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

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, Claudia J. Dood, Paul L. A. M. Corstjens, Govert J. Dam, Eliana Nakano, Simone de Oliveira Castro, Vânia Gomes de Moura Mattaraia, Ronaldo de Carvalho Augusto, Christoph Grunau, R. Alan Wilson and Sergio Verjovski-Almeida ()
Additional contact information
Murilo Sena Amaral: Laboratório de Parasitologia, Instituto Butantan
Daisy Woellner Santos: Laboratório de Parasitologia, Instituto Butantan
Adriana S. A. Pereira: Laboratório de Parasitologia, Instituto Butantan
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
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

Nature Communications, 2021, vol. 12, issue 1, 1-17

Abstract: 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.

Date: 2021
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DOI: 10.1038/s41467-021-26497-0

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