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Antioxidant gene expression and function in in vitro-developing Schistosoma mansoni mother sporocysts: possible role in self-protection

Published online by Cambridge University Press:  20 April 2007

J. J. VERMEIRE  and
T. P. YOSHINO
J. J. VERMEIRE*
Affiliation:
Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, 2115 Observatory Drive, Madison, WI 53706, USA
T. P. YOSHINO
Affiliation:
Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, 2115 Observatory Drive, Madison, WI 53706, USA
*
*Corresponding author: Present address: Program in International Child Health and Department of Pediatrics, Yale University School of Medicine, 464 Congress Avenue, New Haven, CT 06520-8081, USA. Tel: +1 203 737 4063. Fax: +1 203 737 3972. E-mail address: jon.vermeire@yale.edu
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Summary

The ability of the larval forms of Schistosoma mansoni to invade and parasitize their molluscan host, Biomphalaria glabrata, is determined by a multitude of factors. In this study we sought to elucidate the possible mechanisms by which the invading larvae are able to counteract the potentially harmful oxidative environment presented by the host upon initial miracidial infection. This was attempted by examining the gene expression profile of parasite antioxidant enzymes of the linked glutathione-(GSH) thioredoxin (Trx) redox pathway during early intramolluscan larval development. Three such enzymes, the peroxiredoxins (Prx1, Prx2 and Prx3) were examined as to their activity and sites of expression within S. mansoni miracidia and in vitro-cultured mother sporocysts. Results of these studies demonstrated that the H2O2-reducing enzymes Prx1 and 2 are upregulated during early mother sporocyst development compared to miracidia. Immunolocalization studies further indicated that Prx1 and Prx2 proteins are expressed within the apical papillae of miracidia and tegumental syncytium of sporocysts, and are released with parasite excretory-secretory proteins (ESP) during in vitro larval transformation. Removal of Prx1 and Prx2 from larval ESP by immunoabsorption significantly reduced the ability of ESP to breakdown exogenous H2O2, thereby directly linking ESP Prx proteins with H2O2-scavenging activity. Moreover, exposure of live sporocysts to exogenous H2O2 stimulated an upregulation of Prx1 and 2 gene expression suggesting the involvement of H2O2–responsive elements in regulating larval Prx gene expression. These data provide evidence that Prx1 and Prx2 may function in the protection of S. mansoni sporocysts during the early stages of infection.

Keywords

Schistosoma mansonimiracidiasporocystBiomphalaria glabratahydroperoxide metabolismantioxidantthioredoxinperoxiredoxinhaemocyte
Type
Research Article
Information
Parasitology , Volume 134 , Issue 10 , September 2007 , pp. 1369 - 1378
Copyright
Copyright © Cambridge University Press 2007

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