Expression of miR-34c induces G2/M cell cycle arrest in breast cancer cells

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Achari, Chandrani ^a   Winslow, Sofia ^a   Ceder, Yvonne ^a   Larsson, Christer ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

Breast cancer cells; CDC23; Cell cycle arrest; miRNA 34c; PKC

Indexed keywords

ANAPHASE PROMOTING COMPLEX SUBUNIT 8; CYCLIN D1; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; MICRORNA; MICRORNA 34C; PROTEIN KINASE C ALPHA; UNCLASSIFIED DRUG; CDC23 PROTEIN, HUMAN; MIRN34 MICRORNA, HUMAN; THYMIDINE;

ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CANCER INHIBITION; CCND1 GENE; CDC23 GENE; CDK4 GENE; CDK6 GENE; CELL CYCLE REGULATION; CELL DEATH; CELL GROWTH; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOWN REGULATION; G2 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION REGULATION; PRKC ALPHA GENE; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING; BASAL CELL CARCINOMA; BREAST TUMOR; FEMALE; GENETICS; HUMAN; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

APC8 SUBUNIT, ANAPHASE-PROMOTING COMPLEX-CYCLOSOME; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; FEMALE; G2 PHASE CELL CYCLE CHECKPOINTS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; NEOPLASMS, BASAL CELL; THYMIDINE;

EID: 84904779571     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-538     Document Type: Article

References (50)

1. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
2. Guo H, Ingolia NT, Weissman JS, Bartel DP. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010, 466:835-840.
3. Cheng AM, Byrom MW, Shelton J, Ford LP. Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Res 2005, 33:1290-1297.
4. Kloosterman WP, Plasterk RH. The diverse functions of microRNAs in animal development and disease. Dev Cell 2006, 11:441-450.
5. Welch C, Chen Y, Stallings RL. MicroRNA-34a functions as a potential tumor suppressor by inducing apoptosis in neuroblastoma cells. Oncogene 2007, 26:5017-5022.
6. Bagchi A, Mills AA. The quest for the 1p36 tumor suppressor. Cancer Res 2008, 68:2551-2556.
7. Ellsworth RE, Vertrees A, Love B, Hooke JA, Ellsworth DL, Shriver CD. Chromosomal alterations associated with the transition from in situ to invasive breast cancer. Ann Surg Oncol 2008, 15:2519-2525.
8. Dahiya R, McCarville J, Lee C, Hu W, Kaur G, Carroll P, Deng G. Deletion of chromosome 11p15, p12, q22, q23-24 loci in human prostate cancer. Int J Cancer 1997, 72:283-288.
9. Rasio D, Negrini M, Manenti G, Dragani TA, Croce CM. Loss of heterozygosity at chromosome 11q in lung adenocarcinoma: identification of three independent regions. Cancer Res 1995, 55:3988-3991.
10. Hagman Z, Larne O, Edsjo A, Bjartell A, Ehrnstrom RA, Ulmert D, Lilja H, Ceder Y. miR-34c is downregulated in prostate cancer and exerts tumor suppressive functions. Int J Cancer 2010, 127:2768-2776.
11. Roy S, Levi E, Majumdar AP, Sarkar FH. Expression of miR-34 is lost in colon cancer which can be re-expressed by a novel agent CDF. J Hematol Oncol 2012, 5:58.
12. Garofalo M, Jeon YJ, Nuovo GJ, Middleton J, Secchiero P, Joshi P, Alder H, Nazaryan N, Di Leva G, Romano G, Crawford M, Nana-Sinkam P, Croce CM. MiR-34a/c-Dependent PDGFR-alpha/beta Downregulation Inhibits Tumorigenesis and Enhances TRAIL-Induced Apoptosis in Lung Cancer. PLoS One 2013, 8:e67581.
13. Cole KA, Attiyeh EF, Mosse YP, Laquaglia MJ, Diskin SJ, Brodeur GM, Maris JM. A functional screen identifies miR-34a as a candidate neuroblastoma tumor suppressor gene. Mol Cancer Res 2008, 6:735-742.
14. Javeri A, Ghaffarpour M, Taha MF, Houshmand M. Downregulation of miR-34a in breast tumors is not associated with either p53 mutations or promoter hypermethylation while it correlates with metastasis. Med Oncol 2013, 30:413.
15. Yang S, Li Y, Gao J, Zhang T, Li S, Luo A, Chen H, Ding F, Wang X, Liu Z. MicroRNA-34 suppresses breast cancer invasion and metastasis by directly targeting Fra-1. Oncogene 2013, 32:4294-4303.
16. Corney DC, Flesken-Nikitin A, Godwin AK, Wang W, Nikitin AY. MicroRNA-34b and MicroRNA-34c are targets of p53 and cooperate in control of cell proliferation and adhesion-independent growth. Cancer Res 2007, 67:8433-8438.
17. Sun F, Fu H, Liu Q, Tie Y, Zhu J, Xing R, Sun Z, Zheng X. Downregulation of CCND1 and CDK6 by miR-34a induces cell cycle arrest. FEBS Lett 2008, 582:1564-1568.
18. He L, He X, Lim LP, de Stanchina E, Xuan Z, Liang Y, Xue W, Zender L, Magnus J, Ridzon D, Jackson AL, Linsley PS, Chen C, Lowe SW, Cleary MA, Hannon GJ. A microRNA component of the p53 tumour suppressor network. Nature 2007, 447:1130-1134.
19. Toyota M, Suzuki H, Sasaki Y, Maruyama R, Imai K, Shinomura Y, Tokino T. Epigenetic silencing of microRNA-34b/c and B-cell translocation gene 4 is associated with CpG island methylation in colorectal cancer. Cancer Res 2008, 68:4123-4132.
20. Lujambio A, Calin GA, Villanueva A, Ropero S, Sanchez-Cespedes M, Blanco D, Montuenga LM, Rossi S, Nicoloso MS, Faller WJ, Gallagher WM, Eccles SA, Croce CM, Esteller M. A microRNA DNA methylation signature for human cancer metastasis. Proc Natl Acad Sci U S A 2008, 105:13556-13561.
21. Hagman Z, Haflidadottir BS, Ansari M, Persson M, Bjartell A, Edsjo A, Ceder Y. The tumour suppressor miR-34c targets MET in prostate cancer cells. Br J Cancer 2013, 109:1271-1278.
22. Migliore C, Petrelli A, Ghiso E, Corso S, Capparuccia L, Eramo A, Comoglio PM, Giordano S. MicroRNAs impair MET-mediated invasive growth. Cancer Res 2008, 68:10128-10136.
23. Enright AJ, John B, Gaul U, Tuschl T, Sander C, Marks DS. MicroRNA targets in Drosophila. Genome Biol 2003, 5:R1.
24. Maragkakis M, Reczko M, Simossis VA, Alexiou P, Papadopoulos GL, Dalamagas T, Giannopoulos G, Goumas G, Koukis E, Kourtis K, Vergoulis T, Koziris N, Sellis T, Tsanakas P, Hatzigeorgiou AG. DIANA-microT web server: elucidating microRNA functions through target prediction. Nucleic Acids Res 2009, 37:W273-W276.
25. Dweep H, Sticht C, Pandey P, Gretz N. miRWalk-database: prediction of possible miRNA binding sites by " walking" the genes of three genomes. J Biomed Inform 2011, 44:839-847.
26. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M, Rajewsky N. Combinatorial microRNA target predictions. Nat Genet 2005, 37:495-500.
27. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20.
28. Lonne GK, Cornmark L, Zahirovic IO, Landberg G, Jirstrom K, Larsson C. PKCalpha expression is a marker for breast cancer aggressiveness. Mol Cancer 2010, 9:76.
29. Ways DK, Kukoly CA, deVente J, Hooker JL, Bryant WO, Posekany KJ, Fletcher DJ, Cook PP, Parker PJ. MCF-7 breast cancer cells transfected with protein kinase C-alpha exhibit altered expression of other protein kinase C isoforms and display a more aggressive neoplastic phenotype. J Clin Invest 1995, 95:1906-1915.
30. Tam WL, Lu H, Buikhuisen J, Soh BS, Lim E, Reinhardt F, Wu ZJ, Krall JA, Bierie B, Guo W, Chen X, Liu XS, Brown M, Lim B, Weinberg RA. Protein Kinase C alpha Is a Central Signaling Node and Therapeutic Target for Breast Cancer Stem Cells. Cancer Cell 2013, 24:347-364.
31. Cannell IG, Kong YW, Johnston SJ, Chen ML, Collins HM, Dobbyn HC, Elia A, Kress TR, Dickens M, Clemens MJ, Heery DM, Gaestel M, Willis AE, Bushell M. p38 MAPK/MK2-mediated induction of miR-34c following DNA damage prevents Myc-dependent DNA replication. Proc Natl Acad Sci U S A 2010, 107:5375-5380.
32. Bommer GT, Gerin I, Feng Y, Kaczorowski AJ, Kuick R, Love RE, Zhai Y, Giordano TJ, Qin ZS, Moore BB, MacDougald OA, Cho KR, Fearon ER. p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr Biol 2007, 17:1298-1307.
33. Lal A, Thomas MP, Altschuler G, Navarro F, O'Day E, Li XL, Concepcion C, Han YC, Thiery J, Rajani DK, Deutsch A, Hofmann O, Ventura A, Hide W, Lieberman J. Capture of microRNA-bound mRNAs identifies the tumor suppressor miR-34a as a regulator of growth factor signaling. PLoS Genet 2011, 7:e1002363.
34. Di Leva G, Garofalo M, Croce CM. MicroRNAs in Cancer. Annu Rev Pathol 2013, 9:287-314.
35. Lodygin D, Tarasov V, Epanchintsev A, Berking C, Knyazeva T, Korner H, Knyazev P, Diebold J, Hermeking H. Inactivation of miR-34a by aberrant CpG methylation in multiple types of cancer. Cell Cycle 2008, 7:2591-2600.
36. Vrba L, Munoz-Rodriguez JL, Stampfer MR, Futscher BW. miRNA gene promoters are frequent targets of aberrant DNA methylation in human breast cancer. PLoS One 2013, 8:e54398.
37. Henrich KO, Schwab M, Westermann F. 1p36 tumor suppression-a matter of dosage?. Cancer Res 2012, 72:6079-6088.
38. Hampton GM, Mannermaa A, Winqvist R, Alavaikko M, Blanco G, Taskinen PJ, Kiviniemi H, Newsham I, Cavenee WK, Evans GA. Loss of heterozygosity in sporadic human breast carcinoma: a common region between 11q22 and 11q23.3. Cancer Res 1994, 54:4586-4589.
39. Pulido HA, Fakruddin MJ, Chatterjee A, Esplin ED, Beleno N, Martinez G, Posso H, Evans GA, Murty VV. Identification of a 6-cM minimal deletion at 11q23.1-23.2 and exclusion of PPP2R1B gene as a deletion target in cervical cancer. Cancer Res 2000, 60:6677-6682.
40. Li L, Yuan L, Luo J, Gao J, Guo J, Xie X. MiR-34a inhibits proliferation and migration of breast cancer through down-regulation of Bcl-2 and SIRT1. Clin Exp Med 2013, 13:109-117.
41. Hui C, Yujie F, Lijia Y, Long Y, Hongxia X, Yong Z, Jundong Z, Qianyong Z, Mantian M. MicroRNA-34a and microRNA-21 play roles in the chemopreventive effects of 3,6-dihydroxyflavone on 1-methyl-1-nitrosourea-induced breast carcinogenesis. Breast Cancer Res 2012, 14:R80.
42. Lee YM, Lee JY, Ho CC, Hong QS, Yu SL, Tzeng CR, Yang PC, Chen HW. miRNA-34b as a tumor suppressor in estrogen-dependent growth of breast cancer cells. Breast Cancer Res 2011, 13:R116.
43. Tarasov V, Jung P, Verdoodt B, Lodygin D, Epanchintsev A, Menssen A, Meister G, Hermeking H. Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest. Cell Cycle 2007, 6:1586-1593.
44. Li Y, Guessous F, Zhang Y, Dipierro C, Kefas B, Johnson E, Marcinkiewicz L, Jiang J, Yang Y, Schmittgen TD, Lopes B, Schiff D, Purow B, Abounader R. MicroRNA-34a inhibits glioblastoma growth by targeting multiple oncogenes. Cancer Res 2009, 69:7569-7576.
45. Yin D, Ogawa S, Kawamata N, Leiter A, Ham M, Li D, Doan NB, Said JW, Black KL, Phillip Koeffler H. miR-34a functions as a tumor suppressor modulating EGFR in glioblastoma multiforme. Oncogene 2013, 32:1155-1163.
46. Kofman AV, Kim J, Park SY, Dupart E, Letson C, Bao Y, Ding K, Chen Q, Schiff D, Larner J, Abounader R. microRNA-34a promotes DNA damage and mitotic catastrophe. Cell Cycle 2013, 12:3500-3511.
47. Yamakuchi M, Ferlito M, Lowenstein CJ. miR-34a repression of SIRT1 regulates apoptosis. Proc Natl Acad Sci U S A 2008, 105:13421-13426.
48. Liang X, Zhou D, Wei C, Luo H, Liu J, Fu R, Cui S. MicroRNA-34c enhances murine male germ cell apoptosis through targeting ATF1. PLoS One 2012, 7:e33861.
49. Yu F, Jiao Y, Zhu Y, Wang Y, Zhu J, Cui X, Liu Y, He Y, Park EY, Zhang H, Lv X, Ma K, Su F, Park JH, Song E. MicroRNA 34c gene down-regulation via DNA methylation promotes self-renewal and epithelial-mesenchymal transition in breast tumor-initiating cells. J Biol Chem 2012, 287:465-473.
50. Bader AG. miR-34 - a microRNA replacement therapy is headed to the clinic. Front Genet 2012, 3:120.