High-throughput screening of caterpillars as a platform to study host–microbe interactions and enteric immunity

Anton G. Windfelder, Frank H. H. Müller, Benedict Larney, Michael Hentschel, Anna Christina Böhringer, Christoph-Rüdiger Bredow, Florian H. Leinberger, Marian Kampschulte, Lorenz Maier, Yvette M. Bredow, Vera Flocke, Hans Merzendorfer, Gabriele A. Krombach, Andreas Vilcinskas, Jan Grimm, Tina E. Trenczek () and Ulrich Flögel ()
Additional contact information
Anton G. Windfelder: Justus Liebig University Giessen
Frank H. H. Müller: Radiology and Nuclear Medicine Ludwigshafen
Benedict Larney: Memorial Sloan Kettering Cancer Center
Michael Hentschel: Inselspital Bern
Anna Christina Böhringer: University of Siegen
Christoph-Rüdiger Bredow: Technical University of Dresden
Florian H. Leinberger: Justus Liebig University Giessen
Marian Kampschulte: Justus Liebig University Giessen
Lorenz Maier: Inselspital Bern
Yvette M. Bredow: Justus Liebig University Giessen
Vera Flocke: Heinrich Heine University Düsseldorf
Hans Merzendorfer: University of Siegen
Gabriele A. Krombach: University-Hospital Giessen
Andreas Vilcinskas: Fraunhofer Institute for Molecular Biology and Applied Ecology IME
Jan Grimm: Memorial Sloan Kettering Cancer Center
Tina E. Trenczek: Justus Liebig University Giessen
Ulrich Flögel: Heinrich Heine University Düsseldorf

Nature Communications, 2022, vol. 13, issue 1, 1-17

Abstract: Abstract Mammalian models of human disease are expensive and subject to ethical restrictions. Here, we present an independent platform for high-throughput screening, using larvae of the tobacco hornworm Manduca sexta, combining diagnostic imaging modalities for a comprehensive characterization of aberrant phenotypes. For validation, we use bacterial/chemical-induced gut inflammation to generate a colitis-like phenotype and identify significant alterations in morphology, tissue properties, and intermediary metabolism, which aggravate with disease progression and can be rescued by antimicrobial treatment. In independent experiments, activation of the highly conserved NADPH oxidase DUOX, a key mediator of gut inflammation, leads to similar, dose-dependent alterations, which can be attenuated by pharmacological interventions. Furthermore, the developed platform could differentiate pathogens from mutualistic gastrointestinal bacteria broadening the scope of applications also to microbiomics and host-pathogen interactions. Overall, larvae-based screening can complement mammals in preclinical studies to explore innate immunity and host-pathogen interactions, thus representing a substantial contribution to improve mammalian welfare.

Date: 2022
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DOI: 10.1038/s41467-022-34865-7

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