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New insights into the reaction of Schistosoma mansoni cercaria to the human complement system

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Abstract

Schistosomes are parasitic worms that have a complex life cycle. The larval stage cercaria, infectious to mammals, is described as highly susceptible to the complement system, largely due to the glycocalyx that covers the cercarial membrane. In an attempt to have a more complete understanding of cercaria reaction to the complement system, three different approaches were used. Live cercariae exposed to normal human serum (NHS) as source of complement factors were assessed for (i) membrane attack complex (MAC) deposition on the parasite surface, (ii) cercaria survival rate by Hoechst staining of parasite DNA, and (iii) transformation into schistosomula by detection of the glucose transporter protein 4 (SGTP4), a marker for new tegument formation. We found that 82–95 % of cercariae directly exposed to NHS for 18 h were viable and retained their ability to shed the glycocalyx, suggesting minimal tegument damage. In contrast, inhibition of glycocalyx shedding using eserine caused significant MAC binding and parasite death. Culturing complement-exposed cercariae to measure long-term survival showed that more parasites died over time, reaching a survival rate of 18–31 % by day 6 in culture. The reason for this slow death is unknown, but the surviving parasites were able to form a new tegument as shown by detection of SGTP4 on the parasite surface. Furthermore, we found that complement activation significantly damaged the acetabular gland ducts and lysed secretory vesicles released by transforming cercariae. These findings should contribute for future in vivo studies of the effects of the complement system in skin migrating cercariae.

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Acknowledgments

This work was supported by the National Institutes of Health, the National Institute of Allergy and Infectious Diseases (NIH-NIAID), grant AI-095893 to G.K.P. We thank Dr. Patrick Skelly and Dr. Charles Shoemaker from Tufts University, Cumming School of Veterinary Medicine, MA, USA for helpful comments and Dr. Anne Nicholson-Weller from Beth Israel Deaconess Medical Center, MA, USA for advice on the lytic pathway of the complement system. Infected snails were provided by BRI via the NIAID schistosomiasis resource center under NIH-NIAID Contract no. HHSN272201000005I. Parasites were kindly provided by Dr. Skelly through NIH-NIAID Grant AI-056273.

Ethical standards

These studies did not use animal or human subjects. All procedures and analyses in support of this original research were performed in accordance with the ethical standards of the institution.

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The authors declare that they have no conflict of interest.

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Correspondence to Greice Krautz-Peterson.

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Da’dara, A.A., Krautz-Peterson, G. New insights into the reaction of Schistosoma mansoni cercaria to the human complement system. Parasitol Res 113, 3685–3696 (2014). https://doi.org/10.1007/s00436-014-4033-3

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  • DOI: https://doi.org/10.1007/s00436-014-4033-3

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