Macrophage and neutrophil heterogeneity at single-cell spatial resolution in human inflammatory bowel disease

Alba Garrido-Trigo, Ana M. Corraliza, Marisol Veny, Isabella Dotti, Elisa Melón-Ardanaz, Aina Rill, Helena L. Crowell, Ángel Corbí, Victoria Gudiño, Miriam Esteller, Iris Álvarez-Teubel, Daniel Aguilar, M. Carme Masamunt, Emily Killingbeck, Youngmi Kim, Michael Leon, Sudha Visvanathan, Domenica Marchese, Ginevra Caratù, Albert Martin-Cardona, Maria Esteve, Ingrid Ordás, Julian Panés, Elena Ricart, Elisabetta Mereu, Holger Heyn and Azucena Salas ()
Additional contact information
Alba Garrido-Trigo: Inflammatory Bowel Disease Unit, Institut d’Investigacions Biomèdiques August Pi I Sunyer (IDIBAPS), Hospital Clínic
Ana M. Corraliza: Inflammatory Bowel Disease Unit, Institut d’Investigacions Biomèdiques August Pi I Sunyer (IDIBAPS), Hospital Clínic
Marisol Veny: Inflammatory Bowel Disease Unit, Institut d’Investigacions Biomèdiques August Pi I Sunyer (IDIBAPS), Hospital Clínic
Isabella Dotti: Inflammatory Bowel Disease Unit, Institut d’Investigacions Biomèdiques August Pi I Sunyer (IDIBAPS), Hospital Clínic
Elisa Melón-Ardanaz: Inflammatory Bowel Disease Unit, Institut d’Investigacions Biomèdiques August Pi I Sunyer (IDIBAPS), Hospital Clínic
Aina Rill: Josep Carreras Leukaemia Research Institute (IJC)
Helena L. Crowell: University of Zurich, Switzerland. SIB Swiss Institute of Bioinformatics
Ángel Corbí: Consejo Superior de Investigaciones Científicas (CSIC)
Victoria Gudiño: Inflammatory Bowel Disease Unit, Institut d’Investigacions Biomèdiques August Pi I Sunyer (IDIBAPS), Hospital Clínic
Miriam Esteller: Inflammatory Bowel Disease Unit, Institut d’Investigacions Biomèdiques August Pi I Sunyer (IDIBAPS), Hospital Clínic
Iris Álvarez-Teubel: Inflammatory Bowel Disease Unit, Institut d’Investigacions Biomèdiques August Pi I Sunyer (IDIBAPS), Hospital Clínic
Daniel Aguilar: Inflammatory Bowel Disease Unit, Institut d’Investigacions Biomèdiques August Pi I Sunyer (IDIBAPS), Hospital Clínic
M. Carme Masamunt: Inflammatory Bowel Disease Unit, Institut d’Investigacions Biomèdiques August Pi I Sunyer (IDIBAPS), Hospital Clínic
Emily Killingbeck: NanoString Technologies
Youngmi Kim: NanoString Technologies
Michael Leon: NanoString Technologies
Sudha Visvanathan: Boehringer-Ingelheim Pharmaceuticals Inc
Domenica Marchese: Barcelona Institute of Science and Technology (BIST)
Ginevra Caratù: Barcelona Institute of Science and Technology (BIST)
Albert Martin-Cardona: Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD)
Maria Esteve: Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD)
Ingrid Ordás: Inflammatory Bowel Disease Unit, Institut d’Investigacions Biomèdiques August Pi I Sunyer (IDIBAPS), Hospital Clínic
Julian Panés: Inflammatory Bowel Disease Unit, Institut d’Investigacions Biomèdiques August Pi I Sunyer (IDIBAPS), Hospital Clínic
Elena Ricart: Inflammatory Bowel Disease Unit, Institut d’Investigacions Biomèdiques August Pi I Sunyer (IDIBAPS), Hospital Clínic
Elisabetta Mereu: Josep Carreras Leukaemia Research Institute (IJC)
Holger Heyn: Barcelona Institute of Science and Technology (BIST)
Azucena Salas: Inflammatory Bowel Disease Unit, Institut d’Investigacions Biomèdiques August Pi I Sunyer (IDIBAPS), Hospital Clínic

Nature Communications, 2023, vol. 14, issue 1, 1-18

Abstract: Abstract Ulcerative colitis and Crohn’s disease are chronic inflammatory intestinal diseases with perplexing heterogeneity in disease manifestation and response to treatment. While the molecular basis for this heterogeneity remains uncharacterized, single-cell technologies allow us to explore the transcriptional states within tissues at an unprecedented resolution which could further understanding of these complex diseases. Here, we apply single-cell RNA-sequencing to human inflamed intestine and show that the largest differences among patients are present within the myeloid compartment including macrophages and neutrophils. Using spatial transcriptomics in human tissue at single-cell resolution (CosMx Spatial Molecular Imaging) we spatially localize each of the macrophage and neutrophil subsets identified by single-cell RNA-sequencing and unravel further macrophage diversity based on their tissue localization. Finally, single-cell RNA-sequencing combined with single-cell spatial analysis reveals a strong communication network involving macrophages and inflammatory fibroblasts. Our data sheds light on the cellular complexity of these diseases and points towards the myeloid and stromal compartments as important cellular subsets for understanding patient-to-patient heterogeneity.

Date: 2023
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DOI: 10.1038/s41467-023-40156-6

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