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Helicobacter pylori shows tropism to gastric differentiated pit cells dependent on urea chemotaxis

Author

Listed:
  • Carmen Aguilar

    (Julius Maximilians University of Würzburg)

  • Mindaugas Pauzuolis

    (Julius Maximilians University of Würzburg)

  • Malvika Pompaiah

    (Julius Maximilians University of Würzburg)

  • Ehsan Vafadarnejad

    (Helmholtz-Centre for Infection Research (HZI))

  • Panagiota Arampatzi

    (University of Würzburg)

  • Mara Fischer

    (Julius Maximilians University of Würzburg)

  • Dominik Narres

    (Julius Maximilians University of Würzburg)

  • Mastura Neyazi

    (Julius Maximilians University of Würzburg)

  • Özge Kayisoglu

    (Julius Maximilians University of Würzburg)

  • Thomas Sell

    (Charité Universitätsmedizin Berlin)

  • Nils Blüthgen

    (Charité Universitätsmedizin Berlin)

  • Markus Morkel

    (Charité Universitätsmedizin Berlin)

  • Armin Wiegering

    (University Hospital of Würzburg)

  • Christoph-Thomas Germer

    (University Hospital of Würzburg)

  • Stefan Kircher

    (Julius Maximilian University of Würzburg and Comprehensive Cancer Center Mainfranken)

  • Andreas Rosenwald

    (Julius Maximilian University of Würzburg and Comprehensive Cancer Center Mainfranken)

  • Antoine-Emmanuel Saliba

    (Helmholtz-Centre for Infection Research (HZI))

  • Sina Bartfeld

    (Julius Maximilians University of Würzburg
    Technische Universität Berlin and Charité–Universitätsmedizin Berlin
    Technische Universität Berlin)

Abstract

The human gastric epithelium forms highly organized gland structures with different subtypes of cells. The carcinogenic bacterium Helicobacter pylori can attach to gastric cells and subsequently translocate its virulence factor CagA, but the possible host cell tropism of H. pylori is currently unknown. Here, we report that H. pylori preferentially attaches to differentiated cells in the pit region of gastric units. Single-cell RNA-seq shows that organoid-derived monolayers recapitulate the pit region, while organoids capture the gland region of the gastric units. Using these models, we show that H. pylori preferentially attaches to highly differentiated pit cells, marked by high levels of GKN1, GKN2 and PSCA. Directed differentiation of host cells enable enrichment of the target cell population and confirm H. pylori preferential attachment and CagA translocation into these cells. Attachment is independent of MUC5AC or PSCA expression, and instead relies on bacterial TlpB-dependent chemotaxis towards host cell-released urea, which scales with host cell size.

Suggested Citation

  • Carmen Aguilar & Mindaugas Pauzuolis & Malvika Pompaiah & Ehsan Vafadarnejad & Panagiota Arampatzi & Mara Fischer & Dominik Narres & Mastura Neyazi & Özge Kayisoglu & Thomas Sell & Nils Blüthgen & Mar, 2022. "Helicobacter pylori shows tropism to gastric differentiated pit cells dependent on urea chemotaxis," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33165-4
    DOI: 10.1038/s41467-022-33165-4
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    as
    1. Rasa Elmentaite & Natsuhiko Kumasaka & Kenny Roberts & Aaron Fleming & Emma Dann & Hamish W. King & Vitalii Kleshchevnikov & Monika Dabrowska & Sophie Pritchard & Liam Bolt & Sara F. Vieira & Lira Mam, 2021. "Cells of the human intestinal tract mapped across space and time," Nature, Nature, vol. 597(7875), pages 250-255, September.
    2. Mirjana Kessler & Karen Hoffmann & Kristin Fritsche & Volker Brinkmann & Hans-Joachim Mollenkopf & Oliver Thieck & Ana Rita Teixeira da Costa & Elena I. Braicu & Jalid Sehouli & Mandy Mangler & Hilmar, 2019. "Chronic Chlamydia infection in human organoids increases stemness and promotes age-dependent CpG methylation," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    3. Terry Kwok & Dana Zabler & Sylwia Urman & Manfred Rohde & Roland Hartig & Silja Wessler & Rolf Misselwitz & Jürgen Berger & Norbert Sewald & Wolfgang König & Steffen Backert, 2007. "Helicobacter exploits integrin for type IV secretion and kinase activation," Nature, Nature, vol. 449(7164), pages 862-866, October.
    4. Raphael Brandt & Thomas Sell & Mareen Lüthen & Florian Uhlitz & Bertram Klinger & Pamela Riemer & Claudia Giesecke-Thiel & Silvia Schulze & Ismail Amr El-Shimy & Desiree Kunkel & Beatrix Fauler & Thor, 2019. "Cell type-dependent differential activation of ERK by oncogenic KRAS in colon cancer and intestinal epithelium," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    5. Cayetano Pleguezuelos-Manzano & Jens Puschhof & Axel Rosendahl Huber & Arne van Hoeck & Henry M. Wood & Jason Nomburg & Carino Gurjao & Freek Manders & Guillaume Dalmasso & Paul B. Stege & Fernanda L., 2020. "Mutational signature in colorectal cancer caused by genotoxic pks+ E. coli," Nature, Nature, vol. 580(7802), pages 269-273, April.
    6. Florian Erhard & Marisa A. P. Baptista & Tobias Krammer & Thomas Hennig & Marius Lange & Panagiota Arampatzi & Christopher S. Jürges & Fabian J. Theis & Antoine-Emmanuel Saliba & Lars Dölken, 2019. "scSLAM-seq reveals core features of transcription dynamics in single cells," Nature, Nature, vol. 571(7765), pages 419-423, July.
    7. Sandy R. Pernitzsch & Mona Alzheimer & Belinda U. Bremer & Marie Robbe-Saule & Hilde De Reuse & Cynthia M. Sharma, 2021. "Small RNA mediated gradual control of lipopolysaccharide biosynthesis affects antibiotic resistance in Helicobacter pylori," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
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