Table of Contents Author Guidelines Submit a Manuscript
Gastroenterology Research and Practice
Volume 2018, Article ID 9050715, 9 pages
https://doi.org/10.1155/2018/9050715
Research Article

Activation of Signal Transduction and Activator of Transcription 3 Signaling Contributes to Helicobacter-Associated Gastric Epithelial Proliferation and Inflammation

1Department of Gastroenterology, Yokohama City University Graduate School of Medicine, 3-9 Fukuura, Kanazawa-ku, Yokohama 236-0004, Japan
2Advanced Medical Research Center, Yokohama City University, 3-9 Fukuura, Kanazawa-ku, Yokohama 236-0004, Japan

Correspondence should be addressed to Shin Maeda; pj.ca.uc-amahokoy@adeams

Received 23 September 2017; Revised 25 December 2017; Accepted 14 January 2018; Published 8 April 2018

Academic Editor: Haruhiko Sugimura

Copyright © 2018 Yasuaki Ishii et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. N. Uemura, S. Okamoto, S. Yamamoto et al., “Helicobacter pylori infection and the development of gastric cancer,” New England Journal of Medicine, vol. 345, no. 11, pp. 784–789, 2001. View at Publisher · View at Google Scholar · View at Scopus
  2. P. Correa and J. Houghton, “Carcinogenesis of Helicobacter pylori,” Gastroenterology, vol. 133, no. 2, pp. 659–672, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. S. Sue, W. Shibata, and S. Maeda, “Helicobacter pylori-induced signaling pathways contribute to intestinal metaplasia and gastric carcinogenesis,” BioMed Research International, vol. 2015, Article ID 737621, 9 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  4. N. C. Tebbutt, A. S. Giraud, M. Inglese et al., “Reciprocal regulation of gastrointestinal homeostasis by SHP2 and STAT-mediated trefoil gene activation in gp130 mutant mice,” Nature Medicine, vol. 8, no. 10, pp. 1089–1097, 2002. View at Publisher · View at Google Scholar · View at Scopus
  5. T. Hirano, K. Ishihara, and M. Hibi, “Roles of STAT3 in mediating the cell growth, differentiation and survival signals relayed through the IL-6 family of cytokine receptors,” Oncogene, vol. 19, no. 21, pp. 2548–2556, 2000. View at Publisher · View at Google Scholar
  6. J. Bromberg and T. C. Wang, “Inflammation and cancer: IL-6 and STAT3 complete the link,” Cancer Cell, vol. 15, no. 2, pp. 79-80, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. L. M. Judd, K. Bredin, A. Kalantzis, B. J. Jenkins, M. Ernst, and A. S. Giraud, “STAT3 activation regulates growth, inflammation, and vascularization in a mouse model of gastric tumorigenesis,” Gastroenterology, vol. 131, no. 4, pp. 1073–1085, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. G. He, G. Y. Yu, V. Temkin et al., “Hepatocyte IKKβ/NF-κB inhibits tumor promotion and progression by preventing oxidative stress-driven STAT3 activation,” Cancer Cell, vol. 17, no. 3, pp. 286–297, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. H. Lee, A. Herrmann, J. H. Deng et al., “Persistently activated Stat3 maintains constitutive NF-κB activity in tumors,” Cancer Cell, vol. 15, no. 4, pp. 283–293, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. T. Atsumi, R. Singh, L. Sabharwal et al., “Inflammation amplifier, a new paradigm in cancer biology,” Cancer Research, vol. 74, no. 1, pp. 8–14, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Xiang, N. J. Birkbak, V. Vafaizadeh et al., “STAT3 induction of miR-146b forms a feedback loop to inhibit the NF-κB to IL-6 signaling axis and STAT3-driven cancer phenotypes,” Science Signaling, vol. 7, no. 310, article ra11, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Maeda, Y. Hikiba, K. Sakamoto et al., “Ikappa B kinaseβ/nuclear factor-κB activation controls the development of liver metastasis by way of interleukin-6 expression,” Hepatology, vol. 50, no. 6, pp. 1851–1860, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. H. Kinoshita, Y. Hirata, H. Nakagawa et al., “Interleukin-6 mediates epithelial–stromal interactions and promotes gastric tumorigenesis,” PLoS One, vol. 8, no. 4, article e60914, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. L. Lin, B. Hutzen, S. Ball et al., “New curcumin analogues exhibit enhanced growth-suppressive activity and inhibit AKT and signal transducer and activator of transcription 3 phosphorylation in breast and prostate cancer cells,” Cancer Science, vol. 100, no. 9, pp. 1719–1727, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Grivennikov, E. Karin, J. Terzic et al., “IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer,” Cancer Cell, vol. 15, no. 2, pp. 103–113, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Bollrath, T. J. Phesse, V. A. von Burstin et al., “gp130-Mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis,” Cancer Cell, vol. 15, no. 2, pp. 91–102, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. D. M. Bronte-Tinkew, M. Terebiznik, A. Franco et al., “Helicobacter pylori cytotoxin-associated gene A activates the signal transducer and activator of transcription 3 pathway in vitro and in vivo,” Cancer Research, vol. 69, no. 2, pp. 632–639, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Ernst, M. Najdovska, D. Grail et al., “STAT3 and STAT1 mediate IL-11-dependent and inflammation-associated gastric tumorigenesis in gp130 receptor mutant mice,” Journal of Clinical Investigation, vol. 118, no. 5, pp. 1727–1738, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. K. S. Lee, A. Kalantzis, C. B. Jackson et al., “Helicobacter pylori CagA triggers expression of the bactericidal lectin REG3γ via gastric STAT3 activation,” PLoS One, vol. 7, no. 2, article e30786, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Howlett, A. S. Giraud, H. Lescesen et al., “The interleukin-6 family cytokine interleukin-11 regulates homeostatic epithelial cell turnover and promotes gastric tumor development,” Gastroenterology, vol. 136, no. 3, pp. 967–977.e3, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. R. E. Ericksen, S. Rose, C. B. Westphalen et al., “Obesity accelerates Helicobacter felis-induced gastric carcinogenesis by enhancing immature myeloid cell trafficking and TH17 response,” Gut, vol. 63, no. 3, pp. 385–394, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. W. Shibata, S. Takaishi, S. Muthupalani et al., “Conditional deletion of IκB-kinase-β accelerates Helicobacter-dependent gastric apoptosis, proliferation, and preneoplasia,” Gastroenterology, vol. 138, no. 3, pp. 1022–1034.e10, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. W. Shibata, H. Ariyama, C. B. Westphalen et al., “Stromal cell-derived factor-1 overexpression induces gastric dysplasia through expansion of stromal myofibroblasts and epithelial progenitors,” Gut, vol. 62, no. 2, pp. 192–200, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Sue, W. Shibata, E. Kameta et al., “Intestine-specific homeobox (ISX) induces intestinal metaplasia and cell proliferation to contribute to gastric carcinogenesis,” Journal of Gastroenterology, vol. 51, no. 10, pp. 949–960, 2016. View at Publisher · View at Google Scholar · View at Scopus
  25. C. S. Lee, N. J. Sund, R. Behr, P. L. Herrera, and K. H. Kaestner, “Foxa2 is required for the differentiation of pancreatic α-cells,” Developmental Biology, vol. 278, no. 2, pp. 484–495, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Takaishi, G. Cui, D. M. Frederick et al., “Synergistic inhibitory effects of gastrin and histamine receptor antagonists on Helicobacter-induced gastric cancer,” Gastroenterology, vol. 128, no. 7, pp. 1965–1983, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. A. B. Rogers and J. M. Houghton, “Helicobacter-based mouse models of digestive system carcinogenesis,” Methods in Molecular Biology, vol. 511, pp. 267–295, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. W. Shibata, S. Sue, S. Tsumura et al., “Helicobacter-induced gastric inflammation alters the properties of gastric tissue stem/progenitor cells,” BMC Gastroenterology, vol. 17, no. 1, p. 145, 2017. View at Publisher · View at Google Scholar
  29. L. Pedranzini, T. Dechow, M. Berishaj et al., “Pyridone 6, a Pan-Janus-activated kinase inhibitor, induces growth inhibition of multiple myeloma cells,” Cancer Research, vol. 66, no. 19, pp. 9714–9721, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. K. Takeda, K. Noguchi, W. Shi et al., “Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 8, pp. 3801–3804, 1997. View at Publisher · View at Google Scholar · View at Scopus
  31. C. P. Petersen, J. C. Mills, and J. R. Goldenring, “Murine models of gastric corpus preneoplasia,” Cellular and Molecular Gastroenterology and Hepatology, vol. 3, no. 1, pp. 11–26, 2017. View at Publisher · View at Google Scholar · View at Scopus
  32. A. Sarkar, A. J. Huebner, R. Sulahian et al., “Sox2 suppresses gastric tumorigenesis in mice,” Cell Reports, vol. 16, no. 7, pp. 1929–1941, 2016. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Yu, M. Yang, and K. T. Nam, “Mouse models of gastric carcinogenesis,” Journal of Gastric Cancer, vol. 14, no. 2, pp. 67–86, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. J. G. Fox, B. J. Sheppard, C. A. Dangler, M. T. Whary, M. Ihrig, and T. C. Wang, “Germ-line p53-targeted disruption inhibits Helicobacter-induced premalignant lesions and invasive gastric carcinoma through down-regulation of Th1 proinflammatory responses,” Cancer Research, vol. 62, no. 3, pp. 696–702, 2002. View at Google Scholar
  35. S. Nomura, T. Baxter, H. Yamaguchi et al., “Spasmolytic polypeptide expressing metaplasia to preneoplasia in H. felis-infected mice,” Gastroenterology, vol. 127, no. 2, pp. 582–594, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. R. Mejias-Luque, S. K. Linden, M. Garrido et al., “Inflammation modulates the expression of the intestinal mucins MUC2 and MUC4 in gastric tumors,” Oncogene, vol. 29, no. 12, pp. 1753–1762, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Tsugane and S. Sasazuki, “Diet and the risk of gastric cancer: review of epidemiological evidence,” Gastric Cancer, vol. 10, no. 2, pp. 75–83, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. W. Shibata, S. Maeda, Y. Hikiba et al., “c-Jun NH2-terminal kinase 1 is a critical regulator for the development of gastric cancer in mice,” Cancer Research, vol. 68, no. 13, pp. 5031–5039, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. K. Sakamoto, Y. Hikiba, H. Nakagawa et al., “Inhibitor of κB kinase beta regulates gastric carcinogenesis via interleukin-1α expression,” Gastroenterology, vol. 139, no. 1, pp. 226–238.e6, 2010, e226. View at Publisher · View at Google Scholar · View at Scopus
  40. Y.-J. Bang, E. Van Cutsem, A. Feyereislova et al., “Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial,” The Lancet, vol. 376, no. 9742, pp. 687–697, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Hamada, A. Masamune, N. Yoshida, T. Takikawa, and T. Shimosegawa, “IL-6/STAT3 plays a regulatory role in the interaction between pancreatic stellate cells and cancer cells,” Digestive Diseases and Sciences, vol. 61, no. 6, pp. 1561–1571, 2016. View at Publisher · View at Google Scholar · View at Scopus
  42. M. Quante, S. P. Tu, H. Tomita et al., “Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth,” Cancer Cell, vol. 19, no. 2, pp. 257–272, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. K. Takeda, B. E. Clausen, T. Kaisho et al., “Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils,” Immunity, vol. 10, no. 1, pp. 39–49, 1999. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Maeda, H. Kamata, J. L. Luo, H. Leffert, and M. Karin, “IKKβ couples hepatocyte death to cytokine-driven compensatory proliferation that promotes chemical hepatocarcinogenesis,” Cell, vol. 121, no. 7, pp. 977–990, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. T. Tadokoro, Y. Wang, L. S. Barak, Y. Bai, S. H. Randell, and B. L. M. Hogan, “IL-6/STAT3 promotes regeneration of airway ciliated cells from basal stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 35, pp. E3641–E3649, 2014. View at Publisher · View at Google Scholar · View at Scopus
  46. Y. Fujii, K. Yoshihashi, H. Suzuki et al., “CDX1 confers intestinal phenotype on gastric epithelial cells via induction of stemness-associated reprogramming factors SALL4 and KLF5,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 50, pp. 20584–20589, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Takaishi, T. Okumura, S. Tu et al., “Identification of gastric cancer stem cells using the cell surface marker CD44,” Stem Cells, vol. 27, no. 5, pp. 1006–1020, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. H. Kodama, S. Murata, M. Ishida et al., “Prognostic impact of CD44-positive cancer stem-like cells at the invasive front of gastric cancer,” British Journal of Cancer, vol. 116, no. 2, pp. 186–194, 2017. View at Publisher · View at Google Scholar · View at Scopus