Helicobacter pylori-induced histone modification, associated gene expression in gastric epithelial cells, and its implication in pathogenesis
Histone modifications are critical in regulating gene expression, cell cycle, cell proliferation, and development. Relatively few studies have investigated whether Helicobacter pylori, the major cause of human gastric diseases, affects histone modification. We therefore investigated the effects of H...
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Published in | PloS one Vol. 5; no. 4; p. e9875 |
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Main Authors | , , , , , , , , , , |
Format | Journal Article |
Language | English |
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01.04.2010
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Abstract | Histone modifications are critical in regulating gene expression, cell cycle, cell proliferation, and development. Relatively few studies have investigated whether Helicobacter pylori, the major cause of human gastric diseases, affects histone modification. We therefore investigated the effects of H. pylori infection on histone modifications in a global and promoter-specific manner in gastric epithelial cells. Infection of gastric epithelial cells by wild-type H. pylori induced time- and dose-dependent dephosphorylation of histone H3 at serine 10 (H3 Ser10) and decreased acetylation of H3 lysine 23, but had no effects on seven other specific modifications. Different cag pathogenicity island (PAI)-containing-clinical isolates showed similar abilities to induce H3 Ser10 dephosphorylation. Mutation of cagA, vacA, nonphosphorylateable CagA mutant cagA(EPISA), or disruption of the flagella showed no effects, while deletion of the entire cagPAI restored the H3 Ser10 phosphorylation to control levels. Analysis of 27 cagPAI mutants indicated that the genes that caused H3 Ser10 dephosphorylation were similar to those that were previously found to induce interleukin-8, irrespective of CagA translocation. This effect was independent of ERK or p38 pathways and type I interferon signaling. Additionally, c-Jun and hsp70 gene expression was associated with this histone modification. These results demonstrate that H. pylori alters histone modification and host response via a cagA-, vacA-independent, but cagPAI-dependent mechanisms, which contribute to its persistent infection and pathogenesis. |
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AbstractList | Histone modifications are critical in regulating gene expression, cell cycle, cell proliferation, and development. Relatively few studies have investigated whether
Helicobacter pylori
, the major cause of human gastric diseases, affects histone modification. We therefore investigated the effects of
H. pylori
infection on histone modifications in a global and promoter-specific manner in gastric epithelial cells. Infection of gastric epithelial cells by wild-type
H. pylori
induced time- and dose-dependent dephosphorylation of histone H3 at serine 10 (H3 Ser10) and decreased acetylation of H3 lysine 23, but had no effects on seven other specific modifications. Different
cag
pathogenicity island (PAI)-containing-clinical isolates showed similar abilities to induce H3 Ser10 dephosphorylation. Mutation of
cagA, vacA
, nonphosphorylateable CagA mutant
cagA
EPISA
, or disruption of the flagella showed no effects, while deletion of the entire
cag
PAI restored the H3 Ser10 phosphorylation to control levels. Analysis of 27
cag
PAI mutants indicated that the genes that caused H3 Ser10 dephosphorylation were similar to those that were previously found to induce interleukin-8, irrespective of CagA translocation. This effect was independent of ERK or p38 pathways and type I interferon signaling. Additionally,
c-Jun
and
hsp70
gene expression was associated with this histone modification. These results demonstrate that
H. pylori
alters histone modification and host response via a
cagA
-,
vacA
-independent, but
cag
PAI-dependent mechanisms, which contribute to its persistent infection and pathogenesis. Histone modifications are critical in regulating gene expression, cell cycle, cell proliferation, and development. Relatively few studies have investigated whether Helicobacter pylori, the major cause of human gastric diseases, affects histone modification. We therefore investigated the effects of H. pylori infection on histone modifications in a global and promoter-specific manner in gastric epithelial cells. Infection of gastric epithelial cells by wild-type H. pylori induced time- and dose-dependent dephosphorylation of histone H3 at serine 10 (H3 Ser10) and decreased acetylation of H3 lysine 23, but had no effects on seven other specific modifications. Different cag pathogenicity island (PAI)-containing-clinical isolates showed similar abilities to induce H3 Ser10 dephosphorylation. Mutation of cagA, vacA, nonphosphorylateable CagA mutant cagA.sub.EPISA, or disruption of the flagella showed no effects, while deletion of the entire cagPAI restored the H3 Ser10 phosphorylation to control levels. Analysis of 27 cagPAI mutants indicated that the genes that caused H3 Ser10 dephosphorylation were similar to those that were previously found to induce interleukin-8, irrespective of CagA translocation. This effect was independent of ERK or p38 pathways and type I interferon signaling. Additionally, c-Jun and hsp70 gene expression was associated with this histone modification. These results demonstrate that H. pylori alters histone modification and host response via a cagA-, vacA-independent, but cagPAI-dependent mechanisms, which contribute to its persistent infection and pathogenesis. Histone modifications are critical in regulating gene expression, cell cycle, cell proliferation, and development. Relatively few studies have investigated whether Helicobacter pylori, the major cause of human gastric diseases, affects histone modification. We therefore investigated the effects of H. pylori infection on histone modifications in a global and promoter-specific manner in gastric epithelial cells. Infection of gastric epithelial cells by wild-type H. pylori induced time- and dose-dependent dephosphorylation of histone H3 at serine 10 (H3 Ser10) and decreased acetylation of H3 lysine 23, but had no effects on seven other specific modifications. Different cag pathogenicity island (PAI)-containing-clinical isolates showed similar abilities to induce H3 Ser10 dephosphorylation. Mutation of cagA, vacA, nonphosphorylateable CagA mutant cagAEPISA, or disruption of the flagella showed no effects, while deletion of the entire cagPAI restored the H3 Ser10 phosphorylation to control levels. Analysis of 27 cagPAI mutants indicated that the genes that caused H3 Ser10 dephosphorylation were similar to those that were previously found to induce interleukin-8, irrespective of CagA translocation. This effect was independent of ERK or p38 pathways and type I interferon signaling. Additionally, c-Jun and hsp70 gene expression was associated with this histone modification. These results demonstrate that H. pylori alters histone modification and host response via a cagA-, vacA-independent, but cagPAI-dependent mechanisms, which contribute to its persistent infection and pathogenesis. Histone modifications are critical in regulating gene expression, cell cycle, cell proliferation, and development. Relatively few studies have investigated whether Helicobacter pylori, the major cause of human gastric diseases, affects histone modification. We therefore investigated the effects of H. pylori infection on histone modifications in a global and promoter-specific manner in gastric epithelial cells. Infection of gastric epithelial cells by wild-type H. pylori induced time- and dose-dependent dephosphorylation of histone H3 at serine 10 (H3 Ser10) and decreased acetylation of H3 lysine 23, but had no effects on seven other specific modifications. Different cag pathogenicity island (PAI)-containing-clinical isolates showed similar abilities to induce H3 Ser10 dephosphorylation. Mutation of cagA, vacA, nonphosphorylateable CagA mutant cagA(EPISA), or disruption of the flagella showed no effects, while deletion of the entire cagPAI restored the H3 Ser10 phosphorylation to control levels. Analysis of 27 cagPAI mutants indicated that the genes that caused H3 Ser10 dephosphorylation were similar to those that were previously found to induce interleukin-8, irrespective of CagA translocation. This effect was independent of ERK or p38 pathways and type I interferon signaling. Additionally, c-Jun and hsp70 gene expression was associated with this histone modification. These results demonstrate that H. pylori alters histone modification and host response via a cagA-, vacA-independent, but cagPAI-dependent mechanisms, which contribute to its persistent infection and pathogenesis. |
Audience | Academic |
Author | Ding, Song-Ze Haas, Rainer Goldberg, Joanna B Grant, Patrick A Liechti, George Kaparakis-Liaskos, Maria Merrell, D Scott Crowe, Sheila E Fischer, Wolfgang Hatakeyama, Masanori Ferrero, Richard L |
AuthorAffiliation | 1 Department of Microbiology, University of Virginia Health System, Charlottesville, Virginia, United States of America 8 Division of Molecular Oncology, Institute for Genetic Medicine, Hokkaido University, Sapporo, Japan 3 Max von Pettenkofer Institute for Hygiene and Medical Microbiology, Ludwig-Maximilians-University, Munich, Germany 2 Max von Pettenkofer Institut, Munich, Germany University of Hyderabad, India 6 Department of Biochemistry and Molecular Genetics, University of Virginia Health System, Charlottesville, Virginia, United States of America 7 Divison of Gastroenterology and Hepatology, Department of Medicine, University of Virginia Health System, Charlottesville, Virginia, United States of America 4 Centre for Innate Immunity and Infectious Disease, Monash Institute of Medical Research, Clayton, Victoria, Australia 5 Department of Microbiology and Immunology, Uniformed Service University of the Health Sciences, Bethesda, Maryland, United States of America |
AuthorAffiliation_xml | – name: 4 Centre for Innate Immunity and Infectious Disease, Monash Institute of Medical Research, Clayton, Victoria, Australia – name: 1 Department of Microbiology, University of Virginia Health System, Charlottesville, Virginia, United States of America – name: 2 Max von Pettenkofer Institut, Munich, Germany – name: 5 Department of Microbiology and Immunology, Uniformed Service University of the Health Sciences, Bethesda, Maryland, United States of America – name: 6 Department of Biochemistry and Molecular Genetics, University of Virginia Health System, Charlottesville, Virginia, United States of America – name: 8 Division of Molecular Oncology, Institute for Genetic Medicine, Hokkaido University, Sapporo, Japan – name: 3 Max von Pettenkofer Institute for Hygiene and Medical Microbiology, Ludwig-Maximilians-University, Munich, Germany – name: 7 Divison of Gastroenterology and Hepatology, Department of Medicine, University of Virginia Health System, Charlottesville, Virginia, United States of America – name: University of Hyderabad, India |
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BackLink | https://www.ncbi.nlm.nih.gov/pubmed/20368982$$D View this record in MEDLINE/PubMed |
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Copyright | COPYRIGHT 2010 Public Library of Science 2010. This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. 2010 |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: SZD PG RLF RH MH JBG. Performed the experiments: SZD WF MKL GL. Analyzed the data: SZD WF MKL PG RLF RH JBG. Contributed reagents/materials/analysis tools: DSM PG RLF SEC. Wrote the paper: SZD DSM PG RLF SEC RH JBG. |
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SubjectTerms | Acetylation Analysis Antigens, Bacterial - genetics Antigens, Bacterial - physiology Antiulcer agents Bacterial Proteins - genetics Bacterial Proteins - physiology Biological response modifiers c-Jun protein Carcinogens Cell cycle Cell proliferation Cells, Cultured Chemokines Chromatin Clinical isolates Clonal deletion Cytokines Dephosphorylation Disruption Epithelial cells Epithelial Cells - microbiology Epithelial Cells - pathology Flagella Gastric Mucosa - microbiology Gastric Mucosa - pathology Gastroenterology and Hepatology/Gastrointestinal Cancers Gastrointestinal diseases Gene expression Gene Expression Regulation Genetic engineering Genetic research Genetics and Genomics/Epigenetics Health aspects Heat shock proteins Helicobacter infections Helicobacter Infections - pathology Helicobacter pylori Helicobacter pylori - pathogenicity Histone H3 Histones - metabolism Hsp70 protein Humans Immunology/Immunity to Infections Infection Infections Infectious diseases Infectious Diseases/Bacterial Infections Infectious Diseases/Gastrointestinal Infections Inflammation Interferon Interleukin 8 Ischemia Kinases Lysine Medical research Microbiology/Immunity to Infections Mutants Mutation Pathogenesis Pathogenicity Pathogens Phosphorylation Polyamide-imides Protein Processing, Post-Translational Rodents Serine Signaling Streptococcus infections Transcription factors Translocation Trinucleotide repeats |
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Title | Helicobacter pylori-induced histone modification, associated gene expression in gastric epithelial cells, and its implication in pathogenesis |
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