Helicobacter pylori Activates IL-6-STAT3 Signaling in Human Gastric Cancer Cells: Potential Roles for Reactive Oxygen Species

Helicobacter

Volumn 21, Issue 5, 2016, Pages 405-416

  Piao, Juan Yu ^a   Lee, Hee Geum ^a   Kim, Su Jung ^a,b   Kim, Do Hee ^a   Han, Hyeong jun ^a   Ngo, Hoang Kieu Chi ^a   Park, Sin Aye ^a   Woo, Jeong Hwa ^c   Lee, Jeong Sang ^d   Na, Hye Kyung ^c   Cha, Young Nam ^e   Surh, Young Joon ^a,b  

^a Seoul National University   (South Korea)

^b Seoul National University   (South Korea)

^c Sungshin Women's University   (South Korea)

^d Jeonju University   (South Korea)

^e Inha University School of Medicine   (South Korea)

Author keywords

gastritis; Helicobacter pylori; interleukin 6; interleukin 6 receptor; reactive oxygen species; signal transducer and activator of transcription 3

Indexed keywords

INTERLEUKIN 11; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; MYC PROTEIN; REACTIVE OXYGEN METABOLITE; STAT3 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; GASTRIC CANCER CELL LINE; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STOMACH CANCER; STOMACH CARCINOGENESIS;

EID: 84986905075     PISSN: 10834389     EISSN: 15235378     Source Type: Journal    
DOI: 10.1111/hel.12298     Document Type: Article

References (37)

1. Herrera V, Parsonnet J. Helicobacter pylori and gastric adenocarcinoma. Clin Microbiol Infect 2009;15:971–6.
2. Peek RM Jr, Crabtree JE. Helicobacter infection and gastric neoplasia. J Pathol 2006;208:233–48.
3. Polk DB, Peek RM Jr. Helicobacter pylori: gastric cancer and beyond. Nat Rev Cancer 2010;10:403–14.
4. Wroblewski LE, Peek RM Jr, Wilson KT. Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev 2010;23:713–39.
5. Parkin DM. The global health burden of infection-associated cancers in the year 2002. Int J Cancer 2006;118:3030–44.
6. Yu H, Jove R. The STATs of cancer–new molecular targets come of age. Nat Rev Cancer 2004;4:97–105.
7. Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer 2009;9:798–809.
8. Yu H, Lee H, Herrmann A, Buettner R, Jove R. Revisiting STAT3 signalling in cancer: new and unexpected biological functions. Nat Rev Cancer 2014;14:736–46.
9. Bishop JL, Thaper D, Zoubeidi A. The Multifaceted roles of STAT3 signaling in the progression of prostate cancer. Cancers 2014;6:829–59.
10. Masuda M, Wakasaki T, Suzui M, Toh S, Joe AK, Weinstein IB. Stat3 orchestrates tumor development and progression: the Achilles' heel of head and neck cancers? Curr Cancer Drug Targets 2010;10:117–26.
11. Bromberg J. Signal transducers and activators of transcription as regulators of growth, apoptosis and breast development. Breast Cancer Res 2000;2:86–90.
12. Klampfer L. The role of signal transducers and activators of transcription in colon cancer. Front Biosci 2008;13:2888–99.
13. Giraud AS, Menheniott TR, Judd LM. Targeting STAT3 in gastric cancer. Expert Opin Ther Targets 2012;16:889–901.
14. Judd LM, Alderman BM, Howlett M, Shulkes A, Dow C, Moverley J, Grail D, Jenkins BJ, Ernst M, Giraud AS. Gastric cancer development in mice lacking the SHP2 binding site on the IL-6 family co-receptor gp130. Gastroenterology 2004;126:196–207.
15. Judd LM, Bredin K, Kalantzis A, Jenkins BJ, Ernst M, Giraud AS. STAT3 activation regulates growth, inflammation, and vascularization in a mouse model of gastric tumorigenesis. Gastroenterology 2006;131:1073–85.
16. Zhao J, Dong Y, Kang W, Go MY, Tong JH, Ng EK, Chiu PW, Cheng AS, To KF, Sung JJ, Yu J. Helicobacter pylori-induced STAT3 activation and signalling network in gastric cancer. Oncoscience 2014;1:468–75.
17. Bronte-Tinkew DM, Terebiznik M, Franco A, Ang M, Ahn D, Mimuro H, Sasakawa C, Ropeleski MJ, Peek RM Jr, Jones NL. Helicobacter pylori cytotoxin-associated gene A activates the signal transducer and activator of transcription 3 pathway in vitro and in vivo. Cancer Res 2009;69:632–9.
18. Necula LG, Chivu-Economescu M, Stanciulescu EL, Bleotu C, Dima SO, Alexiu I, Dumitru A, Constantinescu G, Popescu I, Diaconu CC, IL-6 and IL-11 as markers for tumor aggressiveness and prognosis in gastric adenocarcinoma patients without mutations in Gp130 subunits. J Gastrointestin Liver Dis 2012;21:23–9.
19. Sugimoto M, Ohno T, Graham DY, Yamaoka Y. Helicobacter pylori outer membrane proteins on gastric mucosal interleukin 6 and 11 expression in Mongolian gerbils. J Gastroenterol Hepatol 2011;26:1677–84.
20. Liou GY, Storz P. Reactive oxygen species in cancer. Free Radical Res 2010;44:479–96.
21. Handa O, Naito Y, Yoshikawa T. Helicobacter pylori: a ROS-inducing bacterial species in the stomach. Inflamm Res 2010;59:997–1003.
22. Lee A, O'Rourke J, De Ungria MC, Robertson B, Daskalopoulos G, Dixon MF. A standardized mouse model of Helicobacter pylori infection: introducing the Sydney strain. Gastroenterology 1997;112:1386–97.
23. Sansone P, Bromberg J. Targeting the interleukin-6/Jak/stat pathway in human malignancies. J Clin Oncol 2012;30:1005–14.
24. Jove R. Preface: STAT signaling. Oncogene 2000;19:2466–7.
25. Xiong H, Du W, Wang JL, Wang YC, Tang JT, Hong J, Fang JY. Constitutive activation of STAT3 is predictive of poor prognosis in human gastric cancer. J Mol Med 2012;90:1037–46.
26. Lee KS, Kalantzis A, Jackson CB, O'Connor L, Murata-Kamiya N, Hatakeyama M, Judd LM, Giraud AS, Menheniott TR. Helicobacter pylori CagA triggers expression of the bactericidal lectin REG3gamma via gastric STAT3 activation. PLoS ONE 2012;7:e30786.
27. Ernst M, Najdovska M, Grail D, et al. STAT3 and STAT1 mediate IL-11-dependent and inflammation-associated gastric tumorigenesis in gp130 receptor mutant mice. J Clin Invest 2008;118:1727–38.
28. Howlett M, Giraud AS, Lescesen H, Jackson CB, Kalantzis A, Van Driel IR, et al. The interleukin-6 family cytokine interleukin-11 regulates homeostatic epithelial cell turnover and promotes gastric tumor development. Gastroenterology 2009;136:967–77.
29. Jackson CB, Judd LM, Menheniott TR, et al. Augmented gp130-mediated cytokine signalling accompanies human gastric cancer progression. J Pathol 2007;213:140–51.
30. Handa O, Naito Y, Yoshikawa T. Redox biology and gastric carcinogenesis: the role of Helicobacter pylori. Redox Rep 2011;16:1–7.
31. Ding SZ, Minohara Y, Fan XJ, Wang J, Reyes VE, Patel J, Dirden-Kramer B, Boldoqh I, Ernst PB, Crowe SE. Helicobacter pylori infection induces oxidative stress and programmed cell death in human gastric epithelial cells. Infect Immun 2007;75:4030–9.
32. Calvino-Fernandez M, Benito-Martinez S, Parra-Cid T. Oxidative stress by Helicobacter pylori causes apoptosis through mitochondrial pathway in gastric epithelial cells. Apoptosis 2008;13:1267–80.
33. Qu Y, Oyan AM, Liu R, et al. Generation of prostate tumor-initiating cells is associated with elevation of reactive oxygen species and IL-6/STAT3 signaling. Cancer Res 2013;73:7090–100.
34. Facchini LM, Penn LZ. The molecular role of Myc in growth and transformation: recent discoveries lead to new insights. FASEB J 1998;12:633–51.
35. Shibuya M, Yokota J, Ueyama Y. Amplification and expression of a cellular oncogene (c-myc) in human gastric adenocarcinoma cells. Mol Cell Biol 1985;5:414–8.
36. Zhu Y, Shu X, Chen J, Xie Y, Xu P, Huang DQ, Lu NH. Effect of Helicobacter pylori eradication on oncogenes and cell proliferation. Eur J Clin Invest 2008;38:628–33.
37. Hayashi Y, Tsujii M, Wang J, et al. CagA mediates epigenetic regulation to attenuate let-7 expression in Helicobacter pylori-related carcinogenesis. Gut 2013;62:1536–46.