Bacillus Calmette–Guérin-Induced Human Mast Cell Activation Relies on IL-33 Priming

Karen M. Garcia-Rodriguez; Anu Goenka; Darren D. Thomson; Rajia Bahri; Chiara Tontini; Barbora Salcman; Rogelio Hernandez-Pando; Silvia Bulfone-Paus

doi:10.3390/ijms23147549

Bacillus Calmette–Guérin-Induced Human Mast Cell Activation Relies on IL-33 Priming

Karen M. Garcia-Rodriguez
, Anu Goenka
, Darren D. Thomson
, Rajia Bahri
, Chiara Tontini
, Barbora Salcman
, Rogelio Hernandez-Pando
, Silvia Bulfone-Paus^*

^*Corresponding author for this work

Research output: Contribution to journal › Article (Academic Journal) › peer-review

12 Citations (Scopus)

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Abstract

Bacillus Calmette-Guérin (BCG) vaccine is an attenuated strain of Mycobacterium bovis that provides weak protection against tuberculosis (TB). Mast cells (MCs) are tissue-resident immune cells strategically that serve as the first line of defence against pathogenic threats. In this study, we investigated the response of human MCs (hMCs) to BCG. We found that naïve hMCs exposed to BCG did not secrete cytokines, degranulate, or support the uptake and intracellular growth of bacteria. Since we could show that in hMCs IL-33 promotes the transcription of host-pathogen interaction, cell adhesion and activation genes, we used IL-33 for cell priming. The treatment of hMCs with IL-33, but not IFN-γ, before BCG stimulation increased IL-8, MCP-1 and IL-13 secretion, and induced an enhanced expression of the mycobacteria-binding receptor CD48. These effects were comparable to those caused by the recombinant Mycobacterium tuberculosis (Mtb) 19-KDa lipoprotein. Finally, stimulation of hMCs with IL-33 incremented MC-BCG interactions. Thus, we propose that IL-33 may improve the immunogenicity of BCG vaccine by sensitising hMCs.

Original language	English
Article number	7549
Journal	International Journal of Molecular Sciences
Volume	23
Issue number	14
DOIs	https://doi.org/10.3390/ijms23147549
Publication status	Published - 7 Jul 2022

Bibliographical note

Funding Information:
Funding: KMGR was funded by the National Council of Science and Technology (CONACyT).

Publisher Copyright:
© 2022 by the authors. Licensee MDPI, Basel, Switzerland.

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

Keywords

mast cells
BCG
IL-33
vaccine booster
M. bovis

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title = "Bacillus Calmette–Gu{\'e}rin-Induced Human Mast Cell Activation Relies on IL-33 Priming",

abstract = "Bacillus Calmette-Gu{\'e}rin (BCG) vaccine is an attenuated strain of Mycobacterium bovis that provides weak protection against tuberculosis (TB). Mast cells (MCs) are tissue-resident immune cells strategically that serve as the first line of defence against pathogenic threats. In this study, we investigated the response of human MCs (hMCs) to BCG. We found that na{\"i}ve hMCs exposed to BCG did not secrete cytokines, degranulate, or support the uptake and intracellular growth of bacteria. Since we could show that in hMCs IL-33 promotes the transcription of host-pathogen interaction, cell adhesion and activation genes, we used IL-33 for cell priming. The treatment of hMCs with IL-33, but not IFN-γ, before BCG stimulation increased IL-8, MCP-1 and IL-13 secretion, and induced an enhanced expression of the mycobacteria-binding receptor CD48. These effects were comparable to those caused by the recombinant Mycobacterium tuberculosis (Mtb) 19-KDa lipoprotein. Finally, stimulation of hMCs with IL-33 incremented MC-BCG interactions. Thus, we propose that IL-33 may improve the immunogenicity of BCG vaccine by sensitising hMCs.",

keywords = "mast cells, BCG, IL-33, vaccine booster, M. bovis",

author = "Garcia-Rodriguez, \{Karen M.\} and Anu Goenka and Thomson, \{Darren D.\} and Rajia Bahri and Chiara Tontini and Barbora Salcman and Rogelio Hernandez-Pando and Silvia Bulfone-Paus",

note = "Funding Information: Funding: KMGR was funded by the National Council of Science and Technology (CONACyT). Publisher Copyright: {\textcopyright} 2022 by the authors. Licensee MDPI, Basel, Switzerland.",

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AU - Garcia-Rodriguez, Karen M.

AU - Goenka, Anu

AU - Thomson, Darren D.

AU - Bahri, Rajia

AU - Tontini, Chiara

AU - Salcman, Barbora

AU - Hernandez-Pando, Rogelio

AU - Bulfone-Paus, Silvia

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N2 - Bacillus Calmette-Guérin (BCG) vaccine is an attenuated strain of Mycobacterium bovis that provides weak protection against tuberculosis (TB). Mast cells (MCs) are tissue-resident immune cells strategically that serve as the first line of defence against pathogenic threats. In this study, we investigated the response of human MCs (hMCs) to BCG. We found that naïve hMCs exposed to BCG did not secrete cytokines, degranulate, or support the uptake and intracellular growth of bacteria. Since we could show that in hMCs IL-33 promotes the transcription of host-pathogen interaction, cell adhesion and activation genes, we used IL-33 for cell priming. The treatment of hMCs with IL-33, but not IFN-γ, before BCG stimulation increased IL-8, MCP-1 and IL-13 secretion, and induced an enhanced expression of the mycobacteria-binding receptor CD48. These effects were comparable to those caused by the recombinant Mycobacterium tuberculosis (Mtb) 19-KDa lipoprotein. Finally, stimulation of hMCs with IL-33 incremented MC-BCG interactions. Thus, we propose that IL-33 may improve the immunogenicity of BCG vaccine by sensitising hMCs.

AB - Bacillus Calmette-Guérin (BCG) vaccine is an attenuated strain of Mycobacterium bovis that provides weak protection against tuberculosis (TB). Mast cells (MCs) are tissue-resident immune cells strategically that serve as the first line of defence against pathogenic threats. In this study, we investigated the response of human MCs (hMCs) to BCG. We found that naïve hMCs exposed to BCG did not secrete cytokines, degranulate, or support the uptake and intracellular growth of bacteria. Since we could show that in hMCs IL-33 promotes the transcription of host-pathogen interaction, cell adhesion and activation genes, we used IL-33 for cell priming. The treatment of hMCs with IL-33, but not IFN-γ, before BCG stimulation increased IL-8, MCP-1 and IL-13 secretion, and induced an enhanced expression of the mycobacteria-binding receptor CD48. These effects were comparable to those caused by the recombinant Mycobacterium tuberculosis (Mtb) 19-KDa lipoprotein. Finally, stimulation of hMCs with IL-33 incremented MC-BCG interactions. Thus, we propose that IL-33 may improve the immunogenicity of BCG vaccine by sensitising hMCs.

KW - mast cells

KW - BCG

KW - IL-33

KW - vaccine booster

KW - M. bovis

UR - https://doi.org/10.3390/ijms23147549

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DO - 10.3390/ijms23147549

M3 - Article (Academic Journal)

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Bacillus Calmette–Guérin-Induced Human Mast Cell Activation Relies on IL-33 Priming

Abstract

Bibliographical note

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Keywords

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