Role of MTA1 in cancer progression and metastasis

Cancer and Metastasis Reviews

Volumn 33, Issue 4, 2014, Pages 879-889

  Sen, Nirmalya ^a   Gui, Bin ^a   Kumar, Rakesh ^a  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

Cancer and metastasis; Chromatin remodeling; Epigenetics; Gene expression; MTA1; Signaling; Therapeutic resistance

Indexed keywords

BINDING PROTEIN; CARRIER PROTEINS AND BINDING PROTEINS; COREPRESSOR PROTEIN; METASTASIS ASSOCIATED PROTEIN 1; NUCLEAR RECEPTOR COACTIVATOR; PROTEIN VARIANT; UNCLASSIFIED DRUG; HISTONE DEACETYLASE; MTA1 PROTEIN, HUMAN; PROTEOME; REPRESSOR PROTEIN;

ARTICLE; BREAST CANCER; CANCER CELL; CANCER GROWTH; CANCER RESISTANCE; CHROMATIN ASSEMBLY AND DISASSEMBLY; ENZYME KINETICS; GENE CONTROL; GENE EXPRESSION; GENE TARGETING; HUMAN; MALIGNANT NEOPLASTIC DISEASE; METASTASIS; NUCLEOSOME; PLASTICITY; PROTEIN ACETYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METHYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; SUMOYLATION; UBIQUITINATION; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; NEOPLASM; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

CHROMATIN ASSEMBLY AND DISASSEMBLY; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONE DEACETYLASES; HUMANS; MI-2 NUCLEOSOME REMODELING AND DEACETYLASE COMPLEX; NEOPLASMS; PROTEOME; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION;

EID: 84914150085     PISSN: 01677659     EISSN: 15737233     Source Type: Journal    
DOI: 10.1007/s10555-014-9515-3     Document Type: Article

References (62)

1. 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. The Journal of Biological Chemistry, 269(37), 22958–22963.
2. Kumar, R., Wang, R. A., & Bagheri-Yarmand, R. (2003). Emerging roles of MTA family members in human cancers. Seminars in Oncology, 30(5 Suppl 16), 30–37.
3. Bowen, N. J., Fujita, N., Kajita, M., & Wade, P. A. (2004). Mi-2/NuRD: multiple complexes for many purposes. Biochimica et Biophysica Acta, 1677(1–3), 52–57.
4. Manavathi, B., & Kumar, R. (2007). Metastasis tumor antigens, an emerging family of multifaceted master coregulators. The Journal of Biological Chemistry, 282(3), 1529–1533.
5. Singh, R. R., & Kumar, R. (2007). MTA family of transcriptional metaregulators in mammary gland morphogenesis and breast cancer. Journal of Mammary Gland Biology and Neoplasia, 12(2–3), 115–125. doi:10.1007/s10911-007-9043-7.
6. Denslow, S. A., & Wade, P. A. (2007). The human Mi-2/NuRD complex and gene regulation. Oncogene, 26(37), 5433–5438.
7. Li, D. Q., Pakala, S. B., Nair, S. S., Eswaran, J., & Kumar, R. Metastasis-associated protein 1/nucleosome remodeling and histone deacetylase complex in cancer. Cancer Res, 72(2), 387–394.
8. 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.
9. Li, W., Ma, L., Zhao, J., Liu, X., Li, Z., & Zhang, Y. (2009). Expression profile of MTA1 in adult mouse tissues. Tissue and Cell, 41(6), 390–399.
10. Liu, J., Xu, D., Wang, H., Zhang, Y., Chang, Y., Zhang, J., et al. The subcellular distribution and function of MTA1 in cancer differentiation. Oncotarget, 5(13), 5153–5164.
11. Ohshiro, K., Rayala, S. K., Wigerup, C., Pakala, S. B., Natha, R. S., Gururaj, A. E., et al. Acetylation-dependent oncogenic activity of metastasis-associated protein 1 co-regulator. EMBO Rep, 11(9), 691–697.
12. Kumar, R., Balasenthil, S., Manavathi, B., Rayala, S. K., & Pakala, S. B. Metastasis-associated protein 1 and its short form variant stimulates Wnt1 transcription through promoting its derepression from Six3 corepressor. Cancer Res, 70(16), 6649–6658.
13. Kumar, R., Balasenthil, S., Pakala, S. B., Rayala, S. K., Sahin, A. A., & Ohshiro, K. Metastasis-associated protein 1 short form stimulates Wnt1 pathway in mammary epithelial and cancer cells. Cancer Res, 70(16), 6598–6608.
14. Pakala, S. B., Rayala, S. K., Wang, R. A., Ohshiro, K., Mudvari, P., Reddy, S. D., et al. MTA1 promotes STAT3 transcription and pulmonary metastasis in breast cancer. Cancer Res, 73(12), 3761–3770.
15. Zhang, X. Y., DeSalle, L. M., Patel, J. H., Capobianco, A. J., Yu, D., Thomas-Tikhonenko, A., et al. (2005). Metastasis-associated protein 1 (MTA1) is an essential downstream effector of the c-MYC oncoprotein. Proceedings of the National Academy of Sciences of the United States of America, 102(39), 13968–13973.
16. Li, D. Q., Divijendra Natha Reddy, S., Pakala, S. B., Wu, X., Zhang, Y., Rayala, S. K., et al. (2009). MTA1 coregulator regulates p53 stability and function. The Journal of Biological Chemistry, 284(50), 34545–34552.
17. Li, D. Q., Pakala, S. B., Reddy, S. D., Ohshiro, K., Peng, S. H., Lian, Y., et al. Revelation of p53-independent function of MTA1 in DNA damage response via modulation of the p21 WAF1-proliferating cell nuclear antigen pathway. J Biol Chem, 285(13), 10044–10052.
18. Li, D. Q., & Kumar, R. Mi-2/NuRD complex making inroads into DNA-damage response pathway. Cell Cycle, 9(11), 2071–2079.
19. Xue, Y., Wong, J., Moreno, G. T., Young, M. K., Cote, J., & Wang, W. (1998). NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Molecular Cell, 2(6), 851–861.
20. Zhang, Y., Ng, H. H., Erdjument-Bromage, H., Tempst, P., Bird, A., & Reinberg, D. (1999). Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation. Genes and Development, 13(15), 1924–1935.
21. Yao, Y. L., & Yang, W. M. (2003). The metastasis-associated proteins 1 and 2 form distinct protein complexes with histone deacetylase activity. The Journal of Biological Chemistry, 278(43), 42560–42568.
22. Liu, X. F., & Bagchi, M. K. (2004). Recruitment of distinct chromatin-modifying complexes by tamoxifen-complexed estrogen receptor at natural target gene promoters in vivo. The Journal of Biological Chemistry, 279(15), 15050–15058.
23. Singh, R. R., Barnes, C. J., Talukder, A. H., Fuqua, S. A., & Kumar, R. (2005). Negative regulation of estrogen receptor alpha transactivation functions by LIM domain only 4 protein. Cancer Research, 65(22), 10594–10601.
24. Khaleque, M. A., Bharti, A., Gong, J., Gray, P. J., Sachdev, V., Ciocca, D. R., et al. (2008). Heat shock factor 1 represses estrogen-dependent transcription through association with MTA1. Oncogene, 27(13), 1886–1893.
25. Mishra, S. K., Mazumdar, A., Vadlamudi, R. K., Li, F., Wang, R. A., Yu, W., et al. (2003). MICoA, a novel metastasis-associated protein 1 (MTA1) interacting protein coactivator, regulates estrogen receptor-alpha transactivation functions. The Journal of Biological Chemistry, 278(21), 19209–19219.
26. Talukder, A. H., Gururaj, A., Mishra, S. K., Vadlamudi, R. K., & Kumar, R. (2004). Metastasis-associated protein 1 interacts with NRIF3, an estrogen-inducible nuclear receptor coregulator. Molecular and Cellular Biology, 24(15), 6581–6591.
27. Talukder, A. H., Mishra, S. K., Mandal, M., Balasenthil, S., Mehta, S., Sahin, A. A., et al. (2003). MTA1 interacts with MAT1, a cyclin-dependent kinase-activating kinase complex ring finger factor, and regulates estrogen receptor transactivation functions. The Journal of Biological Chemistry, 278(13), 11676–11685.
28. Covington, K. R., Brusco, L., Barone, I., Tsimelzon, A., Selever, J., Corona-Rodriguez, A., et al. Metastasis tumor-associated protein 2 enhances metastatic behavior and is associated with poor outcomes in estrogen receptor-negative breast cancer. Breast Cancer Res Treat. doi:10.1007/s10549-013-2709-5.
29. Cui, Y., Niu, A., Pestell, R., Kumar, R., Curran, E. M., Liu, Y., et al. (2006). Metastasis-associated protein 2 is a repressor of estrogen receptor alpha whose overexpression leads to estrogen-independent growth of human breast cancer cells. Molecular Endocrinology, 20(9), 2020–2035.
30. Fujita, N., Jaye, D. L., Kajita, M., Geigerman, C., Moreno, C. S., & Wade, P. A. (2003). MTA3, a Mi-2/NuRD complex subunit, regulates an invasive growth pathway in breast cancer. Cell, 113(2), 207–219.
31. Kumar, R. (2003). Another tie that binds the MTA family to breast cancer. Cell, 113(2), 142–143.
32. Zhang, H., Stephens, L. C., & Kumar, R. (2006). Metastasis tumor antigen family proteins during breast cancer progression and metastasis in a reliable mouse model for human breast cancer. Clinical Cancer Research, 12(5), 1479–1486.
33. Kumar, R., Wang, R. A., Mazumdar, A., Talukder, A. H., Mandal, M., Yang, Z., et al. (2002). A naturally occurring MTA1 variant sequesters oestrogen receptor-alpha in the cytoplasm. Nature, 418(6898), 654–657.
34. Mishra, S. K., Yang, Z., Mazumdar, A., Talukder, A. H., Larose, L., & Kumar, R. (2004). Metastatic tumor antigen 1 short form (MTA1s) associates with casein kinase I-gamma2, an estrogen-responsive kinase. Oncogene, 23(25), 4422–4429.
35. 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.
36. Zhou, J., Zhan, S., Tan, W., Cheng, R., Gong, H., & Zhu, Q. P300 binds to and acetylates MTA2 to promote colorectal cancer cells growth. Biochem Biophys. Res Commun, 444(3), 387–390.
37. Li, D. Q., Ohshiro, K., Reddy, S. D., Pakala, S. B., Lee, M. H., Zhang, Y., et al. (2009). E3 ubiquitin ligase COP1 regulates the stability and functions of MTA1. Proceedings of the National Academy of Sciences of the United States of America, 106(41), 17493–17498.
38. Cong, L., Pakala, S. B., Ohshiro, K., Li, D. Q., & Kumar, R. SUMOylation and SUMO-interacting motif (SIM) of metastasis tumor antigen 1 (MTA1) synergistically regulate its transcriptional repressor function. J Biol Chem, 286(51), 43793–43808.
39. Van Rechem, C., Boulay, G., Pinte, S., Stankovic-Valentin, N., Guerardel, C., & Leprince, D. Differential regulation of HIC1 target genes by CtBP and NuRD, via an acetylation/SUMOylation switch, in quiescent versus proliferating cells. Mol Cell Biol, 30(16), 4045–4059.
40. Nair, S. S., Li, D. Q., & Kumar, R. A core chromatin remodeling factor instructs global chromatin signaling through multivalent reading of nucleosome codes. Mol Cell, 49(4), 704–718.
41. http://www.nursa.org/
42. Yoo, Y. G., Kong, G., & Lee, M. O. (2006). Metastasis-associated protein 1 enhances stability of hypoxia-inducible factor-1alpha protein by recruiting histone deacetylase 1. The EMBO Journal, 25(6), 1231–1241.
43. Deng, X., Du, L., Wang, C., Yang, Y., Li, J., Liu, H., et al. Close association of metastasis-associated protein 1 overexpression with increased angiogenesis and poor survival in patients with histologically node-negative gastric cancer. World J Surg, 37(4), 792–798.
44. Jang, K. S., Paik, S. S., Chung, H., Oh, Y. H., & Kong, G. (2006). MTA1 overexpression correlates significantly with tumor grade and angiogenesis in human breast cancers. Cancer Science, 97(5), 374–379.
45. Li, S. H., Tian, H., Yue, W. M., Li, L., Gao, C., et al. (2012). Metastasis-associated protein 1 nuclear expression is closely associated with tumor progression and angiogenesis in patients with esophageal squamous cell cancer. World Journal of Surgery, 36(3), 623–631.
46. Li, S. H., Tian, H., Yue, W. M., Li, L., Li, W. J., Chen, Z. T., et al. (2011). Overexpression of metastasis-associated protein 1 is significantly correlated with tumor angiogenesis and poor survival in patients with early-stage non-small cell lung cancer. Annals of Surgical Oncology, 18(7), 2048–2056.
47. Kai, L., Wang, J., Ivanovic, M., Chung, Y. T., Laskin, W. B., Schulze-Hoepfner, F., et al. Targeting prostate cancer angiogenesis through metastasis-associated protein 1 (MTA1). Prostate, 71(3), 268–280.
48. Weng, W., Yin, J., Zhang, Y., Qiu, J., & Wang, X. Metastasis-associated protein 1 promotes tumor invasion by downregulation of E-cadherin. Int J Oncol, 44(3), 812–818.
49. Kang, H. J., Lee, M. H., Kang, H. L., Kim, S. H., Ahn, J. R., Na, H., et al. Differential regulation of estrogen receptor alpha expression in breast cancer cells by metastasis-associated protein 1. Cancer Res, 74(5), 1484–1494.
50. Dhasarathy, A., Kajita, M., & Wade, P. A. (2007). The transcription factor snail mediates epithelial to mesenchymal transitions by repression of estrogen receptor-alpha. Molecular Endocrinology, 21(12), 2907–2918.
51. Salot, S., & Gude, R. MTA1-mediated transcriptional repression of SMAD7 in breast cancer cell lines. Eur J Cancer, 49(2), 492–499.
52. Gururaj, A. E., Holm, C., Landberg, G., & Kumar, R. (2006). Breast cancer-amplified sequence 3, a target of metastasis-associated protein 1, contributes to tamoxifen resistance in premenopausal patients with breast cancer. Cell Cycle, 5(13), 1407–1410.
53. Hofer, M. D., Kuefer, R., Varambally, S., Li, H., Ma, J., Shapiro, G. I., et al. (2004). The role of metastasis-associated protein 1 in prostate cancer progression. Cancer Research, 64(3), 825–829.
54. Li, K., Dias, S. J., Rimando, A. M., Dhar, S., Mizuno, C. S., Penman, A. D., et al. (2013). Pterostilbene acts through metastasis-associated protein 1 to inhibit tumor growth, progression and metastasis in prostate cancer. PLoS ONE, 8(3), e57542.
55. Yu, L., Su, Y. S., Zhao, J., Wang, H., & Li, W. Repression of NR4A1 by a chromatin modifier promotes docetaxel resistance in PC-3 human prostate cancer cells. FEBS Lett, 587(16), 2542–2551.
56. Feng, X., Zhang, Q., Xia, S., Xia, B., Zhang, Y., Deng, X., et al. (2014). MTA1 overexpression induces cisplatin resistance in nasopharyngeal carcinoma by promoting cancer stem cells properties. Molecules and Cells. doi:10.14348/molcells.2014.0029.
57. Ghanta, K. S., Li, D. Q., Eswaran, J., & Kumar, R. Gene profiling of MTA1 identifies novel gene targets and functions. PLoS One, 6(2), e17135.
58. Lehner, B., Crombie, C., Tischler, J., Fortunato, A., & Fraser, A. G. (2006). Systematic mapping of genetic interactions in Caenorhabditis elegans identifies common modifiers of diverse signaling pathways. Nature Genetics, 38(8), 896–903.
59. Wu, M., Wang, L., Li, Q., Li, J., Qin, J., & Wong, J. (2013). The MTA family proteins as novel histone H3 binding proteins. Cell Bioscience, 3(1), 1.
60. Toh, Y., Ohga, T., Endo, K., Adachi, E., Kusumoto, H., Haraguchi, M., et al. (2004). Expression of the metastasis-associated MTA1 protein and its relationship to deacetylation of the histone H4 in esophageal squamous cell carcinomas. International Journal of Cancer, 110(3), 362–367.
61. Liu, J., Wang, H., Ma, F., Xu, D., Chang, Y., Zhang, J., et al. (2014). MTA1 regulates higher-order chromatin structure and histone H1-chromatin interaction in-vivo. Mol Oncol. doi:10.1016/j.molonc.2014.08.007.
62. Metzger, E., Wissmann, M., Yin, N., Muller, J. M., Schneider, R., Peters, A. H., et al. (2005). LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature, 437(7057), 436–439.