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Multiplicity of Salmonella Entry Mechanisms, a New Paradigm For Multiplicity of Salmonella entry mechanisms, a new paradigm for Salmonella pathogenesis Philippe Velge, Agnès Wiedemann, Manon Rosselin, Nadia Abed, Zineb Boumart, Anne-Marie Chaussé, Olivier Grépinet, Fatémeh Namdari, Sylvie Roche S.M., Aurore Rossignol, et al. To cite this version: Philippe Velge, Agnès Wiedemann, Manon Rosselin, Nadia Abed, Zineb Boumart, et al.. Multiplicity of Salmonella entry mechanisms, a new paradigm for Salmonella pathogenesis. MicrobiologyOpen, Wiley, 2012, 1 (3), pp.243-258. 10.1002/mbo3.28. hal-02649149 HAL Id: hal-02649149 https://hal.inrae.fr/hal-02649149 Submitted on 29 May 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. Multiplicity of Salmonella entry mechanisms, a new paradigm for Salmonella pathogenesis P. Velge1,2, A. Wiedemann1,2, M. Rosselin1,*, N. Abed1, Z. Boumart1,3, A. M. Chausse´ 1,2, O. Gre´ pinet1,2, F. Namdari1,2, S. M. Roche1,2, A. Rossignol1,2 & I. Virlogeux-Payant1,2 1INRA, UMR1282 Infectiologie et Sante´ Publique, F-37380, Nouzilly, France 2Universite´ Franc¸ois Rabelais de Tours, UMR1282 Infectiologie et Sante´ Publique, F-37000, Tours, France 3Agence Nationale de Se´ curite´ Sanitaire de l’alimentation, de l’environnement et du travail, Laboratoire de Ploufragan-Plouzane´ , Unite´ Hygie` ne et Qualite´ des Produits Avicoles et Porcins, 22440, Ploufragan, France Keywords Abstract Adhesion, invasin, invasion, Salmonella, Trigger, type III secretion system, Zipper The Salmonella enterica species includes about 2600 diverse serotypes, most of which cause a wide range of food- and water-borne diseases ranging from Correspondence self-limiting gastroenteritis to typhoid fever in both humans and animals. P. Velge, INRA of Tours, UMR 1282, ISP Moreover, some serotypes are restricted to a few animal species, whereas other 37380 Nouzilly, France. serotypes are able to infect plants as well as cold- and warm-blooded animals. Tel: ++33-2 47 42 78 93; An essential feature of the pathogenicity of Salmonella is its capacity to cross a Fax: +33-2 47 42 77 79; number of barriers requiring invasion of a large variety of phagocytic and E-mail: [email protected] nonphagocytic cells. The aim of this review is to describe the different entry Funding Information pathways used by Salmonella serotypes to enter different nonphagocytic cell Work in the laboratory was funded by grants types. Until recently, it was accepted that Salmonella invasion of eukaryotic cells from the European EADGENE Network of required only the type III secretion system (T3SS) encoded by the Salmonella Excellence, the European integrated project pathogenicity island-1. However, recent evidence shows that Salmonella can SABRE, the French project RESISAL, funded cause infection in a T3SS-1-independent manner. Currently, two outer by Agenavi and Agence National pour la membrane proteins Rck and PagN have been clearly identified as Salmonella Recherche within the framework of the National Genanimal program. invasins. As Rck mediates a Zipper-like entry mechanism, Salmonella is there- fore the first bacterium shown to be able to induce both Zipper and Trigger Received: 20 February 2012; Revised: 4 May mechanisms to invade host cells. In addition to these known entry pathways, 2012; Accepted: 7 May 2012 recent data have shown that unknown entry routes could be used according to the serotype, the host and the cell type considered, inducing either Zipper-like MicrobiologyOpen 2012; 1(3): 243–258 or Trigger-like entry processes. The new paradigm presented here should doi: 10.1002/mbo3.28 change our classic view of Salmonella pathogenicity. It could also modify our understanding of the mechanisms leading to the different Salmonella-induced *Current address: Department of diseases and to Salmonella-host specificity. Microbiology and Immunology, F. Edward He´ bert School of Medicine, Uniformed Services University of the Health Sciences, Bethesda, Maryland Salmonella and Salmonelloses indica (Guibourdenche et al. 2010). The agglutinating properties of the somatic O, flagellar H, and capsular Vi antigens are used to differentiate more than 2600 sero- The bacteria and diseases logically distinct Salmonella (Guibourdenche et al. 2010). Salmonella is a member of the Enterobacteriaceae family, Strains belonging to S. enterica subsp. enterica cause a large group of Gram-negative, facultative anaerobic and approximately 99% of Salmonella infections in humans nonspore-forming bacilli. The genus Salmonella consists and warm-blooded animals (McClelland et al. 2001). of only two species, Salmonella bongori and Salmonella Moreover, this subspecies is able to infect plants and enterica, and the latter is divided into six subspecies: numerous international outbreaks of S. enterica have been enterica, salamae, arizonae, diarizonae, houtenae, and linked to plant contamination (Pezzoli et al. 2007; Nygard ª 2012 The Authors. Published by Blackwell Publishing Ltd. This is an open access article under the terms of the Creative 243 Commons Attribution Non-Commercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. Multiplicity of Salmonella Entry Mechanisms P. Velge et al. et al. 2008). Serotypes in other subspecies are usually iso- host (Calenge et al. 2009, 2010). In summary, no other lated from cold-blooded animals and the environment, bacterial pathogen belonging to a single species shows but rarely from humans (Uzzau et al. 2000). Salmonella such a remarkable ability to infect different hosts and nomenclature is now based on the name of serotypes induce so many different diseases. belonging to subspecies. For example, Salmonella enterica subsp. enterica serotype Typhimurium is shortened to Host invasion pathways Salmonella Typhimurium (Brenner et al. 2000). From a clinical perspective, Salmonella serotypes may Despite the availability of complete genome sequences of be broadly grouped on the basis of host range and disease isolates representing several serotypes, the molecular outcomes (Uzzau et al. 2000). Host-specific serotypes are mechanisms underlying Salmonella colonization, patho- associated with severe systemic disease in adults of a sin- genesis, and transmission have been described mainly in gle species, which may seldom involve diarrhea (e.g., rodents, and thus little is known about these mechanisms Salmonella Typhi, Salmonella Gallinarum). For example, in farm animals and humans. S. Typhi is a human-specific pathogen causing a septicae- Host infections are usually initiated by ingestion of mic typhoid syndrome (enteric fever). S. Gallinarum has contaminated food or water followed by the passage of a host range restricted to birds and causes a severe sys- the bacteria from the stomach to the intestine. There, the temic disease called fowl typhoid (Shivaprasad 2000). bacteria adhere to and enter the cells lining the intestinal Host-restricted serotypes are primarily associated with epithelium. Passage of the bacteria through the intestinal systemic disease in few hosts (e.g., Salmonella Dublin in wall is believed to be initiated by transcytosis, that is, cattle, Salmonella Choleraesuis in pigs and humans), but invasion of either enterocytes or M cells at the apical side, may cause disease in a limited number of other species migration to the basolateral side, and exocytosis into the (Chiu et al. 2004). Broad host range serotypes, such as interstitial space of the lamina propria (Takeuchi 1967; S. Typhimurium and S. Enteritidis cause the majority of Clark et al. 1994; Muller et al. 2012). Direct capture by + + + high human gastrointestinal salmonelloses (Velge et al. 2005). CD18 phagocytes and CD11b , CD11c ,CX3CR1 They are able to infect, among many other animal species, phagocytes has also been observed (Vazquez-Torres et al. domestic livestock and fowl worldwide, resulting in a 1999; Muller et al. 2012). Within the lamina propria, spectrum of outcomes ranging from severe systemic dis- S. Typhimurium is taken up randomly by the different ease to asymptomatic carriage. For example, in contrast phagocytes (macrophages, dendritic cells, and poly- to S. Gallinarum, which induces a systemic infection only morphonuclear cells) and disseminates rapidly through in fowl, S. Enteritidis and S. Typhimurium generate a efferent lymph in mesenteric lymph nodes and through subclinical intestinal infection in poultry after a short sys- the blood stream in spleen and liver (Salcedo et al. 2001). temic infection, and infected hens can become chronic However, different behaviors have been observed depend- carriers and lay contaminated eggs (Shivaprasad 2000; ing on the serotype and the host. In cattle, S. Dublin Velge et al. 2005). In humans and cattle, infection with transits rapidly through the epithelial layer and associates these broad host range serotypes manifests as entero- with MHC class II-positive cells in the lamina propria. colitis, usually limited to the gastrointestinal tract and These bacteria are predominantly extracellular within
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