GPX4 regulates cellular necrosis and host resistance in Mycobacterium tuberculosis infection

Cellular necrosis during Mycobacterium tuberculosis (Mtb) infection promotes both immunopathology and bacterial dissemination. Glutathione peroxidase-4 (Gpx4) is an enzyme that plays a critical role in preventing iron-dependent lipid peroxidation-mediated cell death (ferroptosis), a process previous...

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Published inThe Journal of experimental medicine Vol. 219; no. 11
Main Authors Amaral, Eduardo P, Foreman, Taylor W, Namasivayam, Sivaranjani, Hilligan, Kerry L, Kauffman, Keith D, Barbosa Bomfim, Caio Cesar, Costa, Diego L, Barreto-Duarte, Beatriz, Gurgel-Rocha, Clarissa, Santana, Monique Freire, Cordeiro-Santos, Marcelo, Du Bruyn, Elsa, Riou, Catherine, Aberman, Kate, Wilkinson, Robert John, Barber, Daniel L, Mayer-Barber, Katrin D, Andrade, Bruno B, Sher, Alan
Format Journal Article
LanguageEnglish
Published United States Rockefeller University Press 07.11.2022
Subjects
Animals
Ferroptosis
Glutathione - metabolism
Glutathione Peroxidase - metabolism
Infectious Disease and Host Defense
Innate Immunity and Inflammation
Lipid Peroxidation
Metabolism
Mice
Mice, Transgenic
Necrosis
Phospholipid Hydroperoxide Glutathione Peroxidase
Tuberculosis - immunology
Tuberculosis - metabolism
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Abstract Cellular necrosis during Mycobacterium tuberculosis (Mtb) infection promotes both immunopathology and bacterial dissemination. Glutathione peroxidase-4 (Gpx4) is an enzyme that plays a critical role in preventing iron-dependent lipid peroxidation-mediated cell death (ferroptosis), a process previously implicated in the necrotic pathology seen in Mtb-infected mice. Here, we document altered GPX4 expression, glutathione levels, and lipid peroxidation in patients with active tuberculosis and assess the role of this pathway in mice genetically deficient in or overexpressing Gpx4. We found that Gpx4-deficient mice infected with Mtb display substantially increased lung necrosis and bacterial burdens, while transgenic mice overexpressing the enzyme show decreased bacterial loads and necrosis. Moreover, Gpx4-deficient macrophages exhibited enhanced necrosis upon Mtb infection in vitro, an outcome suppressed by the lipid peroxidation inhibitor, ferrostatin-1. These findings provide support for the role of ferroptosis in Mtb-induced necrosis and implicate the Gpx4/GSH axis as a target for host-directed therapy of tuberculosis.
AbstractList Cellular necrosis during Mycobacterium tuberculosis (Mtb) infection promotes both immunopathology and bacterial dissemination. Glutathione peroxidase-4 (Gpx4) is an enzyme that plays a critical role in preventing iron-dependent lipid peroxidation–mediated cell death (ferroptosis), a process previously implicated in the necrotic pathology seen in Mtb-infected mice. Here, we document altered GPX4 expression, glutathione levels, and lipid peroxidation in patients with active tuberculosis and assess the role of this pathway in mice genetically deficient in or overexpressing Gpx4. We found that Gpx4-deficient mice infected with Mtb display substantially increased lung necrosis and bacterial burdens, while transgenic mice overexpressing the enzyme show decreased bacterial loads and necrosis. Moreover, Gpx4-deficient macrophages exhibited enhanced necrosis upon Mtb infection in vitro, an outcome suppressed by the lipid peroxidation inhibitor, ferrostatin-1. These findings provide support for the role of ferroptosis in Mtb-induced necrosis and implicate the Gpx4/GSH axis as a target for host-directed therapy of tuberculosis.
Tissue necrosis is a major pathophysiological hallmark of disease progression in tuberculosis. In this study, Amaral et al. show that GPX4, an antioxidant selenoenzyme, is an essential regulator of both lipid peroxidation–mediated cellular necrosis and host resistance in Mycobacterium tuberculosis infection. Cellular necrosis during Mycobacterium tuberculosis (Mtb) infection promotes both immunopathology and bacterial dissemination. Glutathione peroxidase-4 (Gpx4) is an enzyme that plays a critical role in preventing iron-dependent lipid peroxidation–mediated cell death (ferroptosis), a process previously implicated in the necrotic pathology seen in Mtb-infected mice. Here, we document altered GPX4 expression, glutathione levels, and lipid peroxidation in patients with active tuberculosis and assess the role of this pathway in mice genetically deficient in or overexpressing Gpx4. We found that Gpx4-deficient mice infected with Mtb display substantially increased lung necrosis and bacterial burdens, while transgenic mice overexpressing the enzyme show decreased bacterial loads and necrosis. Moreover, Gpx4-deficient macrophages exhibited enhanced necrosis upon Mtb infection in vitro, an outcome suppressed by the lipid peroxidation inhibitor, ferrostatin-1. These findings provide support for the role of ferroptosis in Mtb-induced necrosis and implicate the Gpx4/GSH axis as a target for host-directed therapy of tuberculosis.
Author Barber, Daniel L
Gurgel-Rocha, Clarissa
Kauffman, Keith D
Wilkinson, Robert John
Hilligan, Kerry L
Andrade, Bruno B
Amaral, Eduardo P
Du Bruyn, Elsa
Barreto-Duarte, Beatriz
Aberman, Kate
Mayer-Barber, Katrin D
Costa, Diego L
Riou, Catherine
Namasivayam, Sivaranjani
Barbosa Bomfim, Caio Cesar
Santana, Monique Freire
Foreman, Taylor W
Cordeiro-Santos, Marcelo
Sher, Alan
AuthorAffiliation 3 Departmento de Bioquímica e Imunologia, Programa de Pós-Graduação em Imunologia Básica e Aplicada, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, Brazil
6 Curso de Medicina, Universidade Salvador, Laureate Universities, Salvador, Brazil
18 Faculdade de Medicina, Universidade Federal da Bahia, Salvador, Brazil
2 T Lymphocyte Biology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, MD
11 Programa de Pós-Graduação em Medicina Tropical, Universidade do Estado do Amazonas, Manaus, Brazil
8 Center for Biotechnology and Cell Therapy, D’Or Institute for Research and Education, Sao Rafael Hospital, Salvador, Bahia, Brazil
9 Departmento de Ensino e Pesquisa, Fundação Centro de Controle de Oncologia do Estado do Amazonas, Manaus, Brazil
19 Curso de Medicina, Universidade Faculdade de Tecnologia e Ciências, Salvador, Bahia, Brazil
13 Wellcome Centre for Infectious Disease Researc
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Disclosures: The authors declare no competing interests exist.
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PublicationDate 2022-11-07
PublicationDateYYYYMMDD 2022-11-07
PublicationDate_xml – month: 11
  year: 2022
  text: 2022-11-07
  day: 07
PublicationDecade 2020
PublicationPlace United States
PublicationPlace_xml – name: United States
PublicationTitle The Journal of experimental medicine
PublicationTitleAlternate J Exp Med
PublicationYear 2022
Publisher Rockefeller University Press
Publisher_xml – name: Rockefeller University Press
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Snippet Cellular necrosis during Mycobacterium tuberculosis (Mtb) infection promotes both immunopathology and bacterial dissemination. Glutathione peroxidase-4 (Gpx4)...
Tissue necrosis is a major pathophysiological hallmark of disease progression in tuberculosis. In this study, Amaral et al. show that GPX4, an antioxidant...
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SubjectTerms Animals
Ferroptosis
Glutathione - metabolism
Glutathione Peroxidase - metabolism
Infectious Disease and Host Defense
Innate Immunity and Inflammation
Lipid Peroxidation
Metabolism
Mice
Mice, Transgenic
Necrosis
Phospholipid Hydroperoxide Glutathione Peroxidase
Tuberculosis - immunology
Tuberculosis - metabolism
Title GPX4 regulates cellular necrosis and host resistance in Mycobacterium tuberculosis infection
URI https://www.ncbi.nlm.nih.gov/pubmed/36069923
https://search.proquest.com/docview/2711307858
https://pubmed.ncbi.nlm.nih.gov/PMC9458471
Volume 219
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