Mycobacterium tuberculosis Catalase Inhibits the Formation of Mast Cell Extracellular Traps

Tuberculosis is one of the leading causes of human morbidity and mortality. Mycobacterium tuberculosis (Mtb) employs different strategies to evade and counterattack immune responses persisting for years. Mast cells are crucial during innate immune responses and help clear infections via inflammation...

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Main Authors: Marcia Campillo-Navarro, Kahiry Leyva-Paredes, Luis Donis-Maturano, Gloria M. Rodríguez-López, Rodolfo Soria-Castro, Blanca Estela García-Pérez, Nahum Puebla-Osorio, Stephen E. Ullrich, Julieta Luna-Herrera, Leopoldo Flores-Romo, Héctor Sumano-López, Sonia M. Pérez-Tapia, Sergio Estrada-Parra, Iris Estrada-García, Rommel Chacón-Salinas
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-05-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fimmu.2018.01161/full
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author Marcia Campillo-Navarro
Marcia Campillo-Navarro
Kahiry Leyva-Paredes
Luis Donis-Maturano
Gloria M. Rodríguez-López
Rodolfo Soria-Castro
Blanca Estela García-Pérez
Nahum Puebla-Osorio
Stephen E. Ullrich
Stephen E. Ullrich
Julieta Luna-Herrera
Leopoldo Flores-Romo
Héctor Sumano-López
Sonia M. Pérez-Tapia
Sonia M. Pérez-Tapia
Sergio Estrada-Parra
Iris Estrada-García
Rommel Chacón-Salinas
Rommel Chacón-Salinas
author_facet Marcia Campillo-Navarro
Marcia Campillo-Navarro
Kahiry Leyva-Paredes
Luis Donis-Maturano
Gloria M. Rodríguez-López
Rodolfo Soria-Castro
Blanca Estela García-Pérez
Nahum Puebla-Osorio
Stephen E. Ullrich
Stephen E. Ullrich
Julieta Luna-Herrera
Leopoldo Flores-Romo
Héctor Sumano-López
Sonia M. Pérez-Tapia
Sonia M. Pérez-Tapia
Sergio Estrada-Parra
Iris Estrada-García
Rommel Chacón-Salinas
Rommel Chacón-Salinas
author_sort Marcia Campillo-Navarro
collection DOAJ
description Tuberculosis is one of the leading causes of human morbidity and mortality. Mycobacterium tuberculosis (Mtb) employs different strategies to evade and counterattack immune responses persisting for years. Mast cells are crucial during innate immune responses and help clear infections via inflammation or by direct antibacterial activity through extracellular traps (MCETs). Whether Mtb induce MCETs production is unknown. In this study, we report that viable Mtb did not induce DNA release by mast cells, but heat-killed Mtb (HK-Mtb) did. DNA released by mast cells after stimulation with HK-Mtb was complexed with histone and tryptase. MCETs induced with PMA and HK-Mtb were unable to kill live Mtb bacilli. Mast cells stimulated with HK-Mtb induced hydrogen peroxide production, whereas cells stimulated with viable Mtb did not. Moreover, MCETs induction by HK-Mtb was dependent of NADPH oxidase activity, because its blockade resulted in a diminished DNA release by mast cells. Interestingly, catalase-deficient Mtb induced a significant production of hydrogen peroxide and DNA release by mast cells, indicating that catalase produced by Mtb prevents MCETs release by degrading hydrogen peroxide. Our findings show a new strategy employed by Mtb to overcome the immune response through inhibiting MCETs formation, which could be relevant during early stages of infection.
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spelling doaj.art-4c42bfee889143aba5af4894b04fae6a2022-12-21T17:57:37ZengFrontiers Media S.A.Frontiers in Immunology1664-32242018-05-01910.3389/fimmu.2018.01161362701Mycobacterium tuberculosis Catalase Inhibits the Formation of Mast Cell Extracellular TrapsMarcia Campillo-Navarro0Marcia Campillo-Navarro1Kahiry Leyva-Paredes2Luis Donis-Maturano3Gloria M. Rodríguez-López4Rodolfo Soria-Castro5Blanca Estela García-Pérez6Nahum Puebla-Osorio7Stephen E. Ullrich8Stephen E. Ullrich9Julieta Luna-Herrera10Leopoldo Flores-Romo11Héctor Sumano-López12Sonia M. Pérez-Tapia13Sonia M. Pérez-Tapia14Sergio Estrada-Parra15Iris Estrada-García16Rommel Chacón-Salinas17Rommel Chacón-Salinas18Departamento de Inmunología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, ENCB-IPN, México City, MexicoDepartamento de Fisiología y Farmacología, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México, UNAM, México City, MexicoDepartamento de Inmunología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, ENCB-IPN, México City, MexicoDepartment of Cell Biology, Cinvestav, Instituto Politécnico Nacional, México City, MexicoDepartamento de Inmunología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, ENCB-IPN, México City, MexicoDepartamento de Inmunología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, ENCB-IPN, México City, MexicoDepartamento de Inmunología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, ENCB-IPN, México City, MexicoDepartment of Lymphoma and Myeloma, The University of Texas MD Anderson Cancer Center, Houston, TX, United StatesDepartment of Immunology, The Center for Cancer Immunology Research, The University of Texas MD Anderson Cancer Center, Houston, TX, United StatesThe University of Texas Graduate School of Biological Sciences at Houston, Houston, TX, United StatesDepartamento de Inmunología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, ENCB-IPN, México City, MexicoDepartment of Cell Biology, Cinvestav, Instituto Politécnico Nacional, México City, MexicoDepartamento de Fisiología y Farmacología, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México, UNAM, México City, MexicoDepartamento de Inmunología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, ENCB-IPN, México City, MexicoUnidad de Desarrollo e Investigación en Bioprocesos (UDIBI), Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, ENCB-IPN, México City, MexicoDepartamento de Inmunología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, ENCB-IPN, México City, MexicoDepartamento de Inmunología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, ENCB-IPN, México City, MexicoDepartamento de Inmunología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, ENCB-IPN, México City, MexicoUnidad de Desarrollo e Investigación en Bioprocesos (UDIBI), Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, ENCB-IPN, México City, MexicoTuberculosis is one of the leading causes of human morbidity and mortality. Mycobacterium tuberculosis (Mtb) employs different strategies to evade and counterattack immune responses persisting for years. Mast cells are crucial during innate immune responses and help clear infections via inflammation or by direct antibacterial activity through extracellular traps (MCETs). Whether Mtb induce MCETs production is unknown. In this study, we report that viable Mtb did not induce DNA release by mast cells, but heat-killed Mtb (HK-Mtb) did. DNA released by mast cells after stimulation with HK-Mtb was complexed with histone and tryptase. MCETs induced with PMA and HK-Mtb were unable to kill live Mtb bacilli. Mast cells stimulated with HK-Mtb induced hydrogen peroxide production, whereas cells stimulated with viable Mtb did not. Moreover, MCETs induction by HK-Mtb was dependent of NADPH oxidase activity, because its blockade resulted in a diminished DNA release by mast cells. Interestingly, catalase-deficient Mtb induced a significant production of hydrogen peroxide and DNA release by mast cells, indicating that catalase produced by Mtb prevents MCETs release by degrading hydrogen peroxide. Our findings show a new strategy employed by Mtb to overcome the immune response through inhibiting MCETs formation, which could be relevant during early stages of infection.https://www.frontiersin.org/article/10.3389/fimmu.2018.01161/fulltuberculosisMycobacterium tuberculosismast cellmast cell extracellular trapcatalase
spellingShingle Marcia Campillo-Navarro
Marcia Campillo-Navarro
Kahiry Leyva-Paredes
Luis Donis-Maturano
Gloria M. Rodríguez-López
Rodolfo Soria-Castro
Blanca Estela García-Pérez
Nahum Puebla-Osorio
Stephen E. Ullrich
Stephen E. Ullrich
Julieta Luna-Herrera
Leopoldo Flores-Romo
Héctor Sumano-López
Sonia M. Pérez-Tapia
Sonia M. Pérez-Tapia
Sergio Estrada-Parra
Iris Estrada-García
Rommel Chacón-Salinas
Rommel Chacón-Salinas
Mycobacterium tuberculosis Catalase Inhibits the Formation of Mast Cell Extracellular Traps
Frontiers in Immunology
tuberculosis
Mycobacterium tuberculosis
mast cell
mast cell extracellular trap
catalase
title Mycobacterium tuberculosis Catalase Inhibits the Formation of Mast Cell Extracellular Traps
title_full Mycobacterium tuberculosis Catalase Inhibits the Formation of Mast Cell Extracellular Traps
title_fullStr Mycobacterium tuberculosis Catalase Inhibits the Formation of Mast Cell Extracellular Traps
title_full_unstemmed Mycobacterium tuberculosis Catalase Inhibits the Formation of Mast Cell Extracellular Traps
title_short Mycobacterium tuberculosis Catalase Inhibits the Formation of Mast Cell Extracellular Traps
title_sort mycobacterium tuberculosis catalase inhibits the formation of mast cell extracellular traps
topic tuberculosis
Mycobacterium tuberculosis
mast cell
mast cell extracellular trap
catalase
url https://www.frontiersin.org/article/10.3389/fimmu.2018.01161/full
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