Role of the endogenous antioxidant system in the protection of Schistosoma mansoni primary sporocysts against exogenous oxidative stress

PLoS Neglected Tropical Diseases

Volumn 3, Issue 11, 2009, Pages

  Mourão, Marina De Moraes ^a   Dinguirard, Nathalie ^b   Franco, Glória R ^a   Yoshino, Timothy P ^b  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; GLUTATHIONE TRANSFERASE 26; GLUTATHIONE TRANSFERASE 28; GREEN FLUORESCENT PROTEIN; HYDROGEN PEROXIDE; PEROXIREDOXIN 1; PEROXIREDOXIN 2; RNA; UNCLASSIFIED DRUG; ANTIOXIDANT; HELMINTH PROTEIN; SUPEROXIDE DISMUTASE;

ANTIOXIDANT ACTIVITY; ARTICLE; BIOMPHALARIA GLABRATA; BLOOD CELL; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ENZYME ACTIVITY; IN VITRO STUDY; INCUBATION TIME; LARVAL STAGE; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; SCHISTOSOMA MANSONI; SPOROCYST; WESTERN BLOTTING; ANIMAL; DISEASE MODEL; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MOUSE; OOCYST; PARASITOLOGY; SCHISTOSOMIASIS MANSONI; SNAIL;

ANIMALS; ANTIOXIDANTS; DISEASE MODELS, ANIMAL; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; HELMINTH PROTEINS; HUMANS; HYDROGEN PEROXIDE; MICE; OOCYSTS; OXIDATIVE STRESS; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; SNAILS; SUPEROXIDE DISMUTASE;

EID: 73449138216     PISSN: None     EISSN: None     Source Type: Journal    
DOI: 10.1371/journal.pntd.0000550     Document Type: Article

References (40)

1. Bayne CJ, Hahn UK, Bender RC (2001) Mechanisms of molluscan host resistance and of parasite strategies for survival. Parasitology 123 Suppl: 59-67.
2. Bayne CJ (2009) Successful parasitism of vector snail Biomphalaria glabrata by the human blood fluke (trematode) Schistosoma mansoni: a 2009 assessment. Mol Biochem Parasitol 165: 8-18.
3. Bender RC, Bixler LM, Lerner JP, Bayne CJ (2002) Schistosoma mansoni sporocysts in culture: host plasma hemoglobin contributes to in vitro oxidative stress. J Parasitol 88: 14-18.
4. Hahn UK, Bender RC, Bayne CJ (2000) Production of reactive oxygen species by hemocytes of Biomphalaria glabrata: carbohydrate-specific stimulation. Dev Comp Immunol 24: 531-541.
5. Hahn UK, Bender RC, Bayne CJ (2001) Killing of Schistosoma mansoni sporocysts by hemocytes from resistant Biomphalaria glabrata: role of reactive oxygen species. J Parasitol 87: 292-299.
6. Hahn UK, Bender RC, Bayne CJ (2001) Involvement of nitric oxide in killing of Schistosoma mansoni sporocysts by hemocytes from resistant Biomphalaria glabrata. J Parasitol 87: 778-785.
7. Zelck UE, Von Janowsky B (2004) Antioxidant enzymes in intramolluscan Schistosoma mansoni and ROS-induced changes in expression. Parasitology 128: 493-501.
8. Sayed AA, Williams DL (2004) Biochemical characterization of 2-Cys peroxiredoxins from Schistosoma mansoni. J Biol Chem 279: 26159-26166.
9. Guillou F, Roger E, Mone Y, Rognon A, Grunau C, et al. (2007) Excretory-secretory proteome of larval Schistosoma mansoni and Echinostoma caproni, two parasites of Biomphalaria glabrata. Mol Biochem Parasitol 155: 45-56.
10. Roger E, Mitta G, Mone Y, Bouchut A, Rognon A, et al. (2008) Molecular determinants of compatibility polymorphism in the Biomphalaria glabrata/ Schistosoma mansoni model: New candidates identified by a global comparative proteomics approach. Mol Biochem Parasitol 157: 205-216.
11. Vermeire JJ, Yoshino TP (2007) Antioxidant gene expression and function in in vitro-developing Schistosoma mansoni mother sporocysts: possible role in selfprotection. Parasitology 134: 1369-1378.
12. Williams DL, Sayed AA, Bernier J, Birkeland SR, Cipriano MJ, et al. (2007) Profiling Schistosoma mansoni development using serial analysis of gene expression (SAGE). Exp Parasitol 117: 246-258.
13. Taft AS, Vermeire JJ, Bernier J, Birkeland SR, Cipriano MJ, et al. (2009) Transcriptome analysis of Schistosoma mansoni larval development using serial analysis of gene expression (SAGE). Parasitology 136: 469-485.
14. Wu XJ, Sabat G, Brown JF, Zhang M, Taft A, et al. (2009) Proteomic analysis of Schistosoma mansoni proteins released during in vitro miracidium-to-sporocyst transformation. Mol Biochem Parasitol 164: 32-44.
15. Mei H, Thakur A, Schwartz J, Lo Verde PT (1996) Expression and characterization of glutathione peroxidase activity in the human blood fluke Schistosoma mansoni. Infect Immun 64: 4299-4306.
16. Sayed AA, Cook SK, Williams DL (2006) Redox balance mechanisms in Schistosoma mansoni rely on peroxiredoxins and albumin and implicate peroxiredoxins as novel drug targets. J Biol Chem 281: 17001-17010.
17. Kuntz AN, Davioud-Charvet E, Sayed AA, Califf LL, Dessolin J, et al. (2007) Thioredoxin glutathione reductase from Schistosoma mansoni: an essential parasite enzyme and a key drug target. PLoS Med 4: e206. Erratum in: PLoS Med 4: e264.
18. Loverde PT (1998) Do antioxidants play a role in schistosome host-parasite interactions? Parasitol Today 14: 284-289.
19. Yan F, Yang WK, Li XY, Lin TT, Lun YN, et al. (2008) A trifunctional enzyme with glutathione S-transferase, glutathione peroxidase and superoxide dismutase activity. Biochim Biophys Acta 1780: 869-872.
20. Kwatia MA, Botkin DJ, Williams DL (2000) Molecular and enzymatic characterization of Schistosoma mansoni thioredoxin peroxidase. J Parasitol 86: 908-915.
21. Simurda, MC, van Keulen H, Rekosh DM, LoVerde PT (1988) Schistosoma mansoni: Identification and analysis of an mRNA and a gene encoding superoxide dismutase (Cu/Zn). Exp Parasitol 67: 73-84.
22. Williams DL, Pierce RJ, Cookson E, Capron A (1992) Molecular cloning and sequencing of glutathione peroxidase from Schistosoma mansoni. Mol Biochem Parasitol 52: 127-130.
23. Mkoji GM, Smith JM, Prichard RK (1988) Antioxidant systems in Schistosoma mansoni: correlation between susceptibility to oxidant killing and the levels of scavengers of hydrogen peroxide and oxygen free radicals. Int J Parasitol 18: 661-666.
24. Mkoji GM, Smith JM, Prichard RK (1988) Antioxidant systems in Schistosoma mansoni: evidence for their role in protection of the adult worms against oxidant killing. Int J Parasitol 18: 667-673.
25. Mourão MM, Dinguirard N, Franco GR, Yoshino TP (2009) Phenotypic screen of early-developing larval blood flukes, Schistosoma mansoni, using RNA interference. PLoS Negl Trop Dis 3(8): e502.
26. Boyle JP, Wu XJ, Shoemaker CB, Yoshino TP (2003) Using RNA interference to manipulate endogenous gene expression in Schistosoma mansoni sporocysts. Mol Biochem Parasitol 12: 205-215.
27. Yoshino TP, Laursen JR (1995) Production of Schistosoma mansoni daughter sporocysts from mother sporocysts maintained in synxenic culture with Biomphalaria glabrata embryonic (Bge) cells. J Parasitol 81: 714-722.
28. Chernin E (1963) Observations on hearts explanted in vitro from the snail Australorbis glabratus. J Parasitol 49: 353-364.
29. Sambrook J, Fritsch EF, Maniatis T (1989) SDS-Polyacrylamide gel electrophoresis of proteins. In: Ford N, Nolan C, Ferguson M, eds. Molecular cloning Cold Spring Harbor Laboratory Press. pp 18.47-18.75.
30. Yoshino TP (1981) Comparison of concanavalin A-reactive determinants on hemocytes of two Biomphalaria glabrata snail stocks: Receptor binding and redistribution. Dev Comp Immunol 5: 229-240.
31. Sminia T, Barendsen LA (1978) Comparative morphological and enzyme histochemical study on blood cells of the freshwater snail Lymnaea stagnalis, Biomphalaria glabrata and Bulinus truncates, J Morphol 16: 31-39.
32. Goodall CP, Bender RC, Broderick EJ, Bayne CJ (2004) Constitutive differences in Cu/Zn superoxide dismutase mRNA levels and activity in hemocytes of Biomphalaria glabrata (Mollusca) that are either susceptible or resistant to Schistosoma mansoni (Trematoda). Mol Biochem Parasitol 137: 321-328.
33. Bender RC, Broderick EJ, Goodall CP, Bayne CJ (2005) Respiratory burst of Biomphalaria glabrata hemocytes: Schistosoma mansoni-resistant snails produce more extracellular H2O2 than susceptible snails. J Parasitol 91: 275-279.
34. Goodall CP, Bender RC, Brooks JK, Bayne CJ (2006) Biomphalaria glabrata cytosolic copper/zinc superoxide dismutase (SOD1) gene: association of SOD1 alleles with resistance/susceptibility to Schistosoma mansoni. Mol Biochem Parasitol 147: 207-210.
35. Bender RC, Goodall CP, Blouin MS, Bayne CJ (2007) Variation in expression of Biomphalaria glabrata SOD1: a potential controlling factor in susceptibility/ resistance to Schistosoma mansoni.
36. Alger HM, Williams DL (2002) The disulfide redox system of Schistosoma mansoni and the importance of a multifunctional enzyme, thioredoxin glutathione reductase. Mol Biochem Parasitol 121: 129-139.
37. Fitzpatrick JM, Peak E, Perally S, Chalmers IW, Barrett J, et al. (2009) Anti-schistosomal candidate molecules identified by lifecycle transcriptomic analyses. PLoS Negl Trop Dis 3: In press.
38. Bayne CJ, Buckley PM, DeWan PC (1980) Schistosoma mansoni: cytotoxicity of hemocytes from susceptible snail hosts for sporocysts in plasma from resistant Biomphalaria glabrata. Exp Parasitol 50: 409-416.
39. Simurda MC, van Keulen KH, Rekosh DM, LoVerde PT (1988) Schistosoma mansoni: Idenfication and analysis of an mRNA and a gene encoding superoxide dismutase (Cu/Zn). Exp Parasitol 67: 73-84.
40. Li LC, Okino ST, Zhao H, Pookot D, Place RF, et al. (2006) Small dsRNAs induce transcriptional activation in human cells. Proc Natl Acad Sci USA 103: 17337-17342.