Antioxidant mechanism of heme oxygenase-1 involves an increase in superoxide dismutase and catalase in experimental diabetes

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 289, Issue 2 58-2, 2005, Pages

  Turkseven, Saadet ^a   Kruger, Adam ^a   Mingone, Christopher J ^a   Kaminski, Pawel ^a   Inaba, Muneo ^b   Rodella, Luigi F ^c   Ikehara, Susumu ^b   Wolin, Michael S ^a   Abraham, Nader G ^a  

^a NEW YORK MEDICAL COLLEGE   (United States)

^b KANSAI MEDICAL UNIVERSITY   (Japan)

^c UNIVERSITY OF BRESCIA   (Italy)

Author keywords

Antioxidant enzymes; Endothelial dysfunction; Extracellular superoxide dismutase; Nitric oxide synthase; Oxidative stress; Superoxide

Indexed keywords

ACETYLCHOLINE; ANTIOXIDANT; CATALASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HEME OXYGENASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; MESOPORPHYRIN; SUPEROXIDE; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC ANGIOPATHY; ENDOTHELIUM CELL; ENZYME INDUCTION; IMMUNOHISTOCHEMISTRY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; VASCULAR ENDOTHELIUM;

ACETYLCHOLINE; ANIMALS; ANTIOXIDANTS; AORTA; BLOOD VESSELS; CATALASE; COBALT; DIABETES MELLITUS, EXPERIMENTAL; ENDOTHELIUM, VASCULAR; ENZYME INDUCTION; HEME OXYGENASE (DECYCLIZING); HEME OXYGENASE-1; IMMUNOHISTOCHEMISTRY; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; PROTOPORPHYRINS; RATS; RATS, SPRAGUE-DAWLEY; SUPEROXIDE DISMUTASE; SUPEROXIDES; VASODILATOR AGENTS;

EID: 23744508873     PISSN: 03636135     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpheart.00024.2005     Document Type: Article

References (55)

1. Abraham NG, Drummond GS, Lutton JD, and Kappas A. The biological significance and physiological role of heme oxygenase. Cell Physiol Biochem 6: 129-168, 1996.
2. Abraham NG, Kushida T, McClung J, Weiss M, Quan S, Lafaro R, Darzynkiewicz Z, and Wolin M. Heme oxygenase-1 attenuates glucose-mediated cell growth arrest and apoptosis in human microvessel endothelial cells. Circ Res 93: 507-514, 2003.
3. Abraham NG, Lavrovsky Y, Schwartzman ML, Stoltz RA, Levere RD, Gerritsen ME, Shibahara S, and Kappas A. Transfection of the human heme oxygenase gene into rabbit coronary microvessel endothelial cells: protective effect against heme and hemoglobin toxicity. Proc Natl Acad Sci USA 92: 6798-6802, 1995.
4. Abraham NG, Rezzani R, Rodella L, Kruger A, Taller D, Li VG, Goodman AI, and Kappas A. Overexpression of human heme oxygenase-1 attenuates endothelial cell sloughing in experimental diabetes. Am J Physiol Heart Circ Physiol 287: H2468-H2477, 2004.
5. Adachi T, Ohta H, Hirano K, Hayashi K, and Marklund SL. Non-enzymic glycation of human extracellular superoxide dismutase. Biochem J 279: 263-267, 1991.
6. Balla G, Jacob HS, Balla J, Rosenberg M, Nath K, Apple F, Easton JW, and Vercellotti GM. Ferritin: a cytoprotective antioxidant strategem of endothelium. J Biol Chem 267: 18148-18153, 1992.
7. Baynes JW. Role of oxidative stress in development of complications in diabetes. Diabetes 40: 405-412, 1991.
8. Beyer W, Imlay J, and Fridovich I. Superoxide dismutases. Prog Nucleic Acid Res Mol Biol 40: 221-253, 1991.
9. phox. J Biol Chem 276: 31105-31112, 2001.
10. Brune B and Ullrich V. Inhibition of platelet aggregation by carbon monoxide is mediated by activation of guanylate cyclase. Mol Pharmacol 32: 497-504, 1987.
11. Ceriello A, Dello RP, Amstad P, and Cerutti P. High glucose induces antioxidant enzymes in human endothelial cells in culture. Evidence linking hyperglycemia and oxidative stress. Diabetes 45: 471-477, 1996.
12. Faraci FM and Didion SP. Vascular protection: superoxide dismutase isoforms in the vessel wall. Arterioscler Thromb Vasc Biol 24: 1367-1373, 2004.
13. Fukai T, Folz RJ, Landmesser U, and Harrison DG. Extracellular superoxide dismutase and cardiovascular disease. Cardiovasc Res 55: 239-249, 2002.
14. Gupte SA, Kaminski PM, Floyd B, Agarwal R, Ali N, Ahmad M, Edwards J, and Wolin MS. Cytosolic NADPH may regulate differences in basal NOx oxidase-derived superoxide generation in bovine coronary and pulmonary arteries. Am J Physiol Heart Circ Physiol 288: H13-H21, 2005.
15. Hayashi S, Takamiya R, Yamaguchi T, Matsumoto K, Tojo SJ, Tamatani T, Kitajima M, Makino N, Ishimura Y, and Suematsu M. Induction of heme oxygenase-1 suppresses venular leukocyte adhesion elicited by oxidative stress: role of bilirubin generated by the enzyme. Circ Res 85: 663-671, 1999.
16. Ishikawa K, Navab M, Leitinger N, Fogelman AM, and Lusis AJ. Induction of heme oxygenase-1 inhibits the monocyte transmigration induced by mildly oxidized LDL. J Clin Invest 100: 1209-1216, 1997.
17. Ishizaka N, Aizawa T, Mori I, Taguchi J, Yazaki Y, Nagai R, and Ohno M. Heme oxygenase-1 is upregulated in the rat heart in response to chronic administration of angiotensin II. Am J Physiol Heart Circ Physiol 279: H672-H678, 2000.
18. Johnson RA and Freeman RH. Sustained hypertension in the rat induced by chronic blockade of nitric oxide production. Am J Hypertens 5: 919-922, 1992.
19. Kaide JI, Zhang F, Wei Y, Jiang H, Yu C, Wang WH, Balazy M, Abraham NG, and Nasjletti A. Carbon monoxide of vascular origin attenuates the sensitivity of renal arterial vessels to vasoconstrictors. J Clin Invest 107: 1163-1171, 2001.
20. Kang SW, Adler SG, Nast CC, LaPage J, Gu JL, Nadler JL, and Natarajan R. 12-Lipoxygenase is increased in glucose-stimulated mesangial cells and in experimental diabetic nephropathy. Kidney Int 59: 1354-1362, 2001.
21. Kappas A, Drummond GS, and Vallaes J. A single dose of Sn-mesoporphyrin prevents development of significant hyperbilirubinemia in glucose-6 phosphate dehydrogenase deficient newborns. Pediatrics 108: 25-30, 2001.
22. Kappas A, Simionatto CS, Drummond GS, Sassa S, and Anderson KE. The liver excretes large amounts of heme into bile when heme oxygenase is inhibited competitively by Sn-protoporphyrin. Proc Natl Acad Sci USA 82: 896-900, 1985.
23. Kossenjans W, Eis A, Sahay R, Brockman D, and Myatt L. Role of peroxynitrite in altered fetal-placental vascular reactivity in diabetes or preeclampsia. Am J Physiol Heart Circ Physiol 278: H1311-H1319, 2000.
24. Kushida T, LiVolti G, Goodman AI, and Abraham NG. TNF-α-mediated cell death is attenuated by retrovirus delivery of human heme oxygenase-1 gene into human microvessel endothelial cells. Transplant Proc 34: 2973-2978, 2002.
25. Kwak JY, Takeshige K, Cheung BS, and Minakami S. Bilirubin inhibits the activation of superoxide-producing NADPH oxidase in a neutrophil cell-free system. Biochim Biophys Acta 1076: 369-373, 1991.
26. Leffler CW, Nasjletti A, Yu C, Johnson RA, Fedinec AL, and Walker N. Carbon monoxide and cerebral microvascular tone in newborn pigs. Am J Physiol Heart Circ Physiol 276: H1641-H1646, 1999.
27. Milstien S and Katusic Z. Oxidation of tetrahydrobiopterin by peroxynitrite: implications for vascular endothelial function. Biochem Biophys Res Commun 263: 681-684, 1999.
28. Mingone CJ, Gupte SA, Iesaki T, and Wolin MS. Hypoxia enhances a cGMP-independent nitric oxide relaxing mechanism in pulmonary arteries. Am J Physiol Lung Cell Mol Physiol 285: L296-L304, 2003.
29. 2 production via NADH-derived superoxide. Am J Physiol Heart Circ Physiol 270: H1044-H1053, 1996.
30. Morita T, Perrella MA, Lee M, and Kourembanas S. Smooth muscle cell-derived carbon monoxide is a regulator of vascular cGMP. Proc Natl Acad Sci USA 92: 1475-1479, 1995.
31. Motterlini R, Foresti R, Intaglietta M, and Winslow RM. NO-mediated activation of heme oxgenase: endogenous cytoprotection against oxidative stress to endothelium. Am J Physiol Heart Circ Physiol 270: H107-H114, 1996.
32. Nishikawa Y, Stepp DW, Merkus D, Jones D, and Chilian WM. In vivo role of heme oxygenase in ischemic coronary vasodilation. Am J Physiol Heart Circ Physiol 286: H2296-H2304, 2004.
33. Otterbein LE, Kolls JK, Mantell LL, Cook JL, Alam J, and Choi AM. Exogenous administration of heme oxygenase-1 by gene transfer provides protection against hyperoxia-induced lung injury. J Clin Invest 103: 1047-1054, 1999:
34. Otterbein LE, Zuckerbraun BS, Haga M, Liu F, Song R, Usheva A, Stachulak C, Bodyak N, Smith RN, Csizmadia E, Tyagi S, Akamatsu Y, Flavell RJ, Billiar TR, Tzeng E, Bach FH, Choi AM, and Soares MP. Carbon monoxide suppresses arteriosclerotic lesions associated with chronic graft rejection and with balloon injury. Nat Med 9: 183-190, 2003.
35. Oury TD, Day BJ, and Crapo JD. Extracellular superoxide dismutase: a regulator of nitric oxide bioavailability. Lab Invest 75: 617-636, 1996.
36. Pagano PJ, Ito Y, Tornheim K, Gallop PM, Tauber AI, and Cohen RA. An NADPH oxidase superoxide-generating system in the rabbit aorta. Am J Physiol Heart Circ Physiol 268: H2274-H2280, 1995.
37. Petrache I, Otterbein LE, Alam J, Wiegand GW, and Choi AM. Heme oxygenase-1 inhibits TNF-α-induced apoptosis in cultured fibroblasts. Am J Physiol Lung Cell Mol Physiol 278: L312-L319, 2000.
38. Qadri I, Iwahashi M, Capasso JM, Hopken MW, Flores S, Schaack J, and Simon FR. Induced oxidative stress and activated expression of manganese superoxide dismutase during hepatitis C virus replication: role of JNK, p38 MAPK and AP-1. Biochem J 378: 919-928, 2004.
39. Quan S, Kaminski PM, Yang L, Morita T, Inaba M, Ikehara S, Goodman AI, Wolin MS, and Abraham NG. Heme oxygenase-1 prevents superoxide anion associated endothelial cell sloughing in diabetic rats. Biochem Biophys Res Commun 315: 509-516, 2004.
40. Quan S, Yang L, Shenouda S, Schwartzman ML, Nasjletti A, Goodman AI, and Abraham NG. Expression of human heme oxygenase-1 in the thick ascending limb attenuates angiotensin II-mediated increase in oxidative injury. Kidney Int 65: 1628-1639, 2004.
41. Rajagopalan S, Kurz S, Munzel T, Tarpey M, Freeman BA, Griendling KK, and Harrison DG. Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation. Contribution to alterations of vasomotor tone. J Clin Invest 97: 1916-1923, 1996.
42. Sano K, Nakamura H, and Matsuo T. Mode of inhibitory action of bilirubin on protein kinase C. Pediatr Res 19: 587-590, 1985.
43. Scharte M, Bone HG, Van Aken H, and Meyer J. Increased carbon monoxide in exhaled air of critically ill patients. Biochem Biophys Res Commun 267: 423-426, 2000.
44. Sedlak TW and Snyder SH. Bilirubin benefits: cellular protection by a biliverdin reductase antioxidant cycle. Pediatrics 113: 1776-1782, 2004.
45. Stocker R, McDonagh AF, Glazer AN, and Ames BN. Antioxidant activities of bile pigments: biliverdin and bilirubin. Methods Enzymol 186: 301-309, 1990.
46. Stralin P, Karlsson K, Johansson BO, and Marklund SL. The interstitium of the human arterial wall contains very large amounts of extracellular superoxide dismutase. Arterioscler Thromb Vasc Biol 15: 2032-2036, 1995.
47. 558 expression via the reduction of heme availability. J Biol Chem 279: 28681-28688, 2004.
48. Tang YL, Tang Y, Zhang YC, Qian K, Shen L, and Phillips MI. Protection from ischemic heart injury by a vigilant heme oxygenase-1 plasmid system. Hypertension 43: 746-751, 2004.
49. Vasa M, Fichtischerer S, Aicher A, Adler K, Urbich C, Martin H, Zeiher AM, and Dimmeler S. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res 89: E1-E7, 2001.
50. Ca channels in vascular smooth muscle cells. Pflügers Arch 434: 285-291, 1997.
51. Wever RM, Luscher TF, Cosentino F, and Rabelink TJ. Atherosclerosis and the two faces of endothelial nitric oxide synthase. Circulation 97: 108-112, 1998.
52. Wiesel P, Patel AP, DiFonzo N, Marria PB, Sim CU, Pellacani A, Maemura K, LeBlanc BW, Marino K, Doerschuk CM, Yet SF, Lee ME, and Perrella MA. Endotoxin-induced mortality is related to increased oxidative stress and end-organ dysfunction, not refractory hypotension, in heme oxygenase-1-deficient mice. Circulation 102: 3015-3022, 2000.
53. Wu P, Phillips MI, Bui J, and Terilliger EF. Adeno-associated viral vector mediated transgene integration in nondividing cells. J Virol 72: 5919-5926, 1998.
54. Zhang F, Kaide JI, Yang L, Jiang H, Quan S, Kemp R, Gong W, Balazy M, Abraham NG, and Nasjletti A. CO modulates the pulmonary vascular response to acute hypoxia: relation to endothelin. Am J Physiol Heart Circ Physiol 286: H137-H144, 2004.
55. 2 receptor-mediated apoptosis and adhesion molecular expression in cultured human aortic endothelial cells. Diabetes 51: 198-203, 2002.