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Pollen exposure weakens innate defense against respiratory viruses

Pollen exposure weakens innate defense against respiratory viruses
Pollen exposure weakens innate defense against respiratory viruses

Background: Hundreds of plant species release their pollen into the air every year during early spring. During that period, pollen allergic as well as non-allergic patients frequently present to doctors with severe respiratory tract infections. Our objective was therefore to assess whether pollen may interfere with antiviral immunity. Methods: We combined data from real-life human exposure cohorts, a mouse model and human cell culture to test our hypothesis. Results: Pollen significantly diminished interferon-λ and pro-inflammatory chemokine responses of airway epithelia to rhinovirus and viral mimics and decreased nuclear translocation of interferon regulatory factors. In mice infected with respiratory syncytial virus, co-exposure to pollen caused attenuated antiviral gene expression and increased pulmonary viral titers. In non-allergic human volunteers, nasal symptoms were positively correlated with airborne birch pollen abundance, and nasal birch pollen challenge led to downregulation of type I and -III interferons in nasal mucosa. In a large patient cohort, numbers of rhinoviruspositive cases were correlated with airborne birch pollen concentrations. Conclusion: The ability of pollen to suppress innate antiviral immunity, independent of allergy, suggests that high-risk population groups should avoid extensive outdoor activities when pollen and respiratory virus seasons coincide.

Pollen, antiviral response, lambda interferones, nasal symptoms, non-allergenic pollen compounds, respiratory syncytial virus, rhinovirus;
0105-4538
576-587
Gilles, Stefanie
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Blume, Cornelia
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Wimmer, Maria
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Damialis, Athanasios
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Meulenbroek, Laura
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Gokkaya, Mehmet
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Bergougnan, Carolin
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Eisenbart, Selina
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Sundell, Nicklas
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Lindh, Magnus
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Andersson, Lars-Magnus
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Dahl, Asloeg
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Chaker, Adam
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Kolek, Franziska
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Wagner, Sabrina
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Neumann, Avidan U.
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Akdis, Cezmi A.
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Garssen, Johan
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Westin, Johan
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van't Land, Belinda
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Davies, Donna E.
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Traidl-Hoffmann, Claudia
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Gilles, Stefanie
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Blume, Cornelia
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Wimmer, Maria
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Damialis, Athanasios
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Meulenbroek, Laura
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Gokkaya, Mehmet
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Bergougnan, Carolin
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Eisenbart, Selina
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Sundell, Nicklas
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Lindh, Magnus
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Andersson, Lars-Magnus
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Dahl, Asloeg
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Chaker, Adam
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Kolek, Franziska
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Wagner, Sabrina
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Neumann, Avidan U.
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Akdis, Cezmi A.
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Garssen, Johan
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Westin, Johan
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van't Land, Belinda
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Davies, Donna E.
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Traidl-Hoffmann, Claudia
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Gilles, Stefanie, Blume, Cornelia, Wimmer, Maria, Damialis, Athanasios, Meulenbroek, Laura, Gokkaya, Mehmet, Bergougnan, Carolin, Eisenbart, Selina, Sundell, Nicklas, Lindh, Magnus, Andersson, Lars-Magnus, Dahl, Asloeg, Chaker, Adam, Kolek, Franziska, Wagner, Sabrina, Neumann, Avidan U., Akdis, Cezmi A., Garssen, Johan, Westin, Johan, van't Land, Belinda, Davies, Donna E. and Traidl-Hoffmann, Claudia (2020) Pollen exposure weakens innate defense against respiratory viruses. Allergy, 75 (3), 576-587. (doi:10.1111/all.14047).

Record type: Article

Abstract

Background: Hundreds of plant species release their pollen into the air every year during early spring. During that period, pollen allergic as well as non-allergic patients frequently present to doctors with severe respiratory tract infections. Our objective was therefore to assess whether pollen may interfere with antiviral immunity. Methods: We combined data from real-life human exposure cohorts, a mouse model and human cell culture to test our hypothesis. Results: Pollen significantly diminished interferon-λ and pro-inflammatory chemokine responses of airway epithelia to rhinovirus and viral mimics and decreased nuclear translocation of interferon regulatory factors. In mice infected with respiratory syncytial virus, co-exposure to pollen caused attenuated antiviral gene expression and increased pulmonary viral titers. In non-allergic human volunteers, nasal symptoms were positively correlated with airborne birch pollen abundance, and nasal birch pollen challenge led to downregulation of type I and -III interferons in nasal mucosa. In a large patient cohort, numbers of rhinoviruspositive cases were correlated with airborne birch pollen concentrations. Conclusion: The ability of pollen to suppress innate antiviral immunity, independent of allergy, suggests that high-risk population groups should avoid extensive outdoor activities when pollen and respiratory virus seasons coincide.

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Accepted/In Press date: 24 June 2019
e-pub ahead of print date: 11 September 2019
Published date: 1 March 2020
Additional Information: Funding Information: This research was partly implemented in the framework of the EUCOST Action DiMoPEx (Diagnosis, Monitoring and Prevention of Exposure‐Related Noncommunicable Diseases), under Grant Number CA15129 (EU Framework Program Horizon 2020). The chair of environmental medicine and SIAF received funding by the Christine‐Kühne‐Center for Allergy Research and Education (CK‐Care). MW received a travel scholarship from the Bayerische Forschungsstiftung (BFS) for her work on the RSV mouse model at Utrecht University. Work including HRV (CB and DED) was funded by the Medical Research Council (UK; G0900453) Helmholtz Association, Germany: Impuls‐ und Vernetzungsfonds (IVF). 1 1 Funding Information: Dr Akdis reports grants from Allergopharma, grants from Idorsia, grants from Swiss National Science Foundation, grants from Christine Kühne‐Center for Allergy Research and Education, grants from European Commission's Horison's 2020 Framework Programme, Cure, other from Sanofi‐Aventis_Regeneron, grants from Novartis Research Institutes, grants from Astra Zeneca, grants from Scibase, outside the submitted work. Dr Chaker reports research grants and other from Allergopharma, ALK Abello, ASIT Biotech, Bencard/Allergen Therapeutics, GSK, HAL Allergy, LETI, LOFARMA, Novartis, Phadia/ Thermo Fisher, Zeller, Circassia; further EIT (European Institute of Technology) and DZL: Deutsches Zentrum Lungenforschung (BMBF, governmental), outside the submitted work. Dr Davies reports personal fees from Synairgen, outside the submitted work; In addition, Dr Davies has a patent with royalties paid. Dr Garssen reports and Two (2) affiliations: (1) Danone/Nutricia Research. Function: Director Research & Innovation Immunology and (2) Utrecht University/Utrecht Institute for Pharmaceutical Sciences. Function: Head Division Pharmacology. The remaining authors declare that they have no conflicts of interest. Publisher Copyright: © 2020 EAACI and John Wiley and Sons A/S. Published by John Wiley and Sons Ltd.
Keywords: Pollen, antiviral response, lambda interferones, nasal symptoms, non-allergenic pollen compounds, respiratory syncytial virus, rhinovirus;

Identifiers

Local EPrints ID: 432889
URI: http://eprints.soton.ac.uk/id/eprint/432889
ISSN: 0105-4538
PURE UUID: 3308efe2-be06-474e-aa87-68ac72306fe8
ORCID for Cornelia Blume: ORCID iD orcid.org/0000-0001-6133-7318
ORCID for Donna E. Davies: ORCID iD orcid.org/0000-0002-5117-2991

Catalogue record

Date deposited: 31 Jul 2019 16:30
Last modified: 28 Jul 2022 04:02

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Contributors

Author: Stefanie Gilles
Author: Cornelia Blume ORCID iD
Author: Maria Wimmer
Author: Athanasios Damialis
Author: Laura Meulenbroek
Author: Mehmet Gokkaya
Author: Carolin Bergougnan
Author: Selina Eisenbart
Author: Nicklas Sundell
Author: Magnus Lindh
Author: Lars-Magnus Andersson
Author: Asloeg Dahl
Author: Adam Chaker
Author: Franziska Kolek
Author: Sabrina Wagner
Author: Avidan U. Neumann
Author: Cezmi A. Akdis
Author: Johan Garssen
Author: Johan Westin
Author: Belinda van't Land
Author: Donna E. Davies ORCID iD
Author: Claudia Traidl-Hoffmann

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