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Observation

Shigella-Induced Emergency Granulopoiesis Protects Zebrafish Larvae from Secondary Infection

Alexandra R. Willis, Vincenzo Torraca, Margarida C. Gomes, Jennifer Shelley, Maria Mazon-Moya, Alain Filloux, Cristina Lo Celso, Serge Mostowy
Philippe J. Sansonetti, Editor
Alexandra R. Willis
Section of Microbiology, MRC Centre of Molecular Bacteriology and Infection (CMBI), Imperial College London, London, United Kingdom
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Vincenzo Torraca
Section of Microbiology, MRC Centre of Molecular Bacteriology and Infection (CMBI), Imperial College London, London, United Kingdom
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Margarida C. Gomes
Department of Life Sciences, MRC Centre of Molecular Bacteriology and Infection (CMBI), Imperial College London, London, United Kingdom
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Jennifer Shelley
Section of Microbiology, MRC Centre of Molecular Bacteriology and Infection (CMBI), Imperial College London, London, United Kingdom
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Maria Mazon-Moya
Section of Microbiology, MRC Centre of Molecular Bacteriology and Infection (CMBI), Imperial College London, London, United Kingdom
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Alain Filloux
Department of Life Sciences, MRC Centre of Molecular Bacteriology and Infection (CMBI), Imperial College London, London, United Kingdom
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Cristina Lo Celso
Department of Life Sciences, Imperial College London, London, United KingdomThe Francis Crick Institute, London, United Kingdom
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Serge Mostowy
Section of Microbiology, MRC Centre of Molecular Bacteriology and Infection (CMBI), Imperial College London, London, United KingdomDepartment of Immunology and Infection, London School of Hygiene and Tropical Medicine, London, United Kingdom
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Philippe J. Sansonetti
Pasteur Institute
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DOI: 10.1128/mBio.00933-18
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ABSTRACT

Emergency granulopoiesis is a hematopoietic program of stem cell-driven neutrophil production used to counteract immune cell exhaustion following infection. Shigella flexneri is a Gram-negative enteroinvasive pathogen controlled by neutrophils. In this study, we use a Shigella-zebrafish (Danio rerio) infection model to investigate emergency granulopoiesis in vivo. We show that stem cell-driven neutrophil production occurs in response to Shigella infection and requires macrophage-independent signaling by granulocyte colony-stimulating factor (Gcsf). To test whether emergency granulopoiesis can function beyond homoeostasis to enhance innate immunity, we developed a reinfection assay using zebrafish larvae that have not yet developed an adaptive immune system. Strikingly, larvae primed with a sublethal dose of Shigella are protected against a secondary lethal dose of Shigella in a type III secretion system (T3SS)-dependent manner. Collectively, these results highlight a new role for emergency granulopoiesis in boosting host defense and demonstrate that zebrafish larvae can be a valuable in vivo model to investigate innate immune memory.

IMPORTANCE Shigella is an important human pathogen of the gut. Emergency granulopoiesis is the enhanced production of neutrophils by hematopoietic stem and progenitor cells (HSPCs) upon infection and is widely considered a homoeostatic mechanism for replacing exhausted leukocytes. In this study, we developed a Shigella-zebrafish infection model to investigate stem cell-driven emergency granulopoiesis. We discovered that zebrafish initiate granulopoiesis in response to Shigella infection, via macrophage-independent signaling of granulocyte colony-stimulating factor (Gcsf). Strikingly, larvae primed with a sublethal dose of Shigella are protected against a secondary lethal dose of Shigella in a type III secretion system (T3SS)-dependent manner. Taken together, we show that zebrafish infection can be used to capture Shigella-mediated stem cell-driven granulopoiesis and provide a new model system to study stem cell biology in vivo. Our results also highlight the potential of manipulating stem cell-driven granulopoiesis to boost innate immunity and combat infectious disease.

  • Copyright © 2018 Willis et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Shigella-Induced Emergency Granulopoiesis Protects Zebrafish Larvae from Secondary Infection
Alexandra R. Willis, Vincenzo Torraca, Margarida C. Gomes, Jennifer Shelley, Maria Mazon-Moya, Alain Filloux, Cristina Lo Celso, Serge Mostowy
mBio Jun 2018, 9 (3) e00933-18; DOI: 10.1128/mBio.00933-18

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Shigella-Induced Emergency Granulopoiesis Protects Zebrafish Larvae from Secondary Infection
Alexandra R. Willis, Vincenzo Torraca, Margarida C. Gomes, Jennifer Shelley, Maria Mazon-Moya, Alain Filloux, Cristina Lo Celso, Serge Mostowy
mBio Jun 2018, 9 (3) e00933-18; DOI: 10.1128/mBio.00933-18
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KEYWORDS

emergency granulopoiesis
neutrophils
Shigella
stem cells
zebrafish

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