm. Res, 2009; 32(8):1109-1118.
https://doi.org/10.1007/s12272-009-1802-0
PMid:19727603

57. Leone A.M., Palmer R.M., Knowles R.G. et al. Constitutive and inducible nitric oxide synthases incorporate molecular oxygen into both nitric oxide and citrulline. J. Biol. Chem, 1991; 266(35): 23790-23795.

58. Mallozzi C., Di Stasi A.M., Minetti M. Peroxynitrite modulates tyrosine-dependent signal transduction pathway of human erythrocyte band 3. FASEB J, 1997; 11(14): 1281-1290.
https://doi.org/10.1096/fasebj.11.14.9409547
PMid:9409547

59. Marcondes S., Turko I.V., Murad F. Nitration of succinyl-CoA:3-oxoacid CoA-transferase in rats after endotoxin administration. Proc. Natl. Acad. Sci. USA, 2001; 98(13): 7146-7151.
https://doi.org/10.1073/pnas.141222598
PMid:11416199 PMCid:PMC34637

60. Martyn J.A., Kaneki M., Yasuhara S. Obesity-induced insulin resistance and hyperglycemia: etiologic factors and molecular mechanisms. Anesthesiology, 2008; 109(1): 137-148.
https://doi.org/10.1097/ALN.0b013e3181799d45
PMid:18580184 PMCid:PMC3896971

61. Merriman-Smith B.R., Krushinsky A., Kistler J., Donaldson P.J. Expression patterns for glucose transporters GLUT1 and GLUT3 in the normal rat lens and in models of diabetic cataract. Invest. Ophthalmol. Vis. Sci, 2003; 44(8): 3458-3466.
https://doi.org/10.1167/iovs.02-1235
PMid:12882795

62. Mülsch A., Mordvintcev P.I., Vanin A.F., Busse R. Formation and release of dinitrosyl iron complexes by endothelial cells. Biochem. Biophys. Res. Commun, 1993; 196(3): 1303-1308.
https://doi.org/10.1006/bbrc.1993.2394
PMid:8250885

63. Neumann P., Gertzberg N., Vaughan E. et al. Peroxynitrite mediates TNF-induced endothelial barrier dysfunction and nitration of actin. Am. J. Physiol. Lung. Cell Mol. Physiol, 2006; 290(4): L674-L684.
https://doi.org/10.1152/ajplung.00391.2005
PMid:16284212

64. Nielsen V.G., Crow J.P., Mogal A. et al. Peroxynitrite decreases hemostasis in human plasma in vitro. Anesth. Analg, 2004; 99(1): 21-26.
https://doi.org/10.1213/01.ANE.0000116962.93953.70
PMid:15281495

65. Nishikawa T., Edelstein D., Du X.L. et al. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature, 2000; 404(6779): 787-790.
https://doi.org/10.1038/35008121
PMid:10783895

66. Nogueira-Machado J.A., Chaves M.M. From hyperglycemia to AGE-RAGE interaction on the cell surface: a dangerous metabolic route for diabetic patients. Expert. Opin. Ther. Targets, 2008; 12(7): 871-82.
https://doi.org/10.1517/14728222.12.7.871
PMid:18554155

67. Nohl H., Staniek K., Kozlov A.V. The existence and significance of a mitochondrial nitrite reductase. Redox Rep, 2005; 10(6):281-286.
https://doi.org/10.1179/135100005X83707
PMid:16438799

68. Nomiyama T., Igarashi Y., Taka H. et al. Reduction of insulinstimulated glucose uptake by peroxynitrite is concurrent with tyrosine nitration of insulin receptor substrate-1. Biochem. Biophys. Res. Commun, 2004; 320(3): 639-647.
https://doi.org/10.1016/j.bbrc.2004.06.019
PMid:15240096

69. Nowak P., Kolodziejczyk J., Wachowicz B. Peroxynitrite and fibrinolytic system: the effect of peroxynitrite on plasmin activity. Mol. Cell Biochem, 2004; 267(1-2): 141-146.
https://doi.org/10.1023/B:MCBI.0000049370.23457.10
PMid:15663195

70. Obrosova I.G., Drel V.R., Oltman C.L. et al. Role of nitrosative stress in early neuropathy and vascular dysfunction in streptozotocin-diabetic rats. Am. J. Physiol. Endocrinol. Metab, 2007; 293(6): E1645-55.
https://doi.org/10.1152/ajpendo.00479.2007
PMid:17911342

71. Obrosova I.G., Drel V.R., Pacher P. et al. Oxidative-nitrosative stress and poly(ADP-ribose) polymerase (PARP) activation in experimental diabetic neuropathy: the relation is revisited. Diabetes, 2005; 54 (12): 3435-3441.
https://doi.org/10.2337/diabetes.54.12.3435
PMid:16306359 PMCid:PMC2228259

72. Pacher P., Beckman J.S., Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol. Rev, 2007; 87(1): 315-424.
https://doi.org/10.1152/physrev.00029.2006
PMid:17237348 PMCid:PMC2248324

73. Patel R.P., Moellering D., Murphy-Ullrich J. et al. Cell signaling by reactive nitrogen and oxygen species in atherosclerosis. Free Radic. Biol. Med, 2000; 28(12): 1780-1794.
https://doi.org/10.1016/S0891-5849(00)00235-5

74. Pennathur S., Bergt C., Shao B. et al. Human atherosclerotic intima and blood of patients with established coronary artery disease contain high density lipoprotein damaged by reactive nitrogen species. J. Biol. Chem, 2004; 279(41): 42977-42983.
https://doi.org/10.1074/jbc.M406762200
PMid:15292228

75. Pufahl R.A., Singer C.P., Peariso K.L. et al. Metal ion chaperone function of the soluble Cu(I) receptor Atx1. Science, 1997; 278(5339): 853-856.
https://doi.org/10.1126/science.278.5339.853
PMid:9346482

76. Radi R., Beckman J.S., Bush K.M., Freeman B.A. Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide. J. Biol. Chem, 1991(7): 266, 4244-4250.

77. Radi R., Cassina A., Hodara R. et al. Peroxynitrite reactions and formation in mitochondria. Free Radic. Biol. Med, 2002; 33(11): 1451-1464.
https://doi.org/10.1016/S0891-5849(02)01111-5

78. Rees M.D., Kennett E.C., Whitelock J.M., Davies M.J. Oxidative damage to extracellular matrix and its role in human pathologies. Free Radic. Biol. Med, 2008; 44(12): 1973-2001.
https://doi.org/10.1016/j.freeradbiomed.2008.03.016
PMid:18423414

79. Rubbo H., Denicola A., Radi R. Peroxynitrite inactivates thiolcontaining enzymes of Trypanosoma cruzi energetic metabolism and inhibits cell respiration. Arch. Biochem. Biophys, 1994; 308(1): 96-102.
https://doi.org/10.1006/abbi.1994.1014
PMid:8311481

80. Samouilov A., Kuppusamy P., Zweier J.L. Evaluation of the magnitude and rate of nitric oxide production from nitrite in biological systems. Arch. Biochem. Biophys, 1998; 357(1): 1-7.
https://doi.org/10.1006/abbi.1998.0785
PMid:9721176

81. Schmitz H.D. Reversible nuclear translocation of glyceraldehyde-3-phosphate dehydrogenase upon serum depletion. Eur. J. Cell. Biol, 2001; 80 (6): 419-427.
https://doi.org/10.1078/0171-9335-00174
PMid:11484933

82. Shao B., Bergt C., Fu X. et al. Tyrosine 192 in apolipoprotein A-I is the major site of nitration and chlorination by myeloperoxidase, but only chlorination markedly impairs ABCA1-dependent cholesterol transport. J. Biol. Chem, 2005; 280(7): 5983-5993.
https://doi.org/10.1074/jbc.M411484200
PMid:15574409

83. Shi H., Noguchi N., Xu Y., Niki E. Formation of phospholipid hydroperoxides and its inhibition by alpha-tocopherol in rat brain synaptosomes induced by peroxynitrite. Biochem. Biophys. Res. Commun, 1999; 257(3): 651-656.
https://doi.org/10.1006/bbrc.1999.0434
PMid:10208838

84. Shinohara M. Overexpression of glyoxalase-I in bovine endothelial cells inhibits intracellular advanced glycation endproduct formation and prevents hyperglycemia-induced increases in macromolecular endocytosis. J. Clin. Invest, 1998; 101(5): 1142-1147.
https://doi.org/10.1172/JCI119885
PMid:9486985 PMCid:PMC508666

85. Sokolovsky M., Riordan J.F., Vallee B.L. Conversion of 3-nitrotyrosine to 3-aminotyrosine in peptides and proteins. Biochem. Biophys. Res. Commun, 1967; 27(1): 20-25.
https://doi.org/10.1016/S0006-291X(67)80033-0

86. Stamler J.S. S-nitrosothiols in the blood: roles, amounts, and methods of analysis. Circ. Res., 2004; 94(4): 414-417.
https://doi.org/10.1161/01.RES.0000122071.55721.BC
PMid:15001539

87. Stone J.R., Marletta M.A. Spectral and kinetic studies on the activation of soluble guanylate cyclase by nitric oxide. Biochemistry, 1996; 35(4): 1093-1099.
https://doi.org/10.1021/bi9519718
PMid:8573563

88. Sturgeon B.E., Glover R.E., Chen Y.R. et al. Tyrosine iminoxyl radical formation from tyrosyl radical/nitric oxide and nitrosotyrosine. J. Biol. Chem, 2001; 276(49): 45516-45521.
https://doi.org/10.1074/jbc.M106835200
PMid:11551949

89. Szabo C., Zingarelli B., O'Connor M., Salzman A.L. DNA strand breakage, activation of poly (ADP-ribose) synthetase, cellular energy depletion are involved in the cytotoxicity of macrophages and smooth muscle cells exposed to peroxynitrite. Proc. Natl. Acad. Sci. USA, 1996; 93(5): 1753-1758.
https://doi.org/10.1073/pnas.93.5.1753
PMid:8700830 PMCid:PMC39853

90. Trostchansky A., Ferrer-Sueta G., Batthyany C. et al. Peroxynitrite flux-mediated LDL oxidation is inhibited by manganese porphyrins in the presence of uric acid. Free Radic. Biol. Med, 2003; 35(10): 1293-1300.
https://doi.org/10.1016/j.freeradbiomed.2003.07.004
PMid:14607528

91. Trumpower B.L. The protonmotive Q cycle: energy transduction by coupling of proton translocation to electron transfer by the cytochrome bc1 complex. J. Biol. Chem, 1990: 265(20): 11409-11412.

92. Vanin A.F. Dinitrosyl iron complexes with thiolate ligands: physico-chemistry, biochemistry and physiology. Nitric Oxide, 2009; 21(1): 1-13.
https://doi.org/10.1016/j.niox.2009.03.005
PMid:19366636

93. Vieira H.L., Belzacq A.S., Haouzi D. et al. The adenine nucleotide translocator: a target of nitric oxide, peroxynitrite, 4-hydroxynonenal. Oncogene, 2001; 20(32): 4305-4316.
https://doi.org/10.1038/sj.onc.1204575
PMid:11466611

94. Wallace D.C. Diseases of the mitochondrial DNA. Annu. Rev. Biochem, 1992: 61: 1175-1212.
https://doi.org/10.1146/annurev.bi.61.070192.005523
PMid:1497308

95. Wilkinson-Berka J.L., Miller A.G. Update on the treatment of diabetic retinopathy. Scientific World Journal, 2008; 8: 98-120.
https://doi.org/10.1100/tsw.2008.25
PMid:18264628 PMCid:PMC5848621

96. Zhang Y., Hogg N. S-Nitrosothiols: cellular formation and transport. Free Radic. Biol. Med, 2005; 38(7): 831-838.
https://doi.org/10.1016/j.freeradbiomed.2004.12.016
PMid:15749378

97. Zou M.H., Cohen R., Ullrich V. Peroxynitrite and vascular endothelial dysfunction in diabetes mellitus. Endothelium, 2004; 11(2): 89-97.
https://doi.org/10.1080/10623320490482619
PMid:15370068


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