The role of miR-29b in cancer: Regulation, function, and signaling

OncoTargets and Therapy

Volumn 8, Issue , 2015, Pages 539-548

  Yan, Bin ^a   Guo, Qiong ^b   Fu, Fa Jun ^b   Wang, Zhao ^a   Yin, Zhuo ^a   Wei, Yong Bao ^a   Yang, Jin Rui ^a  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b CHANGSHA CENTRAL HOSPITAL   (China)

Author keywords

Biological function; Cancer; Chemoresistance; MiR 29b; Oncogene; Tumor promoter

Indexed keywords

ALPHA6 INTEGRIN; CYCLIN D2; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; GELATINASE A; HISTONE DEACETYLASE 3; HISTONE LYSINE METHYLTRANSFERASE; HISTONE LYSINE METHYLTRANSFERASE 2; INTERLEUKIN 15; LAMININ; LAMININ GAMMA2; MICRORNA 29B; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN BCL 2; PROTEIN CDC42; PROTEIN KINASE B BETA; PROTEIN MCL 1; PROTEIN P53; PROTEIN P85; SUPPRESSOR OF CYTOKINE SIGNALING 1; UNCLASSIFIED DRUG;

APOPTOSIS; B CELL LYMPHOMA; CANCER CELL; CANCER INHIBITION; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CHEMOSENSITIVITY; CHOLANGIOCARCINOMA CELL LINE; CHROMOSOMAL INSTABILITY; CHRONIC LYMPHATIC LEUKEMIA; COL1A1 GENE; COL1A2 GENE; COL3A1 GENE; COL4A1 GENE; COL5A1 GENE; COL5A2 GENE; DISEASE ASSOCIATION; DNA METHYLATION; DOWN REGULATION; ENZYME REGULATION; EPIGENETIC REPRESSION; FBN GENE; GENE; GENE OVEREXPRESSION; GENE REPRESSION; GENE TARGETING; HUMAN; LAMC1 GENE; LUNG CANCER; METASTASIS; MULTIPLE MYELOMA CELL LINE; NEOPLASM; NONHUMAN; ONCOGENE C MYC; OVARY CANCER; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; TUMOR INVASION; TUMOR MICROENVIRONMENT; TUMOR PROMOTION; TUMOR SUPPRESSOR GENE; UPREGULATION;

EID: 84924266403     PISSN: 11786930     EISSN: 11786930     Source Type: Journal    
DOI: 10.2147/OTT.S75899     Document Type: Review

References (72)

1. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136(2):215–233.
2. Auyeung VC, Ulitsky I, McGeary SE, Bartel DP. Beyond secondary structure: primary-sequence determinants license pri-miRNA hairpins for processing. Cell. 2013;152(4):844–858.
3. Pillai RS, Bhattacharyya SN, Filipowicz W. Repression of protein synthesis by miRNAs: how many mechanisms? Trends Cell Biol. 2007;17(3):118–126.
4. Slack FJ, Weidhaas JB. MicroRNA in cancer prognosis. N Engl J Med. 2008;359(25):2720–2722.
5. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet. 2008;9(2):102–114.
6. Kole AJ, Swahari V, Hammond SM, Deshmukh M. miR-29b is activated during neuronal maturation and targets BH3-only genes to restrict apoptosis. Genes Dev. 2011;25(2):125–130.
7. Han YC, Park CY, Bhagat G, et al. microRNA-29a induces aberrant self-renewal capacity in hematopoietic progenitors, biased myeloid development, and acute myeloid leukemia. J Exp Med. 2010;207(3): 475–489.
8. Nguyen T, Kuo C, Nicholl MB, et al. Downregulation of microRNA-29c is associated with hypermethylation of tumor-related genes and disease outcome in cutaneous melanoma. Epigenetics. 2011;6(3):388–394.
9. Eyholzer M, Schmid S, Wilkens L, Mueller BU, Pabst T. The tumour-suppressive miR-29a/b1 cluster is regulated by CEBPA and blocked in human AML. Br J Cancer. 2010;103(2):275–284.
10. Chang TC, Yu D, Lee YS, et al. Widespread microRNA repression by Myc contributes to tumorigenesis. Nat Genet. 2008;40(1):43–50.
11. Zhang X, Zhao X, Fiskus W, et al. Coordinated silencing of MYC-mediated miR-29 by HDAC3 and EZH2 as a therapeutic target of histone modification in aggressive B-Cell lymphomas. Cancer Cell. 2012;22(4):506–523.
12. Sampath D, Liu C, Vasan K, et al. Histone deacetylases mediate the silencing of miR-15a, miR-16, and miR-29b in chronic lymphocytic leukemia. Blood. 2012;119(5):1162–1172.
13. Mott JL, Kurita S, Cazanave SC, Bronk SF, Werneburg NW, Fernandez-Zapico ME. Transcriptional suppression of mir-29b-1/mir-29a promoter by c-Myc, hedgehog, and NF-kappaB. J Cell Biochem. 2010;110(5):1155–1164.
14. Winbanks CE, Wang B, Beyer C, et al. TGF-beta regulates miR-206 and miR-29 to control myogenic differentiation through regulation of HDAC4. J Biol Chem. 2011;286(16):13805–13814.
15. Wang H, Garzon R, Sun H, et al. NF-kappaB-YY1-miR-29 regulatory circuitry in skeletal myogenesis and rhabdomyosarcoma. Cancer Cell. 2008;14(5):369–381.
16. Chou J, Lin JH, Brenot A, Kim JW, Provot S, Werb Z. GATA3 suppresses metastasis and modulates the tumour microenvironment by regulating microRNA-29b expression. Nat Cell Biol. 2013;15(2):201–213.
17. Steele R, Mott JL, Ray RB. MBP-1 upregulates miR-29b that represses Mcl-1, collagens, and matrix-metalloproteinase-2 in prostate cancer cells. Genes Cancer. 2010;1(4):381–387.
18. Cittelly DM, Finlay-Schultz J, Howe EN, et al. Progestin suppression of miR-29 potentiates dedifferentiation of breast cancer cells via KLF4. Oncogene. 2013;32(20):2555–2564.
19. Schmitt MJ, Philippidou D, Reinsbach SE, et al. Interferon-gamma-induced activation of Signal Transducer and Activator of Transcription 1 (STAT1) up-regulates the tumor suppressing microRNA-29 family in melanoma cells. Cell Commun Signal. 2012;10(1):41.
20. Batliner J, Buehrer E, Federzoni EA, et al. Transcriptional regulation of MIR29B by PU.1 (SPI1) and MYC during neutrophil differentiation of acute promyelocytic leukaemia cells. Br J Haematol. 2012; 157(2):270–274.
21. Garzon R, Liu S, Fabbri M, et al. MicroRNA-29b induces global DNA hypomethylation and tumor suppressor gene reexpression in acute myeloid leukemia by targeting directly DNMT3A and 3B and indirectly DNMT1. Blood. 2009;113(25):6411–6418.
22. Jacobsen A, Silber J, Harinath G, Huse JT, Schultz N, Sander C. Analysis of microRNA-target interactions across diverse cancer types. Nat Struct Mol Biol. 2013;20(11):1325–1332.
23. Amodio N, Leotta M, Bellizzi D, et al. DNA-demethylating and anti-tumor activity of synthetic miR-29b mimics in multiple myeloma. Oncotarget. 2012;3(10):1246–1258.
24. Mishra A, Liu S, Sams GH, et al. Aberrant overexpression of IL-15 initiates large granular lymphocyte leukemia through chromosomal instability and DNA hypermethylation. Cancer Cell. 2012;22(5):645–655.
25. Amodio N, Bellizzi D, Leotta M, et al. miR-29b induces SOCS-1 expression by promoter demethylation and negatively regulates migration of multiple myeloma and endothelial cells. Cell Cycle. 2013; 12(23):3650–3662.
26. Bernot KM, Nemer JS, Santhanam R, et al. Eradicating acute myeloid leukemia in a Mll(PTD/wt):Flt3(ITD/wt) murine model: a path to novel therapeutic approaches for human disease. Blood. 2013; 122(23):3778–3783.
27. Pandey M, Sultana S, Gupta KP. Involvement of epigenetics and microRNA-29b in the urethane induced inception and establishment of mouse lung tumors. Exp Mol Pathol. 2014;96(1):61–70.
28. Tan M, Wu J, Cai Y. Suppression of Wnt signaling by the miR-29 family is mediated by demethylation of WIF-1 in non-small-cell lung cancer. Biochem Biophys Res Commun. 2013;438(4):673–679.
29. Galli R, Paone A, Fabbri M, et al. Toll-like receptor 3 (TLR3) activation induces microRNA-dependent reexpression of functional RARbeta and tumor regression. Proc Natl Acad Sci U S A. 2013;110(24): 9812–9817.
30. Morita S, Horii T, Kimura M, Ochiya T, Tajima S, Hatada I. miR-29 represses the activities of DNA methyltransferases and DNA demethylases. Int J Mol Sci. 2013;14(7):14647–14658.
31. Mott JL, Kobayashi S, Bronk SF, Gores GJ. mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene. 2007;26(42):6133–6140.
32. Aldaz B, Sagardoy A, Nogueira L, et al. Involvement of miRNAs in the differentiation of human glioblastoma multiforme stem-like cells. PLoS One. 2013;8(10):e77098.
33. Garzon R, Heaphy CE, Havelange V, et al. MicroRNA 29b functions in acute myeloid leukemia. Blood. 2009;114(26):5331–5341.
34. Xiong Y, Fang JH, Yun JP, et al. Effects of microRNA-29 on apoptosis, tumorigenicity, and prognosis of hepatocellular carcinoma. Hepatology. 2010;51(3):836–845.
35. Zhang YK, Wang H, Leng Y, et al. Overexpression of microRNA-29b induces apoptosis of multiple myeloma cells through down regulating Mcl-1. Biochem Biophys Res Commun. 2011;414(1):233–239.
36. Park SY, Lee JH, Ha M, Nam JW, Kim VN. miR-29 miRNAs activate p53 by targeting p85 alpha and CDC42. Nat Struct Mol Biol. 2009;16(1): 23–29.
37. Gong JN, Yu J, Lin HS, et al. The role, mechanism and potentially therapeutic application of microRNA-29 family in acute myeloid leukemia. Cell Death Differ. 2014;21(1):100–112.
38. Rossi M, Pitari MR, Amodio N, et al. miR-29b negatively regulates human osteoclastic cell differentiation and function: implications for the treatment of multiple myeloma-related bone disease. J Cell Physiol. 2013;228(7):1506–1515.
39. Melo SA, Kalluri R. miR-29b moulds the tumour microenvironment to repress metastasis. Nat Cell Biol. 2013;15(2):139–140.
40. Ru P, Steele R, Newhall P, Phillips NJ, Toth K, Ray RB. miRNA-29b suppresses prostate cancer metastasis by regulating epithelial-mesenchymal transition signaling. Mol Cancer Ther. 2012;11(5):1166–1173.
41. Poudyal D, Cui X, Le PM, et al. A key role of microRNA-29b for the suppression of colon cancer cell migration by American ginseng. PLoS One. 2013;8(10):e75034.
42. Kinoshita T, Nohata N, Hanazawa T, et al. Tumour-suppressive microRNA-29s inhibit cancer cell migration and invasion by targeting laminin-integrin signalling in head and neck squamous cell carcinoma. Br J Cancer. 2013;109(10):2636–2645.
43. Dai Z, Huang Y, Sadee W. Growth factor signaling and resistance to cancer chemotherapy. Curr Top Med Chem. 2004;4(13):1347–1356.
44. Meng F, Henson R, Lang M, et al. Involvement of human micro-RNA in growth and response to chemotherapy in human cholangiocarcinoma cell lines. Gastroenterology. 2006;130(7):2113–2129.
45. Okamoto K, Miyoshi K, Murawaki Y. miR-29b, miR-205 and miR-221 enhance chemosensitivity to gemcitabine in HuH28 human cholangiocarcinoma cells. PLoS One. 2013;8(10):e77623.
46. Dai F, Zhang Y, Zhu X, Shan N, Chen Y. The anti-chemoresistant effect and mechanism of MUC1 aptamer-miR-29b chimera in ovarian cancer. Gynecol Oncol. 2013;131(2):451–459.
47. Amodio N, Di Martino MT, Foresta U, et al. 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. 2012;3:e436.
48. Mims A, Walker AR, Huang X, et al. Increased anti-leukemic activity of decitabine via AR-42-induced upregulation of miR-29b: a novel epigenetic-targeting approach in acute myeloid leukemia. Leukemia. 2013;27(4):871–878.
49. Blum W, Garzon R, Klisovic RB, et al. Clinical response and miR-29b predictive significance in older AML patients treated with a 10-day schedule of decitabine. Proc Natl Acad Sci U S A. 2010;107(16):7473–7478.
50. Blum W, Schwind S, Tarighat SS, et al. Clinical and pharmacodynamic activity of bortezomib and decitabine in acute myeloid leukemia. Blood. 2012;119(25):6025–6031.
51. Huang X, Schwind S, Yu B, et al. Targeted delivery of microRNA-29b by transferrin-conjugated anionic lipopolyplex nanoparticles: a novel therapeutic strategy in acute myeloid leukemia. Clin Cancer Res. 2013;19(9):2355–2367.
52. Wu Y, Crawford M, Mao Y, et al. Therapeutic delivery of microRNA-29b by cationic lipoplexes for lung cancer. Mol Ther Nucleic Acids. 2013;2:e84.
53. Chen CZ. MicroRNAs as oncogenes and tumor suppressors. N Engl J Med. 2005;353(17):1768–1771.
54. Santanam U, Zanesi N, Efanov A, et al. Chronic lymphocytic leukemia modeled in mouse by targeted miR-29 expression. Proc Natl Acad Sci U S A. 2010;107(27):12210–12215.
55. Kong G, Zhang J, Zhang S, Shan C, Ye L, Zhang X. Upregulated microRNA-29a by hepatitis B virus X protein enhances hepatoma cell migration by targeting PTEN in cell culture model. PLoS One. 2011;6(5):e19518.
56. Cheng J, Guo S, Chen S, et al. An extensive network of TET2-targeting MicroRNAs regulates malignant hematopoiesis. Cell Rep. 2013;5(2):471–481.
57. Xu F, Zhang Q, Cheng W, Zhang Z, Wang J, Ge J. Effect of miR-29b-1* and miR-29c knockdown on cell growth of the bladder cancer cell line T24. J Int Med Res. 2013;41(6):1803–1810.
58. Wang C, Bian Z, Wei D, Zhang JG. miR-29b regulates migration of human breast cancer cells. Mol Cell Biochem. 2011;352(1–2):197–207.
59. Wang C, Gao C, Zhuang JL, Ding C, Wang Y. A combined approach identifies three mRNAs that are down-regulated by microRNA-29b and promote invasion ability in the breast cancer cell line MCF-7. J Cancer Res Clin Oncol. 2012;138(12):2127–2136.
60. Fu J, Tang W, Du P, et al. Identifying microRNA-mRNA regulatory network in colorectal cancer by a combination of expression profile and bioinformatics analysis. BMC Syst Biol. 2012;6:68.
61. Luna C, Li G, Qiu J, Epstein DL, Gonzalez P. Role of miR-29b on the regulation of the extracellular matrix in human trabecular meshwork cells under chronic oxidative stress. Mol Vis. 2009;15:2488–2497.
62. Pekarsky Y, Santanam U, Cimmino A, et al. Tcl1 expression in chronic lymphocytic leukemia is regulated by miR-29 and miR-181. Cancer Res. 2006;66(24):11590–11593.
63. Martinez I, Cazalla D, Almstead LL, Steitz JA, DiMaio D. miR-29 and miR-30 regulate B-Myb expression during cellular senescence. Proc Natl Acad Sci U S A. 2011;108(2):522–527.
64. Fabbri M, Garzon R, Cimmino A, et al. MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci U S A. 2007;104(40):15805–15810.
65. Cortez MA, Nicoloso MS, Shimizu M, et al. miR-29b and miR-125a regulate podoplanin and suppress invasion in glioblastoma. Genes Chromosomes Cancer. 2010;49(11):981–990.
66. Li G, Zhao J, Peng X, Liang J, Deng X, Chen Y. The mechanism involved in the loss of PTEN expression in NSCLC tumor cells. Biochem Biophys Res Commun. 2012;418(3):547–552.
67. Xu H, Cheung IY, Guo HF, Cheung NK. MicroRNA miR-29 modulates expression of immunoinhibitory molecule B7-H3: potential implications for immune based therapy of human solid tumors. Cancer Res. 2009;69(15):6275–6281.
68. MacDonald BT, Tamai K, He X. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell. 2009;17(1):9–26.
69. Lin YC, You L, Xu Z, et al. Wnt signaling activation and WIF-1 silencing in nasopharyngeal cancer cell lines. Biochem Biophys Res Commun. 2006;341(2):635–640.
70. Mazieres J, He B, You L, et al. Wnt inhibitory factor-1 is silenced by promoter hypermethylation in human lung cancer. Cancer Res. 2004;64(14):4717–4720.
71. Gautschi O, Tepper CG, Purnell PR, et al. Regulation of Id1 expression by SRC: implications for targeting of the bone morphogenetic protein pathway in cancer. Cancer Res. 2008;68(7):2250–2258.
72. Rothschild SI, Tschan MP, Federzoni EA, et al. MicroRNA-29b is involved in the Src-ID1 signaling pathway and is dysregulated in human lung adenocarcinoma. Oncogene. 2012;31(38):4221–4232.