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Rhesus macaques self-curing from a schistosome infection can display complete immunity to challenge

Author

Listed:
  • Murilo Sena Amaral

    (Laboratório de Parasitologia, Instituto Butantan)

  • Daisy Woellner Santos

    (Laboratório de Parasitologia, Instituto Butantan
    Instituto de Química, Universidade de Sao Paulo)

  • Adriana S. A. Pereira

    (Laboratório de Parasitologia, Instituto Butantan
    Instituto de Química, Universidade de Sao Paulo)

  • Ana Carolina Tahira

    (Laboratório de Parasitologia, Instituto Butantan)

  • João V. M. Malvezzi

    (Laboratório de Parasitologia, Instituto Butantan)

  • Patrícia Aoki Miyasato

    (Laboratório de Parasitologia, Instituto Butantan)

  • Rafaela de Paula Freitas

    (Laboratório de Parasitologia, Instituto Butantan)

  • Jorge Kalil

    (Heart Institute, Faculty of Medicine, University of Sao Paulo (USP))

  • Elisa M. Tjon Kon Fat

    (Leiden University Medical Center)

  • Claudia J. Dood

    (Leiden University Medical Center)

  • Paul L. A. M. Corstjens

    (Leiden University Medical Center)

  • Govert J. Dam

    (Leiden University Medical Center)

  • Eliana Nakano

    (Laboratório de Parasitologia, Instituto Butantan)

  • Simone de Oliveira Castro

    (Instituto Butantan, Biotério Central)

  • Vânia Gomes de Moura Mattaraia

    (Instituto Butantan, Biotério Central)

  • Ronaldo de Carvalho Augusto

    (LBMC, Laboratoire de Biologie et Modélisation de la Cellule Univ Lyon, ENS de Lyon, Université Claude Bernard Lyon 1, CNRS, UMR 5239, INSERM
    IHPE, Univ. Perpignan Via Domitia, CNRS, IFREMER, Univ Montpellier)

  • Christoph Grunau

    (IHPE, Univ. Perpignan Via Domitia, CNRS, IFREMER, Univ Montpellier)

  • R. Alan Wilson

    (York Biomedical Research Institute, Department of Biology, University of York, Heslington)

  • Sergio Verjovski-Almeida

    (Laboratório de Parasitologia, Instituto Butantan
    Instituto de Química, Universidade de Sao Paulo)

Abstract

The rhesus macaque provides a unique model of acquired immunity against schistosomes, which afflict >200 million people worldwide. By monitoring bloodstream levels of parasite-gut-derived antigen, we show that from week 10 onwards an established infection with Schistosoma mansoni is cleared in an exponential manner, eliciting resistance to reinfection. Secondary challenge at week 42 demonstrates that protection is strong in all animals and complete in some. Antibody profiles suggest that antigens mediating protection are the released products of developing schistosomula. In culture they are killed by addition of rhesus plasma, collected from week 8 post-infection onwards, and even more efficiently with post-challenge plasma. Furthermore, cultured schistosomula lose chromatin activating marks at the transcription start site of genes related to worm development and show decreased expression of genes related to lysosomes and lytic vacuoles involved with autophagy. Overall, our results indicate that enhanced antibody responses against the challenge migrating larvae mediate the naturally acquired protective immunity and will inform the route to an effective vaccine.

Suggested Citation

  • Murilo Sena Amaral & Daisy Woellner Santos & Adriana S. A. Pereira & Ana Carolina Tahira & João V. M. Malvezzi & Patrícia Aoki Miyasato & Rafaela de Paula Freitas & Jorge Kalil & Elisa M. Tjon Kon Fat, 2021. "Rhesus macaques self-curing from a schistosome infection can display complete immunity to challenge," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26497-0
    DOI: 10.1038/s41467-021-26497-0
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    1. Selena Ferrian & Claudia Manca & Sugnet Lubbe & Francesca Conradie & Nazir Ismail & Gilla Kaplan & Clive M Gray & Dorothy Fallows, 2017. "A combination of baseline plasma immune markers can predict therapeutic response in multidrug resistant tuberculosis," PLOS ONE, Public Library of Science, vol. 12(5), pages 1-15, May.
    2. Caryn S. Ross-Innes & Rory Stark & Andrew E. Teschendorff & Kelly A. Holmes & H. Raza Ali & Mark J. Dunning & Gordon D. Brown & Ondrej Gojis & Ian O. Ellis & Andrew R. Green & Simak Ali & Suet-Feung C, 2012. "Differential oestrogen receptor binding is associated with clinical outcome in breast cancer," Nature, Nature, vol. 481(7381), pages 389-393, January.
    3. Fran Supek & Matko Bošnjak & Nives Škunca & Tomislav Šmuc, 2011. "REVIGO Summarizes and Visualizes Long Lists of Gene Ontology Terms," PLOS ONE, Public Library of Science, vol. 6(7), pages 1-9, July.
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