Protein S-Nitrosylation: Determinants of Specificity and Enzymatic Regulation of S-Nitrosothiol-Based Signaling

Antioxidants and Redox Signaling

Volumn 30, Issue 10, 2019, Pages 1331-1351

  Stomberski, Colin T ^a   Hess, Douglas T ^a   Stamler, Jonathan S ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

Author keywords

denitrosylation; nitric oxide; redox signaling; S nitrosylase; S nitrosylation

Indexed keywords

COENZYME A; CYSTEINE; DENITROSYLASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITROSOGLUTATHIONE REDUCTASE; OXIDOREDUCTASE; S NITROSOTHIOL; THIOL; THIOREDOXIN REDUCTASE; UNCLASSIFIED DRUG; PROTEIN;

CELLULAR DISTRIBUTION; CHEMICAL BOND; ENZYME ACTIVITY; HUMAN; HYDROPHOBICITY; MOLECULAR INTERACTION; MOLECULAR WEIGHT; NITROSYLATION; NONHUMAN; OXIDATION; OXIDATION REDUCTION REACTION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; METABOLISM;

ANIMALS; CYSTEINE; HUMANS; NITRIC OXIDE; OXIDATION-REDUCTION; PROTEINS; S-NITROSOTHIOLS; SIGNAL TRANSDUCTION;

EID: 85058355861     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2017.7403     Document Type: Review

References (209)

1. Abunimer A, Smith K, Wu TJ, Lam P, Simonyan V, and Mazumder R. Single-nucleotide variations in cardiac arrhythmias: prospects for genomics and proteomics based biomarker discovery and diagnostics. Genes (Basel) 5: 254-269, 2014.
2. Anand P, Hausladen A, Wang Y, Zhang G, Stomberski C, BrunengraberH,HessDT, and Stamler JS. Identification of Snitroso-CoA reductases that regulate protein S-nitrosylation. Proc Natl Acad Sci U S A 111: 18572-18577, 2014.
3. Anand P and Stamler JS. Enzymatic mechanisms regulating protein S-nitrosylation: implications in health and disease. J Mol Med 90: 233-244, 2012.
4. Andre FR, dos Santos PF, and Rando DG. Theoretical studies of the role of C-terminal cysteines in the process of S-nitrosylation of human Src kinases. J Mol Model 22: 23, 2016.
5. Angelo M, Singel DJ, and Stamler JS. An S-nitrosothiol (SNO) synthase function of hemoglobin that utilizes nitrite as a substrate. Proc Natl Acad Sci U S A 103: 8366-8371, 2006.
6. Arnelle DR and Stamler JS. NO+, NO, and NO-donation by S-nitrosothiols: implications for regulation of physiological functions by S-nitrosylation and acceleration of disulfide formation. Arch Biochem Biophys 318: 279-285, 1995.
7. Arulsamy N, Bohle DS, Butt JA, Irvine GJ, Jordan PA, and Sagan E. Interrelationships between conformational dynamics and the redox chemistry of S-nitroso thiols. J Am Chem Soc 121: 7115-7123, 1999.
8. Baciu C, Cho KB, and Gauld JW. Influence of Cu+ on the RS-NO bond dissociation energy of S-nitrosothiols. J Phys Chem B 109: 1334-1336, 2005.
9. Barouch LA, Harrison RW, Skaf MW, Rosas GO, Cappola TP, Kobeissi ZA, Hobai IA, Lemmon CA, Burnett AL, O'Rourke B, Rodriguez ER, Huang PL, Lima JAC, Berkowitz DE, and Hare JM. Nitric oxide regulates the heart by spatial confinement of nitric oxide synthase isoforms. Nature 416: 337-339, 2002.
10. Barski OA, Gabbay KH, Grimshaw CE, and Bohren KM. Mechanism of human aldehyde reductase: characterization of the active site pocket. Biochemistry 34: 11264-11275, 1995.
11. Barski OA, Tipparaju SM, and Bhatnagar A. The aldoketo reductase superfamily and its role in drug metabolism and detoxification. Drug Metab Rev 40: 553-624, 2008.
12. Bartberger MD, Fukuto JM, and Houk KN. On the acidity and reactivity of HNO in aqueous solution and biological systems. Proc Natl Acad Sci U S A 98: 2194-2198, 2001.
13. Bartberger MD, Houk KN, Powell SC, Mannion JD, Lo KY, Stamler JS, and Toone EJ. Theory, spectroscopy, and crystallographic analysis of S-nitrosothiols: conformational distribution dictates spectroscopic behavior. J Am Chem Soc 122: 5889-5890, 2000.
14. Bartberger MD, Mannion JD, Powell SC, Stamler JS, Houk KN, and Toone EJ. S-N dissociation energies of Snitrosothiols: on the origins of nitrosothiol decomposition rates. J Am Chem Soc 123: 8868-8869, 2001.
15. Bateman RL, Rauh D, Tavshanjian B, and Shokat KM. Human carbonyl reductase 1 is an S-nitrosoglutathione reductase. J Biol Chem 283: 35756-35762, 2008.
16. Beigi F, Gonzalez DR, Minhas KM, Sun QA, Foster MW, Khan SA, Treuer A V, Dulce RA, Harrison RW, Saraiva RM, Premer C, Schulman IH, Stamler JS, and Hare JM. Dynamic denitrosylation via S-nitrosoglutathione reductase regulates cardiovascular function. Proc Natl Acad Sci U S A 109: 4314-4319, 2012.
17. Ben-Lulu S, Ziv T, Admon A, Weisman-Shomer P, and Benhar M. A substrate trapping approach identifies proteins regulated by reversible S-nitrosylation. Mol Cell Proteomics 13: 2573-2583, 2014.
18. Ben-Lulu S, Ziv T, Weisman-Shomer P, and Benhar M. Nitrosothiol-trapping-based proteomic analysis of Snitrosylation in human lung carcinoma cells. PLoS One 12: e0169862, 2017.
19. Benhar M. Nitric oxide and the thioredoxin system: a complex interplay in redox regulation. Biochim Biophys Acta 1850: 2476-2484, 2015.
20. Benhar M, Forrester MT, Hess DT, and Stamler JS. Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins. Science 320: 1050-1054, 2008.
21. Benhar M, Forrester MT, and Stamler JS. Protein denitrosylation: enzymatic mechanisms and cellular functions. Nat Rev Mol Cell Biol 10: 721-732, 2009.
22. Benhar M, Thompson JW, Moseley MA, and Stamler JS. Identification of S-nitrosylated targets of thioredoxin using a quantitative proteomic approach. Biochemistry 49: 6963-6969, 2010.
23. Bhandari V, Choo-Wing R, Chapoval SP, Lee CG, Tang C, Kim YK, Ma B, Baluk P, Lin MI, McDonald DM, Homer RJ, Sessa WC, and Elias JA. Essential role of nitric oxide in VEGF-induced, asthma-like angiogenic, inflammatory, mucus, and physiologic responses in the lung. Proc Natl Acad Sci U S A 103: 11021-11026, 2006.
24. Blonder JP, Mutka SC, Sun X, Qiu J, Green LH, Mehra NK, Boyanapalli R, Suniga M, Look K, Delany C, Richards JP, Looker D, Scoggin C, and Rosenthal GJ. Pharmacologic inhibition of S-nitrosoglutathione reductase protects against experimental asthma in BALB/c mice through attenuation of both bronchoconstriction and inflammation. BMC Pulm Med 14: 3, 2014.
25. Bodas M, Silverberg D, Walworth K, Brucia K, and Vij N. Augmentation of S-nitrosoglutathione controls cigarette smoke-induced inflammatory-oxidative stress and chronic obstructive pulmonary disease-emphysema pathogenesis by restoring cystic fibrosis transmembrane conductance regulator function. Antioxid Redox Signal 27: 433-451, 2017.
26. Bosworth CA, Toledo JC, Zmijewski JW, Li Q, and Lancaster JR. Dinitrosyliron complexes and the mechanism( s) of cellular protein nitrosothiol formation from nitric oxide. Proc Natl Acad Sci U S A 106: 4671-4676, 2009.
27. Brenman JE, Chao DS, Gee SH, McGee AW, Craven SE, Santillano DR, Wu Z, Huang F, Xia H, Peters MF, Froehner SC, and Bredt DS. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha1-syntrophin mediated by PDZ domains. Cell 84: 757-767, 1996.
28. Brown-Steinke K, DeRonde K, Yemen S, and Palmer LA. Gender differences in S-nitrosoglutathione reductase activity in the lung. PLoS One 5: e14007, 2010.
29. Canãs A, López-Sánchez LM, Penãrando J, Valverde A, Conde F, Hernández V, Fuentes E, López-Pedrera C, de la Haba-Rodríguez JR, Aranda E, and Rodríguez-Ariza A. Altered S-nitrosothiol homeostasis provides a survival advantage to breast cancer cells in HER2 tumors and reduces their sensitivity to trastuzumab. Biochim Biophys Acta 1862: 601-610, 2016.
30. Cao Y, Gomes SA, Rangel EB, Paulino EC, Fonseca TL, Li J, Teixeira MB, Gouveia CH, Bianco AC, Kapiloff MS, Balkan W, and Hare JM. S-nitrosoglutathione reductasedependent PPARc denitrosylation participates in MSCderived adipogenesis and osteogenesis. J Clin Invest 125: 1679-1691, 2015.
31. Chakravarti R and Stuehr DJ. Thioredoxin-1 regulates cellular heme insertion by controlling S-nitrosation of glyceraldehyde-3-phosphate dehydrogenase. J Biol Chem 287: 16179-16186, 2012.
32. Chan NL, Rogers PH, and Arnone A. Crystal structure of the S-nitroso form of liganded human hemoglobin. Biochemistry 37: 16459-16464, 1998.
33. Chen Y, Zhao S, Wang Y, Li Y, Bai L, Liu R, Fan J, and Liu E. Homocysteine reduces protein S-nitrosylation in endothelium. Int J Mol Med 34: 1277-1285, 2014.
34. Chen YJ, Ku WC, Lin PY, Chou HC, Khoo KH, and Chen YJ. S-alkylating labeling strategy for site-specific identification of the s-nitrosoproteome. J Proteome Res 9: 6417-6439, 2010.
35. Chen YJ, Lu CT, Su MG, Huang KY, Ching WC, Yang HH, Liao YC, Chen YJ, and Lee TY. dbSNO 2.0: a resource for exploring structural environment, functional and disease association and regulatory network of protein S-nitrosylation. Nucleic Acids Res 43: D503-D511, 2015.
36. Choi LS and Bayley H. S-nitrosothiol chemistry at the single-molecule level. Angew Chem Int Ed Engl 51: 7972-7976, 2012.
37. Choi MS, Nakamura T, Cho SJ, Han X, Holland EA, Qu J, Petsko GA, Yates JR, Liddington RC, and Lipton SA. Transnitrosylation from DJ-1 to PTEN attenuates neuronal cell death in Parkinson's disease models. J Neurosci 34: 15123-15131, 2014.
38. Choi YB, Tenneti L, Le DA, Ortiz J, Bai G, Chen HS, and Lipton SA. Molecular basis of NMDA receptor-coupled ion channel modulation by S-nitrosylation. Nat Neurosci 3: 15-21, 2000.
39. Chung HS, Murray CI, Venkatraman V, Crowgey EL, Rainer PP, Cole RN, Bomgarden RD, Rogers JC, Balkan W, Hare JM, Kass DA, and Van Eyk JE. Dual labeling biotin switch assay to reduce bias derived from different cysteine subpopulations: a method to maximize Snitrosylation detection. Circ Res 117: 846-857, 2015.
40. Collet JF and Messens J. Structure, function, and mechanism of thioredoxin proteins. Antioxid Redox Signal 13: 1205-1216, 2010.
41. Cox AG, Saunders DC, Kelsey PB, Conway AA, Tesmenitsky Y, Marchini JF, Brown KK, Stamler JS, Colagiovanni DB, Rosenthal GJ, Croce KJ, North TE, and Goessling W. S-nitrosothiol signaling regulates liver development and improves outcome following toxic liver injury. Cell Rep 6: 56-69, 2014.
42. Davaapil H, Tsuchiya Y, and Gout I. Signalling functions of coenzyme A and its derivatives in mammalian cells. Biochem Soc Trans 42: 1056-1062, 2014.
43. Denis PA, Ventura ON, Mai HT, and Nguyen MT. Ab initio and density functional study of thionitroso XNS and thiazyl isomers XSN, X= H, F, Cl, Br, OH, SH, NH2, CH3, CF3, and SiF3. J Phys Chem A 108: 5073-5080, 2004.
44. Derakhshan B, Hao G, and Gross SS. Balancing reactivity against selectivity: the evolution of protein S-nitrosylation as an effector of cell signaling by nitric oxide. Cardiovasc Res 75: 210-219, 2007.
45. Doulias PT, Greene JL, Greco TM, Tenopoulou M, Seeholzer SH, Dunbrack RL, and Ischiropoulos H. 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 107: 16958-16963, 2010.
46. Drouin G, Godin JR, and Pagé B. The genetics of vitamin C loss in vertebrates. Curr Genomics 12: 371-378, 2011.
47. Erwin PA, Lin AJ, Golan DE, and Michel T. Receptorregulated dynamic S-nitrosylation of endothelial nitricoxide synthase in vascular endothelial cells. J Biol Chem 280: 19888-19894, 2005.
48. Erwin PA, Mitchell DA, Sartoretto J, Marletta MA, and Michel T. Subcellular targeting and differential Snitrosylation of endothelial nitric-oxide synthase. J Biol Chem 281: 151-157, 2006.
49. Eu JP, Hare JM, Hess DT, Skaf M, Sun J, Cardenas-Navina I, Sun QA, Dewhirst M, Meissner G, and Stamler JS. Concerted regulation of skeletal muscle contractility by oxygen tension and endogenous nitric oxide. Proc Natl Acad Sci U S A 100: 15229-15234, 2003.
50. Eu JP, Sun J, Xu L, Stamler JS, and Meissner G. The skeletal muscle calcium release channel: coupled O2 sensor and NO signaling functions. Cell 102: 499-509, 2000.
51. Fang M, Jaffrey SR, Sawa A, Ye K, Luo X, and Snyder SH. Dexras1: a G protein specifically coupled to neuronal nitric oxide synthase via CAPON. Neuron 28: 183-193, 2000.
52. Fernández MR, Biosca JA, and Parés X. Snitrosoglutathione reductase activity of human and yeast glutathione-dependent formaldehyde dehydrogenase and its nuclear and cytoplasmic localisation. Cell Mol Life Sci 60: 1013-1018, 2003.
53. Fernhoff NB, Derbyshire ER, and Marletta MA. A nitric oxide/cysteine interaction mediates the activation of soluble guanylate cyclase. Proc Natl Acad Sci U S A 106: 21602-21607, 2009.
54. Ferrini ME, Simons BJ, Bassett DJP, Bradley MO, Roberts K, and Jaffar Z. S-nitrosoglutathione reductase inhibition regulates allergen-induced lung inflammation and airway hyperreactivity. PLoS One 8: e70351, 2013.
55. Filipovic MR, Miljkovic JL, Nauser T, Royzen M, Klos K, Shubina T, Koppenol WH, Lippard SJ, and Ivanovic-Burmazovic I. Chemical characterization of the smallest S-nitrosothiol, HSNO; cellular cross-talk of H2S and Snitrosothiols. J Am Chem Soc 134: 12016-12027, 2012.
56. Forrester MT, Seth D, Hausladen A, Eyler CE, Foster MW, Matsumoto A, Benhar M, Marshall HE, and Stamler JS. Thioredoxin-interacting protein (TXNIP) is a feedback regulator of S-nitrosylation.JBiolChem284: 36160-36166, 2009.
57. Forrester MT, Thompson JW, Foster MW, Nogueira L, Moseley MA, and Stamler JS. Proteomic analysis of Snitrosylation and denitrosylation by resin-assisted capture. Nat Biotechnol 27: 557-559, 2009.
58. Foster MW, Hess DT, and Stamler JS. Protein Snitrosylation in health and disease: a current perspective. Trends Mol Med 15: 391-404, 2009.
59. Foster MW, Liu L, Zeng M, Hess DT, and Stamler JS. A genetic analysis of nitrosative stress. Biochemistry 48: 792-799, 2009.
60. Foster MW, McMahon TJ, and Stamler JS. S-nitrosylation in health and disease. Trends Mol Med 9: 160-168, 2003.
61. Foster MW and Stamler JS. New insights into protein S-nitrosylation. Mitochondria as a model system. J Biol Chem 279: 25891-25897, 2004.
62. Fourquet S, Guerois R, Biard D, and Toledano MB. Activation of NRF2 by nitrosative agents and H2O2 involves KEAP1 disulfide formation. J Biol Chem 285: 8463-8471, 2010.
63. Fu Y, Mou Y, Lin BL, Liu L, and Guo QX. Structures of the X-Y-NO molecules and homolytic dissociation energies of the Y-NO bonds (Y = C, N, O, S). J Phys Chem A 106: 12386-12392, 2002.
64. Gabbay KH, Bohren KM, Morello R, Bertin T, Liu J, and Vogel P. Ascorbate synthesis pathway: dual role of ascorbate in bone homeostasis. J Biol Chem 285: 19510-19520, 2010.
65. Gaston B, Reilly J, Drazen JM, Fackler J, Ramdev P, Arnelle D, Mullins ME, Sugarbaker DJ, Chee C, and Singel DJ. Endogenous nitrogen oxides and bronchodilator S-nitrosothiols in human airways. Proc Natl Acad Sci U S A 90: 10957-10961, 1993.
66. Gomes SA, Rangel EB, Premer C, Dulce RA, Cao Y, Florea V, Balkan W, Rodrigues CO, Schally AV, and Hare JM. S-nitrosoglutathione reductase (GSNOR) enhances vasculogenesis by mesenchymal stem cells. Proc Natl Acad Sci U S A 110: 2834-2839, 2013.
67. Gould NS, Evans P, Martínez-Acedo P, Marino SM, Gladyshev VN, Carroll KS, and Ischiropoulos H. Sitespecific proteomic mapping identifies selectively modified regulatory cysteine residues in functionally distinct protein networks. Chem Biol 22: 965-975, 2015.
68. Gow AJ, Chen Q, Hess DT, Day BJ, Ischiropoulos H, and Stamler JS. Basal and stimulated protein S-nitrosylation in multiple cell types and tissues. J Biol Chem 277: 9637-9640, 2002.
69. Gow AJ and Ischiropoulos H. Nitric oxide chemistry and cellular signaling. J Cell Physiol 187: 277-282, 2001.
70. Greco TM, Hodara R, Parastatidis I, Heijnen HFG, Dennehy MK, Liebler DC, and Ischiropoulos H. Identification of S-nitrosylation motifs by site-specific mapping of the S-nitrosocysteine proteome in human vascular smooth muscle cells. Proc Natl Acad Sci U S A 103: 7420-7425, 2006.
71. Guerra D, Ballard K, Truebridge I, and Vierling E. Snitrosation of conserved cysteines modulates activity and stability of S-nitrosoglutathione reductase (GSNOR). Biochemistry 55: 2452-2464, 2016.
72. Haldar SM and Stamler JS. S-nitrosylation: integrator of cardiovascular performance and oxygen delivery. J Clin Invest 123: 101-110, 2013.
73. Hao G, Derakhshan B, Shi L, Campagne F, and Gross SS. SNOSID, a proteomic method for identification of cysteine S-nitrosylation sites in complex protein mixtures. Proc Natl Acad Sci U S A 103: 1012-1017, 2006.
74. Hartmanová T, Tambor V, Lenc?o J, Staab-Weijnitz CA, Maser E, and Wsól V. S-nitrosoglutathione covalently modifies cysteine residues of human carbonyl reductase 1 and affects its activity. Chem Biol Interact 202: 136-145, 2013.
75. Hatzistergos KE, Paulino EC, Dulce RA, Takeuchi LM, Bellio MA, Kulandavelu S, Cao Y, Balkan W, Kanashiro-Takeuchi RM, and Hare JM. S-nitrosoglutathione reductase deficiency enhances the proliferative expansion of adult heart progenitors and myocytes post myocardial infarction. J Am Heart Assoc 4: e001974, 2015.
76. Hess DT, Matsumoto A, Kim SO, Marshall HE, and Stamler JS. Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 6: 150-166, 2005.
77. Hess DT, Matsumoto A, Nudelman R, and Stamler JS. Snitrosylation: spectrum and specificity. Nat Cell Biol 3: E46-E49, 2001.
78. Ho GPH, Selvakumar B, Mukai J, Hester LD, Wang Y, Gogos JA, and Snyder SH. S-nitrosylation and Spalmitoylation reciprocally regulate synaptic targeting of PSD-95. Neuron 71: 131-141, 2011.
79. Hoffmann J, Haendeler J, Zeiher AM, and Dimmeler S. TNFalpha and oxLDL reduce protein S-nitrosylation in endothelial cells. J Biol Chem 276: 41383-41387, 2001.
80. Houk KN, Hietbrink BN, Bartberger MD, McCarren PR, Choi BY, Voyksner RD, Stamler JS, and Toone EJ. Nitroxyl disulfides, novel intermediates in transnitrosation reactions. J Am Chem Soc 125: 6972-6976, 2003.
81. Iborra FJ, Renau-Piqueras J, Portoles M, Boleda MD, Guerri C, and Pares X. Immunocytochemical and biochemical demonstration of formaldhyde dehydrogenase (class III alcohol dehydrogenase) in the nucleus. J Histochem Cytochem 40: 1865-1878, 1992.
82. Ignarro LJ, Buga GM, Wood KS, Byrns RE, and Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci U S A 84: 9265-9269, 1987.
83. Irie T, Sips PY, Kai S, Kida K, Ikeda K, Hirai S, Moazzami K, Jiramongkolchai P, Bloch DB, Doulias PT, Armoundas AA, Kaneki M, Ischiropoulos H, Kranias E, Bloch KD, Stamler JS, and Ichinose F. S-nitrosylation of calcium-handling proteins in cardiac adrenergic signaling and hypertrophy. Circ Res 117: 793-803, 2015.
84. Ito T, Yamakuchi M, and Lowenstein CJ. Thioredoxin increases exocytosis by denitrosylating N-ethylmaleimidesensitive factor. J Biol Chem 286: 11179-11184, 2011.
85. Ivanova LV, Cibich D, Deye G, Talipov MR, and Timerghazin QK. Modeling of S-nitrosothiol-thiol reactions of biological significance: HNO production by S-thiolation requires a proton shuttle and stabilization of polar intermediates. Chembiochem 18: 726-738, 2017.
86. Iwakiri Y, Satoh A, Chatterjee S, Toomre DK, Chalouni CM, Fulton D, Groszmann RJ, Shah VH, and Sessa WC. Nitric oxide synthase generates nitric oxide locally to regulate compartmentalized protein S-nitrosylation and protein trafficking. Proc Natl Acad Sci U S A 103: 19777-19782, 2006.
87. Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, and Snyder SH. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat Cell Biol 3: 193-197, 2001.
88. Jakubowski H. Homocysteine-thiolactone and S-nitrosohomocysteine mediate incorporation of homocysteine into protein in humans. Clin Chem Lab Med 41: 1462-1466, 2003.
89. Jensen DE, Belka GK, and Du Bois GC. SNitrosoglutathione is a substrate for rat alcohol dehydrogenase class III isoenzyme. Biochem J 331: 659-668, 1998.
90. Jia J, Arif A, Terenzi F, Willard B, Plow EF, Hazen SL, and Fox PL. Target-selective protein S-nitrosylation by sequence motif recognition. Cell 159: 623-634, 2014.
91. Jia L, Bonaventura C, Bonaventura J, and Stamler JS. Snitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature 380: 221-226, 1996.
92. Kelleher ZT, Sha Y, Foster MW, Foster WM, Forrester MT, and Marshall HE. Thioredoxin-mediated denitrosylation regulates cytokine-induced nuclear factor jB (NF-jB) activation. J Biol Chem 289: 3066-3072, 2014.
93. Kim SF, Huri DA, and Snyder SH. Inducible nitric oxide synthase binds, S-nitrosylates, and activates cyclooxygenase-2. Science 310: 1966-1970, 2005.
94. Kim SO, Merchant K, Nudelman R, Beyer WF, Keng T, DeAngelo J, Hausladen A, and Stamler JS. OxyR: a molecular code for redox-related signaling. Cell 109: 383-396, 2002.
95. Kornau HC, Schenker LT, Kennedy MB, and Seeburg PH. Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269: 1737-1740, 1995.
96. Kornberg MD, Sen N, Hara MR, Juluri KR, Nguyen JVK, Snowman AM, Law L, Hester LD, and Snyder SH. GAPDH mediates nitrosylation of nuclear proteins. Nat Cell Biol 12: 1094-1100, 2010.
97. Kovacs I and Lindermayr C. Nitric oxide-based protein modification: formation and site-specificity of protein Snitrosylation. Front Plant Sci 4: 137, 2013.
98. Larroy C, Fernández MR, González E, Parés X, and Biosca JA. Characterization of the Saccharomyces cerevisiae YMR318C (ADH6) gene product as a broad specificity NADPH-dependent alcohol dehydrogenase: relevance in aldehyde reduction. Biochem J 361: 163-172, 2002.
99. Lee YI, Giovinazzo D, Kang HC, Lee Y, Jeong JS, Doulias PT, Xie Z, Hu J, Ghasemi M, Ischiropoulos H, Qian J, Zhu H, Blackshaw S, Dawson VL, and Dawson TM. Protein microarray characterization of the S-nitrosoproteome. Mol Cell Proteomics 13: 63-72, 2014.
100. Leonardi R, Zhang YM, Rock CO, and Jackowski S. Coenzyme A: back in action. Prog Lipid Res 44: 125-153, 2005.
101. Leung J, Wei W, and Liu L. S-nitrosoglutathione reductase deficiency increases mutagenesis from alkylation in mouse liver. Carcinogenesis 34: 984-989, 2013.
102. Lima B, Forrester MT, Hess DT, and Stamler JS. Snitrosylation in cardiovascular signaling. Circ Res 106: 633-646, 2010.
103. Lima B, Lam GKW, Xie L, Diesen DL, Villamizar N, Nienaber J, Messina E, Bowles D, Kontos CD, Hare JM, Stamler JS, and Rockman HA. Endogenous Snitrosothiols protect against myocardial injury. Proc Natl Acad Sci U S A 106: 6297-6302, 2009.
104. Lipton AJ, Johnson MA, Macdonald T, Lieberman MW, Gozal D, and Gaston B. S-nitrosothiols signal the ventilatory response to hypoxia. Nature 413: 171-174, 2001.
105. Liu L, Hausladen A, Zeng M, Que L, Heitman J, and Stamler JS. A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410: 490-494, 2001.
106. Liu L, Yan Y, Zeng M, Zhang J, Hanes MA, Ahearn G, McMahon TJ, Dickfeld T, Marshall HE, Que LG, and Stamler JS. Essential roles of S-nitrosothiols in vascular homeostasis and endotoxic shock. Cell 116: 617-628, 2004.
107. Liu X, Miller MJS, Joshi MS, Thomas DD, and Lancaster JR. Accelerated reaction of nitric oxide with O2 within the hydrophobic interior of biological membranes. Proc Natl Acad Sci U S A 95: 2175-2179, 1998.
108. López-Sánchez LM, Corrales FJ, González R, Ferrín G, Muñoz-Castañeda JR, Ranchal I, Hidalgo AB, Briceño J, López-Cillero P, Gómez MA, De La Mata M, Muntané J, and Rodríguez-Ariza A. Alteration of S-nitrosothiol homeostasis and targets for protein S-nitrosation in human hepatocytes. Proteomics 8: 4709-4720, 2008.
109. López-Sánchez LM, Corrales FJ, López-Pedrera C, Aranda E, and Rodríguez-Ariza A. Pharmacological impairment of s-nitrosoglutathione or thioredoxin reductases augments protein S-nitrosation in human hepatocarcinoma cells. Anticancer Res 30: 415-421, 2010.
110. Mahoney CW, Pak JH, and Huang KP. Nitric oxide modification of rat brain neurogranin. Identification of the cysteine residues involved in intramolecular disulfide bridge formation using site-directed mutagenesis. J Biol Chem 271: 28798-28804, 1996.
111. Mannick JB, Hausladen A, Liu L, Hess DT, Zeng M, Miao QX, Kane LS, Gow AJ, and Stamler JS. Fas-induced caspase denitrosylation. Science 284: 651-654, 1999.
112. Marino SM and Gladyshev VN. Structural analysis of cysteine S-nitrosylation: a modified acid-based motif and the emerging role of trans-nitrosylation. J Mol Biol 395: 844-859, 2010.
113. Marozkina NV and Gaston B. S-nitrosylation signaling regulates cellular protein interactions. Biochim Biophys Acta 1820: 722-729, 2012.
114. Marozkina NV, Wang XQ, Stsiapura V, Fitzpatrick A, Carraro S, Hawkins GA, Bleecker E, Meyers D, Jarjour N, Fain SB, Wenzel S, Busse W, Castro M, Panettieri RA, Moore W, Lewis SJ, Palmer LA, Altes T, de Lange EE, Erzurum S, Teague WG, and Gaston B. Phenotype of asthmatics with increased airway S-nitrosoglutathione reductase activity. Eur Respir J 45: 87-97, 2015.
115. Marozkina NV, Wei C, Yemen S, Wallrabe H, Nagji AS, Liu L, Morozkina T, Jones DR, and Gaston B. Snitrosoglutathione reductase in human lung cancer. Am J Respir Cell Mol Biol 46: 63-70, 2012.
116. Martínez-Ruiz A and Lamas S. Signalling by NO-induced protein S-nitrosylation and S-glutathionylation: convergences and divergences. Cardiovasc Res 75: 220-228, 2007.
117. Mayer B, Kleschyov AL, Stessel H, Russwurm M, Munzel T, Koesling D, and Schmidt K. Inactivation of soluble guanylate cyclase by stoichiometric S-nitrosation. Mol Pharmacol 75: 886-891, 2009.
118. McMahon TJ, Exton Stone A, Bonaventura J, Singel DJ, and Stamler JS. Functional coupling of oxygen binding and vasoactivity in S-nitrosohemoglobin. J Biol Chem 275: 16738-16745, 2000.
119. Minning DM, Gow AJ, Bonaventura J, Braun R, Dewhirst M, Goldberg DE, and Stamler JS. Ascaris haemoglobin is a nitric oxide-activated ''deoxygenase.'' Nature 401: 497-502, 1999.
120. Mitchell DA, Erwin PA, Michel T, and Marletta MA. Snitrosation and regulation of inducible nitric oxide synthase. Biochemistry 44: 4636-4647, 2005.
121. Mitchell DA and Marletta MA. Thioredoxin catalyzes the S-nitrosation of the caspase-3 active site cysteine. Nat Chem Biol 1: 154-158, 2005.
122. Mitchell DA, Morton SU, Fernhoff NB, and Marletta MA. Thioredoxin is required for S-nitrosation of procaspase-3 and the inhibition of apoptosis in Jurkat cells. Proc Natl Acad Sci U S A 104: 11609-11614, 2007.
123. Moon Y, Cao Y, Zhu J, Xu Y, Balkan W, Buys ES, Diaz F, Kerrick WG, Hare JM, and Percival JM. GSNOR deficiency enhances in situ skeletal muscle strength, fatigue resistance, and RyR1 S-nitrosylation without impacting mitochondrial content and activity. Antioxid Redox Signal 26: 165-181, 2017.
124. Moore PE, Ryckman KK, Williams SM, Patel N, Summar ML, and Sheller JR. Genetic variants of GSNOR and ADRB2 influence response to albuterol in African-American children with severe asthma. Pediatr Pulmonol 44: 649-654, 2009.
125. Morris S and Hansen JN. Inhibition of Bacillus cereus spore outgrowth by covalent modification of a sulfhydryl group by nitrosothiol and iodoacetate. J Bacteriol 148: 465-471, 1981.
126. Murad F. Cyclic guanosine monophosphate as a mediator of vasodilation. J Clin Invest 78: 1-5, 1986.
127. Murray CI, Uhrigshardt H, O'Meally RN, Cole RN, and Van Eyk JE. Identification and quantification of Snitrosylation by cysteine reactive tandem mass tag switch assay. Mol Cell Proteomics 11: M111.013441, 2012.
128. Nedospasov A, Rafikov R, Beda N, and Nudler E. An autocatalytic mechanism of protein nitrosylation. Proc Natl Acad Sci U S A 97: 13543-13548, 2000.
129. Nikitovic D and Holmgren A. S-nitrosoglutathione is cleaved by the thioredoxin system with liberation of glutathione and redox regulating nitric oxide. J Biol Chem 271: 19180-19185, 1996.
130. Nogales E, Whittaker M, Milligan RA, and Downing KH. High-resolution model of the microtubule. Cell 96: 79-88, 1999.
131. O'Connor T, Ireland LS, Harrison DJ, and Hayes JD. Major differences exist in the function and tissue-specific expression of human aflatoxin B1 aldehyde reductase and the principal human aldo-keto reductase AKR1 family members. Biochem J 343: 487-504, 1999.
132. de Oliveira MG, Shishido SM, Seabra AB, and Morgon NH. Thermal stability of primary S-nitrosothiols: roles of autocatalysis and structural effects on the rate of nitric oxide release. J Phys Chem A 106: 8963-8970, 2002.
133. Oppermann U. Carbonyl reductases: the complex relationships of mammalian carbonyl-and quinone-reducing enzymes and their role in physiology. Annu Rev Pharmacol Toxicol 47: 293-322, 2007.
134. Ovadia H, Haim Y, Nov O, Almog O, Kovsan J, Bashan N, Benhar M, and Rudich A. Increased adipocyte Snitrosylation targets anti-lipolytic action of insulin: relevance to adipose tissue dysfunction in obesity. J Biol Chem 286: 30433-30443, 2011.
135. Ozawa K, Tsumoto H, Wei W, Tang C-H, Komatsubara AT, Kawafune H, Shimizu K, Liu L, and Tsujimoto G. Proteomic analysis of the role of S-nitrosoglutathione reductase in lipopolysaccharide-challenged mice. Proteomics 12: 2024-2035, 2012.
136. Ozawa K, Whalen EJ, Nelson CD, Mu Y, Hess DT, Lefkowitz RJ, and Stamler JS. S-nitrosylation of betaarrestin regulates beta-adrenergic receptor trafficking. Mol Cell 31: 395-405, 2008.
137. Pader I, Sengupta R, Cebula M, Xu J, Lundberg JO, Holmgren A, Johansson K, and Arnér ESJ. Thioredoxinrelated protein of 14 kDa is an efficient l-cystine reductase and S-denitrosylase. Proc Natl Acad Sci U S A 111: 6964-6969, 2014.
138. Paige JS, Xu G, Stancevic B, and Jaffrey SR. Nitrosothiol reactivity profiling identifies S-nitrosylated proteins with unexpected stability. Chem Biol 15: 1307-1316, 2008.
139. Palackal NT, Burczynski ME, Harvey RG, and Penning TM. The ubiquitous aldehyde reductase (AKR1A1) oxidizes proximate carcinogen trans-dihydrodiols to o-quinones: potential role in polycyclic aromatic hydrocarbon activation. Biochemistry 40: 10901-10910, 2001.
140. Palmer LA, Kimberly deRonde, Brown-Steinke K, Gunter S, Jyothikumar V, Forbes MS, and Lewis SJ. Hypoxiainduced changes in protein S-nitrosylation in female mouse brainstem. Am J Respir Cell Mol Biol 52: 37-45, 2015.
141. Palmer RM, Ferrige AG, and Moncada S. Nitric oxide release accounts for the biological activity of endotheliumderived relaxing factor. Nature 327: 524-526, 1987.
142. Pawloski JR, Hess DT, and Stamler JS. Export by red blood cells of nitric oxide bioactivity. Nature 409: 622-626, 2001.
143. Perez-Mato I, Castro C, Ruiz FA, Corrales FJ, and Mato JM. Methionine adenosyltransferase S-nitrosylation is regulated by the basic and acidic amino acids surrounding the target thiol. J Biol Chem 274: 17075-17079, 1999.
144. Perissinotti LL, Leitus G, Shimon L, Estrin D, and Doctorovich F. A unique family of stable and watersoluble S-nitrosothiol complexes. Inorg Chem 47: 4723-4733, 2008.
145. Perreault M and Marette A. Targeted disruption of inducible nitric oxide synthase protects against obesitylinked insulin resistance in muscle. Nat Med 7: 1138-1143, 2001.
146. Qu Z, Meng F, Bomgarden RD, Viner RI, Li J, Rogers JC, Cheng J, Greenlief CM, Cui J, Lubahn DB, Sun GY, and Gu Z. Proteomic quantification and site-mapping of S-nitrosylated proteins using isobaric iodoTMT reagents. J Proteome Res 13: 3200-3211, 2014.
147. Qu ZW, Miao WY, Hu SQ, Li C, Zhuo XL, Zong YY, Wu YP, and Zhang G-Y. N-methyl-d-aspartate receptordependent denitrosylation of neuronal nitric oxide synthase increase the enzyme activity. PLoS One 7: e52788, 2012.
148. Que LG, Liu L, Yan Y, Whitehead GS, Gavett SH, Schwartz DA, and Stamler JS. Protection from experimental asthma by an endogenous bronchodilator. Science 308: 1618-1621, 2005.
149. Que LG, Yang Z, Stamler JS, Lugogo NL, and Kraft M. S-nitrosoglutathione reductase: an important regulator in human asthma. Am J Respir Crit Care Med 180: 226-231, 2009.
150. Raffay TM, Dylag AM, Di Fiore JM, Smith LA, Einisman HJ, Li Y, Lakner MM, Khalil AM, MacFarlane PM, Martin RJ, and Gaston B. S-nitrosoglutathione attenuates airway hyperresponsiveness in murine bronchopulmonary dysplasia. Mol Pharmacol 90: 418-426, 2016.
151. Rafikova O, Rafikov R, and Nudler E. Catalysis of Snitrosothiols formation by serum albumin: the mechanism and implication in vascular control. Proc Natl Acad Sci U S A 99: 5913-5918, 2002.
152. Raju K, Doulias PT, Evans P, Krizman EN, Jackson JG, Horyn O, Daikhin Y, Nissim I, Yudkoff M, Nissim I, Sharp KA, Robinson MB, and Ischiropoulos H. Regulation of brain glutamate metabolism by nitric oxide and Snitrosylation. Sci Signal 8: ra68, 2015.
153. Ravi K, Brennan LA, Levic S, Ross PA, and Black SM. S-nitrosylation of endothelial nitric oxide synthase is associated with monomerization and decreased enzyme activity. Proc Natl Acad Sci U S A 101: 2619-2624, 2004.
154. Rizza S, Montagna C, Cardaci S, Maiani E, Di Giacomo G, Sanchez-Quiles V, Blagoev B, Rasola A, De Zio D, Stamler JS, Cecconi F, and Filomeni G. S-nitrosylation of the mitochondrial chaperone TRAP1 sensitizes hepatocellular carcinoma cells to inhibitors of succinate dehydrogenase. Cancer Res 76: 4170-4182, 2016.
155. Rizzo MA and Piston DW. Regulation of beta cell glucokinase by S-nitrosylation and association with nitric oxide synthase. J Cell Biol 161: 243-248, 2003.
156. Roediger WE. Nitric oxide-dependent nitrosation of cellular CoA: a proposal for tissue responses. Nitric Oxide 5: 83-87, 2001.
157. Roediger WE, Hems R, Wiggins D, and Gibbons GF. Inhibition of hepatocyte lipogenesis by nitric oxide donor: could nitric oxide regulate lipid synthesis? IUBMB Life 56: 35-40, 2004.
158. Romero JM and Bizzozero OA. Intracellular glutathione mediates the denitrosylation of protein nitrosothiols in the rat spinal cord. J Neurosci Res 87: 701-709, 2009.
159. Roy B, du Moulinet d'Hardemare A, and Fontecave M. New thionitrites: synthesis, stability, and nitric oxide generation. J Org Chem 59: 7019-7026, 1994.
160. Savidge TC, Urvil P, Oezguen N, Ali K, Choudhury A, Acharya V, Pinchuk I, Torres AG, English RD, Wiktorowicz JE, Loeffelholz M, Kumar R, Shi L, Nie W, Braun W, Herman B, Hausladen A, Feng H, Stamler JS, and Pothoulakis C. Host S-nitrosylation inhibits clostridial small molecule-activated glucosylating toxins. Nat Med 17: 1136-1141, 2011.
161. Sayed N, Baskaran P, Ma X, van den Akker F, and Beuve A. Desensitization of soluble guanylyl cyclase, the NO receptor, by S-nitrosylation. Proc Natl Acad Sci U S A 104: 12312-12317, 2007.
162. Scharfstein JS, Keaney JF, Slivka A, Welch GN, Vita JA, Stamler JS, and Loscalzo J. In vivo transfer of nitric oxide between a plasma protein-bound reservoir and low molecular weight thiols. J Clin Invest 94: 1432-1439, 1994.
163. Sengupta R, Billiar TR, Kagan VE, and Stoyanovsky DA. Nitric oxide and thioredoxin type 1 modulate the activity of caspase 8 in HepG2 cells. Biochem Biophys Res Commun 391: 1127-1130, 2010.
164. Sengupta R, Ryter SW, Zuckerbraun BS, Tzeng E, Billiar TR, and Stoyanovsky DA. Thioredoxin catalyzes the denitrosation of low-molecular mass and protein S-nitrosothiols. Biochemistry 46: 8472-8483, 2007.
165. Seth D, Hausladen A, Wang YJ, and Stamler JS. Endogenous protein S-nitrosylation in E. coli: regulation by OxyR. Science 336: 470-473, 2012.
166. Seth D and Stamler JS. The SNO-proteome: causation and classifications. Curr Opin Chem Biol 15: 129-136, 2011.
167. Singh SP, Wishnok JS, Keshive M, Deen WM, and Tannenbaum SR. The chemistry of the S-nitrosoglutathione/ glutathione system. Proc Natl Acad Sci U S A 93: 14428-14433, 1996.
168. Sips PY, Irie T, Zou L, Shinozaki S, Sakai M, Shimizu N, Nguyen R, Stamler JS, Chao W, Kaneki M, and Ichinose F. Reduction of cardiomyocyte S-nitrosylation by Snitrosoglutathione reductase protects against sepsis-induced myocardial depression. Am J Physiol Heart Circ Physiol 304: H1134-H1146, 2013.
169. Sliskovic I, Raturi A, and Mutus B. Characterization of the S-denitrosation activity of protein disulfide isomerase. J Biol Chem 280: 8733-8741, 2005.
170. de Smidt O, du Preez JC, and Albertyn J. The alcohol dehydrogenases of Saccharomyces cerevisiae: a comprehensive review. FEMS Yeast Res 8: 967-978, 2008.
171. Staab CA, Alander J, Brandt M, Lengqvist J, Morgenstern R, Grafström RC, and Höög J-O. Reduction of Snitrosoglutathione 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, 2008.
172. Staab CA, Hartmanová T, El-Hawari Y, Ebert B, Kisiela M, Wsol V, Martin HJ, and Maser E. Studies on reduction of S-nitrosoglutathione by human carbonyl reductases 1 and 3. Chem Biol Interact 191: 95-103, 2011.
173. Stamler JS and Hausladen A. Oxidative modifications in nitrosative stress. Nat Struct Biol 5: 247-249, 1998.
174. Stamler JS, Singel DJ, and Loscalzo J. Biochemistry of nitric oxide and its redox-activated forms. Science 258: 1898-1902, 1992.
175. Stamler JS and Toone EJ. The decomposition of thionitrites. Curr Opin Chem Biol 6: 779-785, 2002.
176. Stamler JS, Toone EJ, Lipton SA, and Sucher NJ. (S)NO signals: translocation, regulation, and a consensus motif. Neuron 18: 691-696, 1997.
177. Stoyanovsky DA, Tyurina YY, Tyurin VA, Anand D, Mandavia DN, Gius D, Ivanova J, Pitt B, Billiar TR, and Kagan VE. Thioredoxin and lipoic acid catalyze the denitrosation of low molecular weight and protein Snitrosothiols. J Am Chem Soc 127: 15815-15823, 2005.
178. Straub AC, Billaud M, Johnstone SR, Best AK, Yemen S, Dwyer ST, Looft-Wilson R, Lysiak JJ, Gaston B, Palmer L, and Isakson BE. Compartmentalized connexin 43 S-nitrosylation/denitrosylation regulates heterocellular communication in the vessel wall. Arterioscler Thromb Vasc Biol 31: 399-407, 2011.
179. Sun J, Xin C, Eu JP, Stamler JS, and Meissner G. Cysteine-3635 is responsible for skeletal muscle ryanodine receptor modulation by NO. Proc Natl Acad Sci U S A 98: 11158-11162, 2001.
180. Sun QA, Hess DT, Nogueira L, Yong S, Bowles DE, Eu J, Laurita KR, Meissner G, and Stamler JS. Oxygen-coupled redox regulation of the skeletal muscle ryanodine receptor-Ca2+ release channel by NADPH oxidase 4. Proc Natl Acad Sci U S A 108: 16098-16103, 2011.
181. Szmytkowski C and Maciag K. Total cross section for electron impact on nitrogen monoxide. J Phys B At Mol Opt Phys 24: 4273-4279, 1991.
182. Takahashi M, Miyata S, Fujii J, Inai Y, Ueyama S, Araki M, Soga T, Fujinawa R, Nishitani C, Ariki S, Shimizu T, Abe T, Ihara Y, Nishikimi M, Kozutsumi Y, Taniguchi N, and Kuroki Y. In vivo role of aldehyde reductase. Biochim Biophys Acta 1820: 1787-1796, 2012.
183. Talipov MR and Timerghazin QK. Protein control of Snitrosothiol reactivity: interplay of antagonistic resonance structures. J Phys Chem B 117: 1827-1837, 2013.
184. Tang CH, Wei W, Hanes MA, and Liu L. Hepatocarcinogenesis driven by GSNOR deficiency is prevented by iNOS inhibition. Cancer Res 73: 2897-2904, 2013.
185. Tello D, Tarín C, Ahicart P, Bretón-Romero R, Lamas S, and Martínez-Ruiz A. A ''fluorescence switch'' technique increases the sensitivity of proteomic detection and identification of S-nitrosylated proteins. Proteomics 9: 5359-5370, 2009.
186. Tennyson J and Noble CJ. Low-energy electron scattering by the NO molecule. J Phys B At Mol Phys 19: 4025-4033, 1986.
187. Thom SR, Bhopale VM, Milovanova TN, Yang M, and Bogush M. Thioredoxin reductase linked to cytoskeleton by focal adhesion kinase reverses actin S-nitrosylation and restores neutrophil b(2) integrin function. J Biol Chem 287: 30346-30357, 2012.
188. Timerghazin QK, Peslherbe GH, and English AM. Resonance description of S-nitrosothiols: insights into reactivity. Org Lett 9: 3049-3052, 2007.
189. Tu SI, Byler DM, and Cavanaugh JR. Nitrite inhibition of acyl transfer by coenzyme A via the formation of an S-nitrosothiol derivative. J Agric Food Chem 32: 1057-1060, 1984.
190. Valencia E, Larroy C, OchoaWF, ParésX, Fita I, and Biosca JA. Apo and Holo structures of an NADPH-dependent cinnamyl alcohol dehydrogenase from Saccharomyces cerevisiae. J Mol Biol 341: 1049-1062, 2004.
191. Villanueva C and Giulivi C. Subcellular and cellular locations of nitric oxide synthase isoforms as determinants of health and disease. Free Radic Biol Med 49: 307-316, 2010.
192. Wan C, Borgeson B, Phanse S, Tu F, Drew K, Clark G, Xiong X, Kagan O, Kwan J, Bezginov A, Chessman K, Pal S, Cromar G, Papoulas O, Ni Z, Boutz DR, Stoilova S, Havugimana PC, Guo X, Malty RH, Sarov M, Greenblatt J, Babu M, Derry WB, Tillier ER, Wallingford JB, Parkinson J, Marcotte EM, and Emili A. Panorama of ancient metazoan macromolecular complexes. Nature 525: 339-344, 2015.
193. Wang G, Moniri NH, Ozawa K, Stamler JS, and Daaka Y. Nitric oxide regulates endocytosis by S-nitrosylation of dynamin. Proc Natl Acad Sci U S A 103: 1295-1300, 2006.
194. Wang PG, Xian M, Tang X, Wu X, Wen Z, Cai T, and Janczuk AJ. Nitric oxide donors: chemical activities and biological applications. Chem Rev 102: 1091-1134, 2002.
195. Wei W, Li B, Hanes MA, Kakar S, Chen X, and Liu L. Snitrosylation from GSNOR deficiency impairs DNA repair and promotes hepatocarcinogenesis. Sci Transl Med 2: 19ra13, 2010.
196. Wei W, Yang Z, Tang CH, and Liu L. Targeted deletion of GSNOR in hepatocytes of mice causes nitrosative inactivation of O6-alkylguanine-DNA alkyltransferase and increased sensitivity to genotoxic diethylnitrosamine. Carcinogenesis 32: 973-977, 2011.
197. 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, and Stamler JS. Regulation of beta-adrenergic receptor signaling by Snitrosylation of G-protein-coupled receptor kinase 2. Cell 129: 511-522, 2007.
198. Williams DLH. The chemistry of S-nitrosothiols. Acc Chem Res 32: 869-876, 1999.
199. Williamson JR and Corkey BE. Assay of citric acid cycle intermediates and related compounds-update with tissue metabolite levels and intracellular distribution. In: Biomembranes, Part F: Bioenergetics-Oxidative Phosphorylation, edited by Fleischer S and Packer L. New York, NY: Academic Press, 1979, pp. 200-222.
200. Wong PS, Hyun J, Fukuto JM, Shirota FN, DeMaster EG, Shoeman DW, and Nagasawa HT. Reaction between Snitrosothiols and thiols: generation of nitroxyl (HNO) and subsequent chemistry. Biochemistry 37: 5362-5371, 1998.
201. Wu C, Liu T, Chen W, Oka S, Fu C, Jain MR, Parrott AM, Baykal AT, Sadoshima J, and Li H. Redox regulatory mechanism of transnitrosylation by thioredoxin. Mol Cell Proteomics 9: 2262-2275, 2010.
202. Wu C, Parrott AM, Fu C, Liu T, Marino SM, Gladyshev VN, Jain MR, Baykal AT, Li Q, Oka S, Sadoshima J, Beuve A, Simmons WJ, and Li H. Thioredoxin 1-mediated post-translational modifications: reduction, transnitrosylation, denitrosylation, and related proteomics methodologies. Antioxid Redox Signal 15: 2565-2604, 2011.
203. Wu C, Parrott AM, Liu T, Jain MR, Yang Y, Sadoshima J, and Li H. Distinction of thioredoxin transnitrosylation and denitrosylation target proteins by the ICAT quantitative approach. J Proteomics 74: 2498-2509, 2011.
204. 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, and London SJ. Genetic variation in S-nitrosoglutathione reductase (GSNOR) and childhood asthma. J Allergy Clin Immunol 120: 322-328, 2007.
205. Xu L, Eu JP, Meissner G, and Stamler JS. Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitrosylation. Science 279: 234-237, 1998.
206. Yang Z, Wang ZE, Doulias PT, Wei W, Ischiropoulos H, Locksley RM, and Liu L. Lymphocyte development requires S-nitrosoglutathione reductase. J Immunol 185: 6664-6669, 2010.
207. Zaman K, Sawczak V, Zaidi A, Butler M, Bennett D, Getsy P, Zeinomar M, Greenberg Z, Forbes M, Rehman S, Jyothikumar V, DeRonde K, Sattar A, Smith L, Corey D, Straub A, Sun F, Palmer L, Periasamy A, Randell S, Kelley TJ, Lewis SJ, and Gaston B. Augmentation of CFTR maturation by S-nitrosoglutathione reductase. Am J Physiol Lung Cell Mol Physiol 310: L263-L270, 2016.
208. Zhang R, Hess DT, Qian Z, Hausladen A, Fonseca F, Chaube R, Reynolds JD, and Stamler JS. Hemoglobin bCys93 is essential for cardiovascular function and integrated response to hypoxia. Proc Natl Acad Sci U S A 112: 6425-6430, 2015.
209. Zhang R, Hess DT, Reynolds JD, and Stamler JS. Hemoglobin S-nitrosylation plays an essential role in cardioprotection. J Clin Invest 126: 4654-4658, 2016.