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Subversion Extends from Innate to Adaptive Immune Responses Katja Brunner, Fatoumata Samassa, Philippe Sansonetti, Armelle Phalipon

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Subversion Extends from Innate to Adaptive Immune Responses Katja Brunner, Fatoumata Samassa, Philippe Sansonetti, Armelle Phalipon Shigella -mediated immunosuppression in the human gut: subversion extends from innate to adaptive immune responses Katja Brunner, Fatoumata Samassa, Philippe Sansonetti, Armelle Phalipon To cite this version: Katja Brunner, Fatoumata Samassa, Philippe Sansonetti, Armelle Phalipon. Shigella -mediated immunosuppression in the human gut: subversion extends from innate to adaptive immune re- sponses. Human Vaccines & Immunotherapeutics, Taylor & Francis, 2018, 15 (6), pp.1317-1325. 10.1080/21645515.2019.1594132. pasteur-02874899 HAL Id: pasteur-02874899 https://hal-pasteur.archives-ouvertes.fr/pasteur-02874899 Submitted on 19 Jun 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution - NonCommercial - NoDerivatives| 4.0 International License Human Vaccines & Immunotherapeutics ISSN: 2164-5515 (Print) 2164-554X (Online) Journal homepage: https://www.tandfonline.com/loi/khvi20 Shigella-mediated immunosuppression in the human gut: subversion extends from innate to adaptive immune responses Katja Brunner, Fatoumata Samassa, Philippe J. Sansonetti & Armelle Phalipon To cite this article: Katja Brunner, Fatoumata Samassa, Philippe J. Sansonetti & Armelle Phalipon (2019) Shigella-mediated immunosuppression in the human gut: subversion extends from innate to adaptive immune responses, Human Vaccines & Immunotherapeutics, 15:6, 1317-1325, DOI: 10.1080/21645515.2019.1594132 To link to this article: https://doi.org/10.1080/21645515.2019.1594132 © 2019 Institut Pasteur. Published with Accepted author version posted online: 09 license by Taylor & Francis Group, LLC. Apr 2019. Published online: 19 Apr 2019. Submit your article to this journal Article views: 906 View related articles View Crossmark data Citing articles: 3 View citing articles Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=khvi20 HUMAN VACCINES & IMMUNOTHERAPEUTICS 2019, VOL. 15, NO. 6, 1317–1325 https://doi.org/10.1080/21645515.2019.1594132 REVIEW Shigella-mediated immunosuppression in the human gut: subversion extends from innate to adaptive immune responses Katja Brunnera,b, Fatoumata Samassaa,b, Philippe J. Sansonettia,b,c, and Armelle Phalipona,b aMolecular Microbial Pathogenesis Unit, Department of Cellular Biology of Infection, Institut Pasteur, Paris, France; bINSERM U1202, Paris, France; cChaire de Microbiologie et Maladies Infectieuses, Collège de France, Paris, France ABSTRACT ARTICLE HISTORY The enteropathogen, Shigella, is highly virulent and remarkably adjusted to the intestinal environment Received 12 December 2018 of its almost exclusive human host. Key for Shigella pathogenicity is the injection of virulence effectors Revised 13 February 2019 into the host cell via its type three secretion system (T3SS), initiating disease onset and progression by Accepted 27 February 2019 the vast diversity of the secreted T3SS effectors and their respective cellular targets. The multifaceted KEYWORDS modulation of host signaling pathways exerted by Shigella T3SS effectors, which include the subversion Adaptive immunity; of host innate immune defenses and the promotion of intracellular bacterial survival and dissemination, enteropathogen; type three have been extensively reviewed in the recent past. This review focuses on the human species specificity secretion system; dysentery; of Shigella by discussing some possible evasion mechanisms towards the human, but not non-human or immunomodulation; T cells; rodent gut innate defense barrier, leading to the lack of a relevant animal infection model. In addition, bacterial; bacterial mucosal; subversion mechanisms of the adaptive immune response are highlighted summarizing research immune modulators; advances of the recent years. In particular, the new paradigm of Shigella pathogenicity constituted of infectious disease; mucosal; virulence invasion-independent T3SS effector-mediated targeting of activated, human lymphocytes is discussed. Along with consequences on vaccine development, these findings offer new directions for future research endeavors towards a better understanding of immunity to Shigella infection. Exploring Shigella specificity towards the human induction of biofilm formation, hence facilitating better resis- innate immune barrier in the gut tance to the challenging environmental conditions of the gut.11 Upon entering the colon, Shigella is faced with the The striking selectivity of Shigella as a human-restricted great abundance of resident microbes, the gut microbiota, pathogen relies on its evasion mechanisms of host innate which naturally varies significantly in their composition defenses during gut transit and mucosal invasion, which are across species.12,13 How Shigella establishes its niche in such highly adapted to the human digestive tract. The significance an adverse environment is subject of further investigations of this species specificity becomes evident when considering but of importance is its binding to the mucus layer, which is that up-to-now there is no experimental animal model avail- at its greatest thickness in the colon in comparison to other able, which convincingly mimics human infection, i.e. the sections of the digestive tract.14,15 Immune properties of the onset of dysentery after oral inoculum.1 As an exception, mucus barrier present with marked differences between loca- naturally acquired Shigella infection has been reported for – tion and species and are associated with host selectivity. The some, non-human primates, including Rhesus macaques.2 4 absence of Shigella binding to the small intestinal mucus16,17 Nevertheless, under laboratory conditions, the Rhesus maca- suggests selectivity of the bacterial/mucin interactions which que model requires an inoculum dose of about 108–109 is possibly related to the specific glycan composition present bacteria,5 whereas as few as 102–103 suffice to cause disease in the colonic mucosa. Shigella binds with high affinity to the in humans.6,7 While sharing common features, there is heavily glycosylated mucins isolated from the human colon, as increasing evidence suggesting for important species differ- opposed to those from the guinea pig (less binding) and rat ences in the innate defense systems – in particular between (no binding).16 In addition, the inner mucus layer contains primates and rodents8 – which may provide important leads antimicrobial peptides (AMPs), which are important media- as to understanding susceptibility versus resistance to infec- tors in keeping the epithelial lining sterile. Interestingly, tion observed in these species. For instance, after surviving the AMPs also underlie species-specificity presumably having acidic environment of the stomach,9 Shigella reaches the small adapted to the diverse ecological niches inhabited by mam- intestine where it has to resist to degradation by bile salts that mals and the multitude of microbial challenges faced within.18 commonly vary in composition between humans, non-human Here, the rate of similarities and differences across species are primates, and rodents.10 Interestingly, exposure to human- also dependent on the type of AMPs. For instance, divergence type bile salts was recently shown to increase Shigella viru- exists for α-defensins when comparing mouse and human,18 lence via the upregulation of survival genes as well as the CONTACT Armelle Phalipon [email protected] Molecular Microbial Pathogenesis Unit, Department of Cellular Biology of Infection, Institut Pasteur, Paris, France. © 2019 Institut Pasteur. Published with license by Taylor & Francis Group, LLC. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License (http://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited, and is not altered, transformed, or built upon in any way. 1318 K. BRUNNER ET AL. while in contrast Rhesus monkey β-defensins and cathelici- T3SA is temperature-dependent and only triggered at 37°C,34 dins are close homologs to the human molecules.19 the human body temperature, in order to keep the energetic Considering this homology, the specific down-regulation of costs related to its expression to a minimum. After its assem- cathelicidin and human β-defensin 1 expression by Shigella bly, the T3SA remains inactive, i.e. translocators and several during natural and experimental infection which contributes effectors remain associated to chaperons in the bacterial cyto- to bacterial survival in the intestine20,21 might also happen in plasm, until sensing of the host cell membrane occurs at the Rhesus monkeys, thus contributing to their susceptibility to needle tip complex.35 This acts as activation signal36 and Shigella oral infection. initiates the secretion of the stored translocators and effectors Another key point in the inter-species variation of innate into the host cell cytoplasm37-39
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