MicroRNA-200b and microRNA-200c promote colorectal cancer cell proliferation via targeting the reversion-inducing cysteine-rich protein with Kazal motifs

RNA Biology

Volumn 12, Issue 3, 2015, Pages 276-289

  Pan, Yi ^a   Liang, Hongwei ^a   Chen, Weixu ^b   Zhang, Hongjie ^b   Wang, Nan ^a   Wang, Feng ^c   Zhang, Suyang ^a   Liu, Yanqing ^a   Zhao, Chihao ^a   Yan, Xin ^d   Zhang, Junfeng ^a   Zhang, Chen Yu ^a   Gu, Hongwei ^a   Zen, Ke ^a   Chen, Xi ^a  

^a NANJING UNIVERSITY   (China)

^b THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

^c MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

^d THE AFFILIATED DRUM TOWER HOSPITAL OF NANJING UNIVERSITY MEDICAL SCHOOL   (China)

Author keywords

Cell proliferation; Colorectal cancer; miR 200b c; Oncogene; RECK

Indexed keywords

COMPLEMENTARY DNA; CYSTEINE; MESSENGER RNA; MICRORNA 200B; MICRORNA 200C; PROTEIN P27; REVERSION INDUCING CYSTEINE RICH PROTEIN WITH KAZAL MOTIF; S PHASE KINASE ASSOCIATED PROTEIN 2; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; CYCLIN DEPENDENT KINASE INHIBITOR 1B; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; MICRORNA; MIRN200 MICRORNA, HUMAN; RECK PROTEIN, HUMAN; S PHASE KINASE ASSOCIATED PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; CANCER GROWTH; CELL PROLIFERATION; CELL VIABILITY ASSAY; COLORECTAL CANCER CELL LINE; CONTROLLED STUDY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LUCIFERASE ASSAY; MALE; MOUSE; MTT ASSAY; NONHUMAN; POINT MUTATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; TUMOR GROWTH; TUMOR XENOGRAFT; UPREGULATION; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; CACO 2 CELL LINE; CANCER TRANSPLANTATION; CARCINOGENESIS; COLORECTAL TUMOR; GENE EXPRESSION REGULATION; GENETICS; HT 29 CELL LINE; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CACO-2 CELLS; CARCINOGENESIS; CELL PROLIFERATION; COLORECTAL NEOPLASMS; CYCLIN-DEPENDENT KINASE INHIBITOR P27; GENE EXPRESSION REGULATION, NEOPLASTIC; GPI-LINKED PROTEINS; HT29 CELLS; HUMANS; MICE; MICRORNAS; NEOPLASM TRANSPLANTATION; RNA, SMALL INTERFERING; S-PHASE KINASE-ASSOCIATED PROTEINS; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 84928265689     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.1080/15476286.2015.1017208     Document Type: Article

References (36)

1. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer 2006; 6:857–66. PMID:17060945. http://dx.doi.org/10.1038/nrc1997
2. Ma L, Weinberg RA. Micromanagers of malignancy: role of microRNAs in regulating metastasis. Trends Genet 2008; 24:448–56. PMID:18674843. http://dx.doi.org/10.1016/j.tig.2008.06.004
3. Nicoloso MS, Spizzo R, Shimizu M, Rossi S, Calin GA. MicroRNAs–the micro steering wheel of tumour metastases. Nat Rev Cancer 2009; 9:293–302. PMID:19262572. http://dx.doi.org/10.1038/nrc2619
4. Park SM, Gaur AB, Lengyel E, Peter ME. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Deve 2008; 22:894–907. PMID:18381893. http://dx.doi.org/10.1101/gad. 1640608
5. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, Vadas MA, Khew-Goodall Y, Goodall GJ. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008; 10:593–601. PMID:18376396. http://dx.doi.org/10.1038/ncb1722
6. Burk U, Schubert J, Wellner U, Schmalhofer O, Vincan E, Spaderna S, Brabletz T. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. Embo Rep 2008; 9:582–9. PMID:18483486. http://dx.doi.org/10.1038/embor.2008.74
7. Oh J, Takahashi R, Kondo S, Mizoguchi A, Adachi E, Sasahara RM, Nishimura S, Imamura Y, Kitayama H, Alexander DB, et al. The membrane-anchored MMP inhibitor RECK is a key regulator of extracellular matrix integrity and angiogenesis. Cell 2001; 107:789–800. PMID:11747814. http://dx.doi.org/10.1016/S0092-8674(01)00597-9
8. Miki T, Takegami Y, Okawa K, Muraguchi T, Noda M, Takahashi C. The reversion-inducing cysteine-rich protein with Kazal motifs (RECK) interacts with membrane type 1 matrix metalloproteinase and CD13/aminopeptidase n and modulates their endocytic pathways. J Biol Chem 2007; 282:12341–52. PMID:17329256. http://dx.doi.org/10.1074/jbc.M610948200
9. Omura A, Matsuzaki T, Mio K, Ogura T, Yamamoto M, Fujita A, Okawa K, Kitayama H, Takahashi C, Sato C, et al. RECK Forms Cowbell-shaped Dimers and Inhibits Matrix Metalloproteinase-catalyzed Cleavage of Fibronectin. J Biol Chem 2009; 284:3461–9. PMID:19022775. http://dx.doi.org/10.1074/jbc. M806212200
10. Loayza-Puch F, Yoshida Y, Matsuzaki T, Takahashi C, Kitayama H, Noda M. Hypoxia and RAS-signaling pathways converge on, and cooperatively downregulate, the RECK tumor-suppressor protein through micro-RNAs. Oncogene 2010; 29:2638–48. PMID:20154725. http://dx.doi.org/10.1038/onc.2010.23
11. Noda M, Takahashi C. Recklessness as a hallmark of aggressive cancer. Cancer Sci 2007; 98:1659–65. PMID:17725805. http://dx.doi.org/10.1111/j.1349-7006.2007.00588.x
12. Yoshida Y, Ninomiya K, Hamada H, Noda M. Involvement of the SKP2-p27(KIP1) pathway in suppression of cancer cell proliferation by RECK. Oncogene 2012; 31:4128–38. PMID:22158033. http://dx.doi.org/10.1038/onc.2011.570
13. Chen X, Wang KH, Chen JN, Guo JG, Yin Y, Cai X, Guo X, Wang G, Yang R, Zhu L, et al. In Vitro Evidence Suggests That miR-133a-mediated Regulation of Uncoupling Protein 2 (UCP2) Is an Indispensable Step in Myogenic Differentiation. J Biol Chem 2009; 284:5362–9. PMID:19073597. http://dx.doi.org/10.1074/jbc.M807523200
14. Chang HC, Cho CY, Hung WC. Silencing of the metastasis suppressor RECK by RAS oncogene is mediated by DNA methyltransferase 3b-induced promoter methylation. Cancer Res 2006; 66:8413–20. PMID:16951151. http://dx.doi.org/10.1158/0008-5472.CAN-06-0685
15. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB. Prediction of mammalian microRNA targets. Cell 2003; 115:787–98. PMID:14697198. http://dx.doi.org/10.1016/S0092-8674(03)01018-3
16. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M, et al. Combinatorial microRNA target predictions. Nat Genet 2005; 37:495–500. PMID:15806104. http://dx.doi.org/10.1038/ng1536
17. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS. Human MicroRNA targets. Plos Biol 2004; 2:1862–79. http://dx.doi.org/10.1371/journal. pbio.0020363
18. Thomson DW, Bracken CP, Szubert JM, Goodall GJ. On measuring miRNAs after transient transfection of mimics or antisense inhibitors. PLoS One 2013; 8: e55214. PMID:23358900. http://dx.doi.org/10.1371/journal.pone.0055214
19. Coats S, Flanagan WM, Nourse J, Roberts JM. Requirement of p27Kip1 for restriction point control of the fibroblast cell cycle. Science 1996; 272:877–80. PMID:8629023. http://dx.doi.org/10.1126/science.272.5263.877
20. Carrano AC, Eytan E, Hershko A, Pagano M. SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat Cell Biol 1999; 1:193–9. PMID:10559916. http://dx.doi.org/10.1038/12013
21. Tsvetkov LM, Yeh KH, Lee SJ, Sun H, Zhang H. P27 (Kip1) ubiquitination and degradation is regulated by the SCFSkp2 complex through phosphorylated Thr187 in p27. Curr Biol 1999; 9:661–4. PMID:10375532. http://dx.doi.org/10.1016/S0960-9822(99)80290-5
22. Zhu L. Skp2 knockout reduces cell proliferation and mouse body size: and prevents cancer? Cell Res 2010; 20:605–7. PMID:20502441. http://dx.doi.org/10.1038/cr.2010.71
23. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011; 61:69–90. PMID:21296855. http://dx.doi.org/10.3322/caac.20107
24. Bezerra-de-Souza DL, Bernal MM, Gomez FJ, Gomez GJ. Predictions and estimations of colorectal cancer mortality, prevalence and incidence in Aragon, Spain, for the period 1998-2022. Rev Esp Enferm Dig 2012; 104:518–23. PMID:23268630. http://dx.doi.org/10.4321/S1130-01082012001000003
25. Xi Y, Formentini A, Chien M, Weir DB, Russo JJ, Ju J, Kornmann M, Ju J. Prognostic Values of microRNAs in Colorectal Cancer. Biomark Insights 2006; 2:113–21. PMID:18079988
26. Bandres E, Cubedo E, Agirre X, Malumbres R, Zarate R, Ramirez N, Abajo A, Navarro A, Moreno I, Monzo M, et al. Identification by Real-time PCR of 13 mature microRNAs differentially expressed in colorectal cancer and non-tumoral tissues. Mol Cancer 2006; 5:29. PMID:16854228. http://dx.doi.org/10.1186/1476-4598-5-29
27. Iorio MV, Visone R, Di Leva G, Donati V, Petrocca F, Casalini P, Taccioli C, Volinia S, Liu CG, Alder H, et al. MicroRNA signatures in human ovarian cancer. Cancer Res 2007; 67:8699–707. PMID:17875710. http://dx.doi.org/10.1158/0008-5472.CAN-07-1936
28. Korpal M, Lee ES, Hu G, Kang Y. The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem 2008; 283:14910–4. PMID:18411277. http://dx.doi.org/10.1074/jbc.C800074200
29. Hur K, Toiyama Y, Takahashi M, Balaguer F, Nagasaka T, Koike J, Hemmi H, Koi M, Boland CR, Goel A. MicroRNA-200c modulates epithelial-to-mesenchymal transition (EMT) in human colorectal cancer metastasis. Gut 2013; 62:1315–26. PMID:22735571. http://dx.doi.org/10.1136/gutjnl-2011-301846
30. Chen ML, Liang LS, Wang XK. miR-200c inhibits invasion and migration in human colon cancer cells SW480/620 by targeting ZEB1. Clin Exp Meta 2012; 29:457–69. PMID:22407310. http://dx.doi.org/10.1007/s10585-012-9463-7
31. Wang N, Zhang CQ, He JH, Duan XF, Wang YY, Ji X, Zang WQ, Li M, Ma YY, Wang T, et al. MiR-21 down-regulation suppresses cell growth, invasion and induces cell apoptosis by targeting FASL, TIMP3, and RECK genes in esophageal carcinoma. Dig Dis Sci 2013; 58:1863–70. PMID:23504349. http://dx.doi.org/10.1007/s10620-013-2612-2
32. Jung HM, Phillips BL, Patel RS, Cohen DM, Jakymiw A, Kong WW, Cheng JQ, Chan EK. Keratinizationassociated miR-7 and miR-21 Regulate Tumor Suppressor Reversion-inducing Cysteine-rich Protein with Kazal Motifs (RECK) in Oral Cancer. J Biol Chem 2012; 287:29261–72. PMID:22761427. http://dx.doi.org/10.1074/jbc.M112.366518
33. Reis ST, Pontes-Junior J, Antunes AA, Dall’Oglio MF, Dip N, Passerotti CC, Rossini GA, Morais DR, Nesrallah AJ, Piantino C. miR-21 may acts as an oncomir by targeting RECK, a matrix metalloproteinase regulator, in prostate cancer. BMC Urol 2012; 12:14. PMID:22642976. http://dx.doi.org/10.1186/1471-2490-12-14
34. Han L, Yue X, Zhou X, Lan FM, You G, Zhang W, Zhang KL, Zhang CZ, Cheng JQ, Yu SZ, et al. Micro-RNA-21 expression is regulated by beta-catenin/STAT3 pathway and promotes glioma cell invasion by direct targeting RECK. CNS Neurosci Ther 2012; 18:573–83. PMID:22630347. http://dx.doi.org/10.1111/j.1755-5949.2012.00344.x
35. Evan GI, Vousden KH. Proliferation, cell cycle and apoptosis in cancer. Nature 2001; 411:342–8. PMID:11357141. http://dx.doi.org/10.1038/35077213
36. Loda M, Cukor B, Tam SW, Lavin P, Fiorentino M, Draetta GF, Jessup JM, Pagano M. Increased proteasome-dependent degradation of the cyclin-dependent kinase inhibitor p27 in aggressive colorectal carcinomas. Nat Med 1997; 3:231–4. PMID:9018245. http://dx.doi.org/10.1038/nm0297-231