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Transcytosis of Listeria Monocytogenes Across The Transcytosis of Listeria monocytogenes across the intestinal barrier upon specific targeting of goblet cell accessible E-cadherin Georgios Nikitas, Chantal Deschamps, Olivier Disson, Théodora Niault, Pascale Cossart, Marc Lecuit To cite this version: Georgios Nikitas, Chantal Deschamps, Olivier Disson, Théodora Niault, Pascale Cossart, et al.. Tran- scytosis of Listeria monocytogenes across the intestinal barrier upon specific targeting of goblet cell accessible E-cadherin. Journal of Experimental Medicine, Rockefeller University Press, 2011, 208 (11), pp.2263-2277. 10.1084/jem.20110560. pasteur-02040395 HAL Id: pasteur-02040395 https://hal-pasteur.archives-ouvertes.fr/pasteur-02040395 Submitted on 20 Feb 2019 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 Published Online: 3 October, 2011 | Supp Info: http://doi.org/10.1084/jem.20110560 Downloaded from jem.rupress.org on February 19, 2019 Article Transcytosis of Listeria monocytogenes across the intestinal barrier upon specific targeting of goblet cell accessible E-cadherin Georgios Nikitas,1,4 Chantal Deschamps,1,4 Olivier Disson,1,4 Théodora Niault,1,4 Pascale Cossart,2,5 and Marc Lecuit1,3,4,6 1Microbes and Host Barriers Group, 2Bacteria Cells Interactions Unit, and 3French National Reference Center and World Health Organization Collaborating Center on Listeria, Institut Pasteur, F-75015 Paris, France 4Institut National de la Santé et de la Recherche Médicale (INSERM) Avenir Unité 604, F-75015 Paris, France 5INSERM Unité 604, Institut National de la Recherche Agronomique USC2020, F-75015 Paris, France 6Service des Maladies Infectieuses et Tropicales, Centre d’Infectiologie Necker-Pasteur, Hôpital Necker-Enfants Malades, Sorbonne Paris Cité, Université Paris Descartes, F-75015 Paris, France Listeria monocytogenes (Lm) is a foodborne pathogen that crosses the intestinal barrier upon interaction between its surface protein InlA and its species-specific host receptor E-cadherin (Ecad). Ecad, the key constituent of adherens junctions, is typically situated below tight junctions and therefore considered inaccessible from the intestinal lumen. In this study, we investigated how Lm specifically targets its receptor on intestinal villi and crosses the intestinal epithelium to disseminate systemically. We demonstrate that Ecad is luminally accessible around mucus-expelling goblet cells (GCs), around extruding entero- cytes at the tip and lateral sides of villi, and in villus epithelial folds. We show that upon preferential adherence to accessible Ecad on GCs, Lm is internalized, rapidly transcytosed across the intestinal epithelium, and released in the lamina propria by exocytosis from where it disseminates systemically. Together, these results show that Lm exploits intrinsic tissue heterogeneity to access its receptor and reveal transcytosis as a novel and unantici- pated pathway that is hijacked by Lm to breach the intestinal epithelium and cause systemic infection. CORRESPONDENCE The interaction of the Listeria monocytogenes (Lm) Sousa et al., 2005). Lm has been reported to Marc Lecuit: surface protein InlA with its receptor E-cadherin invade the tip of intestinal villi at sites of cell ex- [email protected] (Ecad), expressed by intestinal epithelial cells trusion (Pentecost et al., 2006, 2010). An in vitro Abbreviation used: AGC, (IECs), is critical for the translocation of this study in cultured epithelial kidney cells (MDCK The Journal of Experimental Medicine cell away from GCs; Ecad, human foodborne pathogen across the intestinal cells) has shown that cell extrusion is associated E-cadherin; GC, goblet cell; barrier and the onset of a systemic infection with junction remodeling that transiently ex- hEcad, human Ecad; IEC, intes- tinal epithelial cell; ITF, intesti- (Lecuit et al., 2001). InlA interaction with Ecad poses Ecad on extruding cells and their immedi- nal trefoil factor; Li, Listeria is species specific: human Ecad (hEcad) is a re- ate neighbors (Pentecost et al., 2006), and in vivo innocua; LLO, listeriolysin O; ceptor for InlA, whereas mouse Ecad (mEcad) is studies have confirmed that this process is ac- Lm, Listeria monocytogenes; mEcad, mouse Ecad; NGC, not (Lecuit et al., 1999). We have shown that in companied by redistribution of apical junctional cell next to GCs; NSF, hosts permissive to InlA–Ecad interaction, such complex proteins (Madara, 1990; Marchiando N-ethylmaleimide–sensitive factor; as transgenic mice expressing hEcad and knockin et al., 2011). Nevertheless, apart from intestinal p.i., postinoculation; TEM, mice expressing humanized mEcad, Lm directly villus tips, the sites of Lm adhesion to and trans- transmission electron micros- copy; TJ, tight junction; WGA, invades enterocytes and crosses the intestinal epi- location across the intestinal epithelium in vivo wheat germ agglutinin. thelium (Lecuit et al., 2001; Disson et al., 2008). have not been investigated systematically, and However, Ecad is an adherens junction protein the molecular mechanisms that lead to Lm actual typically located below tight junctions (TJs) and is therefore thought to be inaccessible to bacteria located in the intestinal lumen (Boller et al., 1985; © 2011 Nikitas et al. This article is distributed under the terms of an Attribution– Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share G. Nikitas and C. Deschamps contributed equally to Alike 3.0 Unported license, as described at http://creativecommons.org/licenses/ this paper. by-nc-sa/3.0/). The Rockefeller University Press $30.00 J. Exp. Med. Vol. 208 No. 11 2263-2277 2263 www.jem.org/cgi/doi/10.1084/jem.20110560 translocation across the intestinal epithelium and release into intestinal epithelium into the lamina propria to cause sys- the lamina propria remain unknown. temic infection. These results illustrate the critical importance In vitro studies have demonstrated that Lm enters into of extending cellular microbiology to three-dimensional nonphagocytic cells within 10 min through a zippering pro- tissue systems to understand the pathophysiology of infec- cess (Mengaud et al., 1996; Cossart and Sansonetti, 2004). Upon tious diseases. internalization, the bacterium is entrapped in a membrane- bound compartment, from which it is able to escape RESULTS within 10–15 min (Myers et al., 2003; Henry et al., 2006). Lm rapidly translocates across the intestinal epithelium Vacuolar escape is mediated by the pore-forming activity To study the early stages of Lm intestinal crossing, we inocu- of the secreted cholesterol-dependent listeriolysin O (LLO; lated intestinal ligated loops of iFABP-hEcad transgenic mice, Garcia-del Portillo and Finlay, 1995; Cossart and Sansonetti, which express hEcad under the control of the iFABP pro- 2004). Upon vacuolar lysis, Lm reaches the cytosol, in which moter (Lecuit et al., 2001), with Lm and imaged whole it can polymerize host actin to form comet tails that propel mount small intestinal tissue by two-photon and confocal bacteria intracellularly and form protrusions that allow Lm microscopy. Noninfected small intestinal tissues immuno- transfer into neighboring cells (see schematic representation labeled for hEcad display a typical epithelial honeycomb-like in Fig. S6 A). This process is strictly dependent on the listerial pattern (Fig. 1 A, Fig. S1 A, and Video 1). In infected intesti- surface protein ActA, which is necessary and sufficient on the nal loops, as early as 30 min postinoculation (p.i.), bacteria bacterial side to mediate actin polymerization (Kocks et al., were associated with intestinal villi (Fig. 1 B): we detected 1992). Actin nucleation around bacteria can be observed Lm adhering to the apical surface of enterocytes, within en- within 15 min after vacuolar escape, and Lm-containing terocytes, and at the basal pole of enterocytes. To our surprise protrusions can be observed 2.5 h upon infection (Tilney given this early time point, we also detected Lm in the lamina et al., 1992). propria (Fig. 1 C and Video 2). Because of the classical intra- The goal of our study was to determine comprehensively cellular cycle of Lm and its time frame in vitro, we would Lm intestinal epithelial target cells and to decipher the mech- have anticipated that Lm intestinal translocation in the lamina anisms of Lm crossing of the intestinal epithelial barrier propria would require at least 45 min to occur. We thus per- in vivo. To identify Lm intestinal epithelial target cells, we first formed a kinetic analysis of Lm invasion of the intestinal tis- studied Ecad luminal accessibility by two-photon and con- sue and studied the contribution of InlA to this process. Using focal imaging of noninfected whole mount intestinal tissue of two-photon and confocal imaging, we compared the associa- humanized transgenic
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