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Adult somatic stem cells in the human parasite Schistosoma mansoni

Nature volume 494, pages 476–479 (2013)Cite this article

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Abstract

Schistosomiasis is among the most prevalent human parasitic diseases, affecting more than 200 million people worldwide1. The aetiological agents of this disease are trematode flatworms (Schistosoma) that live and lay eggs within the vasculature of the host. These eggs lodge in host tissues, causing inflammatory responses that are the primary cause of morbidity. Because these parasites can live and reproduce within human hosts for decades2, elucidating the mechanisms that promote their longevity is of fundamental importance. Although adult pluripotent stem cells, called neoblasts, drive long-term homeostatic tissue maintenance in long-lived free-living flatworms3,4 (for example, planarians), and neoblast-like cells have been described in some parasitic tapeworms5, little is known about whether similar cell types exist in any trematode species. Here we describe a population of neoblast-like cells in the trematode Schistosoma mansoni. These cells resemble planarian neoblasts morphologically and share their ability to proliferate and differentiate into derivatives of multiple germ layers. Capitalizing on available genomic resources6,7 and RNA-seq-based gene expression profiling, we find that these schistosome neoblast-like cells express a fibroblast growth factor receptor orthologue. Using RNA interference we demonstrate that this gene is required for the maintenance of these neoblast-like cells. Our observations indicate that adaptation of developmental strategies shared by free-living ancestors to modern-day schistosomes probably contributed to the success of these animals as long-lived obligate parasites. We expect that future studies deciphering the function of these neoblast-like cells will have important implications for understanding the biology of these devastating parasites.

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Figure 1: Proliferation of somatic cells in adult schistosomes.
Figure 2: Transcriptional profiling identifies genes expressed in proliferative cells.
Figure 3: PSCs self-renew and differentiate.
Figure 4: SmfgfrA is required for the maintenance of somatic stem cells.

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Primary accessions

Gene Expression Omnibus

Data deposits

RNA-seq analyses have been deposited in the NCBI Gene Expression Omnibus under accession number GSE42757.

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Acknowledgements

We thank R. Roberts-Galbraith, M. Issigonis and L. Rouhana for comments on the manuscript; R. King for sharing the cathepsin B plasmid and unpublished protocols; and A. Hernandez for assistance with Illumina sequencing. Schistosome-infected mice were provided by the NIAID Schistosomiasis Resource Center and the Biomedical Research Institute through NIAID contract no. HHSN272201000005I. This work was supported by: NIH F32 HD062124 (J.J.C.) and NIH R21 AI099642 (P.A.N.). P.A.N. is an investigator of the Howard Hughes Medical Institute.

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Authors and Affiliations

  1. Howard Hughes Medical Institute and Department of Cell and Developmental Biology, University of Illinois at Urbana-Champaign, Urbana, 61801, Illinois, USA

    James J. Collins III, Bo Wang, Bramwell G. Lambrus, Marla E. Tharp, Harini Iyer & Phillip A. Newmark

  2. Neuroscience Program, University of Illinois at Urbana-Champaign, Urbana, 61801, Illinois, USA

    James J. Collins III & Phillip A. Newmark

  3. Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, 61801, Illinois, USA

    Bo Wang

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Contributions

J.J.C., B.W., B.G.L., M.E.T. and H.I. performed experiments. J.J.C. and B.W. analysed data. J.J.C. and P.A.N. designed the study and wrote the paper.

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Correspondence to Phillip A. Newmark.

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The authors declare no competing financial interests.

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This file contains Supplementary Figures 1-9, a Supplementary Discussion, Supplementary Tables 2-3 and Supplementary References. (PDF 1610 kb)

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Collins III, J., Wang, B., Lambrus, B. et al. Adult somatic stem cells in the human parasite Schistosoma mansoni . Nature 494, 476–479 (2013). https://doi.org/10.1038/nature11924

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