IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-33165-4.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-33165-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-33165-4?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Huiyuan Zhu & Man Li & Dexi Bi & Huiqiong Yang & Yaohui Gao & Feifei Song & Jiayi Zheng & Ruting Xie & Youhua Zhang & Hu Liu & Xuebing Yan & Cheng Kong & Yefei Zhu & Qian Xu & Qing Wei & Huanlong Qin, 2024. "Fusobacterium nucleatum promotes tumor progression in KRAS p.G12D-mutant colorectal cancer by binding to DHX15," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Pietro Demela & Nicola Pirastu & Blagoje Soskic, 2023. "Cross-disorder genetic analysis of immune diseases reveals distinct gene associations that converge on common pathways," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    3. Wenjie Pan & Xuan Wang & Chunhua Ren & Xiao Jiang & Sanqiang Gong & Zhenyu Xie & Nai-Kei Wong & Xiaomin Li & Jiasheng Huang & Dingding Fan & Peng Luo & Yun Yang & Xinyue Ren & Suzhong Yu & Zhou Qin & , 2024. "Sea cucumbers and their symbiotic microbiome have evolved to feed on seabed sediments," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    4. Mathurin Dorel & Bertram Klinger & Tommaso Mari & Joern Toedling & Eric Blanc & Clemens Messerschmidt & Michal Nadler-Holly & Matthias Ziehm & Anja Sieber & Falk Hertwig & Dieter Beule & Angelika Egge, 2021. "Neuroblastoma signalling models unveil combination therapies targeting feedback-mediated resistance," PLOS Computational Biology, Public Library of Science, vol. 17(11), pages 1-26, November.
    5. Alberto Díez-Sánchez & Håvard T. Lindholm & Pia M. Vornewald & Jenny Ostrop & Rouan Yao & Andrew B. Single & Anne Marstad & Naveen Parmar & Tovah N. Shaw & Mara Martín-Alonso & Menno J. Oudhoff, 2024. "LSD1 drives intestinal epithelial maturation and controls small intestinal immune cell composition independent of microbiota in a murine model," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    6. Teresa Rummel & Lygeri Sakellaridi & Florian Erhard, 2023. "grandR: a comprehensive package for nucleotide conversion RNA-seq data analysis," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    7. Susanne Kessler & Bradly Burke & Geoffroy Andrieux & Jan Schinköthe & Lea Hamberger & Johannes Kacza & Shijun Zhan & Clara Reasoner & Taru S. Dutt & Maria Kaukab Osman & Marcela Henao-Tamayo & Julian , 2024. "Deciphering bat influenza H18N11 infection dynamics in male Jamaican fruit bats on a single-cell level," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    8. Kun Yin & Yiling Xu & Ye Guo & Zhong Zheng & Xinrui Lin & Meijuan Zhao & He Dong & Dianyi Liang & Zhi Zhu & Junhua Zheng & Shichao Lin & Jia Song & Chaoyong Yang, 2024. "Dyna-vivo-seq unveils cellular RNA dynamics during acute kidney injury via in vivo metabolic RNA labeling-based scRNA-seq," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    9. Ewart Kuijk & Onno Kranenburg & Edwin Cuppen & Arne Van Hoeck, 2022. "Common anti-cancer therapies induce somatic mutations in stem cells of healthy tissue," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    10. Francesca Menghi & Edison T. Liu, 2022. "Functional genomics of complex cancer genomes," Nature Communications, Nature, vol. 13(1), pages 1-4, December.
    11. Reza Mirzazadeh & Zaneta Andrusivova & Ludvig Larsson & Phillip T. Newton & Leire Alonso Galicia & Xesús M. Abalo & Mahtab Avijgan & Linda Kvastad & Alexandre Denadai-Souza & Nathalie Stakenborg & Ale, 2023. "Spatially resolved transcriptomic profiling of degraded and challenging fresh frozen samples," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    12. Sujath Abbas & Oriol Pich & Ginny Devonshire & Shahriar A. Zamani & Annalise Katz-Summercorn & Sarah Killcoyne & Calvin Cheah & Barbara Nutzinger & Nicola Grehan & Nuria Lopez-Bigas & Rebecca C. Fitzg, 2023. "Mutational signature dynamics shaping the evolution of oesophageal adenocarcinoma," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    13. Akshaya Ramakrishnan & Aikaterini Symeonidi & Patrick Hanel & Katharina T. Schmid & Maria L. Richter & Michael Schubert & Maria Colomé-Tatché, 2023. "epiAneufinder identifies copy number alterations from single-cell ATAC-seq data," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    14. Jasper Panten & Tobias Heinen & Christina Ernst & Nils Eling & Rebecca E. Wagner & Maja Satorius & John C. Marioni & Oliver Stegle & Duncan T. Odom, 2024. "The dynamic genetic determinants of increased transcriptional divergence in spermatids," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    15. Bernard C. H. Lee & Philip S. Robinson & Tim H. H. Coorens & Helen H. N. Yan & Sigurgeir Olafsson & Henry Lee-Six & Mathijs A. Sanders & Hoi Cheong Siu & James Hewinson & Sarah S. K. Yue & Wai Yin Tsu, 2022. "Mutational landscape of normal epithelial cells in Lynch Syndrome patients," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    16. Jia Li & Alan J. Simmons & Caroline V. Hawkins & Sophie Chiron & Marisol A. Ramirez-Solano & Naila Tasneem & Harsimran Kaur & Yanwen Xu & Frank Revetta & Paige N. Vega & Shunxing Bao & Can Cui & Regin, 2024. "Identification and multimodal characterization of a specialized epithelial cell type associated with Crohn’s disease," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    17. Bibiana Costa & Jennifer Becker & Tobias Krammer & Felix Mulenge & Verónica Durán & Andreas Pavlou & Olivia Luise Gern & Xiaojing Chu & Yang Li & Luka Čičin-Šain & Britta Eiz-Vesper & Martin Messerle , 2024. "Human cytomegalovirus exploits STING signaling and counteracts IFN/ISG induction to facilitate infection of dendritic cells," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    18. Candice R. Gurbatri & Georgette A. Radford & Laura Vrbanac & Jongwon Im & Elaine M. Thomas & Courtney Coker & Samuel R. Taylor & YoungUk Jang & Ayelet Sivan & Kyu Rhee & Anas A. Saleh & Tiffany Chien , 2024. "Engineering tumor-colonizing E. coli Nissle 1917 for detection and treatment of colorectal neoplasia," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    19. Arafath K. Najumudeen & Sigrid K. Fey & Laura M. Millett & Catriona A. Ford & Kathryn Gilroy & Nuray Gunduz & Rachel A. Ridgway & Eve Anderson & Douglas Strathdee & William Clark & Colin Nixon & Jenni, 2024. "KRAS allelic imbalance drives tumour initiation yet suppresses metastasis in colorectal cancer in vivo," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    20. Egle Kvedaraite & Magda Lourda & Natalia Mouratidou & Tim Düking & Avinash Padhi & Kirsten Moll & Paulo Czarnewski & Indranil Sinha & Ioanna Xagoraris & Efthymia Kokkinou & Anastasios Damdimopoulos & , 2024. "Intestinal stroma guides monocyte differentiation to macrophages through GM-CSF," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33165-4. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.