Protein S-nitrosylation: Purview and parameters

Nature Reviews Molecular Cell Biology

Volumn 6, Issue 2, 2005, Pages 150-166

  Hess, Douglas T ^a   Matsumoto, Akio ^a   Kim, Sung Oog ^a   Marshall, Harvey E ^a   Stamler, Jonathan S ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ARGININE; CASPASE; CYCLIC NUCLEOTIDE; GUANOSINE TRIPHOSPHATASE; HYPOXIA INDUCIBLE FACTOR 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; ION CHANNEL; IRON REGULATORY PROTEIN 1; IRON REGULATORY PROTEIN 2; MEMBRANE RECEPTOR; METALLOPROTEIN; METALLOPROTEINASE; MONOMER; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; OXIDOREDUCTASE; PHOSPHATASE; PROTEASOME; PROTEIN TYROSINE KINASE; RYANODINE RECEPTOR; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR; ZINC FINGER PROTEIN;

ALLOSTERISM; CELL COMPARTMENTALIZATION; CELL METABOLISM; ENZYME ACTIVITY; HOMEOSTASIS; HYDROPHOBICITY; MAMMAL CELL; NITROSYLATION; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; UBIQUITINATION;

AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; CYSTEINE; GTP PHOSPHOHYDROLASES; HUMANS; MODELS, BIOLOGICAL; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NITRIC OXIDE; NITROGEN; OXIDATION-REDUCTION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEINS; SIGNAL TRANSDUCTION; SULFHYDRYL COMPOUNDS;

MAMMALIA;

EID: 13444282230     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrm1569     Document Type: Review

References (154)

1. Murad, F. Cyclic guanosine monophosphate as a mediator of vasodilation. J. Clin. Invest. 78, 1-5 (1986).
2. Bredt, D. S. Endogenous nitric oxide synthesis: biological functions and pathophysiology. Free Radic. Res. 31, 577-596 (1999).
3. Stamler, J. S. et al. S-nitrosylation of proteins with nitric oxide: synthesis and characterization of biologically active compounds. Proc. Natl Acad. Sci. USA 89, 444-448 (1992). The first demonstration of protein S-nitrosylation, which showed that proteins in several classes could be modified at active-site or allosteric Cys residues by endogenous and exogenous NO.
4. Stamler, J. S. et al. S-nitrosylation of tissue-type plasminogen activator confers vasodilatory and antiplatelet properties on the enzyme. Proc. Natl Acad. Sci. USA 89, 8087-8091 (1992).
5. Stamler, J. S. et al. in Biology of Nitric Oxide (eds, Moncada, S., Marletta, M. A. & Hibbs, J. B. J.) 20-23 (Portland Press, London, UK, 1992).
6. Stamler, J. S., Lamas, S. & Fang, F. C. Nitrosylation: the prototypic redox-based signaling mechanism. Cell 106, 675-683 (2001).
7. Jaffrey, S. R., Erdjument-Bromage, H., Ferris, C. D., Tempst, P. & Snyder, S. H. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nature Cell Biol. 3, 193-197 (2001). Introduced a method to selectively biotinylate sites of S-nitrosylation within proteins, and applied this method to reveal several endogenous substrates in neural tissue of nNOS-dependent S-nitrosylation.
8. Liu, L. et al. Essential roles of S-nitrosothiols in vascular homeostasis and endotoxic shock. Cell 116, 617-628 (2004). Found that mice with a targeted gene deletion of GSNO reductase have large increases in tissue damage and mortality following endotoxic challenge, which indicated an important role for S-nitrosothiol metabolism in innate immunity, as well as effects on basal SNO levels and vascular tone.
9. de Jesus-Berrios, M. et al. Enzymes that counteract nitrosative stress promote fungal virulence. Curr. Biol. 13, 1963-1968 (2003).
10. Fosfer, M. W., McMahon, T. J. & Stamler, J. S. S-nitrosylation in health and disease. Trends Mol. Med. 9, 160-168 (2003).
11. Lane, P., Hao, G. & Gross, S. S. S-nitrosylation is emerging as a specific and fundamental posttranslational protein modification: head-to-head comparison with O-phosphorylation. Sci. STKE, RE1 (2001).
12. Boehning, D. & Snyder, S. H. Novel neural modulators. Annu. Rev. Neurosci. 26, 105-131 (2003).
13. Barouch, L. A. et al. Nitric oxide regulates the heart by spatial confinement of nitric oxide synthase isoforms. Nature 416, 337-339 (2002).
14. Gow, A. J. et al. Basal and stimulated protein S-nitrosylation in multiple cell types and tissues. J. Biol. Chem. 277, 9637-9640 (2002).
15. Stamler, J. S. & Toone, E. J. The decomposition of thionitriles. Curr. Opin. Chem. Biol. 6, 779-785 (2002).
16. Bartberger, M. D. et al. S-N dissociation energies of S-nitrosothiols: on the origins of nitrosothiol decomposition rates. J. Am. Chem. Soc. 123, 8868-8869 (2001).
17. Stamler, J. S. S-nitrosothiols in the blood: roles, amounts, and methods of analysis. Circ. Res. 94, 414-417 (2004).
18. Ckless, K. et al. In situ detection and visualization of S-nitrosylated proteins following chemical derivatization: identification of Ran GTPase as a target for S-nitrosylation. Nitric Oxide 11, 216-217 (2004).
19. Mannick, J. B. et al. Fas-induced caspase denitrosylation. Science 284, 651-654 (1999). Provided the first demonstration of stimulus-coupled protein de-nitrosylation, which was triggered by activation of a membrane receptor that subserves apoptotic stimulation.
20. Hoffmann, J., Haendeler, J., Zeiher, A. M. & Dimmeler, S. TNFα and oxLDL reduce protein S-nitrosylation in endothelial cells. J. Biol. Chem. 276, 41383-41387 (2001).
21. + 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).
22. Gow, A. J., Luchsinger, B. P., Pawloski, J. R., Singel, D. J. & Stamler, J. S. The oxyhemoglobin reaction of nitric oxide. Proc. Natl Acad. Sci. USA 96, 9027-9032 (1999).
23. Romeo, A. A., Capobianco, J. A. & English, A. M. Superoxide dismutase targets NO from GSNO to Cysβ93 of oxyhemoglobin in concentrated but not dilute solutions of the protein. J. Am. Chem. Soc. 125, 14370-14378 (2003).
24. Mani, K., Cheng, F., Havsmark, B., David, S. & Fransson, L. A. 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 (2004).
25. Inoue, K. et al. Nitrosothiol formation catalyzed by ceruloplasmin. Implication for cytoprotective mechanism in vivo. J. Biol. Chem. 274, 27069-27075 (1999).
26. Stubauer, G., Giuffre, A. & Sarti, P. Mechanism of S-nitrosothiol formation and degradation mediated by copper ions. J. Biol. Chem. 274, 28128-28133 (1999).
27. Tao, L. & English, A. M. Mechanism of S-nitrosation of recombinant human brain calbindin D28K. Biochemistry 42, 3326-3334 (2003).
28. Romeo, A. A., Capobianco, J. A. & English, A. M. Heme nitrosylation of deoxyhemoglobin by S-nitrosoglutathione requires copper. J. Biol. Chem. 277, 24135-24141 (2002).
29. Luchsinger, B. P. et al. Routes to S-nitroso-hemoglobin formation with heme redox and preferential reactivity in the β subunits. Proc. Natl Acad. Sci. USA 100, 461-466 (2003).
30. Foster, M. W. & Stamler, J. S. New insights into protein S-nitrosylation: mitochondria as a model system. J. Biol. Chem. 279, 25891-25897 (2004).
31. Mulsch, A., Mordvintcev, P. I., Vanin, A. F. & Busse, R. Formation and release of dinitrosyl iron complexes by endothelial cells. Biochem. Biophys. Res. Commun. 196, 1303-1308 (1993).
32. Vanin, A. F., Mordvintcev, P. I., Hauschildt, S. & Mulsch, A. The relationship between L-arginine-dependent nitric oxide synthesis, nitrite release and dinitrosyl-iron complex formation by activated macrophages. Biochim. Biophys. Acta 1177, 37-42 (1993).
33. Pawloski, J. R., Hess, D. T. & Stamler, J. S. Export by red blood cells of nitric oxide bioactivity. Nature 409, 622-626 (2001).
34. Patel, J. M., Zhang, J. & Block, E. R. 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, 410-419 (1996).
35. 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. USA 101, 2619-2624 (2004).
36. Kahlos, K., Zhang, J., Block, E. R. & Patel, J. M. Thioredoxin restores nitric oxide-induced inhibition of protein kinase C activity in lung endothelial cells. Mol. Cell. Biochem. 254, 47-54 (2003).
37. Nikitovic, D. & 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).
38. Gaston, B. et al. Endogenous nitrogen oxides and bronchodilator S-nitrosothiols in human airways. Proc. Natl Acad. Sci. USA 90, 10957-10961 (1993).
39. Liu, L. et al. A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410, 490-494 (2001).
40. 2 in S-nitrosylation of the channel. J. Biol. Chem. 278, 8184-8189 (2003).
41. Hess, D. T., Matsumoto, A., Nudelman, R. & Stamler, J. S. S-nitrosylation: spectrum and specificity. Nature Cell Biol. 3, E46-E49 (2001).
42. Campbell, D. L., Stamler, J. S. & Strauss, H. C. Redox modulation of L-type calcium channels in ferret ventricular myocytes. Dual mechanism regulation by nitric oxide and S-nitrosothiols. J. Gen. Physiol. 108, 277-293 (1996).
43. Matsumoto, A., Comatas, K. E., Liu, L. & Stamler, J. S. Screening for nitric oxide-dependent protein-protein interactions. Science 301, 657-661 (2003). Used yeast two-hybrid screening to show S-nitrosylation-facilitated protein-protein interactions, including interactions of NOS with substrates for S-nitrosylation, which were verified in mammalian cells.
44. Matsushita, K. et al. Nitric oxide regulates exocytosis by S-nitrosylation of N-ethylmaleimide-sensitive factor. Cell 115, 139-150 (2003). Showed that the activity of NSF, an essential component of most or all membrane trafficking, is regulated in situ by endogenous S-nitrosylation.
45. Stamler, J. S. et al. Blood flow regulation by S-nitrosohemoglobin in the physiological oxygen gradient. Science 276, 2034-2037 (1997).
46. 2+-release channel of skeletal muscle (RyR1) was activated in situ by S-nitrosylation of a single regulatory Cys, and that S-nitrosylation was gated by oxygen-dependent alteration in the redox status of a small additional set of Cys residues.
47. Lai, T. S. et al. Calcium regulates S-nitrosylation, denitrosylation, and activity of tissue transglutaminase. Biochemistry 40, 4904-4910 (2001).
48. Jia, L., Bonaventura, C., Bonaventura, J. & Stamler, J. S. S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature 380, 221-226 (1996). Showed that haemoglobin is S-nitrosylated endogenously (rather than eliminating nitric oxide) and thereby functions as a source of vasodilatory activity conveyed by red blood cells (which subserves hypoxic vasodilation).
49. James, P. E., Lang, D., Tufnell-Barret, T., Milsom, A. B. & Frenneaux, M. P. Vasorelaxation by red blood cells and impairment in diabetes. Reduced nitric oxide and oxygen delivery by glycated hemoglobin. Circ. Res. 94, 976-983 (2004).
50. Funai, E. F., Davidson, A., Seligman, S. P. & Finlay, T. H. S-nitrosohemoglobin in the fetal circulation may represent a cycle for blood pressure regulation. Biochem. Biophys. Res. Commun. 239, 875-877 (1997).
51. Singel, D. J. & Stamler, J. S. Chemical physiology of blood flow regulation by red blood cells: role of nitric oxide and S-nitrosohemoglobin. Annu. Rev. Physiol. Oct 19 2004 (doi:10.1146/annurev.physiol.67.060603.090918).
52. Stamler, J. S., Toone, E. J., Lipton, S. A. & Sucher, N. J. (S)NO signals: translocation, regulation, and a consensus motif. Neuron 18, 691-696 (1997).
53. Britto, P. J., Knipling, L. & Wolff, J. The local electrostatic environment determines cysteine reactivity of tubulin. J. Biol. Chem. 277, 29018-29027 (2002).
54. Bizzozero, O. A., Bixler, H. A. & Pastuszyn, A. Structural determinants influencing the reaction of cysteine-containing peptides with palmitoyl-coenzyme A and other thioesters. Biochem. Biophys. Acta 1545, 278-288 (2001).
55. Atkins, W. M., Wang, R. W., Bird, A. W., Newton, D. J. & Lu, A. Y. The catalytic mechanism of glutathione S-transferase (GST). Spectroscopic determination of the pKa of Tyr-9 in rat α1-1 GST. J. Biol. Chem. 268, 19188-19191 (1993).
56. Pérez-Mato, I., Castro, C., Ruiz, F. A., Corrales, F. J. & Mato, J. M. Methionine adenosyltransferase S-nitrosylation is regulated by the basic and acidic amino acids surrounding the target thiol. J. Biol. Chem. 274, 17075-17079 (1999). Showed with site-specific mutation the important role of acidic and basic side chains, proximate to Cys thiol, in targeting S-nitrosylation within protein substrates (transnitrosylation by GSNO).
57. Brenman, J. E. et al. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and α1-syntrophin mediated by PDZ domains. Cell 94, 757-767 (1996).
58. Kornau, H. C., Schenker, L. T., Kennedy, M. B. & Seeburg, P. H. Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269, 1737-1740 (1995).
59. Lipton, S. A. et al. Cysteine regulation of protein function - as exemplified by NMDA-receptor modulation. Trends Neurosci. 25, 474-480 (2002).
60. Fang, M. et al. Dexras1: a G protein specifically coupled to neuronal nitric oxide synthase via CAPON. Neuron 28, 183-193 (2000).
61. Rizzo, M. A. & Piston, D. W. Regulation of β cell glucokinase by S-nitrosylation and association with nitric oxide synthase. J. Cell Biol. 161, 243-248 (2003). Showed that glucokinase is bound to nNOS in pancreatic β-cells, and that physiological activation of nNOS by insulin results in S-nitrosylation of glucokinase, its release from nNOS and activation of kinase activity.
62. Giles, N. M., Giles, G. I. & Jacob, C. Multiple roles of cysteine in biocatalysis. Biochem. Biophys. Res. Commun. 300, 1-4 (2003).
63. Stamler, J. S., Singel, D. J. & Loscalzo, J. Biochemistry of nitric oxide and its redox-activated forms. Science 258, 1898-1902 (1992).
64. Mannick, J. B. et al. S-Nitrosylation of mitochondrial caspases. J. Cell Biol. 154, 1111-1116 (2001).
65. Kim, J. E. & Tannenbaum, S. R. S-nitrosation regulates the activation of endogenous procaspase-9 in HT-29 human colon carcinoma cells. J. Biol. Chem. 279, 9758-9764 (2004).
66. Caselli, A., Chiarugi, P., Camici, G., Manao, G. & Ramponi, G. In vivo inactivation of phosphotyrosine protein phosphatases by nitric oxide. FEBS Lett. 374, 249-252 (1995).
67. Callsen, D., Sandau, K. B. & Brune, B. Nitric oxide and superoxide inhibit platelet-derived growth factor receptor phosphotyrosine phosphatases. Free Radic. Biol. Med. 26, 1544-1553 (1999).
68. Xian, M. et al. Inhibition of protein tyrosine phosphatases by low-molecular-weight S-nitrosothiols and S-nitrosylated human serum albumin. Biochem. Biophys. Res. Commun. 268, 310-314 (2000).
69. Li, S. & Whorton, A. R. Regulation of protein tyrosine phosphatase 1B in intact cells by S-nitrosothiols. Arch. Biochem. Biophys. 410, 269-279 (2003).
70. Mikkelsen, R. B. & Wardman, P. Biological chemistry of reactive oxygen and nitrogen and radiation-induced signal transduction mechanisms. Oncogene 22, 5734-5754 (2003).
71. Leiper, J., Murray-Rust, J., McDonald, N. & Vallance, P. S-nitrosylation of dimethylarginine dimethylaminohydrolase regulates enzyme activity: further interactions between nitric oxide synthase and dimethylarginine dimethylaminohydrolase. Proc. Natl Acad. Sci. USA 99, 13527-13532 (2002).
72. Hao, G., Xie, L. & Gross, S. S. Argininosuccinate synthetase is reversibly inactivated by S-nitrosylation in vitro and in vivo. J. Biol. Chem. 279, 36192-36200 (2004).
73. 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. 276, 34458-34464 (2001).
74. Hillary, R. A. & Pegg, A. E. Decarboxylases involved in polyamine biosynthesis and their inactivation by nitric oxide. Biochim. Biophys. Acta 1647, 161-166 (2003).
75. Haendeler, J. et al. Redox regulatory and anti-apoptotic functions of thioredoxin depend on S-nitrosylation at cysteine 69. Nature Cell Biol. 4, 743-749 (2002).
76. Sumbayev, V. V. S-nitrosylation of thioredoxin mediates activation of apoptosis signal-regulating kinase 1. Arch. Biochem. Biophys. 415, 133-136 (2003).
77. Park, H. S. et al. Inhibition of apoptosis signal-regulating kinase 1 (ASK1) by nitric oxide through a thiol-redox mechanism. J. Biol. Chem. 279, 7584-7590 (2003).
78. Park, H. S., Huh, S. H., Kim, M. S., Lee, S. H. & Choi, E. J. Nitric oxide negatively regulates c-Jun N-terminal kinase/stress-activated protein kinase by means of S-nitrosylation. Proc. Natl Acad. Sci. USA 97, 14382-14387 (2000). Showed in intact cells that endogenously produced NO can suppress activity of a protein kinase, JNK, which could be ascribed to S-nitrosylation of a single regulatory cysteine.
79. Lander, H. M., Ogiste, J. S., Pearce, S. F., Levi, R. & Novogrodsky, A. Nitric oxide-stimulated guanine nucleotide exchange on p21ras. J. Biol. Chem. 270, 7017-7020 (1995).
80. dela Torre, A., Schroeder, R. A., Bartlett, S. T. & Kuo, P. C. Differential effects of nitric oxide-mediated S-nitrosylation on p50 and c-jun DNA binding. Surgery 124, 137-141 (1998).
81. Nikitovic, D., Holmgren, A. & Spyrou, G. Inhibition of AP-1 DNA binding by nitric oxide involving conserved cysteine residues in Jun and Fos. Biochem. Biophys. Res. Commun. 242, 109-112 (1998).
82. Monteiro, H. P., Gruia-Gray, J., Peranovich, T. M., de Oliveira, L. C. & Stern, A. Nitric oxide stimulates tyrosine phosphorylation of focal adhesion kinase, Src kinase, and mitogen-activated protein kinases in murine fibroblasts. Free Radic. Biol. Med. 28, 174-182 (2000).
83. Akhand, A. A. et al. Nitric oxide controls src kinase activity through a sulfhydryl group modification-mediated Tyr-527-independent and Tyr-416-linked mechanism. J. Biol. Chem. 274, 25821-25826 (1999).
84. Yun, H. Y., Gonzalez-Zulueta, M., Dawson, V. L. & Dawson, T. M. Nitric oxide mediates N-methyl-D-aspartate receptor-induced activation of p21ras. Proc. Natl Acad. Sci. USA 95, 5773-6778 (1998).
85. Lin, Y. F., Raab-Graham, K., Jan, Y. N. & Jan, L. Y. NO stimulation of ATP-sensitive potassium channels: involvement of Ras/mitogen-activated protein kinase pathway and contribution to neuroprotection. Proc. Natl Acad. Sci. USA 101, 7799-7804 (2004).
86. Jaffrey, S. R., Fang, M. & Snyder, S. H. Nitrosopeptide mapping: a novel methodology reveals S-nitrosylation of dexras1 on a single cysteine residue. Chem. Biol. 9, 1329-1335 (2002).
87. Estrada, C. et al. Nitric oxide reversibly inhibits the epidermal growth factor receptor tyrosine kinase. Biochem. J. 326, 369-376 (1997).
88. Nozik-Grayck, E. et al. Pulmonary vasoconstriction by serotonin is inhibited by S-nitrosoglutathione. Am. J. Physiol. Lung Cell. Mol. Physiol. 282, L1057-L1065 (2002).
89. Lipton, S. A. et al. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 364, 626-632 (1993).
90. Choi, Y. B. et al. Molecular basis of NMDA receptor-coupled ion channel modulation by S-nitrosylation. Nature Neurosci. 3, 15-21 (2000).
91. Sun, J., Xin, C., Eu, J. P., Stamler, J. S. & Meissner, G. Cysteine-3635 is responsible for skeletal muscle ryanodine receptor modulation by NO. Proc. Natl Acad. Sci. USA 98, 11158-11162 (2001).
92. Eu, J. P. et al. Concerted regulation of skeletal muscle contractility by oxygen tension and endogenous nitric oxide. Proc. Natl Acad. Sci. USA 100, 15229-15234 (2003).
93. 2+ activation of RyR1 channels. J. Biol. Chem. 278, 42927-42935 (2003).
94. Sun, J., Xu, L., Eu, J. P., Stamler, J. S. & Meissner, G. Classes of thiols that influence the activity of the skeletal muscle calcium release channel. J. Biol. Chem. 276, 15625-15630 (2001).
95. 2+ release mechanism. J. Biol. Chem. 272, 7069-7077 (1997).
96. Xu, L., Eu, J. P., Meissner, G. & Stamler, J. S. Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitrosylation. Science 279, 234-237 (1998).
97. Xu, K. Y., Huso, D. L., Dawson, T. M., Bredt, D. S. & Becker, L. C. Nitric oxide synthase in cardiac sarcoplasmic reticulum. Proc. Natl Acad. Sci. USA 96, 657-662 (1999).
98. Broillet, M. C. & Firestein, S. Direct activation of the olfactory cyclic nucleotide-gated channel through modification of sulfhydryl groups by NO compounds. Neuron 16, 377-385 (1996).
99. Broillet, M. C. A single intracellular cysteine residue is responsible for the activation of the olfactory cyclic nucleotide-gated channel by NO. J. Biol. Chem. 275, 15135-15141 (2000).
100. Gao, C. et al. S-nitrosylation of heterogeneous nuclear ribonucleoprotein A/B regulates osteopontin transcription in endotoxin-stimulated murine macrophages. J. Biol. Chem. 279, 11236-11243 (2004).
101. Melillo, G. et al. A hypoxia-responsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter. J. Exp. Med. 182, 1683-1693 (1995).
102. Palmer, L. A., Semenza, G. L., Stoler, M. H. & Johns, R. A. Hypoxia induces type II NOS gene expression in pulmonary artery endothelial cells via HIF-1. Am. J. Physiol. 274, L212-L219 (1998).
103. Ambs, S., Hussain, S. P. & Harris, C. C. Interactive effects of nitric oxide and the p53 tumor suppressor gene in carcinogenesis and tumor progression. FASEB J. 11, 443-448 (1997).
104. Davis, M. E., Grumbach, I. M., Fukai, T., Cutchins, A. & Harrison, D. G. Shear stress regulates endothelial nitric-oxide synthase promoter activity through nuclear factor κB binding. J. Biol. Chem. 279, 163-168 (2004).
105. Lowenstein, C. J. et al. Macrophage nitric oxide synthase gene: two upstream regions mediate induction by interferon γ and lipopolysaccharide. Proc. Natl Acad. Sci. USA 90, 9730-9734 (1993).
106. Xie, Q. W., Kashiwabara, Y. & Nathan, C. Role of transcription factor NF-κB/Rel in induction of nitric oxide synthase. J. Biol. Chem. 269, 4705-4708 (1994).
107. Hausladen, A., Privalle, C. T., Keng, T., DeAngelo, J. & Stamler, J. S. Nitrosative stress: activation of the transcription factor OxyR. Cell 86, 719-729 (1996).
108. Kullik, I., Toledano, M. B., Tartaglia, L. A. & Storz, G. Mutational analysis of the redox-sensitive transcriptional regulator OxyR: regions important for oxidation and transcriptional activation. J. Bacteriol. 177, 1275-1284 (1995)
109. Kim, S. O. et al. OxyR: a molecular code for redox-related signaling. Cell 109, 383-396 (2002). Showed that a single regulatory Cys within the bacterial transcription factor OxyR is subject not only to S-nitrosylation but also to additional NO-dependent and NO-independent oxidative modifications, with differential effects on DNA binding and transcriptional response.
110. Pugh, C. W. & Ratcliffe, P. J. Regulation of angiogenesis by hypoxia: role of the HIF system. Nature Med. 9, 677-684 (2003).
111. Sumbayev, V. V., Budde, A., Zhou, J. & Brune, B. HIF-1α protein as a target for S-nitrosation. FEBS Lett. 535, 106-112 (2003).
112. Yasinska, I. M. & Sumbayev, V. V. S-nitrosation of Cys-800 of HIF-1α protein activates its interaction with p300 and stimulates its transcriptional activity. FEBS Lett. 549, 105-109 (2003).
113. Palmer, L. A., Gaston, B. & Johns, R. A. Normoxic stabilization of hypoxia-inducible factor-1 expression and activity: redox-dependent effect of nitrogen oxides. Mol. Pharmacol. 58, 1197-1203 (2000). Provided an initial demonstration, with HIF1, that NO could control the activity of transcription factors by regulating their stability (ubiquitylation and proteasomal degradation).
114. Sandau, K. B., Fandrey, J. & Brune, B. Accumulation of HIF-1α under the influence of nitric oxide. Blood 97, 1009-1015 (2001).
115. Metzen, E., Zhou, J., Jelkmann, W., Fandrey, J. & Brune, B. Nitric oxide impairs normoxic degradation of HIF-1α by inhibition of prolyl hydroxylases. Mol. Biol. Cell 14, 3470-3481 (2003).
116. Yao, D. et al. 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 (2004). Showed, together with reference 117, that the activity of the neuronal E3 ubiquitin ligase parkin is regulated by S-nitrosylation in situ as a result of nitrosative stress induced experimentally or occuring endogenously in the brains of Parkinson's disease patients.
117. Chung, K. K. K. et al. S-nitrosylaton of parkin regulates ubiquitination and compromises parkin's protective function. Science 304, 1328-1331 (2004).
118. Michael, D. & Oren, M. The p53-Mdm2 module and the ubiquitin system. Semin. Cancer Biol. 13, 49-58 (2003).
119. Calmels, S., Hainaut, P. & Ohshima, H. Nitric oxide induces conformational and functional modifications of wild-type p53 tumor suppressor protein. Cancer Res. 57, 3365-3369 (1997).
120. Brune, B., von Knethen, A. & Sandau, K. B. Transcription factors p53 and HIF-1α as targets of nitric oxide. Cell. Signal. 13, 525-533 (2001).
121. Schonhoff, C. M., Daou, M. C., Jones, S. N., Schiffer, C. A. & Ross, A. H. Nitric oxide-mediated inhibition of Hdm2-p53 binding. Biochemistry 41, 13570-13574 (2002).
122. Karin, M. & Ben-Neriah, Y. Phosphorylation meets ubiquitination: the control of NFκB activity. Annu. Rev. Immunol. 18, 621-663 (2000).
123. dela Torre, A., Schroeder, R. A., Punzalan, C. & Kuo, P. C. Endotoxin-mediated S-nitrosylation of p50 alters NF-κB-dependent gene transcription in ANA-1 murine macrophages. J. Immunol. 162, 4101-4108 (1999).
124. Park, S. K., Lin, H. L. & Murphy, S. Nitric oxide regulates nitric oxide synthase-2 gene expression by inhibiting NF-κB binding to DNA. Biochem. J. 322, 609-613 (1997).
125. dela Torre, A., Schroeder, R. A. & Kuo, P. C. Alteration of NF-κB p50 DNA binding kinetics by S-nitrosylation. Biochem. Biophys. Res. Commun. 238, 703-706 (1997).
126. Matthews, J. R., Botting, C. H., Panico, M., Morris, H. R. & Hay, R. T. Inhibition of NF-κB DNA binding by nitric oxide. Nucleic Acids Res. 24, 2236-2242 (1996).
127. Marshall, H. E. & Stamler, J. S. Inhibition of NF-κB by S-nitrosylation. Biochemistry 40, 1688-1693 (2001).
128. Peng, H. B., Libby P. & Liao, J. K. Induction and stabilization of IκBα by nitric oxide mediates inhibition of NF-κB. J. Biol. Chem. 270, 14214-14219 (1995).
129. Marshall, H. E. & Stamler, J. S. Nitrosative stress-induced apoptosis through inhibition of NF-κB. J. Biol. Chem. 277, 34223-34228 (2002).
130. Reynaert, N. L. et al. Nitric oxide represses inhibitory κB kinase through S-nitrosylation. Proc. Natl Acad. Sci. USA 101, 8945-8950 (2004).
131. Pantopoulos, K. & Hentze, M. W. Nitric oxide signaling to iron-regulatory protein: direct control of ferritin mRNA translation and transferrin receptor mRNA stability in transfected fibroblasts. Proc. Natl Acad. Sci. USA 92, 1267-1271 (1995).
132. Kim, S. & Ponka, P. Effects of interferon-γ and lipopolysaccharide on macrophage iron metabolism are mediated by nitric oxide-induced degradation of iron regulatory protein 2. J. Biol. Chem. 275, 6220-6226 (2000).
133. Bouton, C., Oliveira, L. & Drapier, J. C. Converse modulation of IRP1 and IRP2 by immunological stimuli in murine RAW 264.7 macrophages. J. Biol. Chem. 273, 9403-9408 (1998).
134. Kim, S., Wing, S. S. & Ponka, P. S-nitrosylation of IRP2 regulates its stability via the ubiquitin-proteasome pathway. Mol. Cell. Biol. 24, 330-337 (2004).
135. LaVaute, T. et al. Targeted deletion of the gene encoding iron regulatory protein-2 causes misregulation of iron metabolism and neurodegenerative disease in mice. Nature Genet. 27, 209-214 (2001).
136. Jaffrey, S. R., Cohen, N. A., Rouault, T. A., Klausner, R. D. & Snyder, S. H. The iron-responsive element binding protein: a target for synaptic actions of nitric oxide. Proc. Natl Acad. Sci. USA 91, 12994-12998 (1994).
137. Dudev, T. & Lim, C. Factors governing the protonation state of cysteines in proteins: an Ab initio/CDM study. J. Am. Chem. Soc. 124, 6759-6766 (2002).
138. Kroncke, K. D., Klotz, L. O., Suschek, C. V. & Sies, H. Comparing nitrosative versus oxidative stress toward zinc finger-dependent transcription. Unique role for NO. J. Biol. Chem. 277, 13294-13301 (2002).
139. Pearce, L. L. et al. Role of metallothionein in nitric oxide signaling as revealed by a green fluorescent fusion protein. Proc. Natl Acad. Sci. USA 97, 477-482 (2000).
140. + channels. Neuron 41, 351-365 (2004).
141. Gu, Z. et al. S-nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science 297, 1186-1190 (2002).
142. Zhang, Z. et al. Activation of tumor necrosis factor-α-converting enzyme-mediated ectodomain shedding by nitric oxide. J. Biol. Chem. 275, 15839-15844 (2000).
143. Datta, B. et al. Red blood cell nitric oxide as an endocrine vasoregulator: a potential role in congestive heart failure. Circulation 109, 1339-1342 (2004).
144. Massy, Z. A. et al. Increased plasma S-nitrosothiol concentrations predict cardiovascular outcomes among patients with end-stage renal disease: a prospective study. J. Am. Soc. Nephrol. 15, 470-476 (2004).
145. Gow, A. J., Buerk, D. G. & Ischiropoulos, H. A novel reaction mechanism for the formation of S-nitrosothiol in vivo. J. Biol. Chem. 272, 2341-2345 (1997).
146. Houk, K. N. et al. Nitroxyl disulfides, novel intermediates in transnitrosation reactions. J. Am. Chem. Soc. 125, 6972-6976 (2003).
147. Bartberger, M. D. et al. Theory, spectroscopy, and crystallographic analysis of S-nitrosothiols: conformational distribution dictates spectroscopic behavior. J. Am. Chem. Soc. 122, 5889-5890 (2000).
148. Chan, N. L., Kavanaugh, J. S., Rogers, P. H. & Arnone, A. Crystallographic analysis of the interaction of nitric oxide with quaternary-T human hemoglobin. Biochemistry 43, 118-132 (2004).
149. 2 within the hydrophobic interior of biological membranes. Proc. Natl Acad. Sci. USA 95, 2175-2179 (1998).
150. Nedospasov, A., Rafikov, R., Beda, N. & Nudler, E. An autocatalytic mechanism of protein nitrosylation. Proc. Natl Acad. Sci. USA 97, 13543-13548 (2000).
151. Jourd'heuil, D., Jourd'heuil, F. L. & Feelisch, M. Oxidation and nitrosation of thiols at low micromolar exposure to nitric oxide. Evidence for a free radical mechanism. J. Biol. Chem. 278, 15720-15726 (2003).
152. Liu, L. et al. Inactivation of annexin II tetramer by S-nitrosoglutathione. Eur. J. Biochem. 269, 4277-4286 (2002).
153. Ji, Y., Toader, V. & Bennett, B. M. Regulation of microsomal and cytosolic glutathione S-transferase activities by S-nitrosylation. Biochem. Pharmacol. 63, 1397-1404 (2002).
154. Ventura, A. & Pelicci, P. G. Semaphorins: green light for redox signaling? Sci. STKE 2002, PE44 (2002).