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Rationally designed oral vaccines can set an evolutionary trap for Salmonella Typhimurium

Médéric Diard, Erik Bakkeren, Daniel Hoces, Verena Lentsch, Markus Arnoldini, Flurina Böhi, Kathrin Schumann-Moor, Jozef Adamcik, Luca Piccoli, Antonio Lanzavecchia, Beth M. Stadtmueller, Nicholas Donohue, Marjan W. van der Woude, Alyson Hockenberry, Patrick H. Viollier, Laurent Falquet, Daniel Wüthrich, Ferdinando Bonfiglio, Adrian Egli, Giorgia Zandomeneghi, Raffaele Mezzenga, Otto Holst, Beat H. Meier, Wolf-Dietrich Hardt, Emma Slack
doi: https://doi.org/10.1101/824821
Médéric Diard
1Institute for Microbiology, Department of Biology, ETH Zürich, Zürich, Switzerland
2Biozentrum, University of Basel, Basel, Switzerland
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  • For correspondence: emma.slack@hest.ethz.ch
Erik Bakkeren
1Institute for Microbiology, Department of Biology, ETH Zürich, Zürich, Switzerland
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Daniel Hoces
3Institute for Food, Nutrition and Health, ETH Zurich, Zurich, Switzerland
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Verena Lentsch
3Institute for Food, Nutrition and Health, ETH Zurich, Zurich, Switzerland
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Markus Arnoldini
3Institute for Food, Nutrition and Health, ETH Zurich, Zurich, Switzerland
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Flurina Böhi
1Institute for Microbiology, Department of Biology, ETH Zürich, Zürich, Switzerland
17Department of Molecular Mechanisms of Disease, University of Zurich, Zurich, Switzerland
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Kathrin Schumann-Moor
1Institute for Microbiology, Department of Biology, ETH Zürich, Zürich, Switzerland
19University of Zurich, Center of Dental Medicine, Oral Biotechnology & Bioengineering
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Jozef Adamcik
3Institute for Food, Nutrition and Health, ETH Zurich, Zurich, Switzerland
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Luca Piccoli
4Institute for Research in Biomedicine, Università della Svizzera italiana, Bellinzona, Switzerland
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Antonio Lanzavecchia
4Institute for Research in Biomedicine, Università della Svizzera italiana, Bellinzona, Switzerland
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Beth M. Stadtmueller
5Department of Biochemistry, University of Illinois at Urbana-Champaign, Urbana, Illinois USA
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Nicholas Donohue
6York Biomedical Research Institute, Hull York Medical School, University of York, York, UK
18Department of Orthopedics and Trauma, Medical University of Graz, Graz, Austria
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Marjan W. van der Woude
6York Biomedical Research Institute, Hull York Medical School, University of York, York, UK
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Alyson Hockenberry
7Department of Environmental Microbiology, Eawag, Dubendorf, Switzerland
8Department of Environmental Sciences, ETH Zürich, Switzerland
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Patrick H. Viollier
9Microbiology and Molecular Medicine, University of Geneva, Geneva, Switzerland
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Laurent Falquet
10Department of Biology, University of Fribourg, Fribourg, Switzerland
11Swiss Institute of Bioinformatics, Fribourg, Switzerland
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Daniel Wüthrich
12Infection Biology, Basel University Hospital, Basel, Switzerland
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Ferdinando Bonfiglio
13Department of Biomedicine, University of Basel, Basel, Switzerland
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Adrian Egli
12Infection Biology, Basel University Hospital, Basel, Switzerland
13Department of Biomedicine, University of Basel, Basel, Switzerland
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Giorgia Zandomeneghi
14Institute for Physical Chemistry, ETH Zurich, Zurich, Switzerland
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Raffaele Mezzenga
3Institute for Food, Nutrition and Health, ETH Zurich, Zurich, Switzerland
15ETH Zurich, Department of Materials, Wolfgang-Pauli-Strasse 10, 8093 Zürich
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Otto Holst
16Forschungszentrum Borstel, Borstel, Germany
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Beat H. Meier
14Institute for Physical Chemistry, ETH Zurich, Zurich, Switzerland
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Wolf-Dietrich Hardt
1Institute for Microbiology, Department of Biology, ETH Zürich, Zürich, Switzerland
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  • For correspondence: emma.slack@hest.ethz.ch
Emma Slack
1Institute for Microbiology, Department of Biology, ETH Zürich, Zürich, Switzerland
3Institute for Food, Nutrition and Health, ETH Zurich, Zurich, Switzerland
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  • For correspondence: emma.slack@hest.ethz.ch
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Abstract

Secretory antibody responses (Immunoglobulin A, IgA) against repetitive bacterial surface glycans, such as O-antigens and capsules, can protect against intestinal pathogenic Enterobacteriaceae. However, efficacy of such immune responses has been limited by rapid glycan evolution and phase-variation. Here, we track IgA-driven O-antigen variation in Salmonella Typhimurium, and use this to assemble an oligovalent oral vaccine which sets an evolutionary trap. IgA targeting all fitness-neutral O-antigen escape variants of Salmonella Typhimurium rapidly selected for mutants with very short O-antigen: a phenotype known to display major fitness costs and virulence attenuation in naive hosts. Evolutionary trap vaccination therefore represents an alternative concept in vaccine design. This approach capitalizes on the inevitable and rapid evolution of bacteria in the gut, and can combine protection of the individual with elimination of virulent enteropathogen reservoirs.

One sentence summary By tracking vaccine-driven Salmonella evolution in the intestine, it is possible to rationally design oligovalent oral vaccines that generate an evolutionary trap.

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Posted October 31, 2019.
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Rationally designed oral vaccines can set an evolutionary trap for Salmonella Typhimurium
Médéric Diard, Erik Bakkeren, Daniel Hoces, Verena Lentsch, Markus Arnoldini, Flurina Böhi, Kathrin Schumann-Moor, Jozef Adamcik, Luca Piccoli, Antonio Lanzavecchia, Beth M. Stadtmueller, Nicholas Donohue, Marjan W. van der Woude, Alyson Hockenberry, Patrick H. Viollier, Laurent Falquet, Daniel Wüthrich, Ferdinando Bonfiglio, Adrian Egli, Giorgia Zandomeneghi, Raffaele Mezzenga, Otto Holst, Beat H. Meier, Wolf-Dietrich Hardt, Emma Slack
bioRxiv 824821; doi: https://doi.org/10.1101/824821
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Rationally designed oral vaccines can set an evolutionary trap for Salmonella Typhimurium
Médéric Diard, Erik Bakkeren, Daniel Hoces, Verena Lentsch, Markus Arnoldini, Flurina Böhi, Kathrin Schumann-Moor, Jozef Adamcik, Luca Piccoli, Antonio Lanzavecchia, Beth M. Stadtmueller, Nicholas Donohue, Marjan W. van der Woude, Alyson Hockenberry, Patrick H. Viollier, Laurent Falquet, Daniel Wüthrich, Ferdinando Bonfiglio, Adrian Egli, Giorgia Zandomeneghi, Raffaele Mezzenga, Otto Holst, Beat H. Meier, Wolf-Dietrich Hardt, Emma Slack
bioRxiv 824821; doi: https://doi.org/10.1101/824821

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