Cytoprotective role of heme oxygenase-1 and heme degradation derived end products in liver injury

World Journal of Hepatology

Volumn 5, Issue 10, 2013, Pages 541-549

  Origassa, Clarice Silvia Taemi ^a   Câmara, Niels Olsen Saraiva ^b  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Bilirubin; Heme oxygenases; Hepatitis C; Hypoxia; Immunoregulatory; Kupffer cells; Liver ischemia; Polymorphisms

Indexed keywords

EID: 84887329607     PISSN: None     EISSN: 19485182     Source Type: Journal    
DOI: 10.4254/wjh.v5.i10.541     Document Type: Review

References (60)

1. Habtezion A, Kwan R, Yang AL, Morgan ME, Akhtar E, Wanaski SP, Collins SD, Butcher EC, Kamal A, Omary MB. Heme oxygenase-1 is induced in peripheral blood mononuclear cells of patients with acute pancreatitis: a potential therapeutic target. Am J Physiol Gastrointest Liver Physiol 2011; 300: G12-G20 [PMID: 20966033 DOI: 10.1152/ajpgi.00231.2010 3025514]
2. Abdureyim S, Amat N, Umar A, Upur H, Berke B, Moore N. Anti-inflammatory, immunomodulatory, and heme oxygenase-1 inhibitory activities of ravan napas, a formulation of uighur traditional medicine, in a rat model of allergic asthma. Evid Based Complement Alternat Med 2011; 2011: pii: 725926 [PMID: 20953388 DOI: 10.1155/2011/725926]
3. Ozawa E, Abiru S, Nagaoka S, Yano K, Komori A, Migita K, Yatsuhashi H, Taura N, Ichikawa T, Ishibashi H, Nakao K. Ferritin/alanine aminotransferase ratio as a possible marker for predicting the prognosis of acute liver injury. J Gastroenterol Hepatol 2011; 26: 1326-1332 [PMID: 21501222 DOI: 10.1111/j.1440-1746.2011.06743.x]
4. Immenschuh S, Baumgart-Vogt E, Mueller S. Heme oxygenase-1 and iron in liver inflammation: a complex alliance. Curr Drug Targets 2010; 11: 1541-1550 [PMID: 20704547 DOI: 10.2174/1389450111009011541]
5. Brockmann JG, August C, Wolters HH, Homme R, Palmes D, Baba H, Spiegel HU, Dietl KH. Sequence of reperfusion influences ischemia/reperfusion injury and primary graft function following porcine liver transplantation. Liver Transpl 2005; 11: 1214-1222 [DOI: 10.1002/lt.20480]
6. Waltz P, Carchman EH, Young AC, Rao J, Rosengart MR, Kaczorowski D, Zuckerbraun BS. Lipopolysaccaride induces autophagic signaling in macrophages via a TLR4, heme oxygenase-1 dependent pathway. Autophagy 2011; 7: 315-320 [PMID:21307647 DOI: 10.4161/auto.7.3.14044]
7. Gu Q, Wu Q, Jin M, Xiao Y, Xu J, Mao C, Zhao F, Zhang Y, Zhang Y. Heme oxygenase-1 alleviates mouse hepatic failure through suppression of adaptive immune responses. J Pharmacol Exp Ther 2012; 340: 2-10 [PMID: 21946119 DOI: 10.1124/jpet.111.186551]
8. Choi JH, Kim DW, Yun N, Choi JS, Islam MN, Kim YS, Lee SM. Protective effects of hyperoside against carbon tetrachloride-induced liver damage in mice. J Nat Prod 2011; 74: 1055-1060 [PMID: 21428416 DOI: 10.1021/np200001x]
9. Eipel C, Hirschmann M, Abshagen K, Menger MD, Vollmar B. Local interaction of apoptotic hepatocytes and Kupffer cells in a rat model of systemic endotoxemia. Hepatol Res 2007; 37: 863-871 [PMID: 17573953 DOI: 10.1111/j.1872-034X.2007.00133.x]
10. Villarroel P, Flores S, Pizarro F, de Romana DL, Arredondo M. Effect of dietary protein on heme iron uptake by Caco-2 cells. Eur J Nutr 2011; 50: 637-643 [DOI: 10.1007/s00394-011-0173-8]
11. Liu S, Hou W, Yao P, Li N, Zhang B, Hao L, Nussler AK, Liu L. Heme oxygenase-1 mediates the protective role of quercetin against ethanol-induced rat hepatocytes oxidative damage. Toxicol In Vitro 2012; 26: 74-80 [PMID: 22056766 DOI: 10.1016/j.tiv.2011.10.013]
12. Bai CH, Chen JR, Chiu HC, Chou CC, Chau LY, Pan WH. (2010). Shorter GT repeat polymorphism in the heme oxygenase-1 gene promoter has protective effect on ischemic stroke in dyslipidemia patients. J Biomed Sci 2010; 17: 12 [PMID: 20175935 DOI: 10.1186/1423-0127-17-12 2841098]
13. Yamada N, Yamaya M, Okinaga S, Nakayama K, Sekizawa K, Shibahara S, Sasaki H. Microsatellite polymorphism in the heme oxygenase-1 gene promoter is associated with susceptibility to emphysema. Am J Hum Genet 2000; 66: 187-195 [DOI: 10.1086/302729 1288325]
14. D'Silva S, Borse V, Colah RB, Ghosh K, Mukherjee MB. Association of (GT)n repeats promoter polymorphism of heme oxygenase-1 gene with serum bilirubin levels in healthy Indian adults. Genet Test Mol Biomarkers 2011; 15: 215-218 [PMID: 21198350 DOI: 10.1089/gtmb.2010.0132]
15. Abate A, Yang G, Wong RJ, Schroder H, Stevenson DK, Dennery PA. Apigenin decreases hemin-mediated heme oxygenase-1 induction. Free Radic Biol Med 2005; 39: 711-718 [PMID: 16109301]
16. Siasi E, Aleyasin A, Mowla SJ, Sahebkashaf H. Study of GTrepeat expansion in Heme oxygenase-1 gene promoter as genetic cause of male infertility. J Assist Reprod Genet 2011; 28: 737-741 [PMID: 21556890 DOI: 10.1007/s10815-011-9574-03170113]
17. Bozkaya OG, Kumral A, Yesilirmak DC, Ulgenalp A, Duman N, Ercal D, Ozkan H. Prolonged unconjugated hyperbilirubinaemia associated with the haem oxygenase-1 gene promoter polymorphism. Acta Paediatr 2010; 99: 679-683 [PMID: 20121710 DOI: 10.1111/j.1651-2227.2009.01678.x]
18. Taha H, Grochot-Przeczek A, Was H, Kotlinowski J, Kozakowska M, Marek A, Skrzypek K, Lackowska B, Balcerczyk A, Mustafa S, Dulak J, Jozkowicz A. Modulation of inflammatory response by pentoxifylline is independent of heme oxygenase-1 pathway. J Physiol Pharmacol 2009; 60: 3-12 [PMID: 19617639]
19. Hsu M, Muchova L, Morioka I, Wong RJ, Schroder H, Stevenson DK. Tissue-specific effects of statins on the expression of heme oxygenase-1 in vivo. Biochem Biophys Res Commun 2006; 343: 738-744 [PMID:16563347 DOI: 10.1016/j.bbrc.2006.03.036]
20. Jozkowicz A, Huk I, Nigisch A, Weigel G, Dietrich W, Motterlini R, Dulak J. Heme oxygenase and angiogenic activity of endothelial cells: stimulation by carbon monoxide and inhibition by tin protoporphyrin-IX. Antioxid Redox Signal 2003; 5: 155-162 [PMID: 12716475 DOI: 10.1089/152308603764816514]
21. Drechsler Y, Dolganiuc A, Norkina O, Romics L, Li W, Kodys K, Bach FH, Mandrekar P, Szabo G. Heme oxygenase-1 mediates the anti-inflammatory effects of acute alcohol on IL-10 induction involving p38 MAPK activation in monocytes. J Immunol 2006; 177: 2592-2600 [PMID: 16888021]
22. Kawakami T, Takahashi T, Shimizu H, Nakahira K, Takeuchi M, Katayama H, Yokoyama M, Morita K, Akagi R, Sassa S. Highly liver-specific heme oxygenase-1 induction by interleukin-11 prevents carbon tetrachloride-induced hepatotoxicity. Int J Mol Med 2006; 18: 537-546 [PMID: 16964402]
23. Hosick PA, Stec DE. Heme oxygenase, a novel target for the treatment of hypertension and obesity? Am J Physiol Regul Integr Comp Physiol 2012; 302: R207-R214 [PMID: 22071158 DOI: 10.1152/ajpregu.00517.2011 3349392]
24. Ishikawa M, Numazawa S, Yoshida T. Redox regulation of the transcriptional repressor Bach1. Free Radic Biol Med 2005; 38: 1344-1352 [DOI: 10.1016/j.freeradbiomed.2005.01.021]
25. George JF, Braun A, Brusko TM, Joseph R, Bolisetty S, Wasserfall CH, Atkinson MA, Agarwal A, Kapturczak MH. Suppression by CD4 CD25 regulatory T cells is dependent on expression of heme oxygenase-1 in antigen-presenting cells. Am J Pathol 2008; 173: 154-160 [PMID: 18511516 DOI: 10.2353/ajpath.2008.070963 2438293]
26. Hammerich L, Heymann F, Tacke F. Role of IL-17 and Th17 cells in liver diseases. Clin Dev Immunol 2011; 2011: 345803 [PMID: 21197451 DOI: 10.1155/2011/345803 3010664]
27. Durum SK, Mazzucchelli RI. Live from the liver: hepatocyte IL-7. Immunity 2009; 30: 320-321 [PMID: 19303385 DOI: 10.1016/j.immuni.2009.03.001]
28. Bresgen N, Jaksch H, Lacher H, Ohlenschlager I, Uchida K, Eckl PM. Iron-mediated oxidative stress plays an essential role in ferritin-induced cell death. Free Radic Biol Med 2010; 48: 1347-1357 [PMID: 20172024 DOI: 10.1016/j.freeradbiome d.2010.02.019]
29. Johnson GB, Brunn GJ, Tang AH, Platt JL. Evolutionary clues to the functions of the Toll-like family as surveillance receptors. Trends Immunol 2003; 24: 19-24 [PMID: 12495720 DOI: 10.1016/S1471-4906(02)00014-5]
30. Tzima S, Victoratos P, Kranidioti K, Alexiou M, Kollias G. Myeloid heme oxygenase-1 regulates innate immunity and autoimmunity by modulating IFN-beta production. J Exp Med 2009; 206: 1167-1179 [PMID: 19398754 DOI: 10.1084/jem.20081582 2715044]
31. Shen XD, Ke B, Zhai Y, Gao F, Tsuchihashi S, Lassman CR, Busuttil RW, Kupiec-Weglinski JW. Absence of toll-like receptor 4 (TLR4) signaling in the donor organ reduces ischemia and reperfusion injury in a murine liver transplantation model. Liver Transpl 2007; 13: 1435-1443 [PMID: 17902130 DOI: 10.1002/lt.21251]
32. Bonnell MR, Visner GA, Zander DS, Mandalapu S, Kazemfar K, Spears L, Beaver TM. Heme-oxygenase-1 expression correlates with severity of acute cellular rejection in lung transplantation. J Am Coll Surg 2004; 198: 945-952 [PMID: 15194077 DOI: 10.1016/j.jamcollsurg.2004.01.026]
33. Abshagen K, Eipel C, KalffJC, Menger MD, Vollmar B. Kupffer cells are mandatory for adequate liver regeneration by mediating hyperperfusion via modulation of vasoactive proteins. Microcirculation 2008; 15: 37-47 [PMID: 17952799 DOI: 10.1080/10739680701412989]
34. Boonprasert K, Ruengweerayut R, Satarug S, Na-Bangchang, K. Study on the association between environmental cadmium exposure, cytochrome P450-mediated 20-HETE, hemeoxygenase-1 polymorphism and hypertension in Thai population residing in a malaria endemic areas with cadmium pollution. Environ Toxicol Pharmacol 2011; 31: 416-426 [PMID: 21787712 DOI: 10.1016/j.etap.2011.02.003]
35. Järveläinen HA, Fang C, Ingelman-Sundberg M, Lukkari TA, Sippel H, Lindros KO. Kupffer cell inactivation alleviates ethanol-induced steatosis and CYP2E1 induction but not inflammatory responses in rat liver. J Hepatol 2000; 32: 900-910 [PMID: 10898310]
36. Arredondo M, Fuentes M, Jorquera D, Candia V, Carrasco E, Leiva E, Mujica V, Hertrampf E, Perez, F. Cross-talk between body iron stores and diabetes: iron stores are associated with activity and microsatellite polymorphism of the heme oxygenase and type 2 diabetes. Biol Trace Elem Res 2011; 143: 625-636 [DOI: 10.1007/s12011-010-8895-7]
37. Buis CI, van der Steege G, Visser DS, Nolte IM, Hepkema BG, Nijsten M, SlooffMJ, Porte R J. Heme oxygenase-1 genotype of the donor is associated with graft survival after liver transplantation. Am J Transplant 2008; 8: 377-385 [DOI: 10.1111/j.1600-6143.2007.02048.x]
38. Shan Y, Lambrecht RW, Ghaziani T, Donohue SE, Bonkovsky HL. Role of Bach-1 in regulation of heme oxygenase-1 in human liver cells: insights from studies with small interfering RNAS. J Biol Chem 2004; 279: 51769-51774 [PMID: 15465821 DOI: 10.1074/jbc. M409463200]
39. Li J, Gao J, Yan D, Yuan Y, Sah S, Satyal U, Liu M, Han W, Yu Y. Neutralization of chemokine CXCL14 (BRAK) expression reduces CCl4 induced liver injury and steatosis in mice. Eur J Pharmacol 2011; 671: 120-127 [PMID: 21978833 DOI: 10.1016/j.ejphar.2011.09.174]
40. Wang F, Duan ZJ, Sun YJ. Influence of heme oxygenase-1 expression on immune liver fibrosis induced by cobalt protoporphyrin in rats. World J Gastroenterol 2009; 15: 3009-3014 [PMID: 19554654 DOI: 10.3748/wjg.15.3009]
41. Sun L, Shi T, Qiao H, Jiang X, Jiang H, Krissansen GW, Sun X. Hepatic overexpression of heme oxygenase-1 improves liver allograft survival by expanding T regulatory cells. J Surg Res 2011; 166: e187-e194 [PMID: 21227452 DOI: 10.1016/j.jss.2010.11.917]
42. Javanmard SH, Keyhanian K, Loghmani P, Samety AA, Haghdoost F, Rafiei L, Talaei M, Asgari S, Jazi MH, Sarrafzadegan N. Association between heme oxygenase-1 gene promoter polymorphisms and metabolic syndrome in Iranians. Mol Biol Rep 2012; 39: 3355-3360 [DOI: 10.1007/s11033-011-1105-7]
43. Cao J, Li L, Chen C, Zeng LY, Li ZY, Pan XY, Xu KL. [Influence of mouse genetic engineering regulatory T cells infusion on post-allogeneic bone marrow transplantation acute graft-versus-host disease in mice]. Zhonghua Xueyexue Zazhi 2011; 32: 83-88 [PMID: 21429372]
44. Shen XD, Ke B, Zhai Y, Gao F, Busuttil RW, Cheng G, Kupiec-Weglinski JW. Toll-like receptor and heme oxygenase-1 signaling in hepatic ischemia/reperfusion injury. Am J Transplant 2005; 5: 1793-1800 [DOI: 10.1111/j.1600-6143.2005.00932.x]
45. Carchman EH, Rao J, Loughran PA, Rosengart MR, Zuckerbraun BS. Heme oxygenase-1-mediated autophagy protects against hepatocyte cell death and hepatic injury from infection/sepsis in mice. Hepatology 2011; 53: 2053-2062 [DOI: 10.1002/hep.24324]
46. Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, Wang Y, Hood L, Zhu Z, Tian Q, Dong C. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 2005; 6: 1133-1141 [DOI: 10.1038/ni1261 1618871]
47. Smyk-Pearson S, Golden-Mason L, Klarquist J, Burton JR, Jr Tester IA, Wang CC, Culbertson N, Vandenbar, AA, Rosen HR. Functional suppression by FoxP3 CD4 CD25(high) regulatory T cells during acute hepatitis C virus infection. J Infect Dis 2008; 197: 46-57 [DOI: 10.1086/523651]
48. Wu MM, Chiou HY, Lee TC, Chen CL, Hsu LI, Wang YH, Huang WL, Hsieh YC, Yang, TY, Lee CY, Yip PK, Wang CH, Hsueh YM, Chen CJ. GT-repeat polymorphism in the heme oxygenase-1 gene promoter and the risk of carotid atherosclerosis related to arsenic exposure. J Biomed Sci 2010; 17: 70 [DOI: 10.1186/1423-0127-17-70 2939596]
49. Mashreghi MF, Klemz R, Knosalla IS, Gerstmayer B, Janssen U, Buelow R, Jozkowicz A, Dulak J, Volk HD, Kotsch K. Inhibition of dendritic cell maturation and function is independent of heme oxygenase 1 but requires the activation of STAT3. J Immunol 2008; 180: 7919-7930 [PMID: 18523255]
50. Oh GS, Pae HO, Moon MK, Choi BM, Yun YG, Rim JS, Chung HT. Pentoxifylline protects L929 fibroblasts from TNF-alpha toxicity via the induction of heme oxygenase-1. Biochem Biophys Res Commun 2003; 302: 109-113 [PMID: 12593855]
51. Khanna A, Morelli AE, Zhong C, Takayama T, Lu L, Thomson AW. Effects of liver-derived dendritic cell progenitors on Th1-and Th2-like cytokine responses in vitro and in vivo. J Immunol 2000; 164: 1346-1354 [PMID: 10640749]
52. Mehrab-Mohseni M, Sendi H, Steuerwald N, Ghosh S, Schrum LW, Bonkovsky HL. Legalon-SIL downregulates HCV core and NS5A in human hepatocytes expressing fulllength HCV. World J Gastroenterol 2011; 17: 1694-1700 [DOI: 10.3748/wjg.v17.i13.1694 3072633]
53. Paine A, Eiz-Vesper B, Blasczyk R, Immenschuh S. Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential. Biochem Pharmacol 2010; 80: 1895-1903 [DOI: 10.1016/j.bcp.2010.07.014]
54. Zhu Z, Wilson AT, Mathahs MM, Wen F, Brown KE, Luxon, BA, Schmidt WN. Heme oxygenase-1 suppresses hepatitis C virus replication and increases resistance of hepatocytes to oxidant injury. Hepatology 2008; 48: 1430-1439 [DOI: 10.1002/hep.22491 2587102]
55. Richards JA, Wigmore SJ, Devey LR. Heme oxygenase system in hepatic ischemia-reperfusion injury. World J Gastroenterol 2010; 16: 6068-6078 [PMID: 21182221]
56. Kupiec-Weglinski JW, Busuttil RW. Ischemia and reperfusion injury in liver transplantation. Transplant Proc 2005; 37: 1653-1656 [DOI: 10.1016/j.transproceed.2005.03.134]
57. Kim YM, Pae HO, Park JE, Lee YC, Woo JM, Kim NH, Choi YK, Lee, BS, Kim SR, Chung HT. Heme oxygenase in the regulation of vascular biology: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 2011; 14: 137-167 [PMID:20624029 DOI: 10.1089/ars.2010.31532988629]
58. Curjuric I, Imboden M, Schindler C, Downs SH, Hersberger M, Liu SL, Matyas G, Russi EW, Schwartz J, Thun GA, Postma DS, Rochat T, Probst-Hensch NM. HMOX1 and GST variants modify attenuation of FEF25-75% decline due to PM10 reduction. Eur Respir J 2010; 35: 505-514 [PMID: 20190330 DOI: 10.1183/09031936.00044309]
59. Farombi EO, Surh YJ. Heme oxygenase-1 as a potential therapeutic target for hepatoprotection. J Biochem Mol Biol 2006; 39: 479-491 [PMID: 17002867 DOI: 10.5483/BMBRep.2006.39.5.479]
60. Courtney AE, Maxwell AP. Heme oxygenase 1: does it have a role in renal cytoprotection? Am J Kidney Dis 2008; 51: 678-690 [PMID:18371544 DOI: 10.1053/j.ajkd.2007.11.033]