Protective role of heme oxygenase-1 against liver damage caused by hepatic ischemia and reperfusion in rats

Antioxidants and Redox Signaling

Volumn 13, Issue 10, 2010, Pages 1503-1512

  Yun, Nari ^a   Eum, Hyun Ae ^a   Lee, Sun Mee ^a  

^a Sungkyunkwan University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; CYCLOOXYGENASE 2; GLUTATHIONE; HEME OXYGENASE 1; HEMIN; HIGH MOBILITY GROUP B1 PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; MALONALDEHYDE; MESSENGER RNA; PROTOPORPHYRIN ZINC; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; LIPID PEROXIDATION; LIVER INJURY; LIVER ISCHEMIA; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; RAT; REPERFUSION INJURY; TIME; UPREGULATION;

ANIMALS; HEME OXYGENASE-1; HEMIN; HMGB1 PROTEIN; LIPID PEROXIDATION; LIVER DISEASES; MALE; PROTOPORPHYRINS; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; RNA, MESSENGER; TIME FACTORS;

RATTUS;

EID: 77957728132     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2009.2873     Document Type: Article

References (41)

1. Alam J and Cook JL. Transcriptional regulation of the heme oxygenase-1 gene via the stress response element pathway. Curr Pharm Des 9: 2499-2511, 2003.
2. Amersi F, Buelow R, Kato H, Bibo Ke, Coito AJ, Shen XD, Zhao D, Zaky J, Melinek J, Lassman CR, Kolls JK, Alam J, Ritter T, Volk HD, Farmer DG, Ghobrial RM, Busuttil RW, and Kupiec-Weglinski JW. Upregulation of heme oxyge-nase-1 protects genetically fat Zucker rat livers from ischemia=reperfusion injury. J Clin Invest 104: 1631-1639, 1999.
3. Anderson ME. Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol 113: 548-555, 1985.
4. Applegate LA, Luscher P, and Tyrrell RM. Induction of heme oxygenase: A general response to oxidant stress in cultured mammalian cells. Cancer Res 51: 974-978, 1991.
5. Becker T, Zu Vilsendorf AM, Terbish T, Klempnauer J, and Jörns A. Induction of heme oxygenase-1 improves the survival of pancreas grafts by prevention of pancreatitis after transplantation. Transplantation 84: 1644-1655, 2007.
6. Buege JA and Aust SD. Microsomal lipid peroxidation. Methods Enzymol 52: 302-310, 1978.
7. Camhi SL, Alam J, Otterbein L, Sylvester SL, and Choi AMK. Induction of heme oxygenase-1 gene expression by lipo-polysaccharide is mediated by AP-1 activation. Am J Respir Cell Mol Biol 13: 387-398, 1995.
8. Chatterjee PK, Brown PA, Cuzzocrea S, Zacharowski K, Stewart KN, Mota-Filipe H, McDonald MC, and Thie-mermann C. Calpain inhibitor-1 reduces renal ische-mia/reperfusion injury in the rat. Kidney Int 59: 2073-2083, 2001. (Pubitemid 32467599)
9. Csiki I, Yanagisawa K, Haruki N, Nadaf S, Morrow JD, Johnson DH, and Carbone DP. Thioredoxin-1 modulates transcription of cyclooxygenase-2 via hypoxia-inducible factor-1a in non-small cell lung cancer. Cancer Res 66: 143-150, 2006.
10. Eipel C, Eisold M, Schuett H, and Vollmar B. Inhibition of heme hxygenase-1 protects against tissue injury in carbon tetrachloride exposed livers. J Surg Res 139: 113-120, 2007.
11. Fan C, Zwacka RM, and Engelhardt JF. Therapeutic approaches for ischemia/ reperfusion injury in the liver. J Mol Med 77: 577-592, 1999.
12. Gong P, Hu B, Stewart D, Ellerbe M, Figueroa YG, Blank V, Beckamn BS, and Alam J. Cobalt induces heme oxygenase-1 expression by a hypoxia-inducible factor-independent mechanism in Chinese hamster ovary cells: Regulation by Nrf2 and MafG transcription factors. J Biol Chem 276: 27018-27025, 2001.
13. Guo Y, Stein AB, Wu WJ, Tan W, Zhu X, Li QH, Dawn B, Motterlini R, and Bolli R. Administration of a CO-releasing molecule at the time of reperfusion reduces infarct size in vivo. Am J Physiol 286, H1649-H1653, 2004.
14. Horikawa S, Yoneya R, Nagashima Y, Hagiwara K, and Ozasa H. Prior induction of heme oxygenase-1 with glutathione depletor ameliorates the renal ischemia and reperfusion injury in the rat. FEBS Lett 510: 221-224, 2002. (Pubitemid 34093829)
15. Ito K, Ozasa H, Yoneya R, and Horikawa S. Splenectomy ameliorates hepatic ischemia and reperfusion injury mediated by heme oxygenase-1 induction in the rat. Liver 22: 467-473, 2002. (Pubitemid 36004284)
16. Ito K, Ozasa H, Kojima N, Miura M, Iwa T, Senoo H, and Horikawa S. Pharmacological preconditioning protects lung injury induced by intestinal ischemia/reperfusion in rat. Shock 19: 462-468, 2003.
17. Izuishi K, Tsung A, Jeyabalan G, Critchlow ND, Li J, Tracey KJ, Demarco RA, Lotze MT, Fink MP, Geller DA, and Billiar TR. Cutting edge: High-mobility group box 1 preconditioning protects against liver ischemia-reperfusion injury. J Immunol 176: 7154-7158, 2006.
18. Jaeschke H, Farhood A, and Smith CW. Neutrophils contribute to ischemia/reperfusion injury in rat liver in vivo. FASEB J 4: 3355-3359, 1990.
19. Jurgensen JS, Rosenberger C, Wiesener MS, Warnecke C, Horstrup JH, Grafe M, Philipp S, Griethe W, Maxwell PH, Frei U, Bachmann S, Willenbrock R, and Eckardt KU. Persistent induction of HIF-1alpha and \-2alpha in cardiomyo-cytes and stromal cells of ischemic myocardium. FASEB J 18: 1415-1417, 2004.
20. Kaizu T, Tamaki T, Tanaka M, Uchida Y, Tsuchihashi S, Kawamura A, and Kakita A. Preconditioning with tin-protoporphyrin IX attenuates ischemia/reperfusion injury in the rat kidney. Kidney Int 63: 1393-1403, 2003.
21. Li Volti G, Sorrenti V, Murabito P, Galvano F, Veroux M, Gullo A, Acquaviva R, Stacchiotti A, Bonomini F, Vanella L, and Di Giacomo C. Pharmacological induction of heme oxygenase-1 inhibits iNOS and oxidative stress in renal ischemia-reperfusion injury. Transplant Proc 39: 2986-2991, 2007.
22. Ljungman AG, Grum CM, Deeb GM, Bolling SF, and Morganroth ML. Inhibition of cyclooxygenase metabolite production attenuates ischemia-reperfusion lung injury. Am Rev Respir Dis 143: 610-617, 1991.
23. Maines M. Carbon monoxide and nitric oxide homology: Differential modulation of heme oxygenases in brain and detection of protein and activity. Methods Enzymol 268: 473-488, 1996.
24. Malek HA and Saleh DM. Cyclooxygenase-2 inhibitor cel-ecoxib in a rat model of hindlimb ischemia reperfusion. Can J Physiol Pharmacol 87: 353-359, 2009.
25. Radi R, Beckman JS, Bush KM, and Freeman BA. Perox-ynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide. J Biol Chem 266: 4244-4250, 1991.
26. Ryter SW and Choi AM. Therapeutic applications of carbon monoxide in lung disease. Curr Opin Pharmacol 6: 257-262, 2006.
27. Ryter SW, Morse D, and Choi AM. Carbon monoxide and bilirubin: Potential therapies for pulmonary=vascular injury and disease. Am J Respir Cell Mol Biol 36: 175-182, 2007.
28. Scott JR, Cukiernik MA, Ott MC, Bihari A, Badhwar A, Gray DK, Harris KA, Parry NG, and Potter RF. Low-dose inhaled carbon monoxide attenuates the remote intestinal inflammatory response elicited by hindlimb ischemia-reperfusion. Am J Physiol 296: G9-G14, 2009.
29. Serracino-Inglott F, Habib NA, and Mathie RT. Hepatic is-chemia-reperfusion injury. Am J Surg 181: 160-166, 2001.
30. Srisook K and Cha YN. Biphasic induction of heme oxyge-nase-1 expression in macrophages stimulated with lipo-polysaccharide. Biochem Pharmacol 68: 1709-1720, 2004.
31. Suh GY, Jin Y, Yi AK, Wang XM, and Choi AM. CCAAT= enhancer-binding protein mediates carbon monoxide-induced suppression of cyclooxygenase-2. Am J Respir Cell Mol Biol 35: 220-226, 2006.
32. Suttner DM and Dennery PA. Reversal of HO-1 related cy-toprotection with increased expression is due to reactive iron. FASEB J 13: 1800-1809, 1999.
33. Suttner DM, Sridhar K, Lee CS, Tomura T, Hansen TN, and Dennery PA. Protective effects of transient HO-1 over-expression on susceptibility to oxygen toxicity in lung cells. Am J Physiol 276: L443-L451, 1999.
34. Tanaka Y, Maher JM, Chen C, and Klaassen CD. Hepatic ischemia-reperfusion induces renal heme oxygenase-1 via NF-E2-Related Factor 2 in rats and mice. Mol Pharmacol 71: 817-825, 2007.
35. Toda N, Takahashi T, Mizobuchi S, Fujii H, Nakahira K, Takahashi S, Yamashita M, Morita K, Hirakawa M, and Akagi R. Tin chloride pretreatment prevents renal injury in rats with ischemic acute renal failure. Crit Care Med 30: 1512-1522, 2002.
36. Tsoyi K, Lee TY, Lee YS, Kim HJ, Seo HG, Lee JH, and Chang KC. Heme-oxygenase-1 induction and carbon monoxide-releasing molecule inhibit lipopolysaccharide (LPS)-induced high-mobility group box 1 release in vitro and improve survival of mice in LPS-and cecal ligation and puncture-induced sepsis model in vivo. Mol Pharmacol 76: 173-182, 2009.
37. Tsung A, Sahai R, Tanaka H, Nakao A, Fink MP, Lotze MT, Yang H, Li J, Tracey KJ, Geller DA, and Billiar TR. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med 201: 1135-1143, 2005.
38. Tsung A, Klune JR, Zhang X, Jeyabalan G, Cao Z, Peng X, Stolz DB, Geller DA, Rosengart MR, and Billiar TR. HMGB1 release induced by liver ischemia involves Toll-like receptor 4 dependent reactive oxygen species production and calcium-mediated signaling. J Exp Med 204: 2913-2923, 2007.
39. Xue H, Guo H, Li YC, and Hao ZM. Heme oxygenase-1 induction by hemin protects liver cells from ischemia=reperfusion injury in cirrhotic rats. World J Gastroenterol 13: 5384-5390, 2007.
40. Yet SF, Pellacani A, Patterson C, Tan L, Folta SC, Foster L, Lee WS, Hsieh CM, and Perrella MA. Induction of heme oxygenase-1 expression in vascular smooth muscle cells. A link to endotoxic shock. J Biol Chem 272: 4295-4301, 1997.
41. Zhong Z, Ramshesh VK, Rehman H, Currin RT, Sridharan V, Theruvath TP, Kim I, Wright GL, and Lemasters JJ. Activation of the oxygen-sensing signal cascade prevents mi-tochondrial injury after mouse liver ischemia-reperfusion. Am J Physiol 295: G823-G832, 2008.