Literature DB >> 23860501

Dual oxidases control release of hydrogen peroxide by the gastric epithelium to prevent Helicobacter felis infection and inflammation in mice.

Helmut Grasberger1, Mohamad El-Zaatari, Duyen T Dang, Juanita L Merchant.   

Abstract

BACKGROUND & AIMS: Dual oxidases (DUOX) are conserved reduced nicotinamide adenine dinucleotide phosphate oxidases that produce H2O2 at the epithelial cell surface. The DUOX enzyme comprises the DUOX and DUOX maturation factor (DUOXA) subunits. Mammalian genomes encode 2 DUOX isoenzymes (DUOX1/DUOXA1 and DUOX2/DUOXA2). Expression of these genes is up-regulated during bacterial infections and chronic inflammatory diseases of the luminal gastrointestinal tract. The roles of DUOX in cellular interactions with microbes have not been determined in higher vertebrates.
METHODS: Mice with disruptions of Duoxa1 and Duoxa2 genes (Duoxa(-/-) mice) and control mice were infected with Helicobacter felis to create a model of Helicobacter pylori infection--the most common human chronic infection.
RESULTS: Infection with H. felis induced expression of Duox2 and Duoxa2 in the stomachs of wild-type mice, and DUOX protein specifically localized to the apical surface of epithelial cells. H. felis colonized the mucus layer in the stomachs of Duoxa(-/-) mice to a greater extent than in control mice. The increased colonization persisted into the chronic phase of infection and correlated with an increased, yet ineffective, inflammatory response. H. felis colonization also was increased in Duoxa(+/-) mice, compared with controls. We observed reduced expression of the H2O2-inducible katA gene in H. felis that colonized Duoxa(-/-) mice, compared with that found in controls (P = .0002), indicating that Duox causes oxidative stress in these bacteria. In vitro, induction of oxidative defense by H. felis failed to prevent a direct bacteriostatic effect at sustained levels of H2O2 as low as 30 μmol/L.
CONCLUSIONS: Based on studies of Duoxa(-/-) mice, the DUOX enzyme complex prevents gastric colonization by H. felis and the inflammatory response. These findings indicate the nonredundant function of epithelial production of H2O2 in restricting microbial colonization.
Copyright © 2013 AGA Institute. Published by Elsevier Inc. All rights reserved.

Entities:  

Keywords:  ATP; DUOX; DUOXA; Dual Oxidase; FBS; GI; GOX; Gastritis; HRP; KRH; Krebs–Ringer–HEPES buffer; Mouse Model; Mucosal Immunity; NADPH; PBS; adenosine triphosphate; dual oxidase maturation factor; dual oxidases; fetal bovine serum; gastrointestinal; glucose oxidase; horseradish peroxidase; mRNA; messenger RNA; phosphate-buffered saline; reduced nicotinamide adenine dinucleotide phosphate

Mesh:

Substances:

Year:  2013        PMID: 23860501      PMCID: PMC3805753          DOI: 10.1053/j.gastro.2013.07.011

Source DB:  PubMed          Journal:  Gastroenterology        ISSN: 0016-5085            Impact factor:   22.682


  49 in total

1.  Cloning of two human thyroid cDNAs encoding new members of the NADPH oxidase family.

Authors:  X De Deken; D Wang; M C Many; S Costagliola; F Libert; G Vassart; J E Dumont; F Miot
Journal:  J Biol Chem       Date:  2000-07-28       Impact factor: 5.157

2.  Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli.

Authors:  L C Seaver; J A Imlay
Journal:  J Bacteriol       Date:  2001-12       Impact factor: 3.490

Review 3.  Hydrogen peroxide in the human body.

Authors:  B Halliwell; M V Clement; L H Long
Journal:  FEBS Lett       Date:  2000-12-01       Impact factor: 4.124

4.  BCA-1 is highly expressed in Helicobacter pylori-induced mucosa-associated lymphoid tissue and gastric lymphoma.

Authors:  L Mazzucchelli; A Blaser; A Kappeler; P Schärli; J A Laissue; M Baggiolini; M Uguccioni
Journal:  J Clin Invest       Date:  1999-11       Impact factor: 14.808

5.  Up-regulation of IL-17 is associated with bioactive IL-8 expression in Helicobacter pylori-infected human gastric mucosa.

Authors:  F Luzza; T Parrello; G Monteleone; L Sebkova; M Romano; R Zarrilli; M Imeneo; F Pallone
Journal:  J Immunol       Date:  2000-11-01       Impact factor: 5.422

6.  Susceptibility of Helicobacter pylori and its urease activity to the peroxidase-hydrogen peroxide-thiocyanate antimicrobial system.

Authors:  K Shin; K Yamauchi; S Teraguchi; H Hayasawa; I Imoto
Journal:  J Med Microbiol       Date:  2002-03       Impact factor: 2.472

7.  Association of Helicobacter pylori antioxidant activities with host colonization proficiency.

Authors:  Adriana A Olczak; Richard W Seyler; Jonathan W Olson; Robert J Maier
Journal:  Infect Immun       Date:  2003-01       Impact factor: 3.441

8.  Catalase (KatA) and KatA-associated protein (KapA) are essential to persistent colonization in the Helicobacter pylori SS1 mouse model.

Authors:  Andrew G Harris; John E Wilson; Stephen J Danon; Michael F Dixon; Kevin Donegan; Stuart L Hazell
Journal:  Microbiology       Date:  2003-03       Impact factor: 2.777

9.  The spatial orientation of Helicobacter pylori in the gastric mucus.

Authors:  Sören Schreiber; Manuela Konradt; Claudia Groll; Peter Scheid; Guido Hanauer; Hans-Otto Werling; Christine Josenhans; Sebastian Suerbaum
Journal:  Proc Natl Acad Sci U S A       Date:  2004-03-25       Impact factor: 11.205

10.  Calcium flashes orchestrate the wound inflammatory response through DUOX activation and hydrogen peroxide release.

Authors:  William Razzell; Iwan Robert Evans; Paul Martin; Will Wood
Journal:  Curr Biol       Date:  2013-02-07       Impact factor: 10.834

View more
  46 in total

Review 1.  ROS in gastrointestinal inflammation: Rescue Or Sabotage?

Authors:  G Aviello; U G Knaus
Journal:  Br J Pharmacol       Date:  2016-03-03       Impact factor: 8.739

2.  Polymorphic Immune Mechanisms Regulate Commensal Repertoire.

Authors:  Aly A Khan; Leonid Yurkovetskiy; Kelly O'Grady; Joseph M Pickard; Renée de Pooter; Dionysios A Antonopoulos; Tatyana Golovkina; Alexander Chervonsky
Journal:  Cell Rep       Date:  2019-10-15       Impact factor: 9.423

3.  Aquaporin-3 mediates hydrogen peroxide-dependent responses to environmental stress in colonic epithelia.

Authors:  Jay R Thiagarajah; Jeffrey Chang; Jeremy A Goettel; Alan S Verkman; Wayne I Lencer
Journal:  Proc Natl Acad Sci U S A       Date:  2017-01-03       Impact factor: 11.205

4.  The extracellular A-loop of dual oxidases affects the specificity of reactive oxygen species release.

Authors:  Takehiko Ueyama; Megumi Sakuma; Yuzuru Ninoyu; Takeshi Hamada; Corinne Dupuy; Miklós Geiszt; Thomas L Leto; Naoaki Saito
Journal:  J Biol Chem       Date:  2015-01-13       Impact factor: 5.157

Review 5.  Colonization, localization, and inflammation: the roles of H. pylori chemotaxis in vivo.

Authors:  Kevin S Johnson; Karen M Ottemann
Journal:  Curr Opin Microbiol       Date:  2017-12-01       Impact factor: 7.934

Review 6.  Epithelial Toll-like receptors and their role in gut homeostasis and disease.

Authors:  Juan F Burgueño; Maria T Abreu
Journal:  Nat Rev Gastroenterol Hepatol       Date:  2020-02-26       Impact factor: 46.802

Review 7.  The complex roles of NADPH oxidases in fungal infection.

Authors:  Deborah Hogan; Robert T Wheeler
Journal:  Cell Microbiol       Date:  2014-07-07       Impact factor: 3.715

8.  Chemotaxis Allows Bacteria To Overcome Host-Generated Reactive Oxygen Species That Constrain Gland Colonization.

Authors:  Kieran D Collins; Shuai Hu; Helmut Grasberger; John Y Kao; Karen M Ottemann
Journal:  Infect Immun       Date:  2018-04-23       Impact factor: 3.441

Review 9.  Neutrophils and the inflammatory tissue microenvironment in the mucosa.

Authors:  Eric L Campbell; Daniel J Kao; Sean P Colgan
Journal:  Immunol Rev       Date:  2016-09       Impact factor: 12.988

10.  iNOS- and NOX1-dependent ROS production maintains bacterial homeostasis in the ileum of mice.

Authors:  C Matziouridou; S D C Rocha; O A Haabeth; K Rudi; H Carlsen; A Kielland
Journal:  Mucosal Immunol       Date:  2017-12-06       Impact factor: 7.313

View more

北京卡尤迪生物科技股份有限公司 © 2022-2023.