Butyrate inhibits pro-proliferative miR-92a by diminishing c-Myc-induced miR-17-92a cluster transcription in human colon cancer cells

Molecular Cancer

Volumn 14, Issue 1, 2015, Pages

  Hu, Shien ^a   Liu, Lan ^a   Chang, Eugene B ^b   Wang, Jian Ying ^a   Raufman, Jean Pierre ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Butyrate; C Myc; Colon cancer; HDAC inhibitor; MiR 92a; MiRNA; P57

Indexed keywords

ADENOVIRUS VECTOR; BUTYRIC ACID; CASPASE 3; CYCLIN DEPENDENT KINASE INHIBITOR 1C; MESSENGER RNA; MICRORNA; MICRORNA 17; MICRORNA 17 92A; MICRORNA 18A; MICRORNA 19A; MICRORNA 19B; MICRORNA 20A; MICRORNA 92A; MYC PROTEIN; ONCOPROTEIN; PROTEIN DROSHA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VALPROIC ACID; VORINOSTAT; BUTYRIC ACID DERIVATIVE; CDKN1C PROTEIN, HUMAN; HISTONE DEACETYLASE INHIBITOR;

ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; BINDING SITE; CANCER INHIBITION; CANCER TISSUE; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE SILENCING; HCT116 CELL LINE; HT 29 CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; LUCIFERASE ASSAY; MALE; MICROARRAY ANALYSIS; MUTATIONAL ANALYSIS; ONCOGENE; ONCOGENE C MYC; OPEN READING FRAME; P57 GENE; PROMOTER REGION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUNEL ASSAY; COLON TUMOR; DRUG EFFECTS; GENETICS; HCT 116 CELL LINE; HT-29 CELL LINE; METABOLISM; ONCOGENE MYC; PHYSIOLOGY;

APOPTOSIS; BUTYRATES; CELL PROLIFERATION; COLONIC NEOPLASMS; CYCLIN-DEPENDENT KINASE INHIBITOR P57; GENES, MYC; HCT116 CELLS; HISTONE DEACETYLASE INHIBITORS; HT29 CELLS; HUMANS; MICRORNAS;

EID: 84945237892     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/s12943-015-0450-x     Document Type: Article

References (54)

1. Cummings JH, Pomare EW, Branch WJ, Naylor CP, Macfarlane GT. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut. 1987;28(10):1221-7.
2. Chan AT, Giovannucci EL. Primary prevention of colorectal cancer. Gastroenterology. 2010;138(6):2029-43. e10.
3. Dahm CC, Keogh RH, Spencer EA, Greenwood DC, Key TJ, Fentiman IS, et al. Dietary fiber and colorectal cancer risk: a nested case-control study using food diaries. J Natl Cancer Inst. 2010;102(9):614-26.
4. Chen HM, Yu YN, Wang JL, Lin YW, Kong X, Yang CQ, et al. Decreased dietary fiber intake and structural alteration of gut microbiota in patients with advanced colorectal adenoma. Am J Clin Nutr. 2013;97(5):1044-52.
5. Wang T, Cai G, Qiu Y, Fei N, Zhang M, Pang X, et al. Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J. 2012;6(2):320-9.
6. Belcheva A, Irrazabal T, Robertson SJ, Streutker C, Maughan H, Rubino S, et al. Gut microbial metabolism drives transformation of MSH2-deficient colon epithelial cells. Cell. 2014;158(2):288-99.
7. Augenlicht LH, Mariadason JM, Wilson A, Arango D, Yang W, Heerdt BG, et al. Short chain fatty acids and colon cancer. J Nutr. 2002;132(12):3804S-8S.
8. Comalada M, Bailon E, de Haro O, Lara-Villoslada F, Xaus J, Zarzuelo A, et al. The effects of short-chain fatty acids on colon epithelial proliferation and survival depend on the cellular phenotype. J Cancer Res Clin Oncol. 2006;132(8):487-97.
9. Hinnebusch BF, Meng S, Wu JT, Archer SY, Hodin RA. The effects of shortchain fatty acids on human colon cancer cell phenotype are associated with histone hyperacetylation. J Nutr. 2002;132(5):1012-7.
10. Daly K, Shirazi-Beechey SP. Microarray analysis of butyrate regulated genes in colonic epithelial cells. DNA Cell Biol. 2006;25(1):49-62.
11. Mariani MR, Carpaneto EM, Ulivi M, Allfrey VG, Boffa LC. Correlation between butyrate-induced histone hyperacetylation turn-over and c-myc expression. J Steroid Biochem Mol Biol. 2003;86(2):167-71.
12. Krupitza G, Harant H, Dittrich E, Szekeres T, Huber H, Dittrich C. Sodium butyrate inhibits c-myc splicing and interferes with signal transduction in ovarian carcinoma cells. Carcinogenesis. 1995;16(5):1199-205.
13. Tichonicky L, Kruh J, Defer N. Sodium butyrate inhibits c-myc and stimulates c-fos expression in all the steps of the cell-cycle in hepatoma tissue cultured cells. Biol Cell. 1990;69(1):65-7.
14. Souleimani A, Asselin C. Regulation of c-myc expression by sodium butyrate in the colon carcinoma cell line Caco-2. FEBS Lett. 1993;326(1-3):45-50.
15. Hu S, Dong TS, Dalal SR, Wu F, Bissonnette M, Kwon JH, et al. The microbederived short chain fatty acid butyrate targets miRNA-dependent p21 gene expression in human colon cancer. PLoS One. 2011;6(1):e16221.
16. Kim YK, Yu J, Han TS, Park SY, Namkoong B, Kim DH, et al. Functional links between clustered microRNAs: suppression of cell-cycle inhibitors by microRNA clusters in gastric cancer. Nucleic Acids Res. 2009;37(5):1672-81.
17. Ota A, Tagawa H, Karnan S, Tsuzuki S, Karpas A, Kira S, et al. Identification and characterization of a novel gene, C13orf25, as a target for 13q31-q32 amplification in malignant lymphoma. Cancer Res. 2004;64(9):3087-95.
18. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, et al. A microRNA polycistron as a potential human oncogene. Nature. 2005;435(7043):828-33.
19. Ji M, Rao E, Ramachandrareddy H, Shen Y, Jiang C, Chen J, et al. The miR-17-92 microRNA cluster is regulated by multiple mechanisms in B-cell malignancies. Am J Pathol. 2011;179(4):1645-56.
20. Sylvestre Y, De Guire V, Querido E, Mukhopadhyay UK, Bourdeau V, Major F, et al. An E2F/miR-20a autoregulatory feedback loop. J Biol Chem. 2007;282(4):2135-43.
21. Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, et al. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell. 2008;132(5):875-86.
22. Olive V, Bennett MJ, Walker JC, Ma C, Jiang I, Cordon-Cardo C, et al. miR-19 is a key oncogenic component of mir-17-92. Genes Dev. 2009;23(24):2839-49.
23. O'Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT. c-Myc-regulated microRNAs modulate E2F1 expression. Nature. 2005;435(7043):839-43.
24. Dews M, Homayouni A, Yu D, Murphy D, Sevignani C, Wentzel E, et al. Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet. 2006;38(9):1060-5.
25. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, et al. MicroRNA expression profiles classify human cancers. Nature. 2005;435(7043):834-8.
26. Humphreys KJ, Cobiac L, Le Leu RK, Van der Hoek MB, Michael MZ. Histone deacetylase inhibition in colorectal cancer cells reveals competing roles for members of the oncogenic miR-17-92 cluster. Mol Carcinog. 2013;52(6):459-74.
27. Zeiner GM, Norman KL, Thomson JM, Hammond SM, Boothroyd JC. Toxoplasma gondii infection specifically increases the levels of key host microRNAs. PLoS One. 2010;5(1):e8742.
28. Mu P, Han YC, Betel D, Yao E, Squatrito M, Ogrodowski P, et al. Genetic dissection of the miR-17 ~ 92 cluster of microRNAs in Myc-induced B-cell lymphomas. Genes Dev. 2009;23(24):2806-11.
29. Pospisil V, Vargova K, Kokavec J, Rybarova J, Savvulidi F, Jonasova A, et al. Epigenetic silencing of the oncogenic miR-17-92 cluster during PU.1-directed macrophage differentiation. EMBO J. 2011;30(21):4450-64.
30. Thomas M, Lange-Grunweller K, Hartmann D, Golde L, Schlereth J, Streng D, et al. Analysis of Transcriptional Regulation of the Human miR-17-92 Cluster; Evidence for Involvement of Pim-1. Int J Mol Sci. 2013;14(6):12273-96.
31. Davie JR. Inhibition of histone deacetylase activity by butyrate. J Nutr. 2003;133(7 Suppl):2485S-93S.
32. Richon VM, Sandhoff TW, Rifkind RA, Marks PA. Histone deacetylase inhibitor selectively induces p21WAF1 expression and gene-associated histone acetylation. Proc Natl Acad Sci U S A. 2000;97(18):10014-9.
33. Shin S, Lee EM, Cha HJ, Bae S, Jung JH, Lee SM, et al. MicroRNAs that respond to histone deacetylase inhibitor SAHA and p53 in HCT116 human colon carcinoma cells. Int J Oncol. 2009;35(6):1343-52.
34. Dejligbjerg M, Grauslund M, Litman T, Collins L, Qian X, Jeffers M, et al. Differential effects of class I isoform histone deacetylase depletion and enzymatic inhibition by belinostat or valproic acid in HeLa cells. Mol Cancer. 2008;7:70.
35. Sengupta S, Nie J, Wagner RJ, Yang C, Stewart R, Thomson JA. MicroRNA 92b controls the G1/S checkpoint gene p57 in human embryonic stem cells. Stem Cells. 2009;27(7):1524-8.
36. Mogilyansky E, Rigoutsos I. The miR-17/92 cluster: a comprehensive update on its genomics, genetics, functions and increasingly important and numerous roles in health and disease. Cell Death Differ. 2013;20(12):1603-14.
37. Kavanagh E, Joseph B. The hallmarks of CDKN1C (p57, KIP2) in cancer. Biochim Biophys Acta. 2011;1816(1):50-6.
38. Woods K, Thomson JM, Hammond SM. Direct regulation of an oncogenic micro-RNA cluster by E2F transcription factors. J Biol Chem. 2007;282(4):2130-4.
39. Choi KH, Basma H, Singh J, Cheng PW. Activation of CMV promotercontrolled glycosyltransferase and beta-galactosidase glycogenes by butyrate, tricostatin A, and 5-aza-2'-deoxycytidine. Glycoconj J. 2005;22(1-2):63-9.
40. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet. 2010;11(9):597-610.
41. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116(2):281-97.
42. Denli AM, Tops BB, Plasterk RH, Ketting RF, Hannon GJ. Processing of primary microRNAs by the Microprocessor complex. Nature. 2004;432(7014):231-5.
43. Yi R, Qin Y, Macara IG, Cullen BR. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 2003;17(24):3011-6.
44. Tsuchida A, Ohno S, Wu W, Borjigin N, Fujita K, Aoki T, et al. miR-92 is a key oncogenic component of the miR-17-92 cluster in colon cancer. Cancer Sci. 2011;102(12):2264-71.
45. Noura S, Yamamoto H, Sekimoto M, Takemasa I, Miyake Y, Ikenaga M, et al. Expression of second class of KIP protein p57KIP2 in human colorectal carcinoma. Int J Oncol. 2001;19(1):39-47.
46. Li JQ, Wu F, Usuki H, Kubo A, Masaki T, Fujita J, et al. Loss of p57KIP2 is associated with colorectal carcinogenesis. Int J Oncol. 2003;23(6):1537-43.
47. Fornari FF, Gramantieri L, Ferracin M, Veronese A, Sabbioni S, Calin GA, et al. MiR-221 controls CDKN1C/p57 and CDKN1B/p27 expression in human hepatocellular carcinoma. Oncogene. 2008;27(43):5651-61.
48. Liu X, Cheng Y, Zhang S, Lin Y, Yang J, Zhang C. A necessary role of miR-221 and miR-222 in vascular smooth muscle cell proliferation and neointimal hyperplasia. Circ Res. 2009;104(4):476-87.
49. Sun K, Wang W, Zeng JJ, Wu CT, Lei ST, Li GX. MicroRNA-221 inhibits CDKN1C/p57 expression in human colorectal carcinoma. Acta Pharmacol Sin. 2011;32(3):375-84.
50. Shin JY, Kim HS, Park J, Park JB, Lee JY. Mechanism for inactivation of the KIP family cyclin-dependent kinase inhibitor genes in gastric cancer cells. Cancer Res. 2000;60(2):262-5.
51. Cucciolla V, Borriello A, Criscuolo M, Sinisi AA, Bencivenga D, Tramontano A, et al. Histone deacetylase inhibitors upregulate p57Kip2 level by enhancing its expression through Sp1 transcription factor. Carcinogenesis. 2008;29(3):560-7.
52. Davoren PA, McNeill RE, Lowery AJ, Kerin MJ, Miller N. Identification of suitable endogenous control genes for microRNA gene expression analysis in human breast cancer. BMC Mol Biol. 2008;9:76.
53. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3(6):1101-8.
54. Liu L, Rao JN, Zou T, Xiao L, Wang PY, Turner DJ, et al. Polyamines regulate c-Myc translation through Chk2-dependent HuR phosphorylation. Mol Biol Cell. 2009;20(23):4885-98.