Dual localization of glutathione S-transferase in the cytosol and mitochondria: Implications in oxidative stress, toxicity and disease

FEBS Journal

Volumn 278, Issue 22, 2011, Pages 4243-4251

  Raza, Haider ^a  

^a UNITED ARAB EMIRATES UNIVERSITY   (United Arab Emirates)

Author keywords

chemical toxicity; cryptic mitochondrial signal; dual localization of GSTs; glutathione S transferase; Hsp70 chaperone; N terminal signal region; oxidative stress; PKA phosphorylation

Indexed keywords

4 HYDROXYNONENAL; CHAPERONE; GLUTATHIONE; GLUTATHIONE TRANSFERASE; GLUTATHIONE TRANSFERASE A4; GLUTATHIONE TRANSFERASE KAPPA 1 1; GLUTATHIONE TRANSFERASE P1; GSTK1 ENZYME; HEAT SHOCK PROTEIN 70; INSULIN; NITRIC OXIDE; PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); THIOL GROUP; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CHEMICAL MODIFICATION; CYTOSOL; DIABETES MELLITUS; DIMERIZATION; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; GLUTATHIONYLATION; HUMAN; INSULIN RESISTANCE; INTRACELLULAR SIGNALING; INTRACELLULAR TRANSPORT; LIPID METABOLISM; LIVER MITOCHONDRION; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE PERMEABILIZATION; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; OBESITY; OXIDATION REDUCTION STATE; OXIDATIVE PHOSPHORYLATION UNCOUPLING; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN TARGETING; PROTEIN TRANSPORT; REVIEW;

ANIMALS; CYTOPLASM; DIABETES MELLITUS; GLUTATHIONE TRANSFERASE; HUMANS; METABOLIC DETOXICATION, DRUG; MICE; MITOCHONDRIA; OXIDATIVE STRESS; PROTEIN TRANSPORT;

MUS;

EID: 80255127115     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08358.x     Document Type: Review

References (58)

1. Hayes JD, Flanagan JU, &, Jowsey IR, (2005) Glutathione S-transferases. Ann Rev Pharmacol Toxicol 45, 51-88.
2. Zimniak P, &, Singh SP, (2006) Families of glutathione transferases. In Toxicology of Glutathione Transferases (, Awasthi YC, ed.), pp. 11-26. Taylor & Francis CRC Press, Boca Raton, FL.
3. Allocati N, Federici L, Masulli M, &, Di Ilio C, (2009) Glutathione transferases in bacteria. FEBS J 276, 58-75.
4. Zimniak P, (2006) Substrate and reaction mechanism of GSTs. In Toxicology of Glutathione Transferases (, Awasthi YC, ed.), pp. 71-102. Taylor & Francis CRC Press, Boca Raton, FL.
5. Yang Y, &, Awasthi YC, (2006) Glutathione S-transferases as modulators of signal transduction. In Toxicology of Glutathione Transferases (, Awasthi YC, ed.), pp. 205-230. Taylor & Francis CRC Press, Boca Raton, FL.
6. Harris JM, Meyer DJ, Coles B, &, Kettere B, (1991) A novel glutathione transferase (13-13) isolated from the matrix of rat liver mitochondria having structural similarity to class theta enzymes. Biochem J 278, 137-141.
7. Addya S, Mullick J, Fang JK, &, Avadhani NG, (1994) Purification and characterization of a hepatic mitochondrial glutathione S-transferase exhibiting immunochemical relationship to the alpha-class of cytosolic isoenzyme. Arch Biochem Biophys 310, 82-88.
8. Raza H, Robin MA, Fang JK, &, Avadhani NG, (2002) Multiple isoforms of mitochondrial glutathione S-transferases and their differential induction under oxidative stress. Biochem J 366, 45-55. (Pubitemid 34971802)
9. Gallagher EP, Gardner JL, &, Barber DS, (2006) Several glutathione S-transferase isoenzymes that protect against oxidative injury are expressed in human liver mitochondria. Biochem Pharmacol 71, 1619-1628.
10. Morle FP, Rauch C, Petit E, Piton A, Theret N, Coles B, &, Guillouzo A, (2004) Gene and protein characterization of the human glutathione S-transferase kappa and evidence for a peroxisomal localization. J Biol Chem 279, 16246-16253. (Pubitemid 38509318)
11. Lu SC, (2009) Regulation of glutathione synthesis. Mol Aspect Med 30, 42-59.
12. Lash LH, (2006) Mitochondrial glutathione transport: physiological, pathological and toxicological implications. Chem Biol Interact 163, 54-67. (Pubitemid 44572210)
13. Yuan L, &, Kaplowitz N, (2009) Glutathione in liver diseases and hepatotoxicity. Mol Aspect Med 30, 29-41.
14. Kulinsky VI, &, Kolesnichenko LS, (2007) Mitochondrial glutathione. Biochemistry (Mosc) 72, 698-701. (Pubitemid 47123366)
15. Mari M, Morales A, Colell A, Montfort CV, Garcia-Ruiz C, &, Fernandez-Checa JC, (2010) Antioxidants and redox signaling: redox control of liver function in health and disease. Antioxid Redox Signal 12, 1295-1331.
16. Fernandez-Checa JC, &, Kaplowitz N, (2005) Hepatic mitochondrial glutathione: transport and role in disease and toxicity. Toxicol Appl Pharmacol 204, 263-273. (Pubitemid 40545231)
17. Thomson RE, Bigley AL, Foster JR, Jowsey IR, Elcombe CR, Orton TC, &, Hayes JD, (2004) Tissue-specific expression and subcellular distribution of murine glutathione S-transferase class Kappa. J Histochem Cytochem 52, 653-662. (Pubitemid 38658197)
18. Bhagwat SV, Vijayasarathy C, Raza H, Mullick J, &, Avadhani NG, (1998) 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, 831-839. (Pubitemid 28458977)
19. Raza H, &, Avadhani NG, (2006) Mitochondrial glutathione S-transferase pool in health and disease. In Toxicology of Glutathione Transferases (, Awasthi YC, ed.), pp. 277-292. Taylor & Francis CRC Press, Boca Raton, FL.
20. Goto S, Kawakatsu M, Izumi SI, Urata Y, Kageyama K, Ihara Y, Koji T, &, Kondo T, (2009) Glutathione S-transferase π localizes in mitochondria and protect against oxidative stress. Free Radic Biol Med 46, 1392-1403.
21. Robin MA, Anandatheerathavarada HK, Fang JK, Cudic M, Otvos L, &, Avadhani NG, (2001) Mitochondrial targeted cytochrome P450 2E1 (P450 MT5) contain an intact N terminus and requires mitochondrial specific electron transfer proteins for activity. J Biol Chem 276, 24680-24689.
22. Wiedemann N, Frazier AE, &, Pfanner N, (2004) The protein import machinery of mitochondria. J Biol Chem 279, 14473-14476. (Pubitemid 38618831)
23. Anandatheerathavarada HK, Biswas G, Mullick J, Babu SVN, Laszlo O, Pain D, &, Avadhani NG, (1999) Dual targeting of cytochrome P450 2B1 to mitochondria and microsomes involves a novel signal activation by phosphorylation at Ser 128. EMBO J 18, 5494-5504. (Pubitemid 29486369)
24. Avadhani NG, Sangar MC, Bansal S, &, Bajpai P, (2011) Bimodal targeting of cytochrome P450s to endoplasmic reticulum and mitochondria: the concept of chimeric signals. FEBS J 278, 4218-4229.
25. Robin MA, Prabu SK, Raza H, Anandatheerathavarada HK, &, Avadhani NG, (2003) Phosphorylation enhances mitochondrial targeting of GSTA4-4 through increased affinity for binding to cytoplasmic Hsp70. J Biol Chem 278, 18960-18970. (Pubitemid 36799280)
26. Dasari VR, Anandatheerthavarada HK, Robin MA, Boopathi E, Biswas G, Fang JK, Nebert DW, &, Avadhani NG, (2006) Role of protein kinase C-mediated protein phosphorylation in mitochondrial translocation of mouse CYP 1A1, which contains a non-canonical targeting signal. J Biol Chem 281, 30834-30847. (Pubitemid 44582138)
27. Sepuri NB, Yadav S, Anandatheerathavarada HK, &, Avadhani NG, (2007) Mitochondrial targeting of intact CYP2B1 and CYP2E1 and N-terminal truncated CYP1A1 proteins in Sacchromyces cerevisiae: role of protein kinase A in the mitochondrial targeting of CYP 2E1. FEBS J 274, 4615-4630. (Pubitemid 47301721)
28. Sangar MC, Bansal S, &, Avadhani NG, (2010) Bimodal targeting of microsomal cytochrome P450s to mitochondria: implications in drug metabolism and toxicity. Expert Opin Drug Metab Toxicol 6, 1-21.
29. Bansal S, Liu C-P, Sepuri NB, Anandatheerthavarada HK, Selvaraj V, Hoek J, Milne GL, Guengerich FP, &, Avadhani NG, (2010) Mitochondria-targeted cytochrome P450 2E1 induces oxidative damage and augment alcohol-mediated oxidative stress. J Biol Chem 285, 24609-24619.
30. Wang Y, Biswas G, Prabu SK, &, Avadhani NG, (2006) Modulation of mitochondrial metabolic function by phorbol 12-myristate 13-acetate through increased mitochondrial translocation of protein kinase C alpha in C2C12 myocytes. Biochem Pharmacol 72, 881-892. (Pubitemid 44313887)
31. Knockaert L, Fromenty B, &, Robin M-A, (2011) Mechanisms of mitochondrial targeting of cytochrome P450 2E1: physiopathological role in liver injury and obesity. FEBS J 278, 4252-4260.
32. Yogev O, Naamati A, &, Pines O, (2011) Fumarase: a paradigm of dual targeting and dual localized functions. FEBS J 278, 4230-4242.
33. Lluis JM, Buricchi F, Chiarugi P, Morales A, &, Fernandez-Checa JC, (2007) Dual role of mitochondrial reactive oxygen species in hypoxia signaling: activation of nuclear factor-kappa B via c-SRC and oxidant dependent cell death. Cancer Res 67, 7368-7377. (Pubitemid 47206567)
34. Townsend DM, Manevich Y, He L, Hutchens S, Pazoles CJ, &, Tew KD, (2009) Novel role for glutathione S-transferase pi. Regulator of protein S-glutathionylation following oxidative and nitrosative stress. J Biol Chem 284, 436-445.
35. Chen YR, Chen CL, Pfeiffer DR, &, Zweir JL, (2007) Mitochondrila complex II in the post-ischemic heart: oxidative injury and the role of protein S-glutathionylation. J Biol Chem 282, 32640-32654. (Pubitemid 350159288)
36. Hurd TR, Requejo R, Filipovska A, Brown S, Prime TA, Robinson AJ, Feanley IM, &, Murphy MP, (2008) Complex I within oxidatively stressed bovine heart mitochondria is glutathionylated on Cys-531 and Cys-704 of 75-kDa subunit: potential role of Cys residues in decreasing oxidative damage. J Biol Chem 283, 24801-24815.
37. Queiroga CS, Almeida AS, Martel C, Brenner C, Alves PM, &, Vieira HL, (2010) Glutathionylation of adenine nucleotide translocase induced by carbon monoxide prevents mitochondrial membrane permeabilization and apoptosis. J Biol Chem 285, 17077-17088.
38. Adam-Vizi V, &, Chinopoulos C, (2006) Bioenergetics and formation of mitochondrial reactive oxygen species. Trends Pharmacol Sci 27, 639-645. (Pubitemid 44767940)
39. Enns GM, (2003) The contribution of mitochondria to common disorders. Mol Gen Metab 80, 11-26. (Pubitemid 37272232)
40. Wanagat J, Dai D-F, &, Rabinovitch P, (2010) Mitochondrial oxidative stress and mammalian health. Mech Ageing Dev 131, 527-535.
41. Murphy MP, &, Smith RA, (2007) Targeting antioxidants to mitochondria by conjugation to lipophilic cations. Annu Rev Pharmacol Toxicol 47, 629-656.
42. Wei YH, Wu SB, Ma YS, &, Lee HC, (2009) Respiratory function decline and DNA mutation in mitochondria, oxidative stress and altered gene expression during aging. Chang Gung Med J 32, 113-132.
43. Raza H, Prabu SK, Robin MA, &, Avadhani NG, (2004) Elevated mitochondrial cytochrome P450 2E1 and glutathione S-transferase A4-4 in streptozotocin-induced diabetic rats: tissue-specific variations and roles in oxidative stress. Diabetes 53, 185-194. (Pubitemid 38044714)
44. Sivitz WI, &, Yorek MA, (2010) Mitochondrial dysfunction in diabetes: from molecular mechanisms to functional significance and therapeutic opportunities. Antioxd Redox Signal 12, 537-577.
45. Kim J-a, Wei Y, &, Sowers JR, (2008) Role of mitochondrial dysfunction in insulin resistance. Circulation Res 102, 401-414. (Pubitemid 351651099)
46. Prabu SK, Anandatheerathavarada HK, Raza H, Srinivasan S, Spear JF, &, Avadhani NG, (2006) Protein kinase A-mediated phosphorylation modulates cytochrome c oxidase function and augments hypoxia and myocardial ischemia-related injury. J Biol Chem 281, 2061-2070. (Pubitemid 43845794)
47. Raza H, John A, Brown EM, Benedict S, &, Kambal A, (2008) Alterations in mitochondrial respiratory functions, redox metabolism and apoptosis by oxidant 4-hydroxynonenal and antioxidants curcumin and melatonin in PC12 cells. Toxicol Appl Pharmacol 226, 161-168.
48. Ishikawa K, Takenaga K, Akimoto M, Koshikawa N, Yamaguchi A, Imanishi H, Nakada K, Honma Y, &, Hayashi J, (2008) ROS-generating mitochondrial DNA mutations can regulate tumor cell metastasis. Science 320, 661-664. (Pubitemid 351928347)
49. Biswas G, Srinivasan S, Anandatheerthavarada HK, &, Avadhani NG, (2008) Dioxin-mediated tumor progression through activation of mitochondria-to-nucleus. Proc Natl Acad Sci USA 105, 186-191.
50. Curtis JM, Grimsrud PA, Wright WS, Xu X, Foncea RE, Graham DW, Brestoff JR, Wiczer BM, Ilkayeva O, Cianflone K, et al. (2010) Downregulation of adipose glutathione S-transferase A4 leads to increased protein carbonylation, oxidative stress and mitochondrial dysfunction. Diabetes 59, 1132-1142.
51. Awasthi YC, Sharma R, Sharma A, Yadav S, Singhal SS, Chaudhary P, &, Awasthi S, (2008) Self-regulatory role of 4-hydroxynonenal in signaling for stress-induced programmed cell death. Free Rad Biol Med 45, 111-118.
52. Brand MD, Affortit C, Esteves TC, Green K, Lambert AJ, Miwa S, Pakay JL, &, Parker N, (2004) Mitochondrial superoxide: production, biological effects and activation of uncoupling proteins. Free Rad Biol Med 37, 755-767. (Pubitemid 39078548)
53. Birbes H, Luberto C, Hsu YT, El Bawab S, Hannun YA, &, Obeid LM, (2005) A mitochondrial pool of sphingomyelin is involved in TNFalpha-induced Bax translocation to mitochondria. Biochem J 386, 445-451. (Pubitemid 40445868)
54. Whiteman M, Chua YL, Zhang D, Duan W, Liou YC, &, Armstrong JS, (2006) Nitric oxide protects against mitochondrial permeabilization induced by glutathione depletion: role of S-nitrosylation? Biochim Biophys Res Commun 339, 255-262. (Pubitemid 41697543)
55. Turella P, Pedersen JZ, Caccuri AM, Maria FD, Mastroberardino P, Bello ML, Federici G, &, Ricci G, (2003) Glutathione transferase superfamily behaves like storage proteins for dinitro-diglutathionyl-iron complex in heterogeneous systems. J Biol Chem 278, 42294-42299. (Pubitemid 37310497)
56. Frosali S, Leonini A, Ettorre A, Di Maio G, Nuti S, Tavarini S, Di Simplicio P, &, Di Stefano A, (2009) Role of intracellular calcium and S-glutathionylation in cell death induced by a mixture of isothiazolinones in HL60 cells. Biochim Biophys Acta 1793, 572-583.
57. Shield AJ, Murray TP, Cappello JY, Coggan M, &, Board PG, (2010) Polymorphism in the human glutathione transferase kappa (GSTK1) promoter alter gene expression. Genomics 95, 299-305.
58. Morel F, &, Aninat C, (2011) The glutathione transferase kappa family. Drug Metab Rev 43, 281-291.