Epithelial cells provide immunocompetence to the early embryo for bacterial clearance

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• dc.contributor.author Roncero-Carol, Joan
• dc.contributor.author Olaizola-Muñoa, June
• dc.contributor.author Aran, Begoña
• dc.contributor.author Mularoni, Loris
• dc.contributor.author Miret-Cuesta, Marta
• dc.contributor.author Blanco Cabra, Núria
• dc.contributor.author Casals, Marc
• dc.contributor.author Rumbo Roig, Mireia
• dc.contributor.author Solé Inarejos, Miquel
• dc.contributor.author Ojosnegros, Samuel
• dc.contributor.author Alsina i Español, Berta
• dc.contributor.author Torrents, Eduard
• dc.contributor.author Veiga, Anna
• dc.contributor.author Irimia Martínez, Manuel
• dc.contributor.author Hoijman, Esteban
• dc.date.accessioned 2025-07-28T07:08:13Z
• dc.date.available 2025-07-28T07:08:13Z
• dc.date.issued 2025
• dc.description.abstract Early embryos are exposed to environmental perturbations that may influence their development, including bacteria. Despite lacking a proper immune system, the surface epithelium of early embryos (trophectoderm in mammals) can phagocytose defective pluripotent cells. Here, we explore the dynamic interactions between early embryos and bacteria. Quantitative live imaging of infection models developed in zebrafish embryos reveals the efficient phagocytic capability of surface epithelia in detecting, ingesting, and destroying infiltrated E. coli and S. aureus. In vivo single-cell interferences uncover actin-based epithelial zippering protrusions mediating bacterial phagocytosis, safeguarding developmental robustness upon infection. Transcriptomic and inter-scale dynamic analyses of phagocyte-bacteria interactions identify specific features of this epithelial phagocytic program. Notably, live imaging of mouse and human blastocysts supports a conserved role of the trophectoderm in bacterial phagocytosis. This defensive role of the surface epithelium against bacterial infection provides immunocompetence to early embryos, with relevant implications for understanding failures in human embryogenesis.
• dc.description.sponsorship We thank Andrés Hidalgo, Miguel Torres, and Stefanie Wculek for discussions and suggestions for the manuscript. We particularly thank Stephen Forrow, Barbara Tondelli, and Julien Colombelli from IRB, Tania García Becerra from IBMB, and Juana Fernández Rodríguez and Antoni Ventura from IDIBELL, for making possible the mouse experiments. We thank the support of the Animal facility, Bioimaging platform and Biostatistics Unit from IDIBELL, the Genomics unit from CRG, and the flow cytometry services from VHIR and the Parc Cientific of Barcelona. We thank Javier Moreno Santos for the mCherry-expressing strain, Senda Jimenez Delgado for sharing technical expertise, Nelly Henry for the bacteria with different motility, Jeff Rasmussen for the UAS-FYVE plasmid, Jan Roelof van Der Meer for the pHLuorin plasmids, Jeremy H. Lakey for the Caf1 plasmid, Shrikrishnan Sankaran for the fluorescent L. plantarum strains, Ákos T. Kovács for the fluorescent B. subtilis strains, Shang Yang for the BFP plasmid, Kayvon Pedram for the Rhobo6 dye, Verena Ruprecht for the dnFhod1 plasmid, Aitor Lavado for his assistance with the graphic design work, and Jordi Guiu, Victoriano Mulero, and Miguel Moreno Mateos for sharing resources. J.R.-C. acknowledges an FPU fellowship 22/04307 funded by Spanish Ministry of Science and Innovation and an FI fellowship 100057 from AGAUR. E.T. acknowledges funding from MCIN/AEI/10.13039/501100011033 “ERDF A way of making Europe” PID2021-125801OB-100 and AGAUR 2021SGR01545. A.V. acknowledges funding from Instituto de Salud Carlos III (PT23/00092). M.I. acknowledges funding from the Spanish Ministry of Science and Innovation (PID2020-115040GB-I00). E.H. acknowledges support from the Spanish Ministry of Science and Innovation (PID2020-117540GB-I00 and PID2023-151237NB-I00) and the AGAUR (2022-SGR-00974). E.H. held a Serra Hunter Lecturer position by the Generalitat of Catalonia at the University of Barcelona.
• dc.format.mimetype application/pdf
• dc.identifier.citation Roncero-Carol J, Olaizola-Muñoa J, Arán B, Mularoni LS, Miret Cuesta M, Blanco-Cabra N, et al. Epithelial cells provide immunocompetence to the early embryo for bacterial clearance. Cell Host & Microbe. 2025;33(7):1106–20. DOI: 10.1016/j.chom.2025.05.025
• dc.identifier.doi http://dx.doi.org/10.1016/j.chom.2025.05.025
• dc.identifier.issn 1931-3128
• dc.identifier.uri http://hdl.handle.net/10230/71009
• dc.language.iso eng
• dc.publisher Elsevier
• dc.relation.ispartof Cell Host & Microbe. 2025;33(7):1106–20
• dc.relation.projectID info:eu-repo/grantAgreement/ES/3PE/PID2021-125801OB-100
• dc.relation.projectID info:eu-repo/grantAgreement/ES/2PE/PID2020-115040GB-I00
• dc.relation.projectID info:eu-repo/grantAgreement/ES/3PE/PID2023-151237NB-I00
• dc.rights © 2025 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
• dc.rights.accessRights info:eu-repo/semantics/openAccess
• dc.rights.uri http://creativecommons.org/licenses/by/4.0/
• dc.subject.keyword Embryonic development
• dc.subject.keyword Cell dynamics
• dc.subject.keyword Phagocytosis
• dc.subject.keyword Epithelial tissue
• dc.subject.keyword Quantitative live imaging
• dc.subject.keyword Bacterial infections
• dc.subject.keyword Host-pathogen interactions
• dc.subject.keyword Zebrafish
• dc.subject.keyword Human embryo
• dc.title Epithelial cells provide immunocompetence to the early embryo for bacterial clearance
• dc.type info:eu-repo/semantics/article
• dc.type.version info:eu-repo/semantics/publishedVersion