Possible roles of plant sulfurtransferases in detoxification of cyanide, reactive oxygen species, selected heavy metals and arsenate

Molecules

Volumn 20, Issue 1, 2015, Pages 1410-1423

  Most, Parvin ^a,b   Papenbrock, Jutta ^b  

^a LEIBNIZ UNIVERSITY HANNOVER   (Germany)

^b BANGLADESH AGRICULTURAL RESEARCH INSTITUTE   (Bangladesh)

Author keywords

Arsenate; Arsenate reductase; Cyanide; Rhodanese; Sulfurtransferase

Indexed keywords

ARSENIC ACID; ARSENIC ACID DERIVATIVE; CYANIDE; HEAVY METAL; REACTIVE OXYGEN METABOLITE; SULFURTRANSFERASE;

DRUG INACTIVATION; ENZYMOLOGY; METABOLISM; PLANT;

ARSENATES; CYANIDES; INACTIVATION, METABOLIC; METALS, HEAVY; PLANTS; REACTIVE OXYGEN SPECIES; SULFURTRANSFERASES;

EID: 84921684250     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules20011410     Document Type: Review

References (66)

1. Papenbrock, J.; Guretzki, S.; Henne, M. Latest news about the sulfurtransferases of higher plants. Amino Acids 2010, 41, 53-57.
2. Gliubich, F.; Gazerro, M.; Zanotti, G.; Delbono, S.; Bombieri, G.; Berni, R. Active site structural features for chemically modified forms of rhodanase. J. Biol. Chem. 1996, 27, 21054-21061.
3. Westley, J. Rhodanese. Adv. Enzymol. Relat. Areas Mol. Biol. 1973, 39, 327-368.
4. Ray, W.K.; Zeng, G.; Potters, M.B.; Mansuri, A.M.; Larson, T.J. Characterization of a 12-kilodalton rhodanese encoded by glpE of Escherichia coli and its interaction with thioredoxin. J. Bacteriol. 2000, 182, 2277-2284.
5. Spallarossa, A.; Donahue, J.L.; Larson, T.J.; Bolognesi, M.; and Bordo, D. Escherichia coli GlpE is a prototype sulfurtransferase for the single-domain rhodanese homology superfamily. Structure 2001, 9, 1117-1125.
6. Adams, H.; Teertstra, W.; Koster, M.; Tommassen, J. PspE (phage shock protein E) of Escherichia coli is a rhodanese. FEBS Lett. 2002, 518, 173-176.
7. Heidelberg, J.F.; Eisen, J.A.; Nelson, W.C.; Clayton, R.A.; Gwinn, M.L.; Dodson, R.J.; Haft, D.H.; Hickey, E.K.; Peterson, J.D.; Umayam, L.A., et al. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 2000, 406, 477-483.
8. Azumi, Y.; Watanabe, A. Evidence for a senescence-associated gene induced by darkness. Plant Physiol. 1991, 95, 577-583.
9. Oh, S.A.; Lee, S.Y.; Chung, I.K.; Lee, C.H.; Nam, H.G. A senescence-associated gene of Arabidopsis thaliana is distinctively regulated during natural and artificially induced leaf senescence. Plant Mol. Biol. 1996, 30, 739-754.
10. Ploegman, J.H.; Drent, G.; Kalk, K.H.; Hol, W.G. Structure of bovine liver rhodanese. I. Structure determination at 2.5 A resolution and a comparison of the conformation and sequence of its two domains. J. Mol. Biol. 1978, 123, 557-594.
11. Bordo, D.; Deriu, D.; Colnaghi, R.; Carpen, A.; Pagani, S.; Bolognesi, M. The crystal structure of a sulfurtransferase from Azotobacter vinelandii highlights the evolutionary relationship between the rhodanese and phosphatase enzyme families. J. Mol. Biol. 2000, 298, 691-704.
12. Bordo, D.; Bork, P. The rhodanese/Cdc25 phosphatase super family: Sequence structure and functions relations. EMBO Rep. 2002, 3, 741-746.
13. Forlani, F.; Carpen, A.; Pagani, S. Evidence that elongation of the catalytic loop of the Azotobacter vinelandii rhodanese changed selectivity from sulfur-to phosphate-containing substrates. Protein Eng. 2003, 16, 515-519.
14. Hofmann, K.; Bucher, P.; Kajava A.V. A model of Cdc25 phosphatase activity catalytic domain and Cdk-interaction surface based on the presence of a rhodanese homology domain. J. Mol. Biol. 1998, 282, 195-208.
15. Farooq, A.; Chaturvedi, G.; Mujtaba, S.; Plotnikova, O.; Zeng, L.; Dhalluin, C.; Ashton, R.; Zhou, M.M. Solution structure of ERK2 binding domain of MAPK phosphatase MKP-3: Structural insights into MKP-3 activation by ERK2. Mol. Cell 2001, 7, 387-399.
16. Fauman, E.B.; Cogswell, J.P.; Lovejoy, B.; Rocque, W.J.; Holmes, W.; Montana, V.G.; Rink, M.J.; Piwnica-Worms, H.; Saper, M.A. Crystal structure of the catalytic domain of the human cell cycle control phosphatase, Cdc25A. Cell 1998, 93, 617-625.
17. Nagahara, N.; Ito, T.; Minami, M. Mercaptopyruvate sulfurtransferase as a defense against cyanide toxification: Molecular properties and mode of detoxification. Histol. Hispathol. 1999, 14, 1277-1286.
18. Bartels, A.; Mock, H.P.; Papenbrock, J. Differential expression of Arabidopsis sulfurtransferases under various growth conditions. Plant Physiol. Biochem. 2007, 45, 178-187.
19. Bauer, M.; Papenbrock, J. Identification and characterization of single-domain thiosulfate sulfurtransferases from Arabidopsis thaliana. FEBS Lett. 2002, 532, 427-431.
20. Landrieu, I.; da Costa, M.; de Veylder, L.; Dewitte, F.; Vandepoele, K.; Hassan, S.; Wieruszeski, J.M.; Corellou, F.; Faure, J.D.; van Montagu, M.; et al. A small CDC25 dual-specificity tyrosine-phosphatase isoform in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 2004, 101, 13380-13385.
21. Niu, J.S.; Yu, L.; Ma, Z.-Q.; Chen, P.-D.; Liu, D.-J. Molecular cloning, characterization and mapping of a rhodanese like gene in wheat. Acta Genet. Sin. 2002, 29, 266-272.
22. 2+. Plant Mol. Biol. 2003, 52, 81-89.
23. Henny, C.J.; Hallock, R.J.; Hill, E.F. Cyanide and migratory birds at gold-mines in Nevada, USA. Ecotoxicology 1994, 3, 45-58.
24. Yip, W.-K.; Yang, S.F. Cyanide metabolism in relation to ethylene production in plant tissues. Plant Physiol. 1988, 88, 473-476.
25. Doucleff, M.; Terry, N. Pumping out the arsenic. Nat. Biotechnol. 2002, 20, 1094-1096.
26. Oracz, K.; El-Maarouf-Bouteau, H.; Kranner, I.; Bogatek, R.; Corbineau, F.; Bailly, C. The mechanisms involved in seed dormancy alleviation by hydrogen cyanide unravel the role of reactive oxygen species as key factors of cellular signaling during germination. Plant Physiol . 2009, 150, 494-505.
27. Ressler, C.; Tatake, J.G. Vicianin, prunasin, and β-cyanoalanine in common vetch seed as sources of urinary thiocyanate in the rat. J. Agric. Food Chem. 2001, 49, 5075-5080.
28. Cipollone, R.P.; Ascenzi, P.; Tomao, F.; Imperi, P.; Visca, P. Enzymatic detoxification of cyanide: Clues from Pseudomonas aeruginosa Rhodanese. J. Mol. Microbiol. Biotechnol. 2008, 15, 199-211.
29. Meyer, T.; Burow, M.; Bauer, M.; Papenbrock, J. Arabidopsis sulfurtransferases: Investigation of their function during senescence and in cyanide detoxification. Planta 2003, 217, 1-10.
30. Machingura, M.; Ebbs, S.D. Functional redundancies in cyanide tolerance provided by β-cyanoalanine pathway genes in Arabidopsis thaliana. Int. J. Plant Sci. 2014, 175, 346-358.
31. Hatzfeld, Y.; Maruyama, A.; Schmidt, A.; Noji, M.; Ishizawa, K.; Saito, K. β-cyanoalanine synthase is a mitochondrial cysteine synthase-like protein in spinach and Arabidopsis. Plant Physiol . 2000, 123, 1163-1172.
32. Piotrowski, M.; Schonfelder, S.; Weiler, E.W. The Arabidopsis thaliana isogene NIT4 and its orthologs in tobacco encode β-cyano-L-alanine hydratase/nitrilase. J. Biol. Chem. 2001, 276, 2616-2621.
33. Moller, I.M. Plant mitochondria and oxidative stress: Electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu. Rev. Plant Physiol. Mol. Biol. 2001, 52, 561-591.
34. Uhteg, L.C.; Westley, J. Purification and steady-state kinetic analysis of yeast thiosulfate reductase. Arch. Biochem. Biophys. 1979. 195, 211-222.
35. nd ed.; Oxford University Press: Oxford, UK, 2008; p. 231.
36. Mittler, R.; Vanderauwera, S.; Gollery, M.; van Breusegem, F. Reactive oxygen gene network of plants. Trends Plant Sci. 2004, 9, 490-498.
37. Chalapathi Rao, A.S.V.; Reddy, A.R. Glutathione Reductase: A Putative Redox Regulatory System in Plant Cells. Sulfur Assimilation and Abiotic Stresses in Plants; Khan, N.A., Singh, S., Umar S., Eds.; Springer: Heidelberg, Berlin, 2008; pp. 111-147.
38. Ding, S.; Lu, Q.; Zhang, Y.; Yang, Z.; Wen, X.; Zhang, L.; Lu, C. Enhanced sensitivity to oxidative stress in transgenic tobacco plants with decreased glutathione reductase activity leads to a decrease in ascorbate pool and ascorbate redox state. Plant Mol. Biol. 2009, 69, 577-592.
39. Foyer, C.H.; Noctor, G. Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. Plant Cell 2005, 17, 1866-1875.
40. Dixon, D.P.; Davis, B.G.; Edwards, E. Functional divergence in the glutathione transferase super-family in plants: Identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana. J. Biol. Chem. 2002, 277, 30859-30869.
41. Toohey, T.I. Sulphane sulfur in biological systems: A possible regulatory role. Biochemistry 1989, 264, 625-632.
42. Kaczor-Kamińska, M.; Sura, P.; Wróbel, M. Changes in activity of three sulfurtransferases in response to exposure to cadmium, lead and mercury ions. J. Environ. Prot. 2013, 4, 19-28.
43. Tomsett, A.B.; Thurman, D.A. Molecular biology of metal tolerances of plants. Plant Cell Environ. 1988, 11, 383-394.
44. Nocito, F.F.; Pirovano, L.; Cocucci, M.; Sacchi, G.A. Cadmium-induced sulfate uptake in maize roots. Plant Physiol. 2002, 129, 1872-1879.
45. Gutiérez-Alcalá, G.; Gotor, C.; Meyer, A.J.; Fricker, M.; Vega, J.M.; Romeo, L.C. Glutathione biosynthesis in Arabidopsis trichome cells. Proc. Natl. Acad. Sci . USA 2000, 97, 11108-11113.
46. Bick, J.A.; Setterdahl, A.T.; Knaff, D.B.; Chen, Y.; Pitcher, L.H.; Zilinskas, B.A.; Leustek, T. Regulation of the plant-type 5-adenylsulfate reductase by oxidative stress. Biochemistry 2001, 40, 9040-9048.
47. Kazuki, S. Sulfur assimilatory metabolism: The long and smelling road. Plant Physiol. 2004, 136, 2443-2450.
48. Peer, W.A.; Baxter, I.R.; Richards, E.L.; Freeman, J.L.; Murphy, A.S. Phytoremediation and hyperaccumulator plants. In Molecular Biology of Metal Homeostasis and Detoxification; Tamás, M.J., Martinoia, E., Eds.; Springer: Heidelberg, Berlin, Germany, 2005; Volume 14, pp. 299-330.
49. Fernandes, A.P.; Holmgren, A. Glutaredoxin: Glutathione-dependent redox enzymes with functions far beyond a simple thioredoxin backup system. Antioxid. Redox Signal. 2004, 6, 63-74.
50. Duan, G.L.; Zhu, Y.G.; Tong, Y.P.; Cai, C.; Kneer, R. Characterization of arsenate reductase in the extract of roots and fronds of Chinese brake fern, an arsenic hyperaccumulator. Plant Physiol. 2005, 138, 461-469.
51. Sorrell, D.A.; Chrimes, D.; Dickinson, J.R.; Rogers, H.J.; Francis, D. The Arabidopsis CDC25 induces a short cell length when overexpressed in fission yeast: Evidence for cell cycle functions. New Phytol. 2005, 165, 425-428.
52. Landrieu, I.; Hassan, S.; Sauty, M.; Dewitte, F.; Wieruszeski, J.M.; Inzé, D.; de Veylder, L.; Lippens, G. Characterization of the Arabidopsis thaliana Arath; CDC25 dual-specificity tyrosine phosphatase. Biochem. Biophys. Res. Commun. 2004, 322, 734-739.
53. Ogasawara, Y.; Lacourciere, G.; Stadtman, T.C. Formation of a selenium-substituted rhodanese by reaction with selenite and glutathione: Possible role of a protein perselenide in a selenium delivery system. Proc. Natl. Acad. Sci. USA 2001, 98, 9494-9498.
54. Mukhopadhyay, R.; Shi, J.; Rosen, B.P. Purification and characterization of ACR2p, the Saccharomyces cerevisiae arsenate reductase. J. Biol. Chem. 2000, 275, 21149-21157.
55. 5R motif is required for catalytic activity of the Saccharomyces cerevisiae Acr2p arsenate reductase. J. Biol. Chem. 2001, 276, 34738-34742.
56. Mukhopadhyay, R.; Zhou, Y.; Rosen, B.P. Directed evolution of a yeast arsenate reductase into a protein-tyrosine phosphatase. J. Biol. Chem. 2003, 278, 24476-24480.
57. Bleeker, P.M.; Hakvoort, H.W.; Bliek, M.; Souer, E.; Schat, H. Enhanced arsenate reduction by a Cdc25-like tyrosine phosphatase explains increased phytochelatin accumulation in arsenate-tolerant Holcus lanatus. Plant J. 2006, 45, 917-929.
58. Zhou, Y.; Bhattacharjee, H.; Mukhopadhyay, R. Bifunctional role of the leishmanial antimonate reductase LmACR2 as a protein tyrosine phosphatase. Mol. Biochem. Parasitol. 2006, 148, 161-168.
59. Dhankher, O.P.; Rosen, B.P.; McKinney, E.C.; Meagher, R.B. Hyper-accumulation of arsenic in the shoots of Arabidopsis silenced for arsenate reductase, ACR2. Proc. Natl. Acad. Sci. USA 2006, 103, 5413-5418.
60. Leonard, A.; Lauwerys, R. Carcinogenicity, teratogenicity, and mutagenicity of arsenic. Mutat. Res. 1980, 75, 49-62.
61. Helleday, T.; Nilsson, R.; Jenssen D. Arsenic (III) and heavy metal ions induce intrachromosomal homologous recombination in the hprt gene of V79 Chinese hamster cells. Environ. Mol. Mutagen. 2000, 35, 114-122.
62. Chou, W.C.; Jie, C.; Kenedy, A.A.; Jones, R.J.; Trush, M.A.; Dang, C.V. Role of NADPH oxidase in arsenic-induced reactive oxygen species formation and cytotoxicity in myeloid leukemia cells. Proc. Natl. Acad. Sci. USA 2004, 101, 4578-4583.
63. Carbonell, A.A.; Aarabi, M.A.; Delaune, R.D.; Grambrell, R.P.; Patrick, W.H. Arsenic in wetland vegetation: Availability, phytotoxicity, uptake and effects on plants growth and nutrition. Sci. Total Environ. 1998, 217, 189-199.
64. Shah, K.; Nongkynrih, J.M. Metal hyperaccumulation and bioremediation. Biol. Plant. 2007, 51, 618-634.
65. Li, R.; Haile, J.D.; Kennelly, P.J. An arsenate reductase from Synechocystis sp. strain PCC 6803 exhibits a novel combination of catalytic characteristics. J. Bacteriol. 2003, 185, 6780-6789.
66. Shipley, S.; Nordin, A.B.; Tang, C.G.; Kim, S.K. Phytoremediation for arsenic contamination: Arsenate reductase. The Pulse 2008, 6, 1-12.