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  • Samperio Ventayol, PilarUppsala universitet,Institutionen för medicinsk biokemi och mikrobiologi,Science for Life Laboratory, SciLifeLab (author)

Bacterial detection by NAIP/NLRC4 elicits prompt contractions of intestinal epithelial cell layers

  • Article/chapterEnglish2021

Publisher, publication year, extent ...

  • 2021-04-12
  • Proceedings of the National Academy of Sciences,2021
  • printrdacarrier

Numbers

  • LIBRIS-ID:oai:DiVA.org:su-194132
  • https://urn.kb.se/resolve?urn=urn:nbn:se:su:diva-194132URI
  • https://doi.org/10.1073/pnas.2013963118DOI
  • https://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-443193URI

Supplementary language notes

  • Language:English
  • Summary in:English

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  • Subject category:ref swepub-contenttype
  • Subject category:art swepub-publicationtype

Notes

  • The gut epithelium serves to maximize the surface for nutrient and fluid uptake, but at the same time must provide a tight barrier to pathogens and remove damaged intestinal epithelial cells (IECs) without jeopardizing barrier integrity. How the epithelium coordinates these tasks remains a question of significant interest. We used imaging and an optical flow analysis pipeline to study the dynamicity of untransformed murine and human intestinal epithelia, cultured atop flexible hydrogel supports. Infection with the pathogen Salmonella Typhimurium (S.Tm) within minutes elicited focal contractions with inward movements of up to similar to 1,000 IECs. Genetics approaches and chimeric epithelial monolayers revealed contractions to be triggered by the NAIP/NLRC4 inflammasome, which sensed type-III secretion system and flagellar ligands upon bacterial invasion, converting the local tissue into a contraction epicenter. Execution of the response required swift sublytic Gasdermin D pore formation, ion fluxes, and the propagation of a myosin contraction pulse across the tissue. Importantly, focal contractions preceded, and could be uncoupled from, the death and expulsion of infected IECs. In both two-dimensional monolayers and three-dimensional enteroids, multiple infection-elicited contractions coalesced to produce shrinkage of the epithelium as a whole. Monolayers deficient for Caspase-1(-11) or Gasdermin D failed to elicit focal contractions but were still capable of infected IEC death and expulsion. Strikingly, these monolayers lost their integrity to a markedly higher extent than wild-type counterparts. We propose that prompt NAIP/NLRC4/Caspase-1/Gasdermin D/myosin-dependent contractions allow the epithelium to densify its cell packing in infected regions, thereby preventing tissue disintegration due to the subsequent IEC death and expulsion process.

Subject headings and genre

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  • Geiser, PetraUppsala universitet,Institutionen för medicinsk biokemi och mikrobiologi,Science for Life Laboratory, SciLifeLab(Swepub:uu)petma163 (author)
  • Di Martino, Maria LetiziaUppsala universitet,Institutionen för medicinsk biokemi och mikrobiologi,Science for Life Laboratory, SciLifeLab(Swepub:uu)mardi655 (author)
  • Florbrant, AlexandraUppsala universitet,Institutionen för medicinsk biokemi och mikrobiologi,Science for Life Laboratory, SciLifeLab(Swepub:uu)alefl114 (author)
  • Fattinger, Stefan A.Uppsala universitet,Institutionen för medicinsk biokemi och mikrobiologi,Science for Life Laboratory, SciLifeLab,Swiss Fed Inst Technol, Dept Biol, Inst Microbiol, CH-8093 Zurich, Switzerland(Swepub:uu)stefa818 (author)
  • Walder, NaemiSwiss Fed Inst Technol, Dept Biol, Inst Microbiol, CH-8093 Zurich, Switzerland (author)
  • Sima, Eduardo,Ph.D.1975-Uppsala universitet,Gastrointestinalkirurgi(Swepub:uu)edusi537 (author)
  • Shao, FengNatl Inst Biol Sci, Beijing 102206, Peoples R China (author)
  • Gekara, Nelson O.Stockholms universitet,Institutionen för molekylär biovetenskap, Wenner-Grens institut,Stockholm Univ, Wenner Gren Inst, Dept Mol Biosci, S-10691 Stockholm, Sweden(Swepub:su)nege2263 (author)
  • Sundbom, MagnusUppsala universitet,Gastrointestinalkirurgi(Swepub:uu)magsundb (author)
  • Hardt, Wolf-DietrichSwiss Fed Inst Technol, Dept Biol, Inst Microbiol, CH-8093 Zurich, Switzerland (author)
  • Webb, Dominic-LucUppsala universitet,Gastroenterologi/hepatologi(Swepub:uu)domwe127 (author)
  • Hellström, Per M.,1954-Uppsala universitet,Gastroenterologi/hepatologi(Swepub:uu)perhe742 (author)
  • Eriksson, Jens,1982-Uppsala universitet,Institutionen för medicinsk biokemi och mikrobiologi,Science for Life Laboratory, SciLifeLab(Swepub:uu)jeeri205 (author)
  • Sellin, Mikael E.Uppsala universitet,Science for Life Laboratory, SciLifeLab,Institutionen för medicinsk biokemi och mikrobiologi(Swepub:uu)mikse125 (author)
  • Uppsala universitetInstitutionen för medicinsk biokemi och mikrobiologi (creator_code:org_t)

Related titles

  • In:Proceedings of the National Academy of Sciences of the United States of America: Proceedings of the National Academy of Sciences118:160027-84241091-6490

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