Helicobacter pylori and H 2O 2 increase AP endonuclease-1/redox factor-1 expression in human gastric epithelial cells

Song Ze Ding, Ann M. O'Hara, Tim L. Denning, Bernadette Dirden-Kramer, Randy C. Mifflin, Victor Reyes, Kieran A. Ryan, Susan N. Elliott, Tadahide Izumi, Istvan Boldogh, Sankar Mitra, Peter B. Ernst, Sheila E. Crowe

Research output: Contribution to journalArticle

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Abstract

Background & Aims: Helicobacter pylori infection causes inflammation, accumulation of reactive oxygen species, and oxidative DNA damage in the gastric mucosa. Apurinic/apyrimidinic endonuclease-1 (APE-1)/redox factor-1 (Ref-1) repairs damaged DNA and reductively activates transcription factors, including activator protein-1. Considering that H. pylori generate reactive oxygen species and that reactive oxygen species modulate APE-1/Ref-1 in other cell types, we examined the effect of H. pylori, oxidative stress, and antioxidants on APE-1/Ref-1 expression in human gastric epithelial cells. Methods: Human gastric epithelial cell lines or cells isolated from mucosal biopsy samples were stimulated with H. pylori, Campylobacter jejuni, and/or H 2O 2 in the presence or absence of antioxidants. APE-1/Ref-1 expression was assayed by Western blot or reverse-transcription polymerase chain reaction, and its cellular distribution was determined by using indirect conventional and confocal immunofluorescence. New protein synthesis was detected by [S 35]methionine labeling. APE-1/Ref-1 function was assessed by using a luciferase-linked reporter construct containing 3 activator protein 1 binding sites. Results: APE-1/Ref-1 protein and messenger RNA were detected in resting gastric epithelial cells. APE-1/Ref-1 protein expression was increased after stimulation with H 2O 2 or live cag pathogenicity island-bearing H. pylori, but not cag pathogenicity island-negative H. pylori or C. jejuni. H. pylori- or reactive oxygen species-mediated increases in APE-1/Ref-1 expression involved de novo protein synthesis that was inhibited by antioxidants. H. pylori or H 2O 2 also induced nuclear accumulation of APE-1/Ref-1, and overexpression of APE-1/Ref-1 increased activator protein 1 binding activity. Conclusions: The data show that H. pylori or reactive oxygen species enhance APE-1/Ref-1 protein synthesis and nuclear accumulation in human gastric epithelial cells and implicate APE-1/Ref-1 in the modulation of the pathogenesis of H. pylori infection.

Original languageEnglish
Pages (from-to)845-858
Number of pages14
JournalGastroenterology
Volume127
Issue number3
DOIs
StatePublished - Sep 2004

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DNA-(Apurinic or Apyrimidinic Site) Lyase
Transcription Factor AP-1
Endonucleases
Helicobacter pylori
Oxidation-Reduction
Stomach
Epithelial Cells
Reactive Oxygen Species
Genomic Islands
Campylobacter jejuni
Antioxidants
Helicobacter Infections
Proteins
Protein Binding
NFI Transcription Factors
Gastric Mucosa
Luciferases
DNA Repair
Methionine
DNA Damage

ASJC Scopus subject areas

  • Gastroenterology

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Helicobacter pylori and H 2O 2 increase AP endonuclease-1/redox factor-1 expression in human gastric epithelial cells. / Ding, Song Ze; O'Hara, Ann M.; Denning, Tim L.; Dirden-Kramer, Bernadette; Mifflin, Randy C.; Reyes, Victor; Ryan, Kieran A.; Elliott, Susan N.; Izumi, Tadahide; Boldogh, Istvan; Mitra, Sankar; Ernst, Peter B.; Crowe, Sheila E.

In: Gastroenterology, Vol. 127, No. 3, 09.2004, p. 845-858.

Research output: Contribution to journalArticle

Ding, SZ, O'Hara, AM, Denning, TL, Dirden-Kramer, B, Mifflin, RC, Reyes, V, Ryan, KA, Elliott, SN, Izumi, T, Boldogh, I, Mitra, S, Ernst, PB & Crowe, SE 2004, 'Helicobacter pylori and H 2O 2 increase AP endonuclease-1/redox factor-1 expression in human gastric epithelial cells', Gastroenterology, vol. 127, no. 3, pp. 845-858. https://doi.org/10.1053/j.gastro.2004.06.017
Ding, Song Ze ; O'Hara, Ann M. ; Denning, Tim L. ; Dirden-Kramer, Bernadette ; Mifflin, Randy C. ; Reyes, Victor ; Ryan, Kieran A. ; Elliott, Susan N. ; Izumi, Tadahide ; Boldogh, Istvan ; Mitra, Sankar ; Ernst, Peter B. ; Crowe, Sheila E. / Helicobacter pylori and H 2O 2 increase AP endonuclease-1/redox factor-1 expression in human gastric epithelial cells. In: Gastroenterology. 2004 ; Vol. 127, No. 3. pp. 845-858.
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abstract = "Background & Aims: Helicobacter pylori infection causes inflammation, accumulation of reactive oxygen species, and oxidative DNA damage in the gastric mucosa. Apurinic/apyrimidinic endonuclease-1 (APE-1)/redox factor-1 (Ref-1) repairs damaged DNA and reductively activates transcription factors, including activator protein-1. Considering that H. pylori generate reactive oxygen species and that reactive oxygen species modulate APE-1/Ref-1 in other cell types, we examined the effect of H. pylori, oxidative stress, and antioxidants on APE-1/Ref-1 expression in human gastric epithelial cells. Methods: Human gastric epithelial cell lines or cells isolated from mucosal biopsy samples were stimulated with H. pylori, Campylobacter jejuni, and/or H 2O 2 in the presence or absence of antioxidants. APE-1/Ref-1 expression was assayed by Western blot or reverse-transcription polymerase chain reaction, and its cellular distribution was determined by using indirect conventional and confocal immunofluorescence. New protein synthesis was detected by [S 35]methionine labeling. APE-1/Ref-1 function was assessed by using a luciferase-linked reporter construct containing 3 activator protein 1 binding sites. Results: APE-1/Ref-1 protein and messenger RNA were detected in resting gastric epithelial cells. APE-1/Ref-1 protein expression was increased after stimulation with H 2O 2 or live cag pathogenicity island-bearing H. pylori, but not cag pathogenicity island-negative H. pylori or C. jejuni. H. pylori- or reactive oxygen species-mediated increases in APE-1/Ref-1 expression involved de novo protein synthesis that was inhibited by antioxidants. H. pylori or H 2O 2 also induced nuclear accumulation of APE-1/Ref-1, and overexpression of APE-1/Ref-1 increased activator protein 1 binding activity. Conclusions: The data show that H. pylori or reactive oxygen species enhance APE-1/Ref-1 protein synthesis and nuclear accumulation in human gastric epithelial cells and implicate APE-1/Ref-1 in the modulation of the pathogenesis of H. pylori infection.",
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T1 - Helicobacter pylori and H 2O 2 increase AP endonuclease-1/redox factor-1 expression in human gastric epithelial cells

AU - Ding, Song Ze

AU - O'Hara, Ann M.

AU - Denning, Tim L.

AU - Dirden-Kramer, Bernadette

AU - Mifflin, Randy C.

AU - Reyes, Victor

AU - Ryan, Kieran A.

AU - Elliott, Susan N.

AU - Izumi, Tadahide

AU - Boldogh, Istvan

AU - Mitra, Sankar

AU - Ernst, Peter B.

AU - Crowe, Sheila E.

PY - 2004/9

Y1 - 2004/9

N2 - Background & Aims: Helicobacter pylori infection causes inflammation, accumulation of reactive oxygen species, and oxidative DNA damage in the gastric mucosa. Apurinic/apyrimidinic endonuclease-1 (APE-1)/redox factor-1 (Ref-1) repairs damaged DNA and reductively activates transcription factors, including activator protein-1. Considering that H. pylori generate reactive oxygen species and that reactive oxygen species modulate APE-1/Ref-1 in other cell types, we examined the effect of H. pylori, oxidative stress, and antioxidants on APE-1/Ref-1 expression in human gastric epithelial cells. Methods: Human gastric epithelial cell lines or cells isolated from mucosal biopsy samples were stimulated with H. pylori, Campylobacter jejuni, and/or H 2O 2 in the presence or absence of antioxidants. APE-1/Ref-1 expression was assayed by Western blot or reverse-transcription polymerase chain reaction, and its cellular distribution was determined by using indirect conventional and confocal immunofluorescence. New protein synthesis was detected by [S 35]methionine labeling. APE-1/Ref-1 function was assessed by using a luciferase-linked reporter construct containing 3 activator protein 1 binding sites. Results: APE-1/Ref-1 protein and messenger RNA were detected in resting gastric epithelial cells. APE-1/Ref-1 protein expression was increased after stimulation with H 2O 2 or live cag pathogenicity island-bearing H. pylori, but not cag pathogenicity island-negative H. pylori or C. jejuni. H. pylori- or reactive oxygen species-mediated increases in APE-1/Ref-1 expression involved de novo protein synthesis that was inhibited by antioxidants. H. pylori or H 2O 2 also induced nuclear accumulation of APE-1/Ref-1, and overexpression of APE-1/Ref-1 increased activator protein 1 binding activity. Conclusions: The data show that H. pylori or reactive oxygen species enhance APE-1/Ref-1 protein synthesis and nuclear accumulation in human gastric epithelial cells and implicate APE-1/Ref-1 in the modulation of the pathogenesis of H. pylori infection.

AB - Background & Aims: Helicobacter pylori infection causes inflammation, accumulation of reactive oxygen species, and oxidative DNA damage in the gastric mucosa. Apurinic/apyrimidinic endonuclease-1 (APE-1)/redox factor-1 (Ref-1) repairs damaged DNA and reductively activates transcription factors, including activator protein-1. Considering that H. pylori generate reactive oxygen species and that reactive oxygen species modulate APE-1/Ref-1 in other cell types, we examined the effect of H. pylori, oxidative stress, and antioxidants on APE-1/Ref-1 expression in human gastric epithelial cells. Methods: Human gastric epithelial cell lines or cells isolated from mucosal biopsy samples were stimulated with H. pylori, Campylobacter jejuni, and/or H 2O 2 in the presence or absence of antioxidants. APE-1/Ref-1 expression was assayed by Western blot or reverse-transcription polymerase chain reaction, and its cellular distribution was determined by using indirect conventional and confocal immunofluorescence. New protein synthesis was detected by [S 35]methionine labeling. APE-1/Ref-1 function was assessed by using a luciferase-linked reporter construct containing 3 activator protein 1 binding sites. Results: APE-1/Ref-1 protein and messenger RNA were detected in resting gastric epithelial cells. APE-1/Ref-1 protein expression was increased after stimulation with H 2O 2 or live cag pathogenicity island-bearing H. pylori, but not cag pathogenicity island-negative H. pylori or C. jejuni. H. pylori- or reactive oxygen species-mediated increases in APE-1/Ref-1 expression involved de novo protein synthesis that was inhibited by antioxidants. H. pylori or H 2O 2 also induced nuclear accumulation of APE-1/Ref-1, and overexpression of APE-1/Ref-1 increased activator protein 1 binding activity. Conclusions: The data show that H. pylori or reactive oxygen species enhance APE-1/Ref-1 protein synthesis and nuclear accumulation in human gastric epithelial cells and implicate APE-1/Ref-1 in the modulation of the pathogenesis of H. pylori infection.

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