Levosimendan inhibits peroxidation in hepatocytes by modulating apoptosis/autophagy interplay

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Grossini, Elena ^a   Bellofatto, Kevin ^a   Farruggio, Serena ^a   Sigaudo, Lorenzo ^a   Marotta, Patrizia ^a   Raina, Giulia ^a   De Giuli, Veronica ^a   Mary, David ^a   Pollesello, Piero ^a   Minisini, Rosalba ^a   Pirisi, Mario ^a   Vacca, Giovanni ^a  

^a UNIVERSITY OF EASTERN PIEDMONT   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; ISOENZYME; LEVOSIMENDAN; NITRIC OXIDE; ANTIARRHYTHMIC AGENT; CARRIER PROTEIN; HYDRAZONE DERIVATIVE; MITOCHONDRIAL K(ATP) CHANNEL; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; POTASSIUM CHANNEL; PYRIDAZINE DERIVATIVE; SIMENDAN;

ANIMAL CELL; ARTICLE; AUTOPHAGY; CELL ACTIVATION; CELL PROTECTION; CELL SURVIVAL; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME REGULATION; INTRACELLULAR SIGNALING; LIVER CELL; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; MOLECULAR EVOLUTION; NONHUMAN; OXIDATIVE STRESS; PEROXIDATION; RAT; STELLATE CELL; WESTERN BLOTTING; ANIMAL; APOPTOSIS; CYTOLOGY; DRUG EFFECTS; HUMAN; LIPID PEROXIDATION; METABOLISM; SPRAGUE DAWLEY RAT;

RATTUS;

ANIMALS; ANTI-ARRHYTHMIA AGENTS; APOPTOSIS; AUTOPHAGY; BLOTTING, WESTERN; HEPATOCYTES; HUMANS; HYDRAZONES; LIPID PEROXIDATION; MALE; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; POTASSIUM CHANNELS; PYRIDAZINES; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84928139939     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0124742     Document Type: Article

References (54)

1. Basel H, Kavak S, Demir H, Meral I, Ekim H, Bektas H. Effect of levosimendan injection on oxidative stress of rat myocardium. Toxicol Ind Health. 2013; 29:435-440. doi: 10.1177/0748233712436643 PMID: 22362016
2. Gecit I, Kavak S, Yüksel MB, Basel H, Bektas H, Gümrükçüoglu HA, et al. Effect of short-term treatment with levosimendan on oxidative stress in renal tissues of rats. Toxicol Ind Health. 2014; 30:47-51. doi: 10.1177/0748233712451773 PMID: 22722773
3. Sack MN. Mitochondrial depolarization and the role of uncoupling proteins in ischemia tolerance. Cardiovasc Res. 2006; 72:210-219. PMID: 16914124
4. Perrelli MG, Pagliaro P, Penna C. Ischemia/reperfusion injury and cardioprotective mechanisms: Role of mitochondria and reactive oxygen species. World J Cardiol. 2011; 3: 186-200. doi: 10.4330/wjc.v3. i6.186 PMID: 21772945
5. Grossini E, Pollesello P, Bellofatto K, Sigaudo L, Farruggio S, Origlia V, et al. Protective effects elicited by levosimendan against liver ischemia/reperfusion injury in anesthetized rats. Liver Transpl. 2014; 20:361-375. doi: 10.1002/lt.23799 PMID: 24273004
6. Uberti F, Caimmi PP, Molinari C, Mary D, Vacca G, Grossini E. Levosimendan modulates programmed forms of cell death through K(ATP) channels and nitric oxide. J Cardiovasc Pharmacol. 2011; 57: 246-258. doi: 10.1097/FJC.0b013e318204bb55 PMID: 21107279
7. Caimmi PP, Molinari C, Uberti F, Micalizzi E, Valente G, Mary DA, et al. Intracoronary levosimendan prevents myocardial ischemic damages and activates survival signaling through ATP-sensitive potassium channel and nitric oxide. Eur J Cardiothorac Surg. 2011; 39:e59-67. doi: 10.1016/j.ejcts.2010.11. 044 PMID: 21247774
8. Grossini E, Molinari C, Pollesello P, Bellomo G, Valente G, Mary D, et al. Levosimendan protection against kidney ischemia/reperfusion injuries in anesthetized pigs. J Pharmacol Exp Ther. 2012; 342:376-388. doi: 10.1124/jpet.112.193961 PMID: 22566668
9. Codogno P, Meijer AJ. Autophagy and signaling: their role in cell survival and cell death. Cell Death Differ. 2005; 12:1509-1518. PMID: 16247498
10. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell. 2005; 122:927-939. PMID: 16179260
11. Boya P, González-Polo RA, Casares N, Perfettini JL, Dessen P, Larochette N, et al. Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol. 2005; 25:1025-1040. PMID: 15657430
12. Hamacher-Brady A, Brady NR, Gottlieb RA. The interplay between pro death and pro-survival signaling pathways in myocardial ischemia/reperfusion injury: apoptosis meets autophagy. Cardiovasc Drugs Ther. 2006; 20:445-462. PMID: 17149555
13. Bhogal RH, Weston CJ, Curbishley SM, Adams DH, Afford SC. Autophagy: a cyto-protective mechanism which prevents primary human hepatocyte apoptosis during oxidative stress. Autophagy. 2012; 8:545-558. doi: 10.4161/auto.19012 PMID: 22302008
14. Shulman M, Nahmias Y. Long-term culture and coculture of primary rat and human hepatocytes. Mol Biol. 2013; 945:287-302. doi: 10.1007/978-1-62703-125-7-17 PMID: 23097113
15. Xu L, Hui A, Albanis E, Arther M, O'Byrne S, Blaner WS, et al. Human hepatic stellate cell lines, LX-1 and LX-2: new tools for analysis of hepatic fibrosis. Gut. 2005; 54:142-151. PMID: 15591520
16. Maruyama R, Goto K, Takemura G, Ono K, Nagao K, Horie T, et al. Morphological and biochemical characterization of basal and starvation-induced autophagy in isolated adult rat cardiomyocytes. Am J Physiol Heart Circ Physiol. 2008; 295: H1599-H1607. doi: 10.1152/ajpheart.91449.2007 PMID: 18708438
17. Grossini E, Gramaglia C, Farruggio S, Bellofatto K, Anchisi C, Mary D, et al. Asenapine increases nitric oxide release and protects porcine coronary artery endothelial cells against peroxidation. Vascul Pharmacol. 2014; 60:127-141. doi: 10.1016/j.vph.2014.01.008 PMID: 24512732
18. Cappellano G, Uberti F, Caimmi PP, Pietronave S, Mary DA, Dianzani C, et al. Different expression and function of the endocannabinoid system in human epicardial adipose tissue in relation to heart disease. Can J Cardiol. 2013; 29:499-509. doi: 10.1016/j.cjca.2012.06.003 PMID: 22926037
19. Grossini E, Caimmi P, Molinari C, Uberti F, Mary D, Vacca G. CCK receptors-related signaling involved in nitric oxide production caused by gastrin 17 in porcine coronary endothelial cells. Mol Cell Endocrinol. 2012; 350:20-30. doi: 10.1016/j.mce.2011.11.018 PMID: 22138052
20. Shiva S, Sack MN, Greer JJ, Duranski M, Ringwood LA, Burwell L, et al. Nitrite augments tolerance to ischemia/reperfusion injury via the modulation of mitochondrial electron transfer. J Exp Med. 2007 204:2089-2102. PMID: 17682069
21. Thirunavukkarasu C, Watkins SC, Gandhi CR. Mechanisms of endotoxin-induced NO, IL-6, and TNFalpha production in activated rat hepatic stellate cells: role of p38 MAPK. Hepatology. 2006; 44:389-398. PMID: 16871588
22. Svegliati-Baroni G, Saccomanno S, van Goor H, Jansen P, Benedetti A, Moshage H, et al. Involvement of reactive oxygen species and nitric oxide radicals in activation and proliferation of rat hepatic stellate cells. Liver. 2001; 21:1-12. PMID: 11169066
23. Grossini E, Molinari C, Caimmi PP, Uberti F, Vacca G. Levosimendan induces NO production through p38 MAPK, ERK and Akt in porcine coronary endothelial cells: role for mitochondrial K(ATP) channel. Br J Pharmacol. 2009; 156:250-261. doi: 10.1111/j.1476-5381.2008.00024.x PMID: 19154424
24. Czaja MJ. Cell signaling in oxidative stress-induced liver injury. Semin Liver Dis. 2007; 27:378-389. PMID: 17979074
25. Marra F, Gastaldelli A, Svegliati Baroni G, Tell G, Tiribelli C. Molecular basis and mechanisms of progression of non-alcoholic steatohepatitis. Trends Mol Med. 2008; 14:72-81. doi: 10.1016/j.molmed. 2007.12.003 PMID: 18218340
26. Wu D, Cederbaum AI. Oxidative stress and alcoholic liver disease. Semin Liver Dis. 2009; 29:141-154. doi: 10.1055/s-0029-1214370 PMID: 19387914
27. Jaeschke H. Reactive oxygen and mechanisms of inflammatory liver injury. J Gastroenterol Hepatol. 2000; 15:718-724. PMID: 10937675
28. Levine B, Kroemer G. Autophagy in aging, disease and death: the true identity of a cell death impostor. Cell Death Differ. 2009; 16:1-2. doi: 10.1038/cdd.2008.139 PMID: 19079285
29. Chowdhury AA, Chaudhuri J, Biswas N, Manna A, Chatterjee S, Mahato SK, et al. Synergistic apoptosis of CML cells by buthionine sulfoximine and hydroxychavicol correlates with activation of AIF and GSH-ROS-JNK-ERK-iNOS pathway. PLoS One. 2013; e73672. doi: 10.1371/journal.pone.0073672 PMID: 24040019
30. Zhang X, Lemasters JJ. Translocation of iron from lysosomes to mitochondria during ischemia predisposes to injury after reperfusion in rat hepatocytes. Free Radic Biol Med. 2013; 63:243-253. doi: 10. 1016/j.freeradbiomed.2013.05.004 PMID: 23665427
31. Lee HS, Son WC, Ryu JE, Koo BA, Kim YS. Standardized Salvia miltiorrhiza extract suppresses hepatic stellate cell activation and attenuates steatohepatitis induced by a methionine-choline deficient diet in mice. Molecules. 2014; 19:8189-8211. doi: 10.3390/molecules19068189 PMID: 24941342
32. Datta SR, Brunet A, Greenberg ME. Cellular survival: a play in three Akts. Genes Dev. 1999; 13: 2905-2927. PMID: 10579998
33. Gupta NA, Kolachala VL, Jiang R, Abramowsky C, Shenoi A, Kosters A, et al. Mitigation of autophagy ameliorates hepatocellular damage following ischemia reperfusion injury in murine steatotic liver. Am J Physiol Gastrointest Liver Physiol. 2014; ajpgi.00210.2014. doi: 10.1152/ajpgi.00210.2014
34. Raza H, John A. Implications of altered glutathione metabolism in aspirin-induced oxidative stress and mitochondrial dysfunction in HepG2 cells. PLoS One. 2012; doi: 10.1371/journal.pone.0036325
35. Zeng Z, Huang HF, He F, Wu LX, Lin J, Chen MQ. Diazoxide attenuates ischemia/reperfusion injury via upregulation of heme oxygenase-1 after liver transplantation in rats. World J Gastroenterol. 2012; 18:1765-1772. doi: 10.3748/wjg.v18.i15.1765 PMID: 22553400
36. Hai S, Takemura S, Minamiyama Y, Yamasaki K, Yamamoto S, Kodai S, et al. Mitochondrial K(ATP) channel opener prevents ischemia-reperfusion injury in rat liver. Transplant Proc. 2005; 37:428-431. PMID: 15808666
37. Guan LY, Fu PY, Li PD, Li ZN, Liu HY, Xin MG, et al. Mechanisms of hepatic ischemia-reperfusion injury and protective effects of nitric oxide. World J Gastrointest Surg. 2014; 6:122-128. doi: 10.4240/wjgs. v6.i7.122 PMID: 25068009
38. Liaudet L, Soriano FG, Szabó C. Biology of nitric oxide signaling. Crit Care Med. 2000; 28:N37-52. PMID: 10807315
39. Shiva S, Sack MN, Greer JJ, Duranski M, Ringwood LA, Burwel L, et al. Nitrite augments tolerance to ischemia/reperfusion injury via the modulation of mitochondrial electron transfer. J Exp Med.2007; 204:2089-2102. PMID: 17682069
40. Razavi HM, Hamilton JA, Feng Q. Modulation of apoptosis by nitric oxide: implications in myocardial ischemia and heart failure. Pharmacol Ther. 2005; 106:147-162. PMID: 15866317
41. Kim JS, Ohshima S, Pediaditakis P, Lemasters JJ. Nitric oxide protects rat hepatocytes against reperfusion injury mediated by the mitochondrial permeability transition. Hepatology. 2004; 39:1533-1543. PMID: 15185294
42. Diesen DL, Kuo PC. Nitric oxide and redox regulation in the liver: part II. Redox biology in pathologic hepatocytes and implications for intervention. J Surg Res. 2011; 167:96-112. doi: 10.1016/j.jss.2009.10. 006 PMID: 20400112
43. Crabtree MJ, Brixey R, Batchelor H, Hale AB, Channon KM. Integrated redox sensor and effector functions for tetrahydrobiopterin- and glutathionylation-dependent endothelial nitric-oxide synthase uncoupling. J Biol Chem. 2013; 288:561-569. doi: 10.1074/jbc.M112.415992 PMID: 23139420
44. Bhogal RH, Weston CJ, Curbishley SM, Adams DH, Afford SC. A cyto-protective mechanism which prevents primary human hepatocyte apoptosis during oxidative stress. Autophagy. 2012; 8: 545-548. doi: 10.4161/auto.19012 PMID: 22302008
45. Marra F, Pinzani M, DeFranco R, Laffi G, Gentilini P. Involvement of phosphatidylinositol 3-kinase in the activation of extracellular signal-regulated kinase by PDGF in hepatic stellate cells. FEBS Lett. 1995; 376: 141-145. PMID: 7498528
46. Mallat A, Lodder J, Teixeira-Clerc F, Moreau R, Codogno P, Lotersztajn S. Autophagy: a multifaceted partner in liver fibrosis. Biomed Res Int. 2014; 869390. doi: 10.1155/2014/869390 PMID: 25254217
47. Wang W, Zhao C, Zhou J, Zhen Z, Wang Y, Shen C. Simvastatin ameliorates liver fibrosis via mediating nitric oxide synthase in rats with non-alcoholic steatohepatitis-related liver fibrosis. PLoS One. 2013; e76538. doi: 10.1371/journal.pone.0076538 PMID: 24098525
48. Papp Z, Édes I, Fruhwald S, De Hert SG, Salmenperä M, Leppikangas H, et al. Levosimendan: molecular mechanisms and clinical implications: consensus of experts on the mechanisms of action of levosimendan. Int J Cardiol. 2012; 159: 82-87. doi: 10.1016/j.ijcard.2011.07.022 PMID: 21784540
49. Leprán I, Pollesello P, Vajda S, Varró A, Papp JG. Preconditioning effects of levosimendan in a rabbit cardiac ischemia-reperfusion model. J Cardiovasc Pharmacol. 2006; 48:148-152. PMID: 17086092
50. Levijoki J, Pollesello P, Kaheinen P, Haikala H. Improved survival with simendan after experimental myocardial infarction in rats. Eur J. Pharmacol. 2001; 419:243-248. PMID: 11426847
51. Ibrahim MA, Abdel-Gaber SA, Amin EF, Ibrahim SA, Mohammed RK, Abdelrahman AM. Molecular mechanisms contributing to the protective effect of levosimendan in liver ischemia-reperfusion injury. Eur J Pharmacol. 2014; 741:64-73. doi: 10.1016/j.ejphar.2014.07.047 PMID: 25094034
52. Lenz K, Gegenhuber A, Firlinger F, Lohr G, Piringer P. Pilot study of levosimendan: Effect on liver blood flow and liver function in acute decompensated heart failure. Med Klin Intensivmed Notfmed. 2014; 109:267-270. doi: 10.1007/s00063-013-0326-z PMID: 24743943
53. Onody P, Stangl R, Fulop A, Rosero O, Garbaisz D, Turoczi Z, et al. Levosimendan: a cardiovascular drug to prevent liver ischemia-reperfusion injury? PLoS One. 2013; 8:e73758. doi: 10.1371/journal. pone.0073758 PMID: 24040056
54. Memis D, Inal MT, Sut N. The effects of levosimendan vs dobutamine added to dopamine on liver functions assessed with noninvasive liver function monitoring in patients with septic shock. J Crit Care. 2012; 27:318.e1-6. doi: 10.1016/j.jcrc.2011.11.015 PMID: 22227078