A single-cell atlas of the airway epithelium reveals the CFTR-rich pulmonary ionocyte
Open accessAbstract
The functions of epithelial tissues are dictated by the types, abundance and distribution of the differentiated cells they contain. Attempts to restore tissue function after damage require knowledge of how physiological tasks are distributed among cell types, and how cell states vary between homeostasis, injury-repair and disease. In the conducting airway, a heterogeneous basal cell population gives rise to specialized luminal cells that perform mucociliary clearance 1. Here we perform single-cell profiling of human bronchial epithelial cells and mouse tracheal epithelial cells to obtain a comprehensive census of cell types in the conducting airway and their behaviour in homeostasis and regeneration. Our analysis reveals cell states that represent known and novel cell populations, delineates their heterogeneity and identifies distinct differentiation trajectories during homeostasis and tissue repair. Finally, we identified a novel, rare cell type that we call the 'pulmonary ionocyte', which co-expresses FOXI1, multiple subunits of the vacuolar-type H+-ATPase (V-ATPase) and CFTR, the gene that is mutated in cystic fibrosis. Using immunofluorescence, modulation of signalling pathways and electrophysiology, we show that Notch signalling is necessary and FOXI1 expression is sufficient to drive the production of the pulmonary ionocyte, and that the pulmonary ionocyte is a major source of CFTR activity in the conducting airway epithelium.
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Eight cell clusters were annotated on the basis of known cell-type markers of airway epithelial cells66: cycling basal, basal, hillock, secretory, pre-ciliated, ciliated, ionocyte, PNECs, and brush cells.
“We annotated eight cell clusters on the basis of known cell-type markers of airway epithelial cells66: cycling basal, basal, hillock, secretory, pre-ciliated, ciliated, ionocyte, PNECs, and brush cells.”
From Causal identification of single-cell experimental perturbation effects with CINEMA-OT (2023) · cites this paper as [66]
Single-cell transcriptome methods have discovered new cell types and functional cell states, which motivates tools for single-cell chromatin regulation.
“In parallel, methods to measure the transcriptomes of single cells have been used to discover new cell types11 and new functional cell states12,13, and provide additional motivation for the development of tools to measure chromatin regulation at single-cell resolution14.”
From Droplet-based combinatorial indexing for massive-scale single-cell chromatin accessibility (2019) · cites this paper as [11]
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- Authors
- Plasschaert, L. W., Žilionis, R., Choo-Wing, R., Savova, V., Knehr, J., Roma, G., Klein, A. M., & Jaffe, A. B.
- Affiliations
- Harvard University (US)
- Novartis Institutes for BioMedical Research (CH)
- Corresponding author
- Klein, Allon M.
- Jaffe, Aron B.
- Venue
- Nature
- Published
- 2018-08-01
- Volume
- 560
- Issue
- 7718
- Pages
- 377-381
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC6108322
- OpenAlex
- W2885499809
- Cited by
- 1,047
- References
- 39
- Citations by year
- 2026: 57 · 2025: 116 · 2024: 120 · 2023: 133 · 2022: 149 · 2021: 160 · 2020: 178 · 2019: 111 · 2018: 21
- FWCI
- 90.23
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Heart, Lung, and Blood Institute (R01HL141402)
- National Cancer Institute (R33CA212697)
- Topics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Cystic Fibrosis Research Advances
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Neonatal Respiratory Health Research
- Keywords
- airway epithelium, CFTR, cystic fibrosis, conducting airways, tracheal epithelium, bronchial epithelium, FOXI1, Notch signaling, vacuolar H+-ATPase, epithelial differentiation, tissue regeneration, mucociliary clearance, cellular heterogeneity
- MeSH terms
- Adolescent, Adult, Animals, Bronchi, Cell Differentiation, Cells, Cultured, Child, Child, Preschool, Cystic Fibrosis, Epithelial Cells, Female, Fluorescent Antibody Technique, Homeostasis, Humans, Male, Organ Specificity, Regeneration, Trachea, Signal Transduction, Sequence Analysis, RNA, Cystic Fibrosis Transmembrane Conductance Regulator, Gene Expression Profiling, Vacuolar Proton-Translocating ATPases, Mice, Forkhead Transcription Factors, Receptors, Notch, Young Adult, Single-Cell Analysis
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