Abstract
MicroRNAs (miRNAs) are a class of 20–24 nt small non-coding RNAs that regulate a wide range of biological processes through changing the stability and translation of their target messenger RNA (mRNA) genes. Shortly after their identification, many miRNA genes have been found dysregulated in a variety of human cancers, indicating a pathological function of this gene class in mediating cancer progression. Over the past decade, accumulated literature has shown that miRNAs participate in numerous cancer-relevant processes including cell proliferation, apoptosis, differentiation, metabolism, and importantly, metastasis, which accounts for the mortality of approximately 90 % of cancer patients. Several recent publications have linked miRNAs with metastasis-associated protein (MTA) family members. Given the fact that the MTA family members are widely overexpressed in human cancers and their nature of serving as both corepressor and coactivator in gene regulation, it is intriguing to study whether certain miRNAs regulate cancer progression through modulating the expression of MTA family members. In this review, we will focus on recent advances in understanding the regulatory relationship between certain miRNAs and MTA family members.
Similar content being viewed by others
References
Eddy, S. R. (2001). Non-coding RNA genes and the modern RNA world. Nature Reviews Genetics, 2(12), 919–929. doi:10.1038/35103511.
Bartel, D. P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116(2), 281–297.
Bushati, N., & Cohen, S. M. (2007). MicroRNA functions. Annual Review of Cell and Developmental Biology, 23, 175–205. doi:10.1146/annurev.cellbio.23.090506.123406.
Calin, G. A., & Croce, C. M. (2006). MicroRNA signatures in human cancers. Nature Reviews Cancer, 6(11), 857–866. doi:10.1038/nrc1997.
Lu, J., Getz, G., Miska, E. A., Alvarez-Saavedra, E., Lamb, J., Peck, D., et al. (2005). MicroRNA expression profiles classify human cancers. Nature, 435(7043), 834–838. doi:10.1038/nature03702.
Sayed, D., & Abdellatif, M. (2011). MicroRNAs in development and disease. Physiological Reviews, 91(3), 827–887. doi:10.1152/physrev.00006.2010.
Esquela-Kerscher, A., & Slack, F. J. (2006). Oncomirs—microRNAs with a role in cancer. Nature Reviews Cancer, 6(4), 259–269. doi:10.1038/nrc1840.
Hammond, S. M. (2007). MicroRNAs as tumor suppressors. Nature Genetics, 39(5), 582–583.
Chen, C. Z. (2005). MicroRNAs as oncogenes and tumor suppressors. New England Journal of Medicine, 353(17), 1768–1771. doi:10.1056/Nejmp058190.
Nicoloso, M. S., Spizzo, R., Shimizu, M., Rossi, S., & Calin, G. A. (2009). MicroRNAs—the micro steering wheel of tumour metastases. Nature Reviews Cancer, 9(4), 293–302. doi:10.1038/nrc2619.
Ma, L., & Weinberg, R. A. (2008). Micromanagers of malignancy: role of microRNAs in regulating metastasis. Trends in Genetics, 24(9), 448–456. doi:10.1016/j.tig.2008.06.004.
Kim, V. N. (2005). MicroRNA biogenesis: coordinated cropping and dicing. Nature Reviews Molecular Cell Biology, 6(5), 376–385. doi:10.1038/nrm1644.
Bartel, D. P. (2009). MicroRNAs: target recognition and regulatory functions. Cell, 136(2), 215–233. doi:10.1016/j.cell.2009.01.002.
Fabian, M. R., & Sonenberg, N. (2012). The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nature Structural and Molecular Biology, 19(6), 586–593. doi:10.1038/nsmb.2296.
Ameres, S. L., & Zamore, P. D. (2013). Diversifying microRNA sequence and function. Nature Reviews Molecular Cell Biology, 14(8), 475–488. doi:10.1038/nrm3611.
Calin, G. A., Sevignani, C., Dan Dumitru, C., Hyslop, T., Noch, E., Yendamuri, S., et al. (2004). Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proceedings of the National Academy of Sciences of the United States of America, 101(9), 2999–3004. doi:10.1073/Pnas.0307323101.
Gaur, A., Jewell, D. A., Liang, Y., Ridzon, D., Moore, J. H., Chen, C. F., et al. (2007). Characterization of microRNA expression levels and their biological correlates in human cancer cell lines. Cancer Research, 67(6), 2456–2468. doi:10.1158/0008-5472.Can-06-2698.
Connolly, E., Melegari, M., Landgraf, P., Tchaikovskaya, T., Tennant, B. C., Slagle, B. L., et al. (2008). Elevated expression of the miR-17-92 polycistron and miR-21 in hepadnavirus-associated hepatocellular carcinoma contributes to the malignant phenotype. American Journal of Pathology, 173(3), 856–864. doi:10.2353/ajpath.2008.080096.
Diosdado, B., van de Wiel, M. A., Terhaar Sive Droste, J. S., Mongera, S., Postma, C., Meijerink, W. J., et al. (2009). MiR-17-92 cluster is associated with 13q gain and c-myc expression during colorectal adenoma to adenocarcinoma progression. British Journal of Cancer, 101(4), 707–714. doi:10.1038/sj.bjc.6605037.
Inomata, M., Tagawa, H., Guo, Y. M., Kameoka, Y., Takahashi, N., & Sawada, K. (2009). MicroRNA-17-92 down-regulates expression of distinct targets in different B-cell lymphoma subtypes. Blood, 113(2), 396–402. doi:10.1182/blood-2008-07-163907.
Mavrakis, K. J., Wolfe, A. L., Oricchio, E., Palomero, T., de Keersmaecker, K., McJunkin, K., et al. (2010). Genome-wide RNA-mediated interference screen identifies miR-19 targets in Notch-induced T-cell acute lymphoblastic leukaemia. Nature Cell Biology, 12(4), 372–379. doi:10.1038/ncb2037.
Huang, G., Nishimoto, K., Zhou, Z., Hughes, D., & Kleinerman, E. S. (2012). miR-20a encoded by the miR-17-92 cluster increases the metastatic potential of osteosarcoma cells by regulating Fas expression. Cancer Research, 72(4), 908–916. doi:10.1158/0008-5472.CAN-11-1460.
Kim, K., Chadalapaka, G., Lee, S. O., Yamada, D., Sastre-Garau, X., Defossez, P. A., et al. (2012). Identification of oncogenic microRNA-17-92/ZBTB4/specificity protein axis in breast cancer. Oncogene, 31(8), 1034–1044. doi:10.1038/onc.2011.296.
He, L., Thomson, J. M., Hemann, M. T., Hernando-Monge, E., Mu, D., Goodson, S., et al. (2005). A microRNA polycistron as a potential human oncogene. Nature, 435(7043), 828–833. doi:10.1038/Nature03552.
Dews, M., Homayouni, A., Yu, D., Murphy, D., Sevignani, C., Wentzel, E., et al. (2006). Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nature Genetics, 38(9), 1060–1065. doi:10.1038/ng1855.
Johnson, S. M., Grosshans, H., Shingara, J., Byrom, M., Jarvis, R., Cheng, A., et al. (2005). RAS is regulated by the let-7 microRNA family. Cell, 120(5), 635–647. doi:10.1016/J.Cell.2005.01.014.
Chang, T. C., Yu, D., Lee, Y. S., Wentzel, E. A., Arking, D. E., West, K. M., et al. (2008). Widespread microRNA repression by Myc contributes to tumorigenesis. Nature Genetics, 40(1), 43–50. doi:10.1038/ng.2007.30.
Ma, L., Teruya-Feldstein, J., & Weinberg, R. A. (2007). Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature, 449(7163), 682–688. doi:10.1038/nature06174.
Gregory, P. A., Bert, A. G., Paterson, E. L., Barry, S. C., Tsykin, A., Farshid, G., et al. (2008). The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nature Cell Biology, 10(5), 593–601. doi:10.1038/ncb1722.
Tavazoie, S. F., Alarcon, C., Oskarsson, T., Padua, D., Wang, Q. Q., Bos, P. D., et al. (2008). Endogenous human microRNAs that suppress breast cancer metastasis. Nature, 451(7175), 147–152. doi:10.1038/Nature06487.
Zhang, Y., Yang, P., & Wang, X. F. (2014). Microenvironmental regulation of cancer metastasis by miRNAs. Trends in Cell Biology, 24(3), 153–160. doi:10.1016/j.tcb.2013.09.007.
Manavathi, B., & Kumar, R. (2007). Metastasis tumor antigens, an emerging family of multifaceted master coregulators. Journal of Biological Chemistry, 282(3), 1529–1533. doi:10.1074/jbc.R600029200.
Toh, Y., & Nicolson, G. L. (2009). The role of the MTA family and their encoded proteins in human cancers: Molecular functions and clinical implications. Clinical & Experimental Metastasis, 26(3), 215–227. doi:10.1007/s10585-008-9233-8.
Toh, Y., Pencil, S. D., & Nicolson, G. L. (1994). A novel candidate metastasis-associated gene, MTA1, differentially expressed in highly metastatic mammary adenocarcinoma cell-lines—cDNA cloning, expression, and protein analyses. Journal of Biological Chemistry, 269(37), 22958–22963.
Xue, Y. T., Wong, J. M., Moreno, G. T., Young, M. K., Cote, J., & Wang, W. D. (1998). NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Molecular Cell, 2(6), 851–861. doi:10.1016/s1097-2765(00)80299-3.
Ng, H. H., & Bird, A. (2000). Histone deacetylases: silencers for hire. Trends in Biochemical Sciences, 25(3), 121–126.
Denslow, S. A., & Wade, P. A. (2007). The human Mi-2/NuRD complex and gene regulation. Oncogene, 26(37), 5433–5438. doi:10.1038/sj.onc.1210611.
Bowen, N. J., Fujita, N., Kajita, M., & Wade, P. A. (2004). Mi-2/NuRD: multiple complexes for many purposes. Biochimica Et Biophysica Acta - Gene Structure and Expression, 1677(1–3), 52–57. doi:10.1016/j.bbaexp.2003.10.010.
Li, D. Q., Pakala, S. B., Nair, S. S., Eswaran, J., & Kumar, R. (2012). Metastasis-associated protein 1/nucleosome remodeling and histone deacetylase complex in cancer. Cancer Research, 72(2), 387–394. doi:10.1158/0008-5472.CAN-11-2345.
Fujita, N., Jaye, D. L., Kajita, M., Geigerman, C., Moreno, C. S., & Wade, P. A. (2003). MTA3, a Mi-2/NuRD complex subunit, an invasive growth pathway in breast. Cell, 113(2), 207–219. doi:10.1016/s0092-8674(03)00234-4.
Ohshiro, K., Rayala, S. K., Wigerup, C., Pakala, S. B., Natha, R. S., Gururaj, A. E., et al. (2010). Acetylation-dependent oncogenic activity of metastasis-associated protein 1 co-regulator. EMBO Reports, 11(9), 691–697. doi:10.1038/embor.2010.99.
Pakala, S. B., Singh, K., Reddy, S. D., Ohshiro, K., Li, D. Q., Mishra, L., et al. (2011). TGF-beta1 signaling targets metastasis-associated protein 1, a new effector in epithelial cells. Oncogene, 30(19), 2230–2241. doi:10.1038/onc.2010.608.
Mazumdar, A., Wang, R. A., Mishra, S. K., Adam, L., Bagheri-Yarmand, R., Mandal, M., et al. (2001). Transcriptional repression of oestrogen receptor by metastasis-associated protein 1 corepressor. Nature Cell Biology, 3(1), 30–37.
Luo, J. Y., Su, F., Chen, D. L., Shiloh, A., & Gu, W. (2000). Deacetylation of p53 modulates its effect on cell growth and apoptosis. Nature, 408(6810), 377–381.
Yoo, Y. G., Kong, G., & Lee, M. O. (2006). Metastasis-associated protein 1 enhances stability of hypoxia-inducible factor-1 alpha protein by recruiting histone deacetylase 1. EMBO Journal, 25(6), 1231–1241. doi:10.1038/sj.emboj.7601025.
Gururaj, A. E., Singh, R. R., Rayala, S. K., Holm, C., den Hollander, P., Zhang, H., et al. (2006). MTA1, a transcriptional activator of breast cancer amplified sequence 3. Proceedings of the National Academy of Sciences of the United States of America, 103(17), 6670–6675. doi:10.1073/pnas.0601989103.
Balasenthil, S., Gururaj, A. E., Talukder, A. H., Bagheri-Yarmand, R., Arrington, T., Haas, B. J., et al. (2007). Identification of Pax5 as a target of MTA1 in B-cell lymphomas. Cancer Research, 67(15), 7132–7138. doi:10.1158/0008-5472.Can-07-0750.
Cobaleda, C., Schebesta, A., Delogu, A., & Busslinger, M. (2007). Pax5: the guardian of B cell identity and function. Nature Immunology, 8(5), 463–470. doi:10.1038/ni1454.
Pakala, S. B., Bui-Nguyen, T. M., Reddy, S. D., Li, D. Q., Peng, S., Rayala, S. K., et al. (2010). Regulation of NF-kappaB circuitry by a component of the nucleosome remodeling and deacetylase complex controls inflammatory response homeostasis. Journal of Biological Chemistry, 285(31), 23590–23597. doi:10.1074/jbc.M110.139469.
Pakala, S. B., Reddy, S. D., Bui-Nguyen, T. M., Rangparia, S. S., Bommana, A., & Kumar, R. (2010). MTA1 coregulator regulates LPS response via MyD88-dependent signaling. Journal of Biological Chemistry, 285(43), 32787–32792. doi:10.1074/jbc.M110.151340.
Ghanta, K. S., Pakala, S. B., Reddy, S. D., Li, D. Q., Nair, S. S., & Kumar, R. (2011). MTA1 coregulation of transglutaminase 2 expression and function during inflammatory response. Journal of Biological Chemistry, 286(9), 7132–7138. doi:10.1074/jbc.M110.199273.
Coussens, L. M., & Werb, Z. (2002). Inflammation and cancer. Nature, 420(6917), 860–867. doi:10.1038/nature01322.
Mantovani, A., Allavena, P., Sica, A., & Balkwill, F. (2008). Cancer-related inflammation. Nature, 454(7203), 436–444. doi:10.1038/nature07205.
Divijendra, S., Reddy, N., Pakala, S. B., Ohshiro, K., Rayala, S. K., & Kumar, R. (2009). MicroRNA-661, a c/EBP alpha target, inhibits metastatic tumor antigen 1 and regulates its functions. Cancer Research, 69(14), 5639–5642. doi:10.1158/0008-5472.can-09-0898.
Bui-Nguyen, T. M., Pakala, S. B., Sirigiri, D. R., Martin, E., Murad, F., & Kumar, R. (2010). Stimulation of inducible nitric oxide by hepatitis B virus transactivator protein HBx requires MTA1 coregulator. Journal of Biological Chemistry, 285(10), 6980–6986. doi:10.1074/jbc.M109.065987.
Li, Y., VandenBoom, T. G., II, Wang, Z., Kong, D., Ali, S., Philip, P. A., et al. (2010). miR-146a suppresses invasion of pancreatic cancer cells. Cancer Research, 70(4), 1486–1495. doi:10.1158/0008-5472.can-09-2792.
Kaller, M., Liffers, S.-T., Oeljeklaus, S., Kuhlmann, K., Roeh, S., Hoffmann, R., et al. (2011). Genome-wide characterization of miR-34a induced changes in protein and mRNA expression by a combined pulsed SILAC and microarray analysis. Molecular & Cellular Proteomics, 10(8), doi:10.1074/mcp.M111.010462.
Zhou, H., Xu, X., Xun, Q., Yu, D., Ling, J., Guo, F., et al. (2012). microRNA-30c negatively regulates endometrial cancer cells by targeting metastasis-associated gene-1. Oncology Reports, 27(3), 807–812. doi:10.3892/or.2011.1574.
Xia, Y., Chen, Q., Zhong, Z., Xu, C., Wu, C., Liu, B., et al. (2013). Down-regulation of miR-30c promotes the invasion of non-small cell lung cancer by targeting MTA1. Cellular Physiology and Biochemistry, 32(2), 476– 485. doi:10.1159/000354452.
Chu, H., Chen, X., Wang, H., Du, Y., Wang, Y., Zang, W., et al. (2014). MiR-495 regulates proliferation and migration in NSCLC by targeting MTA3. Tumor Biology, 35(4), 3487–3494. doi:10.1007/s13277-013-1460-1.
Baek, D., Villen, J., Shin, C., Camargo, F. D., Gygi, S. P., & Bartel, D. P. (2008). The impact of microRNAs on protein output. Nature, 455(7209), 64–71. doi:10.1038/nature07242.
Selbach, M., Schwanhausser, B., Thierfelder, N., Fang, Z., Khanin, R., & Rajewsky, N. (2008). Widespread changes in protein synthesis induced by microRNAs. Nature, 455(7209), 58–63. doi:10.1038/nature07228.
He, L., He, X., Lim, L. P., de Stanchina, E., Xuan, Z., Liang, Y., et al. (2007). A microRNA component of the p53 tumour suppressor network. Nature, 447(7148), 1130–1134. doi:10.1038/nature05939.
Zhu, X., Zhang, X., Wang, H., Song, Q., Zhang, G., Yang, L., et al. (2012). MTA1 gene silencing inhibits invasion and alters the microRNA expression profile of human lung cancer cells. Oncology Reports, 28(1), 218–224. doi:10.3892/or.2012.1770.
Li, Y., Chao, Y., Fang, Y., Wang, J., Wang, M., Zhang, H., et al. (2013). MTA1 promotes the invasion and migration of non-small cell lung cancer cells by downregulating miR-125b. Journal of Experimental & Clinical Cancer Research, 32, doi:10.1186/1756-9966-32-33.
Kumar, R., Wang, R. A., Mazumdar, A., Talukder, A. H., Mandal, M., Yang, Z. B., et al. (2002). A naturally occurring MTA1 variant sequesters oestrogen receptor-alpha in the cytoplasm. Nature, 418(6898), 654–657. doi:10.1038/nature00889.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zhang, Y., Wang, XF. Post-transcriptional regulation of MTA family by microRNAs in the context of cancer. Cancer Metastasis Rev 33, 1011–1016 (2014). https://doi.org/10.1007/s10555-014-9526-0
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10555-014-9526-0