Cystathionine γ-lyase exacerbates Helicobacter pylori immunopathogenesis by promoting macrophage metabolic remodeling and activation.


Journal

JCI insight
ISSN: 2379-3708
Titre abrégé: JCI Insight
Pays: United States
ID NLM: 101676073

Informations de publication

Date de publication:
22 06 2022
Historique:
received: 28 09 2021
accepted: 10 05 2022
pubmed: 18 5 2022
medline: 24 6 2022
entrez: 17 5 2022
Statut: epublish

Résumé

Macrophages play a crucial role in the inflammatory response to the human stomach pathogen Helicobacter pylori, which infects half of the world's population and causes gastric cancer. Recent studies have highlighted the importance of macrophage immunometabolism in their activation state and function. We have demonstrated that the cysteine-producing enzyme cystathionine γ-lyase (CTH) is upregulated in humans and mice with H. pylori infection. Here, we show that induction of CTH in macrophages by H. pylori promoted persistent inflammation. Cth-/- mice had reduced macrophage and T cell activation in H. pylori-infected tissues, an altered metabolome, and decreased enrichment of immune-associated gene networks, culminating in decreased H. pylori-induced gastritis. CTH is downstream of the proposed antiinflammatory molecule, S-adenosylmethionine (SAM). Whereas Cth-/- mice exhibited gastric SAM accumulation, WT mice treated with SAM did not display protection against H. pylori-induced inflammation. Instead, we demonstrated that Cth-deficient macrophages exhibited alterations in the proteome, decreased NF-κB activation, diminished expression of macrophage activation markers, and impaired oxidative phosphorylation and glycolysis. Thus, through altering cellular respiration, CTH is a key enhancer of macrophage activation, contributing to a pathogenic inflammatory response that is the universal precursor for the development of H. pylori-induced gastric disease.

Identifiants

pubmed: 35579952
pii: 155338
doi: 10.1172/jci.insight.155338
pmc: PMC9309056
doi:
pii:

Substances chimiques

Cystathionine gamma-Lyase EC 4.4.1.1

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NCI NIH HHS
ID : P01 CA028842
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK128200
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA190612
Pays : United States
Organisme : NIAID NIH HHS
ID : R21 AI142042
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK058404
Pays : United States
Organisme : NIAID NIH HHS
ID : T32 AI138932
Pays : United States
Organisme : NCI NIH HHS
ID : P01 CA116087
Pays : United States
Organisme : BLRD VA
ID : I01 BX001453
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA068485
Pays : United States
Organisme : CSRD VA
ID : I01 CX002171
Pays : United States
Organisme : NCI NIH HHS
ID : T32 CA009592
Pays : United States

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Auteurs

Yvonne L Latour (YL)

Department of Pathology, Microbiology, and Immunology.
Division of Gastroenterology, Hepatology, and Nutrition, Department of Medicine, and.

Johanna C Sierra (JC)

Division of Gastroenterology, Hepatology, and Nutrition, Department of Medicine, and.
Center for Mucosal Inflammation and Cancer, Vanderbilt University Medical Center, Nashville, Tennessee, USA.

Jordan L Finley (JL)

Division of Gastroenterology, Hepatology, and Nutrition, Department of Medicine, and.

Mohammad Asim (M)

Division of Gastroenterology, Hepatology, and Nutrition, Department of Medicine, and.

Daniel P Barry (DP)

Division of Gastroenterology, Hepatology, and Nutrition, Department of Medicine, and.

Margaret M Allaman (MM)

Division of Gastroenterology, Hepatology, and Nutrition, Department of Medicine, and.

Thaddeus M Smith (TM)

Division of Gastroenterology, Hepatology, and Nutrition, Department of Medicine, and.

Kara M McNamara (KM)

Division of Gastroenterology, Hepatology, and Nutrition, Department of Medicine, and.
Program in Cancer Biology.

Paula B Luis (PB)

Department of Pharmacology, and.

Claus Schneider (C)

Center for Mucosal Inflammation and Cancer, Vanderbilt University Medical Center, Nashville, Tennessee, USA.
Department of Pharmacology, and.

Justin Jacobse (J)

Department of Pathology, Microbiology, and Immunology.
Division of Gastroenterology, Hepatology, and Nutrition, Department of Medicine, and.

Jeremy A Goettel (JA)

Department of Pathology, Microbiology, and Immunology.
Division of Gastroenterology, Hepatology, and Nutrition, Department of Medicine, and.
Center for Mucosal Inflammation and Cancer, Vanderbilt University Medical Center, Nashville, Tennessee, USA.

M Wade Calcutt (MW)

Department of Biochemistry, Mass Spectrometry Research Center, Vanderbilt University School of Medicine, Nashville, Tennessee, USA.

Kristie L Rose (KL)

Department of Biochemistry, Mass Spectrometry Research Center, Vanderbilt University School of Medicine, Nashville, Tennessee, USA.

Kevin L Schey (KL)

Department of Biochemistry, Mass Spectrometry Research Center, Vanderbilt University School of Medicine, Nashville, Tennessee, USA.

Ginger L Milne (GL)

Division of Clinical Pharmacology, Department of Medicine, Vanderbilt University Medical Center, Nashville, Tennessee, USA.

Alberto G Delgado (AG)

Division of Gastroenterology, Hepatology, and Nutrition, Department of Medicine, and.

M Blanca Piazuelo (MB)

Division of Gastroenterology, Hepatology, and Nutrition, Department of Medicine, and.
Center for Mucosal Inflammation and Cancer, Vanderbilt University Medical Center, Nashville, Tennessee, USA.

Bindu D Paul (BD)

Department of Psychiatry and Behavioral Sciences.
Department of Pharmacology and Molecular Sciences, and.

Solomon H Snyder (SH)

Department of Psychiatry and Behavioral Sciences.
Department of Pharmacology and Molecular Sciences, and.
The Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.

Alain P Gobert (AP)

Division of Gastroenterology, Hepatology, and Nutrition, Department of Medicine, and.
Center for Mucosal Inflammation and Cancer, Vanderbilt University Medical Center, Nashville, Tennessee, USA.

Keith T Wilson (KT)

Department of Pathology, Microbiology, and Immunology.
Division of Gastroenterology, Hepatology, and Nutrition, Department of Medicine, and.
Center for Mucosal Inflammation and Cancer, Vanderbilt University Medical Center, Nashville, Tennessee, USA.
Program in Cancer Biology.
Veterans Affairs Tennessee Valley Healthcare System, Nashville, Tennessee, USA.

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Classifications MeSH