Long noncoding RNA H19-derived miR-675 enhances proliferation and invasion via RUNX1 in gastric cancer cells

Oncology Research

Volumn 23, Issue 3, 2016, Pages 99-107

  Liu, Gao ^a   Xiang, Tian ^a   Wu, Quan Feng ^a   Wang, Wei Xing ^a  

^a WUHAN UNIVERSITY   (China)

Author keywords

Akt mTOR pathway; Gastric cancer; H19; MiR 675; Runt domain transcription factor 1 (RUNX1)

Indexed keywords

LONG NONCODING RNA H19; LONG UNTRANSLATED RNA; TRANSCRIPTION FACTOR RUNX1; UNCLASSIFIED DRUG; H19 LONG NON-CODING RNA; MICRORNA; MIRN675 MICRORNA, HUMAN; MTOR PROTEIN, HUMAN; ONCOPROTEIN; RUNX1 PROTEIN, HUMAN; TARGET OF RAPAMYCIN KINASE;

ADULT; ARTICLE; CARCINOGENESIS; CELL INVASION; CELL PROLIFERATION; CLINICAL FEATURE; CONTROLLED STUDY; DISEASE COURSE; FEMALE; GASTRIC CANCER CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOMACH CANCER; AGED; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; LYMPH NODE METASTASIS; MIDDLE AGED; PATHOLOGY; SIGNAL TRANSDUCTION; STOMACH TUMOR; TUMOR CELL LINE; TUMOR INVASION;

ADULT; AGED; CARCINOGENESIS; CELL LINE, TUMOR; CELL PROLIFERATION; CORE BINDING FACTOR ALPHA 2 SUBUNIT; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LYMPHATIC METASTASIS; MALE; MICRORNAS; MIDDLE AGED; NEOPLASM INVASIVENESS; ONCOGENE PROTEIN V-AKT; RNA, LONG NONCODING; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS; TOR SERINE-THREONINE KINASES;

EID: 84959352152     PISSN: 09650407     EISSN: 15553906     Source Type: Journal    
DOI: 10.3727/096504015X14496932933575     Document Type: Article

References (49)

1. Ferlay, J.; Soerjomataram, I.; Dikshit, R.; Eser, S.; Mathers, C.; Rebelo, M.; Parkin, D. M.; Forman, D.; Bray, F. Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012. Int. J. Cancer 136(5):E359-386;2015.
2. Hartgrink, H. H.; Jansen, E. P.; van Grieken, N. C.; van de Velde, C. J. Gastric cancer. Lancet 374(9688):477-490;2009.
3. Chen, G.; Wang, Z.; Wang, D.; Qiu, C.; Liu, M.; Chen, X.; Zhang, Q.; Yan, G.; Cui, Q. LncRNADisease: A database for long-non-coding RNA-associated diseases. Nucleic Acids Res. 41(Database issue):D983-986;2013.
4. Lalevee, S.; Feil, R. Long noncoding RNAs in human disease: Emerging mechanisms and therapeutic strategies. Epigenomics 7(6):877-879;2015.
5. Ye, N.; Wang, B.; Quan, Z. F.; Cao, S. J.; Wen, X. T.; Huang, Y.; Huang, X. B.; Wu, R.; Ma, X. P.; Yan, Q. G. Functional roles of long non-coding RNA in human breast cancer. Asian Pac. J. Cancer Prev. 15(15):5993-5997;2014.
6. Silva, J. M.; Perez, D. S.; Pritchett, J. R.; Halling, M. L.; Tang, H.; Smith, D. I. Identification of long stress-induced non-coding transcripts that have altered expression in cancer. Genomics 95(6):355-362;2010.
7. Perez, D. S.; Hoage, T. R.; Pritchett, J. R.; Ducharme-Smith, A. L.; Halling, M. L.; Ganapathiraju, S. C.; Streng, P. S.; Smith, D. I. Long, abundantly expressed non-coding transcripts are altered in cancer. Hum. Mol. Genet. 17(5):642-655;2008.
8. Song, H.; Sun, W.; Ye, G.; Ding, X.; Liu, Z.; Zhang, S.; Xia, T.; Xiao, B.; Xi, Y.; Guo, J. Long non-coding RNA expression profile in human gastric cancer and its clinical significances. J. Transl. Med. 11:225;2013.
9. Bhan, A.; Mandal, S. S. Long noncoding RNAs: Emerging stars in gene regulation, epigenetics and human disease. Chem. Med. Chem. 9(9):1932-1956;2014.
10. Wapinski, O.; Chang, H. Y. Long noncoding RNAs and human disease. Trends Cell Biol. 21(6):354-361;2011.
11. Zhang, X.; Gejman, R.; Mahta, A.; Zhong, Y.; Rice, K. A.; Zhou, Y.; Cheunsuchon, P.; Louis, D. N.; Klibanski, A. Maternally expressed gene 3, an imprinted noncoding RNA gene, is associated with meningioma pathogenesis and progression. Cancer Res. 70(6):2350-2358;2010.
12. Liu, Q.; Huang, J.; Zhou, N.; Zhang, Z.; Zhang, A.; Lu, Z.; Wu, F.; Mo, Y. Y. LncRNA loc285194 is a p53-regulated tumor suppressor. Nucleic Acids Res. 41(9):4976-4987;2013.
13. Hung, C. L.; Wang, L. Y.; Yu, Y. L.; Chen, H. W.; Srivastava, S.; Petrovics, G.; Kung, H. J. A long noncoding RNA connects c-Myc to tumor metabolism. Proc. Natl. Acad. Sci. USA 111(52):18697-18702;2014.
14. He, J. H.; Zhang, J. Z.; Han, Z. P.; Wang, L.; Lv, Y. B.; Li, Y. G. Reciprocal regulation of PCGEM1 and miR-145 promote proliferation of LNCaP prostate cancer cells. J. Exp. Clin. Cancer Res. 33:72;2014.
15. Lai, M. C.; Yang, Z.; Zhou, L.; Zhu, Q. Q.; Xie, H. Y.; Zhang, F.; Wu, L. M.; Chen, L. M.; Zheng, S. S. Long non-coding RNA MALAT-1 overexpression predicts tumor recurrence of hepatocellular carcinoma after liver transplantation. Med. Oncol. 29(3):1810-1816;2012.
16. Liu, J. H.; Chen, G.; Dang, Y. W.; Li, C. J.; Luo, D. Z. Expression and prognostic significance of lncRNA MALAT1 in pancreatic cancer tissues. Asian Pac. J. Cancer Prev. 15(7):2971-2977;2014.
17. Ji, P.; Diederichs, S.; Wang, W.; Boing, S.; Metzger, R.; Schneider, P. M.; Tidow, N.; Brandt, B.; Buerger, H.; Bulk, E.; Thomas, M.; Berdel, W. E.; Serve, H.; Muller-Tidow, C. M. A. MAALAT-1, a novel noncoding RNA, and thymosin beta4 predict metastasis and survival in early-stage non-small cell lung cancer. Oncogene 22(39):8031-8041;2003.
18. Lin, R.; Maeda, S.; Liu, C.; Karin, M.; Edgington, T. S. A large noncoding RNA is a marker for murine hepatocellular carcinomas and a spectrum of human carcinomas. Oncogene 26(6):851-858;2007.
19. Adriaenssens, E.; Dumont, L.; Lottin, S.; Bolle, D.; Lepretre, A.; Delobelle, A.; Bouali, F.; Dugimont, T.; Coll, J.; Curgy, J. J. H19 overexpression in breast adenocarcinoma stromal cells is associated with tumor values and steroid receptor status but independent of p53 and Ki-67 expression. Am. J. Pathol. 153(5):1597-1607;1998.
20. Ariel, I.; Miao, H. Q.; Ji, X. R.; Schneider, T.; Roll, D.; de Groot, N.; Hochberg, A.; Ayesh, S. Imprinted H19 oncofetal RNA is a candidate tumour marker for hepatocellular carcinoma. Mol. Pathol. 51(1):21-25;1998.
21. Luo, M.; Li, Z.; Wang, W.; Zeng, Y.; Liu, Z.; Qiu, J. Long non-coding RNA H19 increases bladder cancer metastasis by associating with EZH2 and inhibiting E-cadherin expression. Cancer Lett. 333(2):213-221;2013.
22. Shi, Y.; Wang, Y.; Luan, W.; Wang, P.; Tao, T.; Zhang, J.; Qian, J.; Liu, N.; You, Y. Long non-coding RNA H19 promotes glioma cell invasion by deriving miR-675. PLoS One 9 (1) :e86295;2014.
23. Vennin, C.; Spruyt, N.; Dahmani, F.; Julien, S.; Bertucci, F.; Finetti, P.; Chassat, T.; Bourette, R. P.; Le Bourhis, X.; Adriaenssens, E. H19 non coding RNA-derived miR-675 enhances tumorigenesis and metastasis of breast cancer cells by downregulating c-Cbl and Cbl-b. Oncotarget 6(30):29209-239223;2015.
24. Wang, J.; Song, Y. X.; Wang, Z. N. Non-coding RNAs in gastric cancer. Gene 560(1):1-8;2015.
25. Li, P. F.; Chen, S. C.; Xia, T.; Jiang, X. M.; Shao, Y. F.; Xiao, B. X.; Guo, J. M. Non-coding RNAs and gastric cancer. World J. Gastroenterol. 20(18):5411-5419;2014.
26. Yang, F.; Bi, J.; Xue, X.; Zheng, L.; Zhi, K.; Hua, J.; Fang, G. Up-regulated long non-coding RNA H19 contributes to proliferation of gastric cancer cells. FEBS J. 279(17):3159-3165;2012.
27. Zhuang, M.; Gao, W.; Xu, J.; Wang, P.; Shu, Y. The long non-coding RNA H19-derived miR-675 modulates human gastric cancer cell proliferation by targeting tumor suppressor RUNX1. Biochem. Biophys. Res. Commun. 448(3):315-322;2014.
28. Fijneman, R. J.; Anderson, R. A.; Richards, E.; Liu, J.; Tijssen, M.; Meijer, G. A.; Anderson, J.; Rod, A.; O'Sullivan, M. G.; Scott, P. M.; Cormier, R. T. Runx1 is a tumor suppressor gene in the mouse gastrointestinal tract. Cancer Sci. 103(3):593-599;2012.
29. Fuka, G.; Kantner, H. P.; Grausenburger, R.; Inthal, A.; Bauer, E.; Krapf, G.; Kaindl, U.; Kauer, M.; Dworzak, M. N.; Stoiber, D.; Haas, O. A.; Panzer-Grumayer, R. Silencing of ETV6/RUNX1 abrogates PI3K/AKT/mTOR signaling and impairs reconstitution of leukemia in xenografts. Leukemia. 26(5):927-933;2012.
30. Edwards, H.; Xie, C.; LaFiura, K. M.; Dombkowski, A. A.; Buck, S. A.; Boerner, J L.; Taub, J. W.; Matherly, L. H.; Ge, Y. R. U. RUUNX1 regulates phosphoinositide 3-kinase/AKT pathway: Role in chemotherapy sensitivity in acute megakaryocytic leukemia. Blood 114(13):2744-2752;2009.
31. Karar, J.; Maity, A. PI3K/AKT/mTOR pathway in angiogenesis. Front. Mol. Neurosci. 4:51;2011.
32. Tapia, O.; Riquelme, I.; Leal, P.; Sandoval, A.; Aedo, S.; Weber, H.; Letelier, P.; Bellolio, E.; Villaseca, M.; Garcia, P.; Roa, J. C. The PI3K/AKT/mTOR pathway is activated in gastric cancer with potential prognostic and predictive significance. Virchows Arch. 465(1):25-33;2014.
33. Tsang, W. P.; Ng, E. K.; Ng, S. S.; Jin, H.; Yu, J.; Sung, J. J.; Kwok, T. T. Oncofetal H19-derived miR-675 regulates tumor suppressor RB in human colorectal cancer. Carcinogenesis 31(3):350-358;2010.
34. Li, H.; Yu, B.; Li, J.; Su, L.; Yan, M.; Zhu, Z.; Liu, B. Overexpression of lncRNA H19 enhances carcinogenesis and metastasis of gastric cancer. Oncotarget 5(8):2318-2329;2014.
35. Lv, J.; Ma, L.; Chen, X. L.; Huang, X. H.; Wang, Q. Downregulation of LncRNAH19 and MiR-675 promotes migration and invasion of human hepatocellular carcinoma cells through AKT/GSK-3beta/Cdc25A signaling pathway. J. Huazhong Univ. Sci. Technolog. Med. Sci. 34(3):363-369;2014.
36. Sakakura, C.; Hagiwara, A.; Miyagawa, K.; Nakashima, S.; Yoshikawa, T.; Kin, S.; Nakase, Y.; Ito, K.; Yamagishi, H.; Yazumi, S.; Chiba, T.; Ito, Y. Frequent downregulation of the runt domain transcription factors RUNX1, RUNX3 and their cofactor CBFB in gastric cancer. Int. J. Cancer 113(2):221-228;2005.
37. Gan, L.; Xu, M.; Zhang, Y.; Zhang, X.; Guo, W. Focusing on long noncoding RNA dysregulation in gastric cancer. Tumour Biol. 36(1):129-141;2015.
38. Sun, M.; Jin, F. Y.; Xia, R.; Kong, R.; Li, J. H.; Xu, T. P.; Liu, Y. W.; Zhang, E. B.; Liu, X. H.; De, W. Decreased expression of long noncoding RNA GAS5 indicates a poor prognosis and promotes cell proliferation in gastric cancer. BMC Cancer 14:319;2014.
39. Sun, M.; Xia, R.; Jin, F.; Xu, T.; Liu, Z.; De, W.; Liu, X. Downregulated long noncoding RNA MEG3 is associated with poor prognosis and promotes cell proliferation in gastric cancer. Tumour Biol. 35(2):1065-1073;2014.
40. Mei, D.; Song, H.; Wang, K.; Lou, Y.; Sun, W.; Liu, Z.; Ding, X.; Guo, J. Up-regulation of SUMO1 pseudogene 3(SUMO1P3) in gastric cancer and its clinical association. Med. Oncol. 30(4):709;2013.
41. Ponting, C. P.; Oliver, P. L.; Reik, W. Evolution and functions of long noncoding RNAs. Cell 136(4):629-641;2009.
42. Wang, K. C.; Chang, H. Y. Molecular mechanisms of long noncoding RNAs. Mol. Cell 43(6):904-914;2011.
43. Kim, S. J.; Park, S. E.; Lee, C.; Lee, S. Y.; Jo, J. H.; Kim, J. M.; Oh, Y. K. Alterations in promoter usage and expression levels of insulin-like growth factor-II and H19 genes in cervical carcinoma exhibiting biallelic expression of IGF-II. Biochim. Biophys. Acta 1586(3):307-315;2002.
44. Gao, W. L.; Liu, M.; Yang, Y.; Yang, H.; Liao, Q.; Bai, Y.; Li, Y. X.; Li, D.; Peng, C.; Wang, Y. L. The imprinted H19 gene regulates human placental trophoblast cell proliferation via encoding miR-675 that targets Nodal Modulator 1(NOMO1). RNA Biol. 9(7):1002-1010;2012.
45. Keniry, A.; Oxley, D.; Monnier, P.; Kyba, M.; Dandolo, L.; Smits, G.; Reik, W. The H19 lincRNA is a developmental reservoir of miR-675 that suppresses growth and Igf1r. Nat. Cell Biol. 14(7):659-665;2012.
46. Schmitz, K. J.; Helwig, J.; Bertram, S.; Sheu, S. Y.; Suttorp, A. C.; Seggewiss, J.; Willscher, E.; Walz, M. K.; Worm, K.; Schmid, K. W. Differential expression of microRNA-675, microRNA-139-3p and microRNA-335 in benign and malignant adrenocortical tumours. J. Clin. Pathol. 64(6):529-535;2011.
47. Hernandez, J. M.; Elahi, A.; Clark, C. W.; Wang, J.; Humphries, L. A.; Centeno, B.; Bloom, G.; Fuchs, B. C.; Yeatman, T.; Shibata, D. miR-675 mediates downregulation of Twist1 and Rb in AFP-secreting hepatocellular carcinoma. Ann. Surg. Oncol. 20(Suppl. 3):S625-635;2013.
48. Matouk, I. J.; Raveh, E.; Abu-lail, R.; Mezan, S.; Gilon, M.; Gershtain, E.; Birman, T.; Gallula, J.; Schneider, T.; Barkali, M.; Richler, C.; Fellig, Y.; Sorin, V.; Hubert, A.; Hochberg, A.; Czerniak, A. Oncofetal H19 RNA promotes tumor metastasis. Biochim. Biophys. Acta 1843(7):1414-1426;2014.
49. Wu, D.; Ozaki, T.; Yoshihara, Y.; Kubo, N.; Nakagawara, A. Runt-related transcription factor 1(RUNX1) stimulates tumor suppressor p53 protein in response to DNA damage through complex formation and acetylation. J. Biol. Chem. 288(2):1353-1364;2013.