Nitration transforms a sensitive peroxiredoxin 2 into a more active and robust peroxidase

Journal of Biological Chemistry

Volumn 289, Issue 22, 2014, Pages 15536-15543

  Randall, Lía M ^a,b   Manta, Bruno ^a,c   Hugo, Martín ^b   Gil, Magdalena ^c,d   Batthyàny, Carlos ^b,c   Trujillo, Madia ^b   Poole, Leslie B ^e   Denicola, Ana ^a,b  

^a UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

^b DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

^c INSTITUT PASTEUR DE MONTEVIDEO   (Uruguay)

^d INSTITUTO DE INVESTIGACIONES BIOLÓGICAS CLEMENTE ESTABLE   (Uruguay)

^e WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; COVALENT BONDS;

DISULFIDE BOND FORMATION; IN-VITRO; IN-VIVO; OVEROXIDATIONS; POST-TRANSLATIONAL MODIFICATIONS; REACTIVE CYSTEINE; REDOX SIGNALING;

NITRATION;

PEROXIDASE; PEROXIREDOXIN 2;

ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME KINETICS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MASS SPECTROMETRY; NITRATION; OXIDATION; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEOMICS; SIGNAL TRANSDUCTION;

HYDROGEN PEROXIDE; OVEROXIDATION; OXIDATIVE STRESS; PEROXIREDOXIN; PEROXYNITRITE; POST-TRANSLATIONAL MODIFICATION; REDOX SIGNALING; TYROSINE NITRATION;

ANIMALS; CATALYTIC DOMAIN; ECHINOCOCCUS GRANULOSUS; ENZYME ACTIVATION; ERYTHROCYTES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HOMEODOMAIN PROTEINS; HUMANS; HYDROGEN PEROXIDE; NITROGEN; OXIDATION-REDUCTION; OXIDATIVE STRESS; PEROXYNITROUS ACID; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; THIOREDOXINS; TYROSINE;

EID: 84901717301     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.539213     Document Type: Article

References (58)

1. Rhee, S. G., Chae, H. Z., and Kim, K. (2005) Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic. Biol. Med. 38, 1543-1552
2. Wood, Z. A., Poole, L. B., and Karplus, P. A. (2003) Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300, 650-653
3. Wood, Z. A., Schröder, E., Robin Harris, J., and Poole, L. B. (2003) Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 28, 32-40
4. Hofmann, B., Hecht, H. J., and Flohé, L. (2002) Peroxiredoxins. Biol. Chem. 383, 347-364
5. Copley, S. D., Novak, W. R., and Babbitt, P. C. (2004) Divergence of function in the thioredoxin fold suprafamily: evidence for evolution of peroxiredoxins from a thioredoxin-like ancestor. Biochemistry 43, 13981-13995
6. Schröder, E., Littlechild, J. A., Lebedev, A. A., Errington, N., Vagin, A. A., and Isupov, M. N. (2000) Crystal structure of decameric 2-Cys peroxiredoxin from human erythrocytes at 1.7 A resolution. Structure 8, 605-615
7. Wood, Z. A., Poole, L. B., Hantgan, R. R., and Karplus, P. A. (2002) Dimers to doughnuts: redox-sensitive oligomerization of 2-cysteine peroxiredoxins. Biochemistry 41, 5493-5504
8. Perkins, A., Nelson, K. J., Williams, J. R., Parsonage, D., Poole, L. B., and Karplus, P. A. (2013) The sensitive balance between fully folded and locally unfolded conformations of a model peroxiredoxin. Biochemistry 52, 8708-8721
9. Biteau, B., Labarre, J., and Toledano, M. B. (2003) ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425, 980-984
10. Jönsson, T. J., Murray, M. S., Johnson, L. C., and Lowther, W. T. (2008) Reduction of cysteine sulfinic acid in peroxiredoxin by sulfiredoxin proceeds directly through a sulfinic phosphoryl ester intermediate. J. Biol. Chem. 283, 23846-23851
11. Winterbourn, C. C., and Hampton, M. B. (2008) Thiol chemistry and specificity in redox signaling. Free Radic. Biol. Med. 45, 549-561
12. Flohé, L., and Ursini, F. (2008) Peroxidase: a term of many meanings. Antioxid. Redox Signal. 10, 1485-1490
13. Ferrer-Sueta, G., Manta, B., Botti, H., Radi, R., Trujillo, M., and Denicola, A. (2011) Factors affecting protein thiol reactivity and specificity in peroxide reduction. Chem. Res. Toxicol. 24, 434-450
14. 2-induced signaling. Methods Enzymol. 527, 41-63
15. 2: a quantitative comparison between continuous low-dose and one-time high-dose treatments. Free Radic. Biol. Med. 60, 325-335
16. Lowther, W. T, and Haynes, A. C. (2011) Reduction of cysteine sulfinic acid in eukaryotic, typical 2-Cys peroxiredoxins by sulfiredoxin. Antioxid. Redox Signal. 15, 99-109
17. Moore, R. B., Mankad, M. V., Shriver, S. K., Mankad, V. N., and Plishker, G. A. (1991) Reconstitution of Ca2-dependent K transport in erythrocyte membrane vesicles requires a cytoplasmic protein. J. Biol. Chem. 266, 18964-18968
18. Cho, C. S., Kato, G. J., Yang, S. H., Bae, S. W., Lee, J. S., Gladwin, M. T., and Rhee, S. G. (2010) Hydroxyurea-induced expression of glutathione peroxidase 1 in red blood cells of individuals with sickle cell anemia. Antioxid. Redox Signal. 13, 1-11
19. Manta, B., Hugo, M., Ortiz, C., Ferrer-Sueta, G., Trujillo, M., and Denicola, A. (2009) The peroxidase and peroxynitrite reductase activity of human erythrocyte peroxiredoxin 2. Arch. Biochem. Biophys. 484, 146-154
20. Reed, T. T., Pierce, W. M., Jr., Turner, D. M., Markesbery, W. R., and Butterfield, D. A. (2009) Proteomic identification of nitrated brain proteins in early Alzheimer's disease inferior parietal lobule. J. Cell. Mol. Med. 13, 2019-2029
21. Denicola, A., Alvarez, B., and Thomson, L. (2008) Free Radical Pathophysiology (Alvarez, S. and Evelson, P., eds) pp. 39-55, Transworld Research Network, India
22. Radi, R. (2004) Nitric oxide, oxidants, and protein tyrosine nitration. Proc. Natl. Acad. Sci. U.S.A. 101, 4003-4008
23. Trujillo, M., Ferrer-Sueta, G., and Radi, R. (2008) Peroxynitrite detoxification and its biologic implications. Antioxid. Redox Signal. 10, 1607-1620
24. Trujillo, M., Alvarez, B., Souza, J. M., Romero, N., Castro, L., Thomson, L., and Radi, R. (2010) Nitric Oxide Biology and Pathobiology (Ignarro, L. J., ed) pp. 61-102, Academic Press, Orlando, FL
25. Beckman, J. S., Beckman, T. W., Chen, J., Marshall, P. A., and Freeman, B. A. (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. U.S.A. 87, 1620-1624
26. Romero, N., Radi, R., Linares, E., Augusto, O., Detweiler, C. D., Mason, R. P., and Denicola, A. (2003) Reaction of human hemoglobin with peroxynitrite: isomerization to nitrate and secondary formation of protein radicals. J. Biol. Chem. 278, 44049-44057
27. Poole, L. B., Godzik, A., Nayeem, A., and Schmitt, J. D. (2000) AhpF can be dissected into two functional units: tandem repeats of two thioredoxinlike folds in the N-terminus mediate electron transfer from the thioredoxin reductase-like C-terminus to AhpC. Biochemistry 39, 6602-6615
28. Bonilla, M., Denicola, A., Marino, S. M., Gladyshev, V. N., and Salinas, G. (2011) Linked thioredoxin-glutathione systems in platyhelminth parasites: alternative pathways for glutathione reduction and deglutathionylation. J. Biol. Chem. 286, 4959-4967
29. Pace, C. N., Vajdos, F., Fee, L., Grimsley, G., and Gray, T. (1995) How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 4, 2411-2423
30. Egwim, I. O., and Gruber, H. J. (2001) Spectrophotometric measurement of mercaptans with 4,4′-dithiodipyridine. Anal. Biochem. 288, 188-194
31. Brito, C., Naviliat, M., Tiscornia, A. C., Vuillier, F., Gualco, G., Dighiero, G., Radi, R., and Cayota, A. M. (1999) Peroxynitrite inhibits T lymphocyte activation and proliferation by promoting impairment of tyrosine phosphorylation and peroxynitrite-driven apoptotic death. J. Immunol. 162, 3356-3366
32. Jörnvall, H., and Jollès, P. (2000) Protein structure analysis of today: proteomics in functional genomics. EXS 88, XI-XIII
33. Peskin, A. V., Dickerhof, N., Poynton, R. A., Paton, L. N., Pace, P. E., Hampton, M. B., and Winterbourn, C. C. (2013) Hyperoxidation of peroxiredoxins 2 and 3: rate constants for the reactions of the sulfenic acid of the peroxidatic cysteine. J. Biol. Chem. 288, 14170-14177
34. Nelson, K. J., Parsonage, D., Karplus, P. A., and Poole, L. B. (2013) Evaluating peroxiredoxin sensitivity toward inactivation by peroxide substrates. Methods Enzymol. 527, 21-40
35. Haynes, A. C., Qian, J., Reisz, J. A., Furdui, C. M., and Lowther, W. T. (2013) Molecular basis for the resistance of human mitochondrial 2-Cys peroxiredoxin 3 to hyperoxidation. J. Biol. Chem. 288, 29714-29723
36. Yuan, Y., Knaggs, M., Poole, L., Fetrow, J., and Salsbury, F., Jr. (2010) Conformational and oligomeric effects on the cysteine pKa of tryparedoxin peroxidase. J. Biomol. Struct. Dyn. 28, 51-70
37. Salsbury, F. R., Jr., Yuan, Y., Knaggs, M. H., Poole, L. B., and Fetrow, J. S. (2012) Structural and electrostatic asymmetry at the active site in typical and atypical peroxiredoxin dimers. J. Phys. Chem. B 116, 6832-6843
38. Budde, H., Flohé, L., Hecht, H. J., Hofmann, B., Stehr, M., Wissing, J., and Lünsdorf, H. (2003) Kinetics and redox-sensitive oligomerisation reveal negative subunit cooperativity in tryparedoxin peroxidase of Trypanosoma brucei brucei. Biol. Chem. 384, 619-633
39. 2 is not reflected in its reaction with other oxidants and thiol reagents. J. Biol. Chem. 282, 11885-11892
40. Fomenko, D. E., Koc, A., Agisheva, N., Jacobsen, M., Kaya, A., Malinouski, M., Rutherford, J. C., Siu, K. L., Jin, D. Y., Winge, D. R., and Gladyshev, V. N. (2011) Thiol peroxidases mediate specific genome-wide regulation of gene expression in response to hydrogen peroxide. Proc. Natl. Acad. Sci. U.S.A. 108, 2729-2734
41. Oláhová, M, Taylor, S. R., Khazaipoul, S., Wang, J., Morgan, B. A., Matsumoto, K., Blackwell, T. K., and Veal, E. A. (2008) A redox-sensitive peroxiredoxin that is important for longevity has tissue- and stress-specific roles in stress resistance. Proc. Natl. Acad. Sci. U.S.A. 105, 19839-19844
42. Day, A. M., Brown, J. D., Taylor, S. R., Rand, J. D., Morgan, B. A., and Veal, E. A. (2012) Inactivation of a peroxiredoxin by hydrogen peroxide is critical for thioredoxin-mediated repair of oxidized proteins and cell survival. Mol. Cell 45, 398-408
43. Veal, E. A., Day, A. M., and Morgan, B. A. (2007) Hydrogen peroxide sensing and signaling. Mol. Cell 26, 1-14
44. 2, a necessary evil for cell signaling. Science 312, 1882-1883
45. Koo, K. H., Lee, S., Jeong, S. Y., Kim, E. T., Kim, H. J., Kim, K., Song, K., and Chae, H. Z. (2002) Regulation of thioredoxin peroxidase activity by C-ter- minal truncation. Arch. Biochem. Biophys. 397, 312-318
46. Sayed, A. A., and Williams, D. L. (2004) Biochemical characterization of 2-Cys peroxiredoxins from Schistosoma mansoni. J. Biol. Chem. 279, 26159-26166
47. Ghesquière, B., Colaert, N., Helsens, K., Dejager, L., Vanhaute, C., Verleysen, K., Kas, K., Timmerman, E., Goethals, M., Libert, C., Vandekerckhove, J., and Gevaert, K. (2009) In vitro and in vivo protein-bound tyrosine nitration characterized by diagonal chromatography. Mol. Cell. Proteomics 8, 2642-2652
48. Park, J. W., Piszczek, G., Rhee, S. G., and Chock, P. B. (2011) Glutathionylation of peroxiredoxin I induces decamer to dimers dissociation with concomitant loss of chaperone activity. Biochemistry 50, 3204-3210
49. Fang, J., Nakamura, T., Cho, D. H., Gu, Z., and Lipton, S. A. (2007) SNitrosylation of peroxiredoxin 2 promotes oxidative stress-induced neuronal cell death in Parkinson's disease. Proc. Natl. Acad. Sci. U.S.A. 104, 18742-18747
50. Engelman, R., Weisman-Shomer, P., Ziv, T., Xu, J., Arnér, E. S., and Benhar, M. (2013) Multilevel regulation of 2-Cys peroxiredoxin reaction cycle by S-nitrosylation. J. Biol. Chem. 288, 11312-11324
51. Jang, H. H., Kim, S. Y., Park, S. K., Jeon, H. S., Lee, Y. M., Jung, J. H., Lee, S. Y., Chae, H. B., Jung, Y. J., Lee, K. O., Lim, C. O., Chung, W. S., Bahk, J. D., Yun, D. J., Cho, M. J., and Lee, S. Y. (2006) Phosphorylation and concomitant structural changes in human 2-Cys peroxiredoxin isotype I differentially regulate its peroxidase and molecular chaperone functions. FEBS Lett. 580, 351-355
52. 2 accumulation for cell signaling. Cell 140, 517-528
53. Zykova, T. A., Zhu, F., Vakorina, T. I., Zhang, J., Higgins, L. A., Urusova, D. V., Bode, A. M., and Dong, Z. (2010) T-LAK cell-originated protein kinase (TOPK) phosphorylation of Prx1 at Ser-32 prevents UVB-induced apoptosis in RPMI7951 melanoma cells through the regulation of Prx1 peroxidase activity. J. Biol. Chem. 285, 29138-29146
54. Chang, T. S., Jeong, W., Choi, S. Y., Yu, S., Kang, S. W., and Rhee, S. G. (2002) Regulation of peroxiredoxin I activity by Cdc2-mediated phosphorylation. J. Biol. Chem. 277, 25370-25376
55. Parmigiani, R. B., Xu, W. S., Venta-Perez, G., Erdjument-Bromage, H., Yaneva, M., Tempst, P., and Marks, P. A. (2008) HDAC6 is a specific deacetylase of peroxiredoxins and is involved in redox regulation. Proc. Natl. Acad. Sci. U.S.A. 105, 9633-9638
56. Perry, G., Raina, A. K., Nunomura, A., Wataya, T., Sayre, L. M., and Smith, M. A. (2000) How important is oxidative damage? Lessons from Alzheimer's disease. Free Radic. Biol. Med. 28, 831-834
57. Leite, P. F., Liberman, M., Sandoli de Brito, F., and Laurindo, F. R. (2004) Redox processes underlying the vascular repair reaction. World J. Surg. 28, 331-336
58. Turko, I. V., Li, L., Aulak, K. S., Stuehr, D. J., Chang, J. Y., and Murad, F. (2003) Protein tyrosine nitration in the mitochondria from diabetic mouse heart: implications to dysfunctional mitochondria in diabetes. J. Biol. Chem. 278, 33972-33977