Glutathione S-transferase mediates an ageing response to mitochondrial dysfunction

Mechanisms of Ageing and Development

Volumn 153, Issue , 2016, Pages 14-21

  Dancy, Beverley M ^a   Brockway, Nicole ^a,d   Ramadasan Nair, Renjini ^a   Yang, Yoing ^b   Sedensky, Margaret M ^a,c   Morgan, Philip G ^a,c  

^a SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d LEWIS AND CLARK COLLEGE   (United States)

Author keywords

Caenorhabditis elegans; Glutathione S transferase; Hydroxynonenal; Longevity; Mitochondrial respiratory chain; Reactive oxygen species

Indexed keywords

ALDEHYDE; CAENORHABDITIS ELEGANS PROTEIN; GAS-1 PROTEIN, C ELEGANS; GLUTATHIONE TRANSFERASE; GREEN FLUORESCENT PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; TERT-4-HYDROXY-2-NONENAL;

AGING; ANIMAL; CAENORHABDITIS ELEGANS; CHEMISTRY; DISEASE MODEL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ELECTRON TRANSPORT; METABOLISM; MITOCHONDRION; MUSCLE; PATHOLOGY; PATHOPHYSIOLOGY; PHARYNX; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UPREGULATION;

AGING; ALDEHYDES; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DISEASE MODELS, ANIMAL; ELECTRON TRANSPORT; GLUTATHIONE TRANSFERASE; GREEN FLUORESCENT PROTEINS; MITOCHONDRIA; MITOCHONDRIAL DISEASES; MUSCLES; NADH DEHYDROGENASE; PHARYNX; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84952838261     PISSN: 00476374     EISSN: 18726216     Source Type: Journal    
DOI: 10.1016/j.mad.2015.12.001     Document Type: Article

References (42)

1. Andreux P.A., Mouchiroud L., Wang X., Jovaisaite V., Mottis A., Bichet S., Moullan N., Houtkooper R.H., Auwerx J. A method to identify and validate mitochondrial modulators using mammalian cells and the worm C. elegans. Sci. Rep. 2014, 13(June (4)):5285. PubMed PMID: 24923838; PubMed Central PMCID: PMC4055904. 10.1038/srep05285.
2. Ayyadevara S., Engle M.R., Singh S.P., Dandapat A., Lichti C.F., Benes H., Shmookler Reis R.J., Liebau E., Zimniak P. Lifespan and stress resistance of Caenorhabditis elegans are increased by expression of glutathione transferases capable of metabolizing the lipid peroxidation product 4-hydroxynonenal. Aging Cell 2005, 4(October (5)):257-271. PubMed PMID: 16164425. 10.1111/j.1474-9726.2005.00168.x.
3. Cheng J.Z., Singhal S.S., Saini M., Singhal J., Piper J.T., Van Kuijk F.J., Zimniak P., Awasthi Y.C., Awasthi S. Effects of mGST A4 transfection on 4-hydroxynonenal-mediated apoptosis and differentiation of K562 human erythroleukemia cells. Arch. Biochem. Biophys. 1999, 372(December (1)):29-36. PMID: 10562413 PubMed. 10.1006/abbi.1999.1479.
4. Dancy B.M., Sedensky M.M., Morgan P.G. Mitochondrial bioenergetics and disease in Caenorhabditis elegans. Front. Biosci. (Landmark Ed.) 2015, (January (20)):198-228. PubMed PMID: 25553447. 10.2741/4305.
5. Dancy B.M., Sedensky M.M., Morgan P.G. Effects of the mitochondrial respiratory chain on longevity in C. elegans. Exp. Gerontol. 2014, 56(August):245-255. Epub 2014 Apr 5. PubMed PMID: 24709342. 10.1016/j.exger.2014.03.028.
6. Deponte M. Glutathione catalysis and the reaction mechanisms of glutathione-dependent enzymes. Biochim. Biophys. Acta 2013, 1830(May (5)):3217-3266. Epub 2012 Oct 2. Review. PubMed PMID: 23036594. 10.1016/j.bbagen.2012.09.018.
7. Dingley S., Polyak E., Lightfoot R., Ostrovsky J., Rao M., Greco T., Ischiropoulos H., Falk M.J. Mitochondrial respiratory chain dysfunction variably increases oxidant stress in Caenorhabditis elegans. Mitochondrion 2010, 10(2):125-136. Epub 2009 Nov 10. PubMed PMID: 19900588; PubMed Central PMCID: PMC3638869. 10.1016/j.mito.2009.11.003.
8. Donohoe D.R., Jarvis R.A., Weeks K., Aamodt E.J., Dwyer D.S. Behavioral adaptation in C. elegans produced by antipsychotic drugs requires serotonin and is associated with calcium signaling and calcineurin inhibition. Neurosci. Res. 2009, 64(July (3)):280-289. Epub 2009 Apr 5. PubMed PMID: 19447297; PubMed Central PMCID: PMC2692945. 10.1016/j.neures.2009.03.012.
9. Doonan R., McElwee J.J., Matthijssens F., Walker G.A., Houthoofd K., Back P., Matscheski A., Vanfleteren J.R., Gems D. Against the oxidative damage theory of aging: superoxide dismutases protect against oxidative stress but have little or no effect on life span in Caenorhabditis elegans. Genes Dev. 2008, 22(December (23)):3236-3241. PubMed PMID: 19056880; PubMed Central PMCID: PMC2600764. 10.1101/gad.504808.
10. Falk M.J., Rosenjack J.R., Polyak E., Suthammarak W., Chen Z., Morgan P.G., Sedensky M.M. Subcomplex Ilambda specifically controls integrated mitochondrial functions in Caenorhabditis elegans. PLoS One 2009, 4(August (8)):e6607. PubMed PMID: 19672299; PubMed Central PMCID: PMC2719872. 10.1371/journal.pone.0006607.
11. Falk M.J., Zhang Z., Rosenjack J.R., Nissim I., Daikhin E., Nissim I., Sedensky M.M., Yudkoff M., Morgan P.G. Metabolic pathway profiling of mitochondrial respiratory chain mutants in C. elegans. Mol. Genet. Metab. 2008, 93(4):388-397. Epub 2008 Feb 21. PubMed PMID: 18178500; PubMedCentral PMCID: PMC2424222. 10.1016/j.ymgme.2007.11.007.
12. Felkai S., Ewbank J.J., Lemieux J., Labbé J.C., Brown G.G., Hekimi S. CLK-1 controls respiration, behavior and aging in the nematode Caenorhabditis elegans. EMBO J. 1999, 18(April (7)):1783-1792. PMID: 10202142 PubMed ; PubMed Central PMCID: PMC1171264. 10.1093/emboj/18.7.1783.
13. Hartman P.S., Ishii N., Kayser E.B., Morgan P.G., Sedensky M.M. Mitochondrial mutations differentially affect aging, mutability and anesthetic sensitivity in Caenorhabditis elegans. Mech. Ageing Dev. 2001, 122(August (11)):1187-1201. PubMed PMID: 11389932. 10.1016/s0047-6374(01)00259-7.
14. Harwaldt P., Rahlfs S., Becker K. Glutathione S-transferase of the malarial parasite Plasmodium falciparum: characterization of a potential drug target. Biol. Chem. 2002, 383(May (5)):821-830. PubMed PMID: 12108547. 10.1515/bc.2002.086.
15. Hervé M., Angeli V., Pinzar E., Wintjens R., Faveeuw C., Narumiya S., Capron A., Urade Y., Capron M., Riveau G., Trottein F. Pivotal roles of the parasite PGD2 synthase and of the host D prostanoid receptor 1 in schistosome immune evasion. Eur. J. Immunol. 2003, 33(October (10)):2764-2772. PubMed PMID: 14515260. 10.1002/eji.200324143.
16. Hobson R.J., Hapiak V.M., Xiao H., Buehrer K.L., Komuniecki P.R., Komuniecki R.W. SER-7, a Caenorhabditis elegans 5-HT7-like receptor, is essential for the 5-HT stimulation of pharyngeal pumping and egg laying. Genetics 2005, 172(January (1)):159-169. PubMed PMID: 16204223; PubMed Central PMCID: PMC1456143. 10.1534/genetics.105.044495.
17. Honda Y., Tanaka M., Honda S. Modulation of longevity and diapause by redox regulation mechanisms under the insulin-like signaling control in Caenorhabditis elegans. Exp. Gerontol. 2008, 43(June (6)):520-529. Epub 2008 Mar 18. PubMed PMID: 18406553. 10.1016/j.exger.2008.02.009.
18. Hopkins F.G. On an autoxidisable constituent of the cell. Biochem. J. 1921, 15(2):286-305. PubMed PMID: 16742989; PubMed Central PMCID: PMC1258982. 10.1042/bj0150286.
19. Kayser E.B., Morgan P.G., Hoppel C.L., Sedensky M.M. Mitochondrial expression and function of GAS-1 in Caenorhabditis elegans. J. Biol. Chem. 2001, 276(23):20551-20558. Epub 2001 Feb 20. PubMed PMID: 11278828. 10.1074/jbc.m011066200.
20. Kayser E.B., Morgan P.G., Sedensky M.M. GAS-1: a mitochondrial protein controls sensitivity to volatile anesthetics in the nematode Caenorhabditis elegans. Anesthesiology 1999, 90(2):545-554. PubMed PMID: 9952163. 10.1097/00000542-199902000-00031.
21. Kayser E.B., Sedensky M.M., Morgan P.G. The effects of complex I function and oxidative damage on lifespan and anesthetic sensitivity in Caenorhabditis elegans. Mech. Ageing Dev. 2004, 125(June (6)):455-464. PubMed PMID: 15178135. 10.1016/s0047-6374(04)00074-0.
22. Mapp C.E., Fryer A.A., De Marzo N., Pozzato V., Padoan M., Boschetto P., Strange R.C., Hemmingsen A., Spiteri M.A. Glutathione S-transferase GSTP1 is a susceptibility gene for occupational asthma induced by isocyanates. J. Allergy Clin. Immunol. 2002, 109(May (5)):867-872. PubMed PMID: 11994713. 10.1067/mai.2002.123234.
23. Matsuoka T., Hirata M., Tanaka H., Takahashi Y., Murata T., Kabashima K., Sugimoto Y., Kobayashi T., Ushikubi F., Aze Y., Eguchi N., Urade Y., Yoshida N., Kimura K., Mizoguchi A., Honda Y., Nagai H., Narumiya S. Prostaglandin D2 as a mediator of allergic asthma. Science 2000, 287(March (5460)):2013-2017. PubMed PMID: 10720327. 10.1126/science.287.5460.2013.
24. Mileo A.M., Abbruzzese C., Mattarocci S., Bellacchio E., Pisano P., Federico A., Maresca V., Picardo M., Giorgi A., Maras B., Schininà M.E., Paggi M.G. Human papillomavirus-16 E7 interacts with glutathione S-transferase P1 and enhances its role in cell survival. PLoS One 2009, 4(October (10)):e7254. PubMed PMID: 19826491; PubMed Central PMCID: PMC2758704. 10.1371/journal.pone.0007254.
25. Moreno-Arriola E., Cárdenas-Rodríguez N., Coballase-Urrutia E., Pedraza-Chaverri J., Carmona-Aparicio L., Ortega-Cuellar D. Caenorhabditis elegans: a useful model for studying metabolic disorders in which oxidative stress is a contributing factor. Oxid. Med. Cell. Longev. 2014, 2014:705253. Epub 2014 May 18. PubMed PMID:24955209; PubMed Central PMCID: PMC4052186. 10.1155/2014/705253.
26. Munkácsy E., Rea S.L. The paradox of mitochondrial dysfunction and extended longevity. Exp. Gerontol. 2014, 56(August):221-233. Epub 2014 Apr 1. PubMed PMID: 24699406; PubMed Central PMCID: PMC4104296. 10.1016/j.exger.2014.03.016.
27. Pathare P.P., Lin A., Bornfeldt K.E., Taubert S., Van Gilst M.R. Coordinate regulation of lipid metabolism by novel nuclear receptor partnerships. PLoS Genet. 2012, 8(4):e1002645. Epub 2012 Apr 12. PubMed PMID: 22511885; PubMed Central PMCID: PMC3325191. 10.1371/journal.pgen.1002645.
28. Ramana K.V., Bhatnagar A., Srivastava S., Yadav U.C., Awasthi S., Awasthi Y.C., Srivastava S.K. Mitogenic responses of vascular smooth muscle cells to lipid peroxidation-derived aldehyde 4-hydroxy-trans-2-nonenal (HNE): role of aldose reductase-catalyzed reduction of the HNE-glutathione conjugates in regulating cell growth. J. Biol. Chem. 2006, 281(June (26)):17652-17660. Epub 2006 Apr 28. PubMed PMID: 16648138. 10.1074/jbc.m600270200.
29. Ruzza P., Calderan A. Glutathione transferase (GST)-activated prodrugs. Pharmaceutics 2013, 5(April (2)):220-231. PubMed PMID: 24300447; PubMed Central PMCID: PMC3834953. 10.3390/pharmaceutics5020220.
30. Singh S.P., Coronella J.A., Benes H., Cochrane B.J., Zimniak P. Catalytic function of Drosophila melanogaster glutathione S-transferase DmGSTS1-1 (GST-2) in conjugation of lipid peroxidation end products. Eur. J. Biochem. 2001, 268(May (10)):2912-2923. PubMed PMID: 11358508. 10.1046/j.1432-1327.2001.02179.x.
31. Srivastava S., Liu S.Q., Conklin D.J., Zacarias A., Srivastava S.K., Bhatnagar A. Involvement of aldose reductase in the metabolism of atherogenic aldehydes. Chem. Biol. Interact. 2001, 130-132(January (1-3)):563-571. PubMed PMID: 11306075. 10.1016/s0009-2797(00)00299-4.
32. Suthammarak W., Somerlot B.H., Opheim E., Sedensky M., Morgan P.G. Novel interactions between mitochondrial superoxide dismutases and the electron transport chain. Aging Cell 2013, 12(6):1132-1140. Epub 2013 Sep 11. PubMed PMID: 23895727; PubMed Central PMCID: PMC3838459. 10.1111/acel.12144.
33. Taylor C.M., Wang Q., Rosa B.A., Huang S.C., Powell K., Schedl T., Pearce E.J., Abubucker S., Mitreva M. Discovery of anthelmintic drug targets and drugs using chokepoints in nematode metabolic pathways. PLoS Pathog. 2013, 9(8):e1003505. PubMed PMID: 23935495; PubMed Central PMCID: PMC3731235. 10.1371/journal.ppat.1003505.
34. Tew K.D., Townsend D.M. Glutathione-S-transferases as determinants of cell survival and death. Antioxid. Redox Signal. 2012, 17(December (12)):1728-1737. PubMed PMID: 22540427; PubMed Central PMCID: PMC3474190. 10.1089/ars.2012.4640.
35. Townsend D.M., Tew K.D. The role of glutathione-S-transferase in anti-cancer drug resistance. Oncogene 2003, 22(October (47)):7369-7375. Review. PubMed PMID: 14576844. 10.1038/sj.onc.1206940.
36. Traverso N., Ricciarelli R., Nitti M., Marengo B., Furfaro A.L., Pronzato M.A., Marinari U.M., Domenicotti C. Role of glutathione in cancer progression and chemoresistance. Oxid. Med. Cell. Longev. 2013, 2013:972913. Review. PubMed PMID: 23766865; PubMed Central PMCID: PMC3673338. 10.1155/2013/972913.
37. Tsai L., Szweda P.A., Vinogradova O., Szweda L.I. Structural characterization and immunochemical detection of a fluorophore derived from 4-hydroxy-2-nonenal and lysine. Proc. Natl. Acad. Sci. U. S. A. 1998, 95(July (14)):7975-7980. , http://dx.doi.org/10.1073/pnas.95.14.7975,PubMed PMID: 9653125; PubMed Central PMCID: PMC20914.
38. Tsang W., Sayles L., Grad L., Pilgrim D., Lemire B. Mitochondrial respiratory chain deficiency in Caenorhabditis elegans results in developmental arrest and increased life span. J. Biol. Chem. 2001, 276(34):32240-32246. Epub 2001 Jun 15. PubMed PMID: 11410594. 10.1074/jbc.m103999200.
39. Wu G., Fang Y.Z., Yang S., Lupton J.R., Turner N.D. Glutathione metabolism and its implications for health. J. Nutr. 2004, 134(March (3)):489-492. Review. PubMed PMID: 14988435.
40. Yang W., Hekimi S. Two modes of mitochondrial dysfunction lead independently to lifespan extension in Caenorhabditis elegans. Aging Cell 2010, 9(June (3)):433-447. Epub 2010 Mar 19. PubMed PMID: 20346072. 10.1111/j.1474-9726.2010.00571.x.
41. Yee C., Yang W., Hekimi S. The intrinsic apoptosis pathway mediates the pro-longevity response to mitochondrial ROS in C. elegans. Cell 2014, 157(May (4)):897-909. PubMed PMID: 24813612. 10.1016/j.cell.2014.02.055.
42. Yoneda T., Benedetti C., Urano F., Clark S.G., Harding H.P., Ron D. Compartment-specific perturbation of protein handling activates genes encoding mitochondrial chaperones. J. Cell Sci. 2004, 117(Pt. 18):4055-4066. PubMed PMID: 15280428. 10.1242/jcs.01275.