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Erschienen in: Journal of Clinical Immunology 2/2012

01.04.2012

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

verfasst von: 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

Erschienen in: Journal of Clinical Immunology | Ausgabe 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.
Literatur
1.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat Isaacson PG, Du MQ. MALT lymphoma: from morphology to molecules. Nat Rev Cancer. 2004;4:644–53. PubMedCrossRef Isaacson PG, Du MQ. MALT lymphoma: from morphology to molecules. Nat Rev Cancer. 2004;4:644–53. PubMedCrossRef
30.
Zurück zum Zitat 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
Metadaten
Titel
Interweaving MicroRNAs and Proinflammatory Cytokines in Gastric Mucosa with Reference to H. pylori Infection
verfasst von
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
Publikationsdatum
01.04.2012
Verlag
Springer US
Erschienen in
Journal of Clinical Immunology / Ausgabe 2/2012
Print ISSN: 0271-9142
Elektronische ISSN: 1573-2592
DOI
https://doi.org/10.1007/s10875-011-9626-3

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