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Shigella Impairs T Lymphocyte Dynamics in Vivo

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Shigella Impairs T Lymphocyte Dynamics in Vivo impairs T lymphocyte dynamics in vivo Shigella INAUGURAL ARTICLE Wilmara Salgado-Pabóna,b,1, Susanna Cellic, Ellen T. Arenaa,b, Katharina Nothelfera,b, Pascal Rouxd, Gernot Sellgea,b,2, Elisabetta Frigimelicaa,b,3, Philippe Boussoc, Philippe J. Sansonettia,b,4, and Armelle Phalipona,b aMolecular Microbial Pathogenesis Unit, Department Cell Biology and Infection, bInstitut National de la Santé et de la Recherche Médicale U786, dPlatform for Dynamic Imaging Studies, and cDynamics of Immune Responses Unit, Department of Immunology, Institut Pasteur, 75724 Paris Cedex 15, France This contribution is part of the special series of Inaugural Articles by members of the National Academy of Sciences elected in 2012. Contributed by Philippe J. Sansonetti, January 17, 2013 (sent for review September 12, 2012) The Gram-negative enteroinvasive bacterium Shigella flexneri is infection (12). Information is also scant regarding Shigella’s ca- responsible for the endemic form of bacillary dysentery, an acute pacity to subvert the host acquired immune responses by directly rectocolitis in humans. S. flexneri uses a type III secretion system to interacting with T or B lymphocytes. Such interactions may take inject effector proteins into host cells, thus diverting cellular func- place in the colonic lymphoid follicles after Shigella’s crossing of tions to its own benefit. Protective immunity to reinfection requires the intestinal barrier via M cells located within the follicle-as- several rounds of infection to be elicited and is short-lasting, sociated epithelium, in the lamina propria, or the mesenteric suggesting that S. flexneri interferes with the priming of specific lymph nodes (LNs) (5). immunity. Considering the key role played by T-lymphocyte traf- We recently demonstrated that Shigella invades activated, but + ficking in priming of adaptive immunity, we investigated the im- not resting, human CD4 T cells in vitro, leading to cell migra- pact of S. flexneri on T-cell dynamics in vivo. By using two-photon tion arrest toward a chemoattractant stimulus in a transwell microscopy to visualize bacterium–T-cell cross-talks in the lymph migration assay (13). Whether this occurs in vivo is unknown. In nodes, where the adaptive immunity is initiated, we provide evi- addition, in vivo T cells rapidly integrate multiple signals from dence that S. flexneri, via its type III secretion system, impairs the + the environment to respond to infection, a scenario that is ob- migration pattern of CD4 T cells independently of cognate recog- viously absent in in vitro settings. Therefore, the present study nition of bacterial antigens. We show that bacterial invasion of + + aimed at investigating the targeting of CD4 T cells by Shigella in CD4 T lymphocytes occurs in vivo, and results in cell migration vivo and its impact on T-cell dynamics. We used two-photon + MICROBIOLOGY arrest. In the absence of invasion, CD4 T-cell migration parameters microscopy (2PM) to study Shigella–T lymphocyte cross-talks fl are also dramatically altered. Signals resulting from S. exneri inter- occurring early on in the draining popliteal LN upon footpad actions with subcapsular sinus macrophages and dendritic cells, and inoculation with Shigella. 2PM of live intact tissues has been recruitment of polymorphonuclear cells are likely to contribute to fi fl recently applied to study immune cell dynamics in infectious this phenomenon. These ndings indicate that S. exneri targets T settings (14, 15). The LN is of particular interest because it is lymphocytes in vivo and highlight the role of type III effector secre- within secondary lymphoid organs where pathogen-specific im- tion in modulating host adaptive immune responses. mune responses are orchestrated or fail to be generated. Fur- thermore, the microanatomy and function of the LN is highly host–pathogen cross-talks | imaging conserved regardless of its body localization (reviewed in refs. 16–18). + he bacterium Shigella is an enteroinvasive pathovar of Escher- We report here that Shigella induces CD4 T-cell migration Tichia coli that causes shigellosis, otherwise known as bacillary paralysis in vivo. This might represent a way to sabotage the host fl dysentery, an acute rectocolitis characterized by a rapid in ux of capacity to induce T-cell–mediated immunity and hence impede polymorphonuclear neutrophils (PMNs) to the lamina propria the priming of an effective protective response. that leads to massive tissue destruction (1, 2). Shigella’spath- ogenesis relies on the expression of a type III secretion system Results fi + (T3SS) and its secreted effector proteins. A rst wave of secreted S. flexneri Interacts with CD4 T Cells in Subcapsular Sinus Interfollicular effectors are required for cellular invasion and initiation of the Regions of LN. LNs are characterized by their highly organized ar- fl in ammatory innate response upon bacterial targeting of res- chitecture and cellular compartmentalization. The LN paracortex, ϕ ident macrophages (M s) and intestinal epithelial cells, whereas where T cells home to interact with DCs, is largely inaccessible to a second wave of T3SS effectors targets MAP kinases and the lymph-borne antigens and pathogens, which accumulate in the LN κ NF- B signaling pathway to control the level of the induced subcapsular sinus (SCS) upon draining via lymphatic vessels (14, fl – + in ammatory response (3 5). 15, 19). To assess where S. flexneri meets CD4 T lymphocytes in + Mechanisms and role of T3SS effectors leading to adaptive the LN early on, polyclonal naive CD4 T cells were labeled with immunity to Shigella infection have been poorly investigated. the cytoplasmic dye carboxyfluorescein succinimidyl ester (CFSE) Natural infection fails to elicit a long-lasting protective immu- nity, and several infection episodes are required to generate a short-term, mainly antibody-mediated protection (6, 7). This Author contributions: W.S.-P., P.J.S., and A.P. designed research; W.S.-P., S.C., E.T.A., K.N., suggests that Shigella has evolved strategies to dampen the ac- and A.P. performed research; P.R. and G.S. contributed new reagents/analytic tools; W.S.-P., quired immune response. The induced acute inflammation cer- S.C., E.F., P.B., P.J.S., and A.P. analyzed data; and W.S.-P. and A.P. wrote the paper. tainly contributes to the profile of the specific immunity. Indeed, The authors declare no conflict of interest. fl acute in ammation has been associated with apoptotic cell death Freely available online through the PNAS open access option. of T lymphocytes in rectal biopsies of infected individuals (8, 9), 1Present address: Department of Microbiology, University of Iowa, Iowa City, IA. impairment of dendritic cell (DC) recruitment to the site of 2Present address: University Hospital Aachen, Department Medicine III, 52074 Aachen, Shigella infection in a model of human intestinal xenotransplant Germany. fi + (10), and the predominant priming of Shigella-speci c CD4 3Present address: Department of Microbial Molecular Biology, Novartis Vaccines and Th17 cells conferring limited protection against reinfection in Diagnostics, 53100 Siena, Italy. + a murine model of infection (11). Evidence suggests that CD8 T 4To whom correspondence should be addressed. E-mail: [email protected]. lymphocytes are not required for protective immunity (11). In + This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. fact, antigen-specific CD8 T cells fail to be primed upon Shigella 1073/pnas.1300981110/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1300981110 PNAS Early Edition | 1of6 Downloaded by guest on September 27, 2021 and adoptively transferred into BL6 mice. Approximately 18 h (SEM), with 63% of the cells exhibiting velocities higher than after transfer, mice were inoculated s.c. with physiological water 8 μm/min and only 8% exhibiting velocities of slow migrating cells (for uninfected conditions), DsRed-expressing WT, or T3SS-de- (<4 μm/min; Fig. 2 D and E). These cells also exhibited low arrest − ficient (T3SS ) S. flexneri. The later strain was used to further coefficients (23 ± 1%), with 64% stopping for less than 20% of the analyze the impact of T3SS effectors on T-cell dynamics. Two- time, and only 3% stopping for more than 80% of the time. A photon microscopy was used to generate 3D reconstructions of direct correlation between high velocity and low arrest coefficient intact LNs. In uninfected LNs, T cells were mainly confined to the is consistent with T cells traveling under homeostatic conditions paracortex T-cell zone. However, in areas where the paracortex (Fig. S1A). − extends into the interfollicular regions, they were seen close to the Upon infection with T3SS S. flexneri, T cells migrated at SCS (Fig. 1A). Upon infection, T cells were distributed more lower speeds (6.8 ± 0.16 μm/min), with an approximately twofold diffusely at the periphery of the interfollicular areas (Fig. 1 B and decrease in the percentage of cells (33%) exhibiting velocities C), migrating in between B-cell follicles to gain access to the SCS, μ − higher than 8 m/min, whereas the percentage of cells exhibiting where WT and T3SS S. flexneri were largely found (Fig. 1D). μ − velocities less than 4 m/min was similar (Fig. 2 B, D, and E and Similar bacterial counts were recovered from WT and T3SS Movie S2). The arrest coefficient was increased by approximately infected LNs, thus allowing accurate comparison between the two 1.5 fold (35 ± 2%). This resulted from a decrease in the per- strains and indicating that draining of Shigella into the LN is in- centage of cells exhibiting arrest coefficients less than 20% dependent of T3SS effector secretion. whereas the percentage of cells with arrest coefficients higher + than 80% was similar. Confinement index was increased, in- Shigella Via Its T3SS Drastically Reduces CD4 T-Cell Motility in LN. Based on the aforementioned observations, T-cell migration was dicating that T-cell migration area was more restricted.
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