Asian Pacific Journal of Cancer Prevention

Asian Pacific Journal of Cancer Prevention (아시아태평양암예방학회)
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microRNA-29b: an Emerging Player in Human Cancer

  • Liu, Hao (Department of Pathology, Nanfang Hospital & School of Basic Medical Sciences, Southern Medical University) ;
  • Wang, Bin (Department of Pathology, Nanfang Hospital & School of Basic Medical Sciences, Southern Medical University) ;
  • Lin, Jie (Department of Pathology, Nanfang Hospital & School of Basic Medical Sciences, Southern Medical University) ;
  • Zhao, Liang (Department of Pathology, Nanfang Hospital & School of Basic Medical Sciences, Southern Medical University)
  • Published : 2014.11.28
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Abstract

MicroRNAs (miRNAs) are ubiquitously expressed small, non-coding RNAs that negatively regulate gene expression at a post transcriptional/translational level. They have emerging as playing crucial roles in cancer at all stages ranging from initiation to metastasis. As a tumor suppressor miRNA, aberrant expression of microRNA-29b (miR-29b) has been detected in various types of cancer, and its disturbance is related with tumor development and progression. In this review, we summarize the latest findings with regard to the tumor suppressor signatureof miR-29b and its regulatory mechanisms. Our review highlights the diverse relationships between miR-29b and its target genes in malignant tumors.

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References

  1. Aldaz B, Sagardoy A, Nogueira L, et al (2013). Involvement of miRNAs in the differentiation of human glioblastoma multiforme stem-like cells. PLoS One, 8.
  2. Alenzi FQ, Lotfy M, Wyse R (2010). Swords of cell death: caspase activation and regulation. Asian Pac J Cancer Prev, 11, 271-80.
  3. Amodio N, Bellizzi D, Leotta M, et al (2013). miR-29b induces SOCS-1 expression by promoter demethylation and negatively regulates migration of multiple myeloma and endothelial cells. Cell Cycle, 12, 3650-62. https://doi.org/10.4161/cc.26585
  4. Amodio N, Di Martino MT, Foresta U, et al (2012a). 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, 29, 175.
  5. Amodio N, Leotta M, Bellizzi D, et al (2012b). DNA-demethylating and anti-tumor activity of synthetic miR-29b mimics in multiple myeloma. Oncotarget, 3, 1246-58.
  6. Bartel DP (2009). MicroRNAs: target recognition and regulatory functions. Cell, 136, 215-33. https://doi.org/10.1016/j.cell.2009.01.002
  7. Calin GA, Pekarsky Y, Croce CM (2007). The role of microRNA and other non-coding RNA in the pathogenesis of chronic lymphocytic leukemia. Best Pract Res Clin Haematol, 20, 425-37. https://doi.org/10.1016/j.beha.2007.02.003
  8. Chen KC, Wang YS, Hu CY, et al (2011). OxLDL up-regulates microRNA-29b, leading to epigenetic modifications of MMP-2/MMP-9 genes: a novel mechanism for cardiovascular diseases. Faseb J, 25, 1718-28. https://doi.org/10.1096/fj.10-174904
  9. Chou J, Lin JH, Brenot A, et al (2013). GATA3 suppresses metastasis and modulates the tumour microenvironment by regulating microRNA-29b expression. Nat Cell Biol, 15, 201-13. https://doi.org/10.1038/ncb2672
  10. Cortez MA, Nicoloso MS, Shimizu M, et al (2010). miR-29b and miR-125a regulate podoplanin and suppress invasion in glioblastoma. Genes Chromosomes Cancer, 49, 981-90. https://doi.org/10.1002/gcc.20808
  11. Dai F, Zhang Y, Zhu X, et al (2012). Anticancer role of MUC1 aptamer-miR-29b chimera in epithelial ovarian carcinoma cells through regulation of PTEN methylation. Target Oncol, 7, 217-25. https://doi.org/10.1007/s11523-012-0236-7
  12. Dai F, Zhang Y, Zhu X, et al (2013). The anti-chemoresistant effect and mechanism of MUC1 aptamer-miR-29b chimera in ovarian cancer. Gynecol Oncol, 131, 451-9. https://doi.org/10.1016/j.ygyno.2013.07.112
  13. Espinosa-Parrilla Y, Munoz X, Bonet C, et al (2014). Genetic association of gastric cancer with miRNA clusters including the cancer-related genes MIR29, MIR25, MIR93 and MIR106: Results from the EPIC-EURGAST study. Int J Cancer, 18, 28850.
  14. Eyholzer M, Schmid S, Wilkens L, et al (2010). The tumoursuppressive miR-29a/b1 cluster is regulated by CEBPA and blocked in human AML. Br J Cancer, 103, 275-84. https://doi.org/10.1038/sj.bjc.6605751
  15. Fabbri M, Garzon R, Cimmino A, et al (2007). MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci U S A, 104, 15805-10. https://doi.org/10.1073/pnas.0707628104
  16. Fang JH, Zhou HC, Zeng C, et al (2011). MicroRNA-29b suppresses tumor angiogenesis, invasion, and metastasis by regulating matrix metalloproteinase 2 expression. Hepatology, 54, 1729-40. https://doi.org/10.1002/hep.24577
  17. Garzon R, Garofalo M, Martelli MP, et al (2008). Distinctive microRNA signature of acute myeloid leukemia bearing cytoplasmic mutated nucleophosmin. Proc Natl Acad Sci U S A, 105, 3945-50. https://doi.org/10.1073/pnas.0800135105
  18. Garzon R, Heaphy CE, Havelange V, et al (2009). MicroRNA 29b functions in acute myeloid leukemia. Blood, 114, 5331-41. https://doi.org/10.1182/blood-2009-03-211938
  19. Grant JL, Fishbein MC, Hong LS, et al (2014). A novel molecular pathway for snail-dependent, SPARC-mediated invasion in non-small cell lung cancer pathogenesis. Cancer Prev Res, 7, 150-60. https://doi.org/10.1158/1940-6207.CAPR-13-0263
  20. Hiroki E, Akahira J, Suzuki F, et al (2010). Changes in microRNA expression levels correlate with clinicopathological features and prognoses in endometrial serous adenocarcinomas. Cancer Sci, 101, 241-9. https://doi.org/10.1111/j.1349-7006.2009.01385.x
  21. Kavitha N, Vijayarathna S, Jothy SL, et al (2014). MicroRNAs: Biogenesis, Roles for Carcinogenesis and as Potential Biomarkers for Cancer Diagnosis and Prognosis. Asian Pac J Cancer Prev, 15, 7489-97. https://doi.org/10.7314/APJCP.2014.15.18.7489
  22. Kincaid RP, Burke JM, Sullivan CS (2012). RNA virus microRNA that mimics a B-cell oncomiR. Proc Natl Acad Sci U S A, 109, 3077-82. https://doi.org/10.1073/pnas.1116107109
  23. Kozomara A, Griffiths-Jones S (2011). miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res, 39, 30. https://doi.org/10.1093/nar/gkq736
  24. Leone V, D'Angelo D, Pallante P, et al (2012). Thyrotropin regulates thyroid cell proliferation by up-regulating miR-23b and miR-29b that target SMAD3. J Clin Endocrinol Metab, 97, 3292-301. https://doi.org/10.1210/jc.2012-1349
  25. Li Y, Wang H, Tao K, et al (2013). miR-29b suppresses CML cell proliferation and induces apoptosis via regulation of BCR/ABL1 protein. Exp Cell Res, 319, 1094-101. https://doi.org/10.1016/j.yexcr.2013.02.002
  26. Liston A, Papadopoulou AS, Danso-Abeam D, et al (2012). MicroRNA-29 in the adaptive immune system: setting the threshold. Cell Mol Life Sci, 69, 3533-41. https://doi.org/10.1007/s00018-012-1124-0
  27. Liu L, Zhang Q, Zhang Y, et al (2006). Lentivirus-mediated silencing of Tiam1 gene influences multiple functions of a human colorectal cancer cell line. Neoplasia, 8, 917-24. https://doi.org/10.1593/neo.06364
  28. Ma F, Xu S, Liu X, et al (2011). The microRNA miR-29 controls innate and adaptive immune responses to intracellular bacterial infection by targeting interferon-gamma. Nat Immunol, 12, 861-9. https://doi.org/10.1038/ni.2073
  29. Melo SA, Kalluri R (2013). miR-29b moulds the tumour microenvironment to repress metastasis. Nat Cell Biol, 15, 139-40. https://doi.org/10.1038/ncb2684
  30. Mims A, Walker AR, Huang X, et al (2013). Increased anti-leukemic activity of decitabine via AR-42-induced upregulation of miR-29b: a novel epigenetic-targeting approach in acute myeloid leukemia. Leukemia, 27, 871-8. https://doi.org/10.1038/leu.2012.342
  31. Mott JL, Kobayashi S, Bronk SF, et al (2007). mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene, 26, 6133-40. https://doi.org/10.1038/sj.onc.1210436
  32. Mott JL, Kurita S, Cazanave SC, et al (2010). Transcriptional suppression of mir-29b-1/mir-29a promoter by c-Myc, hedgehog, and NF-kappaB. J Cell Biochem, 110, 1155-64. https://doi.org/10.1002/jcb.22630
  33. Nurul-Syakima AM, Yoke-Kqueen C, Sabariah AR, et al (2011). Differential microRNA expression and identification of putative miRNA targets and pathways in head and neck cancers. Int J Mol Med, 28, 327-36.
  34. Orang AV, Safaralizadeh R, Hosseinpour Feizi MA, et al (2014). Diagnostic and prognostic value of miR-205 in colorectal cancer. Asian Pac J Cancer Prev, 15, 4033-7. https://doi.org/10.7314/APJCP.2014.15.9.4033
  35. Papadopoulou AS, Dooley J, Linterman MA, et al (2011). The thymic epithelial microRNA network elevates the threshold for infection-associated thymic involution via miR-29a mediated suppression of the IFN-alpha receptor. Nat Immunol, 13, 181-7. https://doi.org/10.1038/ni.2193
  36. Papakonstantinou N, Ntoufa S, Chartomatsidou E, et al (2013). Differential microRNA profiles and their functional implications in different immunogenetic subsets of chronic lymphocytic leukemia. Mol Med, 19, 115-23.
  37. Park SY, Lee JH, Ha M, et al (2009). miR-29 miRNAs activate p53 by targeting p85 alpha and CDC42. Nat Struct Mol Biol, 16, 23-9. https://doi.org/10.1038/nsmb.1533
  38. Pekarsky Y, Santanam U, Cimmino A, et al (2006). Tcl1 expression in chronic lymphocytic leukemia is regulated by miR-29 and miR-181. Cancer Res, 66, 11590-3. https://doi.org/10.1158/0008-5472.CAN-06-3613
  39. Pillai RS, Bhattacharyya SN, Filipowicz W (2007). Repression of protein synthesis by miRNAs: how many mechanisms? Trends Cell Biol, 17, 118-26. https://doi.org/10.1016/j.tcb.2006.12.007
  40. Poudyal D, Cui X, Le PM, et al (2013). A key role of microRNA-29b for the suppression of colon cancer cell migration by American ginseng. PLoS One, 8.
  41. Qiang W, Liu Z, Serna VA, et al (2014). Down-regulation of miR-29b is essential for pathogenesis of uterine leiomyoma. Endocrinology, 155, 663-9. https://doi.org/10.1210/en.2013-1763
  42. Rossi M, Pitari MR, Amodio N, et al (2013). miR-29b negatively regulates human osteoclastic cell differentiation and function: implications for the treatment of multiple myeloma-related bone disease. J Cell Physiol, 228, 1506-15. https://doi.org/10.1002/jcp.24306
  43. Rothschild SI, Tschan MP, Federzoni EA, et al (2012). MicroRNA-29b is involved in the Src-ID1 signaling pathway and is dysregulated in human lung adenocarcinoma. Oncogene, 31, 4221-32. https://doi.org/10.1038/onc.2011.578
  44. Ru P, Steele R, Newhall P, et al (2012). miRNA-29b suppresses prostate cancer metastasis by regulating epithelialmesenchymal transition signaling. Mol Cancer Ther, 11, 1166-73. https://doi.org/10.1158/1535-7163.MCT-12-0100
  45. Sandhu R, Rivenbark AG, Mackler RM, et al (2014). Dysregulation of microRNA expression drives aberrant DNA hypermethylation in basal-like breast cancer. Int J Oncol, 44, 563-72.
  46. Santanam U, Zanesi N, Efanov A, et al (2010). Chronic lymphocytic leukemia modeled in mouse by targeted miR-29 expression. Proc Natl Acad Sci U S A, 107, 12210-5. https://doi.org/10.1073/pnas.1007186107
  47. Schmitt MJ, Philippidou D, Reinsbach SE, et al (2012). 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, 10, 10-41. https://doi.org/10.1186/1478-811X-10-10
  48. Sengupta S, den Boon JA, Chen IH, et al (2008). MicroRNA 29c is down-regulated in nasopharyngeal carcinomas, upregulating mRNAs encoding extracellular matrix proteins. Proc Natl Acad Sci USA, 105, 5874-8. https://doi.org/10.1073/pnas.0801130105
  49. Steele R, Mott JL, Ray RB (2010). MBP-1 upregulates miR-29b that represses Mcl-1, collagens, and matrixmetalloproteinase-2 in prostate cancer cells. Genes Cancer, 1, 381-7. https://doi.org/10.1177/1947601910371978
  50. Steiner DF, Thomas MF, Hu JK, et al (2011). MicroRNA-29 regulates T-box transcription factors and interferon-gamma production in helper T cells. Immunity, 35, 169-81. https://doi.org/10.1016/j.immuni.2011.07.009
  51. Svoboda M, Sana J, Fabian P, et al (2012). MicroRNA expression profile associated with response to neoadjuvant chemoradiotherapy in locally advanced rectal cancer patients. Radiat Oncol, 7, 7-195. https://doi.org/10.1186/1748-717X-7-7
  52. Szczyrba J, Nolte E, Hart M, et al (2013). Identification of ZNF217, hnRNP-K, VEGF-A and IPO7 as targets for microRNAs that are downregulated in prostate carcinoma. Int J Cancer, 132, 775-84. https://doi.org/10.1002/ijc.27731
  53. Tan YG, Zhang YF, Guo CJ, et al (2013). Screening of differentially expressed microRNA in ulcerative colitis related colorectal cancer. Asian Pac J Trop Med, 6, 972-6. https://doi.org/10.1016/S1995-7645(13)60174-1
  54. Teng Y, Zhao L, Zhang Y, et al (2014). Id-1, a protein repressed by miR-29b, facilitates the tgfbeta1-induced epithelial-mesenchymal transition in human ovarian cancer cells. Cell Physiol Biochem, 33, 717-30. https://doi.org/10.1159/000358647
  55. Wang B, Li W, Liu H, et al (2014). miR-29b suppresses tumor growth and metastasis in colorectal cancer via downregulating Tiam1 expression and inhibiting epithelialmesenchymal transition. Cell Death Dis, 5, 1335. https://doi.org/10.1038/cddis.2014.304
  56. Wang C, Gao C, Zhuang JL, et al (2012a). 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, 138, 2127-36. https://doi.org/10.1007/s00432-012-1288-x
  57. Wang H, Garzon R, Sun H, et al (2008). NF-kappaB-YY1-miR-29 regulatory circuitry in skeletal myogenesis and rhabdomyosarcoma. Cancer Cell, 14, 369-81. https://doi.org/10.1016/j.ccr.2008.10.006
  58. Wang X, Zhao J, Huang J, et al (2012b). The regulatory roles of miRNA and methylation on oncogene and tumor suppressor gene expression in pancreatic cancer cells. Biochem Biophys Res Commun, 425, 51-7. https://doi.org/10.1016/j.bbrc.2012.07.047
  59. Wotschofsky Z, Liep J, Meyer HA, et al (2012). Identification of metastamirs as metastasis-associated microRNAs in clear cell renal cell carcinomas. Int J Biol Sci, 8, 1363-74. https://doi.org/10.7150/ijbs.5106
  60. Xu CZ, Shi RJ, Chen D, et al (2013a). Potential biomarkers for paclitaxel sensitivity in hypopharynx cancer cell. Int J Clin Exp Pathol, 6, 2745-56.
  61. Xu F, Zhang Q, Cheng W, et al (2013b). Effect of miR-29b-1* and miR-29c knockdown on cell growth of the bladder cancer cell line T24. J Int Med Res, 41, 1803-10. https://doi.org/10.1177/0300060513505266
  62. Yu LN, Zhang QL, Li X, et al (2013). Tiam1 transgenic mice display increased tumor invasive and metastatic potential of colorectal cancer after 1,2-dimethylhydrazine treatment. PLoS One, 8, 73077. https://doi.org/10.1371/journal.pone.0073077
  63. Zhang YK, Wang H, Leng Y, et al (2011). Overexpression of microRNA-29b induces apoptosis of multiple myeloma cells through down regulating Mcl-1. Biochem Biophys Res Commun, 414, 233-9. https://doi.org/10.1016/j.bbrc.2011.09.063
  64. Zhao JJ, Lin J, Lwin T, et al (2010). microRNA expression profile and identification of miR-29 as a prognostic marker and pathogenetic factor by targeting CDK6 in mantle cell lymphoma. Blood, 115, 2630-9. https://doi.org/10.1182/blood-2009-09-243147
  65. Zheng JJ, Yu FJ, Dong PH, et al (2013). Expression of miRNA-29b and its clinical significances in primary hepatic carcinoma. Zhonghua Yi Xue Za Zhi, 93, 888-91 (in Chinese).
  66. Zhu J, Li X, Kong X, et al (2012). Testin is a tumor suppressor and prognostic marker in breast cancer. Cancer Sci, 103, 2092-101. https://doi.org/10.1111/cas.12020

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