Septins restrict inflammation and protect zebrafish larvae from Shigella infection

Maria J. Mazon-Moya, Alexandra R. Willis, Vincenzo Torraca, Laurent Boucontet, Avinash R. Shenoy, Emma Colucci-Guyon and Serge Mostowy 2017. Septins restrict inflammation and protect zebrafish larvae from Shigella infection. PLOS Pathogens. 13 (6) e1006467. https://doi.org/10.1371/journal.ppat.1006467

TitleSeptins restrict inflammation and protect zebrafish larvae from Shigella infection
TypeJournal article
AuthorsMaria J. Mazon-Moya, Alexandra R. Willis, Vincenzo Torraca, Laurent Boucontet, Avinash R. Shenoy, Emma Colucci-Guyon and Serge Mostowy
Abstract

Shigella flexneri, a Gram-negative enteroinvasive pathogen, causes inflammatory destruction of the human intestinal epithelium. Infection by S. flexneri has been well-studied in vitro and is a paradigm for bacterial interactions with the host immune system. Recent work has revealed that components of the cytoskeleton have important functions in innate immunity and inflammation control. Septins, highly conserved cytoskeletal proteins, have emerged as key players in innate immunity to bacterial infection, yet septin function in vivo is poorly understood. Here, we use S. flexneri infection of zebrafish (Danio rerio) larvae to study in vivo the role of septins in inflammation and infection control. We found that depletion of Sept15 or Sept7b, zebrafish orthologs of human SEPT7, significantly increased host susceptibility to bacterial infection. Live-cell imaging of Sept15-depleted larvae revealed increasing bacterial burdens and a failure of neutrophils to control infection. Strikingly, Sept15-depleted larvae present significantly increased activity of Caspase-1 and more cell death upon S. flexneri infection. Dampening of the inflammatory response with anakinra, an antagonist of interleukin-1 receptor (IL-1R), counteracts Sept15 deficiency in vivo by protecting zebrafish from hyper-inflammation and S. flexneri infection. These findings highlight a new role for septins in host defence against bacterial infection, and suggest that septin dysfunction may be an underlying factor in cases of hyper-inflammation.

Article numbere1006467
JournalPLOS Pathogens
Journal citation13 (6)
ISSN1553-7374
Year2017
PublisherPublic Library of Science
Publisher's version
License
CC BY 4.0
File Access Level
Open (open metadata and files)
Digital Object Identifier (DOI)https://doi.org/10.1371/journal.ppat.1006467
Publication dates
Published26 Jun 2017

Related outputs

Editorial: Zebrafish Models for Human Disease Studies
Zang, L., Torraca, V., Shimada, Y. and Nishimura, N. 2022. Editorial: Zebrafish Models for Human Disease Studies. Frontiers in Cell and Developmental Biology. 10 861941. https://doi.org/10.3389/fcell.2022.861941

Septins promote caspase activity and coordinate mitochondrial apoptosis
Hoan Van Ngo, Stevens Robertin, Dominik Brokatzky, Magdalena K. Bielecka, Damián Lobato‐Márquez, Vincenzo Torraca and Serge Mostowy 2022. Septins promote caspase activity and coordinate mitochondrial apoptosis. Cytoskeleton. Advanced online publication. https://doi.org/10.1002/cm.21696

Editorial: Nucleic Acid-Associated Inflammation
Laguette, N., Langevin, C., Olagnier, D., Torraca, V., Vanpouille-Box, C. and Verrier, E.R. 2021. Editorial: Nucleic Acid-Associated Inflammation. Frontiers in Immunology. 12. https://doi.org/10.3389/fimmu.2021.791580

Disruption of Cxcr3 chemotactic signaling alters lysosomal function and renders macrophages more microbicidal
Frida Sommer, Vincenzo Torraca, Yufei Xie, Aliede E. in ‘t Veld, Joost Willemse and Annemarie H. Meijer 2021. Disruption of Cxcr3 chemotactic signaling alters lysosomal function and renders macrophages more microbicidal. Cell Reports. 35 (2) 109000. https://doi.org/10.1016/j.celrep.2021.109000

Deficiency in the autophagy modulator Dram1 exacerbates pyroptotic cell death of Mycobacteria-infected macrophages
Rui Zhang, Monica Varela, Gabriel Forn-Cuní, Vincenzo Torraca, Michiel van der Vaart and Annemarie H. Meijer 2020. Deficiency in the autophagy modulator Dram1 exacerbates pyroptotic cell death of Mycobacteria-infected macrophages. Cell Death and Disease. 11 277. https://doi.org/10.1038/s41419-020-2477-1

Shigella sonnei
Vincenzo Torraca, Kathryn Holt and Serge Mostowy 2020. Shigella sonnei. Trends in Microbiology. 28 (8), pp. P696-697. https://doi.org/10.1016/j.tim.2020.02.011

Frontline Science: Antagonism between regular and atypical Cxcr3 receptors regulates macrophage migration during infection and injury in zebrafish
Sommer, Frida, Torraca, V., Kamel, Sarah M., Lombardi, Amber and Meijer, Annemarie H. 2020. Frontline Science: Antagonism between regular and atypical Cxcr3 receptors regulates macrophage migration during infection and injury in zebrafish. Journal of Leukocyte Biology. 107 (2), pp. 185-203. https://doi.org/10.1002/jlb.2hi0119-006r

Chemokine Receptors and Phagocyte Biology in Zebrafish
Sommer, Frida, Torraca, V. and Meijer, Annemarie H. 2020. Chemokine Receptors and Phagocyte Biology in Zebrafish. Frontiers in Immunology. 11 325. https://doi.org/10.3389/fimmu.2020.00325

Supplementary RNAseq dataset files
Frida Sommer, Torraca, V. and Annemarie H. Meijer 2020. Supplementary RNAseq dataset files. Zenodo. https://doi.org/10.5281/zenodo.3833847

Analysis tools to quantify dissemination of pathology in zebrafish larvae
David R. Stirling, Oniz Suleyman, Eliza Gil, Philip M. Elks, Vincenzo Torraca, Mahdad Noursadeghi and Gillian S. Tomlinson 2020. Analysis tools to quantify dissemination of pathology in zebrafish larvae. Scientific Reports. 10 3149. https://doi.org/10.1038/s41598-020-59932-1

In vivo biomolecular imaging of zebrafish embryos using confocal Raman spectroscopy
Håkon Høgset, Conor C. Horgan, James P. K. Armstrong, Mads S. Bergholt, Vincenzo Torraca, Qu Chen, Timothy J. Keane, Laurence Bugeon, Margaret J. Dallman, Serge Mostowy and Molly M. Stevens 2020. In vivo biomolecular imaging of zebrafish embryos using confocal Raman spectroscopy. Nature Communications . 11 6172. https://doi.org/10.1038/s41467-020-19827-1

Shigella sonnei O-Antigen Inhibits Internalization, Vacuole Escape, and Inflammasome Activation
Watson, Jayne L., Sanchez-Garrido, Julia, Goddard, Philippa J., Torraca, V., Mostowy, Serge, Shenoy, Avinash R. and Clements, Abigail 2019. Shigella sonnei O-Antigen Inhibits Internalization, Vacuole Escape, and Inflammasome Activation. mBio. 10 (6) e02654-19. https://doi.org/10.1128/mbio.02654-19

Shigella sonnei infection of zebrafish reveals that O-antigen mediates neutrophil tolerance and dysentery incidence
Vincenzo Torraca, Myrsini Kaforou, Jayne Watson, Gina M. Duggan, Hazel Guerrero-Gutierrez, Sina Krokowski, Michael Hollinshead, Thomas B. Clarke, Rafal J. Mostowy, Gillian S. Tomlinson, Vanessa Sancho-Shimizu, Abigail Clements and Serge Mostowy 2019. Shigella sonnei infection of zebrafish reveals that O-antigen mediates neutrophil tolerance and dysentery incidence. PLOS Pathogens. 15 (12) e1008006. https://doi.org/10.1371/journal.ppat.1008006

RNAseq Profiling of Leukocyte Populations in Zebrafish Larvae Reveals a cxcl11 Chemokine Gene as a Marker of Macrophage Polarization During Mycobacterial Infection
Rougeot, Julien, Torraca, V., Zakrzewska, Ania, Kanwal, Zakia, Jansen, Hans J., Sommer, Frida, Spaink, Herman P. and Meijer, Annemarie H. 2019. RNAseq Profiling of Leukocyte Populations in Zebrafish Larvae Reveals a cxcl11 Chemokine Gene as a Marker of Macrophage Polarization During Mycobacterial Infection. Frontiers in Immunology. 10 832. https://doi.org/10.3389/fimmu.2019.00832

CXCR4 signaling regulates metastatic onset by controlling neutrophil motility and response to malignant cells
Annemarie Meijer and Torraca, V. 2019. CXCR4 signaling regulates metastatic onset by controlling neutrophil motility and response to malignant cells. Scientific Reports. 9 2399. https://doi.org/10.1038/s41598-019-38643-2

Macrophages target Salmonella by Lc3-associated phagocytosis in a systemic infection model
Masud, Samrah, Prajsnar, Tomasz K., Torraca, V., Lamers, Gerda E. M., Benning, Marianne, Van der Vaart, Michiel and Meijer, Annemarie H. 2019. Macrophages target Salmonella by Lc3-associated phagocytosis in a systemic infection model. Autophagy. 15 (5), pp. 796-812. https://doi.org/10.1080/15548627.2019.1569297

Meeting report: Zebrafish Infection and Immunity 2019
Torraca, V., Gomes, Margarida C., Sarris, Milka and Mostowy, Serge 2019. Meeting report: Zebrafish Infection and Immunity 2019. Lab Animal. 48, pp. 284-287. https://doi.org/10.1038/s41684-019-0400-0

Zebrafish Infection: From Pathogenesis to Cell Biology
Vincenzo Torraca and Serge Mostowy 2018. Zebrafish Infection: From Pathogenesis to Cell Biology. Trends in Cell Biology. 28 (2), pp. P143-156. https://doi.org/10.1016/j.tcb.2017.10.002

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

The inflammatory chemokine Cxcl18b exerts neutrophil-specific chemotaxis via the promiscuous chemokine receptor Cxcr2 in zebrafish
Torraca, V., Otto, Natasja A., Tavakoli-Tameh, Aidin and Meijer, Annemarie H. 2017. The inflammatory chemokine Cxcl18b exerts neutrophil-specific chemotaxis via the promiscuous chemokine receptor Cxcr2 in zebrafish. Developmental & Comparative Immunology. 67, pp. 57-65. https://doi.org/10.1016/j.dci.2016.10.014

The chemokine receptor CXCR4 promotes granuloma formation by sustaining a mycobacteria-induced angiogenesis programme
Annemarie Meijer and Torraca, V. 2017. The chemokine receptor CXCR4 promotes granuloma formation by sustaining a mycobacteria-induced angiogenesis programme. Scientific Reports. 7 45061. https://doi.org/10.1038/srep45061

Functional analysis reveals no transcriptional role for the glucocorticoid receptor beta-isoform in zebrafish
Chatzopoulou, Antonia, Schoonheim, Peter J., Torraca, V., Meijer, Annemarie H., Spaink, Herman P. and Schaaf, Marcel J.M. 2017. Functional analysis reveals no transcriptional role for the glucocorticoid receptor beta-isoform in zebrafish. Molecular and Cellular Endocrinology. 447, pp. 61-70. https://doi.org/10.1016/j.mce.2017.02.036

Modeling Infectious Diseases in the Context of a Developing Immune System
Masud, Samrah, Torraca, V. and Meijer, Annemarie H. 2017. Modeling Infectious Diseases in the Context of a Developing Immune System. Current Topics in Developmental Biology. 124, pp. 277-329. https://doi.org/10.1016/bs.ctdb.2016.10.006

Septins and Bacterial Infection
Torraca, V. and Mostowy, Serge 2016. Septins and Bacterial Infection. Frontiers in Cell and Developmental Biology. https://doi.org/10.3389/fcell.2016.00127

The CXCR3-CXCL11 signaling axis mediates macrophage recruitment and dissemination of mycobacterial infection
Torraca, V., Cui, Chao, Boland, Ralf, Bebelman, Jan-Paul, van der Sar, Astrid M., Smit, Martine J., Siderius, Marco, Spaink, Herman P. and Meijer, Annemarie H. 2015. The CXCR3-CXCL11 signaling axis mediates macrophage recruitment and dissemination of mycobacterial infection. Disease Models and Mechanisms. 8 (3), pp. 253-269. https://doi.org/10.1242/dmm.017756

Macrophage-pathogen interactions in infectious diseases: new therapeutic insights from the zebrafish host model
Torraca, V., Masud, S., Spaink, H.P. and Meijer, A.H. 2014. Macrophage-pathogen interactions in infectious diseases: new therapeutic insights from the zebrafish host model. Disease Models and Mechanisms. 7 (7), pp. 785-797. https://doi.org/10.1242/dmm.015594

Robotic injection of zebrafish embryos for high-throughput screening in disease models
Spaink, Herman P., Cui, Chao, Wiweger, Malgorzata I., Jansen, Hans J., Veneman, Wouter J., Marin-Juez, Ruben, de Sonneville, Jan, Ordas, Anita, Torraca, V., van der Ent, Wietske, Leenders, William P., Meijer, Annemarie H., Snaar-Jagalska, B. Ewa and Dirks, Ron P. 2013. Robotic injection of zebrafish embryos for high-throughput screening in disease models. Methods. 62 (3), pp. 246-254. https://doi.org/10.1016/j.ymeth.2013.06.002

Ultra-small graphene oxide functionalized with polyethylenimine (PEI) for very efficient gene delivery in cell and zebrafish embryos
Zhou, Xiang, Laroche, Fabrice, Lamers, Gerda E. M., Torraca, V., Voskamp, Patrick, Lu, Tao, Chu, Fuqiang, Spaink, Herman P., Abrahams, Jan Pieter and Liu, Zunfeng 2012. Ultra-small graphene oxide functionalized with polyethylenimine (PEI) for very efficient gene delivery in cell and zebrafish embryos. Nano Research. 5, pp. 703-709. https://doi.org/10.1007/s12274-012-0254-x

Permalink - https://westminsterresearch.westminster.ac.uk/item/vq617/septins-restrict-inflammation-and-protect-zebrafish-larvae-from-shigella-infection


Share this

Usage statistics

20 total views
15 total downloads
These values cover views and downloads from WestminsterResearch and are for the period from September 2nd 2018, when this repository was created.