Defining the early stages of intestinal colonisation by whipworms

María A. Duque-Correa (), David Goulding, Faye H. Rodgers, J. Andrew Gillis, Claire Cormie, Kate A. Rawlinson, Allison J. Bancroft, Hayley M. Bennett, Magda E. Lotkowska, Adam J. Reid, Anneliese O. Speak, Paul Scott, Nicholas Redshaw, Charlotte Tolley, Catherine McCarthy, Cordelia Brandt, Catherine Sharpe, Caroline Ridley, Judit Gali Moya, Claudia M. Carneiro, Tobias Starborg, Kelly S. Hayes, Nancy Holroyd, Mandy Sanders, David J. Thornton, Richard K. Grencis and Matthew Berriman ()
Additional contact information
María A. Duque-Correa: Wellcome Genome Campus
David Goulding: Wellcome Genome Campus
Faye H. Rodgers: Wellcome Genome Campus
J. Andrew Gillis: University of Cambridge
Claire Cormie: Wellcome Genome Campus
Kate A. Rawlinson: Wellcome Genome Campus
Allison J. Bancroft: Medicine and Health, University of Manchester
Hayley M. Bennett: Wellcome Genome Campus
Magda E. Lotkowska: Wellcome Genome Campus
Adam J. Reid: Wellcome Genome Campus
Anneliese O. Speak: Wellcome Genome Campus
Paul Scott: Wellcome Genome Campus
Nicholas Redshaw: Wellcome Genome Campus
Charlotte Tolley: Wellcome Genome Campus
Catherine McCarthy: Wellcome Genome Campus
Cordelia Brandt: Wellcome Genome Campus
Catherine Sharpe: Medicine and Health, University of Manchester
Caroline Ridley: Medicine and Health, University of Manchester
Judit Gali Moya: University of Barcelona
Claudia M. Carneiro: Federal University of Ouro Preto, Campus Universitario Morro do Cruzeiro
Tobias Starborg: Medicine and Health, University of Manchester
Kelly S. Hayes: Medicine and Health, University of Manchester
Nancy Holroyd: Wellcome Genome Campus
Mandy Sanders: Wellcome Genome Campus
David J. Thornton: Medicine and Health, University of Manchester
Richard K. Grencis: Medicine and Health, University of Manchester
Matthew Berriman: Wellcome Genome Campus

Nature Communications, 2022, vol. 13, issue 1, 1-15

Abstract: Abstract Whipworms are large metazoan parasites that inhabit multi-intracellular epithelial tunnels in the large intestine of their hosts, causing chronic disease in humans and other mammals. How first-stage larvae invade host epithelia and establish infection remains unclear. Here we investigate early infection events using both Trichuris muris infections of mice and murine caecaloids, the first in-vitro system for whipworm infection and organoid model for live helminths. We show that larvae degrade mucus layers to access epithelial cells. In early syncytial tunnels, larvae are completely intracellular, woven through multiple live dividing cells. Using single-cell RNA sequencing of infected mouse caecum, we reveal that progression of infection results in cell damage and an expansion of enterocytes expressing of Isg15, potentially instigating the host immune response to the whipworm and tissue repair. Our results unravel intestinal epithelium invasion by whipworms and reveal specific host-parasite interactions that allow the whipworm to establish its multi-intracellular niche.

Date: 2022
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DOI: 10.1038/s41467-022-29334-0

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