The Hygiene Hypothesis: Immunological Mechanisms of Airway Tolerance

Overview

Journal Curr Opin Immunol

Publisher Elsevier

Specialty Allergy & Immunology

Date 2018 Jul 10

PMID 29986301

Citations 25

Authors

Eline Haspeslagh

Ines Heyndrickx

Hamida Hammad

Bart N Lambrecht

Affiliations

Soon will be listed here.

Abstract

The hygiene hypothesis was initially proposed as an explanation for the alarming rise in allergy prevalence in the last century. The immunological idea behind this hypothesis was a lack of infections associated with a Western lifestyle and a consequential reduction in type 1 immune responses. It is now understood that the development of tolerance to allergens depends on microbial colonization and immunostimulatory environmental signals during early-life or passed on by the mother. These environmental cues are sensed and integrated by barrier epithelial cells of the lungs and possibly skin, which in turn instruct dendritic cells to regulate or impede adaptive T cell responses. Recent reports also implicate immunoregulatory macrophages as powerful suppressors of allergy by the microbiome. We propose that loss of adequate microbial stimulation due to a Western lifestyle may result in hypersensitive barrier tissues and the observed rise in type 2 allergic disease.

Citing Articles

Risk factors of allergic rhinitis and its prevention strategies.

Chen R, An W, Liu X, Yan J, Huang Y, Zhang J Front Allergy. 2024; 5:1509552.

PMID: 39665077 PMC: 11632107. DOI: 10.3389/falgy.2024.1509552.

Unlocking the potential for microbiome-based therapeutics to address the sustainable development goal of good health and wellbeing.

Gulliver E, Di Simone S, Chonwerawong M, Forster S Microb Biotechnol. 2024; 17(11):e70041.

PMID: 39487814 PMC: 11531172. DOI: 10.1111/1751-7915.70041.

Coinhibitory Molecule VISTA Play an Important Negative Regulatory Role in the Immunopathology of Bronchial Asthma.

Yin J, Chen J, Wang T, Sun H, Yan Y, Zhu C J Asthma Allergy. 2024; 17:813-832.

PMID: 39246611 PMC: 11378793. DOI: 10.2147/JAA.S449867.

Tyndallized bacteria prime bronchial epithelial cells to mount an effective innate immune response against infections.

Di Vincenzo S, Di Sano C, DAnna C, Ferraro M, Malizia V, Bruno A Hum Cell. 2024; 37(4):1080-1090.

PMID: 38814518 PMC: 11194193. DOI: 10.1007/s13577-024-01080-z.

Saliva contact during infancy and allergy development in school-age children.

Kubo Y, Kanazawa N, Fukuda H, Inaba Y, Mikita N, Jinnin M J Allergy Clin Immunol Glob. 2023; 2(3):100108.

PMID: 37779525 PMC: 10509937. DOI: 10.1016/j.jacig.2023.100108.

References

Martin R, Makino H, Cetinyurek Yavuz A, Ben-Amor K, Roelofs M, Ishikawa E . Early-Life Events, Including Mode of Delivery and Type of Feeding, Siblings and Gender, Shape the Developing Gut Microbiota. PLoS One. 2016; 11(6):e0158498. PMC: 4928817. DOI: 10.1371/journal.pone.0158498. View

Naik S, Bouladoux N, Linehan J, Han S, Harrison O, Wilhelm C . Commensal-dendritic-cell interaction specifies a unique protective skin immune signature. Nature. 2014; 520(7545):104-8. PMC: 4667810. DOI: 10.1038/nature14052. View

Deckers J, Sichien D, Plantinga M, Van Moorleghem J, Vanheerswynghels M, Hoste E . Epicutaneous sensitization to house dust mite allergen requires interferon regulatory factor 4-dependent dermal dendritic cells. J Allergy Clin Immunol. 2017; 140(5):1364-1377.e2. DOI: 10.1016/j.jaci.2016.12.970. View

Volz T, Skabytska Y, Guenova E, Chen K, Frick J, Kirschning C . Nonpathogenic bacteria alleviating atopic dermatitis inflammation induce IL-10-producing dendritic cells and regulatory Tr1 cells. J Invest Dermatol. 2013; 134(1):96-104. DOI: 10.1038/jid.2013.291. View

Strachan D . Hay fever, hygiene, and household size. BMJ. 1989; 299(6710):1259-60. PMC: 1838109. DOI: 10.1136/bmj.299.6710.1259. View

Saluzzo S, Gorki A, Rana B, Martins R, Scanlon S, Starkl P . First-Breath-Induced Type 2 Pathways Shape the Lung Immune Environment. Cell Rep. 2017; 18(8):1893-1905. PMC: 5329122. DOI: 10.1016/j.celrep.2017.01.071. View

Plantinga M, Guilliams M, Vanheerswynghels M, Deswarte K, Branco-Madeira F, Toussaint W . Conventional and monocyte-derived CD11b(+) dendritic cells initiate and maintain T helper 2 cell-mediated immunity to house dust mite allergen. Immunity. 2013; 38(2):322-35. DOI: 10.1016/j.immuni.2012.10.016. View

De Kleer I, Kool M, de Bruijn M, Willart M, Van Moorleghem J, Schuijs M . Perinatal Activation of the Interleukin-33 Pathway Promotes Type 2 Immunity in the Developing Lung. Immunity. 2016; 45(6):1285-1298. DOI: 10.1016/j.immuni.2016.10.031. View

Choi H, Park S, Cho J, Park J, Sohn J, Kim Y . The TLR4-associated phospholipase D1 activation is crucial for Der f 2-induced IL-13 production. Allergy. 2015; 70(12):1569-79. DOI: 10.1111/all.12764. View

10.

Simpson A, John S, Jury F, Niven R, Woodcock A, Ollier W . Endotoxin exposure, CD14, and allergic disease: an interaction between genes and the environment. Am J Respir Crit Care Med. 2006; 174(4):386-92. DOI: 10.1164/rccm.200509-1380OC. View

11.

Belkaid Y, Harrison O . Homeostatic Immunity and the Microbiota. Immunity. 2017; 46(4):562-576. PMC: 5604871. DOI: 10.1016/j.immuni.2017.04.008. View

12.

Smits H, Hiemstra P, Prazeres da Costa C, Ege M, Edwards M, Garn H . Microbes and asthma: Opportunities for intervention. J Allergy Clin Immunol. 2016; 137(3):690-7. DOI: 10.1016/j.jaci.2016.01.004. View

13.

Savage J, Lee-Sarwar K, Sordillo J, Bunyavanich S, Zhou Y, OConnor G . A prospective microbiome-wide association study of food sensitization and food allergy in early childhood. Allergy. 2017; 73(1):145-152. PMC: 5921051. DOI: 10.1111/all.13232. View

14.

Lewis B, Sultana R, Sharma R, Noel A, Langohr I, Patial S . Early Postnatal Secondhand Smoke Exposure Disrupts Bacterial Clearance and Abolishes Immune Responses in Muco-Obstructive Lung Disease. J Immunol. 2017; 199(3):1170-1183. DOI: 10.4049/jimmunol.1700144. View

15.

Kuipers H, Heirman C, Hijdra D, Muskens F, Willart M, Van Meirvenne S . Dendritic cells retrovirally overexpressing IL-12 induce strong Th1 responses to inhaled antigen in the lung but fail to revert established Th2 sensitization. J Leukoc Biol. 2004; 76(5):1028-38. DOI: 10.1189/jlb.0604325. View

16.

Hammad H, Lambrecht B . Barrier Epithelial Cells and the Control of Type 2 Immunity. Immunity. 2015; 43(1):29-40. DOI: 10.1016/j.immuni.2015.07.007. View

17.

McSorley H, Blair N, Smith K, McKenzie A, Maizels R . Blockade of IL-33 release and suppression of type 2 innate lymphoid cell responses by helminth secreted products in airway allergy. Mucosal Immunol. 2014; 7(5):1068-78. PMC: 4016792. DOI: 10.1038/mi.2013.123. View

18.

Remot A, Descamps D, Noordine M, Boukadiri A, Mathieu E, Robert V . Bacteria isolated from lung modulate asthma susceptibility in mice. ISME J. 2017; 11(5):1061-1074. PMC: 5437918. DOI: 10.1038/ismej.2016.181. View

19.

Clausen M, Agner T, Lilje B, Edslev S, Johannesen T, Andersen P . Association of Disease Severity With Skin Microbiome and Filaggrin Gene Mutations in Adult Atopic Dermatitis. JAMA Dermatol. 2018; 154(3):293-300. PMC: 5885821. DOI: 10.1001/jamadermatol.2017.5440. View

20.

Takai T, Chen X, Xie Y, Vu A, Le T, Kinoshita H . TSLP expression induced via Toll-like receptor pathways in human keratinocytes. Methods Enzymol. 2014; 535:371-87. DOI: 10.1016/B978-0-12-397925-4.00021-3. View