Mechanism and kinetics of inducible nitric oxide synthase auto- S -nitrosation and inactivation

Biochemistry

Volumn 51, Issue 5, 2012, Pages 1028-1040

  Smith, Brian C ^a   Fernhoff, Nathaniel B ^b   Marletta, Michael A ^a,b  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APPARENT K; CONCENTRATION-DEPENDENT; HEME COFACTOR; INACTIVATION PATHWAY; INDUCIBLE NITRIC OXIDE SYNTHASE; ISOFORMS; KINETIC MODELS; MECHANISM AND KINETICS; NITRIC-OXIDE SYNTHASE; NITROSATION; NITROSOTHIOLS; NO FORMATION; NO RELEASE; NOS ACTIVITY; PARTITION RATIOS; PHYSIOLOGICAL CONCENTRATIONS; PROGRESS CURVES; S-NITROSATION; TIME-SCALES; TRAP CONCENTRATION;

AMINO ACIDS; NITRIC OXIDE; PHYSIOLOGY; PORPHYRINS; ZINC;

CHEMICAL REACTIONS;

ARGININE; NITRIC OXIDE SYNTHASE; S NITROSOTHIOL;

ARTICLE; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME KINETICS; ENZYME MECHANISM; ENZYME METABOLISM; ENZYME RELEASE; ENZYME SYNTHESIS; NITROSATION; PRIORITY JOURNAL;

ANIMALS; ARGININE; BIOTIN; CATALYSIS; DOWN-REGULATION; MICE; MODELS, MOLECULAR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; NITROSATION; S-NITROSOGLUTATHIONE; SUBSTRATE SPECIFICITY;

EID: 84863406254     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201818c     Document Type: Article

References (86)

1. Marletta, M. A., Hurshman, A. R., and Rusche, K. M. (1998) Catalysis by nitric oxide synthase Curr. Opin. Chem. Biol. 2, 656-663 (Pubitemid 128645724)
2. Aktan, F. (2004) iNOS-mediated nitric oxide production and its regulation Life Sci. 75, 639-653 (Pubitemid 38686696)
3. Derbyshire, E. R. and Marletta, M. A. (2009) Biochemistry of soluble guanylate cyclase Handb. Exp. Pharmacol. 17-31
4. Foster, M. W., Hess, D. T., and Stamler, J. S. (2009) Protein S-nitrosylation in health and disease: A current perspective Trends Mol. Med. 15, 391-404
5. Basu, S., Keszler, A., Azarova, N. A., Nwanze, N., Perlegas, A., Shiva, S., Broniowska, K. A., Hogg, N., and Kim-Shapiro, D. B. (2010) A novel role for cytochrome c: Efficient catalysis of S-nitrosothiol formation Free Radical Biol. Med. 48, 255-263
6. Broniowska, K. A., Keszler, A., Basu, S., Kim-Shapiro, D. B., and Hogg, N. (2011) Cytochrome c-mediated formation of S-nitrosothiol in cells Biochem. J. doi: 10.1042/BJ20111294
7. Ravi, K., Brennan, L. A., Levic, S., Ross, P. A., and Black, S. M. (2004) 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 (Pubitemid 38269360)
8. Mitchell, D. A., Erwin, P. A., Michel, T., and Marletta, M. A. (2005) S-Nitrosation and regulation of inducible nitric oxide synthase Biochemistry 44, 4636-4647 (Pubitemid 40396742)
9. Erwin, P. A., Mitchell, D. A., Sartoretto, J., Marletta, M. A., and Michel, T. (2006) Subcellular targeting and differential S-nitrosylation of endothelial nitric-oxide synthase J. Biol. Chem. 281, 151-157 (Pubitemid 43671173)
10. Erwin, P. A., Lin, A. J., Golan, D. E., and Michel, T. (2005) Receptor-regulated dynamic S-nitrosylation of endothelial nitric-oxide synthase in vascular endothelial cells J. Biol. Chem. 280, 19888-19894 (Pubitemid 41379517)
11. Jaffrey, S. R. and Snyder, S. H. (2001) The biotin switch method for the detection of S-nitrosylated proteins Sci. STKE 86, p11-9
12. Kim, S. F., Huri, D. A., and Snyder, S. H. (2005) Inducible nitric oxide synthase binds, S-nitrosylates, and activates cyclooxygenase-2 Science 310, 1966-1970 (Pubitemid 43005992)
13. Matsumoto, A., Comatas, K. E., Liu, L., and Stamler, J. S. (2003) Screening for nitric oxide-dependent protein-protein interactions Science 301, 657-661 (Pubitemid 36927951)
14. Mannick, J. B., Hausladen, A., Liu, L., Hess, D. T., Zeng, M., Miao, Q. X., Kane, L. S., Gow, A. J., and Stamler, J. S. (1999) Fas-induced caspase denitrosylation Science 284, 651-654 (Pubitemid 29289591)
15. Dunn, J., Gutbrod, S., Webb, A., Pak, A., Jandu, S. K., Bhunia, A., Berkowitz, D. E., and Santhanam, L. (2011) S-nitrosation of arginase 1 requires direct interaction with inducible nitric oxide synthase Mol. Cell. Biochem. 355, 83-89
16. Schaller, G. E., Shiu, S.-H., and Armitage, J. P. (2011) Two-component systems and their co-option for eukaryotic signal transduction Curr. Biol. 21, R320-R330
17. Meister, A. and Anderson, M. E. (1983) Glutathione Annu. Rev. Biochem. 52, 711-760 (Pubitemid 13030692)
18. Yap, L.-P., Sancheti, H., Ybanez, M. D., Garcia, J., Cadenas, E., and Han, D. (2010) Determination of GSH, GSSG, and GSNO Using HPLC with Electrochemical Detection Methods Enzymol. 473, 137-147
19. Kluge, I., Gutteck-Amsler, U., Zollinger, M., and Do, K. Q. (1997) S-nitrosoglutathione in rat cerebellum: Identification and quantification by liquid chromatography-mass spectrometry J. Neurochem. 69, 2599-2607 (Pubitemid 27495448)
20. Giustarini, D., Milzani, A., Dalle-Donne, I., and Rossi, R. (2007) Detection of S-nitrosothiols in biological fluids: A comparison among the most widely applied methodologies J. Chromatogr., B: Anal. Technol. Biomed. Life Sci. 851, 124-139 (Pubitemid 46720138)
21. Mitchell, D. A. and Marletta, M. A. (2005) Thioredoxin catalyzes the S-nitrosation of the caspase-3 active site cysteine Nat. Chem. Biol. 1, 154-158
22. Barglow, K. T., Knutson, C. G., Wishnok, J. S., Tannenbaum, S. R., and Marletta, M. A. (2011) Site-specific and redox-controlled S-nitrosation of thioredoxin Proc. Natl. Acad. Sci. U.S.A. 108, E600-E606
23. Rusche, K. M., Spiering, M. M., and Marletta, M. A. (1998) Reactions catalyzed by tetrahydrobiopterin-free nitric oxide synthase Biochemistry 37, 15503-15512 (Pubitemid 28516013)
24. Karow, D. S., Pan, D., Davis, J. H., Behrends, S., Mathies, R. A., and Marletta, M. A. (2005) Characterization of Functional Heme Domains from Soluble Guanylate Cyclase Biochemistry 44, 16266-16274 (Pubitemid 41785825)
25. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72, 248-254
26. Hevel, J. M. and Marletta, M. A. (1994) Nitric-oxide synthase assays Methods Enzymol. 233, 250-258 (Pubitemid 24177548)
27. Antonini, E. and Brunori, M. (1971) Hemoglobin and Myoglobin in Their Reactions with Ligands, North-Holland, Amsterdam.
28. Teale, F. (1959) Cleavage of the haem-protein link by acid methylethylketone Biochim. Biophys. Acta 35, 543-543
29. Paulson, D. R., Addison, A. W., Dolphin, D., and James, B. R. (1979) Preparation of ruthenium(II) and ruthenium(III) myoglobin and the reaction of dioxygen, and carbon monoxide, with ruthenium(II) myoglobin J. Biol. Chem. 254, 7002-7006
30. Rosenfeld, R. J., Bonaventura, J., Szymczyna, B. R., Maccoss, M. J., Arvai, A. S., Yates, J. R., Tainer, J. A., and Getzoff, E. D. (2010) Nitric-oxide Synthase Forms N-NO-pterin and S-NO-Cys: Implications for activity, allostery, and regulation J. Biol. Chem. 285, 31581-31589
31. Buga, G. M., Griscavage, J. M., Rogers, N. E., and Ignarro, L. J. (1993) Negative feedback regulation of endothelial cell function by nitric oxide Circ. Res. 73, 808-812 (Pubitemid 23306125)
32. Rengasamy, A. and Johns, R. A. (1993) Regulation of nitric oxide synthase by nitric oxide Mol. Pharmacol. 44, 124-128 (Pubitemid 23230468)
33. Rogers, N. E. and Ignarro, L. J. (1992) Constitutive nitric oxide synthase from cerebellum is reversibly inhibited by nitric oxide formed from l -arginine Biochem. Biophys. Res. Commun. 189, 242-249 (Pubitemid 23030033)
34. Kotsonis, P., Frey, A., Fröhlich, L. G., Hofmann, H., Reif, A., Wink, D. A., Feelisch, M., and Schmidt, H. H. (1999) Autoinhibition of neuronal nitric oxide synthase: Distinct effects of reactive nitrogen and oxygen species on enzyme activity Biochem. J. 340 (Part 3) 745-752 (Pubitemid 29312873)
35. Hofmann, H. and Schmidt, H. H. (1995) Thiol dependence of nitric oxide synthase Biochemistry 34, 13443-13452
36. Griscavage, J. M., Rogers, N. E., Sherman, M. P., and Ignarro, L. J. (1993) Inducible nitric oxide synthase from a rat alveolar macrophage cell line is inhibited by nitric oxide J. Immunol. 151, 6329-6337 (Pubitemid 23340379)
37. Garrido-del Solo, C., García-Cánovas, F., Havsteen, B. H., and Varón-Castellanos, R. (1993) Kinetic analysis of a Michaelis-Menten mechanism in which the enzyme is unstable Biochem. J. 294 (Part 2) 459-464 (Pubitemid 23268846)
38. Varón, R., García-Cánovas, F., García-Moreno, M., Valero, E., Molina-Alarcón, M., García-Meseguers, M. J., Vidal de Labra, J. A., and Garrido-del Sol, C. (2002) Kinetic analysis of the general modifier mechanism of Botts and Morales involving a suicide substrate J. Theor. Biol. 218, 355-374 (Pubitemid 35203265)
39. Duggleby, R. G. (1986) Progress curves of reactions catalyzed by unstable enzymes. A theoretical approach J. Theor. Biol. 123, 67-80
40. Burke, M. A., Maini, P. K., and Murray, J. D. (1990) On the kinetics of suicide substrates Biophys. Chem. 37, 81-90 (Pubitemid 20287778)
41. Tatsunami, S., Yago, N., and Hosoe, M. (1981) Kinetics of suicide substrates steady-state treatments and computer-aided exact solutions Biochim. Biophys. Acta 662, 226-235
42. Tudela, J., García Cánovas, F., Varón, R., García Carmona, F., Gálvez, J., and Lozano, J. A. (1987) Transient-phase kinetics of enzyme inactivation induced by suicide substrates Biochim. Biophys. Acta 912, 408-416 (Pubitemid 17066100)
43. Waley, S. G. (1991) The kinetics of substrate-induced inactivation Biochem. J. 279 (Part 1) 87-94
44. Eich, R. F., Li, T., Lemon, D. D., Doherty, D. H., Curry, S. R., Aitken, J. F., Mathews, A. J., Johnson, K. A., Smith, R. D., Phillips, G. N., and Olson, J. S. (1996) Mechanism of NO-induced oxidation of myoglobin and hemoglobin Biochemistry 35, 6976-6983 (Pubitemid 26182085)
45. Stuehr, D. J., Kwon, N. S., and Nathan, C. F. (1990) FAD and GSH participate in macrophage synthesis of nitric oxide Biochem. Biophys. Res. Commun. 168, 558-565 (Pubitemid 20164578)
46. Harbrecht, B. G., Di Silvio, M., Chough, V., Kim, Y. M., Simmons, R. L., and Billiar, T. R. (1997) Glutathione regulates nitric oxide synthase in cultured hepatocytes Ann. Surg. 225, 76-87 (Pubitemid 27026806)
47. Komori, Y., Hyun, J., Chiang, K., and Fukuto, J. M. (1995) The role of thiols in the apparent activation of rat brain nitric oxide synthase (NOS) J. Biochem. 117, 923-927
48. Martin, N. I., Woodward, J. J., Winter, M. B., and Marletta, M. A. (2009) 4,4-Difluorinated analogues of l -arginine and N(G)-hydroxy- l -arginine as mechanistic probes for nitric oxide synthase Bioorg. Med. Chem. Lett. 19, 1758-1762
49. Ravichandran, L. V., Johns, R. A., and Rengasamy, A. (1995) Direct and reversible inhibition of endothelial nitric oxide synthase by nitric oxide Am. J. Physiol. 268, H2216-H2223
50. Roman, L. J., Miller, R. T., de la Garza, M. A., Kim, J. J., and Siler Masters, B. S. (2000) The C terminus of mouse macrophage inducible nitric-oxide synthase attenuates electron flow through the flavin domain J. Biol. Chem. 275, 21914-21919 (Pubitemid 30621763)
51. Wei, C. C., Wang, Z. Q., Wang, Q., Meade, A. L., Hille, R., and Stuehr, D. J. (2001) Rapid kinetic studies link tetrahydrobiopterin radical formation to heme-dioxy reduction and arginine hydroxylation in inducible nitric-oxide synthase J. Biol. Chem. 276, 315-319 (Pubitemid 32050321)
52. Wang, Z.-Q., Wei, C.-C., and Stuehr, D. J. (2002) A conserved tryptophan 457 modulates the kinetics and extent of N-hydroxy- l -arginine oxidation by inducible nitric-oxide synthase J. Biol. Chem. 277, 12830-12837 (Pubitemid 34952647)
53. Wang, Z. Q., Wei, C. C., Ghosh, S., Meade, A. L., Hille, R., and Stuehr, D. J. (2001) A conserved tryptophan in nitric oxide synthase regulates heme-dioxy reduction by tetrahydrobiopterin Biochemistry 40, 12819-12825 (Pubitemid 33026628)
54. Lefèvre-Groboillot, D., Boucher, J.-L., Mansuy, D., and Stuehr, D. J. (2006) Reactivity of the heme-dioxygen complex of the inducible nitric oxide synthase in the presence of alternative substrates FEBS J. 273, 180-191
55. Zhao, Y., Brandish, P. E., Ballou, D. P., and Marletta, M. A. (1999) A molecular basis for nitric oxide sensing by soluble guanylate cyclase Proc. Natl. Acad. Sci. U.S.A. 96, 14753-14758 (Pubitemid 30019712)
56. Assreuy, J., Cunha, F. Q., Liew, F. Y., and Moncada, S. (1993) Feedback inhibition of nitric oxide synthase activity by nitric oxide Br. J. Pharmacol. 108, 833-837 (Pubitemid 23067961)
57. Sheehy, A. M., Burson, M. A., and Black, S. M. (1998) Nitric oxide exposure inhibits endothelial NOS activity but not gene expression: A role for superoxide Am. J. Physiol. 274, L833-L841
58. Ma, X. L., Lopez, B. L., Christopher, T. A., Birenbaum, D. S., and Vinten-Johansen, J. (1996) Exogenous NO inhibits basal NO release from vascular endothelium in vitro and in vivo Am. J. Physiol. 271, H2045-H2051
59. Taldone, F. S., Tummala, M., Goldstein, E. J., Ryzhov, V., Ravi, K., and Black, S. M. (2005) Studying the S-nitrosylation of model peptides and eNOS protein by mass spectrometry Nitric Oxide 13, 176-187 (Pubitemid 41443562)
60. Keszler, A., Zhang, Y., and Hogg, N. (2010) Reaction between nitric oxide, glutathione, and oxygen in the presence and absence of protein: How are S-nitrosothiols formed? Free Radical Biol. Med. 48, 55-64
61. Keshive, M., Singh, S., Wishnok, J. S., Tannenbaum, S. R., and Deen, W. M. (1996) Kinetics of S-nitrosation of thiols in nitric oxide solutions Chem. Res. Toxicol. 9, 988-993 (Pubitemid 26301203)
62. Madej, E., Folkes, L. K., Wardman, P., Czapski, G., and Goldstein, S. (2008) Thiyl radicals react with nitric oxide to form S-nitrosothiols with rate constants near the diffusion-controlled limit Free Radical Biol. Med. 44, 2013-2018
63. Lim, C. H., Dedon, P. C., and Deen, W. M. (2008) Kinetic analysis of intracellular concentrations of reactive nitrogen species Chem. Res. Toxicol. 21, 2134-2147
64. Slama-Schwok, A., Négrerie, M., Berka, V., Lambry, J.-C., Tsai, A.-L., Vos, M. H., and Martin, J.-L. (2002) Nitric oxide (NO) traffic in endothelial NO synthase. Evidence for a new NO binding site dependent on tetrahydrobiopterin? J. Biol. Chem. 277, 7581-7586 (Pubitemid 34953157)
65. Lakowicz, J. R. and Weber, G. (1973) Quenching of protein fluorescence by oxygen. Detection of structural fluctuations in proteins on the nanosecond time scale Biochemistry 12, 4171-4179
66. Pant, K. and Crane, B. R. (2006) Nitrosyl-Heme Structures of Bacillus subtilis Nitric Oxide Synthase Have Implications for Understanding Substrate Oxidation Biochemistry 45, 2537-2544
67. Möller, M. N., Li, Q., Lancaster, J. R., and Denicola, A. (2007) Acceleration of nitric oxide autoxidation and nitrosation by membranes IUBMB Life 59, 243-248 (Pubitemid 46763777)
68. Keller, G. A., Barke, R., Harty, J. T., Humphrey, E., and Simmons, R. L. (1985) Decreased hepatic glutathione levels in septic shock. Predisposition of hepatocytes to oxidative stress: An experimental approach Arch. Surg. 120, 941-945 (Pubitemid 15040893)
69. Okabe, H., Irita, K., Taniguchi, S., Kurosawa, K., Tagawa, K., Yoshitake, J., and Takahashi, S. (1994) Endotoxin causes early changes in glutathione concentrations in rabbit plasma and liver J. Surg. Res. 57, 416-419 (Pubitemid 24283596)
70. McKelvey, T. G., Höllwarth, M. E., Granger, D. N., Engerson, T. D., Landler, U., and Jones, H. P. (1988) Mechanisms of conversion of xanthine dehydrogenase to xanthine oxidase in ischemic rat liver and kidney Am. J. Physiol. 254, G753-G760
71. Hothersall, J. S., Cunha, F. Q., Neild, G. H., and Norohna-Dutra, A. A. (1997) Induction of nitric oxide synthesis in J774 cells lowers intracellular glutathione: Effect of modulated glutathione redox status on nitric oxide synthase induction Biochem. J. 322 (Part 2) 477-481 (Pubitemid 27116573)
72. Buchmuller-Rouiller, Y., Corradin, S. B., Smith, J., Schneider, P., Ransijn, A., Jongeneel, C. V., and Mauël, J. (1995) Role of Glutathione in Macrophage Activation: Effect of Cellular Glutathione Depletion on Nitrite Production and Leishmanicidal Activity Cell. Immunol. 164, 73-80
73. Tirmenstein, M. A., Nicholls-Grzemski, F. A., Schmittgen, T. D., Zakrajsek, B. A., and Fariss, M. W. (2000) Glutathione-dependent regulation of nitric oxide production in isolated rat hepatocyte suspensions Antioxid. Redox Signaling 2, 767-777 (Pubitemid 32062327)
74. Ghigo, D., Alessio, P., Foco, A., Bussolino, F., Costamagna, C., Heller, R., Garbarino, G., Pescarmona, G. P., and Bosia, A. (1993) Nitric oxide synthesis is impaired in glutathione-depleted human umbilical vein endothelial cells Am. J. Physiol. 265, C728-C732
75. Murphy, M. E., Piper, H. M., Watanabe, H., and Sies, H. (1991) Nitric oxide production by cultured aortic endothelial cells in response to thiol depletion and replenishment J. Biol. Chem. 266, 19378-19383 (Pubitemid 21908243)
76. Laursen, J. B., Boesgaard, S., Trautner, S., Rubin, I., Poulsen, H. E., and Aldershvile, J. (2001) Endothelium-dependent vasorelaxation in inhibited by in vivo depletion of vascular thiol levels: Role of endothelial nitric oxide synthase Free Radical Res. 35, 387-394 (Pubitemid 32894357)
77. Sugiyama, T. and Michel, T. (2010) Thiol-metabolizing proteins and endothelial redox state: Differential modulation of eNOS and biopterin pathways Am. J. Physiol. 298, H194-H201
78. Song, M., Kellum, J. A., Kaldas, H., and Fink, M. P. (2004) Evidence that glutathione depletion is a mechanism responsible for the anti-inflammatory effects of ethyl pyruvate in cultured lipopolysaccharide-stimulated RAW 264.7 cells J. Pharmacol. Exp. Ther. 308, 307-316 (Pubitemid 38090732)
79. Liu, X., Miller, M. J., Joshi, M. S., Sadowska-Krowicka, H., Clark, D. A., and Lancaster, J. R. (1998) Diffusion-limited reaction of free nitric oxide with erythrocytes J. Biol. Chem. 273, 18709-18713 (Pubitemid 28366253)
80. 2 Proc. Natl. Acad. Sci. U.S.A. 98, 355-360
81. Stamler, J. S., Simon, D. I., Osborne, J. A., Mullins, M. E., Jaraki, O., Michel, T., Singel, D. J., and Loscalzo, J. (1992) S-nitrosylation of proteins with nitric oxide: Synthesis and characterization of biologically active compounds Proc. Natl. Acad. Sci. U.S.A. 89, 444-448
82. Panda, K., Rosenfeld, R. J., Ghosh, S., Getzoff, E. D., and Stuehr, D. J. (2002) Distinct dimer interaction and regulation in nitric-oxide synthase types I, II, and III J. Biol. Chem. 277, 31020-31030 (Pubitemid 34970806)
83. Mayer, B., Pfeiffer, S., Schrammel, A., Koesling, D., Schmidt, K., and Brunner, F. (1998) A new pathway of nitric oxide/cyclic GMP signaling involving S-nitrosoglutathione J. Biol. Chem. 273, 3264-3270 (Pubitemid 28109738)
84. Tsikas, D. (2000) Is S-nitrosoglutathione formed in nitric oxide synthase incubates? FEBS Lett. 483, 83-84
85. ω-hydroxy- l -arginine complex of inducible nitric oxide synthase oxygenase dimer with active and inactive pterins Biochemistry 39, 4608-4621 (Pubitemid 30225324)
86. Beneš, P., Chovancová, E., Kozlíková, B., Pavelka, A., Strnad, O., Brezovský, J., Sustr, V., Klvaňa, M., Szabó, T., Gora, A., Zamborský, M., Biedermannová, L., Medek, P., Damborský, J., and Sochor, J. (2010) CAVER, version 2.1.