Type 2 inflammation drives an airway basal stem cell program through insulin receptor substrate signaling.


Journal

The Journal of allergy and clinical immunology
ISSN: 1097-6825
Titre abrégé: J Allergy Clin Immunol
Pays: United States
ID NLM: 1275002

Informations de publication

Date de publication:
06 2023
Historique:
received: 01 06 2022
revised: 17 01 2023
accepted: 26 01 2023
medline: 9 6 2023
pubmed: 23 2 2023
entrez: 22 2 2023
Statut: ppublish

Résumé

Chronic rhinosinusitis with nasal polyposis (CRSwNP) is a type 2 (T2) inflammatory disease associated with an increased number of airway basal cells (BCs). Recent studies have identified transcriptionally distinct BCs, but the molecular pathways that support or inhibit human BC proliferation and differentiation are largely unknown. We sought to determine the role of T2 cytokines in regulating airway BCs. Single-cell and bulk RNA sequencing of sinus and lung airway epithelial cells was analyzed. Human sinus BCs were stimulated with IL-4 and IL-13 in the presence and absence of inhibitors of IL-4R signaling. Confocal analysis of human sinus tissue and murine airway was performed. Murine BC subsets were sorted for RNA sequencing and functional assays. Fate labeling was performed in a murine model of tracheal injury and regeneration. Two subsets of BCs were found in human and murine respiratory mucosa distinguished by the expression of basal cell adhesion molecule (BCAM). BCAM expression identifies airway stem cells among P63 These findings establish BCAM as a marker of airway stem cells among the BC pool and demonstrate that airway epithelial remodeling in T2 inflammation extends beyond goblet cell metaplasia to the support of a BC stem state poised to perpetuate inflammation.

Sections du résumé

BACKGROUND
Chronic rhinosinusitis with nasal polyposis (CRSwNP) is a type 2 (T2) inflammatory disease associated with an increased number of airway basal cells (BCs). Recent studies have identified transcriptionally distinct BCs, but the molecular pathways that support or inhibit human BC proliferation and differentiation are largely unknown.
OBJECTIVE
We sought to determine the role of T2 cytokines in regulating airway BCs.
METHODS
Single-cell and bulk RNA sequencing of sinus and lung airway epithelial cells was analyzed. Human sinus BCs were stimulated with IL-4 and IL-13 in the presence and absence of inhibitors of IL-4R signaling. Confocal analysis of human sinus tissue and murine airway was performed. Murine BC subsets were sorted for RNA sequencing and functional assays. Fate labeling was performed in a murine model of tracheal injury and regeneration.
RESULTS
Two subsets of BCs were found in human and murine respiratory mucosa distinguished by the expression of basal cell adhesion molecule (BCAM). BCAM expression identifies airway stem cells among P63
CONCLUSIONS
These findings establish BCAM as a marker of airway stem cells among the BC pool and demonstrate that airway epithelial remodeling in T2 inflammation extends beyond goblet cell metaplasia to the support of a BC stem state poised to perpetuate inflammation.

Identifiants

pubmed: 36804595
pii: S0091-6749(23)00211-7
doi: 10.1016/j.jaci.2023.01.030
pii:
doi:

Substances chimiques

Receptor, Insulin EC 2.7.10.1
Interleukin-13 0
Interleukin-4 207137-56-2

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1536-1549

Subventions

Organisme : NIAID NIH HHS
ID : R01 AI134989
Pays : United States
Organisme : NIAID NIH HHS
ID : U19 AI095219
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI175149
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI078908
Pays : United States
Organisme : NIAID NIH HHS
ID : R56 AI134989
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL120952
Pays : United States

Informations de copyright

Copyright © 2023. Published by Elsevier Inc.

Auteurs

Xin Wang (X)

Jeff and Penny Vinik Center for Translational Immunology Research, Division of Allergy and Clinical Immunology, Brigham and Women's Hospital, Boston, Mass; Department of Medicine, Harvard Medical School, Boston, Mass.

Nils R Hallen (NR)

Jeff and Penny Vinik Center for Translational Immunology Research, Division of Allergy and Clinical Immunology, Brigham and Women's Hospital, Boston, Mass; Department of Medicine, Harvard Medical School, Boston, Mass.

Minkyu Lee (M)

Jeff and Penny Vinik Center for Translational Immunology Research, Division of Allergy and Clinical Immunology, Brigham and Women's Hospital, Boston, Mass; Department of Medicine, Harvard Medical School, Boston, Mass.

Sachin Samuchiwal (S)

Jeff and Penny Vinik Center for Translational Immunology Research, Division of Allergy and Clinical Immunology, Brigham and Women's Hospital, Boston, Mass; Department of Medicine, Harvard Medical School, Boston, Mass.

Qihua Ye (Q)

Jeff and Penny Vinik Center for Translational Immunology Research, Division of Allergy and Clinical Immunology, Brigham and Women's Hospital, Boston, Mass; Department of Medicine, Harvard Medical School, Boston, Mass.

Kathleen M Buchheit (KM)

Jeff and Penny Vinik Center for Translational Immunology Research, Division of Allergy and Clinical Immunology, Brigham and Women's Hospital, Boston, Mass; Department of Medicine, Harvard Medical School, Boston, Mass.

Alice Z Maxfield (AZ)

Department of Otolaryngology, Head and Neck Surgery, Brigham and Women's Hospital, Boston, Mass.

Rachel E Roditi (RE)

Department of Otolaryngology, Head and Neck Surgery, Brigham and Women's Hospital, Boston, Mass.

Regan W Bergmark (RW)

Department of Otolaryngology, Head and Neck Surgery, Brigham and Women's Hospital, Boston, Mass.

Neil Bhattacharyya (N)

Department of Otolaryngology, Head and Neck Surgery, Massachusetts Eye and Ear Infirmary, Boston, Mass.

Tessa Ryan (T)

Jeff and Penny Vinik Center for Translational Immunology Research, Division of Allergy and Clinical Immunology, Brigham and Women's Hospital, Boston, Mass; Department of Medicine, Harvard Medical School, Boston, Mass.

Deb Gakpo (D)

Jeff and Penny Vinik Center for Translational Immunology Research, Division of Allergy and Clinical Immunology, Brigham and Women's Hospital, Boston, Mass; Department of Medicine, Harvard Medical School, Boston, Mass.

Soumya Raychaudhuri (S)

Center for Data Sciences, Brigham and Women's Hospital, Boston, Mass; Divisions of Genetics, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Mass; Rheumatology, Inflammation, and Immunity, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Mass; Program in Medical and Population Genetics, Broad Institute of MIT and Harvard, Cambridge, Mass; Versus Arthritis Centre for Genetics and Genomics, Centre for Musculoskeletal Research, Manchester Academic Health Science Centre, University of Manchester, Manchester, United Kingdom.

Dan Dwyer (D)

Jeff and Penny Vinik Center for Translational Immunology Research, Division of Allergy and Clinical Immunology, Brigham and Women's Hospital, Boston, Mass; Department of Medicine, Harvard Medical School, Boston, Mass.

Tanya M Laidlaw (TM)

Jeff and Penny Vinik Center for Translational Immunology Research, Division of Allergy and Clinical Immunology, Brigham and Women's Hospital, Boston, Mass; Department of Medicine, Harvard Medical School, Boston, Mass.

Joshua A Boyce (JA)

Jeff and Penny Vinik Center for Translational Immunology Research, Division of Allergy and Clinical Immunology, Brigham and Women's Hospital, Boston, Mass; Department of Medicine, Harvard Medical School, Boston, Mass.

Maria Gutierrez-Arcelus (M)

Program in Medical and Population Genetics, Broad Institute of MIT and Harvard, Cambridge, Mass; Division of Immunology, Boston Children's Hospital, Boston, Mass.

Nora A Barrett (NA)

Jeff and Penny Vinik Center for Translational Immunology Research, Division of Allergy and Clinical Immunology, Brigham and Women's Hospital, Boston, Mass; Department of Medicine, Harvard Medical School, Boston, Mass. Electronic address: nbarrett@bwh.harvard.edu.

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