Biphasic elevation of bilirubin oxidation during myocardial ischemia reperfusion

Circulation Journal

Volumn 72, Issue 9, 2008, Pages 1520-1527

  Yamamoto, Masaki ^a   Maeda, Hironori ^a   Hirose, Nobuyuki ^a   Yamamoto, Morio ^a   Nakagawa, Aimi ^a   Radhakrishnan, Geethalakshmi ^a   Gopalrao, Rajesh Katare ^a   Sato, Takayuki ^a   Yamaguchi, Tokio ^b   Sasaguri, Shiro ^a  

^a KOCHI MEDICAL SCHOOL   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

Bilirubin; Biopyrrin; Myocardial ischemia reperfusion injury; Nitric oxide; Oxidative stress

Indexed keywords

BILIRUBIN; BIOPYRRIN; DRUG METABOLITE; NITRIC OXIDE SYNTHASE INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLINICAL ASSESSMENT; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL RAT; HEART HEMODYNAMICS; HEART LEFT VENTRICLE ENDDIASTOLIC PRESSURE; HEART MUSCLE ISCHEMIA; IMMUNOHISTOCHEMISTRY; LEFT CORONARY ARTERY; LUNG HEMODYNAMICS; MALE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; REPERFUSION INJURY; UPREGULATION; URINARY EXCRETION;

ANIMALS; BILIRUBIN; BIOLOGICAL MARKERS; DIPYRONE; ENZYME INHIBITORS; LUNG; MALE; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; OXIDATION-REDUCTION; OXIDATIVE STRESS; RATS; TIME FACTORS;

EID: 50449097049     PISSN: 13469843     EISSN: 13474820     Source Type: Journal    
DOI: 10.1253/circj.CJ-07-1079     Document Type: Article

References (43)

1. Tsujita K, Shimomura H, Kaikita K, Kawano H, Hokamaki J, Nagayoshi Y, et al. Long-term efficacy of edaravone in patients with acute myocardial infarction. Circ J 2006; 70: 832-837.
2. Park JL, Lucchesi BR. Mechanisms of myocardial reperfusion injury. Ann Thorac Surg 1999; 68: 1905-1912.
3. Venardos KM, Kaye DM. Myocardial ischemia-reperfusion injury, antioxidant enzyme systems, and selenium: A review. Curr Med Chem 2007; 14: 1539-1549.
4. Kinugasa Y, Ogino K, Furuse Y, Shiomi T, Tsutsui H, Yamamoto T, et al. Allopurinol improves cardiac dysfunction after ischemia-reperfusion via reduction of oxidative stress in isolated perfused rat hearts. Circ J 2003; 67: 781-787.
5. Zweier JL, Talukder MA. The role of oxidants and free radicals in reperfusion injury. Cardiovasc Res 2006; 70: 181-190.
6. Rajesh KG, Sasaguri S, Suzuki R, Maeda H. Antioxidant MCI-186 inhibits mitochondrial permeability transition pore and upregulates Bcl-2 expression. Am J Physiol Heart Circ Physiol 2003; 285: H2171-H2178.
7. Liu P, Hock CE, Nagele R, Wong PY. Formation of nitric oxide, superoxide, and peroxynitrite in myocardial ischemia-reperfusion injury in rats. Am J Physiol 1997; 272: H2327-H2336.
8. Tao L, Gao E, Jiao X, Yuan Y, Li S, Christopher TA, et al. Adiponectin cardioprotection after myocardial ischemia/reperfusion involves the reduction of oxidative/nitrative stress. Circulation 2007; 115: 1408-1416.
9. Kim YM, Bombeck CA, Billiar TR. Nitric oxide as a bifunctional regulator of apoptosis. Circ Res 1999; 84: 253-256.
10. Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: The good, the bad, and ugly. Am J Physiol 1996; 271: C1424-C1437.
11. Harada N, Miura T, Dairaku Y, Kametani R, Shibuya M, Wang R, et al. NO donor-activated PKC-delta plays a pivotal role in ischemic myocardial protection through accelerated opening of mitochondrial K-ATP channels. J Cardiovasc Pharmacol 2004; 44: 35-41.
12. Jugdutt BI. Nitric oxide and cardioprotection during ischemia- reperfusion. Heart Fail Rev 2002; 7: 391-405.
13. Hayasaki T, Kaikita K, Okuma T, Yamamoto E, Kuziel WA, Ogawa H, et al. CC chemokine receptor-2 deficiency attenuates oxidative stress and infarct size caused by myocardial ischemia-reperfusion in mice. Circ J 2006; 70: 342-351.
14. Schulz R, Wambolt R. Inhibition of nitric oxide synthesis protects the isolated working rabbit heart from ischaemia-reperfusion injury. Cardiovasc Res 1995; 30: 432-439.
15. Mori E, Haramaki N, Ikeda H, Imaizumi T. Intra-coronary administration of L-arginine aggravates myocardial stunning through production of peroxynitrite in dogs. Cardiovasc Res 1998; 40: 113-123.
16. Kanno S, Lee PC, Zhang Y, Ho C, Griffith BP, Shears LL 2nd, et al. Attenuation of myocardial ischemia/reperfusion injury by superinduction of inducible nitric oxide synthase. Circulation 2000; 101: 2742-2748.
17. Thirunavukkarasu M, Penumathsa SV, Koneru S, Juhasz B, Zhan L, Otani H, et al. Resveratrol alleviates cardiac dysfunction in streptozotocin-induced diabetes: Role of nitric oxide, thioredoxin, and heme oxygenase. Free Radic Biol Med 2007; 43: 720-729.
18. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN. Bilirubin is an antioxidant of possible physiological importance. Science 1987; 235: 1043-1046.
19. Minetti M, Mallozzi C, Di Stasi AM, Pietraforte D. Bilirubin is an effective antioxidant of peroxynitrite-mediated protein oxidation in human blood plasma. Arch Biochem Biophys 1998; 352: 165-174.
20. Kaur H, Hughes MN, Green CJ, Naughton P, Foresti R, Motterlini R. Interaction of bilirubin and biliverdin with reactive nitrogen species. FEBS Lett 2003; 543: 113-119.
21. Kapitulnik J. Bilirubin: An endogenous product of heme degradation with both cytotoxic and cytoprotective properties. Mol Pharmacol 2004; 66: 773-779.
22. Ockaili R, Natarajan R, Salloum F, Fisher BJ, Jones D, Fowler AA 3rd, et al. HIF-1 activation attenuates postischemic myocardial injury: Role for heme oxygenase-1 in modulating microvascular chemokine generation. Am J Physiol Heart Circ Physiol 2005; 289: H542-H548.
23. Clark JE, Foresti R, Green CJ, Motterlini R. Dynamics of haem oxygenase-1 expression and bilirubin production in cellular protection against oxidative stress. Biochem J 2000; 348: 615-619.
24. Clark JE, Foresti R, Sarathchandra P, Kaur H, Green CJ, Motterlini R. Heme oxygenase-1-derived bilirubin ameliorates postischemic myocardial dysfunction. Am J Physiol Heart Circ Physiol 2000; 278: H643-H651.
25. Yamamoto M, Maeda H, Hirose N, Radhakrishnan G, Katare RG, Hayashi Y, et al. Bilirubin oxidation provoked by nitric oxide radicals predicts the progression of acute cardiac allograft rejection. Am J Transplant 2007; 7: 1897-1906.
26. Yet SF, Tian R, Layne MD, Wang ZY, Maemura K, Solovyeva M, et al. Cardiac-specific expression of heme oxygenase-1 protects against ischemia and reperfusion injury in transgenic mice. Circ Res 2001; 89: 168-173.
27. Naughton P, Hoque M, Green CJ, Foresti R, Motterlini R. Interaction of heme with nitroxyl or nitric oxide amplifies heme oxygenase-1 induction: Involvement of the transcription factor Nrf2. Cell Mol Biol (Noisy-le-grand) 2002; 48: 885-894.
28. Hangaishi M, Ishizaka N, Aizawa T, Kurihara Y, Taguchi J, Nagai R, et al. Induction of heme oxygenase-1 can act protectively against cardiac ischemia/reperfusion in vivo. Biochem Biophys Res Commun 2000; 279: 582-588.
29. Vulapalli SR, Chen Z, Chua BH, Wang T, Liang CS. Cardioselective overexpression of HO-1 prevents I/R-induced cardiac dysfunction and apoptosis. Am J Physiol Heart Circ Physiol 2002; 283: H688-H694.
30. Yamaguchi T, Shioji I, Sugimoto A, Komoda Y, Nakajima H. Chemical structure of a new family of bile pigments from human urine. J Biochem (Tokyo) 1994; 116: 298-303.
31. Yamaguchi T, Shioji I, Sugimoto A, Komoda Y, Nakajima H. Epitope of 24G7 anti-bilirubin monoclonal antibody. Biochim Biophys Acta 1996; 1289: 110-114.
32. Yamaguchi T, Terakado M, Horio F, Aoki K, Tanaka M, Nakajima H. Role of bilirubin as an antioxidant in an ischemia-reperfusion of rat liver and induction of heme oxygenase. Biochem Biophys Res Commun 1996; 223: 129-135.
33. Morita Y, Takahashi H, Kamihata H, Yamamoto Y, Hara K, Iwasaka T. Urinary excretion of biopyrrins, oxidative metabolites of bilirubin, increases after spasm provocation tests in patients with coronary spastic angina. Int J Cardiol 2001; 80: 243-250.
34. Shimomura H, Ogawa H, Takazoe K, Soejima H, Miyamoto S, Sakamoto T, et al. Comparison of urinary biopyrrin levels in acute myocardial infarction (after reperfusion therapy) versus stable angina pectoris and their usefulness in predicting subsequent cardiac events. Am J Cardiol 2002; 90: 108-111.
35. Hokamaki J, Kawano H, Yoshimura M, Soejima H, Miyamoto S, Kajiwara I, et al. Urinary biopyrrins levels are elevated in relation to severity of heart failure. J Am Coll Cardiol 2004; 43: 1880-1885.
36. Yamaguchi T, Hashizume T, Tanaka M, Nakayama M, Sugimoto A, Ikeda S, et al. Bilirubin oxidation provoked by endotoxin treatment is suppressed by feeding ascorbic acid in a rat mutant unable to synthesize ascorbic acid. Eur J Biochem 1997; 245: 233-240.
37. Yamaguchi T, Shioji I, Sugimoto A, Yamaoka M. Psychological stress increases bilirubin metabolites in human urine. Biochem Biophys Res Commun 2002; 293: 517-520.
38. Miyashita T, Yamaguchi T, Motoyama K, Unno K, Nakano Y, Shimoi K. Social stress increases biopyrrins, oxidative metabolites of bilirubin, in mouse urine. Biochem Biophys Res Commun 2006; 349: 775-780.
39. Mayer BX, Mensik C, Krishnaswami S, Derendorf H, Eichler HG, Schmetterer L, et al. Pharmacokinetic-pharmacodynamic profile of systemic nitric oxide-synthase inhibition with L-NMMA in humans. Br J Clin Pharmacol 1999; 47: 539-544.
40. Huang SS, Wei FC, Hung LM. Ischemic preconditioning attenuates postischemic leukocyte-endothelial cell interactions: Role of nitric oxide and protein kinase C. Circ J 2006; 70: 1070-1075.
41. Bhatia M, Moochhala S. Role of inflammatory mediators in the pathophysiology of acute respiratory distress syndrome. J Pathol 2004; 202: 145-156.
42. Hale SL, Leeka JA, Kloner RA. Improved left ventricular function and reduced necrosis after myocardial ischemia/reperfusion in rabbits treated with ranolazine, an inhibitor of the late sodium channel. J Pharmacol Exp Ther 2006; 318: 418-423.
43. Dodd-o JM, Welsh LE, Salazar JD, Walinsky PL, Peck EA, Shake JG, et al. Effect of NADPH oxidase inhibition on cardiopulmonary bypass-induced lung injury. Am J Physiol Heart Circ Physiol 2004; 287: H927-H936.