Gut Microbiota Abrogates Anti-α-Gal IgA Response in Lungs and Protects against Experimental <i>Aspergillus</i> Infection in Poultry

Naturally occurring human antibodies (Abs) of the isotypes IgM and IgG and reactive to the galactose-α-1,3-galactose (α-Gal) epitope are associated with protection against infectious diseases, caused by pathogens expressing the glycan. Gut microbiota bacteria expressing α-Gal regulate the immune res...

Full description

Bibliographic Details
Main Authors: Lourdes Mateos-Hernández, Veronica Risco-Castillo, Edgar Torres-Maravilla, Luis G. Bermúdez-Humarán, Pilar Alberdi, Adnan Hodžić, Angelica Hernández-Jarguin, Sabine Rakotobe, Clemence Galon, Elodie Devillers, Jose de la Fuente, Jacques Guillot, Alejandro Cabezas-Cruz
Format: Article
Language:English
Published: MDPI AG 2020-06-01
Series:Vaccines
Subjects:
Online Access:https://www.mdpi.com/2076-393X/8/2/285
_version_ 1797565978441154560
author Lourdes Mateos-Hernández
Veronica Risco-Castillo
Edgar Torres-Maravilla
Luis G. Bermúdez-Humarán
Pilar Alberdi
Adnan Hodžić
Angelica Hernández-Jarguin
Sabine Rakotobe
Clemence Galon
Elodie Devillers
Jose de la Fuente
Jacques Guillot
Alejandro Cabezas-Cruz
author_facet Lourdes Mateos-Hernández
Veronica Risco-Castillo
Edgar Torres-Maravilla
Luis G. Bermúdez-Humarán
Pilar Alberdi
Adnan Hodžić
Angelica Hernández-Jarguin
Sabine Rakotobe
Clemence Galon
Elodie Devillers
Jose de la Fuente
Jacques Guillot
Alejandro Cabezas-Cruz
author_sort Lourdes Mateos-Hernández
collection DOAJ
description Naturally occurring human antibodies (Abs) of the isotypes IgM and IgG and reactive to the galactose-α-1,3-galactose (α-Gal) epitope are associated with protection against infectious diseases, caused by pathogens expressing the glycan. Gut microbiota bacteria expressing α-Gal regulate the immune response to this glycan in animals lacking endogenous α-Gal. Here, we asked whether the production of anti-α-Gal Abs in response to microbiota stimulation in birds, confers protection against infection by <i>Aspergillus fumigatus</i>, a major fungal pathogen that expresses α-Gal in its surface. We demonstrated that the oral administration of <i>Escherichia coli</i> O86:B7 strain, a bacterium with high α-Gal content, reduces the occurrence of granulomas in lungs and protects turkeys from developing acute aspergillosis. Surprisingly, the protective effect of <i>E. coli</i> O86:B7 was not associated with an increase in circulating anti-α-Gal IgY levels, but with a striking reduction of anti-α-Gal IgA in the lungs of infected turkeys. Subcutaneous immunization against α-Gal did not induce a significant reduction of lung anti-α-Gal IgA and failed to protect against an infectious challenge with <i>A. fumigatus</i>. Oral administration of <i>E. coli</i> O86:B7 was not associated with the upregulation of lung cytokines upon <i>A. fumigatus</i> infection. We concluded that the oral administration of bacteria expressing high levels of α-Gal decreases the levels of lung anti-α-Gal IgA, which are mediators of inflammation and lung damage during acute aspergillosis.
first_indexed 2024-03-10T19:20:18Z
format Article
id doaj.art-d881a47c0c8744258dafc3e24f7452b4
institution Directory Open Access Journal
issn 2076-393X
language English
last_indexed 2024-03-10T19:20:18Z
publishDate 2020-06-01
publisher MDPI AG
record_format Article
series Vaccines
spelling doaj.art-d881a47c0c8744258dafc3e24f7452b42023-11-20T03:06:05ZengMDPI AGVaccines2076-393X2020-06-018228510.3390/vaccines8020285Gut Microbiota Abrogates Anti-α-Gal IgA Response in Lungs and Protects against Experimental <i>Aspergillus</i> Infection in PoultryLourdes Mateos-Hernández0Veronica Risco-Castillo1Edgar Torres-Maravilla2Luis G. Bermúdez-Humarán3Pilar Alberdi4Adnan Hodžić5Angelica Hernández-Jarguin6Sabine Rakotobe7Clemence Galon8Elodie Devillers9Jose de la Fuente10Jacques Guillot11Alejandro Cabezas-Cruz12UMR BIPAR, INRAE, ANSES, Ecole Nationale Vétérinaire d’Alfort, Université Paris-Est, 14 rue Pierre et Marie Curie, 94706 Maisons-Alfort, FranceEA 7380 Dynamyc, UPEC, USC, ANSES, Ecole Nationale Vétérinaire d’Alfort, Université Paris-Est, 94700 Maisons-Alfort, FranceMicalis Institute, AgroParisTech, INRAE, Université Paris-Saclay, 78350 Jouy-en-Josas, FranceMicalis Institute, AgroParisTech, INRAE, Université Paris-Saclay, 78350 Jouy-en-Josas, FranceSaBio, Instituto de Investigación en Recursos Cinegéticos (IREC-CSIC-UCLM-JCCM), Ronda de Toledo s/n, 13005 Ciudad Real, SpainInstitute of Parasitology, Department of Pathobiology, University of Veterinary Medicine Vienna, 1210 Vienna, AustriaSaBio, Instituto de Investigación en Recursos Cinegéticos (IREC-CSIC-UCLM-JCCM), Ronda de Toledo s/n, 13005 Ciudad Real, SpainUMR BIPAR, INRAE, ANSES, Ecole Nationale Vétérinaire d’Alfort, Université Paris-Est, 14 rue Pierre et Marie Curie, 94706 Maisons-Alfort, FranceUMR BIPAR, INRAE, ANSES, Ecole Nationale Vétérinaire d’Alfort, Université Paris-Est, 14 rue Pierre et Marie Curie, 94706 Maisons-Alfort, FranceUMR BIPAR, INRAE, ANSES, Ecole Nationale Vétérinaire d’Alfort, Université Paris-Est, 14 rue Pierre et Marie Curie, 94706 Maisons-Alfort, FranceSaBio, Instituto de Investigación en Recursos Cinegéticos (IREC-CSIC-UCLM-JCCM), Ronda de Toledo s/n, 13005 Ciudad Real, SpainEA 7380 Dynamyc, UPEC, USC, ANSES, Ecole Nationale Vétérinaire d’Alfort, Université Paris-Est, 94700 Maisons-Alfort, FranceUMR BIPAR, INRAE, ANSES, Ecole Nationale Vétérinaire d’Alfort, Université Paris-Est, 14 rue Pierre et Marie Curie, 94706 Maisons-Alfort, FranceNaturally occurring human antibodies (Abs) of the isotypes IgM and IgG and reactive to the galactose-α-1,3-galactose (α-Gal) epitope are associated with protection against infectious diseases, caused by pathogens expressing the glycan. Gut microbiota bacteria expressing α-Gal regulate the immune response to this glycan in animals lacking endogenous α-Gal. Here, we asked whether the production of anti-α-Gal Abs in response to microbiota stimulation in birds, confers protection against infection by <i>Aspergillus fumigatus</i>, a major fungal pathogen that expresses α-Gal in its surface. We demonstrated that the oral administration of <i>Escherichia coli</i> O86:B7 strain, a bacterium with high α-Gal content, reduces the occurrence of granulomas in lungs and protects turkeys from developing acute aspergillosis. Surprisingly, the protective effect of <i>E. coli</i> O86:B7 was not associated with an increase in circulating anti-α-Gal IgY levels, but with a striking reduction of anti-α-Gal IgA in the lungs of infected turkeys. Subcutaneous immunization against α-Gal did not induce a significant reduction of lung anti-α-Gal IgA and failed to protect against an infectious challenge with <i>A. fumigatus</i>. Oral administration of <i>E. coli</i> O86:B7 was not associated with the upregulation of lung cytokines upon <i>A. fumigatus</i> infection. We concluded that the oral administration of bacteria expressing high levels of α-Gal decreases the levels of lung anti-α-Gal IgA, which are mediators of inflammation and lung damage during acute aspergillosis.https://www.mdpi.com/2076-393X/8/2/285alpha-Galmicrobiotaaspergillosis<i>Aspergillus fumigatus</i>granulomascross-protective immunity
spellingShingle Lourdes Mateos-Hernández
Veronica Risco-Castillo
Edgar Torres-Maravilla
Luis G. Bermúdez-Humarán
Pilar Alberdi
Adnan Hodžić
Angelica Hernández-Jarguin
Sabine Rakotobe
Clemence Galon
Elodie Devillers
Jose de la Fuente
Jacques Guillot
Alejandro Cabezas-Cruz
Gut Microbiota Abrogates Anti-α-Gal IgA Response in Lungs and Protects against Experimental <i>Aspergillus</i> Infection in Poultry
Vaccines
alpha-Gal
microbiota
aspergillosis
<i>Aspergillus fumigatus</i>
granulomas
cross-protective immunity
title Gut Microbiota Abrogates Anti-α-Gal IgA Response in Lungs and Protects against Experimental <i>Aspergillus</i> Infection in Poultry
title_full Gut Microbiota Abrogates Anti-α-Gal IgA Response in Lungs and Protects against Experimental <i>Aspergillus</i> Infection in Poultry
title_fullStr Gut Microbiota Abrogates Anti-α-Gal IgA Response in Lungs and Protects against Experimental <i>Aspergillus</i> Infection in Poultry
title_full_unstemmed Gut Microbiota Abrogates Anti-α-Gal IgA Response in Lungs and Protects against Experimental <i>Aspergillus</i> Infection in Poultry
title_short Gut Microbiota Abrogates Anti-α-Gal IgA Response in Lungs and Protects against Experimental <i>Aspergillus</i> Infection in Poultry
title_sort gut microbiota abrogates anti α gal iga response in lungs and protects against experimental i aspergillus i infection in poultry
topic alpha-Gal
microbiota
aspergillosis
<i>Aspergillus fumigatus</i>
granulomas
cross-protective immunity
url https://www.mdpi.com/2076-393X/8/2/285
work_keys_str_mv AT lourdesmateoshernandez gutmicrobiotaabrogatesantiagaligaresponseinlungsandprotectsagainstexperimentaliaspergillusiinfectioninpoultry
AT veronicariscocastillo gutmicrobiotaabrogatesantiagaligaresponseinlungsandprotectsagainstexperimentaliaspergillusiinfectioninpoultry
AT edgartorresmaravilla gutmicrobiotaabrogatesantiagaligaresponseinlungsandprotectsagainstexperimentaliaspergillusiinfectioninpoultry
AT luisgbermudezhumaran gutmicrobiotaabrogatesantiagaligaresponseinlungsandprotectsagainstexperimentaliaspergillusiinfectioninpoultry
AT pilaralberdi gutmicrobiotaabrogatesantiagaligaresponseinlungsandprotectsagainstexperimentaliaspergillusiinfectioninpoultry
AT adnanhodzic gutmicrobiotaabrogatesantiagaligaresponseinlungsandprotectsagainstexperimentaliaspergillusiinfectioninpoultry
AT angelicahernandezjarguin gutmicrobiotaabrogatesantiagaligaresponseinlungsandprotectsagainstexperimentaliaspergillusiinfectioninpoultry
AT sabinerakotobe gutmicrobiotaabrogatesantiagaligaresponseinlungsandprotectsagainstexperimentaliaspergillusiinfectioninpoultry
AT clemencegalon gutmicrobiotaabrogatesantiagaligaresponseinlungsandprotectsagainstexperimentaliaspergillusiinfectioninpoultry
AT elodiedevillers gutmicrobiotaabrogatesantiagaligaresponseinlungsandprotectsagainstexperimentaliaspergillusiinfectioninpoultry
AT josedelafuente gutmicrobiotaabrogatesantiagaligaresponseinlungsandprotectsagainstexperimentaliaspergillusiinfectioninpoultry
AT jacquesguillot gutmicrobiotaabrogatesantiagaligaresponseinlungsandprotectsagainstexperimentaliaspergillusiinfectioninpoultry
AT alejandrocabezascruz gutmicrobiotaabrogatesantiagaligaresponseinlungsandprotectsagainstexperimentaliaspergillusiinfectioninpoultry