Specificity of a third kind: Reactive oxygen and nitrogen intermediates in cell signaling

Journal of Clinical Investigation

Volumn 111, Issue 6, 2003, Pages 769-778

  Nathan, Carl ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE;

ADAPTATION; CELL COMMUNICATION; CELL KILLING; CELL SPECIFICITY; CHEMICAL STRUCTURE; DIFFUSION; IMMUNE SYSTEM; METABOLISM; MOLECULAR INTERACTION; OLIGOMOLECULAR SIGNAL TRANSDUCTION; PRIORITY JOURNAL; REVIEW; SECOND MESSENGER; SIGNAL TRANSDUCTION; ANIMAL; HUMAN; PHYSIOLOGY; SENSITIVITY AND SPECIFICITY;

ANIMALS; HUMANS; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; SECOND MESSENGER SYSTEMS; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION;

EID: 0037365968     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI200318174     Document Type: Review

References (96)

1. Nathan, C. 1992. Nitric oxide as a secretory product of mammalian cells. FASEB J. 6:3051-3064.
2. Palmer, R.M., Ferrige, A.G., and Moncada, S. 1987. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature. 327:524-526.
3. Ignarro, L.J., Buga, G.M., Wood, K.S., Byrns, R.E., and Chaudhuri, G. 1987. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl. Acad. Sci. U. S. A. 84:9265-9269.
4. Arnold, W.P., Mittal, C.K., Katsuki, S., and Murad, F. 1977. Nitric oxide activates guanylate cyclase and increases guanosine 3′: 5′-cyclic monophosphate levels in various tissue preparations. Proc. Natl. Acad. Sci. U. S. A. 74:3203-3207.
5. Schreck, R., Rieber, P., and Baeuerle, P.A. 1991. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J. 10:2247-2258.
6. Amstad, P.A., Krupitza, G., and Cerutti, P.A. 1992. Mechanism of c-fos induction by active oxygen. Cancer Res. 52:3952-3960.
7. Nakamura, H., Nakamura, K., and Yodoi, J. 1997. Redox regulation of cellular activation. Annu. Rev. Immunol. 15:351-369.
8. Beckman, K.B., and Ames, B.N. 1998. The free radical theory of aging matures. Physiol. Rev. 78:547-581.
9. Dalton, T.P., Shertzer, H.G., and Puga, A. 1999. Regulation of gene expression by reactive oxygen. Annu. Rev. Pharmacol. Toxicol. 39:67-101.
10. Finkel, T. 1998. Oxygen radicals and signaling. Curr. Opin. Cell Biol. 10:248-253.
11. Rhee, S.G., Bae, Y.S., Lee, S.R., and Kwon, J. 2000. Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation. Set. STKE. 2000:PE1.
12. Nathan, C., and Shiloh, M.U. 2000. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl. Acad. Sci. U. S. A. 97:8841-8848.
13. Stamler, J.S., Lamas, S., and Fang, F.C. 2001. Nitrosylation. The prototypic redox-based signaling mechanism. Cell. 106:675-683.
14. Bogdan, C. 2001. Nitric oxide and the regulation of gene expression. Trends Cell Biol. 11:66-75.
15. Droge, W. 2002. Free radicals in the physiological control of cell function. Physiol. Rev. 82:47-95.
16. Reth, M. 2002. Hydrogen peroxide as second messenger in lymphocyte activation. Nat. Immunol. 3:1129-1134.
17. Golderer, G., Werner, E.R., Leitner, S., Grobner, P., and Werner-Felmayer, G. 2001. Nitric oxide synthase is induced in sporulation of Physarum polycephalum. Genes Dev. 15:1299-1309.
18. Kuzin, B., Roberts, I., Peunova, N., and Enikolopov, G. 1996. Nitric oxide regulates cell proliferation during Drosophila development. Cell. 87:639-649.
19. Peunova, N., Scheinker, V., Cline, H., and Enikolopov, G. 2001. Nitric oxide is an essential negative regulator of cell proliferation in Xenopus brain. J. Neurosci. 21:8809-8818.
20. Klein, J.A., et al. 2002. The harlequin mouse mutation downregulates apoptosis-inducing factor. Nature. 419:367-374.
21. Gu, Z., et al. 2002. S-nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science. 297:1186-1190.
22. Terman, J.R., Mao, T., Pasterkamp, R.J., Yu, H.H., and Kolodkin, A.L. 2002. MICALs, a family of conserved flavoprotein oxidoreductases, function in plexin-mediated axonal repulsion. Cell. 109:887-900.
23. Nathan, C., and Xie, Q.W. 1994. Nitric oxide synthases: roles, tolls, and controls. Cell. 78:915-918.
24. Lambeth, J.D. 2002. Nox/Duox family of nicotinamide adenine dinucleotide (phosphate) oxidases. Curr. Opin. Hematol. 9:11-17.
25. Ehrt, S., et al. 2001. Reprogramming of the macrophage transcriptome in response to interferon-gamma and Mycobacterium tuberculosis: signaling roles of nitric oxide synthase-2 and phagocyte oxidase. J. Exp. Med. 194:1123-1140.
26. Diefenbach, A., Schindler, H., Rollinghoff, M., Yokoyama, W.M., and Bogdan, C. 1999. Requirement for type 2 NO synthase for IL-12 signaling in innate immunity. Science. 284:951-955.
27. Jordan, J.D., Landau, E.M., and Iyengar, R. 2000. Signaling networks: the origins of cellular multitasking. Cell. 103:193-200.
28. Ingolia, N.T., and Murray, A.W. 2002. Signal transduction. History matters. Science. 297:948-949.
29. Strohman, R. 2002. Maneuvering in the complex path from genotype to phenotype. Science. 296:701-703.
30. Wentworth, P., Jr, et al. 2002. Evidence for antibody-catalyzed ozone formation in bacterial killing and inflammation. Science. 298:2195-2199.
31. Sutherland, E.W. 1972. Studies on the mechanism of hormone action. Science. 177:401-408.
32. Smith, O. 1998. Nobel Prize for NO research. Nat. Med. 4:1215.
33. Levy, D.E., and Darnell, J.E., Jr. 2002. Stats: transcriptional control and biological impact. Nat. Rev. Mol. Cell Biol. 3:651-662.
34. Rich, T.C., et al. 2001. A uniform extracellular stimulus triggers distinct cAMP signals in different compartments of a simple cell. Proc. Natl. Acad. Sci. U. S. A. 98:13049-13054.
35. Davare, M.A., et al. 2001. A beta2 adrenergic receptor signaling complex assembled with the Ca2+ channel Cav1.2. Science. 293:98-101.
36. Bootman, M.D., et al. 2001. Calcium signalling - an overview. Semin. Cell Dev. Biol. 12:3-10.
37. Vieira, O.V., et al. 2001. Distinct roles of class I and class III phosphatidylinositol 3-kinases in phagosome formation and maturation. J. Cell Biol. 155:19-25.
38. Perry, S.J. et al. 2002. Targeting of cyclic AMP degradation to beta 2-adrenergic receptors by beta-arrestins. Science. 298:834-836.
39. Dolmersch, R. 2003. Excitation-transcription coupling: signaling by ion channels to the nucleus. Sci. STKE. 2003:PE4.
40. Dolmetsch, R.E., Xu, K., and Lewis, R.S. 1998. Calcium oscillations increase the efficiency and specificity of gene expression. Nature. 392:933-936.
41. Feske, S., Giltnane, J., Dolmetsch, R., Staudt, L.M., and Rao, A. 2001. Gene regulation mediated by calcium signals in T lymphocytes. Nat. Immunol. 2:316-324.
42. Hardie, D.G., Carling, D., and Carlson, M. 1998. The AMP-activated/SiNF1 protein kinase subfamily: metabolic sensors of the eukaryotic cell? Annu. Rev. Biochem. 67:821-855.
43. Chen, Y., et al. 2000. Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science. 289:625-628.
44. Zippin, J.H., Levin, L.R., and Buck, J. 2001. CO(2)/HCO(3)(-)-responsive soluble adenylyl cyclase as a putative metabolic sensor. Trends Endocrinol. Metab. 12:366-370.
45. Zippin, J.H., et al. 2003. Compartmentalization of bicarbonate-sensitive adenylyl cyclase in distinct signaling microdomains. FASEB J. 17:82-84.
46. Rutter, J., Reick, M., Wu, L.C., and McKnight, S.L. 2001. Regulation of clock and NPAS2 DNA binding by the redox state of NAD cofactors. Science. 293:510-514.
47. Zhang, Q., Piston, D.W., and Goodman, R.H. 2002. Regulation of corepressor function by nuclear NADH. Science. 295:1895-1897.
48. Chatterji, D., and Ojha, A.K. 2001. Revisiting the stringent response, ppGpp and starvation signaling. Curr. Opin. Microbiol. 4:160-165.
49. Dennis, P.B., et al. 2001. Mammalian TOR: a homeostatic ATP sensor. Science. 294:1102-1105.
50. Vaziri, H., et al. 2001. hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell. 107:149-159.
51. Arner, E.S., and Holmgren, A. 2000. Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 267:6102-6109.
52. Jaffrey, S.R., Erdjument-Bromage, H., Ferris, C.D., Tempst, P., and Snyder, S.H. 2001. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat. Cell Biol. 3:193-197.
53. Zheng, M., Aslund, F., and Storz, G. 1998 Activation of the OxyR transcription factor by reversible disulfide bond formation. Science. 279:1718-1721.
54. Mongkolsuk, S., and Helmann, J.D. 2002. Regulation of inducible peroxide stress responses. Mol. Microbiol. 45:9-15.
55. Fuangthong, M., and Helmann, J.D. 2002. The OhrR repressor senses organic hydroperoxides by reversible formation of a cysteine-sulfenic acid derivative. Proc. Natl. Acad. Sci. U. S. A. 99:6690-6695.
56. Delaunay, A., Pflieger, D., Barrault, M.B., Vinh, J., and Toledano, M.B. 2002. A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell. 111:471-481.
57. Kim, S.O., et al. 2002. OxyR: a molecular code for redox-related signaling. Cell. 109:383-396.
58. Ding, H., and Demple, B. 2000. Direct nitric oxide signal transduction via nitrosylation of iron-sulfur centers in the SoxR transcription activator. Proc. Natl. Acad. Sci. U. S. A. 97:5146-5150.
59. Denu, J.M., and Tanner, K.G. 2002. Redox regulation of protein tyrosine phosphatases by hydrogen peroxide: detecting sulfenic acid intermediates and examining reversible inactivation. Methods Enzymol. 348:297-305.
60. Meng, T.C., Fukada, T., and Tonks, N.K. 2002. Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol. Cell. 9:387-399.
61. Xu, D., Rovira, I.I., and Finkel, T. 2002. Oxidants painting the cysteine chapel: redox regulation of PTPs. Dev. Cell. 2:251-252.
62. Zheng, B., et al. 2001. Nonredundant roles of the mPer1 and mPer2 genes in the mammalian circadian clock. Cell. 105:683-694.
63. Dioum, E.M., et al. 2002. NPAS2: a gas-responsive transcription factor. Science. 298:2385-2387.
64. Ivan, M., et al. 2001. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science. 292:464-468.
65. Jaakkola, P., et al. 2001. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science. 292:468-472.
66. Epstein, A.C., et al. 2001. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell. 107:43-54.
67. Bruick, R.K., and McKnight, S.L. 2001. A conserved family of prolyl-4-hydroxylases that modify HIF. Science. 294:1337-1340.
68. Lando, D., Peet, D.J., Whelan, D.A., Gorman, J.J., and Whitelaw, M.L. 2002. Asparagine hydroxylation of the HIF transactivation domain a hypoxic switch. Science. 295:858-861.
69. Semenza, G.L. 2001. HIF-1 and mechanisms of hypoxia sensing. Curr. Opin. Cell Biol. 13:167-171.
70. Hoyos, B., et al. 2000. The cysteine-rich regions of the regulatory domains of Raf and protein kinase C as retinoid receptors. J. Exp. Med. 192:835-845.
71. Taylor, B.L., and Zhulin, I.B. 1999. PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol. Mol. Biol. Rev. 63:479-506.
72. Moncada, S., and Erusalimsky,J.D. 2002. Does nitric oxide modulate mitochondrial energy generation and apoptosis? Nat. Rev. Mol. Cell Biol. 3:214-220.
73. Balmer, Y., et al. 2003. Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proc. Natl. Acad. Sci. U. S. A. 100:370-375.
74. Bryk, R., Griffin, P., and Nathan, C. 2000. Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature. 407:211-215.
75. Bryk, R., Lima, C.D., Erdjument-Bromage, H., Tempst, P., and Nathan, C. 2002. Metabolic enzymes of mycobacteria linked to antioxidant defense by a thioredoxin-like protein. Science. 295:1073-1077.
76. Chang, T.S., et al. 2002. Regulation of peroxiredoxin I activity by Cdc2-mediated phosphorylation. J. Biol. Chem. 277:25370-25376.
77. Haendeler, J., et al. 2002. Redox regulatory and anti-apoptotic functions of thioredoxin depend on S-nitrosylation at cysteine 69. Nat. Cell Biol. 4:743-749.
78. Wolff, J., Cook, G.H., Goldhammer, A.R., and Berkowitz, S.A. 1980. Calmodulin activates prokaryotic adenylate cyclase. Proc. Natl. Acad. Sci. U. S. A. 77:3841-3844.
79. Confer, D.L., and Eaton, J.W. 1982. Phagocyte impotence caused by an invasive bacterial adenylate cyclase. Science. 217:948-950.
80. Mahadev, K., Zilbering, A., Zhu, L., and Goldstein, B.J. 2001. Insulin-stimulated hydrogen peroxide reversibly inhibits protein-tyrosine phosphatase 1b in vivo and enhances the early insulin action cascade. J. Biol. Chem. 276:21938-21942.
81. Mahadev, K., et al. 2001. Hydrogen peroxide generated during cellular insulin stimulation is integral to activation of the distal insulin signaling cascade in 3T3-L1 adipocytes. J. Biol. Chem. 276:48662-48669.
82. Sundaresan, M., Yu, Z.X., Ferrans, V.J., Irani, K., and Finkel, T. 1995. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science. 270:296-299.
83. Bae, Y.S., et al. 1997. Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation. J. Biol. Chem. 272:217-221.
84. Junn, E., et al. 2000. Requirement of hydrogen peroxide generation in TGF-bera 1 signal transduction in human lung fibroblast cells: involvement of hydrogen peroxide and Ca2+ in TGF-beta 1-induced IL-6 expression. J. Immunol. 165:2190-2197.
85. Suzukawa, K., et al. 2000. Nerve growth factor-induced neuronal differentiation requires generation of Rac1-regulated reactive oxygen species. J. Biol. Chem. 275:13175-13178.
86. Griendling, K.K., and Ushio-Fukai, M. 2000. Reactive oxygen species as mediators of angiotensin II signaling. Regul. Pept. 91:21-27.
87. Sattler, M., et al. 1999. Hematopoietic growth factors signal through the formation of reactive oxygen species. Blood. 93:2928-2935.
88. Devadas, S., Zaritskaya, L., Rhee, S.G., Oberley, L., and Williams, M.S. 2002. Discrete generation of superoxide and hydrogen peroxide by T cell receptor stimulation: selective regulation of mitogen-activated protein kinase activation and fas ligand expression. J. Exp. Med. 195:59-70.
89. Featon, D.T. 1997. Seeking wisdom in innate immunity. Nature. 388:323-324.
90. Medzhitov, R., and Janeway, C.A., Jr. 1999. Innate immune induction of the adaptive immune response. Cold Spring Harb. Symp. Quant. Biol. 64:429-435.
91. Nathan, C. 2002. Points of control in inflammation. Nature. 420:846-852.
92. O'Brien, J., Friedlander, A., Dreier, T., Ezzell, J., and Leppla, S. 1985. Effects of anthrax toxin components on human neutrophils. Infect. Immun. 47:306-310.
93. Hanna, P.C., Kruskal, B.A., Ezekowitz, R.A., Bloom, B.R., and Collier, R.J. 1994. Role of macrophage oxidative burst in the action of anthrax lethal toxin. Mol. Med. 1:7-18.
94. Flak, T.A., and Goldman, W.E. 1999. Signalling and cellular specificity of airway nitric oxide production in pertussis. Cell Microbiol. 1:51-60.
95. Stebbins, C.E., and Galan, J.E. 2001. Structural mimicry in bacterial virulence. Nature. 412:701-705.
96. Madden, J.C., Ruiz, N., and Caparon, M. 2001. Cytolysin-mediated translocation (CMT): a functional equivalent of type III secretion in gram-positive bacteria. Cell. 104:143-152.