Nitric oxide and the thioredoxin system: A complex interplay in redox regulation

Biochimica et Biophysica Acta - General Subjects

Volumn 1850, Issue 12, 2015, Pages 2476-2484

  Benhar, Moran ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Cysteine; Nitric oxide; Nitrosylation; Thioredoxin

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; THIOL; THIOREDOXIN; THIOREDOXIN REDUCTASE;

AMINO ACID SEQUENCE; APOPTOSIS; CELL ACTIVITY; ENZYME ACTIVATION; HUMAN; NITROSATIVE STRESS; NITROSYLATION; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; OXIDATION REDUCTION REACTION; PHYSIOLOGY;

ANIMALS; HUMANS; NITRIC OXIDE; OXIDATION-REDUCTION; THIOREDOXINS;

EID: 84942358036     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2015.09.010     Document Type: Review

References (133)

1. H.J. Forman, J.M. Fukuto, and M. Torres Redox signaling: thiol chemistry defines which reactive oxygen and nitrogen species can act as second messengers Am. J. Physiol. Cell Physiol. 287 2004 C246 C256
2. C.C. Winterbourn, and M.B. Hampton Thiol chemistry and specificity in redox signaling Free Radic. Biol. Med. 45 2008 549 561
3. Y.M. Janssen-Heininger, B.T. Mossman, N.H. Heintz, H.J. Forman, B. Kalyanaraman, T. Finkel, J.S. Stamler, S.G. Rhee, and A. van der Vliet Redox-based regulation of signal transduction: principles, pitfalls, and promises Free Radic. Biol. Med. 45 2008 1 17
4. N. Brandes, S. Schmitt, and U. Jakob Thiol-based redox switches in eukaryotic proteins Antioxid. Redox Signal. 11 2009 997 1014
5. B. D'Autreaux, and M.B. Toledano ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis Nat. Rev. Mol. Cell Biol. 8 2007 813 824
6. S.M. Marino, and V.N. Gladyshev Analysis and functional prediction of reactive cysteine residues J. Biol. Chem. 287 2012 4419 4425
7. L.B. Poole The basics of thiols and cysteines in redox biology and chemistry Free Radic. Biol. Med. 80C 2015 148 157
8. N.J. Pace, and E. Weerapana Diverse functional roles of reactive cysteines ACS Chem. Biol. 8 2012 283 296
9. Y.M. Go, and D.P. Jones The redox proteome J. Biol. Chem. 288 2013 26512 26520
10. C.E. Paulsen, and K.S. Carroll Cysteine-mediated redox signaling: chemistry, biology, and tools for discovery Chem. Rev. 113 2013 4633 4679
11. P. Pacher, J.S. Beckman, and L. Liaudet Nitric oxide and peroxynitrite in health and disease Physiol. Rev. 87 2007 315 424
12. J.S. Stamler Redox signaling: nitrosylation and related target interactions of nitric oxide Cell 78 1994 931 936
13. B.G. Hill, B.P. Dranka, S.M. Bailey, J.R. Lancaster Jr., and V.M. Darley-Usmar What part of NO don't you understand? Some answers to the cardinal questions in nitric oxide biology J. Biol. Chem. 285 2010 19699 19704
14. A. Martinez-Ruiz, S. Cadenas, and S. Lamas Nitric oxide signaling: classical, less classical, and nonclassical mechanisms Free Radic. Biol. Med. 51 2011 17 29
15. T.A. Heinrich, R.S. da Silva, K.M. Miranda, C.H. Switzer, D.A. Wink, and J.M. Fukuto Biological nitric oxide signalling: chemistry and terminology Br. J. Pharmacol. 169 2013 1417 1429
16. D.T. Hess, A. Matsumoto, S.O. Kim, H.E. Marshall, and J.S. Stamler Protein S-nitrosylation: purview and parameters Nat. Rev. Mol. Cell Biol. 6 2005 150 166
17. N. Gould, P.T. Doulias, M. Tenopoulou, K. Raju, and H. Ischiropoulos Regulation of protein function and signaling by reversible cysteine S-nitrosylation J. Biol. Chem. 288 2013 26473 26479
18. D. Seth, and J.S. Stamler The SNO-proteome: causation and classifications Curr. Opin. Chem. Biol. 15 2011 129 136
19. Y.J. Chen, C.T. Lu, M.G. Su, K.Y. Huang, W.C. Ching, H.H. Yang, Y.C. Liao, Y.J. Chen, and T.Y. Lee dbSNO 2.0: a resource for exploring structural environment, functional and disease association and regulatory network of protein S-nitrosylation Nucleic Acids Res. 43 2015 D503 D511
20. N.V. Marozkina, and B. Gaston S-nitrosylation signaling regulates cellular protein interactions Biochim. Biophys. Acta 1820 2012 722 729
21. M. Benhar, M.T. Forrester, and J.S. Stamler Protein denitrosylation: enzymatic mechanisms and cellular functions Nat. Rev. Mol. Cell Biol. 10 2009 721 732
22. R. Sengupta, and A. Holmgren The role of thioredoxin in the regulation of cellular processes by S-nitrosylation Biochim. Biophys. Acta 1820 2012 689 700
23. J.S. Paige, G. Xu, B. Stancevic, and S.R. Jaffrey Nitrosothiol reactivity profiling identifies S-nitrosylated proteins with unexpected stability Chem. Biol. 15 2008 1307 1316
24. C.H. Lillig, and A. Holmgren Thioredoxin and related molecules - from biology to health and disease Antioxid. Redox Signal. 9 2007 25 47
25. D.F. Mahmood, A. Abderrazak, K. El Hadri, T. Simmet, and M. Rouis The thioredoxin system as a therapeutic target in human health and disease Antioxid. Redox Signal. 19 2013 1266 1303
26. S. Lee, S.M. Kim, and R.T. Lee Thioredoxin and thioredoxin target proteins: from molecular mechanisms to functional significance Antioxid. Redox Signal. 18 2013 1165 1207
27. E.S. Arner Focus on mammalian thioredoxin reductases - important selenoproteins with versatile functions Biochim. Biophys. Acta 1790 2009 495 526
28. Y. Matsuo, and J. Yodoi Extracellular thioredoxin: a therapeutic tool to combat inflammation Cytokine Growth Factor Rev. 24 2013 345 353
29. L.S. Nakao, R.A. Everley, S.M. Marino, S.M. Lo, L.E. de Souza, S.P. Gygi, and V.N. Gladyshev Mechanism-based proteomic screening identifies targets of thioredoxin-like proteins J. Biol. Chem. 290 2015 5685 5695
30. E.M. Hanschmann, J.R. Godoy, C. Berndt, C. Hudemann, and C.H. Lillig Thioredoxins, glutaredoxins, and peroxiredoxins - molecular mechanisms and health significance: from cofactors to antioxidants to redox signaling Antioxid. Redox Signal. 19 2013 1539 1605
31. A. Holmgren, and J. Lu Thioredoxin and thioredoxin reductase: current research with special reference to human disease Biochem. Biophys. Res. Commun. 396 2010 120 124
32. J.F. Collet, and J. Messens Structure, function, and mechanism of thioredoxin proteins Antioxid. Redox Signal. 13 2010 1205 1216
33. P. Anand, and J.S. Stamler Enzymatic mechanisms regulating protein S-nitrosylation: implications in health and disease J. Mol. Med. 90 2012 233 244 Berlin, Germany
34. K.A. Broniowska, and N. Hogg The chemical biology of S-nitrosothiols Antioxid. Redox Signal. 17 2012 969 980
35. Q. Li, and J.R. Lancaster Jr. A conspectus of cellular mechanisms of nitrosothiol formation from nitric oxide Immunopathol. Dis. Therap. 3 2012 183 191
36. B. Kolesnik, C.L. Heine, R. Schmidt, K. Schmidt, B. Mayer, and A.C. Gorren Aerobic nitric oxide-induced thiol nitrosation in the presence and absence of magnesium cations Free Radic. Biol. Med. 76 2014 286 298
37. J.R. Hickok, S. Sahni, H. Shen, A. Arvind, C. Antoniou, L.W. Fung, and D.D. Thomas Dinitrosyliron complexes are the most abundant nitric oxide-derived cellular adduct: biological parameters of assembly and disappearance Free Radic. Biol. Med. 51 2011 1558 1566
38. C.A. Bosworth, J.C. Toledo Jr., J.W. Zmijewski, Q. Li, and J.R. Lancaster Jr. Dinitrosyliron complexes and the mechanism(s) of cellular protein nitrosothiol formation from nitric oxide Proc. Natl. Acad. Sci. U. S. A. 106 2009 4671 4676
39. S. Basu, A. Keszler, N.A. Azarova, N. Nwanze, A. Perlegas, S. Shiva, K.A. Broniowska, N. Hogg, and D.B. Kim-Shapiro A novel role for cytochrome c: efficient catalysis of S-nitrosothiol formation Free Radic. Biol. Med. 48 2010 255 263
40. B. Mayer, S. Pfeiffer, A. Schrammel, D. Koesling, K. Schmidt, and F. Brunner A new pathway of nitric oxide/cyclic GMP signaling involving S-nitrosoglutathione J. Biol. Chem. 273 1998 3264 3270
41. D.A. Mitchell, P.A. Erwin, T. Michel, and M.A. Marletta S-nitrosation and regulation of inducible nitric oxide synthase Biochemistry 44 2005 4636 4647
42. B.C. Smith, N.B. Fernhoff, and M.A. Marletta Mechanism and kinetics of inducible nitric oxide synthase auto-S-nitrosation and inactivation Biochemistry 51 2012 1028 1040
43. R.J. Rosenfeld, J. Bonaventura, B.R. Szymczyna, M.J. MacCoss, A.S. Arvai, J.R. Yates 3rd, J.A. Tainer, and E.D. Getzoff Nitric-oxide synthase forms N-NO-pterin and S-NO-cys: implications for activity, allostery, and regulation J. Biol. Chem. 285 2010 31581 31589
44. A. Martinez-Ruiz, I.M. Araujo, A. Izquierdo-Alvarez, P. Hernansanz-Agustin, S. Lamas, and J.M. Serrador Specificity in S-nitrosylation: a short-range mechanism for NO signaling? Antioxid. Redox Signal. 19 2013 1220 1235
45. B.C. Smith, and M.A. Marletta Mechanisms of S-nitrosothiol formation and selectivity in nitric oxide signaling Curr. Opin. Chem. Biol. 16 2012 498 506
46. T. Nakamura, and S.A. Lipton Emerging role of protein-protein transnitrosylation in cell signaling pathways Antioxid. Redox Signal. 18 2013 239 249
47. S.M. Marino, and V.N. Gladyshev Structural analysis of cysteine S-nitrosylation: a modified acid-based motif and the emerging role of trans-nitrosylation J. Mol. Biol. 395 2010 844 859
48. J. Jia, A. Arif, F. Terenzi, B. Willard, E.F. Plow, S.L. Hazen, and P.L. Fox Target-selective protein S-nitrosylation by sequence motif recognition Cell 159 2014 623 634
49. N. Hogg The biochemistry and physiology of S-nitrosothiols Annu. Rev. Pharmacol. Toxicol. 42 2002 585 600
50. A. Martinez-Ruiz, and S. Lamas S-nitrosylation: a potential new paradigm in signal transduction Cardiovasc. Res. 62 2004 43 52
51. T. Nakamura, L. Wang, C.C. Wong, F.L. Scott, B.P. Eckelman, X. Han, C. Tzitzilonis, F. Meng, Z. Gu, E.A. Holland, A.T. Clemente, S. Okamoto, G.S. Salvesen, R. Riek, J.R. Yates 3rd, and S.A. Lipton Transnitrosylation of XIAP regulates caspase-dependent neuronal cell death Mol. Cell 39 2010 184 195
52. M.D. Kornberg, N. Sen, M.R. Hara, K.R. Juluri, J.V. Nguyen, A.M. Snowman, L. Law, L.D. Hester, and S.H. Snyder GAPDH mediates nitrosylation of nuclear proteins Nat. Cell Biol. 12 2010 1094 1100
53. M. Xian, X. Chen, Z. Liu, K. Wang, and P.G. Wang Inhibition of papain by S-nitrosothiols Formation of mixed disulfides J. Biol. Chem. 275 2000 20467 20473
54. S. Fourquet, R. Guerois, D. Biard, and M.B. Toledano Activation of NRF2 by nitrosative agents and H2O2 involves KEAP1 disulfide formation J. Biol. Chem. 285 2010 8463 8471
55. R. Engelman, P. Weisman-Shomer, T. Ziv, J. Xu, E.S. Arner, and M. Benhar Multilevel regulation of 2-Cys peroxiredoxin reaction cycle by S-nitrosylation J. Biol. Chem. 288 2013 11312 11324
56. D. Nikitovic, and A. Holmgren S-nitrosoglutathione is cleaved by the thioredoxin system with liberation of glutathione and redox regulating nitric oxide J. Biol. Chem. 271 1996 19180 19185
57. L. Liu, A. Hausladen, M. Zeng, L. Que, J. Heitman, and J.S. Stamler A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans Nature 410 2001 490 494
58. L. Liu, Y. Yan, M. Zeng, J. Zhang, M.A. Hanes, G. Ahearn, T.J. McMahon, T. Dickfeld, H.E. Marshall, L.G. Que, and J.S. Stamler Essential roles of S-nitrosothiols in vascular homeostasis and endotoxic shock Cell 116 2004 617 628
59. Z. Yang, Z.E. Wang, P.T. Doulias, W. Wei, H. Ischiropoulos, R.M. Locksley, and L. Liu Lymphocyte development requires S-nitrosoglutathione reductase J. Immunol. 185 2010 6664 6669
60. R.L. Bateman, D. Rauh, B. Tavshanjian, and K.M. Shokat Human carbonyl reductase 1 is an S-nitrosoglutathione reductase J. Biol. Chem. 283 2008 35756 35762
61. M. Benhar, M.T. Forrester, D.T. Hess, and J.S. Stamler Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins Science 320 2008 1050 1054
62. D.A. Stoyanovsky, Y.Y. Tyurina, V.A. Tyurin, D. Anand, D.N. Mandavia, D. Gius, J. Ivanova, B. Pitt, T.R. Billiar, and V.E. Kagan Thioredoxin and lipoic acid catalyze the denitrosation of low molecular weight and protein S-nitrosothiols J. Am. Chem. Soc. 127 2005 15815 15823
63. M. Benhar, J.W. Thompson, M.A. Moseley, and J.S. Stamler Identification of S-nitrosylated targets of thioredoxin using a quantitative proteomic approach Biochemistry 49 2010 6963 6969
64. P.T. Doulias, J.L. Greene, T.M. Greco, M. Tenopoulou, S.H. Seeholzer, R.L. Dunbrack, and H. Ischiropoulos 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 2010 16958 16963
65. S. Ben-Lulu, T. Ziv, A. Admon, P. Weisman-Shomer, and M. Benhar A substrate trapping approach identifies proteins regulated by reversible S-nitrosylation Mol. Cell. Proteomics 13 2014 2573 2583
66. R. Chakravarti, and D.J. Stuehr Thioredoxin-1 regulates cellular heme insertion by controlling S-nitrosation of glyceraldehyde-3-phosphate dehydrogenase J. Biol. Chem. 287 2012 16179 16186
67. M. Zaffagnini, S. Morisse, M. Bedhomme, C.H. Marchand, M. Festa, N. Rouhier, S.D. Lemaire, and P. Trost Mechanisms of nitrosylation and denitrosylation of cytoplasmic glyceraldehyde-3-phosphate dehydrogenase from Arabidopsis thaliana J. Biol. Chem. 288 2013 22777 22789
68. D.A. Stoyanovsky, M.J. Scott, and T.R. Billiar Glutathione and thioredoxin type 1 cooperatively denitrosate HepG2 cells-derived cytosolic S-nitrosoproteins Org. Biomol. Chem. 11 2013 4433 4437
69. Y.M. Go, J.R. Roede, D.I. Walker, D.M. Duong, N.T. Seyfried, M. Orr, Y. Liang, K.D. Pennell, and D.P. Jones Selective targeting of the cysteine proteome by thioredoxin and glutathione redox systems Mol. Cell. Proteomics 12 2013 3285 3296
70. W. Zheng, Y. Liu, S. Pan, W. Yuan, Y. Dai, and J. Wei Involvements of S-nitrosylation and denitrosylation in the production of polyphenols by Inonotus obliquus Appl. Microbiol. Biotechnol. 90 2011 1763 1772
71. K. Matsushita, C.N. Morrell, B. Cambien, S.X. Yang, M. Yamakuchi, C. Bao, M.R. Hara, R.A. Quick, W. Cao, B. O'Rourke, J.M. Lowenstein, J. Pevsner, D.D. Wagner, and C.J. Lowenstein Nitric oxide regulates exocytosis by S-nitrosylation of N-ethylmaleimide-sensitive factor Cell 115 2003 139 150
72. T. Ito, M. Yamakuchi, and C.J. Lowenstein Thioredoxin increases exocytosis by denitrosylating N-ethylmaleimide-sensitive factor J. Biol. Chem. 286 2011 11179 11184
73. H.E. Marshall, D.T. Hess, and J.S. Stamler S-nitrosylation: physiological regulation of NF-kappaB Proc. Natl. Acad. Sci. U. S. A. 101 2004 8841 8842
74. Z.T. Kelleher, Y. Sha, M.W. Foster, W.M. Foster, M.T. Forrester, and H.E. Marshall Thioredoxin-mediated denitrosylation regulates cytokine-induced nuclear factor kappaB (NF-kappaB) activation J. Biol. Chem. 289 2014 3066 3072
75. Y. Tada, S.H. Spoel, K. Pajerowska-Mukhtar, Z. Mou, J. Song, C. Wang, J. Zuo, and X. Dong Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins Science 321 2008 952 956
76. I. Pader, R. Sengupta, M. Cebula, J. Xu, J.O. Lundberg, A. Holmgren, K. Johansson, and E.S. Arner Thioredoxin-related protein of 14 kDa is an efficient L-cystine reductase and S-denitrosylase Proc. Natl. Acad. Sci. U. S. A. 111 2014 6964 6969
77. W. Jeong, H.W. Yoon, S.R. Lee, and S.G. Rhee Identification and characterization of TRP14, a thioredoxin-related protein of 14 kDa New insights into the specificity of thioredoxin function J. Biol. Chem. 279 2004 3142 3150
78. S. Kneeshaw, S. Gelineau, Y. Tada, G.J. Loake, and S.H. Spoel Selective protein denitrosylation activity of thioredoxin-h5 modulates plant immunity Mol. Cell 56 2014 153 162
79. M.R. Talipov, and Q.K. Timerghazin Protein control of S-nitrosothiol reactivity: interplay of antagonistic resonance structures J. Phys. Chem. B 117 2013 1827 1837
80. J.M. Fukuto, C.J. Cisneros, and R.L. Kinkade A comparison of the chemistry associated with the biological signaling and actions of nitroxyl (HNO) and nitric oxide (NO) J. Inorg. Biochem. 118 2013 201 208
81. M.W. Foster, D.T. Hess, and J.S. Stamler Protein S-nitrosylation in health and disease: a current perspective Trends Mol. Med. 15 2009 391 404
82. T. Nakamura, S. Tu, M.W. Akhtar, C.R. Sunico, S. Okamoto, and S.A. Lipton Aberrant protein s-nitrosylation in neurodegenerative diseases Neuron 78 2013 596 614
83. N. Shahani, and A. Sawa Nitric oxide signaling and nitrosative stress in neurons: role for S-nitrosylation Antioxid. Redox Signal. 14 2011 1493 1504
84. B. Lima, M.T. Forrester, D.T. Hess, and J.S. Stamler S-nitrosylation in cardiovascular signaling Circ. Res. 106 2010 633 646
85. H. Ovadia, Y. Haim, O. Nov, O. Almog, J. Kovsan, N. Bashan, M. Benhar, and A. Rudich Increased adipocyte S-nitrosylation targets anti-lipolytic action of insulin: relevance to adipose tissue dysfunction in obesity J. Biol. Chem. 286 2011 30433 30443
86. L. Yang, E.S. Calay, J. Fan, A. Arduini, R.C. Kunz, S.P. Gygi, A. Yalcin, S. Fu, and G.S. Hotamisligil Metabolism s-nitrosylation links obesity-associated inflammation to endoplasmic reticulum dysfunction Science 349 2015 500 506
87. P.J. Ferret, E. Soum, O. Negre, E.E. Wollman, and D. Fradelizi Protective effect of thioredoxin upon NO-mediated cell injury in THP1 monocytic human cells Biochem. J. 346 Pt 3 2000 759 765
88. R.J. Arai, F.T. Ogata, W.L. Batista, H. Masutani, J. Yodoi, V. Debbas, O. Augusto, A. Stern, and H.P. Monteiro Thioredoxin-1 promotes survival in cells exposed to S-nitrosoglutathione: correlation with reduction of intracellular levels of nitrosothiols and up-regulation of the ERK1/2 MAP kinases Toxicol. Appl. Pharmacol. 233 2008 227 237
89. M.T. Forrester, D. Seth, A. Hausladen, C.E. Eyler, M.W. Foster, A. Matsumoto, M. Benhar, H.E. Marshall, and J.S. Stamler Thioredoxin-interacting protein (txnip) is a feedback regulator of S-nitrosylation J. Biol. Chem. 284 2009 36160 36166
90. K. Edes, P. Cassidy, P.J. Shami, and P.J. Moos JS-K, a nitric oxide prodrug, has enhanced cytotoxicity in colon cancer cells with knockdown of thioredoxin reductase 1 PLoS One 5 2010 e8786
91. A. Canas, L.M. Lopez-Sanchez, A. Valverde-Estepa, V. Hernandez, E. Fuentes, J.R. Munoz-Castaneda, C. Lopez-Pedrera, J.R. De La Haba-Rodriguez, E. Aranda, and A. Rodriguez-Ariza Maintenance of S-nitrosothiol homeostasis plays an important role in growth suppression of estrogen receptor-positive breast tumors Breast Cancer Res. 14 2012 R153
92. S.L. Comtois, M.D. Gidley, and D.J. Kelly Role of the thioredoxin system and the thiol-peroxidases Tpx and Bcp in mediating resistance to oxidative and nitrosative stress in Helicobacter pylori Microbiology 149 2003 121 129
93. T.A. Missall, and J.K. Lodge Function of the thioredoxin proteins in Cryptococcus neoformans during stress or virulence and regulation by putative transcriptional modulators Mol. Microbiol. 57 2005 847 858
94. A.J. Potter, S.P. Kidd, J.L. Edwards, M.L. Falsetta, M.A. Apicella, M.P. Jennings, and A.G. McEwan Thioredoxin reductase is essential for protection of Neisseria gonorrhoeae against killing by nitric oxide and for bacterial growth during interaction with cervical epithelial cells J. Infect. Dis. 199 2009 227 235
95. S. Zhou, T. Narukami, S. Masuo, M. Shimizu, T. Fujita, Y. Doi, Y. Kamimura, and N. Takaya NO-inducible nitrosothionein mediates NO removal in tandem with thioredoxin Nat. Chem. Biol. 9 2013 657 663
96. S.G. Rhee, H.Z. Chae, and K. Kim Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling Free Radic. Biol. Med. 38 2005 1543 1552
97. J.M. Patel, J. Zhang, and E.R. Block Nitric oxide-induced inhibition of lung endothelial cell nitric oxide synthase via interaction with allosteric thiols: role of thioredoxin in regulation of catalytic activity Am. J. Respir. Cell Mol. Biol. 15 1996 410 419
98. J. Zhang, Y.D. Li, J.M. Patel, and E.R. Block Thioredoxin overexpression prevents NO-induced reduction of NO synthase activity in lung endothelial cells Am. J. Physiol. 275 1998 L288 L293
99. K. Ravi, L.A. Brennan, S. Levic, P.A. Ross, and S.M. Black S-nitrosylation of endothelial nitric oxide synthase is associated with monomerization and decreased enzyme activity Proc. Natl. Acad. Sci. U. S. A. 101 2004 2619 2624
100. M. Tummala, V. Ryzhov, K. Ravi, and S.M. Black Identification of the cysteine nitrosylation sites in human endothelial nitric oxide synthase DNA Cell Biol. 27 2008 25 33
101. P.A. Erwin, A.J. Lin, D.E. Golan, and T. Michel Receptor-regulated dynamic S-nitrosylation of endothelial nitric-oxide synthase in vascular endothelial cells J. Biol. Chem. 280 2005 19888 19894
102. P.A. Erwin, D.A. Mitchell, J. Sartoretto, M.A. Marletta, and T. Michel Subcellular targeting and differential S-nitrosylation of endothelial nitric-oxide synthase J. Biol. Chem. 281 2006 151 157
103. D. Volonte, and F. Galbiati Inhibition of thioredoxin reductase 1 by caveolin 1 promotes stress-induced premature senescence EMBO Rep. 10 2009 1334 1340
104. D.M. Dudzinski, J. Igarashi, D. Greif, and T. Michel The regulation and pharmacology of endothelial nitric oxide synthase Annu. Rev. Pharmacol. Toxicol. 46 2006 235 276
105. Z.W. Qu, W.Y. Miao, S.Q. Hu, C. Li, X.L. Zhuo, Y.Y. Zong, Y.P. Wu, and G.Y. Zhang N-methyl-D-aspartate receptor-dependent denitrosylation of neuronal nitric oxide synthase increase the enzyme activity PLoS One 7 2012 e52788
106. Y. Morishima, M. Lau, H.M. Peng, Y. Miyata, J.E. Gestwicki, W.B. Pratt, and Y. Osawa Heme-dependent activation of neuronal nitric oxide synthase by cytosol is due to an Hsp70-dependent, thioredoxin-mediated thiol-disulfide interchange in the heme/substrate binding cleft Biochemistry 50 2011 7146 7156
107. C. Wu, A.M. Parrott, C. Fu, T. Liu, S.M. Marino, V.N. Gladyshev, M.R. Jain, A.T. Baykal, Q. Li, S. Oka, J. Sadoshima, A. Beuve, W.J. Simmons, and H. Li Thioredoxin 1-mediated post-translational modifications: reduction, transnitrosylation, denitrosylation, and related proteomics methodologies Antioxid. Redox Signal. 15 2011 2565 2604
108. R. Sengupta, and A. Holmgren Thioredoxin and thioredoxin reductase in relation to reversible S-nitrosylation Antioxid. Redox Signal. 18 2013 259 269
109. J. Haendeler, J. Hoffmann, V. Tischler, B.C. Berk, A.M. Zeiher, and S. Dimmeler Redox regulatory and anti-apoptotic functions of thioredoxin depend on S-nitrosylation at cysteine 69 Nat. Cell Biol. 4 2002 743 749
110. A. Weichsel, J.L. Brailey, and W.R. Montfort Buried S-nitrosocysteine revealed in crystal structures of human thioredoxin Biochemistry 46 2007 1219 1227
111. A. Weichsel, M. Kem, and W.R. Montfort Crystal structure of human thioredoxin revealing an unraveled helix and exposed S-nitrosation site Protein Sci. 19 2010 1801 1806
112. S.I. Hashemy, and A. Holmgren Regulation of the catalytic activity and structure of human thioredoxin 1 via oxidation and S-nitrosylation of cysteine residues J. Biol. Chem. 283 2008 21890 21898
113. K.T. Barglow, C.G. Knutson, J.S. Wishnok, S.R. Tannenbaum, and M.A. Marletta Site-specific and redox-controlled S-nitrosation of thioredoxin Proc. Natl. Acad. Sci. U. S. A. 108 2011 E600 E606
114. R.J. Arai, H. Masutani, J. Yodoi, V. Debbas, F.R. Laurindo, A. Stern, and H.P. Monteiro Nitric oxide induces thioredoxin-1 nuclear translocation: possible association with the p21Ras survival pathway Biochem. Biophys. Res. Commun. 348 2006 1254 1260
115. P. Schroeder, R. Popp, B. Wiegand, J. Altschmied, and J. Haendeler Nuclear redox-signaling is essential for apoptosis inhibition in endothelial cells-important role for nuclear thioredoxin-1 Arterioscler. Thromb. Vasc. Biol. 27 2007 2325 2331
116. D.A. Mitchell, and M.A. Marletta Thioredoxin catalyzes the S-nitrosation of the caspase-3 active site cysteine Nat. Chem. Biol. 1 2005 154 158
117. D.A. Mitchell, S.U. Morton, N.B. Fernhoff, and M.A. Marletta 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 2007 11609 11614
118. N. Sun, J.R. Hao, X.Y. Li, X.H. Yin, Y.Y. Zong, G.Y. Zhang, and C. Gao GluR6-FasL-Trx2 mediates denitrosylation and activation of procaspase-3 in cerebral ischemia/reperfusion in rats Cell Death Dis. 4 2013 e771
119. H. Tian, D.F. Zhang, B.F. Zhang, H.Z. Li, Q. Zhang, L.T. Li, D.S. Pei, and J.N. Zheng Melanoma differentiation associated gene-7/interleukin-24 induces caspase-3 denitrosylation to facilitate the activation of cancer cell apoptosis J. Interf. Cytokine Res. 35 2015 157 167
120. C. Wu, T. Liu, W. Chen, S. Oka, C. Fu, M.R. Jain, A.M. Parrott, A.T. Baykal, J. Sadoshima, and H. Li Redox regulatory mechanism of transnitrosylation by thioredoxin Mol. Cell. Proteomics 9 2010 2262 2275
121. L. Wang, C. Delahunty, J.H. Prieto, S. Rahlfs, E. Jortzik, J.R. Yates 3rd, and K. Becker Protein S-nitrosylation in plasmodium falciparum Antioxid. Redox Signal. 20 2014 2923 2935
122. Y. Liu, Y. Ma, R. Wang, C. Xia, R. Zhang, K. Lian, R. Luan, L. Sun, L. Yang, W.B. Lau, H. Wang, and L. Tao Advanced glycation end products accelerate ischemia/reperfusion injury through receptor of advanced end product/nitrative thioredoxin inactivation in cardiac microvascular endothelial cells Antioxid. Redox Signal. 15 2011 1769 1778
123. K. Wang, J. Zhang, X. Wang, X. Liu, L. Zuo, K. Bai, J. Shang, L. Ma, T. Liu, L. Wang, W. Wang, X. Ma, and H. Liu Thioredoxin reductase was nitrated in the aging heart after myocardial ischemia/reperfusion Rejuvenation Res. 16 2013 377 385
124. Y.S. Park, N. Fujiwara, Y.H. Koh, Y. Miyamoto, K. Suzuki, K. Honke, and N. Taniguchi Induction of thioredoxin reductase gene expression by peroxynitrite in human umbilical vein endothelial cells Biol. Chem. 383 2002 683 691
125. R. Gonzalez, M.J. Lopez-Grueso, J. Muntane, J.A. Barcena, and C.A. Padilla Redox regulation of metabolic and signaling pathways by thioredoxin and glutaredoxin in NOS-3 overexpressing hepatoblastoma cells Redox Biol. 6 2015 122 134
126. N. Correa-Aragunde, F.J. Cejudo, and L. Lamattina Nitric oxide is required for the auxin-induced activation of NADPH-dependent thioredoxin reductase and protein denitrosylation during root growth responses in arabidopsis Ann. Bot. 2015
127. F.T. Ogata, W.L. Batista, A. Sartori, T.F. Gesteira, H. Masutani, R.J. Arai, J. Yodoi, A. Stern, and H.P. Monteiro Nitrosative/oxidative stress conditions regulate thioredoxin-interacting protein (TXNIP) expression and thioredoxin-1 (TRX-1) nuclear localization PLoS One 8 2013 e84588
128. Y.J. Park, S.J. Yoon, H.W. Suh, D.O. Kim, J.R. Park, H. Jung, T.D. Kim, S.R. Yoon, J.K. Min, H.J. Na, S.J. Lee, H.G. Lee, Y.H. Lee, H.B. Lee, and I. Choi TXNIP deficiency exacerbates endotoxic shock via the induction of excessive nitric oxide synthesis PLoS Pathog. 9 2013 e1003646
129. G. Kronenfeld, R. Engelman, P. Weisman-Shomer, D. Atlas, and M. Benhar Thioredoxin-mimetic peptides as catalysts of S-denitrosylation and anti-nitrosative stress agents Free Radic. Biol. Med. 79 2015 138 146
130. S. Huerta, S. Chilka, and B. Bonavida Nitric oxide donors: novel cancer therapeutics (review) Int. J. Oncol. 33 2008 909 927
131. E.S. Arner, and A. Holmgren The thioredoxin system in cancer Semin. Cancer Biol. 16 2006 420 426
132. S.R. Thom, V.M. Bhopale, T.N. Milovanova, M. Yang, and M. Bogush Thioredoxin reductase linked to cytoskeleton by focal adhesion kinase reverses actin S-nitrosylation and restores neutrophil beta (2) integrin function J. Biol. Chem. 287 2012 30346 30357
133. R. Chakravarti, K. Gupta, A. Majors, L. Ruple, M. Aronica, and D.J. Stuehr Novel insights in mammalian catalase heme maturation: effect of NO and thioredoxin-1 Free Radic. Biol. Med. 2015