Tumor suppressor miR-1 restrains epithelial-mesenchymal transition and metastasis of colorectal carcinoma via the MAPK and PI3K/AKT pathway

Journal of Translational Medicine

Volumn 12, Issue 1, 2014, Pages

  Xu, Lijun ^a   Zhang, Yue ^a   Wang, Hui ^b   Zhang, Guanhua ^a   Ding, Yanqing ^a   Zhao, Liang ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b GUANGZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Colorectal carcinoma; Gene therapy; LIM and SH3 protein 1; MicroRNA; Proteomics; Signal pathway; Tumor metastasis

Indexed keywords

MESSENGER RNA; MICRORNA 1; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; MICRORNA; MIRN1 MICRORNA, HUMAN;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CELL HOMING; CELL PROLIFERATION; COLORECTAL CARCINOMA; CONTROLLED STUDY; DOWN REGULATION; ENZYME PHOSPHORYLATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; LASP1 GENE; METASTASIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEOMICS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR GENE; UPREGULATION; COLORECTAL TUMOR; ENZYMOLOGY; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL PROLIFERATION; COLORECTAL NEOPLASMS; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; MAP KINASE SIGNALING SYSTEM; MICRORNAS; NEOPLASM METASTASIS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT;

EID: 84908144472     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/s12967-014-0244-8     Document Type: Article

References (42)

1. Gupta GP, Massague J. Cancer metastasis: building a framework. Cell 2006, 127:679-695. 10.1016/j.cell.2006.11.001, 17110329.
2. Spano D, Heck C, De Antonellis P, Christofori G, Zollo M. Molecular networks that regulate cancer metastasis. Semin Cancer Biol 2012, 22:234-249. 10.1016/j.semcancer.2012.03.006, 22484561.
3. Ambros V, Lee RC, Lavanway A, Williams PT, Jewell D. MicroRNAs and other tiny endogenous RNAs in C. elegans. Curr Biol 2003, 13:807-818. 10.1016/S0960-9822(03)00287-2, 12747828.
4. Uematsu K, He B, You L, Xu Z, McCormick F, Jablons DM. Activation of the Wnt pathway in non small cell lung cancer: evidence of dishevelled overexpression. Oncogene 2003, 22:7218-7221. 10.1038/sj.onc.1206817, 14562050.
5. Xia X, Yang B, Zhai X, Liu X, Shen K, Wu Z, Cai J. Prognostic Role of microRNA-21 in Colorectal Cancer: a Meta-Analysis. PLoS One 2013, 8:e80426. 10.1371/journal.pone.0080426, 24265822.
6. Zhang J, Lu Y, Yue X, Li H, Luo X, Wang Y, Wang K, Wan J. MiR-124 suppresses growth of human colorectal cancer by inhibiting STAT3. PLoS One 2013, 8:e70300. 10.1371/journal.pone.0070300, 23940556.
7. Lou X, Qi X, Zhang Y, Long H, Yang J. Decreased expression of microRNA-625 is associated with tumor metastasis and poor prognosis in patients with colorectal cancer. J Surg Oncol 2013, 108:230-235. 10.1002/jso.23380, 23861214.
8. Zhou C, Liu G, Wang L, Lu Y, Yuan L, Zheng L, Chen F, Peng F, Li X. MiR-339-5p regulates the growth, colony formation and metastasis of colorectal cancer cells by targeting PRL-1. PLoS One 2013, 8:e63142. 10.1371/journal.pone.0063142, 23696794.
9. Ye J, Wu X, Wu D, Wu P, Ni C, Zhang Z, Chen Z, Qiu F, Xu J, Huang J. miRNA-27b targets vascular endothelial growth factor C to inhibit tumor progression and angiogenesis in colorectal cancer. PLoS One 2013, 8:e60687. 10.1371/journal.pone.0060687, 23593282.
10. Zhao L, Wang H, Liu C, Liu Y, Wang X, Wang S, Sun X, Li J, Deng Y, Jiang Y, Ding Y. Promotion of colorectal cancer growth and metastasis by the LIM and SH3 domain protein 1. Gut 2010, 59:1226-1235. 10.1136/gut.2009.202739, 20660701.
11. Wang H, An H, Wang B, Liao Q, Li W, Jin X, Cui S, Zhang Y, Ding Y, Zhao L. miR-133a represses tumour growth and metastasis in colorectal cancer by targeting LIM and SH3 protein 1 and inhibiting the MAPK pathway. Eur J Cancer 2013, 49:3924-3935. 10.1016/j.ejca.2013.07.149, 23968734.
12. Li D, Yang P, Li H, Cheng P, Zhang L, Wei D, Su X, Peng J, Gao H, Tan Y, Zhao Z, Li Y, Qi Z, Rui Y, Zhang T. MicroRNA-1 inhibits proliferation of hepatocarcinoma cells by targeting endothelin-1. Life Sci 2012, 91:440-447. 10.1016/j.lfs.2012.08.015, 22963810.
13. Hudson RS, Yi M, Esposito D, Watkins SK, Hurwitz AA, Yfantis HG, Lee DH, Borin JF, Naslund MJ, Alexander RB, Dorsey TH, Stephens RM, Croce CM, Ambs S. MicroRNA-1 is a candidate tumor suppressor and prognostic marker in human prostate cancer. Nucleic Acids Res 2012, 40:3689-3703. 10.1093/nar/gkr1222, 22210864.
14. Kojima S, Chiyomaru T, Kawakami K, Yoshino H, Enokida H, Nohata N, Fuse M, Ichikawa T, Naya Y, Nakagawa M, Seki N. Tumour suppressors miR-1 and miR-133a target the oncogenic function of purine nucleoside phosphorylase (PNP) in prostate cancer. Br J Cancer 2012, 106:405-413. 10.1038/bjc.2011.462, 22068816.
15. Leone V, D'Angelo D, Rubio I, de Freitas PM, Federico A, Colamaio M, Pallante P, Medeiros-Neto G, Fusco A. MiR-1 is a tumor suppressor in thyroid carcinogenesis targeting CCND2, CXCR4, and SDF-1alpha. J Clin Endocrinol Metab 2011, 96:E1388-E1398. 10.1210/jc.2011-0345, 21752897.
16. Yoshino H, Chiyomaru T, Enokida H, Kawakami K, Tatarano S, Nishiyama K, Nohata N, Seki N, Nakagawa M. The tumour-suppressive function of miR-1 and miR-133a targeting TAGLN2 in bladder cancer. Br J Cancer 2011, 104:808-818. 10.1038/bjc.2011.23, 21304530.
17. Kawakami K, Enokida H, Chiyomaru T, Tatarano S, Yoshino H, Kagara I, Gotanda T, Tachiwada T, Nishiyama K, Nohata N, Seki N, Nakagawa M. The functional significance of miR-1 and miR-133a in renal cell carcinoma. Eur J Cancer 2012, 48:827-836. 10.1016/j.ejca.2011.06.030, 21745735.
18. Cummins JM, He Y, Leary RJ, Pagliarini R, Diaz LA, Sjoblom T, Barad O, Bentwich Z, Szafranska AE, Labourier E, Raymond CK, Roberts BS, Juhl H, Kinzler KW, Vogelstein B, Velculescu VE. The colorectal microRNAome. Proc Natl Acad Sci U S A 2006, 103:3687-3692. 10.1073/pnas.0511155103, 16505370.
19. Suzuki H, Takatsuka S, Akashi H, Yamamoto E, Nojima M, Maruyama R, Kai M, Yamano HO, Sasaki Y, Tokino T, Shinomura Y, Imai K, Toyota M. Genome-wide profiling of chromatin signatures reveals epigenetic regulation of MicroRNA genes in colorectal cancer. Cancer Res 2011, 71:5646-5658. 10.1158/0008-5472.CAN-11-1076, 21734013.
20. Migliore C, Martin V, Leoni VP, Restivo A, Atzori L, Petrelli A, Isella C, Zorcolo L, Sarotto I, Casula G, Comoglio PM, Columbano A, Giordano S. MiR-1 downregulation cooperates with MACC1 in promoting MET overexpression in human colon cancer. Clin Cancer Res 2012, 18:737-747. 10.1158/1078-0432.CCR-11-1699, 22179665.
21. Zhang YF, Liu L, Ding YQ. Isolation and characterization of human colorectal cancer cell subline with unique metastatic potential in the liver. Nan Fang Yi Ke Da Xue Xue Bao 2007, 27:126-130. 17355917.
22. Liu L, Zhang Q, Zhang Y, Wang S, Ding Y. Lentivirus-mediated silencing of Tiam1 gene influences multiple functions of a human colorectal cancer cell line. Neoplasia 2006, 8:917-924. 10.1593/neo.06364, 17132223.
23. Ioshikhes I, Roy S, Sen CK. Algorithms for mapping of mRNA targets for microRNA. DNA Cell Biol 2007, 26:265-272. 10.1089/dna.2006.0566, 17465893.
24. Larue L, Bellacosa A. Epithelial-mesenchymal transition in development and cancer: role of phosphatidylinositol 3' kinase/AKT pathways. Oncogene 2005, 24:7443-7454. 10.1038/sj.onc.1209091, 16288291.
25. Serpico D, Molino L, Di Cosimo S. microRNAs in breast cancer development and treatment. Cancer Treat Rev 2014, 40:595-604. 10.1016/j.ctrv.2013.11.002, 24286642.
26. Xi JJ. MicroRNAs in Cancer. Cancer Treat Res 2013, 158:119-137. 10.1007/978-3-642-31659-3_5, 24222356.
27. Wang ZM, Du WJ, Piazza GA, Xi Y. MicroRNAs are involved in the self-renewal and differentiation of cancer stem cells. Acta Pharmacol Sin 2013, 34:1374-1380. 10.1038/aps.2013.134, 24122008.
28. Chu Y, Ouyang Y, Wang F, Zheng A, Bai L, Han L, Chen Y, Wang H. MicroRNA-590 Promotes Cervical Cancer Cell Growth and Invasion by Targeting CHL1. J Cell Biochem 2014, 115:847-853. 10.1002/jcb.24726, 24288179.
29. Chai ZT, Kong J, Zhu XD, Zhang YY, Lu L, Zhou JM, Wang LR, Zhang KZ, Zhang QB, Ao JY, Wang M, Wu WZ, Wang L, Tang ZY, Sun HC. MicroRNA-26a Inhibits Angiogenesis by Down-Regulating VEGFA through the PIK3C2alpha/Akt/HIF-1alpha Pathway in Hepatocellular Carcinoma. PLoS One 2013, 8:e77957. 10.1371/journal.pone.0077957, 24194905.
30. Kojima S, Enokida H, Yoshino H, Itesako T, Chiyomaru T, Kinoshita T, Fuse M, Nishikawa R, Goto Y, Naya Y, Nakagawa M, Seki N. The tumor-suppressive microRNA-143/145 cluster inhibits cell migration and invasion by targeting GOLM1 in prostate cancer. J Hum Genet 2014, 59:78-87. 10.1038/jhg.2013.121, 24284362.
31. Zhao L, Wang H, Li J, Liu Y, Ding Y. Overexpression of Rho GDP-dissociation inhibitor alpha is associated with tumor progression and poor prognosis of colorectal cancer. J Proteome Res 2008, 7:3994-4003. 10.1021/pr800271b, 18651761.
32. Nohata N, Sone Y, Hanazawa T, Fuse M, Kikkawa N, Yoshino H, Chiyomaru T, Kawakami K, Enokida H, Nakagawa M, Shozu M, Okamoto Y, Seki N. miR-1 as a tumor suppressive microRNA targeting TAGLN2 in head and neck squamous cell carcinoma. Oncotarget 2011, 2:29-42. 21378409.
33. Hugo H, Ackland ML, Blick T, Lawrence MG, Clements JA, Williams ED, Thompson EW. Epithelial-mesenchymal and mesenchymal-epithelial transitions in carcinoma progression. J Cell Physiol 2007, 213:374-383. 10.1002/jcp.21223, 17680632.
34. 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 Sci 2010, 101:293-299. 10.1111/j.1349-7006.2009.01419.x, 19961486.
35. Liu YN, Yin JJ, Abou-Kheir W, Hynes PG, Casey OM, Fang L, Yi M, Stephens RM, Seng V, Sheppard-Tillman H, Martin P, Kelly K. MiR-1 and miR-200 inhibit EMT via Slug-dependent and tumorigenesis via Slug-independent mechanisms. Oncogene 2013, 32:296-306. 10.1038/onc.2012.58, 22370643.
36. Ye Q, Cai W, Zheng Y, Evers BM, She QB. ERK and AKT signaling cooperate to translationally regulate survivin expression for metastatic progression of colorectal cancer. Oncogene 2014, 33:1828-1839. 10.1038/onc.2013.122, 23624914.
37. Wang F, Song G, Liu M, Li X, Tang H. miRNA-1 targets fibronectin1 and suppresses the migration and invasion of the HEp2 laryngeal squamous carcinoma cell line. FEBS Lett 2011, 585:3263-3269. 10.1016/j.febslet.2011.08.052, 21924268.
38. Tomasetto C, Moog-Lutz C, Regnier CH, Schreiber V, Basset P, Rio MC. Lasp-1 (MLN 50) defines a new LIM protein subfamily characterized by the association of LIM and SH3 domains. FEBS Lett 1995, 373:245-249. 10.1016/0014-5793(95)01040-L, 7589475.
39. Tomasetto C, Regnier C, Moog-Lutz C, Mattei MG, Chenard MP, Lidereau R, Basset P, Rio MC. Identification of four novel human genes amplified and overexpressed in breast carcinoma and localized to the q11-q21.3 region of chromosome 17. Genomics 1995, 28:367-376. 10.1006/geno.1995.1163, 7490069.
40. Lin YH, Park ZY, Lin D, Brahmbhatt AA, Rio MC, Yates JR, Klemke RL. Regulation of cell migration and survival by focal adhesion targeting of Lasp-1. J Cell Biol 2004, 165:421-432. 10.1083/jcb.200311045, 15138294.
41. Grunewald TG, Kammerer U, Schulze E, Schindler D, Honig A, Zimmer M, Butt E. Silencing of LASP-1 influences zyxin localization, inhibits proliferation and reduces migration in breast cancer cells. Exp Cell Res 2006, 312:974-982. 10.1016/j.yexcr.2005.12.016, 16430883.
42. Grunewald TG, Kammerer U, Winkler C, Schindler D, Sickmann A, Honig A, Butt E. Overexpression of LASP-1 mediates migration and proliferation of human ovarian cancer cells and influences zyxin localisation. Br J Cancer 2007, 96:296-305. 10.1038/sj.bjc.6603545, 17211471.