MicroRNA miR-24 promotes cell proliferation by targeting the CDKs inhibitors p27Kip1 and p16INK4a

Journal of Cellular Physiology

Volumn 228, Issue 10, 2013, Pages 2015-2023

  Giglio, Simona ^a   Cirombella, Roberto ^a   Amodeo, Rachele ^a   Portaro, Luciano ^a   Lavra, Luca ^a   Vecchione, Andrea ^a,b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLIN DEPENDENT KINASE INHIBITOR 2A; MICRORNA 24;

ARTICLE; CANCER CELL CULTURE; CARCINOGENESIS; CELL CYCLE; CELL GROWTH; CELL PROLIFERATION; GENE EXPRESSION; HUMAN; HUMAN CELL; KERATINOCYTE; NEOPLASM; PRIORITY JOURNAL;

CELL CYCLE; CELL CYCLE PROTEINS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE INHIBITOR P16; CYCLIN-DEPENDENT KINASE INHIBITOR P27; HUMANS; KERATINOCYTES; MICRORNAS; RNA PROCESSING, POST-TRANSCRIPTIONAL; UP-REGULATION;

EID: 84879516965     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24368     Document Type: Article

References (48)

1. Bartel DP. 2004. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116:281-297.
2. Belletti B, Nicoloso MS, Schiappacassi M, Chimienti E, Berton S, Lovat F, Colombatti A, Baldassarre G. 2005. p27(kip1) functional regulation in human cancer: A potential target for therapeutic designs. Curr Med Chem 12:1589-1605.
3. Bueno MJ, Malumbres M. 2011. MicroRNAs and the cell cycle. Biochim Biophys Acta 1812:592-601, review.
4. Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E, Aldler H, Rattan S, Keating M, Rai K, Rassenti L, Kipps T, Negrini M, Bullrich F, Croce CM. 2002. Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 99:15524-15529.
5. Carleton M, Cleary MA, Linsley PS. 2007. MicroRNAs and cell cycle regulation. Cell Cycle 6:2127-2132.
6. Carnero A, Hannon GJ. 1998. The INK4 family of CDK inhibitors. Curr Top Microbiol Immunol 227:43-55.
7. Cheng AM, Byrom MW, Shelton J, Ford LP. 2005. Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Res 33:1290-1297.
8. Du WW, Fang L, Li M, Yang X, Liang Y, Peng C, Qian W, O'Malley YQ, Askeland RW, Sugg S, Qian J, Lin J, Jiang Z, Yee AJ, Sefton M, Deng Z, Shan SW, Wang CH, Yang BB. 2013. MicroRNA miR-24 enhances tumor invasion and metastasis by targeting PTPN9 and PTPRF to promote EGF signaling. J Cell Sci [Epub ahead of print]. Advance online article February 2013
9. Galardi S, Mercatelli N, Giorda E, Massalini S, Frajese GV, Ciafrè SA, Farace MG. 2007. miR-221 and miR-222 expression affects the proliferation potential of human prostate carcinoma cell lines by targeting p27Kip1. J Biol Chem 282:23716-23724.
10. Guo Y, Fu W, Chen H, Shang C, Zhong M. 2012. miR-24 functions as a tumor suppressor in Hep2 laryngeal carcinoma cells partly through down-regulation of the S100A8 protein. Oncol Rep 27:1097-1103.
11. Harfe BD. 2005. MicroRNAs in vertebrate development. Curr Opin Genet Dev 15:410-415.
12. Hatziapostolou M, Polytarchou C, Aggelidou E, Drakaki A, Poultsides GA, Jaeger SA, Ogata H, Karin M, Struhl F K, Hadzopoulou-Cladaras M, Iliopoulos D. 2011. An HNF4α-miRNA inflammatory feedback circuit regulates hepatocellular oncogenesis. Cell 147:1233-1247.
13. Hengst L, Reed SI. 1998. Inhibitors of the Cip/Kip family. Curr Top Microbiol Immunol 227:25-41.
14. Hu S, Huang M, Nguyen PK, Gong Y, Li Z, Jia F, Lan F, Liu J, Nag D, Robbins RC, Wu JC. 2011. Novel microRNA prosurvival cocktail for improving engraftment and function of cardiac progenitor cell transplantation. Circulation 124:S27-S34.
15. Ivanovska I, Ball AS, Diaz RL, Magnus JF, Kibukawa M, Schelter JM, Kobayashi SV, Lim L, Burchard J, Jackson AL, Linsley PS, Cleary MA. 2008. MicroRNAs in the miR-106b family regulate p21/CDKN1A and promote cell cycle progression. Mol Cell Biol 28:2167-2174 [Epub 2008 Jan 22].
16. Kamb A, Gruis NA, Weaver-Feldhaus J, Liu Q, Harshman K, Tavtigian SV, Stockert E, Day RS III, Johnson BE, Skolnick MH. 1994. A cell cycle regulator potentially involved in genesis of many tumor types. Science 264:436-440.
17. Kedde M, Strasser MJ, Boldajipour B, Oude Vrielink JA, Slanchev K, le Sage C, Nagel R, Voorhoeve PM, van Duijse J, Ørom UA, Lund AH, Perrakis A, Raz E, Agami R. 2007. RNA-binding protein Dnd1 inhibits microRNA access to target mRNA. Cell 131:1273-1286.
18. Kedde M, van Kouwenhove M, Zwart W, Oude Vrielink JA, Elkon R, Agami R. 2010. A Pumilio-induced RNA structure switch in p27-3′ UTR controls miR-221 and miR-222 accessibility. Nat Cell Biol 12:1014-1020.
19. Kim YK, Yu J, Han TS, Park SY, Namkoong B, Kim DH, Hur K, Yoo MW, Lee HJ, Yang HK, Kim VN. 2009. Functional links between clustered microRNAs: Suppression of cell-cycle inhibitors by microRNA clusters in gastric cancer. Nucleic Acids Res 37:1672-1681. DOI: 10.1093/nar/gkp002 [Epub2009 Jan 19].
20. Koff A. 2006. How to decrease p27Kip1 levels during tumor development. Cancer Cell 9:75-76.
21. Lal A, Kim HH, Abdelmohsen K, Kuwano Y, Pullmann R, Jr., Srikantan S, Subrahmanyam R, Martindale JL, Yang X, Ahmed F, Navarro F, Dykxhoorn D, Lieberman J, Gorospe M. 2008. p16(INK4a) translation suppressed by miR-24. PLoS ONE 3:e1864.
22. Lal A, Navarro F, Maher CA, Maliszewski LE, Yan N, O'Day E, Chowdhury D, Dykxhoorn DM, Tsai P, Hofmann O, Becker KG, Gorospe M, Hide W, Lieberman J. 2009. miR-24 inhibits cell proliferation by targeting E2F2, MYC, and other cell-cycle genes via binding to "seedless" 3′UTR microRNA recognition elements. Mol Cell 35:610-625.
23. le Sage C, Nagel R, Agami R. 2007a. Diverse ways to control p27Kip1 function: miRNAs come into play. Cell Cycle 6:2742-2749.
24. le Sage C, Nagel R, Egan DA, Schrier M, Mesman E, Mangiola A, Anile C, Maira G, Mercatelli N, Ciafrè SA, Farace MG, Agami R. 2007b. Regulation of the p27(Kip1) tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation. EMBO J 26:3699-3708.
25. Liang J, Zubovitz J, Petrocelli T, Kotchetkov R, Connor MK, Han K, Lee JH, Ciarallo S, Catzavelos C, Beniston R, Franssen E, Slingerland JM. 2002. PKB/Akt phosphorylates p27, impairs nuclear import of p27 and opposes p27-mediated G1 arrest. Nat Med 8:1153-1160.
26. Lin SC, Liu CJ, Lin JA, Chiang WF, Hung PS, Chang KW. 2010. miR-24 up-regulation in oral carcinoma: Positive association from clinical and in vitro analysis. Oral Oncol 46:204-208.
27. Liu X, Wang A, Heidbreder CE, Jiang L, Yu J, Kolokythas A, Huang L, Dai Y, Zhou X. 2010. MicroRNA-24 targeting RNA-binding protein DND1 in tongue squamous cell carcinoma. FEBS Lett 584:4115-4120.
28. Loda M, Cukor B, Tam SW, Lavin P, Fiorentino M, Draetta GF, Jessup JM, Pagano M. 1997. Increased proteasome-dependent degradation of the cyclin-dependent kinase inhibitor p27 in aggressive colorectal carcinomas. Nat Med 3:231-234.
29. Malhas A, Saunders NJ, Vaux DJ. 2010. The nuclear envelope can control gene expression and cell cycle progression via miRNA regulation. Cell Cycle 9:531-539.
30. Malumbres M, Barbacid M. 2001. To cycle or not to cycle: A critical decision in cancer. Nat Rev Cancer 1:222-231.
31. Nymark P, Guled M, Borze I, Faisal A, Lahti L, Salmenkivi K, Kettunen E, Anttila S, Knuutila S. 2011. Integrative analysis of microRNA, mRNA and aCGH data reveals asbestos- and histology related changes in lung cancer. Genes Chromosomes Cancer 50:585-597.
32. Peters JM. 2006. The anaphase promoting complex/cyclosome: A machine designed to destroy. Nat Rev Mol Cell Biol 7:644-656.
33. Petrocca F, Visone R, Onelli MR, Shah MH, Nicoloso MS, de Martino I, Iliopoulos D, Pilozzi E, Liu CG, Negrini M, Cavazzini L, Volinia S, Alder H, Ruco LP, Baldassarre G, Croce CM, Vecchione A. 2008. E2F1-regulated microRNAs impair TGFbeta-dependent cell-cycle arrest and apoptosis in gastric cancer. Cancer Cell 13:272-286.
34. Poy MN, Eliasson L, Krutzfeldt J, Kuwajima S, Ma X, Macdonald PE, Pfeffer S, Tuschl T, Rajewsky N, Rorsman P, Stoffel M. 2004. A pancreatic islet-specific microRNA regulates insulin secretion. Nature 432:226-230.
35. Serrano M, Hannon GJ, Beach D. 1993. A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature 366:704-707.
36. Sherr CJ, Roberts JM. 1995. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev 9:1149-1163.
37. Slingerland J, Pagano M. 2000. Regulation of the cdk inhibitor p27 and its deregulation in cancer. J Cell Physiol 183:10-17.
38. Takagi S, Nakajima M, Kida K, Yamaura Y, Fukami T, Yokoi T. 2010. MicroRNAs regulate human hepatocyte nuclear factor 4alpha, modulating the expression of metabolic enzymes and cell cycle. J Biol Chem 285:4415-4422.
39. van Kouwenhove M, Kedde M, Agami R. 2011. MicroRNA regulation by RNA-binding proteins and its implications for cancer. Nat Rev Cancer 11:644-656.
40. Vecchione A, Croce CM. 2010. Apoptomirs: Small molecules have gained the license to kill. Endocr Relat Cancer 17:F37-F50.
41. Viglietto G, Motti ML, Fusco A. 2002. Understanding p27(kip1) deregulation in cancer: Down-regulation or mislocalization. Cell Cycle 1:394-400.
42. Visone R, Pallante P, Vecchione A, Cirombella R, Ferracin M, Ferraro A, Volinia S, Coluzzi S, Leone V, Borbone E, Liu CG, Petrocca F, Troncone G, Calin GA, Scarpa A, Colato C, Tallini G, Santoro M, Croce CM, Fusco A. 2007. Specific microRNAs are downregulated in human anaplastic carcinomas. Oncogene 26:7569-7595.
43. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, Prueitt RL, Yanaihara N, Lanza G, Scarpa A, Vecchione A, Negrini M, Harris CC, Croce CM. 2006. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 103:2257-2261.
44. Volgareva G, Zavalishina L, Andreeva Y, Frank G, Krutikova E, Golovina D, Bliev A, Spitkovsky D, Ermilova V, Kisseljov F. 2004. Protein p16 as a marker of dysplastic and neoplastic alterations in cervical epithelial cells. BMC Cancer 4:58.
45. Wang X, Gocek E, Liu CG, Studzinski GP. 2009. MicroRNAs181 regulate the expression of p27Kip1 in human myeloid leukemia cells induced to differentiate by 1, 25-dihydroxyvitamin D3. Cell Cycle 8:736-741 [Epub 2009 Mar 18].
46. Wu Q, Wang C, Lu Z, Guo L, Ge Q. 2012. Analysis of serum genome-wide microRNAs for breast cancer detection. Clin Chim Acta 413:1058-1065.
47. Xu W, Liu M, Peng X, Zhou P, Zhou J, Xu K, Xu H, Jiang S. 2013. miR-24-3p and miR-27a-3p promote cell proliferation in glioma cells via cooperative regulation of MXI1. Int J Oncol 42:757-766.
48. Zaidi SK, Dowdy CR, van Wijnen AJ, Lian JB, Raza A, Stein JL, Croce CM, Stein GS. 2009. Altered Runx1 subnuclear targeting enhances myeloid cell proliferation and blocks differentiation by activating a miR-24/MKP-7/MAPK network. Cancer Res 69:8249-8255 [Epub 2009 Oct 13].