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;
576-587
Gilles, Stefanie
8f2d5d60-95af-4522-a207-77860cc6b7e3
Blume, Cornelia
aa391c64-8718-4238-906b-d6bb1551a07b
Wimmer, Maria
91663e6f-41f1-4039-a4e3-438d23b5a67a
Damialis, Athanasios
62395d27-bf7c-4869-a7d3-c50c94a9d491
Meulenbroek, Laura
c30f7e58-9746-44bc-822c-41952dd000ff
Gokkaya, Mehmet
ecee8734-d80c-4a4b-8f5d-32b7a07aa3ca
Bergougnan, Carolin
7c765bcc-bb99-4991-8654-97d8ad42e0ec
Eisenbart, Selina
6ccb29b9-52ae-4d7d-a0f4-d24701ffbd3d
Sundell, Nicklas
b2c4b773-6906-46e6-9bb7-f52d4980628a
Lindh, Magnus
10e9002a-26e9-462e-bfed-bbdd6a8a8b55
Andersson, Lars-Magnus
a5ca1d8b-0a94-4c92-a91e-8e6a6dabf764
Dahl, Asloeg
ee83ef4c-418c-4fb7-aef2-9757892dbea6
Chaker, Adam
a36ba134-414e-447d-a0e1-2118c8eb5de7
Kolek, Franziska
6b3d68ac-622b-47a7-9af9-9a6b08ed06a7
Wagner, Sabrina
41d06f1e-766b-495f-8527-744e7f96813b
Neumann, Avidan U.
fbb3e72e-ec93-40b6-8fe2-5e1f9abd08df
Akdis, Cezmi A.
4d8f22fa-175c-4594-a3fa-567f1dcddae3
Garssen, Johan
c1e986a4-4121-4c90-be99-aa76672ed653
Westin, Johan
093556f1-222c-46a2-a10e-68aeae7c4911
van't Land, Belinda
8a169676-dd19-4d69-a201-f16e02ba202f
Davies, Donna E.
7de8fdc7-3640-4e3a-aa91-d0e03f990c38
Traidl-Hoffmann, Claudia
f9c2786e-e855-4928-aefc-2cbc8d672628
1 March 2020
Gilles, Stefanie
8f2d5d60-95af-4522-a207-77860cc6b7e3
Blume, Cornelia
aa391c64-8718-4238-906b-d6bb1551a07b
Wimmer, Maria
91663e6f-41f1-4039-a4e3-438d23b5a67a
Damialis, Athanasios
62395d27-bf7c-4869-a7d3-c50c94a9d491
Meulenbroek, Laura
c30f7e58-9746-44bc-822c-41952dd000ff
Gokkaya, Mehmet
ecee8734-d80c-4a4b-8f5d-32b7a07aa3ca
Bergougnan, Carolin
7c765bcc-bb99-4991-8654-97d8ad42e0ec
Eisenbart, Selina
6ccb29b9-52ae-4d7d-a0f4-d24701ffbd3d
Sundell, Nicklas
b2c4b773-6906-46e6-9bb7-f52d4980628a
Lindh, Magnus
10e9002a-26e9-462e-bfed-bbdd6a8a8b55
Andersson, Lars-Magnus
a5ca1d8b-0a94-4c92-a91e-8e6a6dabf764
Dahl, Asloeg
ee83ef4c-418c-4fb7-aef2-9757892dbea6
Chaker, Adam
a36ba134-414e-447d-a0e1-2118c8eb5de7
Kolek, Franziska
6b3d68ac-622b-47a7-9af9-9a6b08ed06a7
Wagner, Sabrina
41d06f1e-766b-495f-8527-744e7f96813b
Neumann, Avidan U.
fbb3e72e-ec93-40b6-8fe2-5e1f9abd08df
Akdis, Cezmi A.
4d8f22fa-175c-4594-a3fa-567f1dcddae3
Garssen, Johan
c1e986a4-4121-4c90-be99-aa76672ed653
Westin, Johan
093556f1-222c-46a2-a10e-68aeae7c4911
van't Land, Belinda
8a169676-dd19-4d69-a201-f16e02ba202f
Davies, Donna E.
7de8fdc7-3640-4e3a-aa91-d0e03f990c38
Traidl-Hoffmann, Claudia
f9c2786e-e855-4928-aefc-2cbc8d672628
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), .
(doi:10.1111/all.14047).
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.
Text
manuscript
- Accepted Manuscript
Text
supplements
- Accepted Manuscript
More information
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
Catalogue record
Date deposited: 31 Jul 2019 16:30
Last modified: 17 Mar 2024 02:33
Export record
Altmetrics
Contributors
Author:
Stefanie Gilles
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:
Claudia Traidl-Hoffmann
Download statistics
Downloads from ePrints over the past year. Other digital versions may also be available to download e.g. from the publisher's website.
View more statistics