Exposure of human keratinocytes to ischemia, hyperglycemia and their combination induces oxidative stress via the enzymes inducible nitric oxide synthase and xanthine oxidase

Journal of Dermatological Science

Volumn 55, Issue 2, 2009, Pages 82-90

  Portugal Cohen, Meital ^a   Kohen, Ron ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Hyperglycemia; Inducible nitric oxide synthase (iNOS); Ischemia reperfusion injury (IRI); Reactive oxygen species (ROS); Total antioxidant scavenging capacity (TSC); Xanthine oxidase (XO)

Indexed keywords

GLUTATHIONE; GLUTATHIONE DISULFIDE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; NITRITE; SUPEROXIDE; URIC ACID; XANTHINE OXIDASE;

ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; DIABETES MELLITUS; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITION; HUMAN; HUMAN CELL; HYPERGLYCEMIA; ISCHEMIA; KERATINOCYTE; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN DEFECT; SKIN INFLAMMATION;

BIOLOGICAL MARKERS; CELL HYPOXIA; CELL LINE; CELL SURVIVAL; GLUCOSE; GLUTATHIONE; GLUTATHIONE DISULFIDE; HUMANS; HYPERGLYCEMIA; INFLAMMATION MEDIATORS; INTERLEUKIN-6; ISCHEMIA; KERATINOCYTES; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; NITRITES; OXIDATIVE STRESS; REPERFUSION INJURY; SUPEROXIDES; URIC ACID; XANTHINE OXIDASE;

EID: 67649644723     PISSN: 09231811     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jdermsci.2009.05.006     Document Type: Article

References (62)

1. Wohlrab J., Wohlrab D., and Meiss F. Skin diseases in diabetes mellitus. J Dtsch Dermatol Ges 5 (2007) 37-53
2. Sheetz M.J., and King G.L. Molecular understanding of hyperglycemia's adverse effects for diabetic complications. JAMA 288 (2002) 2579-2588
3. Ellis E.A., Guberski D.L., Hutson B., and Grant M.B. Time course of NADH oxidase, inducible nitric oxide synthase and peroxynitrite in diabetic retinopathy in the BBZ/WOR rat. Nitric Oxide 6 (2002) 295-304
4. Pacher P., Obrosova I.G., Mabley J.G., and Szabo C. Role of nitrosative stress and peroxynitrite in the pathogenesis of diabetic complications. Emerging new therapeutical strategies. Curr Med Chem 12 (2005) 267-275
5. Hunt J.V., Dean R.T., and Wolff S.P. Hydroxyl radical production and autoxidative glycosylation. Glucose autoxidation as the cause of protein damage in the experimental glycation model of diabetes mellitus and ageing. Biochem J 256 (1988) 205-212
6. 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
7. Van den Enden M.K., Nyengaard J.R., Ostrow E., Burgan J.H., and Williamson J.R. Elevated glucose levels increase retinal glycolysis and sorbitol pathway metabolism. Implications for diabetic retinopathy. Invest Ophthalmol Vis Sci 36 (1995) 1675-1685
8. Haffner S.M., Greenberg A.S., Weston W.M., Chen H., Williams K., and Freed M.I. Effect of rosiglitazone treatment on nontraditional markers of cardiovascular disease in patients with type 2 diabetes mellitus. Circulation 106 (2002) 84-679
9. Kristiansen O.P., and Mandrup-Poulsen T. Interleukin-6 and diabetes: the good, the bad, or the indifferent?. Diabetes 54 Suppl. 2 (2005) S114-S124
10. Crockett E.T., Galligan J.J., Uhal B.D., Harkema J., Roth R., and Pandya K. Protection of early phase hepatic ischemia-reperfusion injury by cholinergic agonists. BMC Clin Pathol 6 (2006) 3
11. Yassin M.M., Harkin D.W., Barros D'Sa A.A., Halliday M.I., and Rowlands B.J. Lower limb ischemia-reperfusion injury triggers a systemic inflammatory response and multiple organ dysfunction. World J Surg 26 (2002) 115-121
12. Chalmers-Redman R.M., Fraser A.D., Ju W.Y., Wadia J., Tatton N.A., and Tatton W.G. Mechanisms of nerve cell death: apoptosis or necrosis after cerebral ischaemia. Int Rev Neurobiol 40 (1997) 1-25
13. Droge W. Free radicals in the physiological control of cell function. Physiol Rev 82 (2002) 47-95
14. Engerson T.D., McKelvey T.G., Rhyne D.B., Boggio E.B., Snyder S.J., and Jones H.P. Conversion of xanthine dehydrogenase to oxidase in ischemic rat tissues. J Clin Invest 79 (1987) 1564-1570
15. McCord J.M. Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med 312 (1985) 159-163
16. Kohen R., and Nyska A. Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicol Pathol 30 (2002) 620-650
17. Cuzzocrea S., Riley D.P., Caputi A.P., and Salvemini D. Antioxidant therapy: a new pharmacological approach in shock, inflammation, and ischemia/reperfusion injury. Pharmacol Rev 53 (2001) 135-159
18. Beckman J.S. Oxidative damage and tyrosine nitration from peroxynitrite. Chem Res Toxicol 9 (1996) 836-844
19. Abd-El-Aleem S.A., Ferguson M.W., Appleton I., Kairsingh S., Jude E.B., Jones K., et al. Expression of nitric oxide synthase isoforms and arginase in normal human skin and chronic venous leg ulcers. J Pathol 191 (2000) 42-434
20. Ferdinandy P. Peroxynitrite: just an oxidative/nitrosative stressor or a physiological regulator as well?. Br J Pharmacol 148 (2006) 1-3
21. Halliwell B., and Gutteride J.M. Free radicals in Biology and medicine (1999), Oxford University Press, Avon
22. Richeson C., Mulder P., Bowry V., and Ingold K. The complex chemistry of peroxynitrite decomposition: new insight. J. Am. Chem. 120 (1998) 7211-7219
23. Szabo C. Multiple pathways of peroxynitrite cytotoxicity. Toxicol Lett 140-141 (2003) 105-112
24. Portugal M., and Kohen R. Peroxynitrite: a key molecule in skin tissue response to different types of stress. In: Valacchi J., and Davis P.A. (Eds). Oxidants in biology-a question of balance (2008), Springer, Netherlands 19-36
25. Abu Raya S., Trembovler V., Shohami E., and Lazarovici P. A tissue culture ischemic device to study eicosanoid release by pheochromocytoma PC12 cultures. J Neurosci Methods 50 (1993) 197-203
26. Tabakman R., Lazarovici P., and Kohen R. Neuroprotective effects of carnosine and homocarnosine on pheochromocytoma PC12 cells exposed to ischemia. J Neurosci Res 68 (2002) 463-469
27. Koren E., Zverev I., Ginsburg I., and Kohen R. Supplementation with antioxidants fails to increase the total antioxidant capacity of several cell lines in culture. Biomed Pharmacother 62 (2008) 179-188
28. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72 (1976) 248-254
29. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65 (1983) 55-63
30. Slater T.F., Sawyer B., and Straeuli U. Studies on succinate-tetrazolium reductase systems. iii. Points of coupling of four different tetrazolium salts. Biochim Biophys Acta (1963) 383-393
31. Cao G., Verdon C.P., Wu A.H., Wang H., and Prior R.L. Automated assay of oxygen radical absorbance capacity with the COBAS FARA II. Clin Chem 41 (1995) 1738-1744
32. Prior R.L., Hoang H., Gu L., Xu X., Bacchiocca M., Howard L., et al. Assays for hydrophilic and lipophilic antioxidant capacity (oxygen radical absorbance capacity (ORAC(FL))) of plasma and other biological and food samples. J Agric Food Chem 51 (2003) 3273-3279
33. Shilo S., Aronis A., Komarnitsky R., and Tirosh O. Selenite sensitizes mitochondrial permeability transition pore opening in vitro and in vivo: a possible mechanism for chemo-protection. Biochem J 370 (2003) 283-290
34. Motchnik P.A., Frei B., and Ames B.N. Measurement of antioxidants in human blood plasma. Methods Enzymol 234 (1994) 269-279
35. Misko T.P., Schilling R.J., Salvemini D., Moore W.M., and Currie M.G. A fluorometric assay for the measurement of nitrite in biological samples. Anal Biochem 214 (1993) 11-16
36. Wang P., Wu P., Siegel M.I., Egan R.W., and Billah M.M. Interleukin (IL)-10 inhibits nuclear factor kappa B (NF kappa B) activation in human monocytes. IL-10 and IL-4 suppress cytokine synthesis by different mechanisms. J Biol Chem 270 (1995) 9558-9563
37. Abramov Y., Schenker J.G., Lewin A., Friedler S., Nisman B., and Barak V. Plasma inflammatory cytokines correlate to the ovarian hyperstimulation syndrome. Hum Reprod 11 (1996) 1381-1386
38. Catrina S.B., Okamoto K., Pereira T., Brismar K., and Poellinger L. Hyperglycemia regulates hypoxia-inducible factor-1alpha protein stability and function. Diabetes 53 (2004) 3226-3232
39. Halliwell B., and Whiteman M. Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean?. Br J Pharmacol 142 (2004) 231-255
40. Ghiselli A., Serafini M., Natella F., and Scaccini C. Total antioxidant capacity as a tool to assess redox status: critical view and experimental data. Free Radic Biol Med 29 (2000) 1106-1114
41. Huang D., Ou B., and Prior R.L. The chemistry behind antioxidant capacity assays. J Agric Food Chem 53 (2005) 1841-1856
42. Prior R.L., and Cao G. In vivo total antioxidant capacity: comparison of different analytical methods. Free Radic Biol Med 27 (1999) 1173-1181
43. Sies H. Total antioxidant capacity: appraisal of a concept. J Nutr 137 (2007) 1493-1495
44. Nishino T., Nakanishi S., and Okamoto K. Conversion of xanthine dehydrogenase into oxidase and its role in reperfusion injury. Biochem Soc Trans 25 (1997) 783-786
45. Daniliuc S., Bitterman H., Rahat M.A., Kinarty A., Rosenzweig D., and Lahat N. Hypoxia inactivates inducible nitric oxide synthase in mouse macrophages by disrupting its interaction with alpha-actinin 4. J Immunol 171 (2003) 3225-3232
46. Kristian T. Metabolic stages, mitochondria and calcium in hypoxic/ischemic brain damage. Cell Calcium 36 (2004) 221-233
47. Halliwell B. Reactive oxygen species and the central nervous system. J Neurochem 59 (1992) 1609-1623
48. Li C., and Jackson R.M. Reactive species mechanisms of cellular hypoxia-reoxygenation injury. Am J Physiol Cell Physiol 282 (2002) C227-C241
49. Go Y.M., and Jones D.P. Redox compartmentalization in eukaryotic cells. Biochim Biophys Acta 1780 (2008) 1273-1290
50. Khamaisi M., Kavel O., Rosenstock M., Porat M., Yuli M., Kaiser N., et al. Effect of inhibition of glutathione synthesis on insulin action: in vivo and in vitro studies using buthionine sulfoximine. Biochem J 349 (2000) 579-586
51. MacGowan S.W., Regan M.C., Malone C., Sharkey O., Young L., Gorey T.F., et al. Superoxide radical and xanthine oxidoreductase activity in the human heart during cardiac operations. Ann Thorac Surg 60 (1995) 1289-1293
52. Squadrito G.L., Cueto R., Splenser A.E., Valavanidis A., Zhang H., Uppu R.M., et al. Reaction of uric acid with peroxynitrite and implications for the mechanism of neuroprotection by uric acid. Arch Biochem Biophys 376 (2000) 333-337
53. Layton M.E., Wood J.G., Yan Z.Y., and Forster J. Ischemia/reperfusion alters uric acid and ascorbic acid levels in liver. J Surg Res 64 (1996) 1-5
54. Chamorro A., Obach V., Cervera A., Revilla M., Deulofeu R., and Aponte J.H. Prognostic significance of uric acid serum concentration in patients with acute ischemic stroke. Stroke 33 (2002) 1048-1052
55. Marletta M.A. Nitric oxide synthase: function and mechanism. Adv Exp Med Biol 338 (1993) 281-284
56. Nathan C., and Xie Q.W. Regulation of biosynthesis of nitric oxide. J Biol Chem 269 (1994) 13725-13728
57. Stamler J.S. Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell 78 (1994) 931-936
58. Millar T.M., Stevens C.R., Benjamin N., Eisenthal R., Harrison R., and Blake D.R. Xanthine oxidoreductase catalyses the reduction of nitrates and nitrite to nitric oxide under hypoxic conditions. FEBS Lett 427 (1998) 225-228
59. Kuo Y.R., Wang F.S., Jeng S.F., Lutz B.S., Huang H.C., and Yang K.D. Nitrosoglutathione improves blood perfusion and flap survival by suppressing iNOS but protecting eNOS expression in the flap vessels after ischemia/reperfusion injury. Surgery 135 (2004) 437-446
60. Luo J.D., Wang Y.Y., Fu W.L., Wu J., and Chen A.F. Gene therapy of endothelial nitric oxide synthase and manganese superoxide dismutase restores delayed wound healing in type 1 diabetic mice. Circulation 110 (2004) 2484-2493
61. Crack P.J., and Taylor J.M. Reactive oxygen species and the modulation of stroke. Free Radic Biol Med 38 (2005) 1433-1444
62. Kimizuka K., Nakao A., Nalesnik M.A., Demetris A.G., Uchiyama T., Ruppert K., et al. Exogenous IL-6 inhibits acute inflammatory responses and prevents ischemia/reperfusion injury after intestinal transplantation. Am J Transplant 4 (2004) 482-494