MicroRNA-27b suppresses Helicobacter pylori-induced gastric tumorigenesis through negatively regulating Frizzled7

Oncology Reports

Volumn 35, Issue 4, 2016, Pages 2441-2450

  Geng, Yan ^a   Lu, Xiaolan ^b   Wu, Xiaokang ^a   Xue, Li ^a   Wang, Xiangling ^a   Xu, Jiru ^b  

^a Departments of Laboratory   (China)

^b XI'AN JIAOTONG UNIVERSITY   (China)

Author keywords

Frizzled7; Gastric cancer; Helicobacter pylori; MiR 27b

Indexed keywords

FRIZZLED 7 PROTEIN; FRIZZLED PROTEIN; MICRORNA; MICRORNA 27B; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; FZD7 PROTEIN, HUMAN; MIRN27 MICRORNA, HUMAN;

3' UNTRANSLATED REGION; ARTICLE; CELL ACTIVATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; GASTRIC CANCER CELL LINE; GENE OVEREXPRESSION; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STOMACH CANCER; STOMACH CARCINOGENESIS; UPREGULATION; WNT SIGNALING PATHWAY; CARCINOGENESIS; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; METABOLISM; PATHOGENICITY; PATHOLOGY; STOMACH TUMOR; TUMOR CELL LINE;

3' UNTRANSLATED REGIONS; CARCINOGENESIS; CELL LINE, TUMOR; CELL PROLIFERATION; FRIZZLED RECEPTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; MICRORNAS; STOMACH NEOPLASMS; WNT SIGNALING PATHWAY;

EID: 84959276566     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or.2016.4572     Document Type: Article

References (54)

1. Siegel RL, Miller KD and Jemal A: Cancer statistics, 2015. CA Cancer J Clin 65: 5-29, 2015.
2. Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, Taniyama K, Sasaki N and Schlemper RJ: Helicobacter pylori infection and the development of gastric cancer. N Engl J Med 345: 784-789, 2001.
3. Wu WK, Cho CH, Lee CW, Fan D, Wu K, Yu J and Sung JJ: Dysregulation of cellular signaling in gastric cancer. Cancer Lett 295: 144-153, 2010.
4. Shen J, Xiao Z, Wu WK, Wang MH, To KF, Chen Y, Yang W, Li MS, Shin VY, Tong JH, et al: Epigenetic silencing of miR?490-3p reactivates the chromatin remodeler SMARCD1 to promote Helicobacter pylori-induced gastric carcinogenesis. Cancer Res 75: 754-765, 2015.
5. Fukase K, Kato M, Kikuchi S, Inoue K, Uemura N, Okamoto S, Terao S, Amagai K, Hayashi S and Asaka M; Japan Gast Study Group: Effect of eradication of Helicobacter pylori on incidence of metachronous gastric carcinoma after endoscopic resection of early gastric cancer: An open-label, randomised controlled trial. Lancet 372: 392-397, 2008.
6. Yong X, Tang B, Li BS, Xie R, Hu CJ, Luo G, Qin Y, Dong H and Yang SM: Helicobacter pylori virulence factor CagA promotes tumorigenesis of gastric cancer via multiple signaling pathways. Cell Commun Signal 13: 30, 2015.
7. Hayashi T, Senda M, Morohashi H, Higashi H, Horio M, Kashiba Y, Nagase L, Sasaya D, Shimizu T, Venugopalan N, et al: Tertiary structure-function analysis reveals the pathogenic signaling potentiation mechanism of Helicobacter pylori oncogenic effector CagA. Cell Host Microbe 12: 20-33, 2012.
8. Ohnishi N, Yuasa H, Tanaka S, Sawa H, Miura M, Matsui A, Higashi H, Musashi M, Iwabuchi K, Suzuki M, et al: Transgenic expression of Helicobacter pylori CagA induces gastrointestinal and hematopoietic neoplasms in mouse. Proc Natl Acad Sci USA 105: 1003-1008, 2008.
9. Suzuki M, Mimuro H, Kiga K, Fukumatsu M, Ishijima N, Morikawa H, Nagai S, Koyasu S, Gilman RH, Kersulyte D, et al: Helicobacter pylori CagA phosphorylation-independent function in epithelial proliferation and inflammation. Cell Host Microbe 5: 23-34, 2009.
10. Tabassam FH, Graham DY and Yamaoka Y: Helicobacter pylori activate epidermal growth factor receptor-and phosphatidylinositol 3-OH kinase-dependent Akt and glycogen synthase kinase 3beta phosphorylation. Cell Microbiol 11: 70-82, 2009.
11. Sokolova O, Vieth M, Gnad T, Bozko PM and Naumann M: Helicobacter pylori promotes eukaryotic protein translation by activating phosphatidylinositol 3 kinase/mTOR. Int J Biochem Cell Biol 55: 157-163, 2014.
12. Franco AT, Israel DA, Washington MK, Krishna U, Fox JG, Rogers AB, Neish AS, Collier-Hyams L, Perez-Perez GI, Hatakeyama M, et al: Activation of beta-catenin by carcinogenic Helicobacter pylori. Proc Natl Acad Sci USA 102: 10646-10651, 2005.
13. Bronte-Tinkew DM, Terebiznik M, Franco A, Ang M, Ahn D, Mimuro H, Sasakawa C, Ropeleski MJ, Peek RM Jr and 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 69: 632-639, 2009.
14. Wei J, Noto J, Zaika E, Romero-Gallo J, Correa P, El-Rifai W, Peek RM and Zaika A: Pathogenic bacterium Helicobacter pylori alters the expression profile of p53 protein isoforms and p53 response to cellular stresses. Proc Natl Acad Sci USA 109: E2543-E2550, 2012.
15. Wei J, Noto JM, Zaika E, Romero-Gallo J, Piazuelo MB, Schneider B, El-Rifai W, Correa P, Peek RM and Zaika AI: Bacterial CagA protein induces degradation of p53 protein in a p14ARF-dependent manner. Gut 64: 1040-1048, 2015.
16. Abu-Elmagd M, Garcia-Morales C and Wheeler GN: Frizzled7 mediates canonical Wnt signaling in neural crest induction. Dev Biol 298: 285-298, 2006.
17. Asad M, Wong MK, Tan TZ, Choolani M, Low J, Mori S, Virshup D, Thiery JP and Huang RY: FZD7 drives in vitro aggressiveness in Stem-A subtype of ovarian cancer via regulation of non-canonical Wnt/PCP pathway. Cell Death Dis 5: e1346, 2014.
18. Xu R Zeng S, Xie W, Sun C, Chen YL, Chen MJ and Zhang L: The expression and function of Frizzled-7 in human renal cell carcinoma. Clin Transl Oncol: Aug 5, 2015 (Epub ahead of print). http://dx.doi.org/10.1007/s12094-015-1362-3.
19. Deng B, Zhang S, Miao Y, Zhang Y, Wen F and Guo K: Down?regulation of Frizzled-7 expression inhibits migration, invasion, and epithelial-mesenchymal transition of cervical cancer cell lines. Med Oncol 32: 102, 2015.
20. Simmons GE Jr, Pandey S, Nedeljkovic-Kurepa A, Saxena M, Wang A and Pruitt K: Frizzled 7 expression is positively regulated by SIRT1 and catenin in breast cancer cells. PLoS One 9: e98861, 2014.
21. Ueno K, Hazama S, Mitomori S, Nishioka M, Suehiro Y, Hirata H, Oka M, Imai K, Dahiya R and Hinoda Y: Down?regulation of frizzled-7 expression decreases survival, invasion and metastatic capabilities of colon cancer cells. Br J Cancer 101: 1374-1381, 2009.
22. Merle P, Kim M, Herrmann M, Gupte A, Lefrançois L, Califano S, Trépo C, Tanaka S, Vitvitski L, de la Monte S, et al: Oncogenic role of the frizzled-7/beta-catenin pathway in hepatocellular carcinoma. J Hepatol 43: 854-862, 2005.
23. White BD, Chien AJ and Dawson DW: Dysregulation of Wnt/catenin signaling in gastrointestinal cancers. Gastroenterology 142: 219-232, 2012.
24. Bartel DP: MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116: 281-297, 2004.
25. Winter J, Jung S, Keller S, Gregory RI and Diederichs S: Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 11: 228-234, 2009.
26. Dalmay T and Edwards DR: MicroRNAs and the hallmarks of cancer. Oncogene 25: 6170-6175, 2006.
27. Esquela-Kerscher A and Slack FJ: Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer 6: 259-269, 2006.
28. Chiyomaru T, Seki N, Inoguchi S, Ishihara T, Mataki H, Matsushita R, Goto Y, Nishikawa R, Tatarano S, Itesako T, et al: Dual regulation of receptor tyrosine kinase genes EGFR and c-Met by the tumor-suppressive microRNA-23b/27b cluster in bladder cancer. Int J Oncol 46: 487-496, 2015.
29. Jiang J, Lv X, Fan L, Huang G, Zhan Y, Wang M and Lu H: MicroRNA-27b suppresses growth and invasion of NSCLC cells by targeting Sp1. Tumour Biol 35: 10019-10023, 2014.
30. Jiang C, Chen X, Alattar M, Wei J and Liu H: MicroRNAs in tumorigenesis, metastasis, diagnosis and prognosis of gastric cancer. Cancer Gene Ther 22: 291-301, 2015.
31. Hatakeyama M: Oncogenic mechanisms of the Helicobacter pylori CagA protein. Nat Rev Cancer 4: 688-694, 2004.
32. Merle P, de la Monte S, Kim M, Herrmann M, Tanaka S, Von Dem Bussche A, Kew MC, Trepo C and Wands JR: Functional consequences of frizzled-7 receptor overexpression in human hepatocellular carcinoma. Gastroenterology 127: 1110-1122, 2004.
33. Kim M, Lee HC, Tsedensodnom O, Hartley R, Lim YS, Yu E, Merle P and Wands JR: Functional interaction between Wnt3 and Frizzled-7 leads to activation of the Wnt/beta-catenin signaling pathway in hepatocellular carcinoma cells. J Hepatol 48: 780-791, 2008.
34. Nambotin SB, Lefrancois L, Sainsily X, Berthillon P, Kim M, Wands JR, Chevallier M, Jalinot P, Scoazec JY, Trepo C, et al: Pharmacological inhibition of Frizzled-7 displays anti-tumor properties in hepatocellular carcinoma. J Hepatol 54: 288-299, 2011.
35. Ueno K, Hiura M, Suehiro Y, Hazama S, Hirata H, Oka M, Imai K, Dahiya R and Hinoda Y: Frizzled-7 as a potential therapeutic target in colorectal cancer. Neoplasia 10: 697-705, 2008.
36. Yang L, Wu X, Wang Y, Zhang K, Wu J, Yuan YC, Deng X, Chen L, Kim CC, Lau S, et al: FZD7 has a critical role in cell proliferation in triple negative breast cancer. Oncogene 30: 4437-4446, 2011.
37. Kirikoshi H, Sekihara H and Katoh M: Up-regulation of Frizzled-7 (FZD7) in human gastric cancer. Int J Oncol 19: 111-115, 2001.
38. Schmuck R, Warneke V, Behrens HM, Simon E, Weichert W and Röcken C: Genotypic and phenotypic characterization of side population of gastric cancer cell lines. Am J Pathol 178: 1792-1804, 2011.
39. King TD, Zhang W, Suto MJ and Li Y: Frizzled7 as an emerging target for cancer therapy. Cell Signal 24: 846-851, 2012.
40. Zhang H, Hao Y, Yang J, Zhou Y, Li J, Yin S, Sun C, Ma M, Huang Y and Xi JJ: Genome-wide functional screening of miR-23b as a pleiotropic modulator suppressing cancer metastasis. Nat Commun 2: 554, 2011.
41. Chen Z, Ma T, Huang C, Zhang L, Lv X, Xu T, Hu T and Li J: miR-27a modulates the MDR1/P-glycoprotein expression by inhibiting FZD7/catenin pathway in hepatocellular carcinoma cells. Cell Signal 25: 2693-2701, 2013.
42. Song J, Gao L, Yang G, Tang S, Xie H, Wang Y, Wang J, Zhang Y, Jin J, Gou Y, et al: miR-199a regulates cell proliferation and survival by targeting FZD7. PLoS One 9: e110074, 2014.
43. Deng B, Zhang Y, Zhang S, Wen F, Miao Y and Guo K: MicroRNA-142-3p inhibits cell proliferation and invasion of cervical cancer cells by targeting FZD7. Tumour Biol 36: 8065-8073, 2015.
44. Li Z, Chen P, Su R, Li Y, Hu C, Wang Y, Arnovitz S, He M, Gurbuxani S, Zuo Z, et al: Overexpression and knockout of miR-126 both promote leukemogenesis. Blood 126: 2005-2015, 2015.
45. Ye J, Wu X, Wu D, Wu P, Ni C, Zhang Z, Chen Z, Qiu F, Xu J and Huang J: miRNA-27b targets vascular endothelial growth factor C to inhibit tumor progression and angiogenesis in colorectal cancer. PLoS One 8: e60687, 2013.
46. Wan L, Zhang L, Fan K and Wang J: miR-27b targets LIMK1 to inhibit growth and invasion of NSCLC cells. Mol Cell Biochem 390: 85-91, 2014.
47. Wang B, Li D, Kovalchuk A, Litvinov D and Kovalchuk O: Ionizing radiation-inducible miR-27b suppresses leukemia proliferation via targeting cyclin A2. Int J Radiat Oncol Biol Phys 90: 53-62, 2014.
48. Takahashi RU, Miyazaki H, Takeshita F, Yamamoto Y, Minoura K, Ono M, Kodaira M, Tamura K, Mori M and Ochiya T: Loss of microRNA-27b contributes to breast cancer stem cell generation by activating ENPP1. Nat Commun 6: 7318, 2015.
49. Goto Y, Kojima S, Nishikawa R, Enokida H, Chiyomaru T, Kinoshita T, Nakagawa M, Naya Y, Ichikawa T and Seki N: The microRNA-23b/27b/24-1 cluster is a disease progression marker and tumor suppressor in prostate cancer. Oncotarget 5: 7748-7759, 2014.
50. Mu W, Hu C, Zhang H, Qu Z, Cen J, Qiu Z, Li C, Ren H, Li Y, He X, et al: miR-27b synergizes with anticancer drugs via p53 activation and CYP1B1 suppression. Cell Res 25: 477-495, 2015.
51. Veliceasa D, Biyashev D, Qin G, Misener S, Mackie AR, Kishore R and Volpert OV: Therapeutic manipulation of angiogenesis with miR-27b. Vasc Cell 7: 6, 2015.
52. Wang YW, Chen X, Gao JW, Zhang H, Ma RR, Gao ZH and Gao P: High expression of cAMP-responsive element-binDing protein 1 (CREB1) is associated with metastasis, tumor stage and poor outcome in gastric cancer. Oncotarget 6: 10646-10657, 2015.
53. Sokolova O, Bozko PM and Naumann M: Helicobacter pylori suppresses glycogen synthase kinase 3beta to promote beta?catenin activity. J Biol Chem 283: 29367-29374, 2008.
54. Gnad T, Feoktistova M, Leverkus M, Lendeckel U and Naumann M: Helicobacter pylori-induced activation of beta?catenin involves low density lipoprotein receptor-related protein 6 and Dishevelled. Mol Cancer 9: 31, 2010.