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Repair of airway epithelia requires metabolic rewiring towards fatty acid oxidation

Epithelial tissues provide front-line barriers shielding the organism from invading pathogens and harmful substances. In the airway epithelium, the combined action of multiciliated and secretory cells sustains the mucociliary escalator required for clearance of microbes and particles from the airway...

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Autores principales: Crotta, Stefania, Villa, Matteo, Major, Jack, Finsterbusch, Katja, Llorian, Miriam, Carmeliet, Peter, Buescher, Joerg, Wack, Andreas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9925445/
https://www.ncbi.nlm.nih.gov/pubmed/36781848
http://dx.doi.org/10.1038/s41467-023-36352-z
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author Crotta, Stefania
Villa, Matteo
Major, Jack
Finsterbusch, Katja
Llorian, Miriam
Carmeliet, Peter
Buescher, Joerg
Wack, Andreas
author_facet Crotta, Stefania
Villa, Matteo
Major, Jack
Finsterbusch, Katja
Llorian, Miriam
Carmeliet, Peter
Buescher, Joerg
Wack, Andreas
author_sort Crotta, Stefania
collection PubMed
description Epithelial tissues provide front-line barriers shielding the organism from invading pathogens and harmful substances. In the airway epithelium, the combined action of multiciliated and secretory cells sustains the mucociliary escalator required for clearance of microbes and particles from the airways. Defects in components of mucociliary clearance or barrier integrity are associated with recurring infections and chronic inflammation. The timely and balanced differentiation of basal cells into mature epithelial cell subsets is therefore tightly controlled. While different growth factors regulating progenitor cell proliferation have been described, little is known about the role of metabolism in these regenerative processes. Here we show that basal cell differentiation correlates with a shift in cellular metabolism from glycolysis to fatty acid oxidation (FAO). We demonstrate both in vitro and in vivo that pharmacological and genetic impairment of FAO blocks the development of fully differentiated airway epithelial cells, compromising the repair of airway epithelia. Mechanistically, FAO links to the hexosamine biosynthesis pathway to support protein glycosylation in airway epithelial cells. Our findings unveil the metabolic network underpinning the differentiation of airway epithelia and identify novel targets for intervention to promote lung repair.
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spelling pubmed-99254452023-02-15 Repair of airway epithelia requires metabolic rewiring towards fatty acid oxidation Crotta, Stefania Villa, Matteo Major, Jack Finsterbusch, Katja Llorian, Miriam Carmeliet, Peter Buescher, Joerg Wack, Andreas Nat Commun Article Epithelial tissues provide front-line barriers shielding the organism from invading pathogens and harmful substances. In the airway epithelium, the combined action of multiciliated and secretory cells sustains the mucociliary escalator required for clearance of microbes and particles from the airways. Defects in components of mucociliary clearance or barrier integrity are associated with recurring infections and chronic inflammation. The timely and balanced differentiation of basal cells into mature epithelial cell subsets is therefore tightly controlled. While different growth factors regulating progenitor cell proliferation have been described, little is known about the role of metabolism in these regenerative processes. Here we show that basal cell differentiation correlates with a shift in cellular metabolism from glycolysis to fatty acid oxidation (FAO). We demonstrate both in vitro and in vivo that pharmacological and genetic impairment of FAO blocks the development of fully differentiated airway epithelial cells, compromising the repair of airway epithelia. Mechanistically, FAO links to the hexosamine biosynthesis pathway to support protein glycosylation in airway epithelial cells. Our findings unveil the metabolic network underpinning the differentiation of airway epithelia and identify novel targets for intervention to promote lung repair. Nature Publishing Group UK 2023-02-13 /pmc/articles/PMC9925445/ /pubmed/36781848 http://dx.doi.org/10.1038/s41467-023-36352-z Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Crotta, Stefania
Villa, Matteo
Major, Jack
Finsterbusch, Katja
Llorian, Miriam
Carmeliet, Peter
Buescher, Joerg
Wack, Andreas
Repair of airway epithelia requires metabolic rewiring towards fatty acid oxidation
title Repair of airway epithelia requires metabolic rewiring towards fatty acid oxidation
title_full Repair of airway epithelia requires metabolic rewiring towards fatty acid oxidation
title_fullStr Repair of airway epithelia requires metabolic rewiring towards fatty acid oxidation
title_full_unstemmed Repair of airway epithelia requires metabolic rewiring towards fatty acid oxidation
title_short Repair of airway epithelia requires metabolic rewiring towards fatty acid oxidation
title_sort repair of airway epithelia requires metabolic rewiring towards fatty acid oxidation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9925445/
https://www.ncbi.nlm.nih.gov/pubmed/36781848
http://dx.doi.org/10.1038/s41467-023-36352-z
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