Characterization of the methionine sulfoxide reductases of schistosoma mansoni

Journal of Parasitology

Volumn 95, Issue 6, 2009, Pages 1421-1428

  Oke, Tolulope T ^a   Moskovitz, Jackob ^b   Williams, David L ^a,c  

^a ILLINOIS STATE UNIVERSITY   (United States)

^b UNIVERSITY OF KANSAS   (United States)

^c RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; CYSTEINE DERIVATIVE; METHIONINE; METHIONINE SULFOXIDE; METHIONINE SULFOXIDE REDUCTASE; METHIONINE SULFOXIDE REDUCTASE B; OXIDIZING AGENT; REACTIVE OXYGEN METABOLITE; RECOMBINANT PROTEIN; ZINC;

ANTIOXIDANT; CAUSE OF DEATH; ENZYME ACTIVITY; GENE EXPRESSION; HOST-PARASITE INTERACTION; INFECTIOUS DISEASE; PARASITOLOGY; POLYMERASE CHAIN REACTION; PROTEIN; PUBLIC HEALTH; SCHISTOSOMIASIS; SYMPTOM;

ARTICLE; CATALYSIS; DEVELOPMENTAL STAGE; DISEASE SEVERITY; EGG; ENZYME ANALYSIS; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; FEMALE; GENE; HOST PARASITE INTERACTION; MALE; MOLECULAR CLONING; MSRB1 GENE; MSRB2 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; SYMPTOM; AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; ANIMAL; BIOMPHALARIA; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MOUSE; OXIDATION REDUCTION REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT;

SCHISTOSOMA; SCHISTOSOMA MANSONI;

AMINO ACID SEQUENCE; ANIMALS; BIOMPHALARIA; CLONING, MOLECULAR; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MALE; METHIONINE; METHIONINE SULFOXIDE REDUCTASES; MICE; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; RECOMBINANT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SCHISTOSOMA MANSONI; SEQUENCE ALIGNMENT;

EID: 76749120427     PISSN: 00223395     EISSN: None     Source Type: Journal    
DOI: 10.1645/GE-2062.1     Document Type: Article

References (51)

1. ABRAMS, W. R., G. WEINBAUM, L. WEISSBACH, H. WEISSBACH, AND N. BROT. 1981. Enzymatic reduction of oxidized a-1-proteinase inhibitor restores biological activity. Proceedings of the National Academy of Sciences of the United States of America 78: 7483-7486.
2. ALGER, H. M., A. A. SAYED, M. J. STADECKER, AND D. L. WILLIAMS. 2002. Molecular and enzymatic characterisation of Schistosoma mansoni thioredoxin. International Journal for Parasitology 32: 1285-1292.
3. AND D. L. WILLIAMS. 2002. The disulfide redox system of Schistosoma mansoni and the importance of a multifunctional enzyme, thioredoxin glutathione reductase. Molecular and Biochemical Parasitology 121: 129-139.
4. BAR-NOY, S., AND J. MOSKOVITZ. 2002. Mouse methionine sulfoxide reductase B: Effect of selenocysteine incorporation on its activity and expression of the seleno-containing enzyme in bacterial and mammalian cells. Biochemical and Biophysical Research Communications 297: 956-961.
5. BOSCHI-MULLER, S., S. AZZA, S. SQANGLIER-CIANFERANI, F. TALFOURNIER, A. VAN DORSSELEAR, AND G. BRANLANT. 2000. A sulfenic acid enzyme intermediate is involved in the catalytic mechanism of peptide methionine sulfoxide reductase from Escherichia coli. Journal of Biological Chemistry 275: 35908-35913.
6. A. OLRY, M. ANTOINE, AND G. BRANLANT. 2005. The enzymology and biochemistry of methionine sulfoxide reductase. Biochimica et Biophysica Acta 1703: 231-238.
7. BROT, N., L. WEISSBACH, J. WERTH, AND H. WEISSBACH. 1981. Enzymatic reduction of protein-bound methionine sulfoxide. Proceedings of the National Academy of Sciences of the United States of America 78: 2155-2158.
8. CALLAHAN, H. L., R. K. CROUCH, AND E. R. JAMES. 1988. Helminth antioxidant enzymes: A protective mechanism against host oxidants? Parasitology Today 4: 218-225.
9. CASS, C. L., J. R. JOHNSON, L. L. CALIFF, T. XU, H. J. HERNANDEZ, M. J. STADECKER, J. R. YATES III, AND D. L. WILLIAMS. 2007. Proteomic analysis of Schistosoma mansoni egg secretions. Molecular and Biochemical Parasitology 155: 84-93.
10. CIOLI, D., C. VALLE, F. ANGELUCCI, AND A. E. MIELE. 2008. Will new antischistosomal drugs finally emerge? Trends in Parasitology 24: 379-382.
11. DAMIAN, R. T. 1987. The exploitation of host immune responses by parasites. Journal of Parasitology 73: 3-13.
12. DAUGHERTY, D. L., D. ROZEMA, P. P. HANSON, AND S. H. GELLMAN. 1998. Artificial chaperone-assisted refolding of citrate synthase. Journal of Biological Chemistry 273: 33961-33971.
13. DOENHOFF, M. J., D. CIOLI, AND J. UTZINGER. 2008. Praziquantel: Mechanisms of action, resistance and new derivatives for schistosomiasis. Current Opinion in Infectious Diseases 21: 659-667.
14. FEDOROV, A., A. F. MERICAN, AND W. GILBERT. 2002. Large-scale comparison of intron positions among animal, plant, and fungal genes. Proceedings of the National Academy of Sciences of the United States of America 99: 16128-16133.
15. HOTEZ, P. J., P. J. BRINDLEY, J. M. BETHONY, C. H. KING, E. J. PEARCE, AND J. JACOBSON. 2008. Helminth infections: The great neglected tropical diseases. Journal of Clinical Investigations 118: 1311-1321.
16. JANOFF, A., H. CARP, P. LAURENT, AND L. RAJU. 1983. The role of oxidative processes in emphysema. American Review of Respiratory Disease 127: 31-38.
17. KIM, H., AND V. GLADYSHEV. 2004. Methionine sulfoxide reduction in mammals: Characterization of methionine-R-sulfoxide reductases. Molecular and Cellular Biology 15: 1055-1064.
18. KUMAR, R. A., A. KOC, R. L. CERNY, AND V. N. GLADYSHEV. 2002. Reaction mechanism, evolutionary analysis and role of zinc in Drosophila methionine-R-sulfoxide reductase. Journal of Biological Chemistry 277: 37527-37535.
19. KUNTZ, A. N., E. DAVIOUD-CHARVET, A. A. SAYED, L. L. CALIFF, J. DESSOLIN, E. S. ARNÉR, AND D. L. WILLIAMS. 2007. Thioredoxin glutathione reductase from Schistosoma mansoni: An essential parasite enzyme and a key drug target. PLoS Medicine 4: e206.
20. KWATIA, M. A., D. J. BOTKIN, AND D. L. WILLIAMS. 2000. Molecular and enzymatic characterization of Schistosoma mansoni thioredoxin peroxidase. Journal of Parasitology 86: 908-915.
21. LEWIS, F. 1998. Schistosomiasis. In Current protocols in immunology, J. E. Coligan, A. M. Kruisbeek, D. H. Margulies, E. M. Shevach, and W. Strober (eds.). John Wiley & Sons Inc., New York, New York (Suppl. 28), p. 19.1.1-19.1.28.
22. LILLIG, C. H., AND A. HOLMGREN. 2007. Thioredoxin and related molecules-from biology to health and disease. Antioxidants and Redox Signaling 9: 25-47.
23. LIVAK, K. J., AND T. D. SCHMITTGEN. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 22DDCt method. Methods 25: 402-408.
24. LOVERDE, P. T. 1998. Do antioxidants play a role in schistosome hostparasite interactions? Parasitology Today 4: 157-162.
25. MEI, H., AND P. T. LOVERDE. 1997. Schistosoma mansoni: The developmental regulation and immunolocalization of antioxidant enzymes. Experimental Parasitology 86: 69-78.
26. MKOJI, G. M., J. M. SMITH, AND R. K. PRICHARD. 1988. Antioxidant systems in Schistosoma mansoni: Correlation between susceptibility to oxidant killing and the levels of scavengers of hydrogen peroxide and oxygen free radicals. International Journal for Parasitology 18: 661-666.
27. MOSKOVITZ, J. 2005. Methionine sulfoxide reductases: Ubiquitous enzymes involved in antioxidant defense, protein regulation, and prevention of aging-associated diseases. Biochimica Biophysica Acta 1703: 213-219.
28. S. BAR-NOY, W. WILLIAMS, J. REQUENA, B. S. BERLETT, AND E. R. STADMAN. 2001. Methionine sulfoxide reductase (MsrA) is a regulator of antioxidant defense and lifespan in mammals. Proceedings of the National Academy of Sciences of the United States of America 98: 12920-12925.
29. B. S. BERLETT, J. M. POSTON, AND E. R. STADTMAN. 1997. The yeast peptide-methionine sulfoxide reductase functions as an antioxidant in vivo. Proceedings of the National Academy of Sciences of the United States of America 94: 9585-9589.
30. 1998. Methionine sulfoxide reductase in antioxidant defense. Methods in Enzymology 300: 239-244.
31. E. FLESCHER, B. S. BERLETT, J. AZARE, J. M. POSTON, AND E. R. STADTMAN. 1998. Overexpression of peptide-methionine sulfoxide reductase in Saccharomyces cerevisiae and human T cells provides them with high resistance to oxidative stress. Proceedings of the National Academy of Sciences of the United States of America 95: 14071-14075.
32. J. M. POSTON, B. S. BERLETT, N. J. NOSWORTHY, R. SZCZEPANOWSKI, AND E. R. STADTMAN. 2000. Identification and characterization of a putative active site for peptide methionine sulfoxide reductase (MsrA) and its substrate stereospecificity. Journal of Biological Chemistry 275: 14167-14172.
33. M. A. RAHMAN, J. STRASSMAN, S. O. YANCEY, S. R. KUSHNER, H. WEISSBACH, AND N. BROT. 1995. Escherichia coli peptide methionine sulfoxide reductase gene: Regulation of expression and role in protecting against oxidative damage. Journal of Bacteriology 177: 502-507.
34. V. K. SINGH, J. REQUENA, B. J.WILKINSON, R. K. JAYASWAL, AND E. R. STADTMAN. 2002. Purification and characterization of methionine sulfoxide reductases from mouse and Staphylococcus aureus and the substrate stereospecificity. Biochemical and Biophysical Research Communications 290: 62-65.
35. H. WEISSBACH, AND N. BROT. 1996. Cloning the expression of a mammalian gene involved in the reduction of methionine sulfoxide residues in proteins. Proceedings of the National Academy of Sciences of the United States of America 93: 2095-2099.
36. NEIERS, F., A. KRIZNIK, S. BOSCHI-MULLER, AND G. BRANLANT. 2004. Evidence for a new sub-class of methionine sulfoxide reductases B with an alternative thioredoxin recognition signature. Journal of Biological Chemistry 279: 42462-42468.
37. RODRIGO, M. J., J.MOSKOVITZ, F. SALAMINI, AND D. BARTELS. 2002. Reverse genetic approaches in plants and yeast suggest a role for novel, evolutionarily conserved, selenoprotein-related genes in oxidative stress defense. Molecular Genetics and Genomics 267: 613-621.
38. ROMERO, H. M., B. S. BERLETT, P. J. JENSEN, E. J. PELL, AND M. TIEN. 2004. Investigations into the role of the plastidial peptide methionine sulfoxide reductase in response to oxidative stress in Arabidopsis. Plant Physiology 136: 3784-3794.
39. RUAN, H., X. D. TANG, M. L. CHEN, M. L. JOINER, G. SUN, N. BROT, H. WEISSBACH, S. H. HEINEMANN, L. IVERSON, C. F. WU, ET AL. 2002. High-quality life extension by the enzyme peptide methionine sulfoxide reductase. Proceedings of the National Academy of Sciences of the United States of America 99: 2748-2753. (Pubitemid 34240532)
40. SAYED, A. A., S. K. COOK, AND D. L. WILLIAMS. 2006. Redox balance mechanisms in Schistosoma mansoni rely on peroxiredoxins and albumin and implicate peroxiredoxins as novel drug targets. Journal of Biological Chemistry 281: 17001-17010.
41. A. SIMEONOV, C. J. THOMAS, J. INGLESE, C. P. AUSTIN, AND D. L. WILLIAMS 2008. Identification of oxadiazoles as new drug leads for the control of schistosomiasis. Nature Medicine 14 407-412.
42. D. L. WILLIAMS. 2004. Biochemical characterization of 2-Cys peroxiredoxins from Schistosoma mansoni. Journal of Biological Chemistry 279: 26159-26166.
43. SIMEONOV, A., A. JADHAV, A. A. SAYED, Y. WANG, M. E. NELSON, C. J. THOMAS, J. INGLESE, D. L. WILLIAMS, AND C. P. AUSTIN. 2008. Quantitative high-throughput screen identifies inhibitors of the Schistosoma mansoni redox cascade. PLoS Neglected Tropical Diseases 2: e127.
44. SINGH, V. K., J. MOSKOVITZ, B. J.WILKINSON, AND R. K. JAYASWAL. 2001. Molecular characterization of a chromosomal locus in Staphylococcus aureus that contributes to oxidative defence and is highly induced by the cell-wall-active antibiotic oxacillin. Microbiology 147: 3037-3045. (Pubitemid 33076992)
45. STEINMANN, P., J. KEISER, R. BOS, M. TANNER, AND J. UTZINGER. 2006. Schistosomiasis and water resources development: Systematic review, meta-analysis, and estimates of people at risk. Lancet Infectious Disease 6: 411-425.
46. TOWNSEND, D. M., K. D. TEW, AND H. TAPIERO. 2003. The importance of glutathione in human disease. Biomedicine and Pharmacotherapy 57: 145-155.
47. VAN DER WERF, M. J., S. J. DE VLAS, S. BROOKER, C. W. LOOMAN, N. J. NAGELKERKE, J. D. HABBEMA, AND D. ENGELS. 2003. Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Tropica 86: 125-139.
48. VERMUND, S. H., D. J. BRADLEY, AND E. RUIZ-TIBEN. 1983. Survival of Schistosoma mansoni in the human host: Estimates from a community-based prospective study in Puerto Rico. American Journal of Tropical Medicine and Hygiene 32: 1040-1048.
49. VIEIRA DOS SANTOS, C., S. CUINE, N. ROUHIER, AND P. REY. 2005. The Arabidopsis plastidic methionine sulfoxide reductase B proteins. Sequence and activity characteristics, comparison of the expression with plastidic methionine sulfoxide reductase A, and induction by photooxidative stress. Plant Physiology 138: 909-922.
50. E. LAUGIER, L. TARRAGO, V.MASSOT, E. ISSAKIDIS-BOURGUET, N. ROUHIER, AND P. REY. 2007. Specificity of thioredoxins and glutaredoxins as electron donors to two distinct classes of Arabidopsis plastidial methionine sulfoxide reductases B. FEBS Letters 581: 4371-4376.
51. WILLIAMS, D. L., H. ASAHI, D. J. BOTKIN, AND M. J. STADECKER. 2001. Schistosome infection stimulates host CD4(+) T helper cell and B-cell responses against a novel egg antigen, thioredoxin peroxidase. Infection and Immunity 69: 1134-1141.