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Septins of Platyhelminths: Identification, Phylogeny, Expression and Localization among Developmental Stages of Schistosoma mansoni

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      Abstract

      Septins are a family of eukaryotic GTP binding proteins conserved from yeasts to humans. Originally identified in mutants of budding yeast, septins participate in diverse cellular functions including cytokinesis, organization of actin networks, cell polarity, vesicle trafficking and many others. Septins assemble into heteroligomers to form filaments and rings. Here, four septins of Schistosoma mansoni are described, which appear to be conserved within the phylum Platyhelminthes. These orthologues were related to the SEPT5, SEPT10 and SEPT7 septins of humans, and hence we have termed the schistosome septins SmSEPT5, SmSEPT10, SmSEPT7.1 and SmSEPT7.2. Septin transcripts were detected throughout the developmental cycle of the schistosome and a similar expression profile was observed for septins in the stages examined, consistent with concerted production of these proteins to form heterocomplexes. Immunolocalization analyses undertaken with antibodies specific for SmSEPT5 and SmSEPT10 revealed a broad tissue distribution of septins in the schistosomulum and colocalization of septin and actin in the longitudinal and circular muscles of the sporocyst. Ciliated epidermal plates of the miracidium were rich in septins. Expression levels for these septins were elevated in germ cells in the miracidium and sporocyst. Intriguingly, septins colocalize with the protonephridial system of the cercaria, which extends laterally along the length of this larval stage. Together, the findings revealed that schistosomes expressed several septins which likely form filaments within the cells, as in other eukaryotes. Identification and localization demonstrating a broad distribution of septins across organs and tissues of schistosome contributes towards the understanding of septins in schistosomes and other flatworms.

      Author Summary

      Schistosoma mansoni is one of the causative agents of schistosomiasis, a neglected tropical disease affecting over 230 million people in the developing world. Research on new therapies for this parasitic disease has been facilitated by the recent publication of a curated draft sequence of the schistosome genome. Here, we describe proteins from the septin family found in the genome of S. mansoni. The septins are increasingly recognized as central components of the cytoskeleton of eukaryotic cells. They are linked to numerous cellular functions, although the precise role(s) of these proteins is not fully understood. Schistosome septins were seen in the miracidium and sporocyst larval stages, on superficial structures, within epidermal plates and in muscles. Notably, septins were prominently expressed in the germ cells of larval stages of the blood fluke. In addition, septins were ubiquitously immuno-localized throughout the organs and tissues of the schistosomulum stage of the parasite. This is the first report on septins in schistosomes; these proteins are broadly distributed among organs and tissues of the parasite where they likely perform diverse functions. Identification and localization demonstrating a broad distribution of septins across organs and tissues of schistosome contributes towards the understanding of septins in schistosomes and other flatworms.

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            Author and article information

            Affiliations
            [1 ]Departamento de Física e Informática, Instituto de Física de São Carlos, Universidade de São Paulo, São Carlos, São Paulo, Brazil
            [2 ]Department of Microbiology, Immunology & Tropical Medicine, and Research Center for Neglected Tropical and Infectious Diseases of Poverty, School of Medicine & Health Sciences, The George Washington University, Washington, D.C., United States of America
            [3 ]Departamento de Genética, Facultad de Medicina, Universidad de la República (UDELAR), Montevideo, Uruguay
            [4 ]Center for Microscopy and Image Analysis, The George Washington University, Washington, D.C., United States of America
            Rush University Medical Center, United States of America
            Author notes

            The authors have declared that no competing interests exist.

            Conceived and designed the experiments: AEZ GR APUA RDM PJB. Performed the experiments: AEZ GR AP. Analyzed the data: AEZ GR AP VHM APUA RDM PJB. Contributed reagents/materials/analysis tools: AEZ GR VHM RDM AP. Wrote the paper: AEZ GR VHM AP APUA RDM PJB.

            Contributors
            Role: Editor
            Journal
            PLoS Negl Trop Dis
            PLoS Negl Trop Dis
            plos
            plosntds
            PLoS Neglected Tropical Diseases
            Public Library of Science (San Francisco, USA )
            1935-2727
            1935-2735
            December 2013
            19 December 2013
            : 7
            : 12
            24367716 3868516 PNTD-D-13-00556 10.1371/journal.pntd.0002602

            This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

            Counts
            Pages: 14
            Funding
            This work was supported by NIH Shared Instrumentation Grant S10RR025565 and CNPq INCT-INBEQMeDI grant. AEZ received a CNPq and CAPES fellowship (BEX: 9193/11-1). RDM and APUA are recipients of productivity fellowships from CNPq. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
            Categories
            Research Article

            Infectious disease & Microbiology

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