Airway administration of OM-85, a bacterial lysate, blocks experimental asthma by targeting dendritic cells and the epithelium/IL-33/ILC2 axis.

Bacterial lysate OM-85 adaptive immunity airway compartment allergic inflammation asthma innate immunity intranasal route microbial interventions

Journal

The Journal of allergy and clinical immunology
ISSN: 1097-6825
Titre abrégé: J Allergy Clin Immunol
Pays: United States
ID NLM: 1275002

Informations de publication

Date de publication:
03 2022
Historique:
received: 19 02 2021
revised: 26 08 2021
accepted: 02 09 2021
pubmed: 25 9 2021
medline: 26 4 2022
entrez: 24 9 2021
Statut: ppublish

Résumé

Microbial interventions against allergic asthma have robust epidemiologic underpinnings and the potential to recalibrate disease-inducing immune responses. Oral administration of OM-85, a standardized lysate of human airways bacteria, is widely used empirically to prevent respiratory infections and a clinical trial is testing its ability to prevent asthma in high-risk children. We previously showed that intranasal administration of microbial products from farm environments abrogates experimental allergic asthma. We sought to investigate whether direct administration of OM-85 to the airway compartment protects against experimental allergic asthma; and to identify protective cellular and molecular mechanisms activated through this natural route. Different strains of mice sensitized and challenged with ovalbumin or Alternaria received OM-85 intranasally, and cardinal cellular and molecular asthma phenotypes were measured. Airway transfer experiments assessed whether OM-85-treated dendritic cells protect allergen-sensitized, OM-85-naive mice against asthma. Airway OM-85 administration suppressed allergic asthma in all models acting on multiple innate and adaptive immune targets: the airway epithelium/IL-33/ILC2 axis, lung allergen-induced type 2 responses, and dendritic cells whose Myd88/Trif-dependent tolerogenic reprogramming was sufficient to transfer OM-85-induced asthma protection. We provide the first demonstration that administering a standardized bacterial lysate to the airway compartment protects from experimental allergic asthma by engaging multiple immune pathways. Because protection required a cumulative dose 27- to 46-fold lower than the one reportedly active through the oral route, the efficacy of intranasal OM-85 administration may reflect its direct access to the airway mucosal networks controlling the initiation and development of allergic asthma.

Sections du résumé

BACKGROUND
Microbial interventions against allergic asthma have robust epidemiologic underpinnings and the potential to recalibrate disease-inducing immune responses. Oral administration of OM-85, a standardized lysate of human airways bacteria, is widely used empirically to prevent respiratory infections and a clinical trial is testing its ability to prevent asthma in high-risk children. We previously showed that intranasal administration of microbial products from farm environments abrogates experimental allergic asthma.
OBJECTIVES
We sought to investigate whether direct administration of OM-85 to the airway compartment protects against experimental allergic asthma; and to identify protective cellular and molecular mechanisms activated through this natural route.
METHODS
Different strains of mice sensitized and challenged with ovalbumin or Alternaria received OM-85 intranasally, and cardinal cellular and molecular asthma phenotypes were measured. Airway transfer experiments assessed whether OM-85-treated dendritic cells protect allergen-sensitized, OM-85-naive mice against asthma.
RESULTS
Airway OM-85 administration suppressed allergic asthma in all models acting on multiple innate and adaptive immune targets: the airway epithelium/IL-33/ILC2 axis, lung allergen-induced type 2 responses, and dendritic cells whose Myd88/Trif-dependent tolerogenic reprogramming was sufficient to transfer OM-85-induced asthma protection.
CONCLUSIONS
We provide the first demonstration that administering a standardized bacterial lysate to the airway compartment protects from experimental allergic asthma by engaging multiple immune pathways. Because protection required a cumulative dose 27- to 46-fold lower than the one reportedly active through the oral route, the efficacy of intranasal OM-85 administration may reflect its direct access to the airway mucosal networks controlling the initiation and development of allergic asthma.

Identifiants

pubmed: 34560105
pii: S0091-6749(21)01403-2
doi: 10.1016/j.jaci.2021.09.013
pmc: PMC8901455
mid: NIHMS1743541
pii:
doi:

Substances chimiques

Allergens 0
Broncho-Vaxom 0
Cell Extracts 0
Interleukin-33 0
Ovalbumin 9006-59-1

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

943-956

Subventions

Organisme : NIAID NIH HHS
ID : P01 AI148104
Pays : United States
Organisme : NIAID NIH HHS
ID : R21 AI144722
Pays : United States
Organisme : NIEHS NIH HHS
ID : T32 ES007091
Pays : United States
Organisme : NHLBI NIH HHS
ID : T32 HL007249
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2021 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved.

Références

Nat Rev Immunol. 2021 Nov;21(11):739-751
pubmed: 33846604
J Allergy Clin Immunol. 2015 Jul;136(1):59-68.e14
pubmed: 25617223
Immunol Allergy Clin North Am. 2019 May;39(2):141-150
pubmed: 30954166
Int Immunol. 2016 Jan;28(1):23-8
pubmed: 26232596
J Clin Invest. 2018 Nov 1;128(11):4856-4869
pubmed: 30153109
N Engl J Med. 2002 Sep 19;347(12):869-77
pubmed: 12239255
Nat Med. 2016 Oct;22(10):1187-1191
pubmed: 27618652
Sci Transl Med. 2015 Sep 30;7(307):307ra152
pubmed: 26424567
Curr Opin Immunol. 2014 Dec;31:31-7
pubmed: 25278425
Nat Med. 2019 Mar;25(3):448-453
pubmed: 30643289
J Allergy Clin Immunol. 2020 Aug;146(2):270-272
pubmed: 32333916
Front Immunol. 2021 Feb 18;12:618807
pubmed: 33679760
Nat Med. 2014 Feb;20(2):159-66
pubmed: 24390308
Science. 1998 Dec 18;282(5397):2258-61
pubmed: 9856949
Nat Microbiol. 2019 Nov;4(11):1851-1861
pubmed: 31332384
Int Immunopharmacol. 2018 Jan;54:198-209
pubmed: 29154122
Lancet. 2001 Oct 6;358(9288):1129-33
pubmed: 11597666
J Allergy Clin Immunol. 2014 Sep;134(3):509-20
pubmed: 25085341
J Allergy Clin Immunol. 2019 Sep;144(3):870-872.e11
pubmed: 31185221
Mucosal Immunol. 2011 Jan;4(1):43-52
pubmed: 20668438
Am J Respir Crit Care Med. 1997 Apr;155(4):1356-61
pubmed: 9105079
Lancet. 2020 Sep 19;396(10254):854-866
pubmed: 32910907
J Immunol. 2009 Feb 15;182(4):2502-10
pubmed: 19201906
J Immunol. 2013 Jul 1;191(1):25-9
pubmed: 23733880
J Allergy Clin Immunol. 2005 Sep;116(3):623-9
pubmed: 16159634
Mucosal Immunol. 2013 May;6(3):464-73
pubmed: 23549447
N Engl J Med. 2016 Aug 4;375(5):411-421
pubmed: 27518660
J Allergy Clin Immunol. 2019 Nov;144(5):1391-1401.e10
pubmed: 31401285
Nat Med. 2020 Nov;26(11):1766-1775
pubmed: 33139948
Nat Rev Gastroenterol Hepatol. 2019 Nov;16(11):656-661
pubmed: 31562390
Immunity. 2013 Feb 21;38(2):322-35
pubmed: 23352232
Nat Commun. 2018 Jan 10;9(1):141
pubmed: 29321519
Am J Respir Crit Care Med. 2021 Apr 1;203(7):802-808
pubmed: 33493428
Lancet. 2013 Oct 19;382(9901):1360-72
pubmed: 24041942
Front Immunol. 2020 Dec 02;11:601494
pubmed: 33424847
Chest. 2002 Dec;122(6):2042-9
pubmed: 12475845
N Engl J Med. 2016 Nov 10;375(19):1898-1899
pubmed: 27959651
Mucosal Immunol. 2011 Jan;4(1):53-65
pubmed: 20811345
J Allergy Clin Immunol. 2014 Sep;134(3):583-592.e6
pubmed: 24636086
J Allergy Clin Immunol. 2010 Oct;126(4):763-9
pubmed: 20920766
Am J Physiol Lung Cell Mol Physiol. 2012 Oct 1;303(7):L577-88
pubmed: 22865552
Clin Exp Allergy. 2020 Mar;50(3):282-290
pubmed: 31581343
Mucosal Immunol. 2019 Mar;12(2):299-311
pubmed: 30664706
BMC Bioinformatics. 2008 Dec 29;9:559
pubmed: 19114008
J Immunol. 2016 Dec 15;197(12):4541-4551
pubmed: 27815425
Curr Opin Allergy Clin Immunol. 2018 Jun;18(3):198-209
pubmed: 29561355
Eur J Immunol. 2013 Apr;43(4):907-17
pubmed: 23319328
J Clin Invest. 2013 Feb;123(2):844-54
pubmed: 23298832

Auteurs

Vadim Pivniouk (V)

Department of Cellular and Molecular Medicine, The University of Arizona, Tucson, Ariz; Asthma and Airway Disease Research Center, The University of Arizona, Tucson, Ariz; BIO5 Institute, The University of Arizona, Tucson, Ariz. Electronic address: vadimp@arizona.edu.

Joao A Gimenes-Junior (JA)

Asthma and Airway Disease Research Center, The University of Arizona, Tucson, Ariz.

Peace Ezeh (P)

Asthma and Airway Disease Research Center, The University of Arizona, Tucson, Ariz.

Ashley Michael (A)

Asthma and Airway Disease Research Center, The University of Arizona, Tucson, Ariz.

Oksana Pivniouk (O)

Asthma and Airway Disease Research Center, The University of Arizona, Tucson, Ariz.

Seongmin Hahn (S)

Asthma and Airway Disease Research Center, The University of Arizona, Tucson, Ariz.

Sydney R VanLinden (SR)

Asthma and Airway Disease Research Center, The University of Arizona, Tucson, Ariz.

Sean P Malone (SP)

Asthma and Airway Disease Research Center, The University of Arizona, Tucson, Ariz.

Amir Abidov (A)

Medical Student Research Program, College of Medicine, The University of Arizona, Tucson, Ariz.

Dayna Anderson (D)

Asthma and Airway Disease Research Center, The University of Arizona, Tucson, Ariz.

Justyna Gozdz (J)

Asthma and Airway Disease Research Center, The University of Arizona, Tucson, Ariz.

Avery DeVries (A)

Asthma and Airway Disease Research Center, The University of Arizona, Tucson, Ariz; BIO5 Institute, The University of Arizona, Tucson, Ariz.

Fernando D Martinez (FD)

Asthma and Airway Disease Research Center, The University of Arizona, Tucson, Ariz; BIO5 Institute, The University of Arizona, Tucson, Ariz.

Christian Pasquali (C)

OM Pharma SA, Geneva, Switzerland.

Donata Vercelli (D)

Department of Cellular and Molecular Medicine, The University of Arizona, Tucson, Ariz; Asthma and Airway Disease Research Center, The University of Arizona, Tucson, Ariz; BIO5 Institute, The University of Arizona, Tucson, Ariz; Arizona Center for the Biology of Complex Diseases, The University of Arizona, Tucson, Ariz.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH