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Open AccessArticle

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

1
UMR BIPAR, INRAE, ANSES, Ecole Nationale Vétérinaire d’Alfort, Université Paris-Est, 14 rue Pierre et Marie Curie, 94706 Maisons-Alfort, France
2
EA 7380 Dynamyc, UPEC, USC, ANSES, Ecole Nationale Vétérinaire d’Alfort, Université Paris-Est, 94700 Maisons-Alfort, France
3
Micalis Institute, AgroParisTech, INRAE, Université Paris-Saclay, 78350 Jouy-en-Josas, France
4
SaBio, Instituto de Investigación en Recursos Cinegéticos (IREC-CSIC-UCLM-JCCM), Ronda de Toledo s/n, 13005 Ciudad Real, Spain
5
Institute of Parasitology, Department of Pathobiology, University of Veterinary Medicine Vienna, 1210 Vienna, Austria
6
Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Tamaulipas, Tamaulipas 87000, Mexico
7
Department of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, OK 74078, USA
*
Author to whom correspondence should be addressed.
These authors contributed equally to this work.
Vaccines 2020, 8(2), 285; https://doi.org/10.3390/vaccines8020285
Received: 4 May 2020 / Revised: 2 June 2020 / Accepted: 4 June 2020 / Published: 7 June 2020
(This article belongs to the Special Issue Development of Cross-Protective Vaccines)
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 Aspergillus fumigatus, a major fungal pathogen that expresses α-Gal in its surface. We demonstrated that the oral administration of Escherichia coli 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 E. coli 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 A. fumigatus. Oral administration of E. coli O86:B7 was not associated with the upregulation of lung cytokines upon A. fumigatus 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. View Full-Text
Keywords: alpha-Gal; microbiota; aspergillosis; Aspergillus fumigatus; granulomas; cross-protective immunity alpha-Gal; microbiota; aspergillosis; Aspergillus fumigatus; granulomas; cross-protective immunity
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    Doi: 10.5281/zenodo.3784889
    Link: http://doi.org/10.5281/zenodo.3784890
    Description: Supplementary Materials: The following are available online at www.mdpi.com/xxx/s1, Supplementary Figure S1. Levels of circulating IgY against Galα1-3Gal (A), circulating IgY against Galα1-3Galβ1-4GlcNAc (B) and circulating IgA against Galα1-3Gal (C) were measured by indirect ELISA in control turkeys treated with PBS, Supplementary Figure S2. The specificity of turkey anti-α-Gal Abs was tested by indirect ELISA in animals treated with PBS, E. coli BL21 and E. coli O86:B7. In comparison with the untreated group, a reduction in reactivity against Galα1-3Gal-HSA was observed after the antigen was pretreated with α-galactosidase. Supplementary Figure S3. Levels of circulating IgY against Galα1-3Gal (A), circulating IgY against Galα1-3Galβ1-4GlcNAc (B) and circulating IgA against Galα1-3Gal (C) were measured in turkey sera by indirect ELISA in animals immunized with α-Gal-BSA (Galα1-3Gal-BSA) or the mock vaccine (PBS). Levels of IgA against Galα1-3Gal (D), and Galα1-3Galβ1-4GlcNAc (E) were measured in turkey lungs. Levels of circulating IgY (F) and circulating IgA (G) against Galα1-3Gal were measured by indirect ELISA in sera of chickens immunized with α-Gal-BSA (Galα1-3Gal-BSA) or the mock vaccine (PBS). Supplementary Video S1. Video of turkey treated with E. coli O86:B7 and challenged with A. fumigatus. E. coli O86:B7 protects the turkeys from developing OMB, gasping and hyperpnea. Supplementary Video S2. Video of control turkey treated with PBS and challenged with A. fumigatus. Turkeys in this group developed OMB, gasping and hyperpnea. Supplementary Video S3. Video of turkey treated with E. coli BL21 and challenged with A. fumigatus. Turkeys in this group developed OMB, gasping and hyperpnea.
MDPI and ACS Style

Mateos-Hernández, L.; Risco-Castillo, V.; Torres-Maravilla, E.; Bermúdez-Humarán, L.G.; Alberdi, P.; Hodžić, A.; Hernández-Jarguin, A.; Rakotobe, S.; Galon, C.; Devillers, E.; de la Fuente, J.; Guillot, J.; Cabezas-Cruz, A. Gut Microbiota Abrogates Anti-α-Gal IgA Response in Lungs and Protects against Experimental Aspergillus Infection in Poultry. Vaccines 2020, 8, 285.

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