Whole genome survey of the glutathione transferase family in the brown algal model Ectocarpus siliculosus

Marine Genomics

Volumn 1, Issue 3-4, 2008, Pages 135-148

  Franco, Pierre Olivier de ^a,b   Rousvoal, Sylvie ^a,b   Tonon, Thierry ^a,b   Boyen, Catherine ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b CNRS   (France)

Author keywords

Evolution; GST; Kappa class; MAPEG; Marine algae; Oxylipins; Sigma class; Stress response

Indexed keywords

ALGAE; ECTOCARPUS SILICULOSUS; PHAEOPHYCEAE;

EID: 63049117821     PISSN: 18747787     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.margen.2009.01.003     Document Type: Article

References (78)

1. Agianian B., Tucker P.A., Schouten A., Leonard K., Bullard B., and Gros P. Structure of a drosophila Sigma class glutathione S-transferase reveals a novel active site topography suited for lipid peroxidation products. J. Mol. Biol. 326 (2003) 151-165
2. Armstrong R.N. Structure, catalytic mechanism, and evolution of the glutathione transferases. Chem. Res. Toxicol. 10 (1997) 2-18
3. Baldauf S. The deep roots of eukaryotes. Science 300 (2003) 1703-1706
4. Bartling D., Radzio R., Steiner U., and Weiler E.W. A glutathione-S-transferase with glutathione-peroxidase activity from Arabidopsis thaliana - molecular cloning and functional characterization. Eur. J. Biochem. 216 (1993) 579-586
5. Bartsch I., Wiencke C., Bischof K., Buchholz C.M., Buck B.H., Eggert A., Feuerpfeil P., Hanelt D., Jacobsen S., Karez R., Karsten U., Molis M., Roleda M.Y., Schubert H., Schumann R., Valentin K., Weinberger F., and Wiese J. The genus Laminaria sensu lato: recent insights and developments. Eur. J. Phycol. 43 (2008) 1-86
6. Board P.G., Baker R.T., Chelvanayagam G., and Jermiin L.S. Zeta, a novel class of glutathione transferases in a range of species from plants to humans. Biochem. J. 328 (1997) 929-935
7. Board P.G., Coggan M., Chelvanayagam G., Easteal S., Jermiin L.S., Schulte G.K., Danley D.E., Hoth L.R., Griffor M.C., Kamath A.V., Rosner M.H., Chrunyk B.A., Perregaux D.E., Gabel C.A., Geoghegan K.F., and Pandit J. Identification, characterization, and crystal structure of the omega class glutathione transferases. J. Biol. Chem. 275 (2000) 24798-24806
8. Booth J., Boyland E., and Sims P. An enzyme from rat liver catalysing conjugations with glutathione. Biochem. J. 79 (1961) 516-524
9. Bouarab K., Adas F., Gaquerel E., Kloareg B., Salaun J., and Potin P. The innate immunity of a marine red alga involves oxylipins from both the eicosanoid and octadecanoid pathways. Plant Physiol. 135 (2004) 1838-1848
10. Bradford M.M. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
11. Bresell A., Weinander R., Lundqvist G., Raza H., Shimoji M., Sun T.-H., Balk L., Wiklund R., Eriksson J., Jansson C., Persson B., Jakobsson P.-J., and Morgenstern R. Bioinformatic and enzymatic characterization of the MAPEG superfamily. FEBS J. 272 (2005) 1688-1703
12. Cairrao E., Couderchet M., Soares A.M.V.M., and Guilhermino L. Glutathione-S-transferase activity of Fucus spp. as a biomarker of environmental contamination. Aquat. Toxicol. 70 (2004) 277-286
13. Cedergreen N., and Streibig J.C. The toxicity of herbicides to non-target aquatic plants and algae: assessment of predictive factors and hazard. Pest Manag. Sci. 61 (2005) 1152-1160
14. Cha C.J., Kim S.J., Kim Y.H., Stingley R., and Cerniglia C.E. Molecular cloning, expression and characterization of a novel class glutathione S-transferase from the fungus Cunninghamella elegans. Biochem. J. 368 (2002) 589-595
15. Charrier B., Coelho S.M., Le Bail A., Tonon T., Michel G., Potin P., Kloareg B., Boyen C., Peters A.F., and Cock J.M. Development and physiology of the brown alga Ectocarpus siliculosus: two centuries of research. New Phytol. 177 (2008) 319-332
16. Cho S.-G., Lee Y.H., Park H.-S., Ryoo K., Kang K.W., Park J., Eom S.-J., Kim M.J., Chang T.-S., Choi Y., Shim J., Kim Y., Dong M.-S., Lee M.-J., Kim S.G., Ichijo H., and Choi E.-J. Glutathione S-transferase mu modulates the stress-activated signals by suppressing apoptosis signal-regulating kinase 1. J. Biol. Chem. 276 (2001) 12749-12755
17. Coleman J.O.D., Randall R., and BlakeKalff M.M.A. Detoxification of xenobiotics in plant cells by glutathione conjugation and vacuolar compartmentalization: a fluorescent assay using monochlorobimane. Plant Cell Environ. 20 (1997) 449-460
18. Collén J., and Davison I.R. Reactive oxygen metabolism in intertidal Fucus spp. (Phaeophyceae). J. Phycol. 35 (1999) 62-69
19. Collén J., Roeder V., Rousvoal S., Collin O., Kloareg B., and Boyen C. An expressed sequence tag analysis of thallus and regenerating protoplasts of Chondrus crispus (Gigartinales, Rhodophyceae). J. Phycol 42 (2006) 104-112
20. Combes B., and Stakelum G.S. A liver enzyme that conjugates sulfobromophthalein sodium with glutathione. J. Clin. Invest. 40 (1961) 981-988
21. Correa J., Castilla J., Ramirez M., Varas M., Lagos N., Vergara S., Moenne A., Roman D., and Brown M. Copper, copper mine tailings and their effect on the marine algae in Northern Chile. J. Appl. Phycol. 11 (1999) 57-67
22. Cosse A., Leblanc C., and Potin P. Dynamic defense of marine macroalgae against pathogens: from early activated to gene regulated responses. Adv. Bot. Res. 46 (2007) 222-266
23. Dereeper A., Guignon V., Blanc G., Audic S., Buffet S., Chevenet F., Dufayard J.F., Guindon S., Lefort V., Lescot M., Claverie J.M., and Gascuel O. Phylogeny fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36 (2008) 465-469
24. Ding Y.C., Ortelli F., Rossiter L.C., Hemingway J., and Ranson H. The Anopheles gambiae glutathione transferase supergene family: annotation, phylogeny and expression profiles. BMC Genomics 4 (2003) 35-50
25. Dixon D.P., Lapthorn A., and Edwards R. Plant glutathione transferases. Genome Biol. 3 (2002) 3004.1-3004.10
26. Dring M. Stress resistance and disease resistance in seaweeds: the role of reactive oxygen metabolism. Adv. Bot. Res. 43 (2006) 176-207
27. Edwards R., Dixon D.P., and Walbot V. Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci. 5 (2000) 193-198
28. Fernandez-Canon J.M., and Penalva M.A. Characterization of a fungal maleylacetoacetate isomerase gene and identification of its human homologue. J. Biol. Chem. 273 (1998) 329-337
29. Frova C. Glutathione transferases in the genomics era: new insights and perspectives. Biomol. Eng. 23 (2006) 149-169
30. Funk C. Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294 (2001) 1871-1875
31. Gaquerel E., Hervé C., Labrière C., Boyen C., Potin P., and Salaün J.-P. Evidence for oxylipin synthesis and induction of a new polyunsaturated fatty acid hydroxylase activity in Chondrus crispus in response to methyljasmonate. Biochim. Biophys. Acta-Mol. Cell Biol. Lipids 1771 (2007) 565-575
32. Gerwick W.H., Roberts M.A., Vulpanovici A., and Ballantine D.L. Biogenesis and biological function of marine algal oxylipins. Adv. Exp. Med. Biol. 447 (1999) 211-218
33. Hall T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series (1999) 95-98
34. Hayes J.D., Flanagan J.U., and Jowsey I.R. Glutathione transferases. Annu. Rev. Pharmacol. Toxicol. 45 (2005) 51-88
35. Hervé C., de Franco P.-O., Groisillier A., Tonon T., and Boyen C. New members of the glutathione transferase family discovered in red and brown algae. Biochem. J. 412 (2008) 535-544
36. Ishikawa T. The ATP-dependent glutathione S-conjugate export pump. Trends Biochem. Sci. 17 (1992) 463-469
37. Jakobsson P.J., Mancini J.A., Riendeau D., and Ford-Hutchinson A.W. Identification and characterization of a novel microsomal enzyme with glutathione-dependent transferase and peroxidase activities. J. Biol. Chem. 272 (1997) 22934-22939
38. Jakobsson P.J., Morgenstern R., Mancini J., Ford-Hutchinson A., and Persson B. Common structural features of MAPEG - a widespread superfamily of membrane associated proteins with highly divergent functions in eicosanoid and glutathione metabolism. Protein Sci. 8 (1999) 689-692
39. Jowsey I.R., Thomson A.M., Flanagan J.U., Murdock P.R., Moore G.B.T., Meyer D.J., Murphy G.J., Smith S.A., and Hayes J.D. Mammalian class Sigma glutathione S-transferases: catalytic properties and tissue-specific expression of human and rat GSH-dependent prostaglandin D-2 synthases. Biochem. J. 359 (2001) 507-516
40. Kanaoka Y., Ago H., Inagaki E., Nanayama T., Miyano M., Kikuno R., Fujii Y., Eguchi N., Toh H., Urade Y., and Hayaishi O. Cloning and crystal structure of hematopoietic prostaglandin D synthase. Cell 90 (1997) 1085-1095
41. Kanaoka Y., Fujimori K., Kikuno R., Sakaguchi Y., Urade Y., and Hayaishi O. Structure and chromosomal localization of human and mouse genes for hematopoietic prostaglandin D synthase - conservation of the ancestral genomic structure of sigma-class glutathione S-transferase. Eur. J. Biochem. 267 (2000) 3315-3322
42. Konishi T., Kato K., Araki T., Shiraki K., Takagi M., and Tamaru Y. A new class of glutathione S-transferase from the hepatopancreas of the red sea bream Pagrus major. Biochem. J. 388 (2005) 299-307
43. Küpper F.C., Kloareg B., Guern J., and Potin P. Oligoguluronates elicit an oxidative burst in the brown algal kelp Laminaria digitata. Plant Physiol. 125 (2001) 278-291
44. Küpper F.C., Gaquerel E., Boneberg E.-M., Morath S., Salaun J.-P., and Potin P. Early events in the perception of lipopolysaccharides in the brown alga Laminaria digitata include an oxidative burst and activation of fatty acid oxidation cascades. J. Exp. Bot. 57 (2006) 1991-1999
45. Le Bail A., Dittami S., de Franco P.-O., Rousvoal S., Cock M., Tonon T., and Charrier B. Normalisation genes for expression analyses in the brown alga model Ectocarpus siliculosus. BMC Mol. Biol. 9 (2008) 75
46. Li G., and Moriyama E.N. Vector NTI, a balanced all-in-one sequence analysis suite. Brief. Bioinform. 5 (2004) 378-388
47. Marrs K.A. The functions and regulation of glutathione transferases in plants. Annu Rev. Plant Biol. 47 (1996) 127-158
48. Meyer D.J., Muimo R., Thomas M., Coates D., and Isaac R.E. Purification and characterization of prostaglandin-H E-isomerase, a sigma-class glutathione S-transferase, from Ascaridia galli. Biochem. J. 1996 (1996) 223-227
49. Monaco R., Friedman F.K., Hyde M.J., Chen J.M., Manolatus S., Adler V., Ronai Z., Koslosky W., and Pincus M.R. Identification of a glutathione-S-transferase effector domain for inhibition of jun kinase, by molecular dynamics. J. Protein Chem. 18 (1999) 859-866
50. Morel F., Rauch C., Petit E., Piton A., Theret N., Coles B., and Guillouzo A. Gene and protein characterization of the human glutathione S-transferase Kappa and evidence for a peroxisomal localization. J. Biol. Chem. 279 (2004) 16246-16253
51. Nebert D.W., and Vasiliou V. Analysis of the glutathione S-transferase (GST) gene family. Hum. Genomics 1 (2004) 460-464
52. Nei M., and Rooney A.P. Concerted and birth-and-death evolution of multigene families. Annu. Rev. Genet. 39 (2005) 121-152
53. Nei M., Rogozin I.B., and Piontkivska H. Purifying selection and birth-and-death evolution in the ubiquitin gene family. Proc. Natl. Acad. Sci. USA 97 (2000) 10866-10871
54. Pearson W.R. Phylogenies of glutathione transferase families. Methods Enzymol. 401 (2005) 186-204
55. Pemble S.E., Wardle A.F., and Taylor J.B. Glutathione S-transferase class Kappa: characterization by the cloning of rat mitochondrial GST and identification of a human homologue. Biochem. J. 319 (1996) 749-754
56. Peters A.F., Marie D., Scornet D., Kloareg B., and Cock J.M. Proposal of Ectocarpus siliculosus (Ectocarpales, Phaeophyceae) as a model organism for brown algal genetics and genomics. J. Phycol. 50 (2004) 1079-1088
57. Pflugmacher S., Schroder P., and Sandermann Jr. H. Taxonomic distribution of plant glutathione S-transferases acting on xenobiotics. Phytochemistry 54 (2000) 267-273
58. Pieniazek D., Bukowska B., and Duda W. Comparison of the effect of Roundup Ultra 360 SL pesticide and its active compound glyphosate on human erythrocytes. Pestic. Biochem. Physiol. 79 (2004) 58-63
59. Ranson H., and Hemingway J. Mosquito glutathione transferases. Methods Enzymol. 401 (2005) 226-241
60. Ritter A., Goulitquer S., Salaün J.P., Tonon T., Correa J.A., and Potin P. Copper stress induces biosynthesis of octadecanoid and eicosanoid oxygenated derivatives in the brown algal kelp Laminaria digitata. New Phytol. 180 (2008) 809-821
61. Roeder V., Collén J., Rousvoal S., Corre E., Leblanc L., and Boyen C. Identification of stress genes transcripts in Laminaria digitata (Phaeophyceae) protoplast cultures by expressed sequence tag analysis. J. Phycol. 41 (2005) 1227-1235
62. Rowley A.F., Vogan C.L., Taylor G.W., and Clare A.S. Prostaglandins in non-insectan invertebrates: recent insights and unsolved problems. J. Exp. Biol. 208 (2005) 3-14
63. Sawicki R., Singh S.P., Mondal A.K., Benes H., and Zimniak P. Cloning, expression and biochemical characterization of one Epsilon-class (GST-3) and ten Delta-class (GST-1) glutathione S-transferases from Drosophila melanogaster, and identification of additional nine members of the Epsilon class. Biochem. J. 370 (2003) 661-669
64. Schmidt-Krey I., Mitsuoka K., Hirai T., Murata K., Cheng Y., Fujiyoshi Y., Morgenstern R., and Hebert H. The three-dimensional map of microsomal glutathione transferase 1 at 6 Angstrom resolution. EMBO J. 19 (2000) 6311-6316
65. Schuller D.J., Liu Q., Kriksunov I.A., Campbell A.M., Barrett J., Brophy P.M., and Hao Q. Crystal structure of a new class of glutathione transferase from the model human hookworm nematode Heligmosomoides polygyrus. Proteins 61 (2005) 1024-1031
66. Sheehan D., Meade G., Foley V.M., and Dowd C.A. Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem. J. 360 (2001) 1-16
67. Singh S.P., Coronella J.A., Benes H., Cochrane B.J., and Zimniak P. Catalytic function of Drosophila melanogaster glutathione S-transferase DmGSTS1-1 (GST-2) in conjugation of lipid peroxidation end products. Eur. J. Biochem. 268 (2001) 2912-2923
68. Soranzo N., Gorla M.S., Mizzi L., De Toma G., and Frova C. Organisation and structural evolution of the rice glutathione S-transferase gene family. Mol. Genet. Genomics 271 (2004) 511-521
69. Stanley D. Prostaglandins and other eicosanoids in insects: biological significance. Annu. Rev. Entomol. 51 (2006) 25-44
70. Starr R.C., and Zeikus J.A. The culture collection of algae at the University of Texas at Austin. J. Phycol. 29 (1993) 90-95
71. Tamura K., Dudley J., Nei M., and Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24 (2007) 1596-1599
72. Thom R., Dixon D.P., Edwards R., Cole D.J., and Lapthorn A.J. The structure of a zeta class glutathione S-transferase from Arabidopsis thaliana: characterisation of a GST with novel active-site architecture and a putative role in tyrosine catabolism. J. Mol. Biol. 308 (2001) 949-962
73. Thomson A.M., Meyer D.J., and Hayes J.D. Sequence, catalytic properties and expression of chicken glutathione dependent prostaglandin D2 synthase, a novel class Sigma glutathione S-transferase. Biochem. J. 333 (1998) 317-325
74. Tu C.P.D., and Akgul B. Drosophila glutathione S-transferases. Methods Enzymol. 401 (2005) 204-226
75. Valles S.M., Perera O.P., and Strong C.A. Gene structure and expression of the glutathione S-transferase, SiGSTS1, from the red imported fire ant, Solenopsis invicta. Arch. Insect Biochem. Physiol. 61 (2006) 239-245
76. Wagner U., Edwards R., Dixon D.P., and Mauch F. Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol. Biol. 49 (2002) 515-532
77. Yamamoto K., Miake F., and Aso Y. Purification and characterization of a novel sigma-class glutathione S-transferase of the fall webworm, Hyphantria cunea. J. Appl. Entomol. 131 (2007) 466-471
78. Zhang J.Z. Evolution by gene duplication: an update. Trends Ecol. Evol. 18 (2003) 292-298