Reconstitution of the Mitochondrial PrxIII Antioxidant Defence Pathway: General Properties and Factors Affecting PrxIII Activity and Oligomeric State

Journal of Molecular Biology

Volumn 372, Issue 4, 2007, Pages 1022-1033

  Cao, Zhenbo ^a   Bhella, David ^b   Lindsay, J Gordon ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b INSTITUTE OF VIROLOGY   (United Kingdom)

Author keywords

mitochondrial; oligomeric state; overoxidation; peroxiredoxin; ROS

Indexed keywords

ANTIOXIDANT; HYDROGEN PEROXIDE; PEROXIDE; PEROXIREDOXIN; PEROXIREDOXIN PRXIII; REACTIVE OXYGEN METABOLITE; THIOREDOXIN; THIOREDOXIN REDUCTASE; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; MITOCHONDRION; OXIDATION REDUCTION STATE; PEROXIDATION; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION; TRANSMISSION ELECTRON MICROSCOPY;

MAMMALIA;

EID: 34548439447     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.07.018     Document Type: Article

References (43)

1. Boveris A., and Chance B. The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem. J. 134 (1973) 707-716
2. Cadenas E., Boveris A., Ragan C.I., and Stoppani A.O. Production of superoxide radicals and hydrogen peroxide by NADH-ubiquinone reductase and ubiquinol-cytochrome c reductase from beef-heart mitochondria. Arch. Biochem. Biophys. 180 (1977) 248-257
3. Turrens J.F. Superoxide production by the mitochondrial respiratory chain. Biosci. Rep. 17 (1997) 3-8
4. Starkov A.A., Fiskum G., Chinopoulos C., Lorenzo B.J., Browne S.E., Patel M.S., and Beal M.F. Mitochondrial alpha-ketoglutarate dehydrogenase complex generates reactive oxygen species. J. Neurosci. 24 (2004) 7779-7788
5. Li Y., Huang T.T., Carlson E.J., Melov S., Ursell P. C., Olson J.L., et al. Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nature Genet. 11 (1995) 376-381
6. Lebovitz R.M., Zhang H., Vogel H., Cartwright Jr. J., Dionne L., Lu N., et al. Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proc. Natl Acad. Sci. USA 93 (1996) 9782-9787
7. Van Remmen H., Williams M.D., Guo Z., Estlack L., Yang H., Carlson E.J., et al. Knockout mice heterozygous for Sod2 show alterations in cardiac mitochondrial function and apoptosis. Am. J. Physiol. Heart Circ. Physiol. 281 (2001) H1422-H1432
8. Radi R., Turrens J.F., Chang L.Y., Bush K.M., Crapo J.D., and Freeman B.A. Detection of catalase in rat heart mitochondria. J. Biol. Chem. 266 (1991) 22028-22034
9. Panfili E., Sandri G., and Ernster L. Distribution of glutathione peroxidases and glutathione reductase in rat brain mitochondria. FEBS Letters 290 (1991) 35-37
10. Esworthy R.S., Ho Y.S., and Chu F.F. The Gpx1 gene encodes mitochondrial glutathione peroxidase in the mouse liver. Arch. Biochem. Biophys. 340 (1997) 59-63
11. Ho Y.S., Magnenat J.L., Bronson R.T., Cao J., Gargano M., Sugawara M., and Funk C.D. Mice deficient in cellular glutathione peroxidase develop normally and show no increased sensitivity to hyperoxia. J. Biol. Chem. 272 (1997) 16644-16651
12. Legault J., Carrier C., Petrov P., Renard P., Remacle J., and Mirault M.E. Mitochondrial GPx1 decreases induced but not basal oxidative damage to mtDNA in T47D cells. Biochem. Biophys. Res. Commun. 272 (2000) 416-422
13. Wood Z.A., Poole L.B., and Karplus P.A. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300 (2003) 650-653
14. Link A.J., Robison K., and Church G.M. Comparing the predicted and observed properties of proteins encoded in the genome of Escherichia coli K-12. Electrophoresis 18 (1997) 1259-1313
15. Chae H.Z., Kim H.J., Kang S.W., and Rhee S.G. Characterization of three isoforms of mammalian peroxiredoxin that reduce peroxides in the presence of thioredoxin. Diabetes Res. Clin. Pract. 45 (1999) 101-112
16. Bryk R., Griffin P., and Nathan C. Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407 (2000) 211-215
17. Seo M.S., Kang S.W., Kim K., Baines I.C., Lee T.H., and Rhee S.G. Identification of a new type of mammalian peroxiredoxin that forms an intramolecular disulfide as a reaction intermediate. J. Biol. Chem. 275 (2000) 20346-20354
18. Gourlay L.J., Bhella D., Kelly S.M., Price N.C., and Lindsay J.G. Structure-function analysis of recombinant substrate protein 22 kDa (SP-22). A mitochondrial 2-CYS peroxiredoxin organized as a decameric toroid. J. Biol. Chem. 278 (2003) 32631-32637
19. Cao Z., Roszak A.W., Gourlay L.J., Lindsay J.G., and Isaacs N.W. Bovine mitochondrial peroxiredoxin III forms a two-ring catenane. Structure (Camb.) 13 (2005) 1661-1664
20. Guimaraes B.G., Souchon H., Honore N., Saint-Joanis B., Brosch R., Shepard W., et al. Structure and mechanism of the alkyl hydroperoxidase AhpC, a key element of the Mycobacterium tuberculosis defense system against oxidative stress. J. Biol. Chem. 280 (2005) 25735-25742
21. Holmgren A. Thioredoxin structure and mechanism: conformational changes on oxidation of the active-site sulfhydryls to a disulfide. Structure 3 (1995) 239-243
22. Stadtman T.C. Selenocysteine. Annu. Rev. Biochem. 65 (1996) 83-100
23. Tamura T., and Stadtman T.C. A new selenoprotein from human lung adenocarcinoma cells: purification, properties, and thioredoxin reductase activity. Proc. Natl Acad. Sci. USA 93 (1996) 1006-1011
24. Jang H.H., Lee K.O., Chi Y.H., Jung B.G., Park S. K., Park J.H., et al. Two enzymes in one; two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function. Cell 117 (2004) 625-635
25. Meissner U., Schroder E., Scheffler D., Martin A.G., and Harris J.R. Formation, TEM study and 3D reconstruction of the human erythrocyte peroxiredoxin-2 dodecahedral higher-order assembly. Micron 38 (2007) 29-39
26. Watabe S., Hiroi T., Yamamoto Y., Fujioka Y., Hasegawa H., Yago N., and Takahashi S.Y. SP-22 is a thioredoxin-dependent peroxide reductase in mitochondria. Eur. J. Biochem. 249 (1997) 52-60
27. Araki M., Nanri H., Ejima K., Murasato Y., Fujiwara T., Nakashima Y., and Ikeda M. Antioxidant function of the mitochondrial protein SP-22 in the cardiovascular system. J. Biol. Chem. 274 (1999) 2271-2278
28. Chang T.S., Cho C.S., Park S., Yu S., Kang S.W., and Rhee S.G. Peroxiredoxin III, a mitochondrion-specific peroxidase, regulates apoptotic signaling by mitochondria. J. Biol. Chem. 279 (2004) 41975-41984
29. Zhou Y., Kok K.H., Chun A.C., Wong C.M., Wu H. W., Lin M.C., et al. Mouse peroxiredoxin V is a thioredoxin peroxidase that inhibits p53-induced apoptosis. Biochem. Biophys. Res. Commun. 268 (2000) 921-927
30. Banmeyer I., Marchand C., Clippe A., and Knoops B. Human mitochondrial peroxiredoxin 5 protects from mitochondrial DNA damages induced by hydrogen peroxide. FEBS Letters 579 (2005) 2327-2333
31. Arner E.S., Sarioglu H., Lottspeich F., Holmgren A., and Bock A. High-level expression in Escherichia coli of selenocysteine-containing rat thioredoxin reductase utilizing gene fusions with engineered bacterial-type SECIS elements and co-expression with the selA, selB and selC genes. J. Mol. Biol. 292 (1999) 1003-1016
32. Gorlatov S.N., and Stadtman T.C. Human thioredoxin reductase from HeLa cells: selective alkylation of selenocysteine in the protein inhibits enzyme activity and reduction with NADPH influences affinity to heparin. Proc. Natl Acad. Sci. USA 95 (1998) 8520-8525
33. Zhong L., and Holmgren A. Essential role of selenium in the catalytic activities of mammalian thioredoxin reductase revealed by characterization of recombinant enzymes with selenocysteine mutations. J. Biol. Chem. 275 (2000) 18121-18128
34. Yang K.S., Kang S.W., Woo H.A., Hwang S.C., Chae H.Z., Kim K., and Rhee S.G. Inactivation of human peroxiredoxin I during catalysis as the result of the oxidation of the catalytic site cysteine to cysteine-sulfinic acid. J. Biol. Chem. 277 (2002) 38029-38036
35. Woo H.A., Chae H.Z., Hwang S.C., Yang K.S., Kang S.W., Kim K., and Rhee S.G. Reversing the inactivation of peroxiredoxins caused by cysteine sulfinic acid formation. Science 300 (2003) 653-656
36. Biteau B., Labarre J., and Toledano M.B. ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425 (2003) 980-984
37. Kitano K., Niimura Y., Nishiyama Y., and Miki K. Stimulation of peroxidase activity by decamerization related to ionic strength: AhpC protein from Amphibacillus xylanus. J. Biochem. (Tokyo) 126 (1999) 313-319
38. Kristensen P., Rasmussen D.E., and Kristensen B.I. Properties of thiol-specific anti-oxidant protein or calpromotin in solution. Biochem. Biophys. Res. Commun. 262 (1999) 127-131
39. Chauhan R., and Mande S.C. Characterization of the Mycobacterium tuberculosis H37Rv alkyl hydroperoxidase AhpC points to the importance of ionic interactions in oligomerization and activity. Biochem. J. 354 (2001) 209-215
40. Wood Z.A., Poole L.B., Hantgan R.R., and Karplus P. A. Dimers to doughnuts: redox-sensitive oligomerization of 2-cysteine peroxiredoxins. Biochemistry 41 (2002) 5493-5504
41. Wood Z.A., Schroder E., Robin Harris J., and Poole L.B. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 28 (2003) 32-40
42. Parsonage D., Youngblood D.S., Sarma G.N., Wood Z.A., Karplus P.A., and Poole L.B. Analysis of the link between enzymatic activity and oligomeric state in AhpC, a bacterial peroxiredoxin. Biochemistry 44 (2005) 10583-10592
43. Lee B.I., Kim K.H., Park S.J., Eom S.H., Song H.K., and Suh S.W. Ring-shaped architecture of RecR: implications for its role in homologous recombinational DNA repair. EMBO J. 23 (2004) 2029-2038