MiR-206 inhibits HGF-induced epithelial-mesenchymal transition and angiogenesis in non-small cell lung cancer via c-Met /PI3k/ Akt/mTOR pathway

Oncotarget

Volumn 7, Issue 14, 2016, Pages 18247-18261

  Chen, Qing Yong ^a   Jiao, De Min ^a   Wu, Yu Quan ^a   Chen, Jun ^a   Wang, Jian ^a   Tang, Xia Li ^a   Mou, Hao ^a   Hu, Hui Zhen ^a   Song, Jia ^a   Yan, Jie ^a   Wu, Li Jun ^a   Chen, Jianyan ^b   Wang, Zhiwei ^c,d  

^a 117th Hospital of PLA   (China)

^b SOUTHERN MEDICAL UNIVERSITY   (China)

^c HARVARD MEDICAL SCHOOL   (United States)

^d SOOCHOW UNIVERSITY   (China)

Author keywords

Angiogenesis; Epithelial mesenchymal transition; HGF; Lung cancer; MiR 206

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; MICRORNA; MICRORNA 206; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE B; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; UNCLASSIFIED DRUG; HGF PROTEIN, HUMAN; MET PROTEIN, HUMAN; MIRN206 MICRORNA, HUMAN; MTOR PROTEIN, HUMAN; TARGET OF RAPAMYCIN KINASE;

95D CELL LINE; A549 CELL LINE; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CANCER TISSUE; CAPILLARY TUBE; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME INHIBITION; EPITHELIAL MESENCHYMAL TRANSITION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LUNG CANCER CELL LINE; MALE; METASTASIS; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR VASCULARIZATION; UMBILICAL VEIN ENDOTHELIAL CELL; A-549 CELL LINE; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; CANCER TRANSPLANTATION; CELL MOTION; GENETICS; LUNG; LUNG TUMOR; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; TUMOR INVASION; VASCULARIZATION; XENOGRAFT;

A549 CELLS; ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL MOVEMENT; EPITHELIAL-MESENCHYMAL TRANSITION; HEPATOCYTE GROWTH FACTOR; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LUNG; LUNG NEOPLASMS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; MICRORNAS; NEOPLASM INVASIVENESS; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-MET; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TRANSPLANTATION, HETEROLOGOUS;

EID: 84975481276     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.7570     Document Type: Article

References (47)

1. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA:a cancer journal for clinicians. 2015; 65:87-108
2. Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science. 2011; 331:1559-1564
3. Iwatsuki M, Mimori K, Yokobori T, Ishi H, Beppu T, Nakamori S, Baba H, Mori M. Epithelial-mesenchymal transition in cancer development and its clinical significance. Cancer science. 2010; 101:293-299
4. Meng F, Wu G. The rejuvenated scenario of epithelialmesenchymal transition (EMT) and cancer metastasis. Cancer metastasis reviews. 2012; 31:455-467
5. Fakhrejahani E, Toi M. Tumor angiogenesis:pericytes and maturation are not to be ignored. Journal of oncology. 2012; 2012:261750
6. Griffioen AW. Therapeutic approaches of angiogenesis inhibition:are we tackling the problem at the right levelOE Trends in cardiovascular medicine. 2007; 17:171-176
7. Kong W, He L, Richards EJ, Challa S, Xu CX, Permuth-Wey J, Lancaster JM, Coppola D, Sellers TA, Djeu JY, Cheng JQ. Upregulation of miRNA-155 promotes tumour angiogenesis by targeting VHL and is associated with poor prognosis and triple-negative breast cancer. Oncogene. 2014; 33:679-689
8. Gao D, Vahdat LT, Wong S, Chang JC, Mittal V. Microenvironmental regulation of epithelial-mesenchymal transitions in cancer. Cancer research. 2012; 72:4883-4889
9. Gentile A, Trusolino L, Comoglio PM. The Met tyrosine kinase receptor in development and cancer. Cancer metastasis reviews. 2008; 27:85-94
10. Maemura M, Iino Y, Yokoe T, Horiguchi J, Takei H, Koibuchi Y, Horii Y, Takeyoshi I, Ohwada S, Morishita Y. Serum concentration of hepatocyte growth factor in patients with metastatic breast cancer. Cancer letters. 1998; 126:215-220
11. Feng Y, Minca EC, Lanigan C, Liu A, Zhang W, Yin L, Pennell NA, Farver C, Tubbs R, Ma PC. High MET receptor expression but not gene amplification in ALK 2p23 rearrangement positive non-small-cell lung cancer. Journal of thoracic oncology. 2014; 9:646-653
12. Umeguchi H, Sueoka-Aragane N, Kobayashi N, Nakamura T, Sato A, Takeda Y, Hayashi S, Sueoka E, Kimura S. Usefulness of plasma HGF level for monitoring acquired resistance to EGFR tyrosine kinase inhibitors in non-small cell lung cancer. Oncology reports. 2015; 33:391-396
13. Huang J, Hao P, Chen H, Hu W, Yan Q, Liu F, Han ZG. Genome-wide identification of Schistosoma japonicum microRNAs using a deep-sequencing approach. PloS one. 2009; 4:e8206
14. Yao Q, Xu H, Zhang QQ, Zhou H, Qu LH. MicroRNA-21 promotes cell proliferation and down-regulates the expression of programmed cell death 4 (PDCD4) in HeLa cervical carcinoma cells. Biochemical and biophysical research communications. 2009; 388:539-542
15. Ohta K, Hoshino H, Wang J, Ono S, Iida Y, Hata K, Huang SK, Colquhoun S, Hoon DS. MicroRNA-93 activates c-Met/PI3K/Akt pathway activity in hepatocellular carcinoma by directly inhibiting PTEN and CDKN1A. Oncotarget. 2015; 6:3211-3224. doi:10.18632/oncotarget.3085
16. Bai J, Mei P, Zhang C, Chen F, Li C, Pan Z, Liu H, Zheng J. BRG1 is a prognostic marker and potential therapeutic target in human breast cancer. PloS one. 2013; 8:e59772
17. Yang Q, Zhang C, Huang B, Li H, Zhang R, Huang Y, Wang J. Downregulation of microRNA-206 is a potent prognostic marker for patients with gastric cancer. European journal of gastroenterology & hepatology. 2013; 25:953-957
18. Ren J, Huang HJ, Gong Y, Yue S, Tang LM, Cheng SY. MicroRNA-206 suppresses gastric cancer cell growth and metastasis. Cell & bioscience. 2014; 4:26
19. Wang S, Lu S, Geng S, Ma S, Liang Z, Jiao B. Decreased expression of microRNA-206 correlates with poor clinical outcome in patients with malignant astrocytomas. Pathology oncology research :POR. 2014
20. Chen X, Yan Q, Li S, Zhou L, Yang H, Yang Y, Liu X, Wan X. Expression of the tumor suppressor miR-206 is associated with cellular proliferative inhibition and impairs invasion in ERalpha-positive endometrioid adenocarcinoma. Cancer letters. 2012; 314:41-53
21. Yan D, Dong Xda E, Chen X, Wang L, Lu C, Wang J, Qu J, Tu L. MicroRNA-1/206 targets c-Met and inhibits rhabdomyosarcoma development. The Journal of biological chemistry. 2009; 284:29596-29604
22. Zhang Y, Tang H, Cai J, Zhang T, Guo J, Feng D, Wang Z. Ovarian cancer-associated fibroblasts contribute to epithelial ovarian carcinoma metastasis by promoting angiogenesis, lymphangiogenesis and tumor cell invasion. Cancer letters. 2011; 303:47-55
23. Nohata N, Hanazawa T, Enokida H, Seki N. microRNA-1/133a and microRNA-206/133b clusters:dysregulation and functional roles in human cancers. Oncotarget. 2012; 3:9-21. doi:10.18632/oncotarget.424
24. Liu H, Cao YD, Ye WX, Sun YY. Effect of microRNA-206 on cytoskeleton remodelling by downregulating Cdc42 in MDA-MB-231 cells. Tumori. 2010; 96:751-755
25. Zhang T, Liu M, Wang C, Lin C, Sun Y, Jin D. Downregulation of MiR-206 promotes proliferation and invasion of laryngeal cancer by regulating VEGF expression. Anticancer research. 2011; 31:3859-3863
26. Peng Y, Guo JJ, Liu YM, Wu XL. MicroRNA-34A inhibits the growth, invasion and metastasis of gastric cancer by targeting PDGFR and MET expression. Bioscience reports. 2014; 34
27. Elliman SJ, Howley BV, Mehta DS, Fearnhead HO, Kemp DM, Barkley LR. Selective repression of the oncogene cyclin D1 by the tumor suppressor miR-206 in cancers. Oncogenesis. 2014; 3:e113
28. Nagai T, Arao T, Furuta K, Sakai K, Kudo K, Kaneda H, Tamura D, Aomatsu K, Kimura H, Fujita Y, Matsumoto K, Saijo N, Kudo M, Nishio K. Sorafenib inhibits the hepatocyte growth factor-mediated epithelial mesenchymal transition in hepatocellular carcinoma. Molecular cancer therapeutics. 2011; 10:169-177
29. Birchmeier C, Birchmeier W, Gherardi E, Vande Woude GF. Met, metastasis, motility and more. Nature reviews Molecular cell biology. 2003; 4:915-925
30. Ma PC, Jagadeeswaran R, Jagadeesh S, Tretiakova MS, Nallasura V, Fox EA, Hansen M, Schaefer E, Naoki K, Lader A, Richards W, Sugarbaker D, Husain AN, Christensen JG, Salgia R. Functional expression and mutations of c-Met and its therapeutic inhibition with SU11274 and small interfering RNA in non-small cell lung cancer. Cancer research. 2005; 65:1479-1488
31. Chen QY, Jiao DM, Yan L, Wu YQ, Hu HZ, Song J, Yan J, Wu LJ, Xu LQ, Shi JG. Comprehensive gene and microRNA expression profiling reveals miR-206 inhibits MET in lung cancer metastasis. Molecular bioSystems. 2015; 11:2290-2302
32. Yang X, Zhang XF, Lu X, Jia HL, Liang L, Dong QZ, Ye QH, Qin LX. MicroRNA-26a suppresses angiogenesis in human hepatocellular carcinoma by targeting hepatocyte growth factor-cMet pathway. Hepatology. 2014; 59:1874-1885
33. Whittaker S, Marais R, Zhu AX. The role of signaling pathways in the development and treatment of hepatocellular carcinoma. Oncogene. 2010; 29:4989-5005
34. Matsumoto K, Nakamura T. Emerging multipotent aspects of hepatocyte growth factor. Journal of biochemistry. 1996; 119:591-600
35. Siegfried JM, Weissfeld LA, Luketich JD, Weyant RJ, Gubish CT, Landreneau RJ. The clinical significance of hepatocyte growth factor for non-small cell lung cancer. The Annals of thoracic surgery. 1998; 66:1915-1918
36. Bharti A, Ma PC, Maulik G, Singh R, Khan E, Skarin AT, Salgia R. Haptoglobin alpha-subunit and hepatocyte growth factor can potentially serve as serum tumor biomarkers in small cell lung cancer. Anticancer research. 2004; 24:1031-1038
37. Olivero M, Rizzo M, Madeddu R, Casadio C, Pennacchietti S, Nicotra MR, Prat M, Maggi G, Arena N, Natali PG, Comoglio PM, Di Renzo MF. Overexpression and activation of hepatocyte growth factor/scatter factor in human non-small-cell lung carcinomas. British journal of cancer. 1996; 74:1862-1868
38. Zheng Z, Yan D, Chen X, Huang H, Chen K, Li G, Zhou L, Zheng D, Tu L, Dong XD. MicroRNA-206:Effective Inhibition of Gastric Cancer Progression through the c-Met Pathway. PloS one. 2015; 10:e0128751
39. Xia Y, Wu Y, Liu B, Wang P, Chen Y. Downregulation of miR-638 promotes invasion and proliferation by regulating SOX2 and induces EMT in NSCLC. FEBS letters. 2014; 588:2238-2245
40. Li J, Wang Y, Luo J, Fu Z, Ying J, Yu Y, Yu W. miR-134 inhibits epithelial to mesenchymal transition by targeting FOXM1 in non-small cell lung cancer cells. FEBS letters. 2012; 586:3761-3765
41. Chen D, Huang J, Zhang K, Pan B, Chen J, De W, Wang R, Chen L. MicroRNA-451 induces epithelial-mesenchymal transition in docetaxel-resistant lung adenocarcinoma cells by targeting proto-oncogene c-Myc. European journal of cancer. 2014; 50:3050-3067
42. Trusolino L, Comoglio PM. Scatter-factor and semaphorin receptors:cell signalling for invasive growth. Nature reviews Cancer. 2002; 2:289-300
43. Mariani M, McHugh M, Petrillo M, Sieber S, He S, Andreoli M, Wu Z, Fiedler P, Scambia G, Shahabi S, Ferlini C. HGF/c-Met axis drives cancer aggressiveness in the neo-adjuvant setting of ovarian cancer. Oncotarget. 2014; 5:4855-4867. doi:10.18632/oncotarget.2049
44. Sun C, Liu Z, Li S, Yang C, Xue R, Xi Y, Wang L, Wang S, He Q, Huang J, Xie S, Jiang W, Li D. Downregulation of c-Met and Bcl2 by microRNA-206, activates apoptosis, and inhibits tumor cell proliferation, migration and colony formation. Oncotarget. 2015; 6:25533-25574. doi:10.18632/oncotarget.4575
45. Anand S, Majeti BK, Acevedo LM, Murphy EA, Mukthavaram R, Scheppke L, Huang M, Shields DJ, Lindquist JN, Lapinski PE, King PD, Weis SM, Cheresh DA. MicroRNA-132-mediated loss of p120RasGAP activates the endothelium to facilitate pathological angiogenesis. Nature medicine. 2010; 16:909-914
46. Yamakuchi M, Lotterman CD, Bao C, Hruban RH, Karim B, Mendell JT, Huso D, Lowenstein CJ. P53-induced microRNA-107 inhibits HIF-1 and tumor angiogenesis. Proceedings of the National Academy of Sciences of the United States of America. 2010; 107:6334-6339
47. Wang L, Ye X, Cai X, Su J, Ma R, Yin X, Zhou X, Li H, Wang Z. Curcumin suppresses cell growth and invasion and induces apoptosis by down-regulation of Skp2 pathway in glioma cells. Oncotarget. 2015; 6:18027-18037. doi:10.18632/oncotarget.4090