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The fungal glutathione S-transferase system. Evidence of new classes in the wood-degrading basidiomycete Phanerochaete chrysosporium

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Abstract

The recent release of several basidiomycete genome sequences allows an improvement of the classification of fungal glutathione S-transferases (GSTs). GSTs are well-known detoxification enzymes which can catalyze the conjugation of glutathione to non-polar compounds that contain an electrophilic carbon, nitrogen, or sulfur atom. Following this mechanism, they are able to metabolize drugs, pesticides, and many other xenobiotics and peroxides. A genomic and phylogenetic analysis of GST classes in various sequenced fungi—zygomycetes, ascomycetes, and basidiomycetes—revealed some particularities in GST distribution, in comparison with previous analyses with ascomycetes only. By focusing essentially on the wood-degrading basidiomycete Phanerochaete chrysosporium, this analysis highlighted a new fungal GST class named GTE, which is related to bacterial etherases, and two new subclasses of the omega class GSTs. Moreover, our phylogenetic analysis suggests a relationship between the saprophytic behavior of some fungi and the number and distribution of some GST isoforms within specific classes.

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References

  1. Frova C (2006) Glutathione transferases in the genomics era: new insights and perspectives. Biomol Eng 23:149–169

    Article  CAS  PubMed  Google Scholar 

  2. Hayes JD, Flanagan JU, Jowsey IR (2005) Glutathione transferases. Annu Rev Pharmacol Toxicol 45:51–88

    Article  CAS  PubMed  Google Scholar 

  3. Shimada T (2006) Xenobiotic-metabolizing enzymes involved in activation and detoxification of carcinogenic polycyclic aromatic hydrocarbons. Drug Metab Pharmacokinet 21:257–276

    Article  CAS  PubMed  Google Scholar 

  4. Coleman JOD, Randall R, Blake-Kalff MMA (1997) Detoxification of xenobiotics in plant cells by glutathione conjugation and vacuolar compartmentalization: a fluorescent assay using monochlorobimane. Plant Cell Env 20:449–460

    Article  CAS  Google Scholar 

  5. Dixon DP, Edwards R (2009) Selective binding of glutathione conjugates of fatty acid derivatives by plant glutathione transferases. J Biol Chem (in press). doi:10.1074/jbc.M109.020107

  6. Balogh LM, Roberts AG, Shireman LM, Greene RJ, Atkins WM (2008) The stereochemical course of 4-hydroxy-2-nonenal metabolism by glutathione S-transferases. J Biol Chem 283:16702–16710

    Article  CAS  PubMed  Google Scholar 

  7. Dalhoff K, Buus Jensen K, Enghusen Poulsen H (2005) Cancer and molecular biomarkers of phase 2. Methods Enzymol 400:618–627

    Article  CAS  PubMed  Google Scholar 

  8. Usami H, Kusano Y, Kumagai T, Osada S, Itoh K, Kobayashi A, Yamamoto M, Uchida K (2005) Selective induction of the tumor marker glutathione S-transferase P1 by proteasome inhibitors. J Biol Chem 280:25267–25276

    Article  CAS  PubMed  Google Scholar 

  9. Haas S, Pierl C, Harth V, Pesch B, Rabstein S, Brüning T, Ko Y, Hamann U, Justenhoven C, Brauch H, Fischer HP (2006) Expression of xenobiotic and steroid hormone metabolizing enzymes in human breast carcinomas. Int J Cancer 119:1785–1791

    Article  CAS  PubMed  Google Scholar 

  10. Hossain QS, Ulziikhishig E, Lee KK, Yamamoto H, Aniya Y (2009) Contribution of liver mitochondrial membrane-bound glutathione transferase to mitochondrial permeability transition pores. Toxicol Appl Pharmacol 235:77–85

    Article  CAS  PubMed  Google Scholar 

  11. Allocati N, Favaloro B, Masulli M, Alexeyev MF, Di Ilio C (2003) Proteus mirabilis glutathione S-transferase B1-1 is involved in protective mechanisms against oxidative and chemical stresses. Biochem J 373:305–311

    Article  CAS  PubMed  Google Scholar 

  12. Masai E, Ichimura A, Sato Y, Miyauchi K, Katayama Y, Fukuda M (2003) Roles of the enantioselective glutathione S-transferases in cleavage of beta-aryl ether. J Bacteriol 185:1768–1775

    Article  CAS  PubMed  Google Scholar 

  13. Lloyd-Jones G, Lau PC (1997) Glutathione S-transferase-encoding gene as a potential probe for environmental bacterial isolates capable of degrading polycyclic aromatic hydrocarbons. Appl Environ Microbiol 63:3286–3290

    CAS  PubMed  Google Scholar 

  14. Barreto L, Garcera A, Jansson K, Sunnerhagen P, Herrero E (2006) A peroxisomal glutathione transferase of Saccharomyces cerevisiae is functionally related to sulfur amino acid metabolism. Eukaryot Cell 5:1748–1759

    Article  CAS  PubMed  Google Scholar 

  15. Oakley AJ (2005) Glutathione transferases: new functions. Curr Opin Struct Biol 15:716–723

    Article  CAS  PubMed  Google Scholar 

  16. Hayes JD, Pulford DJ (1995) The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit Rev Biochem Mol Biol 30:445–600

    Article  CAS  PubMed  Google Scholar 

  17. Vararattanavech A, Ketterman AJ (2007) A functionally conserved basic residue in glutathione transferases interacts with the glycine moiety of glutathione and is pivotal for enzyme catalysis. Biochem J 406:247–256

    Article  CAS  PubMed  Google Scholar 

  18. Caccuri AM, Antonini G, Board PG, Parker MW, Nicotra M, Lo Bello M, Federici G, Ricci G (1999) Proton release on binding of glutathione to alpha, Mu and Delta class glutathione transferases. Biochem J 344(Pt 2):419–425

    Article  CAS  PubMed  Google Scholar 

  19. Zhang ZR, Bai M, Wang XY, Zhou JM, Perrett S (2008) “Restoration” of glutathione transferase activity by single-site mutation of the yeast prion protein Ure2. J Mol Biol 384:641–651

    Article  CAS  PubMed  Google Scholar 

  20. Dourado DF, Fernandes PA, Mannervik B, Ramos MJ (2008) Glutathione transferase: new model for glutathione activation. Chemistry 14:9591–9598

    Article  CAS  PubMed  Google Scholar 

  21. Vuillemier S, Pagni M (2002) The elusive roles of bacterial glutathione S-transferases: new lessons from genomes. Appl Microbiol Biotechnol 58:138–146

    Article  Google Scholar 

  22. McGoldrick S, O’Sullivan SM, Sheehan D (2005) Glutathione transferase-like proteins encoded in genomes of yeasts and fungi: insights into evolution of a multifunctional protein superfamily. FEMS Microbiol Lett 242:1–12

    Article  CAS  PubMed  Google Scholar 

  23. Vuillemier S (1997) Bacterial glutathione S-transferases: what are they good for? J Bacteriol 179:1431–1441

    Google Scholar 

  24. Masai E, Katayama Y, Fukuda M (2007) Genetic and biochemical investigations on bacterial catabolic pathways for lignin-derived aromatic compounds. Biosci Biotechnol Biochem 71:1–15

    Article  CAS  PubMed  Google Scholar 

  25. Veal EA, Toone WM, Jones N, Morgan BA (2002) Distinct roles for glutathione S-transferases in the oxidative stress response in Schizosaccharomyces pombe. J Biol Chem 277:35523–35531

    Article  CAS  PubMed  Google Scholar 

  26. Garcera A, Barreto L, Piedrafita L, Tamarit J, Herrero E (2006) Saccharomyces cerevisiae cells have three Omega class glutathione S-transferases acting as 1-Cys thiol transferases. Biochem J 398:187–196

    Article  CAS  PubMed  Google Scholar 

  27. Choi JH, Lou W, Vancura A (1998) A novel membrane-bound glutathione S-transferase functions in the stationary phase of the yeast Saccharomyces cerevisiae. J Biol Chem 273:29915–29922

    Article  CAS  PubMed  Google Scholar 

  28. Rai R, Tate JJ, Cooper TG (2003) Ure2, a prion precursor with homology to glutathione S-transferase, protects Saccharomyces cerevisiae cells from heavy metal ion and oxidant toxicity. J Biol Chem 278:12826–12833

    Article  CAS  PubMed  Google Scholar 

  29. Wickner RB, Koh TJ, Crowley JC, O’Neil J, Kaback DB (1987) Molecular cloning of chromosome I DNA from Saccharomyces cerevisiae: isolation of the MAK16 gene and analysis of an adjacent gene essential for growth at low temperatures. Yeast 3:51–57

    Article  CAS  PubMed  Google Scholar 

  30. Koonin EV, Mushegian AR, Tatusov RL, Altschul SF, Bryant SH, Bork P, Valencia A (1994) Eukaryotic translation elongation factor 1 gamma contains a glutathione transferase domain—study of a diverse, ancient protein superfamily using motif search and structural modeling. Protein Sci 3:2045–2054

    Article  CAS  PubMed  Google Scholar 

  31. Collinson EJ, Grant CM (2003) Role of yeast glutaredoxins as glutathione S-transferases. J Biol Chem 278:22492–22497

    Article  CAS  PubMed  Google Scholar 

  32. Adamis PD, Gomes DS, Pinto ML, Panek AD, Eleutherio EC (2004) The role of glutathione transferases in cadmium stress. Toxicol Lett 154:81–88

    Article  CAS  PubMed  Google Scholar 

  33. Herrero E, Ros J, Tamarit J, Belli G (2006) Glutaredoxins in fungi. Photosynth Res 89:127–140

    Article  CAS  PubMed  Google Scholar 

  34. Mariani D, Mathias CJ, da Silva CG, Herdeiro Rda S, Pereira R, Panek AD, Eleutherio EC, Pereira MD (2008) Involvement of glutathione transferases, Gtt1and Gtt2, with oxidative stress response generated by H2O2 during growth of Saccharomyces cerevisiae. Redox Rep 13:246–254

    Article  CAS  PubMed  Google Scholar 

  35. Castro FA, Mariani D, Panek AD, Eleutherio EC, Pereira MD (2008) Cytotoxicity mechanism of two naphthoquinones (menadione and plumbagin) in Saccharomyces cerevisiae. PLoS ONE 3(12):e3999

    Article  PubMed  Google Scholar 

  36. Morel M, Kohler A, Martin F, Gelhaye E, Rouhier N (2008) Comparison of the thiol-dependent antioxidant systems in the ectomycorrhizal Laccaria bicolor and the saprotrophic Phanerochaete chrysosporium. New Phytol 180:391–407

    Article  CAS  PubMed  Google Scholar 

  37. Jeppesen MG, Ortiz P, Shepard W, Kinzy TG, Nyborg J, Andersen GR (2003) The crystal structure of the glutathione S-transferase-like domain of elongation factor 1Bgamma from Saccharomyces cerevisiae. J Biol Chem 278:47190–47198

    Article  CAS  PubMed  Google Scholar 

  38. Prade L, Huber R, Bieseler B (1998) Structures of herbicides in complex with their detoxifying enzyme glutathione S-transferase—explanations for the selectivity of the enzyme in plants. Structure 6:1445–1452

    Article  CAS  PubMed  Google Scholar 

  39. Gronwald JW, Plaisance KL (1998) Isolation and characterization of glutathione S-transferase isozymes from sorghum. Plant Physiol 117:877–892

    Article  CAS  PubMed  Google Scholar 

  40. Cho HY, Lee HJ, Kong KH (2007) A phi class glutathione S-transferase from Oryza sativa (OsGSTF5): molecular cloning, expression and biochemical characteristics. J Biochem Mol Biol 40:511–516

    CAS  PubMed  Google Scholar 

  41. Sappl PG, Carroll AJ, Clifton R, Lister R, Whelan J, Harvey Millar A, Singh KB (2009) The Arabidopsis glutathione transferase gene family displays complex stress regulation and co-silencing multiple genes results in altered metabolic sensitivity to oxidative stress. Plant J 58:53–68

    Article  CAS  Google Scholar 

  42. Matsuzaki F, Shimizu M, Wariishi H (2008) Proteomic and metabolomic analyses of the white-rot fungus Phanerochaete chrysosporium exposed to exogenous benzoic acid. J Proteome Res 7:2342–2350

    Article  CAS  PubMed  Google Scholar 

  43. Kim HG, Kim BC, Park EH, Ahn K, Lim CJ (2004) Differential regulation of three genes encoding glutathione S-transferases in Schizosaccharomyces pombe. Mol Cells 18:332–339

    CAS  PubMed  Google Scholar 

  44. Sheehan D, Meade G, Foley VM, Dowd CA (2001) Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem J 360:1–16

    Article  CAS  PubMed  Google Scholar 

  45. Allocati N, Federici L, Masulli M, Di Ilio C (2009) Glutathione transferases in bacteria. FEBS J 276:58–75

    Article  CAS  PubMed  Google Scholar 

  46. Magasanik B (2005) The transduction of the nitrogen regulation signal in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 102:16537–16538

    Article  CAS  PubMed  Google Scholar 

  47. Shewmaker F, Mull L, Nakayashiki T, Masison DC, Wickner RB (2007) Ure2p function is enhanced by its prion domain in Saccharomyces cerevisiae. Genetics 176:1557–1565

    Article  CAS  PubMed  Google Scholar 

  48. Baudin-Baillieu A, Fernandez-Bellot E, Reine F, Coissac E, Cullin C (2003) Conservation of the prion properties of Ure2p through evolution. Mol Biol Cell 14:3449–3458

    Article  CAS  PubMed  Google Scholar 

  49. Edskes HK, McCann LM, Hebert AM, Wickner RB (2009) Prion variants and species barriers among Saccharomyces Ure2 proteins. Genetics 181:1159–1167

    Article  CAS  PubMed  Google Scholar 

  50. Zhang ZR, Perrett S (2009) Novel glutaredoxin activity of the yeast prion protein Ure2 reveals a native-like dimer within fibrils. J Biol Chem 284:14058–140067

    Article  CAS  PubMed  Google Scholar 

  51. Fraser JA, Davis MA, Hynes MJ (2002) A gene from Aspergillus nidulans with similarity to URE2 of Saccharomyces cerevisiae encodes a glutathione S-transferase which contributes to heavy metal and xenobiotic resistance. Appl Environ Microbiol 68:2802–2808

    Article  CAS  PubMed  Google Scholar 

  52. Board PG, Coggan M, Chelvanayagam G, Easteal S, Jermiin LS, Schulte GK, Danley DE, Hoth LR, Griffor MC, Kamath AV, Rosner MH, Chrunyk BA, Perregaux DE, Gabel CA, Geoghegan KF, Pandit J (2000) Identification, characterization, and crystal structure of the Omega class glutathione transferases. J Biol Chem 275:24798–24806

    Article  CAS  PubMed  Google Scholar 

  53. Whitbread AK, Masoumi A, Tetlow N, Schmuck E, Coggan M, Board PG (2005) Characterization of the omega class of glutathione transferases. Methods Enzymol 401:78–99

    Article  CAS  PubMed  Google Scholar 

  54. Zakharyan RA, Sampayo-Reyes A, Healy SM, Tsaprailis G, Board PG, Liebler DC, Aposhian HV (2001) Human monomethylarsonic acid (MMA(V)) reductase is a member of the glutathione-S-transferase superfamily. Chem Res Toxicol 14:1051–1057

    Article  CAS  PubMed  Google Scholar 

  55. Dulhunty A, Gage P, Curtis S, Chelvanayagam G, Board P (2001) The glutathione transferase structural family includes a nuclear chloride channel and a ryanodine receptor calcium release channel modulator. J Biol Chem 276:3319–3323

    Article  CAS  PubMed  Google Scholar 

  56. Board PG, Anders MW (2007) Glutathione transferase omega 1 catalyzes the reduction of S-(phenacyl)glutathiones to acetophenones. Chem Res Toxicol 20:149–154

    Article  CAS  PubMed  Google Scholar 

  57. Board PG, Coggan M, Cappello J, Zhou H, Oakley AJ, Anders MW (2008) S-(4-Nitrophenacyl)glutathione is a specific substrate for glutathione transferase omega 1-1. Anal Biochem 374:25–30

    Article  CAS  PubMed  Google Scholar 

  58. Burmeister C, Luersen K, Heinick A, Hussein A, Domagalski M, Walter RD, Liebau E (2008) Oxidative stress in Caenorhabditis elegans: protective effects of the Omega class glutathione transferase (GSTO-1). FASEB J 22:343–354

    Article  CAS  PubMed  Google Scholar 

  59. McCarthy DL, Navarrete S, Willett WS, Babbitt PC, Copley SD (1996) Exploration of the relationship between tetrachlorohydroquinone dehalogenase and the glutathione S-transferase superfamily. Biochemistry 35:14634–14642

    Article  CAS  PubMed  Google Scholar 

  60. Reddy GV, Gold MH (2001) Purification and characterization of glutathione conjugate reductase: a component of the tetrachlorohydroquinone reductive dehalogenase system from Phanerochaete chrysosporium. Arch Biochem Biophys 391:271–277

    Article  CAS  PubMed  Google Scholar 

  61. Hruz T, Laule O, Szabo G, Wessendrop F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P (2008) Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinform

  62. Bousset L, Belrhali H, Melki R, Morera S (2001) Crystal structures of the yeast prion Ure2p functional region in complex with glutathione and related compounds. Biochemistry 40:13564–13573

    Article  CAS  PubMed  Google Scholar 

  63. Schmuck E, Cappello J, Coggan M, Brew J, Cavanaugh JA, Blackburn AC, Baker RT, Eyre HJ, Sutherland GR, Board PG (2008) Deletion of Glu155 causes a deficiency of glutathione transferase Omega 1-1 but does not alter sensitivity to arsenic trioxide and other cytotoxic drugs. Int J Biochem Cell Biol 40:2553–2559

    Article  CAS  PubMed  Google Scholar 

  64. Masai E, Kubota S, Katayama Y, Kawai S, Yamasaki M, Morohoshi N (1993) Characterization of the C alpha-dehydrogenase gene involved in the cleavage of beta-aryl ether by Pseudomonas paucimobilis. Biosci Biotechnol Biochem 57:1655–1659

    Article  CAS  PubMed  Google Scholar 

  65. Otsuka Y, Sonoki T, Ikeda S, Kajita S, Nakamura M, Katayama Y (2003) Detection and characterization of a novel extracellular fungal enzyme that catalyzes the specific and hydrolytic cleavage of lignin guaiacylglycerol beta-aryl ether linkages. Eur J Biochem 270:2353–2362

    Article  CAS  PubMed  Google Scholar 

  66. Masai E, Katayama Y, Kawai S, Nishikawa S, Yamasaki M, Morohoshi N (1991) Cloning and sequencing of the gene for a Pseudomonas paucimobilis enzyme that cleaves beta-aryl ether. J Bacteriol 173:7950–7955

    CAS  PubMed  Google Scholar 

  67. Martin F, Aerts A, Ahrén D, Brun A, Danchin EG, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V, Salamov A, Shapiro HJ, Wuyts J, Blaudez D, Buée M, Brokstein P, Canbäck B, Cohen D, Courty PE, Coutinho PM, Delaruelle C, Detter JC, Deveau A, DiFazio S, Duplessis S, Fraissinet-Tachet L, Lucic E, Frey-Klett P, Fourrey C, Feussner I, Gay G, Grimwood J, Hoegger PJ, Jain P, Kilaru S, Labbé J, Lin YC, Legué V, Le Tacon F, Marmeisse R, Melayah D, Montanini B, Muratet M, Nehls U, Niculita-Hirzel H, Oudot-Le Secq MP, Peter M, Quesneville H, Rajashekar B, Reich M, Rouhier N, Schmutz J, Yin T, Chalot M, Henrissat B, Kües U, Lucas S, Van de Peer Y, Podila GK, Polle A, Pukkila PJ, Richardson PM, Rouzé P, Sanders IR, Stajich JE, Tunlid A, Tuskan G, Grigoriev IV (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452:88–92

    Article  CAS  PubMed  Google Scholar 

  68. Yadav JS, Doddapaneni H, Subramanian V (2006) P450ome of the white rot fungus Phanerochaete chrysosporium: structure, evolution and regulation of expression of genomic P450 clusters. Biochem Soc Trans 34:1165–1169

    Article  CAS  PubMed  Google Scholar 

  69. Matityahu A, Hadar Y, Dosoretz CG, Belinky PA (2008) Gene silencing by RNA Interference in the white rot fungus Phanerochaete chrysosporium. Appl Environ Microbiol 74:5359–5365

    Article  CAS  PubMed  Google Scholar 

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Acknowledgment

The research was supported by an ANR project (ANR-06-BLAN-0386).

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  1. IFR 110 Ecosystèmes Forestiers, Agroressources, Bioprocédés et Alimentation, Unité Mixte de Recherches INRA UHP 1136 Interaction Arbres Microorganismes, Université Nancy I BP 239, 54506, Vandoeuvre-lès-Nancy Cedex, France

    Mélanie Morel, Andrew A. Ngadin, Jean-Pierre Jacquot & Eric Gelhaye

  2. Laboratoire de Génomique Fonctionnelle des Champignons Pathogènes des Plantes, Unité Mixte de Recherches 5240, CNRS-UCB-INSA-Bayer CropScience Microbiologie, Adaptation et Pathogénie, Bayer CropScience, 69263, Lyon cedex 9, France

    Michel Droux

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  1. Mélanie Morel
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Morel, M., Ngadin, A.A., Droux, M. et al. The fungal glutathione S-transferase system. Evidence of new classes in the wood-degrading basidiomycete Phanerochaete chrysosporium . Cell. Mol. Life Sci. 66, 3711–3725 (2009). https://doi.org/10.1007/s00018-009-0104-5

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