Hydrogen sulfide improves survival after cardiac arrest and cardiopulmonary resuscitation via a nitric oxide synthase 3-dependent mechanism in mice

Circulation

Volumn 120, Issue 10, 2009, Pages 888-896

  Minamishima, Shizuka ^a   Bougaki, Masahiko ^a   Sips, Patrick Y ^a   De Yu, Jia ^a   Minamishima, Yoji Andrew ^b   Elrod, John W ^c   Lefer, David J ^d   Bloch, Kenneth D ^a   Ichinose, Fumito ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Cardiopulmonary resuscitation; Heart arrest; Myocardial contraction; Nitric oxide synthase; Physiology

Indexed keywords

CYSTATHIONINE GAMMA LYASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYDROGEN SULFIDE; CARDIOTONIC AGENT; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PROTEIN KINASE B; SODIUM SULFIDE; SULFIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARTIFICIAL VENTILATION; BRAIN CORTEX; CIRCULATION; CONTROLLED STUDY; ENZYME DEFICIENCY; ENZYME MECHANISM; ENZYME PHOSPHORYLATION; HEART ARREST; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RESUSCITATION; SUDDEN DEATH; SURVIVAL RATE; ANIMAL; APOPTOSIS; BRAIN; C57BL MOUSE; DRUG EFFECT; ENZYMOLOGY; HEART; HEART CONTRACTION; HEART MITOCHONDRION; IN VITRO STUDY; METABOLISM; MORTALITY; MOUSE MUTANT; NERVOUS SYSTEM; PATHOPHYSIOLOGY; PHOSPHORYLATION; REPERFUSION INJURY; SIGNAL TRANSDUCTION; UPREGULATION;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; APOPTOSIS; BRAIN; CARDIOPULMONARY RESUSCITATION; CARDIOTONIC AGENTS; CYSTATHIONINE GAMMA-LYASE; HEART; HEART ARREST; HYDROGEN SULFIDE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA, HEART; MYOCARDIAL CONTRACTION; MYOCARDIAL REPERFUSION INJURY; MYOCYTES, CARDIAC; NERVOUS SYSTEM; NITRIC OXIDE SYNTHASE TYPE III; OXIDATIVE STRESS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SULFIDES; SURVIVAL RATE; UP-REGULATION;

EID: 70349769626     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.108.833491     Document Type: Article

References (30)

1. Nadkarni VM, Larkin GL, Peberdy MA, Carey SM, Kaye W, Mancini ME, Nichol G, Lane-Truitt T, Potts J, Ornato JP, Berg RA, for the National Registry of Cardiopulmonary Resuscitation Investigators. First documented rhythm and clinical outcome from in-hospital cardiac arrest among children and adults. JAMA. 2006;295:50-57.
2. Adrie C, Adib-Conquy M, Laurent I, Monchi M, Vinsonneau C, Fitting C, Fraisse F, Dinh-Xuan AT, Carli P, Spaulding C, Dhainaut JF, Cavaillon JM. Successful cardiopulmonary resuscitation, after cardiac arrest as a "sepsis-like" syndrome. Circulation. 2002;106:562-568.
3. 2S: a landscape view of gas biology. Keio J Med. 2002;51:1-10.
4. Stipanuk. MH, Beck. PW. Characterization of the enzymic capacity for cysteine desulphhydration in liver and kidney of the rat. Biochem J. 1982;15;206:267-277.
5. 5. Szabo C. Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov. 2007;6:917-935. (Pubitemid 350042399)
6. 6. Fiorucci S, Distrutti E, Cirino G, Wallace JL. The emerging roles of hydrogen, sulfide in the gastrointestinal tract and liver. Gastroenterology. 2006;131:259-271. (Pubitemid 44043128)
7. 7. Wang J, Huff AM, Spence JD, Hegele RA. Single nucleotide polymorphism in CTH associated with variation in plasma homocysteine concentration. Clin Genet. 2004;65:483-486. (Pubitemid 38786870)
8. 8. Blackstone E, Morrison M, Roth MB. H2S induces a suspended animation-like state in mice. Science. 2005;308:518. (Pubitemid 40570576)
9. Volpato GP, Searles R, Yu B, Scherrer-Crosbie M, Bloch KD, khinose F, Zapol WM. Inhaled hydrogen, sulfide : a rapidly reversible inhibitor of cardiac and metabolic function in the mouse. Anesthesiology. 2008;108:659-668.
10. Morrison ML, Blackwood JE, Lcckett SL, Iwata A, Winn RK, Roth MB. Surviving blood, loss using hydrogen sulfide. J Trauma. 2008;65:183-188.
11. 11. Qu K, Chen CPLH, Halliwell B, Moore PK, Wong PTH. Hydrogen sulfide is a mediator of cerebral ischemic damage. Stroke. 2006;37:889-893. (Pubitemid 43731927)
12. 12. Li L, Bhatia M, Zhu YZ, Zhu YC, Ramnath RD, Wang ZJ, Anuar FB, Whiteman M, Salto-Tellez M, Moore PK. Hydrogen sulfide is a novel mediator of lipopolysaccharide-induced inflammation in the mouse. FASEB J. 2005;19:1196-1198. (Pubitemid 40946463)
13. 13. Elrod JW, Calvert JW, Morrison J, Doeller JE, Kraus DW, Tao L, Jiao X, ScaliaR, 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. 2007;104:15560-15565. (Pubitemid 47502956)
14. 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. 2008;33:906-913.
15. Yong QC, Lee SW, Foo CS, Neo KL, Chen X, Bian JS. Endogenous hydrogen sulphide mediates the cardioprotection induced by ischemic postconditioning. Am J Physiol. 2008;295:H1330-H1340.
16. Jha S, Calvert JW, Duranski MR, Ramachandran A, Lefer DJ. Hydrogen, sulfide attenuates hepatic ischemia-reperfusion injury: role of antioxidant and antiapoptotic signaling. Am J Physiol. 2008;295:H801-H806.
17. Tripatara P, SA Patel N, Collino M, Gallicchio M, Kieswich. J, Castiglia S, Benetti E, Stewart KN, Brown PA, Yaqoob MM, Fantozzi R, Thiemermann C. Generation of endogenous hydrogen, sulfide by cystathionine y-lyase limits renal ischemia/reperfusion injury and dysfunction. Lab Invest. 2008;88:1038-1048.
18. 18. Abella BS, Zhao D, Alvarado J, Hamann K, Vanden Hoek TL, Becker LB. Intra-arrest cooling improves outcomes in a murine cardiac arrest model. Circulation. 2004;109:2786-2791. (Pubitemid 38744554)
19. Nishida T, Yu JD, Minamishima S, Sips PY, Searles RJ, Buys ES, Janssens S, Brouckaert P, Bloch KD, Ichinose F. Protective effects of nitric oxide synthase 3 and soluble guanylate cyclase on the outcome of cardiac arrest and cardiopulmonary resuscitation in mice. Crit Care Med. 2009;37:256-262.
20. 20. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA, Brunskill EW, Sayen MR, Gottlieb RA, Dorn GW, Robbins J, Molkentin JD. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition, in cell death. Nature. 2005;434:658-662. (Pubitemid 40488559)
21. 21. Kofler J, Hattori K, Sawada M, DeVries AC, Martin LJ, Hum. PD, Traystman RJ. Histopathological and behavioral characterization of a novel model of cardiac arrest and cardiopulmonary resuscitation in mice. J Neurosa Methods. 2004;136:33-44. (Pubitemid 38569869)
22. Hausenloy DJ, Yellon DM. New directions for protecting the heart against ischaemia-reperfusion injury: targeting the reperfusion, injury salvage kinase (RISK)-pathway. Cardiovasc Res. 2004;61:448-460.
23. 23. Young LH, Li J, Baron SJ, Russell RR. AMP-activated protein kinase: a key stress signaling pathway in the heart. Trends Cardiovasc Med. 2005; 15:110-118. (Pubitemid 41021735)
24. 24. Doeller JE, Isbell TS, Benavides G, Koenitzer J, Patel H, Patel RP, Lancaster JR Jr, Darley-Usmar VM, Kraus DW. Polarographic measurement of hydrogen, sulfide production and consumption by mammalian, tissues. Anal Biochem. 2005;341:40-51. (Pubitemid 40615718)
25. 25. Yang G, Yang W, Wu L, Wang R. H2S, endoplasmic reticulum stress, and apoptosis of insulin-secreting beta cells. J Biol Chem 2007;282:16567-16576. (Pubitemid 47100397)
26. 26. Tong H, Imahashi K, Steenbergen C, Murphy E. Phosphorylation of glycogen synthase kinase-3β during preconditioning through a phosphatidylinositol-3-kinase-dependent pathway is cardioprotective. Circ Res. 2002;90:377-379. (Pubitemid 34633905)
27. Das A, Xi L, Kukreja RC. Protein, kinase G-dependent cardioprotective mechanism of phosphodiesterase-5 inhibition involves phosphorylation of ERK and GSK3β. J Biol Chem. 2008;283: 29572-29585.
28. 28. Cohen MV, Yang XM, Downey JM. The pH hypothesis of postconditioning: staccato reperfusion reintroduces oxygen, and perpetuates myocardial acidosis. Circulation. 2007;115:1895-1903. (Pubitemid 46598903)
29. 29. Tsujimoto Y, Shimizu S. Role of the mitochondrial membrane permeability transition in cell death. Apoptosis. 2007;12:835-840. (Pubitemid 46653286)
30. 30. Pan TT, Feng ZN, Lee SW, Moore PK, Bian JS. Endogenous hydrogen sulfide contributes to the cardioprotection by metabolic inhibition preconditioning in the rat ventricular myocytes. J Mol Cell Cardiol. 2006;40:119-130. (Pubitemid 43012123)