Enzymatic mechanisms regulating protein S-nitrosylation: implications in health and disease (original) (raw)
References
Benhar M, Forrester MT, Stamler JS (2009) Protein denitrosylation: enzymatic mechanisms and cellular functions. Nat Rev Mol Cell Biol 10:721–732 PubMedCAS Google Scholar
Murad F (1986) Cyclic guanosine monophosphate as a mediator of vasodilation. J Clin Invest 78:1–5 ArticlePubMedCAS Google Scholar
Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS (2005) Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 6:150–166 ArticlePubMedCAS Google Scholar
Foster MW, McMahon TJ, Stamler JS (2003) S-nitrosylation in health and disease. Trends Mol Med 9:160–168 ArticlePubMedCAS Google Scholar
Perez-Mato I, Castro C, Ruiz FA, Corrales FJ, Mato JM (1999) Methionine adenosyltransferase S-nitrosylation is regulated by the basic and acidic amino acids surrounding the target thiol. J Biol Chem 274:17075–17079 ArticlePubMedCAS Google Scholar
Savidge TC, Urvil P, Oezguen N, Ali K, Choudhury A, Acharya V, Pinchuk I, Torres AG, English RD, Wiktorowicz JE et al (2011) Host S-nitrosylation inhibits clostridial small molecule-activated glucosylating toxins. Nat Med 17:1136–1141 ArticlePubMedCAS Google Scholar
Seth D, Stamler JS (2011) The SNO-proteome: causation and classifications. Curr Opin Chem Biol 15:129–136 ArticlePubMedCAS Google Scholar
Stamler JS, Toone EJ, Lipton SA, Sucher NJ (1997) (S)NO signals: translocation, regulation, and a consensus motif. Neuron 18:691–696 ArticlePubMedCAS Google Scholar
Kim SF, Huri DA, Snyder SH (2005) Inducible nitric oxide synthase binds, S-nitrosylates, and activates cyclooxygenase-2. Science 310:1966–1970 ArticlePubMedCAS Google Scholar
Nedospasov A, Rafikov R, Beda N, Nudler E (2000) An autocatalytic mechanism of protein nitrosylation. Proc Natl Acad Sci USA 97:13543–13548 ArticlePubMedCAS Google Scholar
Foster MW, Forrester MT, Stamler JS (2009) A protein microarray-based analysis of S-nitrosylation. Proc Natl Acad Sci USA 106:18948–18953 ArticlePubMedCAS Google Scholar
Doulias PT, Greene JL, Greco TM, Tenopoulou M, Seeholzer SH, Dunbrack RL, Ischiropoulos H (2010) Structural profiling of endogenous S-nitrosocysteine residues reveals unique features that accommodate diverse mechanisms for protein S-nitrosylation. Proc Natl Acad Sci USA 107:16958–16963 ArticlePubMedCAS Google Scholar
Marino SM, Gladyshev VN (2010) Structural analysis of cysteine S-nitrosylation: a modified acid-based motif and the emerging role of trans-nitrosylation. J Mol Biol 395:844–859 ArticlePubMedCAS Google Scholar
Foster MW, Stamler JS (2004) New insights into protein S-nitrosylation. Mitochondria as a model system. J Biol Chem 279:25891–25897 ArticlePubMedCAS Google Scholar
Bosworth CA, Toledo JC Jr, Zmijewski JW, Li Q, Lancaster JR Jr (2009) Dinitrosyliron complexes and the mechanism(s) of cellular protein nitrosothiol formation from nitric oxide. Proc Natl Acad Sci 106:4671–4676 ArticlePubMedCAS Google Scholar
Foster MW, Liu L, Zeng M, Hess DT, Stamler JS (2009) A genetic analysis of nitrosative stress. Biochemistry 48:792–799 ArticlePubMedCAS Google Scholar
Jia L, Bonaventura C, Bonaventura J, Stamler JS (1996) S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature 380:221–226 ArticlePubMedCAS Google Scholar
Gow AJ, Stamler JS (1998) Reactions between nitric oxide and haemoglobin under physiological conditions. Nature 391:169–173 ArticlePubMedCAS Google Scholar
Basu S, Keszler A, Azarova NA, Nwanze N, Perlegas A, Shiva S, Broniowska KA, Hogg N, Kim-Shapiro DB (2010) A novel role for cytochrome c: efficient catalysis of S-nitrosothiol formation. Free Radic Biol Med 48:255–263 ArticlePubMedCAS Google Scholar
Inoue K, Akaike T, Miyamoto Y, Okamoto T, Sawa T, Otagiri M, Suzuki S, Yoshimura T, Maeda H (1999) Nitrosothiol formation catalyzed by ceruloplasmin. Implication for cytoprotective mechanism in vivo. J Biol Chem 274:27069–27075 ArticlePubMedCAS Google Scholar
Mani K, Cheng F, Havsmark B, David S, Fransson LA (2004) Involvement of glycosylphosphatidylinositol-linked ceruloplasmin in the copper/zinc-nitric oxide-dependent degradation of glypican-1 heparan sulfate in rat C6 glioma cells. J Biol Chem 279:12918–12923 ArticlePubMedCAS Google Scholar
Petersen MG, Dewilde S, Fago A (2008) Reactions of ferrous neuroglobin and cytoglobin with nitrite under anaerobic conditions. J Inorg Biochem 102:1777–1782 ArticlePubMedCAS Google Scholar
Weichsel A, Maes EM, Andersen JF, Valenzuela JG, Shokhireva T, Walker FA, Montfort WR (2005) Heme-assisted S-nitrosation of a proximal thiolate in a nitric oxide transport protein. Proc Natl Acad Sci USA 102:594–599 ArticlePubMedCAS Google Scholar
Singel DJ, Stamler JS (2005) Chemical physiology of blood flow regulation by red blood cells: the role of nitric oxide and S-nitrosohemoglobin. Annu Rev Physiol 67:99–145 ArticlePubMedCAS Google Scholar
Pawloski JR, Hess DT, Stamler JS (2001) Export by red blood cells of nitric oxide bioactivity. Nature 409:622–626 ArticlePubMedCAS Google Scholar
Pawloski JR, Hess DT, Stamler JS (2005) Impaired vasodilation by red blood cells in sickle cell disease. Proc Natl Acad Sci USA 102:2531–2536 ArticlePubMedCAS Google Scholar
Reynolds JD, Ahearn GS, Angelo M, Zhang J, Cobb F, Stamler JS (2007) S-nitrosohemoglobin deficiency: a mechanism for loss of physiological activity in banked blood. Proc Natl Acad Sci USA 104:17058–17062 ArticlePubMedCAS Google Scholar
McMahon TJ, Ahearn GS, Moya MP, Gow AJ, Huang YC, Luchsinger BP, Nudelman R, Yan Y, Krichman AD, Bashore TM et al (2005) A nitric oxide processing defect of red blood cells created by hypoxia: deficiency of S-nitrosohemoglobin in pulmonary hypertension. Proc Natl Acad Sci USA 102:14801–14806 ArticlePubMedCAS Google Scholar
Liu L, Yan Y, Zeng M, Zhang J, Hanes MA, Ahearn G, McMahon TJ, Dickfeld T, Marshall HE, Que LG et al (2004) Essential roles of S-nitrosothiols in vascular homeostasis and endotoxic shock. Cell 116:617–628 ArticlePubMedCAS Google Scholar
Crawford JH, Chacko BK, Pruitt HM, Piknova B, Hogg N, Patel RP (2004) Transduction of NO-bioactivity by the red blood cell in sepsis: novel mechanisms of vasodilation during acute inflammatory disease. Blood 104:1375–1382 ArticlePubMedCAS Google Scholar
Doctor A, Platt R, Sheram ML, Eischeid A, McMahon T, Maxey T, Doherty J, Axelrod M, Kline J, Gurka M et al (2005) Hemoglobin conformation couples erythrocyte S-nitrosothiol content to O2 gradients. Proc Natl Acad Sci USA 102:5709–5714 ArticlePubMedCAS Google Scholar
Erzurum SC, Ghosh S, Janocha AJ, Xu W, Bauer S, Bryan NS, Tejero J, Hemann C, Hille R, Stuehr DJ et al (2007) Higher blood flow and circulating NO products offset high-altitude hypoxia among Tibetans. Proc Natl Acad Sci USA 104:17593–17598 ArticlePubMedCAS Google Scholar
Janocha AJ, Koch CD, Tiso M, Ponchia A, Doctor A, Gibbons L, Gaston B, Beall CM, Erzurum SC (2011) Nitric oxide during altitude acclimatization. N Engl J Med 365:1942–1944 ArticlePubMedCAS Google Scholar
Tristan C, Shahani N, Sedlak TW, Sawa A (2011) The diverse functions of GAPDH: views from different subcellular compartments. Cell Signal 23:317–323 ArticlePubMedCAS Google Scholar
Hara MR, Agrawal N, Kim SF, Cascio MB, Fujimuro M, Ozeki Y, Takahashi M, Cheah JH, Tankou SK, Hester LD et al (2005) S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat Cell Biol 7:665–674 ArticlePubMedCAS Google Scholar
Kornberg MD, Sen N, Hara MR, Juluri KR, Nguyen JV, Snowman AM, Law L, Hester LD, Snyder SH (2010) GAPDH mediates nitrosylation of nuclear proteins. Nat Cell Biol 12:1094–1100 ArticlePubMedCAS Google Scholar
Salvesen GS, Duckett CS (2002) IAP proteins: blocking the road to death’s door. Nat Rev Mol Cell Biol 3:401–410 ArticlePubMedCAS Google Scholar
Nakamura T, Wang L, Wong CC, Scott FL, Eckelman BP, Han X, Tzitzilonis C, Meng F, Gu Z, Holland EA et al (2010) Transnitrosylation of XIAP regulates caspase-dependent neuronal cell death. Mol Cell 39:184–195 ArticlePubMedCAS Google Scholar
Cruz JC, Tsai LH (2004) A Jekyll and Hyde kinase: roles for Cdk5 in brain development and disease. Curr Opin Neurobiol 14:390–394 ArticlePubMedCAS Google Scholar
Qu J, Nakamura T, Cao G, Holland EA, McKercher SR, Lipton SA (2011) S-nitrosylation activates Cdk5 and contributes to synaptic spine loss induced by beta-amyloid peptide. Proc Natl Acad Sci USA 108:14330–14335 ArticlePubMedCAS Google Scholar
Cho DH, Nakamura T, Fang J, Cieplak P, Godzik A, Gu Z, Lipton SA (2009) S-nitrosylation of Drp1 mediates beta-amyloid-related mitochondrial fission and neuronal injury. Science 324:102–105 ArticlePubMedCAS Google Scholar
Lillig CH, Holmgren A (2007) Thioredoxin and related molecules—from biology to health and disease. Antioxid Redox Signal 9:25–47 ArticlePubMedCAS Google Scholar
Mitchell DA, Marletta MA (2005) Thioredoxin catalyzes the S-nitrosation of the caspase-3 active site cysteine. Nat Chem Biol 1:154–158 ArticlePubMedCAS Google Scholar
Mitchell DA, Morton SU, Fernhoff NB, Marletta MA (2007) Thioredoxin is required for S-nitrosation of procaspase-3 and the inhibition of apoptosis in Jurkat cells. Proc Natl Acad Sci USA 104:11609–11614 ArticlePubMedCAS Google Scholar
Wu C, Liu T, Chen W, Oka S, Fu C, Jain MR, Parrott AM, Baykal AT, Sadoshima J, Li H (2010) Redox regulatory mechanism of transnitrosylation by thioredoxin. Mol Cell Proteomics 9:2262–2275 ArticlePubMedCAS Google Scholar
Hashemy SI, Holmgren A (2008) Regulation of the catalytic activity and structure of human thioredoxin 1 via oxidation and S-nitrosylation of cysteine residues. J Biol Chem 283:21890–21898 ArticlePubMedCAS Google Scholar
Benhar M, Forrester MT, Hess DT, Stamler JS (2008) Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins. Science 320:1050–1054 ArticlePubMedCAS Google Scholar
Ito T, Yamakuchi M, Lowenstein CJ (2011) Thioredoxin increases exocytosis by denitrosylating _N_-ethylmaleimide-sensitive factor. J Biol Chem 286:11179–11184 ArticlePubMedCAS Google Scholar
Ovadia H, Haim Y, Nov O, Almog O, Kovsan J, Bashan N, Benhar M, Rudich A (2011) Increased adipocyte S-nitrosylation targets anti-lipolytic action of insulin: relevance to adipose tissue dysfunction in obesity. J Biol Chem 286:30433–30443 ArticlePubMedCAS Google Scholar
Forrester MT, Seth D, Hausladen A, Eyler CE, Foster MW, Matsumoto A, Benhar M, Marshall HE, Stamler JS (2009) Thioredoxin-interacting protein (Txnip) is a feedback regulator of S-nitrosylation. J Biol Chem 284:36160–36166 ArticlePubMedCAS Google Scholar
Benhar M, Thompson JW, Moseley MA, Stamler JS (2010) Identification of S-nitrosylated targets of thioredoxin using a quantitative proteomic approach. Biochemistry 49:6963–6969 ArticlePubMedCAS Google Scholar
Forrester MT, Thompson JW, Foster MW, Nogueira L, Moseley MA, Stamler JS (2009) Proteomic analysis of S-nitrosylation and denitrosylation by resin-assisted capture. Nat Biotechnol 27:557–559 ArticlePubMedCAS Google Scholar
Nikitovic D, Holmgren A (1996) S-nitrosoglutathione is cleaved by the thioredoxin system with liberation of glutathione and redox regulating nitric oxide. J Biol Chem 271:19180–19185 ArticlePubMedCAS Google Scholar
Stoyanovsky DA, Tyurina YY, Tyurin VA, Anand D, Mandavia DN, Gius D, Ivanova J, Pitt B, Billiar TR, Kagan VE (2005) Thioredoxin and lipoic acid catalyze the denitrosation of low molecular weight and protein S-nitrosothiols. J Am Chem Soc 127:15815–15823 ArticlePubMedCAS Google Scholar
Wu C, Parrott AM, Fu C, Liu T, Marino SM, Gladyshev VN, Jain MR, Baykal AT, Li Q, Oka S et al (2011) Thioredoxin 1-mediated post-translational modifications: reduction, transnitrosylation, denitrosylation, and related proteomics methodologies. Antioxid Redox Signal 15:2565–2604 ArticlePubMedCAS Google Scholar
Bateman RL, Rauh D, Tavshanjian B, Shokat KM (2008) Human carbonyl reductase 1 is an S-nitrosoglutathione reductase. J Biol Chem 283:35756–35762 ArticlePubMedCAS Google Scholar
Gaston B, Reilly J, Drazen JM, Fackler J, Ramdev P, Arnelle D, Mullins ME, Sugarbaker DJ, Chee C, Singel DJ et al (1993) Endogenous nitrogen oxides and bronchodilator S-nitrosothiols in human airways. Proc Natl Acad Sci USA 90:10957–10961 ArticlePubMedCAS Google Scholar
Jensen DE, Belka GK, Du Bois GC (1998) S-nitrosoglutathione is a substrate for rat alcohol dehydrogenase class III isoenzyme. Biochem J 331(Pt 2):659–668 PubMedCAS Google Scholar
Liu L, Hausladen A, Zeng M, Que L, Heitman J, Stamler JS (2001) A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410:490–494 ArticlePubMedCAS Google Scholar
Staab CA, Alander J, Brandt M, Lengqvist J, Morgenstern R, Grafstrom RC, Hoog JO (2008) Reduction of S-nitrosoglutathione by alcohol dehydrogenase 3 is facilitated by substrate alcohols via direct cofactor recycling and leads to GSH-controlled formation of glutathione transferase inhibitors. Biochem J 413:493–504 ArticlePubMedCAS Google Scholar
Paige JS, Xu G, Stancevic B, Jaffrey SR (2008) Nitrosothiol reactivity profiling identifies S-nitrosylated proteins with unexpected stability. Chem Biol 15:1307–1316 ArticlePubMedCAS Google Scholar
Que LG, Liu L, Yan Y, Whitehead GS, Gavett SH, Schwartz DA, Stamler JS (2005) Protection from experimental asthma by an endogenous bronchodilator. Science 308:1618–1621 ArticlePubMedCAS Google Scholar
Whalen EJ, Foster MW, Matsumoto A, Ozawa K, Violin JD, Que LG, Nelson CD, Benhar M, Keys JR, Rockman HA et al (2007) Regulation of beta-adrenergic receptor signaling by S-nitrosylation of G-protein-coupled receptor kinase 2. Cell 129:511–522 ArticlePubMedCAS Google Scholar
Ozawa K, Whalen EJ, Nelson CD, Mu Y, Hess DT, Lefkowitz RJ, Stamler JS (2008) S-nitrosylation of beta-arrestin regulates beta-adrenergic receptor trafficking. Mol Cell 31:395–405 ArticlePubMedCAS Google Scholar
Wei W, Li B, Hanes MA, Kakar S, Chen X, Liu L (2010) S-nitrosylation from GSNOR deficiency impairs DNA repair and promotes hepatocarcinogenesis. Sci Transl Med 2:19ra13 ArticlePubMedCAS Google Scholar
Choudhry S, Que LG, Yang Z, Liu L, Eng C, Kim SO, Kumar G, Thyne S, Chapela R, Rodriguez-Santana JR et al (2010) GSNO reductase and beta2-adrenergic receptor gene–gene interaction: bronchodilator responsiveness to albuterol. Pharmacogenet Genomics 20:351–358 ArticlePubMedCAS Google Scholar
Moore PE, Ryckman KK, Williams SM, Patel N, Summar ML, Sheller JR (2009) Genetic variants of GSNOR and ADRB2 influence response to albuterol in African-American children with severe asthma. Pediatr Pulmonol 44:649–654 ArticlePubMed Google Scholar
Wu H, Romieu I, Sienra-Monge JJ, Estela Del Rio-Navarro B, Anderson DM, Jenchura CA, Li H, Ramirez-Aguilar M, Del Carmen Lara-Sanchez I, London SJ (2007) Genetic variation in S-nitrosoglutathione reductase (GSNOR) and childhood asthma. J Allergy Clin Immunol 120:322–328 ArticlePubMedCAS Google Scholar
Que LG, Yang Z, Stamler JS, Lugogo NL, Kraft M (2009) S-nitrosoglutathione reductase: an important regulator in human asthma. Am J Respir Crit Care Med 180:226–231 ArticlePubMedCAS Google Scholar
Lima B, Lam GK, Xie L, Diesen DL, Villamizar N, Nienaber J, Messina E, Bowles D, Kontos CD, Hare JM et al (2009) Endogenous S-nitrosothiols protect against myocardial injury. Proc Natl Acad Sci USA 106:6297–6302 ArticlePubMedCAS Google Scholar
Sun X, Qiu J, Strong SA, Green LS, Wasley JW, Blonder JP, Colagiovanni DB, Mutka SC, Stout AM, Richards JP et al (2011) Discovery of potent and novel S-nitrosoglutathione reductase inhibitors devoid of cytochrome P450 activities. Bioorg Med Chem Lett 21:5849–5853 ArticlePubMedCAS Google Scholar
Sun X, Qiu J, Strong SA, Green LS, Wasley JW, Colagiovanni DB, Mutka SC, Blonder JP, Stout AM, Richards JP et al (2011) Structure–activity relationships of pyrrole based S-nitrosoglutathione reductase inhibitors: pyrrole regioisomers and propionic acid replacement. Bioorg Med Chem Lett 21:3671–3675 ArticlePubMedCAS Google Scholar
Colagiovanni DB, Drolet DW, Langlois-Forget E, Piche MP, Looker D, Rosenthal GJ (2011) A nonclinical safety and pharmacokinetic evaluation of N6022: a first-in-class S-nitrosoglutathione reductase inhibitor for the treatment of asthma. Regul Toxicol Pharmacol 62:115–124 ArticlePubMedCAS Google Scholar
Feechan A, Kwon E, Yun BW, Wang Y, Pallas JA, Loake GJ (2005) A central role for S-nitrosothiols in plant disease resistance. Proc Natl Acad Sci USA 102:8054–8059 ArticlePubMedCAS Google Scholar
Yun BW, Feechan A, Yin M, Saidi NB, Le Bihan T, Yu M, Moore JW, Kang JG, Kwon E, Spoel SH et al (2011) S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478:264–268 ArticlePubMedCAS Google Scholar
Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X (2008) Plant immunity requires conformational changes [corrected] of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–956 ArticlePubMedCAS Google Scholar
Chen R, Sun S, Wang C, Li Y, Liang Y, An F, Li C, Dong H, Yang X, Zhang J et al (2009) The Arabidopsis PARAQUAT RESISTANT2 gene encodes an S-nitrosoglutathione reductase that is a key regulator of cell death. Cell Res 19:1377–1387 ArticlePubMedCAS Google Scholar
Lee U, Wie C, Fernandez BO, Feelisch M, Vierling E (2008) Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in Arabidopsis. Plant cell 20:786–802 ArticlePubMedCAS Google Scholar
Jourd’heuil D, Laroux FS, Miles AM, Wink DA, Grisham MB (1999) Effect of superoxide dismutase on the stability of S-nitrosothiols. Arch Biochem Biophys 361:323–330 ArticlePubMed Google Scholar
Hou Y, Guo Z, Li J, Wang PG (1996) Seleno compounds and glutathione peroxidase catalyzed decomposition of S-nitrosothiols. Biochem Biophys Res Commun 228:88–93 ArticlePubMedCAS Google Scholar
Trujillo M, Alvarez MN, Peluffo G, Freeman BA, Radi R (1998) Xanthine oxidase-mediated decomposition of S-nitrosothiols. J Biol Chem 273:7828–7834 ArticlePubMedCAS Google Scholar
Sliskovic I, Raturi A, Mutus B (2005) Characterization of the S-denitrosation activity of protein disulfide isomerase. J Biol Chem 280:8733–8741 ArticlePubMedCAS Google Scholar
Uehara T, Nakamura T, Yao D, Shi ZQ, Gu Z, Ma Y, Masliah E, Nomura Y, Lipton SA (2006) S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature 441:513–517 ArticlePubMedCAS Google Scholar
Abrams AJ, Farooq A, Wang G (2011) S-nitrosylation of ApoE in Alzheimer’s disease. Biochemistry 50:3405–3407 ArticlePubMedCAS Google Scholar
Yao D, Gu Z, Nakamura T, Shi ZQ, Ma Y, Gaston B, Palmer LA, Rockenstein EM, Zhang Z, Masliah E et al (2004) Nitrosative stress linked to sporadic Parkinson’s disease: S-nitrosylation of parkin regulates its E3 ubiquitin ligase activity. Proc Natl Acad Sci USA 101:10810–10814 ArticlePubMedCAS Google Scholar
Chung KK, Thomas B, Li X, Pletnikova O, Troncoso JC, Marsh L, Dawson VL, Dawson TM (2004) S-nitrosylation of parkin regulates ubiquitination and compromises parkin’s protective function. Science 304:1328–1331 ArticlePubMedCAS Google Scholar
Fang J, Nakamura T, Cho DH, Gu Z, Lipton SA (2007) S-nitrosylation of peroxiredoxin 2 promotes oxidative stress-induced neuronal cell death in Parkinson’s disease. Proc Natl Acad Sci USA 104:18742–18747 ArticlePubMedCAS Google Scholar
Tsang AH, Lee YI, Ko HS, Savitt JM, Pletnikova O, Troncoso JC, Dawson V, Dawson TM, Chung KK (2009) S-nitrosylation of XIAP compromises neuronal survival in Parkinson Disease. Proc Natl Acad Sci USA 106:4900–4905 ArticlePubMedCAS Google Scholar
Gu Z, Kaul M, Yan B, Kridel SJ, Cui J, Strongin A, Smith JW, Liddington RC, Lipton SA (2002) S-nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science 297:1186–1190 ArticlePubMedCAS Google Scholar
Gonzalez DR, Beigi F, Treuer AV, Hare JM (2007) Deficient ryanodine receptor S-nitrosylation increases sarcoplasmic reticulum calcium leak and arrhythmogenesis in cardiomyocytes. Proc Natl Acad Sci USA 104:20612–20617 ArticlePubMedCAS Google Scholar
Ueda K, Valdivia C, Medeiros-Domingo A, Tester DJ, Vatta M, Farrugia G, Ackerman MJ, Makielski JC (2008) Syntrophin mutation associated with long QT syndrome through activation of the nNOS-SCN5A macromolecular complex. Proc Natl Acad Sci USA 105:9355–9360 ArticlePubMedCAS Google Scholar
Gandley RE, Tyurin VA, Huang W, Arroyo A, Daftary A, Harger G, Jiang J, Pitt B, Taylor RN, Hubel CA et al (2005) S-nitrosoalbumin-mediated relaxation is enhanced by ascorbate and copper: effects in pregnancy and preeclampsia plasma. Hypertension 45:21–27 PubMedCAS Google Scholar
Tyurin VA, Liu SX, Tyurina YY, Sussman NB, Hubel CA, Roberts JM, Taylor RN, Kagan VE (2001) Elevated levels of S-nitrosoalbumin in preeclampsia plasma. Circ Res 88:1210–1215 ArticlePubMedCAS Google Scholar
Zhang HH, Wang YP, Chen DB (2011) Analysis of nitroso-proteomes in normotensive and severe preeclamptic human placentas. Biol Reprod 84:966–975 ArticlePubMedCAS Google Scholar
Palmer LA, Doctor A, Chhabra P, Sheram ML, Laubach VE, Karlinsey MZ, Forbes MS, Macdonald T, Gaston B (2007) S-nitrosothiols signal hypoxia-mimetic vascular pathology. J Clin Invest 117:2592–2601 ArticlePubMedCAS Google Scholar
Mukhopadhyay S, Lee J, Sehgal PB (2008) Depletion of the ATPase NSF from Golgi membranes with hypo-S-nitrosylation of vasorelevant proteins in endothelial cells exposed to monocrotaline pyrrole. Am J Physiol Heart Circ Physiol 295:H1943–H1955 ArticlePubMedCAS Google Scholar
Godoy LC, Moretti AI, Jurado MC, Oxer D, Janiszewski M, Ckless K, Velasco IT, Laurindo FR, Souza HP (2010) Loss of CD40 endogenous S-nitrosylation during inflammatory response in endotoxemic mice and patients with sepsis. Shock 33:626–633 PubMedCAS Google Scholar
Sun J, Picht E, Ginsburg KS, Bers DM, Steenbergen C, Murphy E (2006) Hypercontractile female hearts exhibit increased S-nitrosylation of the L-type Ca2+ channel alpha1 subunit and reduced ischemia/reperfusion injury. Circ Res 98:403–411 ArticlePubMedCAS Google Scholar
Burger DE, Lu X, Lei M, Xiang FL, Hammoud L, Jiang M, Wang H, Jones DL, Sims SM, Feng Q (2009) Neuronal nitric oxide synthase protects against myocardial infarction-induced ventricular arrhythmia and mortality in mice. Circulation 120:1345–1354 ArticlePubMedCAS Google Scholar
Carnes CA, Janssen PM, Ruehr ML, Nakayama H, Nakayama T, Haase H, Bauer JA, Chung MK, Fearon IM, Gillinov AM et al (2007) Atrial glutathione content, calcium current, and contractility. J Biol Chem 282:28063–28073 ArticlePubMedCAS Google Scholar
Asada K, Kurokawa J, Furukawa T (2009) Redox- and calmodulin-dependent S-nitrosylation of the KCNQ1 channel. J Biol Chem 284:6014–6020 ArticlePubMedCAS Google Scholar
Bai CX, Namekata I, Kurokawa J, Tanaka H, Shigenobu K, Furukawa T (2005) Role of nitric oxide in Ca2+ sensitivity of the slowly activating delayed rectifier K+ current in cardiac myocytes. Circ Res 96:64–72 ArticlePubMedCAS Google Scholar
Milsom AB, Jones CJ, Goodfellow J, Frenneaux MP, Peters JR, James PE (2002) Abnormal metabolic fate of nitric oxide in type I diabetes mellitus. Diabetologia 45:1515–1522 ArticlePubMedCAS Google Scholar
Padron J, Peiro C, Cercas E, Llergo JL, Sanchez-Ferrer CF (2000) Enhancement of S-nitrosylation in glycosylated hemoglobin. Biochem Biophys Res Commun 271:217–221 ArticlePubMedCAS Google Scholar
Ding SY, Tribble ND, Kraft CA, Markwardt M, Gloyn AL, Rizzo MA (2010) Naturally occurring glucokinase mutations are associated with defects in posttranslational S-nitrosylation. Mol Endocrinol 24:171–177 ArticlePubMedCAS Google Scholar
Carvalho-Filho MA, Ueno M, Hirabara SM, Seabra AB, Carvalheira JB, de Oliveira MG, Velloso LA, Curi R, Saad MJ (2005) S-nitrosation of the insulin receptor, insulin receptor substrate 1, and protein kinase B/Akt: a novel mechanism of insulin resistance. Diabetes 54:959–967 ArticlePubMedCAS Google Scholar
Pauli JR, Ropelle ER, Cintra DE, Carvalho-Filho MA, Moraes JC, De Souza CT, Velloso LA, Carvalheira JB, Saad MJ (2008) Acute physical exercise reverses S-nitrosation of the insulin receptor, insulin receptor substrate 1 and protein kinase B/Akt in diet-induced obese Wistar rats. J Physiol 586:659–671 ArticlePubMedCAS Google Scholar
Massy ZA, Fumeron C, Borderie D, Tuppin P, Nguyen-Khoa T, Benoit MO, Jacquot C, Buisson C, Drueke TB, Ekindjian OG et al (2004) Increased pasma S-nitrosothiol concentrations predict cardiovascular outcomes among patients with end-stage renal disease: a prospective study. J Am Soc Nephrol 15:470–476 ArticlePubMedCAS Google Scholar
Marozkina NV, Yemen S, Borowitz M, Liu L, Plapp M, Sun F, Islam R, Erdmann-Gilmore P, Townsend RR, Lichti CF et al (2010) Hsp 70/Hsp 90 organizing protein as a nitrosylation target in cystic fibrosis therapy. Proc Natl Acad Sci USA 107:11393–11398 ArticlePubMedCAS Google Scholar
Guo CJ, Atochina-Vasserman EN, Abramova E, Foley JP, Zaman A, Crouch E, Beers MF, Savani RC, Gow AJ (2008) S-nitrosylation of surfactant protein-D controls inflammatory function. PLoS Biol 6:e266 ArticlePubMedCAS Google Scholar
Lim KH, Ancrile BB, Kashatus DF, Counter CM (2008) Tumour maintenance is mediated by eNOS. Nature 452:646–649 ArticlePubMedCAS Google Scholar
Li F, Sonveaux P, Rabbani ZN, Liu S, Yan B, Huang Q, Vujaskovic Z, Dewhirst MW, Li CY (2007) Regulation of HIF-1alpha stability through S-nitrosylation. Mol Cell 26:63–74 ArticlePubMedCAS Google Scholar
Bellinger AM, Reiken S, Carlson C, Mongillo M, Liu X, Rothman L, Matecki S, Lacampagne A, Marks AR (2009) Hypernitrosylated ryanodine receptor calcium release channels are leaky in dystrophic muscle. Nat Med 15:325–330 ArticlePubMedCAS Google Scholar
Durham WJ, Aracena-Parks P, Long C, Rossi AE, Goonasekera SA, Boncompagni S, Galvan DL, Gilman CP, Baker MR, Shirokova N et al (2008) RyR1 S-nitrosylation underlies environmental heat stroke and sudden death in Y522S RyR1 knockin mice. Cell 133:53–65 ArticlePubMedCAS Google Scholar
Marozkina NV, Yemen S, Wei C, Wallrabe H, Nagji AS, Liu L, Morozkina T, Jones DR, Gaston B (2011) S-nitrosoglutathione reductase in human lung cancer. Am J Respir Cell Mol Biol 46:63–70 ArticleCAS Google Scholar
Straub AC, Billaud M, Johnstone SR, Best AK, Yemen S, Dwyer ST, Looft-Wilson R, Lysiak JJ, Gaston B, Palmer L et al (2011) Compartmentalized connexin 43 s-nitrosylation/denitrosylation regulates heterocellular communication in the vessel wall. Arterioscler Thromb Vasc Biol 31:399–407 ArticlePubMedCAS Google Scholar
Malhotra D, Thimmulappa RK, Mercado N, Ito K, Kombairaju P, Kumar S, Ma J, Feller-Kopman D, Wise R, Barnes P et al (2011) Denitrosylation of HDAC2 by targeting Nrf2 restores glucocorticosteroid sensitivity in macrophages from COPD patients. J Clin Invest 121:4289–4302 ArticlePubMedCAS Google Scholar