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Pharmacological and autoradiographical characterization of serotonin transporter-like activity in sporocysts of the human blood fluke, Schistosoma mansoni

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Abstract

The present study focuses on the role of the biogenic monoamine serotonin (5-hydroxytryptamine) in the biology of sporocyst stages of the human blood fluke, Schistosoma mansoni, and its importance during obligate development within its snail host Biomphalaria glabrata. Based on previous work demonstrating that snails infected with S. mansoni have reduced levels of 5-hydroxytryptamine, we hypothesized that sporocysts actively transport this molecule from the host milieu. Intact sporocysts isolated in vitro take up exogenous 5-hydroxytryptamine via a high-affinity mechanism (K m=1.4 μmol l−1), and this serotonin transporter-like activity is dependent upon extracellular Na+ and Cl− and is highly sensitive to previously characterized serotonin transporter inhibitors. Autoradiography suggests that transported [3H]5-hydroxytryptamine localizes within the body of the sporocyst, and in many cases is found in apical gland cells. Moreover, serotonin transporter-like activity is absent in free-swimming miracidia, the infective stage for the snail host, and the increase in larval serotonin transporter-like activity after miracidium-to-sporocyst transformation is accompanied by a corresponding decrease in steady-state levels of transcripts for tryptophan hydroxylase, the rate-limiting enzyme in serotonin biosynthesis. Overall our data suggest that S. mansoni larvae express surface-exposed serotonin transporter-like molecules, and that the transition from free-living miracidium to parasitic mother sporocyst is characterized by an increased dependence upon exogenous 5-hydroxytryptamine.

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Fig. 1A–C.
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Abbreviations

5-HT:

5-hydroxytryptamine

CBSS:

Chernin's balanced salt solution

SERT:

serotonin transporter

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Acknowledgements

The authors wish to thank Laura Johnston and Kate Zachman for technical assistance, and Dr. Fred Lewis (Biomedical Research Institute, Rockville, MD, USA) and Dr. Jim Tracy (University of Wisconsin-Madison) for providing infected mice. Dr. John Svaren (University of Wisconsin-Madison) and members of his laboratory were extremely helpful in the design and analysis of qPCR experiments. This research was supported by Individual NIH predoctoral NRSA No. MH12992 to J.P.B., NIH Grant Nos. AI38263 and AI15503 to T.P.Y. and NIAID schistosome supply contract No. AI55270 to Dr. Lewis. All experimental protocols involving animals complied with the Principles of animal care, revised 1985 of the National Institutes of Health publication no. 86-23.

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Authors and Affiliations

  1. Department of Animal Health and Biomedical Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, 1656 Linden Drive West, Madison, WI 53706, USA

    J. P. Boyle & J. F. Hillyer

  2. Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, 2115 Observatory Drive, Madison, WI 53706, USA

    T. P. Yoshino

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  1. J. P. Boyle
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Correspondence to T. P. Yoshino.

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Boyle, J.P., Hillyer, J.F. & Yoshino, T.P. Pharmacological and autoradiographical characterization of serotonin transporter-like activity in sporocysts of the human blood fluke, Schistosoma mansoni . J Comp Physiol A 189, 631–641 (2003). https://doi.org/10.1007/s00359-003-0429-8

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