Impaired autophagy contributes to hepatocellular damage during ischemia/reperfusion: Heme oxygenase-1 as a possible regulator

Free Radical Biology and Medicine

Volumn 68, Issue , 2014, Pages 168-177

  Yun, Nari ^a   Cho, Hong Ik ^a   Lee, Sun Mee ^a  

^a Sungkyunkwan University   (South Korea)

Author keywords

Autophagy; Calpains; Carbon monoxide; Heme oxygenase 1; Liver ischemia reperfusion

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; BECLIN 1; CALPAIN 1; CALPAIN 2; CASPASE 3; HEME OXYGENASE 1; MAMMALIAN TARGET OF RAPAMYCIN; MICROTUBULE ASSOCIATED PROTEIN 1;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL MODEL; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; AUTOPHAGY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; IN VITRO STUDY; LIGHT CHAIN; LIVER CELL; LIVER CELL DAMAGE; LIVER ISCHEMIA; LIVER NECROSIS; MALE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RAT; REPERFUSION INJURY; SYSTEMATIC REVIEW; TRANSMISSION ELECTRON MICROSCOPY;

AUTOPHAGY; CALPAINS; CARBON MONOXIDE; HEME OXYGENASE-1; LIVER ISCHEMIA/REPERFUSION;

ANIMALS; APOPTOSIS; AUTOPHAGY; CYTOPROTECTION; HEME OXYGENASE-1; HEPATOCYTES; LIVER; MEMBRANE PROTEINS; OXIDATIVE STRESS; RATS; REACTIVE OXYGEN SPECIES; REPERFUSION INJURY;

EID: 84891802277     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.12.014     Document Type: Article

References (44)

1. J. Cardinal, P. Pan, and A. Tsung Protective role of cisplatin in ischemic liver injury through induction of autophagy Autophagy 5 2009 1211 1212
2. A. Tsung, J.R. Klune, X. Zhang, G. Jeyabalan, Z. Cao, X. Peng, D.B. Stolz, D.A. Geller, M.R. Rosengart, and T.R. Billiar HMGB1 release induced by liver ischemia involves Toll-like receptor 4 dependent reactive oxygen species production and calcium-mediated signaling J. Exp. Med. 204 2007 2913 2923
3. C. He, and D.J. Klionsky Regulation mechanisms and signaling pathways of autophagy Annu. Rev. Genet. 43 2009 67 93
4. R.H. Bhogal, C.J. Weston, S.M. Curbishley, D.H. Adams, and S.C. Afford Autophagy: a cyto-protective mechanism which prevents primary human hepatocyte apoptosis during oxidative stress Autophagy 8 2012 545 558
5. S. Bolisetty, A.M. Traylor, J. Kim, R. Joseph, K. Ricart, A. Landar, and A. Agarwal Heme oxygenase-1 inhibits renal tubular macroautophagy in acute kidney injury J. Am. Soc. Nephrol. 21 2010 1702 1712
6. B. Levine, and J. Yuan Autophagy in cell death: an innocent convict? J. Clin. Invest. 115 2005 2679 2688
7. G. Kroemer, and B. Levine Autophagic cell death: the story of a misnomer Nat. Rev. Mol. Cell. Biol. 9 2008 1004 1010
8. T. Shintani, and D.J. Klionsky Autophagy in health and disease: a double-edged sword Science 306 2004 990 995
9. J. Huang, G.Y. Lam, and J.H. Brumell Autophagy signaling through reactive oxygen species Antioxid. Redox Signal. 14 2011 2215 2231
10. J. Sadoshima The role of autophagy during ischemia/reperfusion Autophagy 4 2008 402 403
11. J.S. Kim, T. Nitta, D. Mohuczy, K.A. O'Malley, L.L. Moldawer, W.A. Dunn Jr, and K.E. Behrns Impaired autophagy: a mechanism of mitochondrial dysfunction in anoxic rat hepatocytes Hepatology 47 2008 1725 1736
12. J.H. Wang, I.S. Ahn, T.D. Fischer, J.I. Byeon, W.A. Dunn Jr, K.E. Behrns, C. Leeuwenburgh, and J.S. Kim Autophagy suppresses age-dependent ischemia and reperfusion injury in livers of mice Gastroenterology 141 2011 2188 2199
13. B. Ravikumar, C. Vacher, Z. Berger, J.E. Davies, S. Luo, L.G. Oroz, F. Scaravilli, D.F. Easton, R. Duden, C.J. O'Kane, and D.C. Rubinsztein Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease Nat. Genet. 36 2004 585 595
14. S. Sarkar, R.A. Floto, Z. Berger, S. Imarisio, A. Cordenier, M. Pasco, L.J. Cook, and D.C. Rubinsztein Lithium induces autophagy by inhibiting inositol monophosphatase J. Cell Biol. 170 2005 1101 1111
15. J. Liang, S.H. Shao, Z.X. Xu, B. Hennessy, Z. Ding, M. Larrea, S. Kondo, D.J. Dumont, J.U. Gutterman, C.L. Walker, J.M. Slingerland, and G.B. Mills The energy sensing LKB1-AMPK pathway regulates p27(kip1) phosphorylation mediating the decision to enter autophagy or apoptosis Nat. Cell Biol. 9 2007 218 224
16. M. Deffieu, I. Bhatia-Kissova, B. Salin, A. Galinier, S. Manon, and N. Camougrand Glutathione participates in the regulation of mitophagy in yeast J. Biol. Chem. 284 2009 14828 14837
17. F. Amersi, R. Buelow, H. Kato, B. Ke, A.J. Coito, X.D. Shen, D. Zhao, J. Zaky, J. Melinek, C.R. Lassman, J.K. Kolls, J. Alam, T. Ritter, H.D. Volk, D.G. Farmer, R.M. Ghobrial, R.W. Busuttil, and J.W. Kupiec-Weglinski Upregulation of heme oxygenase-1 protects genetically fat Zucker rat livers from ischemia/reperfusion injury J. Clin. Invest. 104 1999 1631 1639
18. D. Morse, L. Lin, A.M. Choi, and S.W. Ryter Heme oxygenase-1, a critical arbitrator of cell death pathways in lung injury and disease Free Radic. Biol. Med. 47 2009 1 12
19. N. Yun, H.A. Eum, and S.M. Lee Protective role of heme oxygenase-1 against liver damage caused by hepatic ischemia and reperfusion in rats Antioxid. Redox Signal. 13 2010 1503 1512
20. D.J. Slebos, S.W. Ryter, M. van der Toorn, F. Liu, F. Guo, C.J. Baty, J.M. Karlsson, S.C. Watkins, H.P. Kim, X. Wang, J.S. Lee, D.S. Postma, H.F. Kauffman, and A.M. Choi Mitochondrial localization and function of heme oxygenase-1 in cigarette smoke-induced cell death Am. J. Respir. Cell Mol. Biol. 36 2007 409 417
21. T. Kaizu, T. Tamaki, M. Tanaka, Y. Uchida, S. Tsuchihashi, A. Kawamura, and A. Kakita Preconditioning with tin-protoporphyrin IX attenuates ischemia/reperfusion injury in the rat kidney Kidney Int. 63 2003 1393 1403
22. K. Ito, H. Ozasa, N. Kojima, M. Miura, T. Iwa, H. Senoo, and S. Horikawa Pharmacological preconditioning protects lung injury induced by intestinal ischemia/reperfusion in rat Shock 19 2003 462 468
23. N. Gurusamy, I. Lekli, N.V. Gorbunov, M. Gherghiceanu, L.M. Popescu, and D.K. Das Cardioprotection by adaptation to ischaemia augments autophagy in association with BAG-1 protein J. Cell. Mol. Med. 13 2009 373 387
24. X.H. Zhang, N. Zhang, J.M. Lu, Q.Z. Kong, and Y.F. Zhao Tetrazolium violet induced apoptosis and cell cycle arrest in human lung cancer A549 cells Biomol. Ther. 20 2012 177 182
25. D.W. Kim, H.I. Cho, K.M. Kim, S.J. Kim, J.S. Choi, Y.S. Kim, and S.M. Lee Isorhamnetin-3-O-galactoside protects against CCl4-induced hepatic injury in mice Biomol. Ther. 20 2012 406 412
26. M.A. West, T.R. Billiar, R.D. Curran, B.J. Hyland, and R.L. Simmons Evidence that rat Kupffer cells stimulate and inhibit hepatocyte protein synthesis in vitro by different mechanisms Gastroenterology 96 1989 1572 1582
27. T. Qian, A.L. Nieminen, B. Herman, and J.J. Lemasters Mitochondrial permeability transition in pH-dependent reperfusion injury to rat hepatocytes Am. J. Physiol. 273 1997 C1783 C1792
28. N.Y. Spencer, W. Zhou, Q. Li, Y. Zhang, M. Luo, Z. Yan, T.J. Lynch, D. Abbott, B. Banfi, and J.F. Engelhardt Hepatocytes produce TNF-alpha following hypoxia-reoxygenation and liver ischemia-reperfusion in a NADPH oxidase- and c-Src-dependent manner Am. J. Physiol. Gastrointest. Liver Physiol. 305 2013 G84 G94
29. L. Portal, V. Martin, R. Assaly, A. d'Anglemont de Tassigny, S. Michineau, A. Berdeaux, B. Ghaleh, and S. Pons A model of hypoxia-reoxygenation on isolated adult mouse cardiomyocytes: characterization, comparison with ischemia-reperfusion, and application to the cardioprotective effect of regular treadmill exercise J. Cardiovasc. Pharmacol. Ther. 18 2013 367 375
30. H.M. Ni, A. Bockus, N. Boggess, H. Jaeschke, and W.X. Ding Activation of autophagy protects against acetaminophen-induced hepatotoxicity Hepatology 55 2012 222 232
31. K. Gotoh, Z. Lu, M. Morita, M. Shibata, M. Koike, S. Waguri, K. Dono, Y. Doki, E. Kominami, A. Sugioka, M. Monden, and Y. Uchiyama Participation of autophagy in the initiation of graft dysfunction after rat liver transplantation Autophagy 5 2009 351 360
32. A. Hamacher-Brady, N.R. Brady, and R.A. Gottlieb Enhancing macroautophagy protects against ischemia/reperfusion injury in cardiac myocytes J. Biol. Chem. 281 2006 29776 29787
33. M.B. Doyle, N. Vachharajani, J.R. Wellen, C.D. Anderson, J.A. Lowell, S. Shenoy, E.M. Brunt, and W.C. Chapman Short- and long-term outcomes after steatotic liver transplantation Arch. Surg. 145 2010 653 660
34. D. Wang, Y. Ma, Z. Li, K. Kang, X. Sun, S. Pan, J. Wang, H. Pan, L. Liu, D. Liang, and H. Jiang The role of AKT1 and autophagy in the protective effect of hydrogen sulphide against hepatic ischemia/reperfusion injury in mice Autophagy 8 2012 954 962
35. F. Vigneron, P. Dos Santos, S. Lemoine, M. Bonnet, L. Tariosse, T. Couffinhal, C. Duplaa, and B. Jaspard-Vinassa GSK-3beta at the crossroads in the signalling of heart preconditioning: implication of mTOR and Wnt pathways Cardiovasc. Res. 90 2011 49 56
36. A. Williams, S. Sarkar, P. Cuddon, E.K. Ttofi, S. Saiki, F.H. Siddiqi, L. Jahreiss, A. Fleming, D. Pask, P. Goldsmith, C.J. O'Kane, R.A. Floto, and D.C. Rubinsztein Novel targets for Huntington's disease in an mTOR-independent autophagy pathway Nat. Chem. Biol. 4 2008 295 305
37. W. Gao, W.X. Ding, D.B. Stolz, and X.M. Yin Induction of macroautophagy by exogenously introduced calcium Autophagy 4 2008 754 761
38. J. Evankovich, R. Zhang, J.S. Cardinal, L. Zhang, J. Chen, H. Huang, D. Beer-Stolz, T.R. Billiar, M.R. Rosengart, and A. Tsung Calcium/calmodulin- dependent protein kinase IV limits organ damage in hepatic ischemia-reperfusion injury through induction of autophagy Am. J. Physiol. Gastrointest. Liver Physiol. 303 2012 G189 G198
39. R. Russo, L. Berliocchi, A. Adornetto, G.P. Varano, F. Cavaliere, C. Nucci, D. Rotiroti, L.A. Morrone, G. Bagetta, and M.T. Corasaniti Calpain-mediated cleavage of Beclin-1 and autophagy deregulation following retinal ischemic injury in vivo Cell Death Dis. 2 2011 e144
40. H.P. Kim, H.O. Pae, S.H. Back, S.W. Chung, J.M. Woo, Y. Son, and H.T. Chung Heme oxygenase-1 comes back to endoplasmic reticulum Biochem. Biophys. Res. Commun. 404 2011 1 5
41. A. Paine, B. Eiz-Vesper, R. Blasczyk, and S. Immenschuh Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential Biochem. Pharmacol. 80 2010 1895 1903
42. E.H. Carchman, J. Rao, P.A. Loughran, M.R. Rosengart, and B.S. Zuckerbraun Heme oxygenase-1-mediated autophagy protects against hepatocyte cell death and hepatic injury from infection/sepsis in mice Hepatology 53 2011 2053 2062
43. H.S. Kim, P.A. Loughran, J. Rao, T.R. Billiar, and B.S. Zuckerbraun Carbon monoxide activates NF-kappaB via ROS generation and Akt pathways to protect against cell death of hepatocytes Am. J. Physiol. Gastrointest. Liver Physiol. 295 2008 G146 G152
44. H. Malhi, and R.J. Kaufman Endoplasmic reticulum stress in liver disease J. Hepatol. 54 2011 795 809