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Helicobacter pylori-mediated protection from allergy is associated with IL-10-secreting peripheral blood regulatory T cells

Hussain, Khiyam; Letley, Darren P.; Greenaway, A. Borgel; Kenefeck, Rupert; Winter, Jody A.; Tomlinson, William; Rhead, Joanne; Staples, Emily; Kaneko, Kazuyo; Atherton, John C.; Robinson, Karen

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Authors

Khiyam Hussain

Darren P. Letley

A. Borgel Greenaway

Rupert Kenefeck

Jody A. Winter

William Tomlinson

Joanne Rhead

Emily Staples

Kazuyo Kaneko

John C. Atherton

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KAREN ROBINSON karen.robinson@nottingham.ac.uk
Professor in Gastrointestinal Infection and Immunity



Abstract

© 2016 Hussain, Letley, Greenaway, Kenefeck, Winter, Tomlinson, Rhead, Staples, Kaneko, Atherton and Robinson. Helicobacter pylori infections are usually established in early childhood and continuously stimulate immunity, including T-helper 1 (Th1), Th17, and regulatory T-cell (Treg) responses, throughout life. Although known to be the major cause of peptic ulcer disease and gastric cancer, disease occurs in a minority of those who are infected. Recently, there has been much interest in beneficial effects arising from infection with this pathogen. Published data robustly show that the infection is protective against asthma in mouse models. Epidemiological studies show that H. pylori is inversely associated with human allergy and asthma, but there is a paucity of mechanistic data to explain this. Since Th1 and Treg responses are reported to protect against allergic responses, we investigated if there were links between the human systemic Th1 and Treg response to H. pylori and allergen-specific IgE levels. The human cytokine and T-cell responses were examined using peripheral blood mononuclear cells (PBMCs) from 49 infected and 58 uninfected adult patients. Concentrations of total and allergen-specific plasma IgE were determined by ELISA and ImmunoCAP assays. These responses were analyzed according to major virulence factor genotypes of the patients' colonizing H. pylori strains. An in vitro assay was employed, using PBMCs from infected and uninfected donors, to determine the role of Treg cytokines in the suppression of IgE. Significantly higher frequencies of IL-10-secreting CD4+CD25hi Tregs, but not H. pylori-specific Th1 cells, were present in the peripheral blood of infected patients. Total and allergen-specific IgE concentrations were lower when there was a strong Treg response, and blocking IL-10 in vitro dramatically restored IgE responses. IgE concentrations were also significantly lower when patients were infected with CagA+ strains or those expressing the more active i1 form of VacA. The systemic IL-10+ Treg response is therefore likely to play a role in H. pylori-mediated protection against allergy in humans.

Citation

Hussain, K., Letley, D. P., Greenaway, A. B., Kenefeck, R., Winter, J. A., Tomlinson, W., …Robinson, K. (2016). Helicobacter pylori-mediated protection from allergy is associated with IL-10-secreting peripheral blood regulatory T cells. Frontiers in Immunology, 7, Article 71. https://doi.org/10.3389/fimmu.2016.00071

Journal Article Type Article
Acceptance Date Feb 15, 2016
Online Publication Date Mar 7, 2016
Publication Date Mar 7, 2016
Deposit Date Oct 15, 2018
Publicly Available Date Oct 15, 2018
Journal Frontiers in Immunology
Electronic ISSN 1664-3224
Publisher Frontiers Media
Peer Reviewed Peer Reviewed
Volume 7
Article Number 71
DOI https://doi.org/10.3389/fimmu.2016.00071
Keywords Helicobacter pylori, allergy, regulatory T cells, interleukin-10, IgE
Public URL https://nottingham-repository.worktribe.com/output/1164882
Publisher URL https://www.frontiersin.org/articles/10.3389/fimmu.2016.00071/full

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