MIR-29b Downregulates Canonical Wnt Signaling by Suppressing Coactivators of β-Catenin in Human Colorectal Cancer Cells

Journal of Cellular Biochemistry

Volumn 115, Issue 11, 2014, Pages 1974-1984

  Subramanian, Maitreyi ^a   Rao, Srinivasa R ^a,b   Thacker, Pooja ^a   Chatterjee, Suvro ^c   Karunagaran, Devarajan ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY MADRAS   (India)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c ANNA UNIVERSITY   (India)

Author keywords

ANGIOGENESIS; BCL9L; COLORECTAL CANCER; MIR 29b; SNAIL; TCF7L2; Wnt SIGNALING

Indexed keywords

BETA CATENIN; MICRORNA 29B; PROTEIN P53; TRANSCRIPTION FACTOR 7 LIKE 2; TRANSCRIPTION FACTOR SNAIL; UVOMORULIN; BCL9L PROTEIN, HUMAN; CTNNB1 PROTEIN, HUMAN; DNA BINDING PROTEIN; MICRORNA; MIRN29 MICRORNA, HUMAN; SNAIL FAMILY TRANSCRIPTION FACTORS; TCF7L2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

3' UNTRANSLATED REGION; ARTICLE; CELL GROWTH; COLORECTAL CANCER; DOWN REGULATION; ECTOPIC EXPRESSION; ENDOTHELIUM CELL; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSACTIVATION; WESTERN BLOTTING; WNT SIGNALING PATHWAY; COLORECTAL TUMOR; GENE EXPRESSION REGULATION; GENETICS; HCT116 CELL LINE; HEK293 CELL LINE; METABOLISM; TUMOR CELL LINE;

BETA CATENIN; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; DNA-BINDING PROTEINS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HCT116 CELLS; HEK293 CELLS; HUMANS; MICRORNAS; TRANSCRIPTION FACTOR 7-LIKE 2 PROTEIN; TRANSCRIPTION FACTORS; WNT SIGNALING PATHWAY;

EID: 84941074765     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24869     Document Type: Article

References (57)

1. Amodio N, Di Martino MT, Foresta U, Leone E, Lionetti M, Leotta M, Gulla AM, Pitari MR, Conforti F, Rossi M, Agosti V, Fulciniti M, Misso G, Morabito F, Ferrarini M, Neri A, Caraglia M, Munshi NC, Anderson KC, Tagliaferri P, Tassone P,. 2012. MiR-29b sensitizes multiple myeloma cells to bortezomib-induced apoptosis through the activation of a feedback loop with the transcription factor Sp1. Cell Death Dis 3: e436.
2. Brembeck FH, Schwarz-Romond T, Bakkers J, Wilhelm S, Hammerschmidt M, Birchmeier W,. 2004. Essential role of BCL9-2 in the switch between beta-catenin's adhesive and transcriptional functions. Genes Dev 18: 2225-2230.
3. Chou J, Lin JH, Brenot A, Kim JW, Provot S, Werb Z,. 2013. GATA3 suppresses metastasis and modulates the tumour microenvironment by regulating microRNA-29b expression. Nat Cell Biol 15: 201-213.
4. Clevers H,. 2006. Wnt/beta-catenin signaling in development and disease. Cell 127: 469-480.
5. DasGupta R, Kaykas A, Moon RT, Perrimon N,. 2005. Functional genomic analysis of the Wnt-wingless signaling pathway. Science 308: 826-833.
6. de Herreros AG, Peiro S, Nassour M, Savagner P,. 2010. Snail family regulation and epithelial mesenchymal transitions in breast cancer progression. J Mammary Gland Biol Neoplasia 15: 135-147.
7. de la Roche M, Worm J, Bienz M,. 2008. The function of BCL9 in Wnt/beta-catenin signaling and colorectal cancer cells. BMC Cancer 8: 199.
8. Dyer BW, Ferrer FA, Klinedinst DK, Rodriguez R,. 2000. A noncommercial dual luciferase enzyme assay system for reporter gene analysis. Anal Biochem 282: 158-161.
9. Fang JH, Zhou HC, Zeng C, Yang J, Liu Y, Huang X, Zhang JP, Guan XY, Zhuang SM,. 2011. MicroRNA-29b suppresses tumor angiogenesis, invasion, and metastasis by regulating matrix metalloproteinase 2 expression. Hepatology 54: 1729-1740.
10. Friedman RC, Farh KK, Burge CB, Bartel DP,. 2009. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19: 92-105.
11. Gilles C, Polette M, Mestdagt M, Nawrocki-Raby B, Ruggeri P, Birembaut P, Foidart JM,. 2003. Transactivation of vimentin by beta-catenin in human breast cancer cells. Cancer Res 63: 2658-2664.
12. Gottardi CJ, Wong E, Gumbiner BM,. 2001. E-cadherin suppresses cellular transformation by inhibiting beta-catenin signaling in an adhesion-independent manner. J Cell Biol 153: 1049-1060.
13. Gradl D, Kuhl M, Wedlich D,. 1999. The Wnt/Wg signal transducer beta-catenin controls fibronectin expression. Mol Cell Biol 19: 5576-5587.
14. Graham TA, Ferkey DM, Mao F, Kimelman D, Xu W,. 2001. Tcf4 can specifically recognize beta-catenin using alternative conformations. Nat Struct Biol 8: 1048-1052.
15. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B, Kinzler KW,. 1998. Identification of c-MYC as a target of the APC pathway. Science 281: 1509-1512.
16. Huang K, Zhang JX, Han L, You YP, Jiang T, Pu PY, Kang CS,. 2010. MicroRNA roles in beta-catenin pathway. Mol Cancer 9: 252.
17. Hwang WL, Yang MH, Tsai ML, Lan HY, Su SH, Chang SC, Teng HW, Yang SH, Lan YT, Chiou SH, Wang HW,. 2011. SNAIL regulates interleukin-8 expression, stem cell-like activity, and tumorigenicity of human colorectal carcinoma cells. Gastroenterology 291 (291): e1-e5.
18. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS,. 2004. Human MicroRNA targets. PLoS Biol 2: e363.
19. Kapinas K, Kessler C, Ricks T, Gronowicz G, Delany AM,. 2010. MiR-29 modulates Wnt signaling in human osteoblasts through a positive feedback loop. J Biol Chem 285: 25221-25231.
20. Kim PJ, Plescia J, Clevers H, Fearon ER, Altieri DC,. 2003. Survivin and molecular pathogenesis of colorectal cancer. Lancet 362: 205-209.
21. Kuo TY, Hsi E, Yang IP, Tsai PC, Wang JY, Juo SH,. 2012. Computational analysis of mRNA expression profiles identifies microRNA-29a/c as predictor of colorectal cancer early recurrence. PLoS One 7: e31587.
22. Larson EM, Doughman DJ, Gregerson DS, Obritsch WF,. 1997. A new, simple, nonradioactive, nontoxic in vitro assay to monitor corneal endothelial cell viability. Invest Ophthalmol Vis Sci 38: 1929-1933.
23. Le NH, Franken P, Fodde R,. 2008. Tumour-stroma interactions in colorectal cancer: converging on beta-catenin activation and cancer stemness. Br J Cancer 98: 1886-1893.
24. Lewis BP, Burge CB, Bartel DP,. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20.
25. Li Z, Hassan MQ, Jafferji M, Aqeilan RI, Garzon R, Croce CM, van Wijnen AJ, Stein JL, Stein GS, Lian JB,. 2009. Biological functions of miR-29b contribute to positive regulation of osteoblast differentiation. J Biol Chem 284: 15676-15684.
26. Lin Z, Yin Q, Flemington E,. 2004. Identification of a negative regulatory element in the Epstein-Barr virus Zta transactivation domain that is regulated by the cell cycle control factors c-Myc and E2F1. J Virol 78: 11962-11971.
27. Liu W, Dong X, Mai M, Seelan RS, Taniguchi K, Krishnadath KK, Halling KC, Cunningham JM, Boardman LA, Qian C, Christensen E, Schmidt SS, Roche PC, Smith DI, Thibodeau SN,. 2000. Mutations in AXIN2 cause colorectal cancer with defective mismatch repair by activating beta-catenin/TCF signalling. Nat Genet 26: 146-147.
28. Liu Y, Huang T, Zhao X, Cheng L,. 2011. MicroRNAs modulate the Wnt signaling pathway through targeting its inhibitors. Biochem Biophys Res Commun 408: 259-264.
29. Luna C, Li G, Qiu J, Epstein DL, Gonzalez P,. 2009. Role of miR-29b on the regulation of the extracellular matrix in human trabecular meshwork cells under chronic oxidative stress. Mol Vis 15: 2488-2497.
30. MacDonald BT, Tamai K, He X,. 2009. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 17: 9-26.
31. Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, Vogelstein B, Kinzler KW,. 1997. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275: 1787-1790.
32. Mott JL, Kobayashi S, Bronk SF, Gores GJ,. 2007. Mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene 26: 6133-6140.
33. Park SY, Lee JH, Ha M, Nam JW, Kim VN,. 2009. MiR-29 miRNAs activate p53 by targeting p85 alpha and CDC42. Nat Struct Mol Biol 16: 23-29.
34. Pekarsky Y, Croce CM,. 2010. Is miR-29 an oncogene or tumor suppressor in CLL? Oncotarget 1: 224-227.
35. Pekarsky Y, Santanam U, Cimmino A, Palamarchuk A, Efanov A, Maximov V, Volinia S, Alder H, Liu CG, Rassenti L, Calin GA, Hagan JP, Kipps T, Croce CM,. 2006. Tcl1 expression in chronic lymphocytic leukemia is regulated by miR-29 and miR-181. Cancer Res 66: 11590-11593.
36. Pereira DM, Rodrigues PM, Borralho PM, Rodrigues CM,. 2013. Delivering the promise of miRNA cancer therapeutics. Drug Discov Today 18: 282-289.
37. Petersen CP, Reddien PW,. 2009. Wnt signaling and the polarity of the primary body axis. Cell 139: 1056-1068.
38. Rodrigues NR, Rowan A, Smith ME, Kerr IB, Bodmer WF, Gannon JV, Lane DP,. 1990. P53 mutations in colorectal cancer. Proc Natl Acad Sci USA 87: 7555-7559.
39. Rother K, Johne C, Spiesbach K, Haugwitz U, Tschop K, Wasner M, Klein-Hitpass L, Moroy T, Mossner J, Engeland K,. 2004. Identification of Tcf-4 as a transcriptional target of p53 signalling. Oncogene 23: 3376-3384.
40. Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP,. 2011. A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 146: 353-358.
41. Sambrook J, Russell DW,. 2006. Assay for beta-galactosidase in Extracts of Mammalian Cells. CSH Protoc.
42. Schepeler T,. 2013. Emerging roles of microRNAs in the Wnt signaling network. Crit Rev Oncog 18: 357-371.
43. Shukla GC, Singh J, Barik S,. 2011. MicroRNAs: Processing, maturation, target recognition and regulatory functions. Mol Cell Pharmacol 3: 83-92.
44. Stambolic V, Ruel L, Woodgett JR,. 1996. Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr Biol 6: 1664-1668.
45. Steele R, Mott JL, Ray RB,. 2010. MBP-1 upregulates miR-29b that represses Mcl-1, collagens, and matrix-metalloproteinase-2 in prostate cancer cells. Genes Cancer 1: 381-387.
46. Stemmer V, de Craene B, Berx G, Behrens J,. 2008. Snail promotes Wnt target gene expression and interacts with beta-catenin. Oncogene 27: 5075-5080.
47. Takada K, Zhu D, Bird GH, Sukhdeo K, Zhao JJ, Mani M, Lemieux M, Carrasco DE, Ryan J, Horst D, Fulciniti M, Munshi NC, Xu W, Kung AL, Shivdasani RA, Walensky LD, Carrasco DR,. 2012. Targeted disruption of the BCL9/beta-catenin complex inhibits oncogenic Wnt signaling. Sci Transl Med 4:148ra 117.
48. Tetsu O, McCormick F,. 1999. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398: 422-426.
49. Veeman MT, Slusarski DC, Kaykas A, Louie SH, Moon RT,. 2003. Zebrafish prickle, a modulator of noncanonical Wnt/Fz signaling, regulates gastrulation movements. Curr Biol 13: 680-685.
50. Villarreal G, Jr., Oh DJ, Kang MH, Rhee DJ,. 2011. Coordinated regulation of extracellular matrix synthesis by the microRNA-29 family in the trabecular meshwork. Invest Ophthalmol Vis Sci 52: 3391-3397.
51. Wong MH, Rubinfeld B, Gordon JI,. 1998. Effects of forced expression of an NH2-terminal truncated beta-Catenin on mouse intestinal epithelial homeostasis. J Cell Biol 141: 765-777.
52. Yang LH, Xu HT, Han Y, Li QC, Liu Y, Zhao Y, Yang ZQ, Dong QZ, Miao Y, Dai SD, Wang EH,. 2010. Axin downregulates TCF-4 transcription via beta-catenin, but not p53, and inhibits the proliferation and invasion of lung cancer cells. Mol Cancer 9: 25.
53. Yang J, Zhang W, Evans PM, Chen X, He X, Liu C,. 2006. Adenomatous polyposis coli (APC) differentially regulates beta-catenin phosphorylation and ubiquitination in colon cancer cells. J Biol Chem 281: 17751-17757.
54. Yu PN, Yan MD, Lai HC, Huang RL, Chou YC, Lin WC, Yeh LT, Lin YW,. 2013. Downregulation of miR-29 contributes to cisplatin resistance of ovarian cancer cells. Int J Cancer 134: 542-551.
55. Zhang X, Gaspard JP, Chung DC,. 2001. Regulation of vascular endothelial growth factor by the Wnt and K-ras pathways in colonic neoplasia. Cancer Res 61: 6050-6054.
56. Zhao S, Fernald RD,. 2005. Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol 12: 1047-1064.
57. Zhou BP, Deng J, Xia W, Xu J, Li YM, Gunduz M, Hung MC,. 2004. Dual regulation of Snail by GSK-3beta-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat Cell Biol 6: 931-940.