An overview of mechanisms of redox signaling

Journal of Molecular and Cellular Cardiology

Volumn 73, Issue , 2014, Pages 2-9

  Forman, Henry Jay ^a,b   Ursini, Fulvio ^c   Maiorino, Matilde ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF PADOVA   (Italy)

Author keywords

4 Hydroxynonenal; Hydrogen peroxide; Hydroperoxide; Peroxidases; Reactive oxygen species; Signal transduction

Indexed keywords

4 HYDROXYNONENAL; APOPTOSIS SIGNAL REGULATING KINASE 1; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLOSPORIN; CYSTEINE; ELECTROPHILE; GLUTATHIONE; GLUTATHIONE PEROXIDASE 1; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATE; HYDROGEN PEROXIDE; HYDROPEROXIDE DERIVATIVE; HYDROXYL RADICAL; LIPID HYDROPEROXIDE; NITROGEN OXIDE; NUCLEOPHILE; PEROXIDASE; PEROXIREDOXIN 6; PEROXYNITRITE; PEROXYNITROUS ACID; POLYPHENOL DERIVATIVE; PROTEIN S; QUINONE DERIVATIVE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SELENOCYSTEINE PEROXIDASE DERIVATIVE; SINGLET OXYGEN; SUPEROXIDE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ALKYLATION; ANTIOXIDANT ACTIVITY; BINDING SITE; CATALYSIS; CHEMICAL REACTION KINETICS; ENZYME ACTIVITY; HYDROLYSIS; IONIZATION; LIPID PEROXIDATION; METABOLITE; MICROENVIRONMENT; NONHUMAN; NUCLEOPHILICITY; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REVIEW; SECOND MESSENGER; SIGNAL TRANSDUCTION; HUMAN; MALE; METABOLISM; PHYSIOLOGY;

HUMANS; HYDROGEN PEROXIDE; MALE; OXIDATION-REDUCTION; PEROXIDASES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84901833395     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.01.018     Document Type: Review

References (70)

1. Li Q., Lancaster J.R. A conspectus of cellular mechanisms of nitrosothiol formation from nitric oxide. Forum Immunopathol Dis Ther 2012, 3:183-191.
2. Toppo S., Flohé L., Ursini F., Vanin S., Maiorino M. Catalytic mechanisms and specificities of glutathione peroxidases: variations of a basic scheme. Biochim Biophys Acta 2009, 1790:1486-1500.
3. Doulias P.T., Tenopoulou M., Greene J.L., Raju K., Ischiropoulos H. Nitric oxide regulates mitochondrial fatty acid metabolism through reversible protein S-nitrosylation. Sci Signal 2013, 6:rs1.
4. Murphy M.P., Holmgren A., Larsson N.G., Halliwell B., Chang C.J., Kalyanaraman B., et al. Unraveling the biological roles of reactive oxygen species. Cell Metab 2011, 13:361-366.
5. Forman H.J., Maiorino M., Ursini F. Signaling functions of reactive oxygen species. Biochemistry 2010, 49:835-842.
6. Forman H.J. Reactive oxygen species and alpha, beta-unsaturated aldehydes as second messengers in signal transduction. Ann N Y Acad Sci 2010, 1203:35-44.
7. Levonen A.L., Landar A., Ramachandran A., Ceaser E.K., Dickinson D.A., Zanoni G., et al. Cellular mechanisms of redox cell signalling: role of cysteine modification in controlling antioxidant defences in response to electrophilic lipid oxidation products. Biochem J 2004, 378:373-382.
8. Winterbourn C.C. Reconciling the chemistry and biology of reactive oxygen species. Nat Chem Biol 2008, 4:278-286.
9. Poole L.B., Nelson K.J. Discovering mechanisms of signaling-mediated cysteine oxidation. Curr Opin Chem Biol 2008, 12:18-24.
10. Flohe L. Changing paradigms in thiology from antioxidant defense toward redox regulation. Methods Enzymol 2010, 473:1-39.
11. Allen D.G., Lamb G.D., Westerblad H. Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 2008, 88:287-332.
12. Moss J., Vaughan M. ADP-ribosylation of guanyl nucleotide-binding regulatory proteins by bacterial toxins. Adv Enzymol Relat Areas Mol Biol 1988, 61:303-379.
13. Liu J., Farmer J.D., Lane W.S., Friedman J., Weissman I., Schreiber S.L. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 1991, 66:807-815.
14. Wood Z.A., Poole L.B., Karplus P.A. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 2003, 300:650-653.
15. Porter N.A. A perspective on free radical autoxidation: the physical organic chemistry of polyunsaturated fatty acid and sterol peroxidation. J Org Chem 2013, 78:3511-3524.
16. Esterbauer H., Zollner H., Schaur R.J. Aldehydes formed by lipid peroxidation: mechanisms of formation, occurrence and determination. Membrane Lipid Oxidation 1990, 239-268. CRC Press, Boca Raton, FL. C. Vigo-Pelfrey (Ed.).
17. Maiorino M., Coassin M., Roveri A., Ursini F. Microsomal lipid peroxidation: effect of vitamin E and its functional interaction with phospholipid hydroperoxide glutathione peroxidase. Lipids 1989, 24:721-726.
18. Sawyer D.T., Valentine J.S. How super is superoxide?. Acc Chem Res 1981, 14:393-400.
19. Winterbourn C.C., Metodiewa D. Reaction of superoxide with glutathione and other thiols. Methods Enzymol 1995, 251:81-86.
20. Forman H.J., Fridovich I. Superoxide dismutase: a comparison of rate constants. Arch Biochem Biophys 1973, 158:396-400.
21. Gardner P.R., Raineri I., Epstein L.B., White C.W. Superoxide radical and iron modulate aconitase activity in mammalian cells. J Biol Chem 1995, 270:13399-13405.
22. Fujikawa M., Kobayashi K., Kozawa T. Direct oxidation of the [2Fe-2S] cluster in SoxR protein by superoxide: distinct differential sensitivity to superoxide-mediated signal transduction. J Biol Chem 2012, 287:35702-35708.
23. Pryor W.A., Squadrito G.L. The chemistry of peroxynitrite: a product from the reaction of nitric oxide with superoxide. Am J Physiol 1995, 268:L699-L722.
24. Sies H., Sharov V.S., Klotz L.O., Briviba K. Glutathione peroxidase protects against peroxynitrite-mediated oxidations. A new function for selenoproteins as peroxynitrite reductase. J Biol Chem 1997, 272:27812-27817.
25. Trujillo M., Ferrer-Sueta G., Radi R. Kinetic studies on peroxynitrite reduction by peroxiredoxins. Methods Enzymol 2008, 441:173-196.
26. Deeb R.S., Nuriel T., Cheung C., Summers B., Lamon B.D., Gross S.S., et al. Characterization of a cellular denitrase activity that reverses nitration of cyclooxygenase. Am J Physiol Heart Circ Physiol 2013, 305:H687-H698.
27. Lindahl M., Mata-Cabana A., Kieselbach T. The disulfide proteome and other reactive cysteine proteomes: analysis and functional significance. Antioxid Redox Signal 2011, 14:2581-2642.
28. Wang J., Boja E.S., Tan W., Tekle E., Fales H.M., English S., et al. Reversible glutathionylation regulates actin polymerization in A431 cells. J Biol Chem 2001, 276:47763-47766.
29. Chen C.A., Wang T.Y., Varadharaj S., Reyes L.A., Hemann C., Talukder M.A., et al. S-glutathionylation uncouples eNOS and regulates its cellular and vascular function. Nature 2010, 468:1115-1118.
30. Aracena P., Sanchez G., Donoso P., Hamilton S.L., Hidalgo C. S-glutathionylation decreases Mg2+ inhibition and S-nitrosylation enhances Ca2+ activation of RyR1 channels. J Biol Chem 2003, 278:42927-42935.
31. Sanchez G., Pedrozo Z., Domenech R.J., Hidalgo C., Donoso P. Tachycardia increases NADPH oxidase activity and RyR2 S-glutathionylation in ventricular muscle. J Mol Cell Cardiol 2005, 39:982-991.
32. Salsman S.J., Hensley K., Floyd R.A. Sensitivity of protein tyrosine phosphatase activity to the redox environment, cytochrome C, and microperoxidase. Antioxid Redox Signal 2005, 7:1078-1088.
33. Shelton M.D., Chock P.B., Mieyal J.J. Glutaredoxin: role in reversible protein s-glutathionylation and regulation of redox signal transduction and protein translocation. Antioxid Redox Signal 2005, 7:348-366.
34. Gallogly M.M., Starke D.W., Mieyal J.J. Mechanistic and kinetic details of catalysis of thiol-disulfide exchange by glutaredoxins and potential mechanisms of regulation. Antioxid Redox Signal 2009, 11:1059-1081.
35. Manevich Y., Fisher A.B. Peroxiredoxin 6, a 1-Cys peroxiredoxin, functions in antioxidant defense and lung phospholipid metabolism. Free Radic Biol Med 2005, 38:1422-1432.
36. Board P.G., Menon D. Glutathione transferases, regulators of cellular metabolism and physiology. Biochim Biophys Acta 1830, 2013:3267-3288.
37. Gallogly M.M., Mieyal J.J. Mechanisms of reversible protein glutathionylation in redox signaling and oxidative stress. Curr Opin Pharmacol 2007, 7:381-391.
38. Chakravarthi S., Jessop C.E., Bulleid N.J. The role of glutathione in disulphide bond formation and endoplasmic-reticulum-generated oxidative stress. EMBO Rep 2006, 7:271-275.
39. Gupta V., Carroll K.S. Sulfenic acid chemistry, detection and cellular lifetime. Biochim Biophys Acta 2014, 2:847-875.
40. Radi R., Beckman J.S., Bush K.M., Freeman B.A. Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide. J Biol Chem 1991, 266:4244-4250.
41. Tanner J.J., Parsons Z.D., Cummings A.H., Zhou H., Gates K.S. Redox regulation of protein tyrosine phosphatases: structural and chemical aspects. Antioxid Redox Signal 2011, 15:77-97.
42. Gow A.J., Buerk D.G., Ischiropoulos H. A novel reaction mechanism for the formation of S-nitrosothiol in vivo. J Biol Chem 1997, 272:2841-2845.
43. Kirichenko A., Li L., Morandi M.T., Holian A. 4-hydroxy-2-nonenal-protein adducts and apoptosis in murine lung cells after acute ozone exposure. Toxicol Appl Pharmacol 1996, 141:416-424.
44. Forman H.J., Davies K.J., Ursini F. How do nutritional antioxidants really work: nucleophilic tone and para-hormesis versus free radical scavenging in vivo. Free Radic Biol Med 2014, 66:24-35.
45. Coles B., Wilson I., Wardman P., Hinson J.A., Nelson S.D., Ketterer B. The spontaneous and enzymatic reaction of N-acetyl-p-benzoquinonimine with glutathione: a stopped-flow kinetic study. Arch Biochem Biophys 1988, 264:253-260.
46. Maiorino M., Ursini F., Bosello V., Toppo S., Tosatto S.C., Mauri P., et al. The thioredoxin specificity of Drosophila GPx: a paradigm for a peroxiredoxin-like mechanism of many glutathione peroxidases. J Mol Biol 2007, 365:1033-1046.
47. Delaunay A., Pflieger D., Barrault M.B., Vinh J., Toledano M.B. A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell 2002, 111:471-481.
48. Ursini F., Heim S., Kiess M., Maiorino M., Roveri A., Wissing J., et al. Dual function of the selenoprotein PHGPx during sperm maturation. Science 1999, 285:1393-1396.
49. Maiorino M., Roveri A., Benazzi L., Bosello V., Mauri P., Toppo S., et al. Functional interaction of phospholipid hydroperoxide glutathione peroxidase with sperm mitochondrion-associated cysteine-rich protein discloses the adjacent cysteine motif as a new substrate of the selenoperoxidase. J Biol Chem 2005, 280:38395-38402.
50. Bosello-Travain V., Conrad M., Cozza G., Negro A., Quartesan S., Rossetto M., et al. Protein disulfide isomerase and glutathione are alternative substrates in the one Cys catalytic cycle of glutathione peroxidase 7. Biochim Biophys Acta 1830, 2013:3846-3857.
51. Wei P.C., Hsieh Y.H., Su M.I., Jiang X., Hsu P.H., Lo W.T., et al. Loss of the oxidative stress sensor NPGPx compromises GRP78 chaperone activity and induces systemic disease. Mol Cell 2012, 48:747-759.
52. Saitoh M., Nishitoh H., Fujii M., Takeda K., Tobiume K., Sawada Y., et al. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J 1998, 17:2596-2606.
53. Liu H., Zhang H., Iles K.E., Rinna A., Merrill G., Yodoi J., et al. The ADP-stimulated NADPH oxidase activates the ASK-1/MKK4/JNK pathway in alveolar macrophages. Free Radic Res 2006, 40:865-874.
54. Jarvis R.M., Hughes S.M., Ledgerwood E.C. Peroxiredoxin 1 functions as a signal peroxidase to receive, transduce, and transmit peroxide signals in mammalian cells. Free Radic Biol Med 2012, 53:1522-1530.
55. Lu J., Holmgren A. Thioredoxin system in cell death progression. Antioxid Redox Signal 2012, 17:1738-1747.
56. Zhou J., Chng W.J. Roles of thioredoxin binding protein (TXNIP) in oxidative stress, apoptosis and cancer. Mitochondrion 2013, 13:163-169.
57. 2 involves KEAP1 disulfide formation. J Biol Chem 2010, 285:8463-8471.
58. Zhang D.D., Hannink M. Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress. Mol Cell Biol 2003, 23:8137-8151.
59. Hong F., Sekhar K.R., Freeman M.L., Liebler D.C. Specific patterns of electrophile adduction trigger Keap1 ubiquitination and Nrf2 activation. J Biol Chem 2005, 280:31768-31775.
60. Hong F., Freeman M.L., Liebler D.C. Identification of sensor cysteines in human Keap1 modified by the cancer chemopreventive agent sulforaphane. Chem Res Toxicol 2005, 18:1917-1926.
61. Hur W., Gray N.S. Small molecule modulators of antioxidant response pathway. Curr Opin Chem Biol 2011, 15:162-173.
62. Luo Y., Eggler A.L., Liu D., Liu G., Mesecar A.D., van Breemen R.B. Sites of alkylation of human Keap1 by natural chemoprevention agents. J Am Soc Mass Spectrom 2007, 18:2226-2232.
63. Ohnuma T., Nakayama S., Anan E., Nishiyama T., Ogura K., Hiratsuka A. Activation of the Nrf2/ARE pathway via S-alkylation of cysteine 151 in the chemopreventive agent-sensor Keap1 protein by falcarindiol, a conjugated diacetylene compound. Toxicol Appl Pharmacol 2010, 244:27-36.
64. Rachakonda G., Xiong Y., Sekhar K.R., Stamer S.L., Liebler D.C., Freeman M.L. Covalent modification at Cys151 dissociates the electrophile sensor Keap1 from the ubiquitin ligase CUL3. Chem Res Toxicol 2008, 21:705-710.
65. Velichkova M., Hasson T. Keap1 in adhesion complexes. Cell Motil Cytoskeleton 2003, 56:109-119.
66. Awasthi Y.C., Yang Y., Tiwari N.K., Patrick B., Sharma A., Li J., et al. Regulation of 4-hydroxynonenal-mediated signaling by glutathione S-transferases. Free Radic Biol Med 2004, 37:607-619.
67. Forman H.J., Dickinson D.A., Iles K.E. HNE-signaling pathways leading to its elimination. Mol Aspects Med 2003, 24:189-194.
68. Parola M., Robino G., Marra F., Pinzani M., Bellomo G., Leonarduzzi G., et al. HNE interacts directly with JNK isoforms in human hepatic stellate cells. J Clin Invest 1998, 102:1942-1950.
69. Uchida K., Shiraishi M., Naito Y., Torii Y., Nakamura Y., Osawa T. Activation of stress signaling pathways by the end product of lipid peroxidation. 4-hydroxy-2-nonenal is a potential inducer of intracellular peroxide production. J Biol Chem 1999, 274:2234-2242.
70. McClung J.P., Roneker C.A., Mu W., Lisk D.J., Langlais P., Liu F., et al. Development of insulin resistance and obesity in mice overexpressing cellular glutathione peroxidase. Proc Natl Acad Sci U S A 2004, 101:8852-8857.