Comparative metabolomics analysis of bronchial epithelium during barrier establishment after allergen exposure

Abstract Background Several studies have shown a correlation between an altered metabolome and respiratory allergies. The epithelial barrier hypothesis proposes that an epithelial barrier dysfunction can result in allergic diseases development. Der p 1 allergen from house dust mite is a renowned epi...

Full description

Bibliographic Details
Main Authors: Juan Carlos López‐Rodríguez, Juan Rodríguez‐Coira, Sara Benedé, Coral Barbas, Domingo Barber, María Teresa Villalba, María Marta Escribese, Alma Villaseñor, Eva Batanero
Format: Article
Language:English
Published: Wiley 2021-09-01
Series:Clinical and Translational Allergy
Subjects:
Online Access:https://doi.org/10.1002/clt2.12051
_version_ 1818399864386486272
author Juan Carlos López‐Rodríguez
Juan Rodríguez‐Coira
Sara Benedé
Coral Barbas
Domingo Barber
María Teresa Villalba
María Marta Escribese
Alma Villaseñor
Eva Batanero
author_facet Juan Carlos López‐Rodríguez
Juan Rodríguez‐Coira
Sara Benedé
Coral Barbas
Domingo Barber
María Teresa Villalba
María Marta Escribese
Alma Villaseñor
Eva Batanero
author_sort Juan Carlos López‐Rodríguez
collection DOAJ
description Abstract Background Several studies have shown a correlation between an altered metabolome and respiratory allergies. The epithelial barrier hypothesis proposes that an epithelial barrier dysfunction can result in allergic diseases development. Der p 1 allergen from house dust mite is a renowned epithelial barrier disruptor and allergy initiator due to its cysteine‐protease activity. Here, we compared the metabolic profile of the bronchial epithelium exposed or not to Der p 1 during barrier establishment to understand its active role in allergy development. Methods Calu‐3 cells were cultivated in air‐liquid interface cultures and exposed to either Der p 1 or Ole e 1 allergens during barrier establishment. The comparative metabolomics analysis of apical and basolateral media were performed using liquid chromatography and capillary electrophoresis both coupled to mass spectrometry. Results We showed that epithelial barrier disruption by Der p 1 was associated with a specific metabolic profile, which was highly dependent on the state of the epithelium at the time of contact. Moreover, an apical‐basolateral distribution of the metabolites was also observed, indicating a compartmentalization of the response with differential metabolic patterns. A number of metabolites were changed by Der p 1, mainly related to amino acids metabolism, such as L‐arginine, L‐kynurenine and L‐methionine. Conclusion This work is the first report on the metabolic response in human bronchial epithelial cells associated with cysteine‐protease Der p 1 activity, which could contribute to allergy development. Moreover, it supports a reformulated epithelial barrier hypothesis that might help to explain allergies and their increasing prevalence.
first_indexed 2024-12-14T07:27:27Z
format Article
id doaj.art-8e2bcd1070b0447bb4f06735abf306e1
institution Directory Open Access Journal
issn 2045-7022
language English
last_indexed 2024-12-14T07:27:27Z
publishDate 2021-09-01
publisher Wiley
record_format Article
series Clinical and Translational Allergy
spelling doaj.art-8e2bcd1070b0447bb4f06735abf306e12022-12-21T23:11:29ZengWileyClinical and Translational Allergy2045-70222021-09-01117n/an/a10.1002/clt2.12051Comparative metabolomics analysis of bronchial epithelium during barrier establishment after allergen exposureJuan Carlos López‐Rodríguez0Juan Rodríguez‐Coira1Sara Benedé2Coral Barbas3Domingo Barber4María Teresa Villalba5María Marta Escribese6Alma Villaseñor7Eva Batanero8Departamento de Bioquímica y Biología Molecular Facultad de Ciencias Químicas Universidad Complutense de Madrid Madrid SpainCentro de Metabolómica y Bioanálisis (CEMBIO) Facultad de Farmacia Universidad San Pablo CEU CEU Universities Madrid SpainDepartamento de Bioquímica y Biología Molecular Facultad de Ciencias Químicas Universidad Complutense de Madrid Madrid SpainCentro de Metabolómica y Bioanálisis (CEMBIO) Facultad de Farmacia Universidad San Pablo CEU CEU Universities Madrid SpainInstituto de Medicina Molecular Aplicada (IMMA) Departamento de Ciencias Médicas Básicas Facultad de Medicina Universidad San Pablo‐CEU CEU Universities Madrid SpainDepartamento de Bioquímica y Biología Molecular Facultad de Ciencias Químicas Universidad Complutense de Madrid Madrid SpainInstituto de Medicina Molecular Aplicada (IMMA) Departamento de Ciencias Médicas Básicas Facultad de Medicina Universidad San Pablo‐CEU CEU Universities Madrid SpainCentro de Metabolómica y Bioanálisis (CEMBIO) Facultad de Farmacia Universidad San Pablo CEU CEU Universities Madrid SpainDepartamento de Bioquímica y Biología Molecular Facultad de Ciencias Químicas Universidad Complutense de Madrid Madrid SpainAbstract Background Several studies have shown a correlation between an altered metabolome and respiratory allergies. The epithelial barrier hypothesis proposes that an epithelial barrier dysfunction can result in allergic diseases development. Der p 1 allergen from house dust mite is a renowned epithelial barrier disruptor and allergy initiator due to its cysteine‐protease activity. Here, we compared the metabolic profile of the bronchial epithelium exposed or not to Der p 1 during barrier establishment to understand its active role in allergy development. Methods Calu‐3 cells were cultivated in air‐liquid interface cultures and exposed to either Der p 1 or Ole e 1 allergens during barrier establishment. The comparative metabolomics analysis of apical and basolateral media were performed using liquid chromatography and capillary electrophoresis both coupled to mass spectrometry. Results We showed that epithelial barrier disruption by Der p 1 was associated with a specific metabolic profile, which was highly dependent on the state of the epithelium at the time of contact. Moreover, an apical‐basolateral distribution of the metabolites was also observed, indicating a compartmentalization of the response with differential metabolic patterns. A number of metabolites were changed by Der p 1, mainly related to amino acids metabolism, such as L‐arginine, L‐kynurenine and L‐methionine. Conclusion This work is the first report on the metabolic response in human bronchial epithelial cells associated with cysteine‐protease Der p 1 activity, which could contribute to allergy development. Moreover, it supports a reformulated epithelial barrier hypothesis that might help to explain allergies and their increasing prevalence.https://doi.org/10.1002/clt2.12051air‐liquid interface culturebronchial epitheliumDer p 1metabolomerespiratory allergy
spellingShingle Juan Carlos López‐Rodríguez
Juan Rodríguez‐Coira
Sara Benedé
Coral Barbas
Domingo Barber
María Teresa Villalba
María Marta Escribese
Alma Villaseñor
Eva Batanero
Comparative metabolomics analysis of bronchial epithelium during barrier establishment after allergen exposure
Clinical and Translational Allergy
air‐liquid interface culture
bronchial epithelium
Der p 1
metabolome
respiratory allergy
title Comparative metabolomics analysis of bronchial epithelium during barrier establishment after allergen exposure
title_full Comparative metabolomics analysis of bronchial epithelium during barrier establishment after allergen exposure
title_fullStr Comparative metabolomics analysis of bronchial epithelium during barrier establishment after allergen exposure
title_full_unstemmed Comparative metabolomics analysis of bronchial epithelium during barrier establishment after allergen exposure
title_short Comparative metabolomics analysis of bronchial epithelium during barrier establishment after allergen exposure
title_sort comparative metabolomics analysis of bronchial epithelium during barrier establishment after allergen exposure
topic air‐liquid interface culture
bronchial epithelium
Der p 1
metabolome
respiratory allergy
url https://doi.org/10.1002/clt2.12051
work_keys_str_mv AT juancarloslopezrodriguez comparativemetabolomicsanalysisofbronchialepitheliumduringbarrierestablishmentafterallergenexposure
AT juanrodriguezcoira comparativemetabolomicsanalysisofbronchialepitheliumduringbarrierestablishmentafterallergenexposure
AT sarabenede comparativemetabolomicsanalysisofbronchialepitheliumduringbarrierestablishmentafterallergenexposure
AT coralbarbas comparativemetabolomicsanalysisofbronchialepitheliumduringbarrierestablishmentafterallergenexposure
AT domingobarber comparativemetabolomicsanalysisofbronchialepitheliumduringbarrierestablishmentafterallergenexposure
AT mariateresavillalba comparativemetabolomicsanalysisofbronchialepitheliumduringbarrierestablishmentafterallergenexposure
AT mariamartaescribese comparativemetabolomicsanalysisofbronchialepitheliumduringbarrierestablishmentafterallergenexposure
AT almavillasenor comparativemetabolomicsanalysisofbronchialepitheliumduringbarrierestablishmentafterallergenexposure
AT evabatanero comparativemetabolomicsanalysisofbronchialepitheliumduringbarrierestablishmentafterallergenexposure