Signaling by S-nitrosylation in the heart

Journal of Molecular and Cellular Cardiology

Volumn 73, Issue , 2014, Pages 18-25

  Murphy, Elizabeth ^a   Kohr, Mark ^a,b   Menazza, Sara ^a   Nguyen, Tiffany ^a   Evangelista, Alicia ^a   Sun, Junhui ^a   Steenbergen, Charles ^b  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b DEPARTMENT OF PATHOLOGY   (United States)

Author keywords

Cardioportection; Nitric oxide; Oxidation

Indexed keywords

CYSTEINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GELATINASE A; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INDUCIBLE NITRIC OXIDE SYNTHASE; MEMBRANE PROTEIN; MYOSIN LIGHT CHAIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN BCL 2; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; TRIM72 PROTEIN; UNCLASSIFIED DRUG; S NITROSOTHIOL;

ACYLATION; BINDING KINETICS; CARDIAC RESYNCHRONIZATION THERAPY; CARDIOVASCULAR DISEASE; CELL FUNCTION; DISULFIDE BOND; ENZYME ACTIVITY; HEART FUNCTION; HEART MUSCLE CELL; HEART PROTECTION; ISCHEMIC PRECONDITIONING; NITROSYLATION; OXIDATION; OXIDATION REDUCTION STATE; PRENYLATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN SUBUNIT; PROTEIN SYNTHESIS; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; HEART; HUMAN; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY;

ANIMALS; HEART; HUMANS; NITRIC OXIDE; OXIDATION-REDUCTION; PROTEIN PROCESSING, POST-TRANSLATIONAL; S-NITROSOTHIOLS; SIGNAL TRANSDUCTION;

EID: 84901823953     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.01.003     Document Type: Review

References (71)

1. Kohr M.J., Aponte A.M., Sun J., Wang G., Murphy E., Gucek M., et al. Characterization of potential S-nitrosylation sites in the myocardium. Am J Physiol Heart Circ Physiol 2011, 300(4):H1327-H1335.
2. Doulias P.T., Greene J.L., Greco T.M., Tenopoulou M., Seeholzer S.H., Dunbrack R.L., et al. Structural profiling of endogenous S-nitrosocysteine residues reveals unique features that accommodate diverse mechanisms for protein S-nitrosylation. Proc Natl Acad Sci U S A Sep 28 2010, 107(39):16958-16963.
3. Murray C.I., Kane L.A., Uhrigshardt H., Wang S.B., Van Eyk J.E. Site-mapping of in vitro S-nitrosation in cardiac mitochondria: implications for cardioprotection. Mol Cell Proteomics Mar 2011, 10(3). [M110 004721].
4. Sun J., Morgan M., Shen R.F., Steenbergen C., Murphy E. Preconditioning results in S-nitrosylation of proteins involved in regulation of mitochondrial energetics and calcium transport. Circ Res Nov 26 2007, 101(11):1155-1163.
5. Chen C.A., Druhan L.J., Varadharaj S., Chen Y.R., Zweier J.L. Phosphorylation of endothelial nitric-oxide synthase regulates superoxide generation from the enzyme. J Biol Chem Oct 3 2008, 283(40):27038-27047.
6. Ravi K., Brennan L.A., Levic S., Ross P.A., Black S.M. S-nitrosylation of endothelial nitric oxide synthase is associated with monomerization and decreased enzyme activity. Proc Natl Acad Sci U S A Feb 24 2004, 101(8):2619-2624.
7. Zweier J.L., Wang P., Samouilov A., Kuppusamy P. Enzyme-independent formation of nitric oxide in biological tissues. Nat Med Aug 1995, 1(8):804-809.
8. Anand P., Stamler J.S. Enzymatic mechanisms regulating protein S-nitrosylation: implications in health and disease. J Mol Med (Berl) Mar 2012, 90(3):233-244.
9. Wu C., Parrott A.M., Fu C., Liu T., Marino S.M., Gladyshev V.N., et al. Thioredoxin 1-mediated post-translational modifications: reduction, transnitrosylation, denitrosylation, and related proteomics methodologies. Antioxid Redox Signal Nov 1 2012, 15(9):2565-2604.
10. Benhar M., Forrester M.T., Stamler J.S. Protein denitrosylation: enzymatic mechanisms and cellular functions. Nat Rev Mol Cell Biol Oct 2009, 10(10):721-732.
11. Barouch L.A., Harrison R.W., Skaf M.W., Rosas G.O., Cappola T.P., Kobeissi Z.A., et al. Nitric oxide regulates the heart by spatial confinement of nitric oxide synthase isoforms. Nature Mar 21 2002, 416(6878):337-339.
12. Iwakiri Y., Satoh A., Chatterjee S., Toomre D.K., Chalouni C.M., Fulton D., et al. Nitric oxide synthase generates nitric oxide locally to regulate compartmentalized protein S-nitrosylation and protein trafficking. Proc Natl Acad Sci U S A Dec 26 2006, 103(52):19777-19782.
13. Zhang Y.H., Casadei B. Sub-cellular targeting of constitutive NOS in health and disease. J Mol Cell Cardiol Feb 2012, 52(2):341-350.
14. Damy T., Ratajczak P., Robidel E., Bendall J.K., Oliviero P., Boczkowski J., et al. Up-regulation of cardiac nitric oxide synthase 1-derived nitric oxide after myocardial infarction in senescent rats. FASEB J Oct 2003, 17(13):1934-1936.
15. Damy T., Ratajczak P., Shah A.M., Camors E., Marty I., Hasenfuss G., et al. Increased neuronal nitric oxide synthase-derived NO production in the failing human heart. Lancet Apr 24 2004, 363(9418):1365-1367.
16. Kornberg M.D., Sen N., Hara M.R., Juluri K.R., Nguyen J.V., Snowman A.M., et al. GAPDH mediates nitrosylation of nuclear proteins. Nat Cell Biol Nov 2010, 12(11):1094-1100.
17. Pawloski J.R., Hess D.T., Stamler J.S. Export by red blood cells of nitric oxide bioactivity. Nature 2001, 409(6820):622-626.
18. Nakamura T., Wang L., Wong C.C., Scott F.L., Eckelman B.P., Han X., et al. Transnitrosylation of XIAP regulates caspase-dependent neuronal cell death. Mol Cell 2010, 39(2):184-195.
19. Mitchell D.A., Marletta M.A. Thioredoxin catalyzes the S-nitrosation of the caspase-3 active site cysteine. Nat Chem Biol 2005, 1(3):154-158.
20. Wu C., Liu T., Chen W., Oka S., Fu C., Jain M.R., et al. Redox regulatory mechanism of transnitrosylation by thioredoxin. Molecular 2010, 9(10):2262-2275.
21. Bauer P.M., Buga G.M., Fukuto J.M., Pegg A.E., Ignarro L.J. Nitric oxide inhibits ornithine decarboxylase via S-nitrosylation of cysteine 360 in the active site of the enzyme. J Biol Chem Sep 14 2001, 276(37):34458-34464.
22. Whalen E.J., Foster M.W., Matsumoto A., Ozawa K., Violin J.D., Que L.G., et al. Regulation of beta-adrenergic receptor signaling by S-nitrosylation of G-protein-coupled receptor kinase 2. Cell May 4 2007, 129(3):511-522.
23. Nguyen T.T., Stevens M.V., Kohr M., Steenbergen C., Sack M.N., Murphy E. Cysteine 203 of cyclophilin D is critical for cyclophilin D activation of the mitochondrial permeability transition pore. J Biol Chem Nov 18 2011, 286(46):40184-40192.
24. Murphy E., Kohr M., Sun J., Nguyen T., Steenbergen C. S-nitrosylation: a radical way to protect the heart. J Mol Cell Cardiol Mar 2011, 52(3):568-577.
25. Doulias P.T., Tenopoulou M., Greene J.L., Raju K., Ischiropoulos H. Nitric oxide regulates mitochondrial fatty acid metabolism through reversible protein S-nitrosylation. Sci Signal Jan 1 2013, 6(256):rs1.
26. Sips P.Y., Irie T., Zou L., Shinozaki S., Sakai M., Shimizu N., et al. Reduction of cardiomyocyte S-nitrosylation by S-nitrosoglutathione reductase protects against sepsis-induced myocardial depression. Am J Physiol Heart Circ Physiol Apr 15 2013, 304(8):H1134-H1146.
27. Hara M.R., Agrawal N., Kim S.F., Cascio M.B., Fujimuro M., Ozeki Y., et al. S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat Cell Biol Jul 2005, 7(7):665-674.
28. Ozawa K., Whalen E.J., Nelson C.D., Mu Y., Hess D.T., Lefkowitz R.J., et al. S-nitrosylation of beta-arrestin regulates beta-adrenergic receptor trafficking. Mol Cell Aug 8 2008, 31(3):395-405.
29. Jung S.M., Jandu S., Steppan J., Belkin A., An S.S., Pak A., et al. Increased tissue transglutaminase activity contributes to central vascular stiffness in eNOS knockout mice. Am J Physiol Heart Circ Physiol Sep 2013, 305(6):H803-H810.
30. Qu J., Liu G.H., Huang B., Chen C. Nitric oxide controls nuclear export of APE1/Ref-1 through S-nitrosation of cysteines 93 and 310. Nucleic Acids Res 2007, 35(8):2522-2532.
31. Um H.C., Jang J.H., Kim D.H., Lee C., Surh Y.J. Nitric oxide activates Nrf2 through S-nitrosylation of Keap1 in PC12 cells. Nitric 2011, 25(2):161-168.
32. Clements C.M., McNally R.S., Conti B.J., Mak T.W., Ting J.P. DJ-1, a cancer- and Parkinson's disease-associated protein, stabilizes the antioxidant transcriptional master regulator Nrf2. Proc Natl Acad Sci U S A 2006, 103(41):15091-15096.
33. Sen N., Hara M.R., Ahmad A.S., Cascio M.B., Kamiya A., Ehmsen J.T., et al. GOSPEL: a neuroprotective protein that binds to GAPDH upon S-nitrosylation. Neuron 2009, 63(1):81-91.
34. Polewicz D., Cadete V.J., Doroszko A., Hunter B.E., Sawicka J., Szczesna-Cordary D., et al. Ischemia induced peroxynitrite dependent modifications of cardiomyocyte MLC1 increases its degradation by MMP-2 leading to contractile dysfunction. J Cell Mol Med May 2010, 15(5):1136-1147.
35. Ho G.P., Selvakumar B., Mukai J., Hester L.D., Wang Y., Gogos J.A., et al. S-nitrosylation and S-palmitoylation reciprocally regulate synaptic targeting of PSD-95. Neuron Jul 14 2011, 71(1):131-141.
36. Evangelista A.M., Kohr M.J., Murphy E. S-nitrosylation: specificity, occupancy, and interaction with other post-translational modifications. Antioxid Redox Signal Oct 10 2012, 19(11):1209-1219.
37. Wang S.B., Foster D.B., Rucker J., O'Rourke B., Kass D.A., Van Eyk J.E. Redox regulation of mitochondrial ATP synthase: implications for cardiac resynchronization therapy. Circ Res Sep 16 2011, 109(7):750-757.
38. Kohr M.J., Sun J., Aponte A., Wang G., Gucek M., Murphy E., et al. Simultaneous measurement of protein oxidation and S-nitrosylation during preconditioning and ischemia/reperfusion injury with resin-assisted capture. Circ Res Feb 18 2011, 108(4):418-426.
39. Yakushev S., Band M., van Patot MC Tissot, Gassmann M., Avivi A., Bogdanova A. Cross talk between S-nitrosylation and S-glutathionylation in control of the Na,K-ATPase regulation in hypoxic heart. Am J Physiol Heart Circ Physiol Dec 1 2012, 303(11):H1332-H1343.
40. Dumitrescu C., Biondi R., Xia Y., Cardounel A.J., Druhan L.J., Ambrosio G., et al. Myocardial ischemia results in tetrahydrobiopterin (BH4) oxidation with impaired endothelial function ameliorated by BH4. Proc Natl Acad Sci U S A Sep 18 2007, 104(38):15081-15086.
41. Chen C.A., Wang T.Y., Varadharaj S., Reyes L.A., Hemann C., Talukder M.A., et al. S-glutathionylation uncouples eNOS and regulates its cellular and vascular function. Nature Dec 23 2010, 468(7327):1115-1118.
42. Crabtree M.J., Brixey R., Batchelor H., Hale A.B., Channon K.M. Integrated redox sensor and effector functions for tetrahydrobiopterin- and glutathionylation-dependent endothelial nitric-oxide synthase uncoupling. J Biol Chem Jan 4 2013, 288(1):561-569.
43. Zweier J.L., Wang P., Kuppusamy P. Direct measurement of nitric oxide generation in the ischemic heart using electron paramagnetic resonance spectroscopy. J Biol Chem Jan 6 1995, 270(1):304-307.
44. Kwak Y.D., Ma T., Diao S., Zhang X., Chen Y., Hsu J., et al. NO signaling and S-nitrosylation regulate PTEN inhibition in neurodegeneration. Mol Neurodegener 2010, 5:49.
45. Azad N., Vallyathan V., Wang L., Tantishaiyakul V., Stehlik C., Leonard S.S., et al. S-nitrosylation of Bcl-2 inhibits its ubiquitin-proteasomal degradation. A novel antiapoptotic mechanism that suppresses apoptosis. J Biol Chem Nov 10 2006, 281(45):34124-34134.
46. Li F., Sonveaux P., Rabbani Z.N., Liu S., Yan B., Huang Q., et al. Regulation of HIF-1alpha stability through S-nitrosylation. Mol Cell Apr 13 2007, 26(1):63-74.
47. Lima B., Lam G.K., Xie L., Diesen D.L., Villamizar N., Nienaber J., et al. Endogenous S-nitrosothiols protect against myocardial injury. Proc Natl Acad Sci U S A Apr 14 2009, 106(15):6297-6302.
48. Chung K.K., Thomas B., Li X., Pletnikova O., Troncoso J.C., Marsh L., et al. S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function. Science May 28 2004, 304(5675):1328-1331.
49. Yao D., Gu Z., Nakamura T., Shi Z.Q., Ma Y., Gaston B., et al. Nitrosative stress linked to sporadic Parkinson's disease: S-nitrosylation of parkin regulates its E3 ubiquitin ligase activity. Proc Natl Acad Sci U S A Jul 20 2004, 101(29):10810-10814.
50. Ozawa K., Komatsubara A.T., Nishimura Y., Sawada T., Kawafune H., Tsumoto H., et al. S-nitrosylation regulates mitochondrial quality control via activation of parkin. Sci Rep 2013, 3:2202.
51. Trempe J.F., Sauve V., Grenier K., Seirafi M., Tang M.Y., Menade M., et al. Structure of parkin reveals mechanisms for ubiquitin ligase activation. Science Jun 21 2013, 340(6139):1451-1455.
52. Cao C.M., Zhang Y., Weisleder N., Ferrante C., Wang X., Lv F., et al. MG53 constitutes a primary determinant of cardiac ischemic preconditioning. Circulation 2010, 121(23):2565-2574.
53. Cai C., Masumiya H., Weisleder N., Matsuda N., Nishi M., Hwang M., et al. MG53 nucleates assembly of cell membrane repair machinery. Nat Cell Biol 2009, 11(1):56-64.
54. Covian R., Balaban R.S. Cardiac mitochondrial matrix and respiratory complex protein phosphorylation. Am J Physiol Heart Circ Physiol Oct 15 2012, 303(8):H940-H966.
55. Solaro R.J., van der Velden J. Why does troponin I have so many phosphorylation sites? Fact and fancy. J Mol Cell Cardiol May 2010, 48(5):810-816.
56. Chakravarti R., Aulak K.S., Fox P.L., Stuehr D.J. GAPDH regulates cellular heme insertion into inducible nitric oxide synthase. Proc Natl Acad Sci U S A Oct 19 2010, 107(42):18004-18009.
57. Kohr M.J., Aponte A., Sun J., Gucek M., Steenbergen C., Murphy E. Measurement of S-nitrosylation occupancy in the myocardium with cysteine-reactive tandem mass tags: short communication. Circ Res 2012, 111(10):1308-1312.
58. Chouchani E.T., Methner C., Nadtochiy S.M., Logan A., Pell V.R., Ding S., et al. Cardioprotection by S-nitrosation of a cysteine switch on mitochondrial complex I. Nat Med Jun 2013, 19(6):753-759.
59. Doulias P.T., Tenopoulou M., Raju K., Spruce L.A., Seeholzer S.H., Ischiropoulos H. Site specific identification of endogenous S-nitrosocysteine proteomes. J Proteomics Jun 5 2013, 92:195-203.
60. Obal D., Dai S., Keith R., Dimova N., Kingery J., Zheng Y.T., et al. Cardiomyocyte-restricted overexpression of extracellular superoxide dismutase increases nitric oxide bioavailability and reduces infarct size after ischemia/reperfusion. Basic Res Cardiol 2012, 107(6):305.
61. Hare J.M., Stamler J.S. NO/redox disequilibrium in the failing heart and cardiovascular system. J Clin Invest Mar 2005, 115(3):509-517.
62. Moens A.L., Takimoto E., Tocchetti C.G., Chakir K., Bedja D., Cormaci G., et al. Reversal of cardiac hypertrophy and fibrosis from pressure overload by tetrahydrobiopterin: efficacy of recoupling nitric oxide synthase as a therapeutic strategy. Circulation May 20 2008, 117(20):2626-2636.
63. Silberman G.A., Fan T.H., Liu H., Jiao Z., Xiao H.D., Lovelock J.D., et al. Uncoupled cardiac nitric oxide synthase mediates diastolic dysfunction. Circulation Feb 2 2010, 121(4):519-528.
64. Jeong E.M., Monasky M.M., Gu L., Taglieri D.M., Patel B.G., Liu H., et al. Tetrahydrobiopterin improves diastolic dysfunction by reversing changes in myofilament properties. J Mol Cell Cardiol Mar 2012, 56:44-54.
65. Moens A.L., Kietadisorn R., Lin J.Y., Kass D. Targeting endothelial and myocardial dysfunction with tetrahydrobiopterin. J Mol Cell Cardiol Oct 2011, 51(4):559-563.
66. Moens A.L., Ketner E.A., Takimoto E., Schmidt T.S., O'Neill C.A., Wolin M.S., et al. Bi-modal dose-dependent cardiac response to tetrahydrobiopterin in pressure-overload induced hypertrophy and heart failure. J Mol Cell Cardiol Oct 2011, 51(4):564-569.
67. Cunnington C., Van Assche T., Shirodaria C., Kylintireas I., Lindsay A.C., Lee J.M., et al. Systemic and vascular oxidation limits the efficacy of oral tetrahydrobiopterin treatment in patients with coronary artery disease. Circulation Mar 20 2012, 125(11):1356-1366.
68. Idigo W.O., Reilly S., Zhang M.H., Zhang Y.H., Jayaram R., Carnicer R., et al. Regulation of endothelial nitric-oxide synthase (NOS) S-glutathionylation by neuronal NOS: evidence of a functional interaction between myocardial constitutive NOS isoforms. J Biol Chem Dec 21 2012, 287(52):43665-43673.
69. Doshi A.A., Ziolo M.T., Wang H., Burke E., Lesinski A., Binkley P. A promoter polymorphism of the endothelial nitric oxide synthase gene is associated with reduced mRNA and protein expression in failing human myocardium. J Card Fail Apr 2010, 16(4):314-319.
70. Cattaruzza M., Guzik T.J., Slodowski W., Pelvan A., Becker J., Halle M., et al. Shear stress insensitivity of endothelial nitric oxide synthase expression as a genetic risk factor for coronary heart disease. Circ Res Oct 15 2004, 95(8):841-847.
71. Matsa L.S., Rangaraju A., Vengaldas V., Latifi M., Jahromi H.M., Ananthapur V., et al. Haplotypes of NOS3 gene polymorphisms in dilated cardiomyopathy. PLoS One 2013, 8(7):e70523.