Exogenous hydrogen sulfide protects against doxorubicin-induced inflammation and cytotoxicity by inhibiting p38MAPK/NFκB pathway in H9c2 cardiac cells

Cellular Physiology and Biochemistry

Volumn 32, Issue 6, 2013, Pages 1668-1680

  Guo, Runmin ^a   Wu, Keng ^a   Chen, Jingfu ^a   Mo, Liqiu ^b   Hua, Xiaoxiao ^b   Zheng, Dongdan ^c   Chen, Peixi ^d   Chen, Gang ^c   Xu, Wenming ^c   Feng, Jianqiang ^d  

^a GUANGDONG MEDICAL UNIVERSITY   (China)

^b Department of Anesthesiology ^*  (China)

^c SUN YAT SEN UNIVERSITY   (China)

^d SUN YAT SEN UNIVERSITY   (China)

Author keywords

Cardiotoxicity; Doxorubicin; Hydrogen sulfide; Inflammation; Nuclear factor B; p38 mitogen activated protein kinases

Indexed keywords

ACETYLCYSTEINE; DOXORUBICIN; HYDROGEN SULFIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1BETA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE P38; NITRIC OXIDE; PYRROLIDINE DITHIOCARBAMATE; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CARDIOTOXICITY; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DONOR; DRUG EXPOSURE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE TRANSLOCATION; HEART MUSCLE CELL; INFLAMMATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; ANIMAL CELL; ENZYME INHIBITION; HEART PROTECTION; NONHUMAN; RAT;

ACETYLCYSTEINE; ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; CELL LINE; CELL SURVIVAL; DOXORUBICIN; INFLAMMATION; INTERLEUKIN-1BETA; INTERLEUKIN-6; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROLINE; RATS; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SULFITES; THIOCARBAMATES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84890448089     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000356602     Document Type: Article

References (47)

1. Ma Y, Kurtyka CA, Boyapalle S, Sung SS, Lawrence H, Guida W, Cress WD: A small-molecule E2F inhibitor blocks growth in a melanoma culture model. Cancer Res 2008;68:6292-6299.
2. Li L, Takemura G, Li Y, Miyata S, Esaki M, Okada H, Kanamori H, Khai NC, Maruyama R, Ogino A, Minatoguchi S, Fujiwara T, Fujiwara H: Preventive effect of erythropoietin on cardiac dysfunction in doxorubicin-induced cardiomyopathy. Circulation 2006;113:535-543.
3. Muggia FM, Green MD: New anthracycline antitumor antibiotics. Crit Rev Oncol Hematol 1991;11:43-64.
4. Scully RE, Lipshultz SE: Anthracycline cardiotoxicity in long-term survivors of childhood cancer. Cardiovasc Toxicol 2007;7:122-128.
5. Hrdina R, Gersl V, Klimtova I, Simunek T, Machackova J, Adamcova M: Anthracycline-induced cardiotoxicity. Acta Medica (Hradec Kralove) 2000;43:75-82.
6. Minotti G, Menna P, Salvatorelli E, Cairo G, Gianni L: Anthracyclines: Molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol Rev 2004;56:185-229.
7. Wang XY, Yang CT, Zheng DD, Mo LQ, Lan AP, Yang ZL, Hu F, Chen PX, Liao XX, Feng JQ: Hydrogen sulfide protects H9c2 cells against doxorubicin-induced cardiotoxicity through inhibition of endoplasmic reticulum stress. Mol Cell Biochem 2012;363:419-426.
8. Chiosi E, Spina A, Sorrentino A, Romano M, Sorvillo L, Senatore G, D'Auria R, Abbruzzese A, Caraglia M, Naviglio S, Illiano G: Change in TNF-α receptor expression is a relevant event in doxorubicin-induced H9c2 cardiomyocyte cell death. J Interferon Cytokine Res 2007;27:589-597.
9. Riad A, Bien S, Westermann D, Becher PM, Loya K, Landmesser U, Kroemer HK, Schultheiss HP, Tschope C: Pretreatment with statin attenuates the cardiotoxicity of doxorubicin in mice. Cancer Res 2009;69:695-699.
10. Guo R, Lin J, Xu W, Shen N, Mo L, Zhang C, Feng J: Hydrogen sulfide attenuates doxorubicin-induced cardiotoxicity by inhibition of the p38 MAPK pathway in H9c2 cells. Int J Mol Med 2013;31:644-650.
11. Bien S, Riad A, Ritter CA, Gratz M, Olshausen F, Westermann D, Grube M, Krieg T, Ciecholewski S, Felix SB, Staudt A, Schultheiss HP, Ewert R, Volker U, Tschope C, Kroemer HK: The endothelin receptor blocker bosentan inhibits doxorubicin-induced cardiomyopathy. Cancer Res 2007;67:10428-10435.
12. Sheng Z, Knowlton K, Chen J, Hoshijima M, Brown JH, Chien KR: Cardiotrophin 1 (CT-1) inhibition of cardiac myocyte apoptosis via a mitogen-activated protein kinase-dependent pathway. Divergence from downstream CT-1 signals for myocardial cell hypertrophy. J Biol Chem 1997;272:5783-5791.
13. Sugden PH, Clerk A: "Stress-responsive" mitogen-activated protein kinases (c-jun n-terminal kinases and p38 mitogen-activated protein kinases) in the myocardium. Circ Res 1998;83:345-352.
14. Guo R, Xu W, Lin J, Mo L, Hua X, Chen P, Wu K, Zheng D, Feng J: Activation of the p38 MAPK/NF-κB pathway contributes to doxorubicin-induced inflammation and cytotoxicity in H9c2 cardiac cells. Mol Med Rep 2013;8:603-608.
15. Lowicka E, Beltowski J: Hydrogen sulfide (H2S) - the third gas of interest for pharmacologists. Pharmacol Rep 2007;59:4-24.
16. Moore PK, Bhatia M, Moochhala S: Hydrogen sulfide: From the smell of the past to the mediator of the future? Trends Pharmacol Sci 2003;24:609-611.
17. El-Seweidy MM, Sadik NA, Shaker OG: Role of sulfurous mineral water and sodium hydrosulfide as potent inhibitors of fibrosis in the heart of diabetic rats. Arch Biochem Biophys 2011;506:48-57.
18. Dong XB, Yang CT, Zheng DD, Mo LQ, Wang XY, Lan AP, Hu F, Chen PX, Feng JQ, Zhang MF, Liao XX: Inhibition of ROS-activated ERK1/2 pathway contributes to the protection of H2S against chemical hypoxia-induced injury in H9c2 cells. Mol Cell Biochem 2012;362:149-157.
19. Yang Z, Yang C, Xiao L, Liao X, Lan A, Wang X, Guo R, Chen P, Hu C, Feng J: Novel insights into the role of HSP90 in cytoprotection of H2S against chemical hypoxia-induced injury in H9c2 cardiac myocytes. Int J Mol Med 2011;28:397-403.
20. Chen SL, Yang CT, Yang ZL, Guo RX, Meng JL, Cui Y, Lan AP, Chen PX, Feng JQ: Hydrogen sulphide protects H9c2 cells against chemical hypoxia-induced injury. Clin Exp Pharmacol Physiol 2010;37:316-321.
21. Calvert JW, Jha S, Gundewar S, Elrod JW, Ramachandran A, Pattillo CB, Kevil CG, Lefer DJ: Hydrogen sulfide mediates cardioprotection through Nrf2 signaling. Circ Res 2009;105:365-374.
22. Yang C, Yang Z, Zhang M, Dong Q, Wang X, Lan A, Zeng F, Chen P, Wang C, Feng J: Hydrogen sulfide protects against chemical hypoxia-induced cytotoxicity and inflammation in hacat cells through inhibition of ROS/ NF-kappab/COX-2 pathway. PloS one 2011;6:e21971.
23. Lan A, Xu W, Zhang H, Hua X, Zheng D, Guo R, Shen N, Hu F, Feng J, Liu D: Inhibition of ROS-activated p38 MAPK pathway is involved in the protective effect of H2S against chemical hypoxia-induced inflammation in PC12 cells. Neurochem Res 2013;38:1454-1466.
24. Hu LF, Wong PT, Moore PK, Bian JS: Hydrogen sulfide attenuates lipopolysaccharide-induced inflammation by inhibition of p38 mitogen-activated protein kinase in microglia. J Neurochem 2007;100:1121-1128.
25. Su YW, Liang C, Jin HF, Tang XY, Han W, Chai LJ, Zhang CY, Geng B, Tang CS, Du JB: Hydrogen sulfide regulates cardiac function and structure in adriamycin-induced cardiomyopathy. Circ J 2009;73:741-749.
26. Liu B, Li H, Qu H, Sun B: Nitric oxide synthase expressions in adr-induced cardiomyopathy in rats. J Biochem Mol Biol 2006;39:759-765.
27. Aldieri E, Bergandi L, Riganti C, Costamagna C, Bosia A, Ghigo D: Doxorubicin induces an increase of nitric oxide synthesis in rat cardiac cells that is inhibited by iron supplementation. Toxicol Appl Pharmacol 2002;185:85-90.
28. Cigremis Y, Parlakpinar H, Polat A, Colak C, Ozturk F, Sahna E, Ermis N, Acet A: Beneficial role of aminoguanidine on acute cardiomyopathy related to doxorubicin-treatment. Mol Cell Biochem 2006;285:149-154.
29. Madonna R, Di Napoli P, Massaro M, Grilli A, Felaco M, De Caterina A, Tang D, De Caterina R, Geng YJ: Simvastatin attenuates expression of cytokine-inducible nitric-oxide synthase in embryonic cardiac myoblasts. J Biol Chem 2005;280:13503-13511.
30. Birks EJ, Yacoub MH, Burton PS, Owen V, Pomerance A, O'Halloran A, Banner NR, Khaghani A, Latif N: Activation of apoptotic and inflammatory pathways in dysfunctional donor hearts. Transplantation 2000;70:1498-1506.
31. Teng X, Zhang H, Snead C, Catravas JD: Molecular mechanisms of inos induction by IL-1 beta and IFN-? in rat aortic smooth muscle cells. Am J Physiol Cell Physiol 2002;282:C144-152.
32. Sauter KA, Wood LJ, Wong J, Iordanov M, Magun BE: Doxorubicin and daunorubicin induce processing and release of interleukin-1β through activation of the NLRP3 inflammasome. Cancer Biol Ther 2011;11:1008-1016.
33. Zordoky BN, Anwar-Mohamed A, Aboutabl ME, El-Kadi AO: Acute doxorubicin toxicity differentially alters cytochrome p450 expression and arachidonic acid metabolism in rat kidney and liver. Drug Metab Dispos 2011;39:1440-1450.
34. Huang CC, Chen PC, Huang CW, Yu J: Aristolochic acid induces heart failure in zebrafish embryos that is mediated by inflammation. Toxicol Sci 2007;100:486-494.
35. Dinarello CA: Il-1: Discoveries, controversies and future directions. Eur J Immunol 2010;40:599-606.
36. Zhu J, Zhang J, Xiang D, Zhang Z, Zhang L, Wu M, Zhu S, Zhang R, Han W: Recombinant human interleukin-1 receptor antagonist protects mice against acute doxorubicin-induced cardiotoxicity. Eur J Pharmacol 2010;643:247-253.
37. Huang CY, Fujimura M, Noshita N, Chang YY, Chan PH: SOD1 down-regulates NF-κB and c-Myc expression in mice after transient focal cerebral ischemia. J Cereb Blood Flow Metab 2001;21:163-173.
38. Kang YJ, Wingerd BA, Arakawa T, Smith WL: Cyclooxygenase-2 gene transcription in a macrophage model of inflammation. J Immunol 2006;177:8111-8122.
39. Karin M, Ben-Neriah Y: Phosphorylation meets ubiquitination: The control of NF-κB activity. Annu Rev Immunol 2000;18:621-663.
40. Varin R, Mulder P, Richard V, Tamion F, Devaux C, Henry JP, Lallemand F, Lerebours G, Thuillez C: Exercise improves flow-mediated vasodilatation of skeletal muscle arteries in rats with chronic heart failure. Role of nitric oxide, prostanoids, and oxidant stress. Circulation 1999;99:2951-2957.
41. Haywood GA, Tsao PS, von der Leyen HE, Mann MJ, Keeling PJ, Trindade PT, Lewis NP, Byrne CD, Rickenbacher PR, Bishopric NH, Cooke JP, McKenna WJ, Fowler MB: Expression of inducible nitric oxide synthase in human heart failure. Circulation 1996;93:1087-1094.
42. Wang R: Two's company, three's a crowd: Can H2S be the third endogenous gaseous transmitter? FASEB J 2002;16:1792-1798.
43. Li L, Bhatia M, Moore PK: Hydrogen sulphide-a novel mediator of inflammation? Curr Opin Pharmacol 2006;6:125-129.
44. Zhang H, Zhi L, Moore PK, Bhatia M: Role of hydrogen sulfide in cecal ligation and puncture-induced sepsis in the mouse. Curr Opin Pharmacol 2006;290:L1193-1201.
45. Mok YY, Atan MS, Yoke Ping C, Zhong Jing W, Bhatia M, Moochhala S, Moore PK: Role of hydrogen sulphide in haemorrhagic shock in the rat: Protective effect of inhibitors of hydrogen sulphide biosynthesis. Br J Pharmacol 2004;143:881-889.
46. Bhatia M, Wong FL, Fu D, Lau HY, Moochhala SM, Moore PK: Role of hydrogen sulfide in acute pancreatitis and associated lung injury. FASEB J 2005;19:623-625.
47. Kloesch B, Liszt M, Broell J: H2S transiently blocks IL-6 expression in rheumatoid arthritic fibroblast-like synoviocytes and deactivates p44/42 mitogen-activated protein kinase. Cell Biol Int 2010;34:477-484.