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Here, using the gerbil model, permissive to internalin (Inl) A\/B-mediated pathways like in humans, we demonstrate that\n                      <jats:italic>Lm<\/jats:italic>\n                      crosses the intestinal villi at 48 h post-infection. In contrast, the single isogenic (\n                      <jats:italic>lap<\/jats:italic>\n                      <jats:sup>\u2212<\/jats:sup>\n                      or \u0394\n                      <jats:italic>inlA<\/jats:italic>\n                      ) or double (\n                      <jats:italic>lap<\/jats:italic>\n                      <jats:sup>\u2212<\/jats:sup>\n                      \u0394\n                      <jats:italic>inlA<\/jats:italic>\n                      ) mutant strains show significant defects. LAP promotes\n                      <jats:italic>Lm<\/jats:italic>\n                      translocation via endocytosis of cell-cell junctional complex in enterocytes that do not display luminal E-cadherin. In comparison, InlA facilitates\n                      <jats:italic>Lm<\/jats:italic>\n                      translocation at cells displaying apical E-cadherin during cell extrusion and mucus expulsion from goblet cells. LAP hijacks caveolar endocytosis to traffic integral junctional proteins to the early and recycling endosomes. Pharmacological inhibition in a cell line and genetic knockout of caveolin-1 in mice prevents LAP-induced intestinal permeability, junctional endocytosis, and\n                      <jats:italic>Lm<\/jats:italic>\n                      translocation. Furthermore, LAP-Hsp60-dependent tight junction remodeling is also necessary for InlA access to E-cadherin for\n                      <jats:italic>Lm<\/jats:italic>\n                      intestinal barrier crossing in InlA-permissive hosts.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>IMPORTANCE<\/jats:title>\n                    <jats:p>\n                      <jats:italic>Listeria monocytogenes<\/jats:italic>\n                      (\n                      <jats:italic>Lm<\/jats:italic>\n                      ) is a foodborne pathogen with high mortality (20%\u201330%) and hospitalization rates (94%), particularly affecting vulnerable groups such as pregnant women, fetuses, newborns, seniors, and immunocompromised individuals. Invasive listeriosis involves\n                      <jats:italic>Lm<\/jats:italic>\n                      \u2019s internalin (InlA) protein binding to E-cadherin to breach the intestinal barrier. However, non-functional InlA variants have been identified in\n                      <jats:italic>Lm<\/jats:italic>\n                      isolates, suggesting InlA-independent pathways for translocation. Our study reveals that\n                      <jats:italic>Listeria<\/jats:italic>\n                      adhesion protein (LAP) and InlA cooperatively assist\n                      <jats:italic>Lm<\/jats:italic>\n                      entry into the gut lamina propria in a gerbil model, mimicking human listeriosis in early infection stages. LAP triggers caveolin-1-mediated endocytosis of critical junctional proteins, transporting them to early and recycling endosomes, facilitating\n                      <jats:italic>Lm<\/jats:italic>\n                      passage through enterocytes. Furthermore, LAP-Hsp60-mediated junctional protein endocytosis precedes InlA\u2019s interaction with basolateral E-cadherin, emphasizing LAP and InlA\u2019s cooperation in enhancing\n                      <jats:italic>Lm<\/jats:italic>\n                      intestinal translocation. This understanding is vital in combating the severe consequences of\n                      <jats:italic>Lm<\/jats:italic>\n                      infection, including sepsis, meningitis, encephalitis, and brain abscess.\n                    <\/jats:p>\n                  <\/jats:sec>","DOI":"10.1128\/mbio.02821-23","type":"journal-article","created":{"date-parts":[[2024,2,20]],"date-time":"2024-02-20T09:00:21Z","timestamp":1708419621000},"update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":16,"title":["<i>Listeria<\/i>\n                    adhesion protein orchestrates caveolae-mediated apical junctional remodeling of epithelial barrier for\n                    <i>Listeria monocytogenes<\/i>\n                    translocation"],"prefix":"10.1128","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8405-2961","authenticated-orcid":true,"given":"Rishi","family":"Drolia","sequence":"first","affiliation":[{"name":"Department of Food Science, Molecular Food Microbiology Laboratory, Purdue University, West Lafayette, Indiana, USA"},{"name":"Department of Biological Science, Old Dominion University, Norfolk, Virginia, USA"},{"name":"Department of Biological Science, Eastern Kentucky University, Richmond, Kentucky, USA"},{"name":"Purdue Institute of Inflammation, Immunology, and Infectious Disease, Purdue University, West Lafayette, Indiana, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Donald B.","family":"Bryant","sequence":"additional","affiliation":[{"name":"Department of Biological Science, Eastern Kentucky University, Richmond, Kentucky, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shivendra","family":"Tenguria","sequence":"additional","affiliation":[{"name":"Department of Food Science, Molecular Food Microbiology Laboratory, Purdue University, West Lafayette, Indiana, USA"},{"name":"Purdue Institute of Inflammation, Immunology, and Infectious Disease, Purdue University, West Lafayette, Indiana, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zuri A.","family":"Jules-Culver","sequence":"additional","affiliation":[{"name":"Department of Biological Science, Old Dominion University, Norfolk, Virginia, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jessie","family":"Thind","sequence":"additional","affiliation":[{"name":"Department of Biological Science, Eastern Kentucky University, Richmond, Kentucky, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Breanna","family":"Amelunke","sequence":"additional","affiliation":[{"name":"Department of Biological Science, Eastern Kentucky University, Richmond, Kentucky, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dongqi","family":"Liu","sequence":"additional","affiliation":[{"name":"Department of Food Science, Molecular Food Microbiology Laboratory, Purdue University, West Lafayette, Indiana, USA"},{"name":"Purdue Institute of Inflammation, Immunology, and Infectious Disease, Purdue University, West Lafayette, Indiana, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicholas L. 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