Journal of Gastric Cancer

The Korean Gastric Cancer Association (대한위암학회)
권호 표지
DOI QR코드

DOI QR Code

Dysregulation of MicroRNA-196b-5p and MicroRNA-375 in Gastric Cancer

  • Lee, Seung Woo (Division of Gastroenterology, Department of Internal Medicine, Daejeon St. Mary's Hospital, School of Medicine, The Catholic University of Korea) ;
  • Park, Ki Cheol (Clinical Research Institute, Daejeon St. Mary's Hospital, School of Medicine, The Catholic University of Korea) ;
  • Kim, Jeong Goo (Department of General Surgery, Daejeon St. Mary's Hospital, School of Medicine, The Catholic University of Korea) ;
  • Moon, Sung Jin (Division of Gastroenterology, Department of Internal Medicine, Daejeon St. Mary's Hospital, School of Medicine, The Catholic University of Korea) ;
  • Kang, Sang Bum (Division of Gastroenterology, Department of Internal Medicine, Daejeon St. Mary's Hospital, School of Medicine, The Catholic University of Korea) ;
  • Lee, Dong Soo (Division of Gastroenterology, Department of Internal Medicine, Daejeon St. Mary's Hospital, School of Medicine, The Catholic University of Korea) ;
  • Sul, Hae Joung (Department of Pathology, Daejeon St. Mary's Hospital, School of Medicine, The Catholic University of Korea) ;
  • Ji, Jeong Seon (Division of Gastroenterology, Department of Internal Medicine, Incheon St. Mary's Hospital, School of Medicine, The Catholic University of Korea) ;
  • Jeong, Hyun Yong (Department of Internal Medicine, Chungnam National University School of Medicine)
  • Received : 2016.07.29
  • Accepted : 2016.09.22
  • Published : 2016.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Purpose: Dysregulated microRNAs (miRNAs) can contribute to cancer development by leading to abnormal proliferation of cells, apoptosis, and differentiation. Although several miRNAs that are related to gastric cancer have been identified, the reported results have been inconsistent. The aim of this study was to determine miRNA expression profiles and validate miRNAs up- and down-regulated in gastric cancer. Materials and Methods: We evaluated 34 primary gastric cancer tissues and paired adjacent nontumorous gastric tissues. Total RNA was extracted, and low-molecular-weight RNAs (<200 nucleotides) were isolated for further analysis. Two pairs of tissues were processed for GeneChip microarray analysis, and the identified up- and down-regulated miRNAs were validated by real-time quantitative polymerase chain reaction (qPCR). Results: In the set of differentially expressed miRNAs, 5 were overexpressed by more than 2 fold, and 5 were reduced by 2 fold or less in gastric cancer tissues compared with normal gastric tissues. Four of these miRNAs (miR-196b-5p, miR-375, miR-483-5p, and miR-486-5p) were then validated by qPCR, and the relative expression levels of 2 miRNAs (miR-196b-5p and miR-375) were significantly different between cancer and normal tissues. Conclusions: Our results revealed that the expression of miR-196b-5p and miR-375 significantly correlates with gastric cancer. These miRNAs could therefore serve as diagnostic biomarkers of gastric cancer.

Keywords

References

  1. Danaei G, Vander Hoorn S, Lopez AD, Murray CJ, Ezzati M; Comparative Risk Assessment collaborating group (Cancers). Causes of cancer in the world: comparative risk assessment of nine behavioural and environmental risk factors. Lancet 2005;366:1784-1793. https://doi.org/10.1016/S0140-6736(05)67725-2
  2. Jung KW, Park S, Kong HJ, Won YJ, Lee JY, Seo HG, et al. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2009. Cancer Res Treat 2012;44:11-24. https://doi.org/10.4143/crt.2012.44.1.11
  3. Hartgrink HH, Jansen EP, van Grieken NC, van de Velde CJ. Gastric cancer. Lancet 2009;374:477-490. https://doi.org/10.1016/S0140-6736(09)60617-6
  4. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer 2006;6:857-866. https://doi.org/10.1038/nrc1997
  5. Iorio MV, Croce CM. MicroRNAs in cancer: small molecules with a huge impact. J Clin Oncol 2009;27:5848-5856. https://doi.org/10.1200/JCO.2009.24.0317
  6. Link A, Kupcinskas J, Wex T, Malfertheiner P. Macro-role of microRNA in gastric cancer. Dig Dis 2012;30:255-267. https://doi.org/10.1159/000336919
  7. Edge SB, Compton CC. The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol 2010;17:1471-1474. https://doi.org/10.1245/s10434-010-0985-4
  8. Melo S, Villanueva A, Moutinho C, Davalos V, Spizzo R, Ivan C, et al. Small molecule enoxacin is a cancer-specific growth inhibitor that acts by enhancing TAR RNA-binding protein 2-mediated microRNA processing. Proc Natl Acad Sci U S A 2011;108:4394-4399. https://doi.org/10.1073/pnas.1014720108
  9. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A 2006;103:2257-2261. https://doi.org/10.1073/pnas.0510565103
  10. Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S, et al. MicroRNA gene expression deregulation in human breast cancer. Cancer Res 2005;65:7065-7070. https://doi.org/10.1158/0008-5472.CAN-05-1783
  11. Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, Yi M, et al. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 2006;9:189-198. https://doi.org/10.1016/j.ccr.2006.01.025
  12. Bloomston M, Frankel WL, Petrocca F, Volinia S, Alder H, Hagan JP, et al. MicroRNA expression patterns to differentiate pancreatic adenocarcinoma from normal pancreas and chronic pancreatitis. JAMA 2007;297:1901-1908. https://doi.org/10.1001/jama.297.17.1901
  13. Wang F, Sun GP, Zou YF, Hao JQ, Zhong F, Ren WJ. Micro-RNAs as promising biomarkers for gastric cancer. Cancer Biomark 2012;11:259-267. https://doi.org/10.3233/CBM-2012-00284
  14. Li T, Lu YY, Zhao XD, Guo HQ, Liu CH, Li H, et al. MicroRNA-296-5p increases proliferation in gastric cancer through repression of Caudal-related homeobox 1. Oncogene 2014;33:783-793. https://doi.org/10.1038/onc.2012.637
  15. Li X, Zhang Y, Zhang H, Liu X, Gong T, Li M, et al. miRNA-223 promotes gastric cancer invasion and metastasis by targeting tumor suppressor EPB41L3. Mol Cancer Res 2011;9:824-833. https://doi.org/10.1158/1541-7786.MCR-10-0529
  16. Li X, Zhang Y, Zhang Y, Ding J, Wu K, Fan D. Survival prediction of gastric cancer by a seven-microRNA signature. Gut 2010;59:579-585. https://doi.org/10.1136/gut.2008.175497
  17. Tsujiura M, Komatsu S, Ichikawa D, Shiozaki A, Konishi H, Takeshita H, et al. Circulating miR-18a in plasma contributes to cancer detection and monitoring in patients with gastric cancer. Gastric Cancer 2015;18:271-279. https://doi.org/10.1007/s10120-014-0363-1
  18. Tsujiura M, Ichikawa D, Komatsu S, Shiozaki A, Takeshita H, Kosuga T, et al. Circulating microRNAs in plasma of patients with gastric cancers. Br J Cancer 2010;102:1174-1179. https://doi.org/10.1038/sj.bjc.6605608
  19. Zeng Z, Wang J, Zhao L, Hu P, Zhang H, Tang X, et al. Potential role of microRNA-21 in the diagnosis of gastric cancer: a meta-analysis. PLoS One 2013;8:e73278. https://doi.org/10.1371/journal.pone.0073278
  20. McGlinn E, Yekta S, Mansfield JH, Soutschek J, Bartel DP, Tabin CJ. In ovo application of antagomiRs indicates a role for miR-196 in patterning the chick axial skeleton through Hox gene regulation. Proc Natl Acad Sci U S A 2009;106:18610-18615. https://doi.org/10.1073/pnas.0910374106
  21. Chen C, Zhang Y, Zhang L, Weakley SM, Yao Q. MicroRNA-196: critical roles and clinical applications in development and cancer. J Cell Mol Med 2011;15:14-23. https://doi.org/10.1111/j.1582-4934.2010.01219.x
  22. Hui AB, Shi W, Boutros PC, Miller N, Pintilie M, Fyles T, et al. Robust global micro-RNA profiling with formalin-fixed paraffin-embedded breast cancer tissues. Lab Invest 2009;89:597-606. https://doi.org/10.1038/labinvest.2009.12
  23. Zhang Y, Li M, Wang H, Fisher WE, Lin PH, Yao Q, et al. Profiling of 95 microRNAs in pancreatic cancer cell lines and surgical specimens by real-time PCR analysis. World J Surg 2009;33:698-709. https://doi.org/10.1007/s00268-008-9833-0
  24. Schotte D, Chau JC, Sylvester G, Liu G, Chen C, van der Velden VH, et al. Identification of new microRNA genes and aberrant microRNA profiles in childhood acute lymphoblastic leukemia. Leukemia 2009;23:313-322. https://doi.org/10.1038/leu.2008.286
  25. Maru DM, Singh RR, Hannah C, Albarracin CT, Li YX, Abraham R, et al. MicroRNA-196a is a potential marker of progression during Barrett's metaplasia-dysplasia-invasive adenocarcinoma sequence in esophagus. Am J Pathol 2009;174:1940-1948. https://doi.org/10.2353/ajpath.2009.080718
  26. Schimanski CC, Frerichs K, Rahman F, Berger M, Lang H, Galle PR, et al. High miR-196a levels promote the oncogenic phenotype of colorectal cancer cells. World J Gastroenterol 2009;15:2089-2096. https://doi.org/10.3748/wjg.15.2089
  27. Braig S, Mueller DW, Rothhammer T, Bosserhoff AK. MicroRNA miR-196a is a central regulator of HOX-B7 and BMP4 expression in malignant melanoma. Cell Mol Life Sci 2010;67:3535-3548. https://doi.org/10.1007/s00018-010-0394-7
  28. Tsai KW, Hu LY, Wu CW, Li SC, Lai CH, Kao HW, et al. Epigenetic regulation of miR-196b expression in gastric cancer. Genes Chromosomes Cancer 2010;49:969-980. https://doi.org/10.1002/gcc.20804
  29. Liao YL, Hu LY, Tsai KW, Wu CW, Chan WC, Li SC, et al. Transcriptional regulation of miR-196b by ETS2 in gastric cancer cells. Carcinogenesis 2012;33:760-769. https://doi.org/10.1093/carcin/bgs023
  30. Sun M, Liu XH, Li JH, Yang JS, Zhang EB, Yin DD, et al. MiR-196a is upregulated in gastric cancer and promotes cell proliferation by downregulating p27(kip1). Mol Cancer Ther 2012;11:842-852. https://doi.org/10.1158/1535-7163.MCT-11-1015
  31. Tsai MM, Wang CS, Tsai CY, Chen CY, Chi HC, Tseng YH, et al. MicroRNA-196a/-196b promote cell metastasis via negative regulation of radixin in human gastric cancer. Cancer Lett 2014;351:222-231. https://doi.org/10.1016/j.canlet.2014.06.004
  32. Xie J, Tan ZH, Tang X, Mo MS, Liu YP, Gan RL, et al. MiR-374b-5p suppresses RECK expression and promotes gastric cancer cell invasion and metastasis. World J Gastroenterol 2014;20:17439-17447. https://doi.org/10.3748/wjg.v20.i46.17439
  33. Liu J, Ma L, Wang Z, Wang L, Liu C, Chen R, et al. MicroRNA expression profile of gastric cancer stem cells in the MKN-45 cancer cell line. Acta Biochim Biophys Sin (Shanghai) 2014;46:92-99. https://doi.org/10.1093/abbs/gmt135
  34. Chang H, Kim N, Park JH, Nam RH, Choi YJ, Lee HS, et al. Different microRNA expression levels in gastric cancer depending on Helicobacter pylori infection. Gut Liver 2015;9:188-196. https://doi.org/10.5009/gnl13371
  35. Poy MN, Eliasson L, Krutzfeldt J, Kuwajima S, Ma X, Macdonald PE, et al. A pancreatic islet-specific microRNA regulates insulin secretion. Nature 2004;432:226-230. https://doi.org/10.1038/nature03076
  36. Kloosterman WP, Lagendijk AK, Ketting RF, Moulton JD, Plasterk RH. Targeted inhibition of miRNA maturation with morpholinos reveals a role for miR-375 in pancreatic islet development. PLoS Biol 2007;5:e203. https://doi.org/10.1371/journal.pbio.0050203
  37. Yan JW, Lin JS, He XX. The emerging role of miR-375 in cancer. Int J Cancer 2014;135:1011-1018. https://doi.org/10.1002/ijc.28563
  38. Ding L, Xu Y, Zhang W, Deng Y, Si M, Du Y, et al. MiR-375 frequently downregulated in gastric cancer inhibits cell proliferation by targeting JAK2. Cell Res 2010;20:784-793. https://doi.org/10.1038/cr.2010.79
  39. Tsukamoto Y, Nakada C, Noguchi T, Tanigawa M, Nguyen LT, Uchida T, et al. MicroRNA-375 is downregulated in gastric carcinomas and regulates cell survival by targeting PDK1 and 14-3-3zeta. Cancer Res 2010;70:2339-2349. https://doi.org/10.1158/0008-5472.CAN-09-2777
  40. Miao L, Liu K, Xie M, Xing Y, Xi T. miR-375 inhibits Helicobacter pylori-induced gastric carcinogenesis by blocking JAK2-STAT3 signaling. Cancer Immunol Immunother 2014;63:699-711. https://doi.org/10.1007/s00262-014-1550-y
  41. Zhang X, Yan Z, Zhang J, Gong L, Li W, Cui J, et al. Combination of hsa-miR-375 and hsa-miR-142-5p as a predictor for recurrence risk in gastric cancer patients following surgical resection. Ann Oncol 2011;22:2257-2266. https://doi.org/10.1093/annonc/mdq758
  42. Wang L, Shi M, Hou S, Ding B, Liu L, Ji X, et al. MiR-483-5p suppresses the proliferation of glioma cells via directly targeting ERK1. FEBS Lett 2012;586:1312-1327. https://doi.org/10.1016/j.febslet.2012.03.035
  43. Qiao Y, Ma N, Wang X, Hui Y, Li F, Xiang Y, et al. MiR-483-5p controls angiogenesis in vitro and targets serum response factor. FEBS Lett 2011;585:3095-3100. https://doi.org/10.1016/j.febslet.2011.08.039
  44. Shen J, Wang A, Wang Q, Gurvich I, Siegel AB, Remotti H, et al. Exploration of genome-wide circulating microRNA in hepatocellular carcinoma: MiR-483-5p as a potential biomarker. Cancer Epidemiol Biomarkers Prev 2013;22:2364-2373. https://doi.org/10.1158/1055-9965.EPI-13-0237
  45. Oh HK, Tan AL, Das K, Ooi CH, Deng NT, Tan IB, et al. Genomic loss of miR-486 regulates tumor progression and the OLFM4 antiapoptotic factor in gastric cancer. Clin Cancer Res 2011;17:2657-2667. https://doi.org/10.1158/1078-0432.CCR-10-3152
  46. Solomides CC, Evans BJ, Navenot JM, Vadigepalli R, Peiper SC, Wang ZX. MicroRNA profiling in lung cancer reveals new molecular markers for diagnosis. Acta Cytol 2012;56:645-654. https://doi.org/10.1159/000343473
  47. Tan X, Qin W, Zhang L, Hang J, Li B, Zhang C, et al. A 5-micro RNA signature for lung squamous cell carcinoma diagnosis and hsa-miR-31 for prognosis. Clin Cancer Res 2011;17:6802-6811. https://doi.org/10.1158/1078-0432.CCR-11-0419
  48. Zhu C, Ren C, Han J, Ding Y, Du J, Dai N, et al. A five-microRNA panel in plasma was identified as potential biomarker for early detection of gastric cancer. Br J Cancer 2014;110:2291-2299. https://doi.org/10.1038/bjc.2014.119
  49. Wang J, Wang Q, Liu H, Hu B, Zhou W, Cheng Y. MicroRNA expression and its implication for the diagnosis and therapeutic strategies of gastric cancer. Cancer Lett 2010;297:137-143. https://doi.org/10.1016/j.canlet.2010.07.018

Cited by

  1. MicroRNA-342 inhibits the progression of glioma by directly targeting PAK4 vol.38, pp.2, 2016, https://doi.org/10.3892/or.2017.5783
  2. MicroRNA-326 inhibits cell proliferation and invasion, activating apoptosis in hepatocellular carcinoma by directly targeting LIM and SH3 protein 1 vol.38, pp.3, 2017, https://doi.org/10.3892/or.2017.5810
  3. Methylation of the HOXA10 Promoter Directs miR-196b-5p-Dependent Cell Proliferation and Invasion of Gastric Cancer Cells vol.16, pp.4, 2016, https://doi.org/10.1158/1541-7786.mcr-17-0655
  4. Prognostic impact of miR-196a/b expression in adult acute myeloid leukaemia: a single-centre, retrospective cohort study vol.46, pp.9, 2016, https://doi.org/10.1177/0300060518777399
  5. Cigarette smoke and chewing tobacco alter expression of different sets of miRNAs in oral keratinocytes vol.8, pp.None, 2016, https://doi.org/10.1038/s41598-018-25498-2
  6. MicroRNAs expression profiles as diagnostic biomarkers of gastric cancer: a systematic literature review vol.24, pp.2, 2016, https://doi.org/10.1080/1354750x.2018.1539765
  7. High Expression of miR-196b Predicts Poor Prognosis in Patients with Ovarian Cancer vol.13, pp.None, 2016, https://doi.org/10.2147/ott.s254942
  8. Long noncoding RNA LINC00629 restrains the progression of gastric cancer by upregulating AQP4 through competitively binding to miR‐196b‐5p vol.235, pp.3, 2016, https://doi.org/10.1002/jcp.29203
  9. RP5-1120P11.3 promotes hepatocellular carcinoma development via the miR-196b-5p-WIPF2 axis vol.98, pp.2, 2016, https://doi.org/10.1139/bcb-2019-0053
  10. miR‐196b‐5p controls adipocyte differentiation and lipogenesis through regulating mTORC1 and TGF‐β signaling vol.34, pp.7, 2016, https://doi.org/10.1096/fj.201901562rr
  11. MicroRNA -196b is related to the overall survival of patients with esophageal squamous cell carcinoma and facilitates tumor progression by regulating SOCS2 (Suppressor Of Cytokine Signaling 2) vol.12, pp.1, 2016, https://doi.org/10.1080/21655979.2021.1982329
  12. Helicobacter pylori induces gastric cancer via down‐regulating miR‐375 to inhibit dendritic cell maturation vol.26, pp.4, 2016, https://doi.org/10.1111/hel.12813