Listeria Adhesion Protein Induces Intestinal Epithelial Barrier Dysfunction for Bacterial Translocation

Abreu, 2003, TLR signaling at the intestinal epithelial interface, J. Endotoxin Res., 9, 322, 10.1177/09680519030090050901 Baldwin, 2003, A gene-expression program reflecting the innate immune response of cultured intestinal epithelial cells to infection by Listeria monocytogenes, Genome Biol., 4, R2, 10.1186/gb-2002-4-1-r2 Berger, 2016, Mitochondrial function controls intestinal epithelial stemness and proliferation, Nat. Commun., 7, 13171, 10.1038/ncomms13171 Bierne, 2002, Inactivation of the srtA gene in Listeria monocytogenes inhibits anchoring of surface proteins and affects virulence, Mol. Microbiol., 43, 869, 10.1046/j.1365-2958.2002.02798.x Bonazzi, 2008, Successive post-translational modifications of E-cadherin are required for InlA-mediated internalization of Listeria monocytogenes, Cell. Microbiol., 10, 2208, 10.1111/j.1462-5822.2008.01200.x Bou Ghanem, 2012, InlA promotes dissemination of Listeria monocytogenes to the mesenteric lymph nodes during food borne infection of mice, PLoS Pathog., 8, e1003015, 10.1371/journal.ppat.1003015 Burkholder, 2010, Listeria monocytogenes uses Listeria adhesion protein (LAP) to promote bacterial transepithelial translocation and induces expression of LAP receptor Hsp60, Infect. Immun., 78, 5062, 10.1128/IAI.00516-10 Burkholder, 2009, Expression of LAP, a SecA2-dependent secretory protein, is induced under anaerobic environment, Microbes Infect., 11, 859, 10.1016/j.micinf.2009.05.006 Chiba, 2011, Listerial invasion protein internalin B promotes entry into ileal Peyer’s patches in vivo, Microbiol. Immunol., 55, 123, 10.1111/j.1348-0421.2010.00292.x Chun, 2010, Cytosolic Hsp60 is involved in the NF-kappaB-dependent survival of cancer cells via IKK regulation, PLoS One, 5, e9422, 10.1371/journal.pone.0009422 Clayburgh, 2005, Epithelial myosin light chain kinase-dependent barrier dysfunction mediates T cell activation-induced diarrhea in vivo, J. Clin. Invest., 115, 2702, 10.1172/JCI24970 Corr, 2006, An in vitro cell-culture model demonstrates internalin- and hemolysin-independent translocation of Listeria monocytogenes across M cells, Microb. Pathog., 41, 241, 10.1016/j.micpath.2006.08.003 Czuprynski, 2003, A/J mice are susceptible and C57BL/6 mice are resistant to Listeria monocytogenes infection by intragastric inoculation, Infect. Immun., 71, 682, 10.1128/IAI.71.2.682-689.2003 Disson, 2008, Conjugated action of two species-specific invasion proteins for fetoplacental listeriosis, Nature, 455, 1114, 10.1038/nature07303 Dramsi, 1995, Entry of Listeria monocytogenes into hepatocytes requires expression of InIB, a surface protein of the internalin multigene family, Mol. Microbiol., 16, 251, 10.1111/j.1365-2958.1995.tb02297.x Dziewanowska, 2000, Staphylococcal fibronectin binding protein interacts with heat shock protein 60 and integrins: role in internalization by epithelial cells, Infect. Immun., 68, 6321, 10.1128/IAI.68.11.6321-6328.2000 Gelbíčová, 2015, A novel mutation leading to a premature stop codon in inlA of Listeria monocytogenes isolated from neonatal listeriosis, New Microbiol., 38, 293 Gilbert, 2012, Enterocyte STAT5 promotes mucosal wound healing via suppression of myosin light chain kinase-mediated loss of barrier function and inflammation, EMBO Mol. Med., 4, 109, 10.1002/emmm.201100192 Gouin, 2010, The Listeria monocytogenes InlC protein interferes with innate immune responses by targeting the IkappaB kinase subunit IKKalpha, Proc. Natl. Acad. Sci. USA, 107, 17333, 10.1073/pnas.1007765107 Hecht, 1996, Expression of the catalytic domain of myosin light chain kinase increases paracellular permeability, Am. J. Physiol., 271, C1678, 10.1152/ajpcell.1996.271.5.C1678 Hisamatsu, 2003, CARD15/NOD2 functions as an antibacterial factor in human intestinal epithelial cells, Gastroenterology, 124, 993, 10.1053/gast.2003.50153 Holch, 2013, Listeria monocytogenes strains encoding premature stop codons in inlA invade mice and guinea pig fetuses in orally dosed dams, J. Med. Microbiol., 62, 1799, 10.1099/jmm.0.057505-0 Jagadeesan, 2010, LAP, an alcohol acetaldehyde dehydrogenase enzyme in Listeria, promotes bacterial adhesion to enterocyte-like Caco-2 cells only in pathogenic species, Microbiology, 156, 2782, 10.1099/mic.0.036509-0 Jagadeesan, 2011, N-terminal Gly(224)-Gly(411) domain in Listeria adhesion protein interacts with host receptor Hsp60, PLoS ONE, 6, e20694, 10.1371/journal.pone.0020694 Jaradat, 2003, A Listeria adhesion protein-deficient Listeria monocytogenes strain shows reduced adhesion primarily to intestinal cell lines, Med. Microbiol. Immunol. (Berl.), 192, 85, 10.1007/s00430-002-0150-1 Jung, 1995, A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion, J. Clin. Invest., 95, 55, 10.1172/JCI117676 Kayal, 2002, Listeriolysin O secreted by Listeria monocytogenes induces NF-kappaB signalling by activating the IkappaB kinase complex, Mol. Microbiol., 44, 1407, 10.1046/j.1365-2958.2002.02973.x Kobayashi, 2005, Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract, Science, 307, 731, 10.1126/science.1104911 Kocks, 1992, L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein, Cell, 68, 521, 10.1016/0092-8674(92)90188-I Lecuit, 1999, A single amino acid in E-cadherin responsible for host specificity towards the human pathogen Listeria monocytogenes, EMBO J., 18, 3956, 10.1093/emboj/18.14.3956 Lecuit, 2001, A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier, Science, 292, 1722, 10.1126/science.1059852 Lecuit, 2007, Functional genomic studies of the intestinal response to a foodborne enteropathogen in a humanized gnotobiotic mouse model, J. Biol. Chem., 282, 15065, 10.1074/jbc.M610926200 Ma, 2004, TNF-alpha-induced increase in intestinal epithelial tight junction permeability requires NF-kappa B activation, Am. J. Physiol. Gastrointest. Liver Physiol., 286, G367, 10.1152/ajpgi.00173.2003 Ma, 2005, Mechanism of TNF-alpha modulation of Caco-2 intestinal epithelial tight junction barrier: role of myosin light-chain kinase protein expression, Am. J. Physiol. Gastrointest. Liver Physiol., 288, G422, 10.1152/ajpgi.00412.2004 Mansell, 2000, A novel function of InIB from Listeria monocytogenes: activation of NF-kappaB in J774 macrophages, Cell. Microbiol., 2, 127, 10.1046/j.1462-5822.2000.00038.x Marchiando, 2011, The epithelial barrier is maintained by in vivo tight junction expansion during pathologic intestinal epithelial shedding, Gastroenterology, 140, 1208, 10.1053/j.gastro.2011.01.004 Mengaud, 1996, E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells, Cell, 84, 923, 10.1016/S0092-8674(00)81070-3 Nikitas, 2011, Transcytosis of Listeria monocytogenes across the intestinal barrier upon specific targeting of goblet cell accessible E-cadherin, J. Exp. Med., 208, 2263, 10.1084/jem.20110560 Oeckinghaus, 2011, Crosstalk in NF-κB signaling pathways, Nat. Immunol., 12, 695, 10.1038/ni.2065 Owens, 2005, A strategy to identify stable membrane-permeant peptide inhibitors of myosin light chain kinase, Pharm. Res., 22, 703, 10.1007/s11095-005-2584-9 Pentecost, 2006, Listeria monocytogenes invades the epithelial junctions at sites of cell extrusion, PLoS Pathog., 2, e3, 10.1371/journal.ppat.0020003 Portnoy, 1988, Role of hemolysin for the intracellular growth of Listeria monocytogenes, J. Exp. Med., 167, 1459, 10.1084/jem.167.4.1459 Pron, 1998, Comprehensive study of the intestinal stage of listeriosis in a rat ligated ileal loop system, Infect. Immun., 66, 747, 10.1128/IAI.66.2.747-755.1998 Radoshevich, 2018, Listeria monocytogenes: towards a complete picture of its physiology and pathogenesis, Nat. Rev. Microbiol., 16, 32, 10.1038/nrmicro.2017.126 Rajabian, 2009, The bacterial virulence factor InlC perturbs apical cell junctions and promotes cell-to-cell spread of Listeria, Nat. Cell Biol., 11, 1212, 10.1038/ncb1964 Regan, 2013, Identification of TLR10 as a key mediator of the inflammatory response to Listeria monocytogenes in intestinal epithelial cells and macrophages, J. Immunol., 191, 6084, 10.4049/jimmunol.1203245 Speth, 1999, A 60 kD heat-shock protein-like molecule interacts with the HIV transmembrane glycoprotein gp41, Mol. Immunol., 36, 619, 10.1016/S0161-5890(99)00082-6 Stevenson, 1994, Concentration-dependent effects of cytochalasin D on tight junctions and actin filaments in MDCK epithelial cells, J. Cell Sci., 107, 367, 10.1242/jcs.107.3.367 Tilney, 1989, Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes, J. Cell Biol., 109, 1597, 10.1083/jcb.109.4.1597 Tsuchiya, 2005, Listeriolysin O-induced membrane permeation mediates persistent interleukin-6 production in Caco-2 cells during Listeria monocytogenes infection in vitro, Infect. Immun., 73, 3869, 10.1128/IAI.73.7.3869-3877.2005 Vabulas, 2001, Endocytosed HSP60s use toll-like receptor 2 (TLR2) and TLR4 to activate the toll/interleukin-1 receptor signaling pathway in innate immune cells, J. Biol. Chem., 276, 31332, 10.1074/jbc.M103217200 Wampler, 2004, Heat shock protein 60 acts as a receptor for the Listeria adhesion protein in Caco-2 cells, Infect. Immun., 72, 931, 10.1128/IAI.72.2.931-936.2004 Wollert, 2007, Extending the host range of Listeria monocytogenes by rational protein design, Cell, 129, 891, 10.1016/j.cell.2007.03.049 Xanthoudakis, 1999, Hsp60 accelerates the maturation of pro-caspase-3 by upstream activator proteases during apoptosis, EMBO J., 18, 2049, 10.1093/emboj/18.8.2049