Signaling functions of reactive oxygen species

Biochemistry

Volumn 49, Issue 5, 2010, Pages 835-842

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

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYTIC CYSTEINES; ENZYMATIC CATALYSIS; ENZYMATIC PRODUCTION; GENERAL CONSTRAINTS; MECHANISM OF OXIDATION; NONENZYMATIC REACTION; OXIDATION STATE; PHYSIOLOGICAL PROCESS; POTENTIAL MECHANISM; PROTEIN THIOLS; REACTIVE OXYGEN SPECIES; REDOX SIGNALING; REDOX SWITCH; SECOND MESSENGER; SELENOCYSTEINE; SIGNALING FUNCTIONS; SULFENIC ACIDS; THERMODYNAMIC AND KINETIC CONSIDERATIONS; THIOL OXIDATION; THIOL PEROXIDASE;

CATALYTIC OXIDATION; OXYGEN;

SIGNALING;

CYSTEINE; DISULFIDE; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; SELENOCYSTEINE; SULFENIC ACID DERIVATIVE; SUPEROXIDE; THIOL;

AUTOOXIDATION; CATALYSIS; ENZYME CHEMISTRY; ENZYME KINETICS; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; REACTION ANALYSIS; REVIEW; SECOND MESSENGER; SIGNAL TRANSDUCTION; THERMODYNAMICS;

ANIMALS; CYSTEINE; HUMANS; HYDROGEN PEROXIDE; PEROXIREDOXINS; REACTIVE OXYGEN SPECIES; SECOND MESSENGER SYSTEMS; SIGNAL TRANSDUCTION;

EID: 75749136883     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi9020378     Document Type: Review

References (101)

1. Hemler, M. E., and Lands, W. E. (1980) Evidence for a peroxide-initiated free radical mechanism of prostaglandin biosynthesis. J. Biol. Chem. 255, 6253-6261.
2. Morrow, J. D., Awad, J. A., Wu, A., Zackert, W. E., Daniel, V. C., and Roberts, L. J., II (1996) Nonenzymatic free radical-catalyzed generation of thromboxane-like compounds (isothromboxanes) in vivo. J. Biol. Chem. 271, 23185-23190.
3. Benedetti, A., Comporti, M., and Esterbauer, H. (1980) Identification of 4-hydroxynonenal as a cytotoxic product originating from the peroxidation of liver microsomal lipids. Biochim. Biophys. Acta 620, 281-296.
4. Mohler, E. R., Franklin, M. T., and Adam, L. P. (1996) Intracellular signaling by 8-epi-prostaglandin F2R is mediated by thromboxane A2/prostaglandin endoperoxide receptors in porcine carotid arteries. Biochem. Biophys. Res. Commun. 225, 915-923.
5. Wagner, R. S., Weare, C., Jin, N., Mohler, E. R., and Rhoades, R. A. (1997) Characterization of signal transduction events stimulated by 8-epi-prostaglandin(PG)F2α in rat aortic rings. Prostaglandins 54, 581-599.
6. Parola, M., Robino, G., Marra, F., Pinzani, M., Bellomo, G., Leonarduzzi, G., Chiarugi, P., Camandola, S., Poli, G., Waeg, G., Gentilini, P., and Dianzani, M. U. (1998) HNE interacts directly with JNK isoforms in human hepatic stellate cells. J. Clin. Invest. 102, 1942-1950.
7. Castello, L., Marengo, B., Nitti, M., Froio, T., Domenicotti, C., Biasi, F., Leonarduzzi, G., Pronzato, M. A., Marinari, U. M., Poli, G., and Chiarpotto, E. (2005) 4-Hydroxynonenal signalling to apoptosis in isolated rat hepatocytes: The role of PKC-δ. Biochim. Biophys. Acta 1737, 83-93.
8. Czech, M. P. (1976) Differential effects of sulfhydryl reagents on activation and deactivation of the fat cell hexose transport system. J. Biol. Chem. 251, 1164-1170.
9. Mukherjee, S. P., Lane, R. H., and Lynn, W. S. (1978) Endogenous hydrogen peroxide and peroxidative metabolism in adipocytes in response to insulin and sulfhydryl reagents. Biochem. Pharmacol. 27, 2589-2594.
10. Mukherjee, S. P., and Mukherjee, C. (1982) Similar activities of nerve growth factor and its homologue proinsulin in intracellular hydrogen peroxide production and metabolism in adipocytes. Transmembrane signalling relative to insulin-mimicking cellular effects. Biochem. Pharmacol. 31, 3163-3172.
11. Burdon, R. H., Gill, V., and Rice-Evans, C. (1989) Cell proliferation and oxidative stress. Free Radical Res. Commun. 7, 149-159.
12. Schreck, R., Rieber, P., and Baeuerle, P. A. (1991) Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kB transcription factor and HIV-1. EMBO J. 10, 2247-2258.
13. Kaul, N., and Forman, H. J. (1996) Activation of NF-κB by the respiratory burst of macrophages. Free Radical Biol. Med. 21, 401-405.
14. Suh, Y. A., Arnold, R. S., Lassegue, B., Shi, J., Xu, X., Sorescu, D., Chung, A. B., Griendling, K. K., and Lambeth, J. D. (1999) Cell transformation by the superoxide-generating oxidase Mox1. Nature 401, 79-82.
15. phox homologues in vascular smooth muscle cells: Nox1 mediates angiotensin II-induced superoxide formation and redox-sensitive signaling pathways. Circ. Res. 88, 888-894.
16. phox: Cloning and tissue expression of Nox3, Nox4, and Nox5. Gene 269, 131-140.
17. Winterbourn, C. C., and Metodiewa, D. (1995) Reaction of super-oxide with glutathione and other thiols. Methods Enzymol. 251, 81-86.
18. Forman, H. J., and Fridovich, I. (1973) Superoxide dismutase: A comparison of rate constants. Arch. Biochem. Biophys. 158, 396-400.
19. Hawkins, B. J., Madesh, M., Kirkpatrick, C. J., and Fisher, A. B. (2007) Superoxide flux in endothelial cells via the chloride channel-3 mediates intracellular signaling. Mol. Biol. Cell 18, 2002-2012.
20. Bauer, G. (2002) Signaling and proapoptotic functions of transformed cell-derived reactive oxygen species. Prostaglandins, Leukotrienes Essent. Fatty Acids 66, 41-56.
21. Levonen, A. L., Landar, A., Ramachandran, A., Ceaser, E. K., Dickinson, D. A., Zanoni, G., Morrow, J. D., and Darley-Usmar, V. M. (2004) Cellular mechanisms of redox cell signalling: Role of cysteine modification in controlling antioxidant defences in response to electrophilic lipid oxidation products. Biochem. J. 378, 373-382.
22. Rinna, A., and Forman, H. J. (2008) SHP-1 inhibition by 4-hydroxynonenal activates Jun N-terminal kinase and glutamate cysteine ligase. Am. J. Respir. Cell Mol. Biol. 39, 97-104.
23. Cadenas, E., Stess, H., Nastaincyzk, W., and Ullrich, V. (1983) Formation of singlet oxygen detected by low level chemiluminescenceduring enzymatic reduction of prostaglandin G2 to H2. Hoppe-Seyler's Z. Physiol. Chem. 304, 519-528.
24. Chance, B., and Oshino, N. (1971) Kinetics and mechanisms of catalase in peroxisomes of the mitochondrial fraction. Biochem. J. 122, 225-233.
25. Loschen, G., Flohé, L., and Chance, B. (1971) Respiratory chain linked H2O2 production in pigeon heart mitochondria. FEBS Lett. 18, 261.
26. Boveris, A., and Chance, B. (1973) The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem. J. 134, 707-716.
27. Cadenas, E., and Boveris, A. (1980) Enhancement of hydrogen peroxide formation by protophores and ionophores in antimycin-supplemented mitochondria. Biochem. J. 188, 31-37.
28. Nègre-Salvayre, A., Hirtz, C., Carrera, G., Cazenave, R., Troly, M., Salvayre, R., Pénicaud, L., and Casteilla, L. (1997) A role for uncoupling protein-2 as a regulator of mitochondrial hydrogen peroxide generation. FASEB J. 11, 809-815.
29. Poderoso, J. J., Carreras, M. C., Lisdero, C., Riobo, N., Schopfer, F., and Boveris, A. (1996) Nitric oxide inhibits electron transfer and increases superoxide radical production in rat heart mitochondria and submitochondrial particles. Arch. Biochem. Biophys. 328, 85-92.
30. Lizasoain, I., Moro, M. A., Knowles, R. G., Darley-Usmar, V., and Moncada, S. (1996) Nitric oxide and peroxynitrite exert distinct effects on mitochondrial respiration which are differentially blocked by glutathione or glucose. Biochem. J. 314 (Part 3), 877-880.
31. Loschen, G., Azzi, A., Richter, C., and Flohé, L. (1974) Superoxide radicals as precursors of mitochondrial hydrogen peroxide. FEBS Lett. 42, 68.
32. Forman, H. J., and Kennedy, J. A. (1974) Role of superoxide radical in mitochondrial dehydrogenase reactions. Biochem. Biophys. Res. Commun. 60, 1044-1050.
33. Winterbourn, C. C., French, J. K., and Claridge, R. F. (1978) Superoxide dismutase as an inhibitor of reactions of semiquinone radicals. FEBS Lett. 94, 269-272.
34. Dupuy, C., Ohayon, R., Valent, A., Noel-Hudson, M. S., Deme, D., and Virion, A. (1999) Purification of a novel flavoprotein involved in the thyroid NADPH oxidase. Cloning of the porcine and human cdnas. J. Biol. Chem. 274, 37265-37269.
35. Edens, W. A., Sharling, L., Cheng, G., Shapira, R., Kinkade, J. M., Lee, T., Edens, H. A., Tang, X., Sullards, C., Flaherty, D. B., Benian, G. M., and Lambeth, J. D. (2001) Tyrosine cross-linking of extracellular matrix is catalyzed by Duox, a multidomain oxidase/peroxidase with homology to the phagocyte oxidase subunit gp91phox. J. Cell Biol. 154, 879-891.
36. Massey, V., Strickland, S., Mayhew, S. G., Howell, L. G., Engel, P. C., Matthews, R. G., Schuman, M., and Sullivan, P. A. (1969) The production of superoxide anion radicals in the reaction of reduced flavins and flavoproteins with molecular oxygen. Biochem. Biophys. Res. Commun. 36, 891-897.
37. Erich, E. H. (1966) Gmelin Handbuch der Anorganischen Chemie, 8th ed., p 429, Springer-Verlag Chemie, Weinheim, Germany.
38. Kerr, J. A. (1966) Bond dissociation energies by kinetic methods. Chem. Rev. 66, 465-500.
39. Barton, J. P., Packer, J. E., and Sims, R. J. (1973) Kinetics of the reaction of hydrogen peroxide with cysteine and cysteamine. J. Chem. Soc., Perkin Trans. 11, 1547-1549.
40. Winterbourn, C. C., and Metodiewa, D. (1999) Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide. Free Radical Biol. Med. 27, 322-328.
41. Brigelius-Flohé, R., Friedrichs, B., Maurer, S., Schultz, M., and Streicher, R. (1997) Interleukin-1-induced nuclear factor κB activation is inhibited by overexpression of phospholipid hydroperoxide glutathione peroxidase in a human endothelial cell line. Biochem. J. 328 (Part 1), 199-203.
42. Dubbs, J. M., and Mongkolsuk, S. (2007) Peroxiredoxins in bacterial antioxidant defense. Subcell. Biochem. 44, 143-193.
43. Pradáč, J., and Koryta, J. (1968) Electrode processes of the sulfhydryl-disulfide system I. Cystine at a platinum electrode. J. Electro-anal. Chem. 17, 167-175.
44. Howie, J. K., Houts, J. J., and Sawyer, D. T. (1977) Oxidation-reduction chemistry of DL-R-lipoic acid, propanedithiol, and trimethylene disulfide in aprotic and in aqueous media. J. Am. Chem. Soc. 99, 6323-6326.
45. Bontempelli, G., Magno, F., and Mazzocchin, G. (1973) Electrochemical oxidation of phenyldisulfide in acetonitrile medium. J. Electroanal. Chem. 42, 57-67.
46. Wood, Z. A., Poole, L. B., and Karplus, P. A. (2003) Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300, 650-653.
47. Woo, H. A., Chae, H. Z., Hwang, S. C., Yang, K. S., Kang, S. W., Kim, K., and Rhee, S. G. (2003) Reversing the inactivation of peroxiredoxins caused by cysteine sulfinic acid formation. Science 300, 653-656.
48. Fisher, A. B., Dodia, C., Manevich, Y., Chen, J. W., and Feinstein, S. I. (1999) Phospholipid hydroperoxides are substrates for non-selenium glutathione peroxidase. J. Biol. Chem. 274, 21326-21334.
49. Tosatto, S. C., Bosello, V., Fogolari, F., Mauri, P., Roveri, A., Toppo, S., Flohé, L., Ursini, F., and Maiorino, M. (2008) The catalytic site of glutathione peroxidases. Antioxid. Redox Signaling 10, 1515-1526.
50. Wood, Z. A., Schroder, E., Robin Harris, J., and Poole, L. B. (2003) Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 28, 32-40.
51. Seo, Y. H., and Carroll, K. S. (2009) Profiling protein thiol oxidation in tumor cells using sulfenic acid-specific antibodies. Proc. Natl. Acad. Sci. U.S.A. 106, 16163-16168.
52. Maiorino, M., Ursini, F., Bosello, V., Toppo, S., Tosatto, S. C., Mauri, P., Becker, K., Roveri, A., Bulato, C., Benazzi, L., De Palma, A., and Flohé, L. (2007) The thioredoxin specificity of Drosophila GPx: A paradigm for a peroxiredoxin-like mechanism of many glutathione peroxidases. J. Mol. Biol. 365, 1033-1046.
53. Trujillo, M., Mauri, P., Benazzi, L., Comini, M., De Palma, A., Flohé, L., Radi, R., Stehr, M., Singh, M., Ursini, F., and Jaeger, T. (2006) The mycobacterial thioredoxin peroxidase can act as a one-cysteine peroxiredoxin. J. Biol. Chem. 281, 20555-20566.
54. Toppo, S., Flohé, L., Ursini, F., Vanin, S., and Maiorino, M. (2009) Catalytic mechanisms and specificities of glutathione peroxidases: Variations of a basic scheme. Biochim. Biophys. Acta 1790, 1486-1500.
55. Trujillo, M., Ferrer-Sueta, G., Thomson, L., Flohé, L., and Radi, R. (2007) Kinetics of peroxiredoxins and their role in the decomposition of peroxynitrite. Subcell. Biochem. 44, 83-113.
56. 2 is not reflected in its reaction with other oxidants and thiol reagents. J. Biol. Chem. 282, 11885-11892.
57. Low, F. M., Hampton, M. B., Peskin, A. V., and Winterbourn, C. C. (2007) Peroxiredoxin 2 functions as a noncatalytic scavenger of low-level hydrogen peroxide in the erythrocyte. Blood 109, 2611-2617.
58. Parsonage, D., Youngblood, D. S., Sarma, G. N., Wood, Z. A., Karplus, P. A., and Poole, L. B. (2005) Analysis of the link between enzymatic activity and oligomeric state in AhpC, a bacterial peroxiredoxin. Biochemistry 44, 10583-10592.
59. Zheng, M., Aslund, F., and Storz, G. (1998) Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279, 1718-1721.
60. Poole, L. B., Klomsiri, C., Knaggs, S. A., Furdui, C. M., Nelson, K. J., Thomas, M. J., Fetrow, J. S., Daniel, L. W., and King, S. B. (2007) Fluorescent and affinity-based tools to detect cysteine sulfenic acid formation in proteins. Bioconjugate Chem. 18, 2004-2017.
61. Woo, H. A., Chae, H. Z., Hwang, S. C., Yang, K. S., Kang, S. W., Kim, K., and Rhee, S. G. (2003) Reversing the inactivation of peroxiredoxins caused by cysteine sulfinic acid formation. Science 300, 653-656.
62. Zheng, M., Wang, X., Templeton, L. J., Smulski, D. R., LaRossa, R. A., and Storz, G. (2001) DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J. Bacteriol. 183, 4562-4570.
63. Aslund, F., Zheng, M., Beckwith, J., and Storz, G. (1999) Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thiol-disulfide status. Proc. Natl. Acad. Sci. U.S.A. 96, 6161-6165.
64. Choi, H., Kim, S., Mukhopadhyay, P., Cho, S., Woo, J., Storz, G., and Ryu, S. (2001) Structural basis of the redox switch in the OxyR transcription factor. Cell 105, 103-113.
65. Kim, S. O., Merchant, K., Nudelman, R., Beyer, W. F., Jr., Keng, T., DeAngelo, J., Hausladen, A., and Stamler, J. S. (2002) OxyR: A molecular code for redox-related signaling. Cell 109, 383-396.
66. Claiborne, A., Yeh, J. I., Mallett, T. C., Luba, J., Crane, E. J., Charrier, V., and Parsonage, D. (1999) Protein-sulfenic acids: diverse roles for an unlikely player in enzyme catalysis and redox regulation. Biochemistry 38, 15407-15416.
67. Abate, C., Patel, L., Rauscher, I., and Curran, T. (1990) Redox regulation of fos and jun DNA-binding activity in vitro. Science 249, 1157-1161.
68. Xanthoudakis, S., Miao, G., Vang, F., Pan, Y.-C., and Curran, T. (1992) Redox activation of Fos-Jun DNA binding activity is mediated by a DNA repair enzyme. EMBO J. 11, 3323-3335.
69. Ellis, H. R., and Poole, L. B. (1997) Novel application of 7-chloro-4-nitrobenzo-2-oxa-1,3-diazole to identify cysteine sulfenic acid in the AhpC component of alkyl hydroperoxide reductase. Biochemistry 36, 15013-15018.
70. 2 receptor and redoxtransducer in gene activation. Cell 111, 471-481.
71. Barrett, W. C., DeGnore, J. P., Konig, S., Fales, H. M., Keng, Y. F., Zhang, Z. Y., Yim, M. B., and Chock, P. B. (1999) Regulation of PTP1B via glutathionylation of the active site cysteine 215. Biochemistry 38, 6699-6705.
72. +-dependent isocitrate dehydrogenase activity. Free Radical Res. 43, 409-416.
73. Silva, G. M., Netto, L. E., Discola, K. F., Piassa-Filho, G. M., Pimenta, D. C., Barcena, J. A., and Demasi, M. (2008) Role of glutaredoxin 2 and cytosolic thioredoxins in cysteinyl-based redox modification of the 20S proteasome. FEBS J. 275, 2942-2955.
74. Hidalgo, C., Sanchez, G., Barrientos, G., and Aracena-Parks, P. (2006) A transverse tubule NADPH oxidase activity stimulates calcium release from isolated triads via ryanodine receptor type 1S-glutathionylation. J. Biol. Chem. 281, 26473-26482.
75. Xie, Y., Kole, S., Precht, P., Pazin, M. J., and Bernier, M. (2009) S-Glutathionylation impairs signal transducer and activator of transcription 3 activation and signaling. Endocrinology 150, 1122-1131.
76. Huang, Z., Pinto, J. T., Deng, H., and Richie, J. P., Jr. (2008) Inhibition of caspase-3 activity and activation by protein glutathionylation. Biochem. Pharmacol. 75, 2234-2244.
77. Cruz, C. M., Rinna, A., Forman, H. J., Ventura, A. L., Persechini, P. M., and Ojcius, D. M. (2007) ATP activates a reactive oxygen species-dependent oxidative stress response and secretion of proinflammatory cytokines in macrophages. J. Biol. Chem. 282, 2871-2879.
78. Akerboom, T. P., Bilzer, M., and Sies, H. (1982) The relationship of biliary glutathione disulfide efflux and intracellular glutathione disulfide content in perfused rat liver. J. Biol. Chem. 257, 4248-4252.
79. Chakravarthi, S., Jessop, C. E., and Bulleid, N. J. (2006) The role of glutathione in disulphide bond formation and endoplasmic-reticulum-generated oxidative stress. EMBO Rep. 7, 271-275.
80. Saitoh, M., Nishitoh, H., Fujii, M., Takeda, K., Tobiume, K., Sawada, Y., Kawabata, M., Miyazono, K., and Ichijo, H. (1998) Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J. 17, 2596-2606.
81. Liu, H., Zhang, H., Iles, K. E., Rinna, A., Merrill, G., Yodoi, J., Torres, M., and Forman, H. J. (2006) The ADP-stimulated NADPH oxidase activates the ASK-1/MKK4/JNK pathway in alveolar macrophages. Free Radical Res. 40, 865-874.
82. Jeong, W., Chang, T. S., Boja, E. S., Fales, H. M., and Rhee, S. G. (2004) Roles of TRP14, a thioredoxin-related protein in tumor necrosis factor-R signaling pathways. J. Biol. Chem. 279, 3151-3159.
83. Denu, J. M., and Tanner, K. G. (1998) Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: Evidence for a sulfenic acid intermediate and implications for redox regulation. Biochemistry 37, 5633-5642.
84. Sohn, J., and Rudolph, J. (2003) Catalytic and chemical competence of regulation of cdc25 phosphatase by oxidation/reduction. Biochemistry 42, 10060-10070.
85. van Montfort, R. L., Congreve, M., Tisi, D., Carr, R., and Jhoti, H. (2003) Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B. Nature 423, 773-777.
86. Salmeen, A., Andersen, J. N., Myers, M. P., Meng, T. C., Hinks, J. A., Tonks, N. K., and Barford, D. (2003) Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature 423, 769-773.
87. Guengerich, F. P., Fang, Q., Liu, L., Hachey, D. L., and Pegg, A. E. (2003) O6-Alkylguanine-DNA alkyltransferase: Low pKa and high reactivity of cysteine 145. Biochemistry 42, 10965-10970.
88. Meister, A., Griffith, O. W., Novogrodsky, A., and Tate, S. S. (1979) New aspects of glutathione metabolism and translocation in mammals. Ciba Found. Symp., 135-161.
89. Skorey, K., Waddleton, D., Therien, M., and Leriche, T. (2006) Enzyme occupancy measurement of intracellular protein tyrosine phosphatase 1B using photoaffinity probes. Anal. Biochem. 349, 49-61.
90. Rinna, A., Torres, M., and Forman, H. J. (2006) Stimulation of the alveolar macrophage respiratory burst by ADP causes selective glutathionylation of protein tyrosine phosphatase 1B. Free Radical Biol. Med. 41, 86-91.
91. Biteau, B., Labarre, J., and Toledano, M. B. (2003) ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425, 980-984.
92. Chang, T. S., Jeong, W., Woo, H. A., Lee, S. M., Park, S., and Rhee, S. G. (2004) Characterization of mammalian sulfiredoxin and its reactivation of hyperoxidized peroxiredoxin through reduction of cysteine sulfinic acid in the active site to cysteine. J. Biol. Chem. 279, 50994-51001.
93. Phalen, T. J., Weirather, K., Deming, P. B., Anathy, V., Howe, A. K., van der Vliet, A., Jonsson, T. J., Poole, L. B., and Heintz, N. H. (2006) Oxidation state governs structural transitions in peroxiredoxin II that correlate with cell cycle arrest and recovery. J. Cell Biol. 175, 779-789.
94. Choi, M. H., Lee, I. K., Kim, G. W., Kim, B. U., Han, Y. H., Yu, D. Y., Park, H. S., Kim, K. Y., Lee, J. S., Choi, C., Bae, Y. S., Lee, B. I., Rhee, S. G., and Kang, S. W. (2005) Regulation of PDGF signalling and vascular remodelling by peroxiredoxin II. Nature 435, 347-353.
95. Veal, E. A., Findlay, V. J., Day, A. M., Bozonet, S. M., Evans, J. M., Quinn, J., and Morgan, B. A. (2004) A2-Cys peroxiredoxin regulates peroxide-induced oxidation and activation of a stress-activated MAP kinase. Mol. Cell 15, 129-139.
96. 2-terminal kinase signaling in lung cancer cells through interaction with the glutathione S-transferase Pi/c-Jun NH2-terminal kinase complex. Cancer Res. 66, 7136-7142.
97. Wen, S. T., and Van Etten, R. A. (1997) The PAG gene product, a stress-induced protein with antioxidant properties, is an Abl SH3-binding protein and a physiological inhibitor of c-Abl tyrosine kinase activity. Genes Dev. 11, 2456-2467.
98. Mu, Z. M., Yin, X. Y., and Prochownik, E. V. (2002) Pag, a putative tumor suppressor, interacts with the Myc Box II domain of c-Myc and selectively alters its biological function and target gene expression. J. Biol. Chem. 277, 43175-43184.
99. Maiorino, M., Chu, F. F., Ursini, F., Davies, K. J., Doroshow, J. H., and Esworthy, R. S. (1991) Phospholipid hydroperoxide glutathione peroxidase is the 18-kDa selenoprotein expressed in human tumor cell lines. J. Biol. Chem. 266, 7728-7732.
100. Chevallet, M., Wagner, E., Luche, S., van Dorsselaer, A., Leize-Wagner, E., and Rabilloud, T. (2003) Regeneration of peroxiredoxins during recovery after oxidative stress: only some over-oxidized peroxiredoxins can be reduced during recovery after oxidative stress. J. Biol. Chem. 278, 37146-37153.
101. Stone, J. R. (2004) An assessment of proposed mechanisms for sensing hydrogen peroxide in mammalian systems. Arch. Biochem. Biophys. 422, 119-124.