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Published in: Journal of Clinical Immunology 2/2012

01-04-2012

Interweaving MicroRNAs and Proinflammatory Cytokines in Gastric Mucosa with Reference to H. pylori Infection

Authors: Hajime Isomoto, Kayoko Matsushima, Naoki Inoue, Tomayoshi Hayashi, Toshiyuki Nakayama, Masaki Kunizaki, Shigekazu Hidaka, Masaaki Nakayama, Junzo Hisatsune, Masahiro Nakashima, Takeshi Nagayasu, Kazuhiko Nakao, Toshiya Hirayama

Published in: Journal of Clinical Immunology | Issue 2/2012

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Abstract

Using endoscopic biopsies, gastric mucosal expression levels of interleukin (IL)-1β, IL-6, IL-8, and tumor necrosis factor-alpha (TNF-α) messenger RNA (mRNA) and microRNAs (miRNAs) that were differentially expressed in association with Helicobacter pylori were assessed by quantitative reverse-transcriptase polymerase chain reaction. Among the H. pylori-positive mucosa, 17 out of 29 miRNAs had significant correlations with at least one of the four proinflammatory cytokines in expression. Among the 17 miRNAs, 15 were associated with the degree of neutrophil infiltration and, more prominently, the degree of mononuclear cell infiltration, according to the updated Sydney system. Persistent H. pylori infection may affect the mucosal expression profiles of miRNAs via chronic inflammation mediated by proinflammatory cytokines. There were significant positive correlations between certain miRNAs including the microRNA-200 family and IL-1β, IL-6, or TNF-α mRNA in H. pylori-negative gastric mucosa. Underscoring the causal association between miRNAs and proinflammatory cytokines may provide insights into the pathogenesis of H. pylori-associated gastritis linking to gastric carcinogenesis.
Literature
1.
go back to reference Blaser MJ, Atherton JC. Helicobacter pylori persistence: biology and disease. J Clin Invest. 2004;113:321–33.PubMed Blaser MJ, Atherton JC. Helicobacter pylori persistence: biology and disease. J Clin Invest. 2004;113:321–33.PubMed
2.
go back to reference Ernst PB, Gold BD. The disease spectrum of Helicobacter pylori: the immunopathogenesis of gastroduodenal ulcer and gastric cancer. Annu Rev Microbiol. 2000;54:615–40.PubMedCrossRef Ernst PB, Gold BD. The disease spectrum of Helicobacter pylori: the immunopathogenesis of gastroduodenal ulcer and gastric cancer. Annu Rev Microbiol. 2000;54:615–40.PubMedCrossRef
3.
go back to reference Shimoyama T, Crabtree JE. Bacterial factors and immune pathogenesis in Helicobacter pylori infection. Gut. 1998;43:S2–5.PubMedCrossRef Shimoyama T, Crabtree JE. Bacterial factors and immune pathogenesis in Helicobacter pylori infection. Gut. 1998;43:S2–5.PubMedCrossRef
4.
go back to reference Konturek PC, Konturek SJ, Brzozowski T. Helicobacter pylori infection in gastric cancerogenesis. J Physiol Pharmacol. 2009;60:3–21.PubMed Konturek PC, Konturek SJ, Brzozowski T. Helicobacter pylori infection in gastric cancerogenesis. J Physiol Pharmacol. 2009;60:3–21.PubMed
5.
go back to reference Isomoto H, Mizuta Y, Miyazaki M, Takeshima F, Omagari K, Murase K, et al. Implication of NF-kappaB in Helicobacter pylori-associated gastritis. Am J Gastroenterol. 2000;95:2768–76.PubMed Isomoto H, Mizuta Y, Miyazaki M, Takeshima F, Omagari K, Murase K, et al. Implication of NF-kappaB in Helicobacter pylori-associated gastritis. Am J Gastroenterol. 2000;95:2768–76.PubMed
6.
go back to reference Schetter AJ, Heegaard NH, Harris CC. Inflammation and cancer: interweaving microRNA, free radical, cytokine and p53 pathways. Carcinogenesis. 2010;31:37–49.PubMedCrossRef Schetter AJ, Heegaard NH, Harris CC. Inflammation and cancer: interweaving microRNA, free radical, cytokine and p53 pathways. Carcinogenesis. 2010;31:37–49.PubMedCrossRef
7.
go back to reference Bak RO, Mikkelsen JG. Regulation of cytokines by small RNAs during skin inflammation. J Biomed Sci. 2010;17:53.PubMedCrossRef Bak RO, Mikkelsen JG. Regulation of cytokines by small RNAs during skin inflammation. J Biomed Sci. 2010;17:53.PubMedCrossRef
8.
9.
go back to reference Kloosterman WP, Plasterk RH. The diverse functions of microRNAs in animal development and disease. Dev Cell. 2006;11:441–50.PubMedCrossRef Kloosterman WP, Plasterk RH. The diverse functions of microRNAs in animal development and disease. Dev Cell. 2006;11:441–50.PubMedCrossRef
10.
go back to reference Sonkoly E, Pivarcsi A. Advances in microRNAs: implications for immunity and inflammatory diseases. J Cell Mol Med. 2009;13:24–38.PubMedCrossRef Sonkoly E, Pivarcsi A. Advances in microRNAs: implications for immunity and inflammatory diseases. J Cell Mol Med. 2009;13:24–38.PubMedCrossRef
11.
go back to reference Wu F, Zikusoka M, Trindade A, Dassopoulos T, Harris ML, Bayless TM, et al. MicroRNAs are differentially expressed in ulcerative colitis and alter expression of macrophage inflammatory peptide-2 alpha. Gastroenterology. 2008;135:1624–35.PubMedCrossRef Wu F, Zikusoka M, Trindade A, Dassopoulos T, Harris ML, Bayless TM, et al. MicroRNAs are differentially expressed in ulcerative colitis and alter expression of macrophage inflammatory peptide-2 alpha. Gastroenterology. 2008;135:1624–35.PubMedCrossRef
12.
go back to reference Matsushima K, Isomoto H, Inoue N, Nakayama T, Hayashi T, Nakayama M, et al. MicroRNA signatures in Helicobacter pylori-infected gastric mucosa. Int J Cancer. 2011;128:361–70.PubMedCrossRef Matsushima K, Isomoto H, Inoue N, Nakayama T, Hayashi T, Nakayama M, et al. MicroRNA signatures in Helicobacter pylori-infected gastric mucosa. Int J Cancer. 2011;128:361–70.PubMedCrossRef
13.
go back to reference Asirvatham AJ, Magner WJ, Tomasi TB. miRNA regulation of cytokine genes. Cytokine. 2009;45:58–69.PubMedCrossRef Asirvatham AJ, Magner WJ, Tomasi TB. miRNA regulation of cytokine genes. Cytokine. 2009;45:58–69.PubMedCrossRef
14.
go back to reference Tili E, Michaille JJ, Costinean S, Croce CM. MicroRNAs, the immune system and rheumatic disease. Nat Clin Pract Rheumatol. 2008;4:534–41.PubMedCrossRef Tili E, Michaille JJ, Costinean S, Croce CM. MicroRNAs, the immune system and rheumatic disease. Nat Clin Pract Rheumatol. 2008;4:534–41.PubMedCrossRef
15.
go back to reference Nguyen GH, Schetter AJ, Chou DB, Bowman ED, Zhao R, Hawkes JE, et al. Inflammatory and microRNA gene expression as prognostic classifier of Barrett's-associated esophageal adenocarcinoma. Clin Cancer Res. 2010;16:5824–34.PubMedCrossRef Nguyen GH, Schetter AJ, Chou DB, Bowman ED, Zhao R, Hawkes JE, et al. Inflammatory and microRNA gene expression as prognostic classifier of Barrett's-associated esophageal adenocarcinoma. Clin Cancer Res. 2010;16:5824–34.PubMedCrossRef
16.
go back to reference Dixon MF, Genta RM, Yardley JH, Correa P. Classification and grading of gastritis. The updated Sydney system. International Workshop on the Histopathology of Gastritis, Houston 1994. Am J Surg Pathol. 1996;20:1161–81.PubMedCrossRef Dixon MF, Genta RM, Yardley JH, Correa P. Classification and grading of gastritis. The updated Sydney system. International Workshop on the Histopathology of Gastritis, Houston 1994. Am J Surg Pathol. 1996;20:1161–81.PubMedCrossRef
17.
go back to reference Yoshida A, Isomoto H, Hisatsune J, Nakayama M, Nakashima Y, Matsushima K, et al. Enhanced expression of CCL20 in human Helicobacter pylori-associated gastritis. Clin Immunol. 2009;130:290–7.PubMedCrossRef Yoshida A, Isomoto H, Hisatsune J, Nakayama M, Nakashima Y, Matsushima K, et al. Enhanced expression of CCL20 in human Helicobacter pylori-associated gastritis. Clin Immunol. 2009;130:290–7.PubMedCrossRef
18.
go back to reference Ferrero RL. Innate immune recognition of the extracellular mucosal pathogen, Helicobacter pylori. Mol Immunol. 2005;42:879–85.PubMedCrossRef Ferrero RL. Innate immune recognition of the extracellular mucosal pathogen, Helicobacter pylori. Mol Immunol. 2005;42:879–85.PubMedCrossRef
19.
go back to reference Li N, Xu X, Xiao B, Zhu ED, Li BS, Liu Z, et al. H. pylori related proinflammatory cytokines contribute to the induction of miR-146a in human gastric epithelial cells. Mol Biol Rep. 2011. doi:10.1007/s11033-011-1257-5. Li N, Xu X, Xiao B, Zhu ED, Li BS, Liu Z, et al. H. pylori related proinflammatory cytokines contribute to the induction of miR-146a in human gastric epithelial cells. Mol Biol Rep. 2011. doi:10.​1007/​s11033-011-1257-5.
20.
go back to reference Chen CZ, Li L, Lodish HF, Bartel DP. MicroRNAs modulate hematopoietic lineage differentiation. Science. 2004;303:83–6.PubMedCrossRef Chen CZ, Li L, Lodish HF, Bartel DP. MicroRNAs modulate hematopoietic lineage differentiation. Science. 2004;303:83–6.PubMedCrossRef
21.
go back to reference Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol. 2008;10:593–601.PubMedCrossRef Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol. 2008;10:593–601.PubMedCrossRef
22.
go back to reference Korpal M, Lee ES, Hu G, Kang Y. The miR-200 family inhibits epithelial–mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem. 2008;283:14910–4.PubMedCrossRef Korpal M, Lee ES, Hu G, Kang Y. The miR-200 family inhibits epithelial–mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem. 2008;283:14910–4.PubMedCrossRef
23.
go back to reference Gregory PA, Bracken CP, Bert AG, Goodall GJ. MicroRNAs as regulators of epithelial–mesenchymal transition. Cell Cycle. 2008;7:3112–8.PubMedCrossRef Gregory PA, Bracken CP, Bert AG, Goodall GJ. MicroRNAs as regulators of epithelial–mesenchymal transition. Cell Cycle. 2008;7:3112–8.PubMedCrossRef
24.
go back to reference Kalluri R, Weinberg RA. The basics of epithelial–mesenchymal transition. J Clin Invest. 2009;119:1420–8.PubMedCrossRef Kalluri R, Weinberg RA. The basics of epithelial–mesenchymal transition. J Clin Invest. 2009;119:1420–8.PubMedCrossRef
25.
go back to reference Belair C, Darfeuille F, Staedel C. Helicobacter pylori and gastric cancer: possible role of microRNAs in this intimate relationship. Clin Microbiol Infect. 2009;15:806–12.PubMedCrossRef Belair C, Darfeuille F, Staedel C. Helicobacter pylori and gastric cancer: possible role of microRNAs in this intimate relationship. Clin Microbiol Infect. 2009;15:806–12.PubMedCrossRef
26.
go back to reference Wessler S, Backert S. Molecular mechanisms of epithelial-barrier disruption by Helicobacter pylori. Trends Microbiol. 2008;16:397–405.PubMedCrossRef Wessler S, Backert S. Molecular mechanisms of epithelial-barrier disruption by Helicobacter pylori. Trends Microbiol. 2008;16:397–405.PubMedCrossRef
27.
go back to reference Murata-Kamiya N, Kurashima Y, Teishikata Y, Yamahashi Y, Saito Y, Higashi H, et al. Helicobacter pylori CagA interacts with E-cadherin and deregulates the beta-catenin signal that promotes intestinal transdifferentiation in gastric epithelial cells. Oncogene. 2007;26:4617–26.PubMedCrossRef Murata-Kamiya N, Kurashima Y, Teishikata Y, Yamahashi Y, Saito Y, Higashi H, et al. Helicobacter pylori CagA interacts with E-cadherin and deregulates the beta-catenin signal that promotes intestinal transdifferentiation in gastric epithelial cells. Oncogene. 2007;26:4617–26.PubMedCrossRef
28.
go back to reference Guilford PJ, Hopkins JB, Grady WM, Markowitz SD, Willis J, Lynch H, et al. E-cadherin germline mutations define an inherited cancer syndrome dominated by diffuse gastric cancer. Hum Mutat. 1999;14:249–55.PubMedCrossRef Guilford PJ, Hopkins JB, Grady WM, Markowitz SD, Willis J, Lynch H, et al. E-cadherin germline mutations define an inherited cancer syndrome dominated by diffuse gastric cancer. Hum Mutat. 1999;14:249–55.PubMedCrossRef
29.
30.
go back to reference Craig VJ, Cogliatti SB, Rehrauer H, Wündisch T, Müller A. Epigenetic silencing of microRNA-203 dysregulates ABL1 expression and drives Helicobacter-associated gastric lymphomagenesis. Cancer Res. 2011;71:3616–24.PubMedCrossRef Craig VJ, Cogliatti SB, Rehrauer H, Wündisch T, Müller A. Epigenetic silencing of microRNA-203 dysregulates ABL1 expression and drives Helicobacter-associated gastric lymphomagenesis. Cancer Res. 2011;71:3616–24.PubMedCrossRef
Metadata
Title
Interweaving MicroRNAs and Proinflammatory Cytokines in Gastric Mucosa with Reference to H. pylori Infection
Authors
Hajime Isomoto
Kayoko Matsushima
Naoki Inoue
Tomayoshi Hayashi
Toshiyuki Nakayama
Masaki Kunizaki
Shigekazu Hidaka
Masaaki Nakayama
Junzo Hisatsune
Masahiro Nakashima
Takeshi Nagayasu
Kazuhiko Nakao
Toshiya Hirayama
Publication date
01-04-2012
Publisher
Springer US
Published in
Journal of Clinical Immunology / Issue 2/2012
Print ISSN: 0271-9142
Electronic ISSN: 1573-2592
DOI
https://doi.org/10.1007/s10875-011-9626-3

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