Mitochondrial targeting of peroxiredoxin 5 is preserved from annelids to mammals but is absent in pig Sus scrofa domesticus

Mitochondrion

Volumn 11, Issue 6, 2011, Pages 973-981

  Van der Eecken, Valérie ^a   Clippe, André ^a   Van Veldhoven, Paul P ^b   Knoops, Bernard ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Annelids; Mammals; Mitochondrion; Peroxiredoxin; Subcellular targeting

Indexed keywords

PEROXIREDOXIN 5;

ANIMAL CELL; ANIMAL TISSUE; ANNELID WORM; ARENICOLA MARINA; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOMESTIC PIG; ENZYME LOCALIZATION; HUMAN; HUMAN CELL; LIVER HOMOGENATE; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; RAT;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL EVOLUTION; HUMANS; MAMMALS; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; PEROXIREDOXINS; POLYCHAETA; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT;

ANIMALIA; ANNELIDA; ARENICOLA MARINA; MAMMALIA; SUIDAE; SUS SCROFA DOMESTICA;

EID: 82755193704     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2011.06.013     Document Type: Article

References (49)

1. Arai M., Imai H., Sumi D., Imanaka T., Takano T., Chiba N., Nakagawa Y. Import into mitochondria of phospholipid hydroperoxide glutathione peroxidase requires a leader sequence. Biochem. Biophys. Res. Commun. 1996, 227:433-439.
2. Araki M., Nanri H., Ejima K., Murasato Y., Fujiwara T., Nakashima Y., Ikeda M. Antioxidant function of the mitochondrial protein SP-22 in the cardiovascular system. J. Biol. Chem. 1999, 274:2271-2278.
3. Asayama K., Yokota S., Dobashi K., Hayashibe H., Kawaoi A., Nakazawa S. Purification and immunoelectron microscopic localization of cellular glutathione peroxidase in rat hepatocytes: quantitative analysis by postembedding method. Histochemistry 1994, 102:213-219.
4. Banmeyer I., Marchand C., Clippe A., Knoops B. Human mitochondrial peroxiredoxin 5 protects from mitochondrial DNA damages induced by hydrogen peroxide. FEBS Lett. 2005, 579:2327-2333.
5. Banmeyer I., Marchand C., Verhaeghe C., Vucic B., Rees J.F., Knoops B. Overexpression of human peroxiredoxin 5 in subcellular compartments of Chinese hamster ovary cells: effects on cytotoxicity and DNA damage caused by peroxides. Free Radic. Biol. Med. 2004, 36:65-77.
6. Birdsey G.M., Lewin J., Cunningham A.A., Bruford M.W., Danpure C.J. Differential enzyme targeting as an evolutionary adaptation to herbivory in carnivora. Mol. Biol. Evol. 2004, 21:632-646.
7. Cox A.G., Winterbourn C.C., Hampton M.B. Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling. Biochem. J. 2010, 425:313-325.
8. De Simoni S., Goemaere J., Knoops B. Silencing of peroxiredoxin 3 and peroxiredoxin 5 reveals the role of mitochondrial peroxiredoxins in the protection of human neuroblastoma SH-SY5Y cells toward MPP+. Neurosci. Lett. 2008, 433:219-224.
9. Declercq P.E., Haagsman H.P., Van Veldhoven P., Debeer L.J., Van Golde L.M., Mannaerts G.P. Rat liver dihydroxyacetone-phosphate acyltransferases and their contribution to glycerolipid synthesis. J. Biol. Chem. 1984, 259:9064-9075.
10. Dubuisson M., Vander Stricht D., Clippe A., Etienne F., Nauser T., Kissner R., Koppenol W.H., Rees J.F., Knoops B. Human peroxiredoxin 5 is a peroxynitrite reductase. FEBS Lett. 2004, 571:161-165.
11. Emanuelsson O., Nielsen H., Brunak S., von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 2000, 300:1005-1016.
12. Esworthy R.S., Ho Y.S., Chu F.F. The Gpx1 gene encodes mitochondrial glutathione peroxidase in the mouse liver. Arch. Biochem. Biophys. 1997, 340:59-63.
13. Herbette S., Roeckel-Drevet P., Drevet J.R. Seleno-independent glutathione peroxidases - more than simple antioxidant scavengers. FEBS J. 2007, 274:2163-2180.
14. Holbrook J.D., Birdsey G.M., Yang Z., Bruford M.W., Danpure C.J. Molecular adaptation of alanine:glyoxylate aminotransferase targeting in primates. Mol. Biol. Evol. 2000, 17:387-400.
15. Jezek P., Hlavata L. Mitochondria in homeostasis of reactive oxygen species in cell, tissues, and organism. Int. J. Biochem. Cell Biol. 2005, 37:2478-2503.
16. Kinnula V.L., Lehtonen S., Sormunen R., Kaarteenaho-Wiik R., Kang S.W., Rhee S.G., Soini Y. Overexpression of peroxiredoxins I, II, III, V, and VI in malignant mesothelioma. J. Pathol. 2002, 196:316-323.
17. Knoops B., Clippe A., Bogard C., Arsalane K., Wattiez R., Hermans C., Duconseille E., Falmagne P., Bernard A. Cloning and characterization of AOEB166, a novel mammalian antioxidant enzyme of the peroxiredoxin family. J. Biol. Chem. 1999, 274:30451-30458.
18. Knoops B., Goemaere J., Van der Eecken V., Declercq J.P. Peroxiredoxin 5: structure, mechanism and function of the mammalian atypical 2-Cys peroxiredoxin. Antioxid. Redox. Signal 2011, 15:817-829.
19. Kropotov A., Sedova V., Ivanov V., Sazeeva N., Tomilin A., Krutilina R., Oei S.L., Griesenbeck J., Buchlow G., Tomilin N. A novel human DNA-binding protein with sequence similarity to a subfamily of redox proteins which is able to repress RNA-polymerase-III-driven transcription of the Alu-family retroposons in vitro. Eur. J. Biochem. 1999, 260:336-346.
20. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
21. Legault J., Carrier C., Petrov P., Renard P., Remacle J., Mirault M.E. Mitochondrial GPx1 decreases induced but not basal oxidative damage to mtDNA in T47D cells. Biochem. Biophys. Res. Commun. 2000, 272:416-422.
22. Leyens G., Knoops B., Donnay I. Expression of peroxiredoxins in bovine oocytes and embryos produced in vitro. Mol. Reprod. Dev. 2004, 69:243-251.
23. Li J., Li L., Zhang S., Zhang G. Cloning, genomic structure, and expression analysis of peroxiredoxin V from bay scallop Argopecten irradians. Fish. Shellfish. Immunol 2011, 30:309-316.
24. Lu J.L., Vallat J.M., Pollard J.D., Knoops B., Ouvrier R. Expression of the antioxidant enzyme peroxiredoxin 5 in the human peripheral nervous system. J. Peripher. Nerv. Syst. 2006, 11:318-324.
25. Mowbray A.L., Kang D.H., Rhee S.G., Kang S.W., Jo H. Laminar shear stress up-regulates peroxiredoxins (PRX) in endothelial cells: PRX 1 as a mechanosensitive antioxidant. J. Biol. Chem. 2008, 283:1622-1627.
26. Nguyen-Nhu N.T., Berck J., Clippe A., Duconseille E., Cherif H., Boone C., Van der Eecken V., Bernard A., Banmeyer I., Knoops B. Human peroxiredoxin 5 gene organization, initial characterization of its promoter and identification of alternative forms of mRNA. Biochim. Biophys. Acta 2007, 1769:472-483.
27. Nguyen-nhu N.T., Knoops B. Mitochondrial and cytosolic expression of human peroxiredoxin 5 in Saccharomyces cerevisiae protect yeast cells from oxidative stress induced by paraquat. FEBS Lett. 2003, 544:148-152.
28. Nielsen H., Engelbrecht J., Brunak S., von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 1997, 10:1-6.
29. Oberley T.D., Verwiebe E., Zhong W., Kang S.W., Rhee S.G. Localization of the thioredoxin system in normal rat kidney. Free Radic. Biol. Med. 2001, 30:412-424.
30. Pagliarini D.J., Calvo S.E., Chang B., Sheth S.A., Vafai S.B., Ong S.E., Walford G.A., Sugiana C., Boneh A., Chen W.K., Hill D.E., Vidal M., Evans J.G., Thorburn D.R., Carr S.A., Mootha V.K. A mitochondrial protein compendium elucidates complex I disease biology. Cell 2008, 134:112-123.
31. Panfili E., Sandri G., Ernster L. Distribution of glutathione peroxidases and glutathione reductase in rat brain mitochondria. FEBS Lett. 1991, 290:35-37.
32. Peng Y., Yang P.H., Guo Y., Ng S.S., Liu J., Fung P.C., Tay D., Ge J., He M.L., Kung H.F., Lin M.C. Catalase and peroxiredoxin 5 protect Xenopus embryos against alcohol-induced ocular anomalies. Invest. Ophthalmol. Vis. Sci. 2004, 45:23-29.
33. Peng Y., Yang P.H., Ng S.S., Lum C.T., Kung H.F., Lin M.C. Protection of Xenopus laevis embryos against alcohol-induced delayed gut maturation and growth retardation by peroxiredoxin 5 and catalase. J. Mol. Biol. 2004, 340:819-827.
34. Radyuk S.N., Michalak K., Klichko V.I., Benes J., Rebrin I., Sohal R.S., Orr W.C. Peroxiredoxin 5 confers protection against oxidative stress and apoptosis and also promotes longevity in Drosophila. Biochem. J. 2009, 419:437-445.
35. Rhee S.G., Chae H.Z., Kim K. Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic. Biol. Med. 2005, 38:1543-1552.
36. Schneider M., Forster H., Boersma A., Seiler A., Wehnes H., Sinowatz F., Neumuller C., Deutsch M.J., Walch A., Hrabe de Angelis M., Wurst W., Ursini F., Roveri A., Maleszewski M., Maiorino M., Conrad M. Mitochondrial glutathione peroxidase 4 disruption causes male infertility. FASEB J. 2009, 23:3233-3242.
37. Seiler A., Schneider M., Forster H., Roth S., Wirth E.K., Culmsee C., Plesnila N., Kremmer E., Radmark O., Wurst W., Bornkamm G.W., Schweizer U., Conrad M. Glutathione peroxidase 4 senses and translates oxidative stress into 12/15-lipoxygenase dependent- and AIF-mediated cell death. Cell Metab. 2008, 8:237-248.
38. Seo M.S., Kang S.W., Kim K., Baines I.C., Lee T.H., Rhee S.G. Identification of a new type of mammalian peroxiredoxin that forms an intramolecular disulfide as a reaction intermediate. J. Biol. Chem. 2000, 275:20346-20354.
39. Trujillo M., Clippe A., Manta B., Ferrer-Sueta G., Smeets A., Declercq J.P., Knoops B., Radi R. Pre-steady state kinetic characterization of human peroxiredoxin 5: taking advantage of Trp84 fluorescence increase upon oxidation. Arch. Biochem. Biophys. 2007, 467:95-106.
40. Ursini F., Heim S., Kiess M., Maiorino M., Roveri A., Wissing J., Flohe L. Dual function of the selenoprotein PHGPx during sperm maturation. Science 1999, 285:1393-1396.
41. Usmanova N., Tomilin N., Zhivotovsky B., Kropotov A. Transcription factor GABP/NRF-2 controlling biogenesis of mitochondria regulates basal expression of peroxiredoxin V but the mitochondrial function of peroxiredoxin V is dispensable in the dog. Biochimie 2011, 93:306-313.
42. Utsunomiya H., Komatsu N., Yoshimura S., Tsutsumi Y., Watanabe K. Exact ultrastructural localization of glutathione peroxidase in normal rat hepatocytes: advantages of microwave fixation. J. Histochem. Cytochem. 1991, 39:1167-1174.
43. Van Veldhoven P.P., Croes K., Asselberghs S., Herdewijn P., Mannaerts G.P. Peroxisomal beta-oxidation of 2-methyl-branched acyl-CoA esters: stereospecific recognition of the 2S-methyl compounds by trihydroxycoprostanoyl-CoA oxidase and pristanoyl-CoA oxidase. FEBS Lett. 1996, 388:80-84.
44. Wang M.X., Wei A., Yuan J., Clippe A., Bernard A., Knoops B., Murrell G.A. Antioxidant enzyme peroxiredoxin 5 is upregulated in degenerative human tendon. Biochem. Biophys. Res. Commun. 2001, 284:667-673.
45. Watabe S., Kohno H., Kouyama H., Hiroi T., Yago N., Nakazawa T. Purification and characterization of a substrate protein for mitochondrial ATP-dependent protease in bovine adrenal cortex. J. Biochem. 1994, 115:648-654.
46. Wattiez R., Hermans C., Bernard A., Lesur O., Falmagne P. Human bronchoalveolar lavage fluid: two-dimensional gel electrophoresis, amino acid microsequencing and identification of major proteins. Electrophoresis 1999, 20:1634-1645.
47. Wood Z.A., Schroder E., Robin H.J., Poole L.B. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 2003, 28:32-40.
48. Yamashita H., Avraham S., Jiang S., London R., Van Veldhoven P.P., Subramani S., Rogers R.A., Avraham H. Characterization of human and murine PMP20 peroxisomal proteins that exhibit antioxidant activity in vitro. J. Biol. Chem. 1999, 274:29897-29904.
49. Zhang S., Liu Z., Yuan J., Lin M., Sawant M.S., Xu A. Cloning and characterization of AmphiPrxV, a new member of peroxiredoxin family from the amphioxus Branchiostoma belcheri tsingtauense. Curr. Sci. 2003, 84:213-218.