Histone deacetylase inhibition in colorectal cancer cells reveals competing roles for members of the oncogenic miR-17-92 cluster

Molecular Carcinogenesis

Volumn 52, Issue 6, 2013, Pages 459-474

  Humphreys, Karen J ^a   Cobiac, Lynne ^a,b   Le Leu, Richard K ^a,b   Van der Hoek, Mark B ^c,d   Michael, Michael Z ^a  

^a FLINDERS MEDICAL CENTRE   (Australia)

^b CSIRO   (Australia)

^c Adelaide Microarray Centre   (Australia)

^d UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Butyrate; Colorectal cancer; Epigenetic; Histone deacetylase inhibitors; MicroRNAs; MiR 17 92

Indexed keywords

BCL2L11 PROTEIN; BUTYRIC ACID; CYCLIN DEPENDENT KINASE 19; CYCLIN DEPENDENT KINASE INHIBITOR 1A; HISTONE DEACETYLASE; MICRORNA; NEDD9 PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; TRICHOSTATIN A; UNCLASSIFIED DRUG; VORINOSTAT;

APOPTOSIS; ARTICLE; CANCER CELL; CANCER CHEMOTHERAPY; CARCINOGENESIS; CELL PROLIFERATION; CELL STRAIN HCT116; CELL STRAIN HT29; COLORECTAL CANCER; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; ENZYME INHIBITION; EPIGENETICS; GENE CLUSTER; GENE EXPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADENOCARCINOMA; APOPTOSIS REGULATORY PROTEINS; BUTYRIC ACID; COLORECTAL NEOPLASMS; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HCT116 CELLS; HISTONE DEACETYLASE INHIBITORS; HT29 CELLS; HUMANS; HYDROXAMIC ACIDS; MEMBRANE PROTEINS; MICRORNAS; PHOSPHOPROTEINS; PROTO-ONCOGENE PROTEINS; PTEN PHOSPHOHYDROLASE; RNA, MESSENGER; TRANSFECTION;

EID: 84876425427     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.21879     Document Type: Article

References (53)

1. Bingham SA, Day NE, Luben R, et al. Dietary fibre in food and protection against colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC): An observational study. Lancet 2003; 361: 1496- 1501.
2. WCRF, AICR, editors. Food, nutrition, physical activity and the prevention of cancer: A global perspective. Washington DC: AICR; 2007.
3. Young GP, Hu Y, Le Leu RK, Nyskohus L. Dietary fibre and colorectal cancer: A model for environment-gene interactions. Mol Nutr Food Res 2005; 49: 571- 584.
4. Sealy L, Chalkley R. The effect of sodium butyrate on histone modification. Cell 1978; 14: 115- 121.
5. Hinnebusch BF, Meng S, Wu JT, Archer SY, Hodin RA. The effects of short-chain fatty acids on human colon cancer cell phenotype are associated with histone hyperacetylation. J Nutr 2002; 132: 1012- 1017.
6. Mariadason JM, Corner GA, Augenlicht LH. Genetic reprogramming in pathways of colonic cell maturation induced by short chain fatty acids: Comparison with trichostatin A, sulindac, and curcumin and implications for chemoprevention of colon cancer. Cancer Res 2000; 60: 4561- 4572.
7. Medina V, Afonso JJ, Alvarez-Arguelles H, Hernandez C, Gonzalez F. Sodium butyrate inhibits carcinoma development in a 1, 2-dimethylhydrazine-induced rat colon cancer. JPEN J Parenter Enteral Nutr 1998; 22: 14- 17.
8. Kameue C, Tsukahara T, Yamada K, et al. Dietary sodium gluconate protects rats from large bowel cancer by stimulating butyrate production. J Nutr 2004; 134: 940- 944.
9. Le Leu RK, Brown IL, Hu Y, Esterman A, Young GP. Suppression of azoxymethane-induced colon cancer development in rats by dietary resistant starch. Cancer Biol Ther 2007; 6: 1621- 1626.
10. Daly K, Shirazi-Beechey SP. Microarray analysis of butyrate regulated genes in colonic epithelial cells. DNA Cell Biol 2006; 25: 49- 62.
11. Wilson AJ, Chueh AC, Togel L, et al. Apoptotic sensitivity of colon cancer cells to histone deacetylase inhibitors is mediated by an Sp1/Sp3-activated transcriptional program involving immediate-early gene induction. Cancer Res 2010; 70: 609- 620.
12. Iacomino G, Tecce MF, Grimaldi C, Tosto M, Russo GL. Transcriptional response of a human colon adenocarcinoma cell line to sodium butyrate. Biochem Biophys Res Commun 2001; 285: 1280- 1289.
13. LaBonte MJ, Wilson PM, Fazzone W, Groshen S, Lenz H-J, Ladner RD. DNA microarray profiling of genes differentially regulated by the histone deacetylase inhibitors vorinostat and LBH589 in colon cancer cell lines. BMC Med Genomics 2009; 2: 67.
14. Siavoshian S, Segain JP, Kornprobst M, et al. Butyrate and trichostatin A effects on the proliferation/differentiation of human intestinal epithelial cells: Induction of cyclin D3 and p21 expression. Gut 2000; 46: 507- 514.
15. Hutvagner G, Zamore PD. A microRNA in a multiple-turnover RNAi enzyme complex. Science 2002; 297: 2056- 2060.
16. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: Are the answers in sight? Nat Rev Genet 2008; 9: 102- 114.
17. Guo H, Ingolia NT, Weissman JS, Bartel DP. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010; 466: 835- 840.
18. Slattery ML, Wolff E, Hoffman MD, Pellatt DF, Milash B, Wolff RK. MicroRNAs and colon and rectal cancer: Differential expression by tumor location and subtype. Genes Chromosomes Cancer 2011; 50: 196- 206.
19. Lu J, Getz G, Miska EA, et al. MicroRNA expression profiles classify human cancers. Nature 2005; 435: 834- 838.
20. Cummins JM, He Y, Leary RJ, et al. The colorectal microRNAome. Proc Natl Acad Sci USA 2006; 103: 3687- 3692.
21. Chen X, Guo X, Zhang H, et al. Role of miR-143 targeting KRAS in colorectal tumorigenesis. Oncogene 2009; 28: 1385- 1392.
22. Michael MZ, O' Connor SM, van Holst Pellekaan NG, Young GP, James RJ. Reduced accumulation of specific microRNAs in colorectal neoplasia. Mol Cancer Res 2003; 1: 882- 891.
23. Slaby O, Svoboda M, Michalek J, Vyzula R. MicroRNAs in colorectal cancer: Translation of molecular biology into clinical application. Mol Cancer 2009; 8: 102.
24. Slaby O, Svoboda M, Fabian P, et al. Altered expression of miR-21, miR-31, miR-143 and miR-145 is related to clinicopathologic features of colorectal cancer. Oncology 2007; 72: 397- 402.
25. Diosdado B, van de Wiel MA, Terhaar Sive Droste JS, et al. MiR-17-92 cluster is associated with 13q gain and c-myc expression during colorectal adenoma to adenocarcinoma progression. Br J Cancer 2009; 101: 707- 714.
26. He L, Thomson JM, Hemann MT, et al. A microRNA polycistron as a potential human oncogene. Nature 2005; 435: 828- 833.
27. Tanzer A, Stadler PF. Molecular evolution of a microRNA cluster. J Mol Biol 2004; 339: 327- 335.
28. Saito Y, Jones PA. Epigenetic activation of tumor suppressor microRNAs in human cancer cells. Cell Cycle 2006; 5: 2220- 2222.
29. Lujambio A, Calin GA, Villanueva A, et al. A microRNA DNA methylation signature for human cancer metastasis. Proc Natl Acad Sci USA 2008; 105: 13556- 13561.
30. Bandres E, Agirre X, Bitarte N, et al. Epigenetic regulation of microRNA expression in colorectal cancer. Int J Cancer 2009; 125: 2737- 2743.
31. Li C-J, Li RW, Elsasser TH. MicroRNA, (miRNA) expression is regulated by butyrate-induced epigenetic modulation of gene expression in bovine cells. Genet Epigenetics 2010; 3: 23- 32.
32. Hu S, Dong TS, Dalal SR, et al. The microbe-derived short chain fatty acid butyrate targets miRNA-dependent p21 gene expression in human colon cancer. PLoS ONE 2011; 6: e16221.
33. Shin S, Lee E-M, Cha HJ, et al. MicroRNAs that respond to histone deacetylase inhibitor SAHA and p53 in HCT116 human colon carcinoma cells. Int J Oncol 2009; 35: 1343- 1352.
34. Thomson JM, Parker J, Perou CM, Hammond SM. A custom microarray platform for analysis of microRNA gene expression. Nat Methods 2004; 1: 47- 53.
35. Smyth GK. Limma: Linear models for microarray data. In: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W, editors. Bioinformatics and computational biology solutions using R and bioconductor. New York: Springer; 2005. pp. 397- 420.
36. Muller PY, Janovjak H, Miserez AR, Dobbie Z. Processing of gene expression data generated by quantitative real-time RT-PCR. Biotechniques 2002; 32: 1372- 1374 [Erratum appears in Biotechniques. 2002 Sep;33(3):514].
37. Megraw M, Sethupathy P, Corda B, Hatzigeorgiou AG. miRGen: A database for the study of animal microRNA genomic organization and function. Nucleic Acids Res 2007; 35: (Database issue): D149- D155.
38. Mu P, Han Y-C, Betel D, et al. Genetic dissection of the miR-17∼92 cluster of microRNAs in Myc-induced B-cell lymphomas. Genes Dev 2009; 23: 2806- 2811.
39. Ventura A, Young AG, Winslow MM, et al. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 2008; 132: 875- 886.
40. Petrocca F, Visone R, Onelli MR, et al. E2F1-regulated microRNAs impair TGFbeta-dependent cell-cycle arrest and apoptosis in gastric cancer. Cancer Cell 2008; 13: 272- 286.
41. Olive V, Bennett MJ, Walker JC, et al. miR-19 is a key oncogenic component of mir-17-92. Genes Dev 2009; 23: 2839- 2849.
42. Inomata M, Tagawa H, Guo Y-M, Kameoka Y, Takahashi N, Sawada K. MicroRNA-17-92 down-regulates expression of distinct targets in different B-cell lymphoma subtypes. Blood 2009; 113: 396- 402.
43. O'Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 2005; 435: 839- 843.
44. Woods K, Thomson JM, Hammond SM. Direct regulation of an oncogenic micro-RNA cluster by E2F transcription factors. J Biol Chem 2007; 282: 2130- 2134.
45. Hayashita Y, Osada H, Tatematsu Y, et al. A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res 2005; 65: 9628- 9632.
46. Rada-Iglesias A, Enroth S, Ameur A, et al. Butyrate mediates decrease of histone acetylation centered on transcription start sites and down-regulation of associated genes. Genome Res 2007; 17: 708- 719.
47. Hinnebusch BF, Henderson JW, Siddique A, et al. Transcriptional activation of the enterocyte differentiation marker intestinal alkaline phosphatase is associated with changes in the acetylation state of histone H3 at a specific site within its promoter region in vitro. J Gastrointest Surg 2003; 7: 237- 244 (discussion 244-235).
48. Yan H-l, Xue G, Mei Q, et al. Repression of the miR-17-92 cluster by p53 has an important function in hypoxia-induced apoptosis. EMBO J 2009; 28: 2719- 2732.
49. Tsang WP, Kwok TT. The miR-18a* microRNA functions as a potential tumor suppressor by targeting on K-Ras. Carcinogenesis 2009; 30: 953- 959.
50. Li Y, Bavarva JH, Wang Z, et al. HEF1, a novel target of Wnt signaling, promotes colonic cell migration and cancer progression. Oncogene 2011; 30: 2633- 2643.
51. Xia D, Holla VR, Wang D, Menter DG, DuBois RN. HEF1 is a crucial mediator of the proliferative effects of prostaglandin E(2) on colon cancer cells. Cancer Res 2010; 70: 824- 831.
52. Malumbres M, Harlow E, Hunt T, et al. Cyclin-dependent kinases: A family portrait. Nat Cell Biol 2009; 11: 1275- 1276.
53. Firestein R, Bass AJ, Kim SY, et al. CDK8 is a colorectal cancer oncogene that regulates beta-catenin activity. Nature 2008; 455: 547- 551.