Glutathione S-transferase π localizes in mitochondria and protects against oxidative stress

Free Radical Biology and Medicine

Volumn 46, Issue 10, 2009, Pages 1392-1403

  Goto, Shinji ^a   Kawakatsu, Miho ^a   Izumi, Shin ichi ^a   Urata, Yoshishige ^a   Kageyama, Kan ^a   Ihara, Yoshito ^b   Koji, Takehiko ^a   Kondo, Takahito ^a  

^a NAGASAKI UNIVERSITY GRADUATE SCHOOL OF BIOMEDICAL SCIENCES   (Japan)

^b WAKAYAMA MEDICAL UNIVERSITY   (Japan)

Author keywords

Antimycin A; Free radicals; Glutathione S transferase ; Mitochondria; Mitochondrial targeting signal; Oxidative stress; Rotenone

Indexed keywords

ALANINE; AMINO ACID; ANTIMYCIN A1; ARGININE; GLUTATHIONE TRANSFERASE P1; GREEN FLUORESCENT PROTEIN; REACTIVE OXYGEN METABOLITE; ROTENONE; SMALL INTERFERING RNA;

ALTERNATIVE RNA SPLICING; ARTICLE; CELL NUCLEUS; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; CYTOSOL; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MUTATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN TRANSPORT; STEADY STATE;

ANIMALS; ANTIMYCIN A; ARGININE; CERCOPITHECUS AETHIOPS; COS CELLS; CYTOPROTECTION; EPITHELIAL CELLS; GLUTATHIONE S-TRANSFERASE PI; HUMANS; MEMBRANE POTENTIALS; MITOCHONDRIA; MUTAGENESIS, SITE-DIRECTED; OXIDATIVE STRESS; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; RNA, SMALL INTERFERING; ROTENONE; UNCOUPLING AGENTS;

MAMMALIA;

EID: 64449083797     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.02.025     Document Type: Article

References (48)

1. Roise D., and Schatz G. Mitochondrial presequences. J. Biol. Chem. 263 (1988) 4509-4511
2. Sturtz L.A., Diekert K., Jensen R., Lill L.T., and Culotta V.C. A fraction of yeast Cu,Zn-superoxide dismutase and its metallochaperone, CCS, localize to the intermembrane space of mitochondria: a physiological role for SOD1 in guarding against mitochondrial oxidative damage. J. Biol. Chem. 276 (2001) 38084-38089
3. Borchert A., Savaskan N.E., and Kuhn H. Regulation of expression of the phospholipid hydroperoxide/sperm nucleus glutathione peroxidase gene: tissue-specific expression pattern and identification of functional cis-and trans-regulatory elements. J. Biol. Chem. 278 (2002) 2571-2580
4. Arai M., Imai H., Sumi D., Imanaka T., Takano T., Chiba N., and Nakagawa Y. Import into mitochondria of phospholipid hydroperoxide glutathione peroxidase requires a leader sequence. Biochem. Biophys. Res. Commun. 227 (1996) 433-439
5. 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
6. Outten C.E., and Culotta V.C. Alternative start sites in the Saccharomyces cerevisiae GLR1 gene are responsible for mitochondrial and cytosolic isoforms of glutathione reductase. J. Biol. Chem. 279 (2004) 7785-7791
7. Lundberg M., Johansson C., Chandra J., Enoksson M., Jacobsson G., Ljung J., Johansson M., and Holmgren A. Cloning and expression of a novel human glutaredoxin (Grx2) with mitochondrial and nuclear isoforms. J. Biol. Chem. 276 (2001) 26269-26275
8. Spyrou G., Enmark E., Miranda-Vizuete A., and Gustafsson J. Cloning and expression of a novel mammalian thioredoxin. J. Biol. Chem. 272 (1997) 2936-2941
9. Chasseaud L.F. The role of glutathione and glutathione S-transferases in the metabolism of chemical carcinogens and other electrophilic agents. Adv. Cancer Res. 29 (1979) 175-274
10. Meyer D.J., Beale D., Tan K.H., Coles B., and Ketterer B. Glutathione transferases in primary rat hepatomas: the isolation of a form with GSH peroxidase activity. FEBS Lett. 184 (1985) 139-143
11. Satoh K., Kitahara A., Soma Y., Inaba Y., Hatayama I., and Sato K. Purification, induction, and distribution of placental glutathione transferase: a new marker enzyme for preneoplastic cells in the rat chemical hepatocarcinogenesis. Proc. Natl. Acad. Sci. USA 82 (1985) 3964-3968
12. Mannervik B., Castro V.M., Danielson U.H., Tahir M.K., Hansson J., and Ringborg U. Expression of class Pi glutathione transferase in human malignant melanoma cells. Carcinogenesis 8 (1987) 1929-1932
13. Howie A.F., Forrester L.M., Glancey M.J., Schlager J.J., Powis G., Beckett G.J., Hayes J.D., and Wolf C.R. Glutathione S-transferase and glutathione peroxidase expression in normal and tumour human tissues. Carcinogenesis 11 (1990) 451-458
14. Saburi Y., Nakagawa M., Ono M., Sakai M., Muramatsu M., Kohno K., and Kuwano M. Increased expression of glutathione S-transferase gene in cis-diamminedichloroplatinum(II)-resistant variants of a Chinese hamster ovary cell line. Cancer Res. 49 (1989) 7020-7025
15. Batist G., Tulpule A., Sinha B.K., Katki A.G., Myers C.E., and Cowan K.H. Overexpression of a novel anionic glutathione transferase in multidrug-resistant human breast cancer cells. J. Biol. Chem. 261 (1986) 15544-15549
16. Wang Y.Y., Teicher B.A., Shea T.C., Holden S.A., Rosbe K.W., al-Achi A., and Henner W.D. Cross-resistance and glutathione-S-transferase-pi levels among four human melanoma cell lines selected for alkylating agent resistance. Cancer Res. 49 (1989) 6185-6192
17. Goto S., Ihara Y., Urata Y., Izumi S., Abe K., Koji T., and Kondo T. Doxorubicin-induced DNA intercalation and scavenging by nuclear glutathione S-transferase π. FASEB J. 14 (2001) 2702-2714
18. Kamada K., Goto S., Okunaga T., Ihara Y., Tsuji K., Kawai Y., Uchida K., Osawa T., Matsuo T., Nagata I., and Kondo T. Nuclear glutathione S-transferase π prevents apoptosis by reducing the oxidative stress-induced formation of exocyclic DNA products. Free Radic. Biol. Med. 37 (2004) 1875-1884
19. Harris J.M., Meyer D.J., Coles B., and Ketterer B. A novel glutathione transferase (13-13) isolated from the matrix of rat liver mitochondria having structural similarity to class Theta enzymes. Biochem. J. 278 (1991) 137-141
20. Kraus P., Wigand J., and Ostermaier R. Mitochondrial glutathione transferases: the alkylation of mitochondrial membrane yields a catalyst with glutathione-transferase-like properties. Biol. Chem. Hoppe Seyler 367 (1986) 937-941
21. Bhagwat S.V., Vijayasarathy C., Raza H., Mullick J., and Avadhani N.G. Preferential effects of nicotine and 4-(N-methyl-N-nitrosamine)-1-(3-pyridyl)-1-butanone on mitochondrial glutathione S-transferase A4-4 induction and increased oxidative stress in the rat brain. Biochem. Pharmacol. 56 (1998) 831-839
22. Addya S., Mullick J., Fang J.K., and Avadhani N.G. Purification and characterization of a hepatic mitochondrial glutathione S-transferase exhibiting immunochemical relationship to the Alpha-class of cytosolic isoenzymes. Arch. Biochem. Biophys. 310 (1994) 82-88
23. Jowsey I.R., Thomson R.E., Orton T.C., Elcombe C.R., and Hayes J.D. Biochemical and genetic characterization of a murine class Kappa glutathione S-transferase. Biochem. J. 373 (2003) 559-569
24. Raza H., Robin M.A., Fang J.K., and Avadhani N.G. Multiple isoforms of mitochondrial glutathione S-transferases and their differential induction under oxidative stress. Biochem. J. 366 (2002) 45-55
25. Gardner J.L., and Gallagher E.P. Development of a peptide antibody specific to human glutathione S-transferase Alpha 4-4 (hGSTA4-4) reveals preferential localization in human liver mitochondria. Arch. Biochem. Biophys. 390 (2001) 19-27
26. Gallagher E.P., Gardner J.L., and Barber D.S. Several glutathione S-transferase isozymes that protect against oxidative injury are expressed in human liver mitochondria. Biochem. Pharmacol. 71 (2006) 1619-1628
27. Rapaport D. Biogenesis of the mitochondrial TOM complex. Trends Biochem. Sci. 27 (2002) 191-197
28. Wiedemann N., Frazier A.E., and Pfanner N. The protein import machinery of mitochondria. J. Biol. Chem. 279 (2004) 14473-14476
29. Koehler C. New developments in mitochondrial assembly. Annu. Rev. Cell Dev. Biol. 20 (2004) 309-335
30. Koehler C.M., Merchant S., and Schatz G. How membrane proteins travel across the mitochondrial intermembrane space. Trends Biochem. Sci. 24 (1999) 428-432
31. Pfanner N., and Geissler A. Versatility of the mitochondrial protein import machinery. Nat. Rev. Mol. Cell. Biol. 2 (2001) 339-349
32. Chicco A.J., and Sparagna G.C. Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am. J. Physiol. Cell Physiol. 292 (2007) 33-44
33. Nomura K., Imai H., Koumura T., Kobayashi T., and Nakagawa Y. Mitochondrial phospholipid hydroperoxide glutathione peroxidase inhibits the release of cytochrome c from mitochondria by suppressing the peroxidation of cardiolipin in hypoglycaemia-induced apoptosis. Biochem. J. 351 (2000) 183-193
34. Shiratori Y., Soma Y., Maruyama H., Sato S., Takano A., and Sato K. Immunohistochemical detection of the placental form of glutathione S-transferase in dysplastic and neoplastic human uterine cervix lesions. Cancer Res. 47 (1987) 6806-6809
35. Matsuda K., Yoshida K., Taya Y., Nakamura K., Nakamura Y., and Arakawa H. p53AIP1 regulates the mitochondrial apoptotic pathway. Cancer Res. 62 (2002) 2883-2889
36. Vance J.E. Phospholipid synthesis in a membrane fraction associated with mitochondria. J. Biol. Chem. 265 (1990) 7248-7256
37. Redinbaugh M.G., and Turley R.B. Adaptation of the bicinchoninic acid protein assay for use with microtiter plates and sucrose gradient fractions. Anal. Biochem. 153 (1986) 267-271
38. Izumi S., Kimura M., Kimura T., Wada A., Hirayama T., Ichinose A., and Koji T. Induction of active invagination of plasma membranes by Helicobacter pylori cytotoxin, VacA, in cultured gastric cells: an immunoelectron microscopic study. Acta Histochem. Cytochem. 33 (2000) 89-94
39. Goto S., Kamada K., Soh Y., Ihara Y., and Kondo T. Significance of nuclear glutathione S-transferase π in resistance to anti-cancer drugs. Jpn. J. Cancer Res. 9 (2002) 1047-1056
40. Chattopadhyay R., Wiederhold L., Szczesny B., Boldogh I., Hazra T., Izumi T.K., and Mitra S. Identification and characterization of mitochondrial abasic (AP)-endonuclease in mammalian cells. Nucleic Acids Res. 34 (2006) 2067-2076
41. Suh K.S., Mutoh M., Nagashima K., Fernandez-Salas E., Edwards L.E., Hayes D.D., Crutchley J.M., Marin K.G., Dumont R.A., Levy J.M., Cheng C., Garfield S., and Yuspa S.H. The organellar chloride channel protein CLIC4/mtCLIC translocates to the nucleus in response to cellular stress and accelerates apoptosis. J. Biol. Chem. 279 (2004) 4632-4641
42. Wang Y., Lyu Y.L., and Wang J.C. Dual localization of human DNA topoisomerase IIIalpha to mitochondria and nucleus. Proc. Natl. Acad. Sci. USA 99 (2002) 12114-12119
43. Robin M.A., Prabu S.K., Raza H., Anandatheerthavarada H.K., and Avadhani N.G. Phosphorylation enhances mitochondrial targeting of GSTA4-4 through increased affinity for binding to cytoplasmic Hsp70. J. Biol. Chem. 278 (2003) 18960-18970
44. Vassarotti A., Stroud R., and Douglas M. Independent mutations at the amino terminus of a protein act as surrogate signals for mitochondrial import. EMBO J. 6 (1987) 705-711
45. Lain B., Iriarte A., Mattingly J.R., Moreno J.I., and Martinez-Carrion M. Structural features of the precursor to mitochondrial aspartate aminotransferase responsible for binding to hsp70. J. Biol. Chem. 270 (1995) 24732-24739
46. Garry M.R., Kavanagh T.J., Faustman E.M., Sidhu J.S., Liao R., Ware C., Vliet P.A., and Deeb S.S. Sensitivity of mouse lung fibroblasts heterozygous for GPx4 to oxidative stress. Free Radic. Biol. Med. 44 (2008) 1075-1087
47. Zimniak P., Singhal S.S., Srivastava S.K., Awasthi S., Sharma R., Hyden J.B., and Awasthi Y.C. Estimation of genomic complexity, heterologous expression, and enzymatic characterization of mouse glutathione S-transferase mGSTA4-4 (GST 5.7). J. Biol. Chem. 269 (1994) 992-1000
48. Singhal S.S., Zimniak P., Awasthi S., Piper J.T., He N.G., Teng J.I., Petersen D.R., and Awasthi Y.C. Several closely related glutathione S-transferase isozymes catalyzing conjugation of 4-hydroxynonenal are differentially expressed in human tissues. Arch. Biochem. Biophys. 311 (1994) 242-250