Hydrogen sulfide preconditions the db/db diabetic mouse heart against ischemia-reperfusion injury by activating Nrf2 signaling in an Erk-dependent manner

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 304, Issue 9, 2013, Pages

  Peake, Bridgette F ^a   Nicholson, Chad K ^a   Lambert, Jonathan P ^a   Hood, Rebecca L ^a   Amin, Hena ^a   Amin, Sana ^a   Calvert, John W ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Hydrogen sulfide; Myocardial infarction; Nuclear factor E2 related factor; Type 2 diabetes

Indexed keywords

HEME OXYGENASE 1; HYDROGEN SULFIDE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 3; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; SODIUM SULFIDE; TRANSCRIPTION FACTOR NRF2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FRACTIONATION; CHROMATIN IMMUNOPRECIPITATION; ENZYME ACTIVATION; HEART INFARCTION; HEART MUSCLE INJURY; HEART MUSCLE ISCHEMIA; HEART PROTECTION; IN VIVO STUDY; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

HYDROGEN SULFIDE; MYOCARDIAL INFARCTION; NUCLEAR FACTOR E2-RELATED FACTOR; TYPE 2 DIABETES;

ANIMALS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; DIABETES MELLITUS, TYPE 2; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION; HEME OXYGENASE-1; HYDROGEN SULFIDE; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MYOCARDIAL REPERFUSION INJURY; NAD(P)H DEHYDROGENASE (QUINONE); NF-E2-RELATED FACTOR 2; SULFIDES;

EID: 84878618892     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00796.2012     Document Type: Article

References (38)

1. Cai H, Harrison DG. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res 87: 840-844, 2000.
2. Calvert JW, Gundewar S, Jha S, Elrod JW, Lefer DJ. Hydrogen sulfide therapy attenuates left ventricular dysfunction and reduces mortality in a murine model of heart failure. Circulation 118: S441-S331, 2008.
3. 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 105: 365-374, 2009.
4. Denizalti M, Bozkurt TE, Akpulat U, Sahin-Erdemli I, Abacioglu N. The vasorelaxant effect of hydrogen sulfide is enhanced in streptozotocininduced diabetic rats. Naunyn Schmiedebergs Arch Pharmacol 383: 509-517, 2011.
5. 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 506: 48-57, 2011.
6. Elrod JW, Calvert JW, Morrison J, Doeller JE, Kraus DW, Tao L, Jiao X, Scalia R, Kiss L, Szabo C, Kimura H, Chow CW, Lefer DJ. Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function. Proc Natl Acad Sci USA 104: 15560-15565, 2007.
7. Fisher CD, Augustine LM, Maher JM, Nelson DM, Slitt AL, Klaassen CD, Lehman-McKeeman LD, Cherrington NJ. Induction of drugmetabolizing enzymes by garlic and allyl sulfide compounds via activation of constitutive androstane receptor and nuclear factor E2-related factor 2. Drug Metab Dispos 35: 995-1000, 2007.
8. Gao Y, Yao X, Zhang Y, Li W, Kang K, Sun L, Sun X. The protective role of hydrogen sulfide in myocardial ischemia-reperfusion-induced injury in diabetic rats. Int J Cardiol 152: 177-183, 2011.
9. Goven D, Boutten A, Lecon-Malas V, Boczkowski J, Bonay M. Prolonged cigarette smoke exposure decreases heme oxygenase-1 and alters Nrf2 and Bach1 expression in human macrophages: roles of the MAP kinases ERK(1/2) and JNK. FEBS Lett 583: 3508-3518, 2009.
10. Hourihan JM, Kenna JG, Hayes JD. The gasotransmitter hydrogen sulfide induces Nrf2-target genes by inactivating the keap1 ubiquitin ligase substrate adaptor through formation of a disulfide bond between Cys-226 and Cys-613. Antioxid Redox Signal. In press.
11. Jain AK, Jaiswal AK. GSK-3beta acts upstream of Fyn kinase in regulation of nuclear export and degradation of NF-E2 related factor 2. J Biol Chem 282: 16502-16510, 2007.
12. Jain SK, Bull R, Rains JL, Bass PF, Levine SN, Reddy S, McVie R, Bocchini JA. Low levels of hydrogen sulfide in the blood of diabetes patients and streptozotocin-treated rats causes vascular inflammation? Antioxid Redox Signal 12: 1333-1337, 2010.
13. Jay D, Hitomi H, Griendling KK. Oxidative stress and diabetic cardiovascular complications. Free Radic Biol Med 40: 183-192, 2006.
14. Jyrkkanen HK, Kuosmanen S, Heinaniemi M, Laitinen H, Kansanen E, Mella-Aho E, Leinonen H, Yla-Herttuala S, Levonen AL. Novel insights into the regulation of antioxidant-response-element-mediated gene expression by electrophiles: induction of the transcriptional repressor BACH1 by Nrf2. Biochem J 440: 167-174, 2011.
15. Kaspar JW, Jaiswal AK. Antioxidant-induced phosphorylation of tyrosine 486 leads to rapid nuclear export of Bach1 that allows Nrf2 to bind to the antioxidant response element and activate defensive gene expression. J Biol Chem 285: 153-162, 2010.
16. Kensler TW, Wakabayashi N, Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47: 89-116, 2007.
17. Kimura H, Shibuya N, Kimura Y. Hydrogen sulfide is a signaling molecule and a cytoprotectant. Antioxid Redox Signal 17: 45-57, 2012.
18. Lau A, Villeneuve NF, Sun Z, Wong PK, Zhang DD. Dual roles of Nrf2 in cancer. Pharmacol Res 58: 262-270, 2008.
19. Levitt MD, Abdel-Rehim MS, Furne J. Free and acid-labile hydrogen sulfide concentrations in mouse tissues: anomalously high free hydrogen sulfide in aortic tissue. Antioxid Redox Signal 15: 373-378, 2011.
20. Mikami Y, Shibuya N, Kimura Y, Nagahara N, Ogasawara Y, Kimura H. Thioredoxin and dihydrolipoic acid are required for 3-mercaptopyruvate sulfurtransferase to produce hydrogen sulfide. Biochem J 439: 479-485, 2011.
21. Nagahara N, Katayama A. Post-translational regulation of mercaptopyruvate sulfurtransferase via a low redox potential cysteine-sulfenate in the maintenance of redox homeostasis. J Biol Chem 280: 34569-34576, 2005.
22. Nicholson CK, Calvert JW. Hydrogen sulfide and ischemia-reperfusion injury. Pharmacol Res 62: 289-297, 2010.
23. Predmore BL, Kondo K, Bhushan S, Zlatopolsky MA, King AL, Aragon JP, Grinsfelder DB, Condit ME, Lefer DJ. The polysulfide diallyl trisulfide protects the ischemic myocardium by preservation of endogenous hydrogen sulfide and increasing nitric oxide bioavailability. Am J Physiol Heart Circ Physiol 302: H2410-H2418, 2012.
24. Shibuya N, Tanaka M, Yoshida M, Ogasawara Y, Togawa T, Ishii K, Kimura H. 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid Redox Signal 11: 703-714, 2009.
25. Sodha NR, Clements RT, Feng J, Liu Y, Bianchi C, Horvath EM, Szabo C, Sellke FW. The effects of therapeutic sulfide on myocardial apoptosis in response to ischemia-reperfusion injury. Eur J Cardiothorac Surg 33: 906-913, 2008.
26. Sun Z, Zhang S, Chan JY, Zhang DD. Keap1 controls postinduction repression of the Nrf2-mediated antioxidant response by escorting nuclear export of Nrf2. Mol Cell Biol 27: 6334-6349, 2007.
27. Suzuki K, Olah G, Modis K, Coletta C, Kulp G, Gero D, Szoleczky P, Chang T, Zhou Z, Wu L, Wang R, Papapetropoulos A, Szabo C. Hydrogen sulfide replacement therapy protects the vascular endothelium in hyperglycemia by preserving mitochondrial function. Proc Natl Acad Sci USA 108: 13829-13834, 2011.
28. Szabo C. Roles of hydrogen sulfide in the pathogenesis of diabetes mellitus and its complications. Antioxid Redox Signal 17: 68-80, 2012.
29. Taniguchi S, Kimura T, Umeki T, Kimura Y, Kimura H, Ishii I, Itoh N, Naito Y, Yamamoto H, Niki I. Protein phosphorylation involved in the gene expression of the hydrogen sulphide producing enzyme cystathionine gamma-lyase in the pancreatic beta-cell. Mol Cell Endocrinol 350: 31-38, 2012.
30. Tanito M, Agbaga MP, Anderson RE. Upregulation of thioredoxin system via Nrf2-antioxidant responsive element pathway in adaptiveretinal neuroprotection in vivo and in vitro. Free Radic Biol Med 42: 1838-1850, 2007.
31. Wakabayashi N, Dinkova-Kostova AT, Holtzclaw WD, Kang MI, Kobayashi A, Yamamoto M, Kensler TW, Talalay P. Protection against electrophile and oxidant stress by induction of the phase 2 response: fate of cysteines of the Keap1 sensor modified by inducers. Proc Natl Acad Sci USA 101: 2040-2045, 2004.
32. Whiteman M, Gooding KM, Whatmore JL, Ball CI, Mawson D, Skinner K, Tooke JE, Shore AC. Adiposity is a major determinant of plasma levels of the novel vasodilator hydrogen sulphide. Diabetologia 53: 1722-1726, 2010.
33. Wintner EA, Deckwerth TL, Langston W, Bengtsson A, Leviten D, Hill P, Insko MA, Dumpit R, VandenEkart E, Toombs CF, Szabo C. A monobromobimane-based assay to measure the pharmacokinetic profile of reactive sulphide species in blood. Br J Pharmacol 160: 941-957, 2010.
34. Yang G, Zhao K, Ju Y, Mani S, Cao Q, Puukila S, Khaper N, Wu L, Wang R. Hydrogen sulfide protects against cellular senescence via Ssulfhydration of keap1 and activation of Nrf2. Antioxid Redox Signal. In press.
35. Yin T, Hou R, Liu S, Lau WB, Wang H, Tao L. Nitrative inactivation of thioredoxin-1 increases vulnerability of diabetic hearts to ischemia/ reperfusion injury. J Mol Cell Cardiol 49: 354-361, 2010.
36. Yuan P, Xue H, Zhou L, Qu L, Li C, Wang Z, Ni J, Yu C, Yao T, Huang Y, Wang R, Lu L. Rescue of mesangial cells from high glucoseinduced over-proliferation and extracellular matrix secretion by hydrogen sulfide. Nephrol Dial Transplant 26: 2119-2126, 2011.
37. Yusuf M, Kwong Huat BT, Hsu A, Whiteman M, Bhatia M, Moore PK. Streptozotocin-induced diabetes in the rat is associated with enhanced tissue hydrogen sulfide biosynthesis. Biochem Biophys Res Commun 333: 1146-1152, 2005.
38. Zhu H, Itoh K, Yamamoto M, Zweier JL, Li Y. Role of Nrf2 signaling in regulation of antioxidants and phase 2 enzymes in cardiac fibroblasts: protection against reactive oxygen and nitrogen species-induced cell injury. FEBS Lett 579: 3029-3036, 2005.