Protein S-nitrosylation: A role of nitric oxide signaling in cardiac ischemic preconditioning

( views:82, downloads:0 )
Author:
Junhui SUN(Junhui SUN,Corresponding author. Tel: +1-301-4968192; Fax: +1-301-4020190; Email: sun1@mail.nih.gov)
Journal Title:
ACTA PHYSIOLOGICA SINICA
Issue:
Volume 59, Issue 05, 2007
DOI:
Key Word:
S-nitrosylation; ischemic preconditioning; nitric oxide; cardioprotection

Abstract: Nitric oxide (NO) has been shown as an important signaling messenger involved in cardioprotection of ischemic preconditioning (IPC). To date, most studies suggest that NO might provide its protective effects by regulating the mitochondrial ATP-sensitive potassium (KATP) channel via the classic NO/cGMP-dependent pathway. However, there is emerging data suggesting that NO might also elicit its physiological role through protein S-nitrosylation. Protein S-nitrosylation, the covalent attachment of an NO moiety to sulfhydryl group(s) of cysteine residue(s) of proteins, is a reversible post-translational protein modification involved in redox-based cellular signaling. IPC has been found to increase S-nitrosothiol content and result in increased S-nitrosylation of proteins, which not only induces the structural and functional changes of modified proteins, but also prevents the target cysteine residue(s) from the further oxidative modification. In addition, S-nitrosothiols could elicit pharmacological preconditioning effect and protect against myocardial ischemia-reperfusion injury. Thus, protein S-nitrosylation is emerging as an important contributor to cardioprotection in IPC, providing protection from cellular oxidative and nitrosative stress.

  • [1]Murry C,Jennings R,Reimer K.Preconditioning with ischemia:a delay of lethal cell injury in ischemic myocardium.Circulation 1986; 74:1124-1136.
  • [2]Yellon DM,Downey JM.Preconditioning the myocardium:from cellular physiology to clinical cardiology.Physiol Rev 2003; 83:1113-1151.
  • [3]Bolli R.Preconditioning:a paradigm shift in the biology of myocardial ischemia.Am J Physiol 2007; 292:H19-H27.
  • [4]Hausenloy DJ,Yellon DM.Survival kinases in ischemic preconditioning and postconditioning.Cardiovasc Res 2006; 70:240-253.
  • [5]Das DK,Maulik N.Preconditioning potentiates redox signaling and converts death signal into survival signal.Arch Biochem Biophys 2003; 420:305-311.
  • [6]Saini HK,Machackova J,Dhalla NS.Role of reactive oxygen species in ischemic preconditioning of subcellular organelles in the heart.Antioxid Redox Signal 2004; 6:393-404.
  • [7]Cohen MV,Yang XM,Downey JM.Nitric oxide is a preconditioning mimetic and cardioprotectant and is the basis of many available infarct-sparing strategies.Cardiovasc Res 2006; 70:231-239.
  • [8]Jones SP,Bolli R.The ubiquitous role of nitric oxide in cardioprotection.J Mol Cell Cardiol 2006; 40:16-23.
  • [9]Seddon M,Shah AM,Casadei B.Cardiomyocytes as effectors of nitric oxide signalling.Cardiovasc Res 2007; 75:315-326.
  • [10]Belge C,Massion PB,Pelat M,Balligand JL.Nitric oxide and the heart:update on new paradigms.Ann NY Acad Sci 2005; 1047:173-182.
  • [11]Hare JM,Stamler JS.NO/redox disequilibrium in the failing heart and cardiovascular system.J Clin Invest 2005; 115:509-517.
  • [12]Schulz R,Kelm M,Heusch G.Nitric oxide in myocardial ischemia/reperfusion injury.Cardiovasc Res 2004; 61:402-413.
  • [13]Hess DT,Matsumoto A,Kim SO,Marshall HE,Stamler JS.Protein S-nitrosylation:purview and parameters.Nat Rev Mol Cell Biol 2005; 6:150-166.
  • [14]Martinez-Ruiz A,Lamas S.S-nitrosylation:a potential new paradigm in signal transduction.Cardiovasc Res 2004; 62:43-52.
  • [15]Sun J,Steenbergen C,Murphy E.S-nitrosylation:NO-related redox signaling to protect against oxidative stress.Antioxid Redox Signal 2006; 8:1693-1705.
  • [16]Marina Prendes MG,Gonzalez M,Savino EA,Varela A.Role of endogenous nitric oxide in classic preconditioning in rat hearts.Regul Pept 2007; 139:141-145.
  • [17]Andelova E,Bartekova M,Pancza D,Styk J,Ravingerova T.The role of NO in ischemia/reperfusion injury in isolated rat heart.Gen Physiol Biophys 2005; 24:411-426.
  • [18]Lochner A,Marais E,Du Toit E,Moolman J.Nitric oxide triggers classic ischemic preconditioning.Ann NY Acad Sci 2002;962:402-414.
  • [19]Cuong DV,Kim N,Youm JB,Joo H,Warda M,Lee J,Park WS,Kim T,Kang S,Kim H,Han J.Nitric oxide-cGMP-protein kinase G signaling pathway induces anoxic preconditioning through activation of ATP-sensitive K+ channels in rat hearts.Am J Physiol 2006; 290:H1808-H1817.
  • [20]Jaburek M,Costa AD,Burton JR,Costa CL,Garlid KD.Mitochondrial PKCε and mitochondrial ATP-sensitive K+ channel copurify and coreconstitute to form a functioning signaling module in proteoliposomes.Circ Res 2006; 99:878-883.
  • [21]Atar S,Ye Y,Lin Y,Freeberg SY,Nishi SP,Rosanio S,Huang M,Uretsky BF,Perez-Polo JR,Birnbaum Y.Atorvastatin-induced cardioprotection is mediated by increasing inducible nitric oxide synthase and consequent S-nitrosylation of cyclooxygenase-2.Am J Physiol 2006; 290:H1960-H1968.
  • [22]Burwell LS,Nadtochiy SM,Tompkins AJ,Young S,Brookes PS.Direct evidence for S-nitrosation of mitochondrial complex I.Biochem J 2006; 394:627-634.
  • [23]Nadtochiy SM,Burwell LS,Brookes PS.Cardioprotection and mitochondrial S-nitrosation:Effects of S-nitroso-2-mercaptopropionyl glycine (SNO-MPG) in cardiac ischemia-reperfusion injury.J Mol Cell Cardiol 2007; 42:812-825.
  • [24]Hess DT,Matsumoto A,Nudelman R,Stamler JS.S-nitrosylation:spectrum and specificity.Nat Cell Biol 2001; 3:E46-E49.
  • [25]Derakhshan B,Hao G,Gross SS.Balancing reactivity against selectivity:The evolution of protein S-nitrosylation as an effector of cell signaling by nitric oxide.Cardiovasc Res 2007; 75:210-219.
  • [26]Iwakiri Y,Satoh A,Chatterjee S,Toomre DK,Chalouni CM,Fulton D,Groszmann RJ,Shah VH,Sessa WC.Nitric oxide synthase generates nitric oxide locally to regulate compartmentalized protein S-nitrosylation and protein trafficking.Proc Natl Acad Sci USA 2006; 103:19777-19782.
  • [27]Dawn B,Bolli R.Role of nitric oxide in myocardial preconditioning.Ann NY Acad Sci 2002; 962:18-41.
  • [28]Eu JP,Sun J,Xu L,Stamler G,Meissner G.The skeletal muscle calcium release channel:coupled O2 sensor and NO signaling functions.Cell 2000; 102:499-509.
  • [29]Gow A,Doctor A,Mannick J,Gaston B.S-Nitrosothiol measurements in biological systems.J Chromatog B 2007; 851:140-151.
  • [30]Zhang Y,Hogg N.S-Nitrosothiols:cellular formation and transport.Free Rad Biol Med 2005; 38:831-838.
  • [31]Ghelardoni S,Frascarelli S,Ronca-Testoni S,Zucchi R.S-Nitrosothiol detection in isolated perfused rat heart.Mol Cell Biochem 2003; 252:347-351.
  • [32]Sun J,Picht E,Ginsburg KS,Bers DM,Steenbergen C,Murphy E.Hypercontractile female hearts exhibit increased S-Nitrosylation of the L-type Ca2+ channel α1 subunit and reduced ischemia/reperfusion injury.Circ Res 2006; 98:403-411.
  • [33]Sun J,Morgan M,Shen R,Steenbergen C,Murphy E.Preconditioning results in S-nitrosylation of proteins involved in regulation of mitochondrial energetics and calcium transport.Circ Res 2007;in press.
  • [34]Jaffrey SR,Snyder SH.The biotin switch method for the detection of S-nitrosylated proteins.Sci STKE 2001; 86:PL1.
  • [35]Kettenhofen NJ,Broniowska KA,Keszler A,Zhang Y,Hogg N.Proteomic methods for analysis of S-nitrosation.J Chromatog B 2007; 851:152-159.
  • [36]Lowenstein CJ.Nitric oxide regulation of protein trafficking in the cardiovascular system.Cardiovasc Res 2007; 75:240-246.
  • [37]Whalen EJ,Foster MW,Matsumoto A,Ozawa K,Violin JD,Que LG,Nelson CD,Benhar M,Keys JR,Rockman HA,Koch WJ,Daaka Y,Lefkowitz RJ,Stamler JS.Regulation of β-adrenergic receptor signaling by S-nitrosylation of G-proteincoupled receptor kinase 2.Cell 2007; 129:511-522.
  • [38]Hare JM.Nitric oxide and excitation-contraction coupling.J Mol Cell Cardiol 2003; 35:719-729.
  • [39]Zima AV,Blatter LA.Redox regulation of cardiac calcium channels and transporters.Cardiovasc Res 2006; 71:310-321.
  • [40]Morad M,Suzuki YJ.Redox regulation of cardiac muscle calcium signaling.Antioxid Redox Signal 2000; 2:65-71.
  • [41]Barouch LA,Harrison RW,Skaf MW,Rosas GO,Cappola TP,Kobeissi ZA,Hobai,IA,Lemmon CA,Bumett AL,O'Rourke B,Rodriguez ER,Huang PL,Lima JA,Berkowitz DE,Hare JM.Nitric oxide regulates the heart by spatial confinement of nitric oxide synthase isoforms.Nature 2002; 416:337-339.
  • [42]Xu KY,Huso DL,Dawson TM,Bredt DS,Becker LC.Nitric oxide synthase in cardiac sarcoplasmic reticulum.Proc Natl Acad Sci USA 1999; 96:657-662.
  • [43]Feron O,Dessy C,Opel DJ,Arstall MA,Kelly RA,Michel T.Modulation of the endothelial nitric oxide synthase-caveolin interaction in cardiac myocytes.Implications for the autonomic regulation of heart rate.J Biol Chem 1998; 273:30249-30254.
  • [44]Feron O,Balligand JL.Caveolins and the regulation of endothelial nitric oxide synthase in the heart.Cardiovasc Res 2006; 69:788-797.
  • [45]Cartwright EJ,Oceandy D,Neyses L.Plasma membrane calcium ATPase and its relationship to nitric oxide signaling in the heart.Ann NY Acad Sci 2007; 1099:247-253.
  • [46]Xu L,Eu JP,Meissner G,Stamler JS.Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitrosylation.Science 1998; 279:234-237.
  • [47]Triggle D.L-type calcium channel.Curr Pharm Des 2006; 12:443-457.
  • [48]Cohen RA,Adachi T.Nitric oxide-induced vasodilatation:regulation by physiologic S-glutathiolation and pathologic oxidation of the sarcoplasmic endoplasmic reticulum calcium ATPase.Trends Cardiovasc Med 2006; 16:109-114.
  • [49]Zucchi R,Ronca R,Ronca-Testoni S.Modulation of sarcoplasmic reticulum function:a new strategy in cardioprotection?Pharmacol Ther 2001; 89:47-65.
  • [50]Piper HM,Kasseckert S,Abdallah Y.The sarcoplasmic reticulum as the primary target of reperfusion protection.Cardiovasc Res 2006; 70:170-173.
  • [51]Adachi T,Weibrod RM,Pimentel DR,Ying J,Sharov VS,Schoneich C,Cohen RA.S-Glutathiolation by peroxynitrite activates SERCA during arterial relaxation by nitric oxide.Nat Med 2004; 10:1200-1207.
  • [52]Martinez-Ruiz A,Lamas S.Signalling by NO-induced protein S-nitrosylation and S-glutathionylation:convergences and divergences.Cardiovasc Res 2007; 75:220-228.
  • [53]Halestrap AP.Calcium,mitochondria and reperfusion injury:a pore way to die.Biochem Soc Trans 2006; 34:232-237.
  • [54]Steenbergen C,Perlman ME,London RE,Murphy E.Mechanism of preconditioning.Ionic alterations.Circ Res 1993; 72:112-125.
  • [55]Grove GJ,Atwal KS,Sleph PG,Wang FL,Monshizadegan H,Monticello T,Green DW.Excessive ATP hydrolysis in ischemic myocardium by mitochondrial F1F0-ATPase:effect of selective pharmacological inhibition of mitochondrial ATPase hydrolase activity.Am J Physiol 2004; 287:H1747-H1755.
  • [56]Vander Heide RS,Hill ML,Reimer KA,Jennings RB.Effect of reversible ischemia on the activity of the mitochondrial ATPase:relationship to ischemic preconditioning.J Mol Cell Cardiol 1996;28:103-112.
  • [57]Lundberg KC,Szweda LI.Preconditioning prevents loss in mitochondrial function and release of cytochrome c during prolonged cardiac ischemia/reperfusion.Arch Biochem Biophys 2006; 453:130-134.
  • [58]Weiss RG,de Albuquerque CP,Vandegaer K,Chacko VP,Gerstenblith G.Attenuated glycogenolysis reduces glycolytic catabolite accumulation during ischemia in preconditioned rat hearts.Circ Res 1996; 79:435-446.
  • [59]Leist M,Single B,Naumann H,Fava E,Simon B,Kuhnle S,Nicotera P.Inhibition of mitochondrial ATP generation by nitric oxide switches apoptosis to necrosis.Exp Cell Res 1999; 249:396-403.
  • [60]Zhang J,Jin B,Li L,Block ER,Patel JM.Nitric oxide-induced persistent inhibition and nitrosylation of active site cysteine residues of mitochondrial cytochrome-c oxidase in lung endothelial cells.Am J Physiol 2005; 288:C840-C849.
  • [61]Mohr S,Hallak H,de Boitte A,Lapetina EG,Brune B.Nitric oxide-induced S-glutathionylation and inactivation of glyceraldehyde-3-phosphate dehydrogenase.J Biol Chem 1999; 274:9427-9430.
  • [62]Moon KH,Kim B J,Song BJ.Inhibition of mitochondrial aldehyde dehydrogenase by nitric oxide-mediated S-nitrosylation.FEBS Lett 2005; 579:6115-6120.
  • [63]Arstall MA,Bailey C,Gross WL,Bak M,Balligand JL,Kelly RA.Reversible S-nitrosation of creatine kinase by nitric oxide in adult rat ventricular myocytes.J Mol Cell Cardiol 1998; 30:979-988.
  • [64]Berthonneche C,Toufektsian MC,Tanguy S,Ghezzi C,Leiris JD,Boucher F.Does nitric oxide contribute to progressive cardiac tissue damage and dysfunction after infarction? Antioxid Redox Signal 2007; 9:757-763.
  • [65]Passeri J,Bloch KD.Nitric oxide and cardiac remodeling.Heart Fail Clin 2005; 1:275-286.
  • [66]Massion PB,Balligand JL.Relevance of nitric oxide for myocardial remodeling.Curr Heart Fail Rep 2007; 4:18-25.
  • [67]Lange S,Agarkova I,Perriard JC,Ehler E.The sarcomeric M-band during development and in disease.J Muscle Res Cell Motil 2005; 26:375-379.
  • [68]Machackova J,Barta J,Dhalla NS.Myofibrillar remodeling in cardiac hypertrophy,heart failure and cardiomyopathies.Can J Cardiol 2006; 22:953-968.
  • [69]Melino G,Catani MV,Corazzari M,Guerrieri P,Bernassola F.Nitric oxide can inhibit apoptosis or switch it into necrosis.Cell Mol Life Sci 2000; 57:612-622.
  • [70]Mannick JB.Regulation of apoptosis by protein S-nitrosylation.Amino Acids 2007; 32:523-526.
  • [71]Melino G,Bernassola F,Knight RA,Corasaniti MT,Nistico G,Finazzi-Agro A.S-nitrosylation regulates apoptosis.Nature 1997; 388:432-433.
  • [72]Maejima Y,Adachi S,Morikawa K,Ito H,Isobe M.Nitric oxide inhibits myocardial apoptosis by preventing caspase-3 activity via S-nitrosylation.J Mol Cell Cardiol 2005; 38:163-174.
  • [73]Piot CA,Martini JF,Bui SK,Wolfe CL.Ischemic preconditioning attenuates ischemia/reperfusion-induced activation of caspases and subsequent cleavage of poly(ADP-ribose) polymerase in rat hearts in vivo.Cardiovasc Res 1999; 44:536-542.
  • [74]LaPointe MC,Mendez M,Leung A,Tao Z,Yang XP.Inhibition of cyclooxygenase-2 improves cardiac function after myocardial infarction in the mouse.Am J Physiol 2004; 286:H1416-H1424.
  • [75]Bolli R,Shinmura K,Tang XL,Kodani E,Xuan YT,Guo Y,Dawn B.Discovery of a new function of cyclooxygenase (COX)-2:COX-2 is a cardioprotective protein that alleviates ischemia/reperfusion injury and mediates the late phase of preconditioning.Cardiovasc Res 2002; 55:506-519.
  • [76]Lai TS,Hausladen A,Slaughter TF,Eu JP,Stamler JS,Greenberg CS.Calcium regulates S-nitrosylation,denitrosylation,and activity of tissue transglutaminase.Biochemistry 2001; 40:4904-4910.
  • [77]Das DK.Thioredoxin regulation of ischemic preconditioning.Antioxid Redox Signal 2004; 6:405-412.
  • [78]Tao L,Gao E,Bryan NS,Qu Y,Liu H,Hu A,Christopher TA,Lopez BL,Yodoi J,Koch WJ,Feelisch M,Ma XL.Cardioprotective effects of thioredoxin in myocardial ischemia and reperfusion:role of S-nitrosafion.Proc Natl Acad Sci USA 2004; 101:11471-11476.
  • [79]Hoffmann J,Dimmeler S,Haendeler J.Shear stress increases the amount of S-nitrosylated molecules in endothelial cells:important role for signal transduction.FEBS Lett 2003; 551:153-158.
  • [80]Haendeler J,Hoffmann J,Tischler V,Berk BC,Zeiher AM,Dimmeler S.Redox regulatory and anti-apoptotic functions of thioredoxin depend on S-nitrosylation at cysteine 69.Nat Cell Biol 2002; 4:743-749.
  • [81]Sumbayev VV.S-nitrosylation of thioredoxin mediates activation of apoptosis signal-regulating kinase 1.Arch Biochem Biophys 2003; 415:133-136.
  • [82]Yasinska IM,Kozhukhar AV,Sumbayev VV.S-Nitrosation of thioredoxin in the nitrogen monoxide/superoxide system activates apoptosis signal-regulating kinase 1.Arch Biochem Biophys 2004; 428:198-203.
  • [83]Selemidis S,Dusting GJ,Peshavariya H,Kemp-Harper BK,Drummond GR.Nitric oxide suppresses NADPH oxidase-dependent superoxide production by S-nitrosylation in human endothelial cells.Cardiovasc Res 2007; 75:349-358.
  • [84]Hausenloy DJ,Tsang A,Mocanu MM,Yellon DM.Ischemic preconditioning protects by activating prosurvival kinases at reperfusion.Am J Physiol 2005; 288:H971-H976.
  • [85]Oudit GY,Sun H,Kerfant BG,Crackower MA,Penninger JM,Backx PH.The role of phosphoinositide-3 kinase and PTEN in cardiovascular physiology and disease.J Mol Cell Cardiol 2004;37:449-471.
  • [86]Lim S,Clement MV.Phosphorylation of the survival kinase Akt by superoxide is dependent on an ascorbate-reversible oxidation of PTEN.Free Rad Biol Med 2007; 42:1178-1192.
  • [87]Carver DJ,Gaston B,deRonde K,Palmer LA.Akt-mediated activation of HIF-1 in pulmonary vascular endothelial cells by S-nitrosoglutathione.Am J Respir Cell Mol Biol 2007; 37:255-263.
  • [88]Li F,Sonveaux P,Rabbani ZN,Liu S,Yan B,Huang Q,Vujaskovic Z,Dewhirst MW,Li CY.Regulation of HIF-lalpha stability through S-nitrosylation.Mol Cell 2007; 26:63-74.
  • [89]Marshall HE,Stamler JS.Inhibition of NF-κB by S-Nitrosylation.Biochemistry 2001; 40:1688-1693.
  • [90]Reynaert NL,Ckless K,Korn SH,Vos N,Guala AS,Wouters EF,van der Vliet A,Janssen-Heininger YM.Nitric oxide represses inhibitory κB kinase through S-nitrosylation.Proc Natl Acad Sci USA 2004; 101:8945-8950.
  • [91]Tong H,Rockman HA,Koch WJ,Steenbergen C,Murphy E.G protein-coupled receptor internalization signaling is required for cardioprotection in ischemic preconditioning.Circ Res 2004;94:1133-1141.
  • [92]Cheng F,Mani K,van den Born J,Ding K,Belting M,Fransson LA.Nitric oxide-dependent processing of heparan sulfate in recycling S-nitrosylated glypican-1 takes place in caveolin-1-con-taining endosomes.J Biol Chem 2002; 277:44431-44439.
  • [93]Williams JG,Pappu K,Campbell SL.Structural and biochemical studies of p21Ras S-nitrosylation and nitric oxide-mediated guanine nucleotide exchange.Proc Natl Acad Sci USA 2003; 100:6376-6381.
  • [94]Matsushita K,Morrell CN,Cambien B,Yang S,Yamakuchi M,Bao C,Hara MR,Quick RA,Cao W,O'Rourke B,Lowenstein JM,Pevsner J,Wagner DD,Lowenstein CJ.Nitric oxide regulates exocytosis by S-nitrosylation of N-ethylmaleimide-sensitive factor.Cell 2003; 115:139-150.
  • [95]Uehara T,Nakamura T,Yao D,Shi Z,Gu Z,Ma Y,Masliah E,Nomura Y,Lipton SA.S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration.Nature 2006; 441:513-517.
  • [96]Wang G,Moniri NH,Ozawa K,Stamler JS,Daaka Y.Nitric oxide regulates endocytosis by S-nitrosylation of dynamin.Proc Natl Acad Sci USA 2006; 103:1295-1300.
  • [97]Kang-Decker N,Cao S,Chatterjee S,Yao J,Egan LJ,Semela D,Mukhopadhyay D,Shah V.Nitric oxide promotes endothelial cell survival signaling through S-nitrosylation and activation of dynamin-2.J Cell Sci 2007; 120:492-501.
  • [98]Asanuma H,Nakai K,Sanada S,Minamino T,Takashima S,Ogita H,Fujita M,Hirata A,Wakeno M,Takahama H,Kim J,Asakura M,Sakuma I,Kitabatake A,Hori M,Komamura K,Kitakaze M.S-nitrosylated and pegylated hemoglobin,a newly developed artificial oxygen carrier,exerts cardioprotection against ischemic hearts.J Mol Cell Cardiol 2007; 42:924-930.
WanfangData CO.,Ltd All Rights Reserved
About WanfangData | Contact US
Healthcare Department, Fuxing Road NO.15, Haidian District Beijing, 100038 P.R.China
Tel:+86-010-58882616 Fax:+86-010-58882615 Email:yiyao@wanfangdata.com.cn