An epigenetic regulator: Methyl-CpG-binding domain protein 1 (MBD1)

International Journal of Molecular Sciences

Volumn 16, Issue 3, 2015, Pages 5125-5140

  Li, Lu ^a   Chen, Bi Feng ^a,b   Chan, Wai Yee ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b WUHAN UNIVERSITY OF TECHNOLOGY   (China)

Author keywords

Cancer; Epigenetic regulation; Methyl CpG binding domain protein 1; Nervous system; Transcriptional repression

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; GAMMA INTERFERON; METHYL CPG BINDING PROTEIN; METHYL CPG BINDING PROTEIN 2; MICRORNA; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 1A; RETINOBLASTOMA PROTEIN; STAT1 PROTEIN; TISSUE INHIBITOR OF METALLOPROTEINASE 3; UVOMORULIN; DNA BINDING PROTEIN; MBD1 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ALTERNATIVE RNA SPLICING; APOPTOSIS; BREAST CANCER; CANCER CELL LINE; CANCER RISK; CARCINOGENESIS; CELL DIFFERENTIATION; CELL PROLIFERATION; DNA DAMAGE; DNA METHYLATION; DNA POLYMORPHISM; EPIGENETICS; GENE EXPRESSION; GENETIC TRANSCRIPTION; HETEROCHROMATIN; LUNG CANCER; NERVOUS SYSTEM; PANCREAS CANCER; PROSTATE CANCER; REGULATOR GENE; REVIEW; ANTAGONISTS AND INHIBITORS; GENETIC EPIGENESIS; GENETICS; HUMAN; METABOLISM; NEOPLASM; PATHOLOGY;

CARCINOGENESIS; DNA METHYLATION; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; HUMANS; NEOPLASMS; NERVOUS SYSTEM; TRANSCRIPTION FACTORS;

EID: 84925871438     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms16035125     Document Type: Review

References (70)

1. Smith, Z.D.; Meissner, A. DNA methylation: Roles in mammalian development. Nat. Rev. Genet. 2013, 14, 204–220.
2. Jones, P.A. Functions of DNA methylation: Islands, start sites, gene bodies and beyond. Nat. Rev. Genet. 2012, 13, 484–492.
3. Svedruzic, Z.M. Dnmt1 structure and function. Prog. Mol. Biol. Transl. Sci. 2011, 101, 221–254.
4. Chedin, F. The DNMT3 family of mammalian de novo DNA methyltransferases. Prog. Mol. Biol. Transl. Sci. 2011, 101, 255–285.
5. Okano, M.; Bell, D.W.; Haber, D.A.; Li, E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999, 99, 247–257.
6. Chen, B.F.; Chan, W.Y. The de novo DNA methyltransferase DNMT3A in development and cancer. Epigenetics 2014, 9, 669–677.
7. Meehan, R.R.; Lewis, J.D.; McKay, S.; Kleiner, E.L.; Bird, A.P. Identification of a mammalian protein that binds specifically to DNA containing methylated CpGs. Cell 1989, 58, 499–507.
8. Parry, L.; Clarke, A.R. The roles of the methyl-CpG binding proteins in cancer. Genes Cancer 2011, 2, 618–630.
9. Roloff, T.C.; Ropers, H.H.; Nuber, U.A. Comparative study of methyl-CpG-binding domain proteins. BMC Genomics 2003, 4, doi:10.1186/1471-2164-4-1.
10. Hung, M.S.; Shen, C.K. Eukaryotic methyl-CpG-binding domain proteins and chromatin modification. Eukaryot. Cell 2003, 2, 841–846.
11. Hendrich, B.; Tweedie, S. The methyl-CpG binding domain and the evolving role of DNA methylation in animals. Trends Genet. 2003, 19, 269–277.
12. Schultz, D.C.; Ayyanathan, K.; Negorev, D.; Maul, G.G.; Rauscher, F.J. SETDB1: A novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev. 2002, 16, 919–932.
13. Groner, A.C.; Meylan, S.; Ciuffi, A.; Zangger, N.; Ambrosini, G.; Denervaud, N.; Bucher, P.; Trono, D. KRAB-zinc finger proteins and KAP1 can mediate long-range transcriptional repression through heterochromatin spreading. PLoS Genet. 2010, 6, e1000869.
14. Falandry, C.; Fourel, G.; Galy, V.; Ristriani, T.; Horard, B.; Bensimon, E.; Salles, G.; Gilson, E.; Magdinier, F. CLLD8/KMT1F is a lysine methyltransferase that is important for chromosome segregation. J. Biol. Chem. 2010, 285, 20234–20241.
15. Hendrich, B.; Bird, A. Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol. Cell. Biol. 1998, 18, 6538–6547.
16. Laget, S.; Joulie, M.; Le Masson, F.; Sasai, N.; Christians, E.; Pradhan, S.; Roberts, R.J.; Defossez, P.A. The human proteins MBD5 and MBD6 associate with heterochromatin but they do not bind methylated DNA. PLoS One 2010, 5, e11982.
17. Le Guezennec, X.; Vermeulen, M.; Brinkman, A.B.; Hoeijmakers, W.A.; Cohen, A.; Lasonder, E.; Stunnenberg, H.G. MBD2/NuRD and MBD3/NuRD, two distinct complexes with different biochemical and functional properties. Mol. Cell. Biol. 2006, 26, 843–851.
18. Baymaz, H.I.; Fournier, A.; Laget, S.; Ji, Z.; Jansen, P.W.; Smits, A.H.; Ferry, L.; Mensinga, A.; Poser, I.; Sharrocks, A.; et al. MBD5 and MBD6 interact with the human PR-DUB complex through their methyl-CpG-binding domain. Proteomics 2014, 14, 2179–2189.
19. Jorgensen, H.F.; Ben-Porath, I.; Bird, A.P. MBD1 is recruited to both methylated and nonmethylated CpGs via distinct DNA binding domains. Mol. Cell. Biol. 2004, 24, 3387–3395.
20. Xu, J.; Zhu, W.; Xu, W.; Yao, W.; Zhang, B.; Xu, Y.; Ji, S.; Liu, C.; Long, J.; Ni, Q.; Yu, X. Up-regulation of MBD1 promotes pancreatic cancer cell epithelial-mesenchymal transition and invasion by epigenetic down-regulation of E-cadherin. Curr. Mol. Med. 2013, 13, 387–400.
21. Luo, G.; Jin, C.; Long, J.; Fu, D.; Yang, F.; Xu, J.; Yu, X.; Chen, W.; Ni, Q. RNA interference of MBD1 in BxPC-3 human pancreatic cancer cells delivered by PLGA-poloxamer nanoparticles. Cancer Biol. Ther. 2009, 8, 594–598.
22. Xu, J.; Zhu, W.; Xu, W.; Cui, X.; Chen, L.; Ji, S.; Qin, Y.; Yao, W.; Liu, L.; Liu, C, et al. Silencing of MBD1 reverses pancreatic cancer therapy resistance through inhibition of DNA damage repair. Int. J. Oncol. 2013, 42, 2046–2052.
23. Xu, J.; Liu, C.; Yu, X.J.; Jin, C.; Fu, D.L.; Ni, Q.X. Activation of multiple tumor suppressor genes by MBD1 siRNA in pancreatic cancer cell line BxPC-3. Zhonghua Yi Xue Za Zhi 2008, 88, 1948–1951.
24. Yaqinuddin, A.; Abbas, F.; Naqvi, S.Z.; Bashir, M.U.; Qazi, R.; Qureshi, S.A. Silencing of MBD1 and MeCP2 in prostate-cancer-derived PC3 cells produces differential gene expression profiles and cellular phenotypes. Biosci. Rep. 2008, 28, 319–326.
25. Schenk, M.; Leib-Mosch, C.; Schenck, I.U.; Jaenicke, M.; Indraccolo, S.; Saeger, H.D.; Dallenbach-Hellweg, G.; Hehlmann, R. Lower frequency of allele loss on chromosome 18q in human breast cancer than in colorectal tumors. J. Mol. Med. 1996, 74, 155–159.
26. Bader, S.; Walker, M.; McQueen, H.A.; Sellar, R.; Oei, E.; Wopereis, S.; Zhu, Y.; Peter, A.; Bird, A.P.; Harrison, D.J. MBD1, MBD2 and CGBP genes at chromosome 18q21 are infrequently mutated in human colon and lung cancers. Oncogene 2003, 22, 3506–3510.
27. Harlid, S.; Ivarsson, M.I.; Butt, S.; Hussain, S.; Grzybowska, E.; Eyfjord, J.E.; Lenner, P.; Forsti, A.; Hemminki, K.; Manjer, J.; et al. A candidate CpG SNP approach identifies a breast cancer associated ESR1-SNP. Int. J. Cancer 2011, 129, 1689–1698.
28. Liu, H.; Jin, G.; Wang, H.; Wu, W.; Liu, Y.; Qian, J.; Fan, W.; Ma, H.; Miao, R.; Hu, Z, et al. Methyl-CpG binding domain 1 gene polymorphisms and lung cancer risk in a Chinese population. Biomarkers 2008, 13, 607–617.
29. Zhao, X.; Ueba, T.; Christie, B.R.; Barkho, B.; McConnell, M.J.; Nakashima, K.; Lein, E.S.; Eadie, B.D.; Willhoite, A.R.; Muotri, A.R, et al. Mice lacking methyl-CpG binding protein 1 have deficits in adult neurogenesis and hippocampal function. Proc. Natl. Acad. Sci. USA 2003, 100, 6777–6782.
30. Allan, A.M.; Liang, X.; Luo, Y.; Pak, C.; Li, X.; Szulwach, K.E.; Chen, D.; Jin, P.; Zhao, X. The loss of methyl-CpG binding protein 1 leads to autism-like behavioral deficits. Hum. Mol. Genet. 2008, 17, 2047–2057.
31. Li, H.; Yamagata, T.; Mori, M.; Yasuhara, A.; Momoi, M.Y. Mutation analysis of methyl-CpG binding protein family genes in autistic patients. Brain Dev. 2005, 27, 321–325.
32. Yonan, A.L.; Alarcon, M.; Cheng, R.; Magnusson, P.K.; Spence, S.J.; Palmer, A.A.; Grunn, A.; Juo, S.H.; Terwilliger, J.D.; Liu, J.; et al. A genomewide screen of 345 families for autism-susceptibility loci. Am. J. Hum. Genet. 2003, 73, 886–897.
33. Li, X.; Barkho, B.Z.; Luo, Y.; Smrt, R.D.; Santistevan, N.J.; Liu, C.; Kuwabara, T.; Gage, F.H.; Zhao, X. Epigenetic regulation of the stem cell mitogen Fgf-2 by MBD1 in adult neural stem/progenitor cells. J. Biol. Chem. 2008, 283, 27644–27652.
34. Liu, C.; Teng, Z.Q.; Santistevan, N.J.; Szulwach, K.E.; Guo, W.; Jin, P.; Zhao, X. Epigenetic regulation of miR-184 by MBD1 governs neural stem cell proliferation and differentiation. Cell Stem Cell 2010, 6, 433–444.
35. Liu, C.; Teng, Z.Q.; McQuate, A.L.; Jobe, E.M.; Christ, C.C.; von Hoyningen-Huene, S.J.; Reyes, M.D.; Polich, E.D.; Xing, Y.; Li, Y, et al. An epigenetic feedback regulatory loop involving microRNA-195 and MBD1 governs neural stem cell differentiation. PLoS One 2013, 8, e51436.
36. Monnier, P.; Martinet, C.; Pontis, J.; Stancheva, I.; Ait-Si-Ali, S.; Dandolo, L. H19 lncRNA controls gene expression of the imprinted gene network by recruiting MBD1. Proc. Natl. Acad. Sci. USA 2013, 110, 20693–20698.
37. Ng, H.H.; Jeppesen, P.; Bird, A. Active repression of methylated genes by the chromosomal protein MBD1. Mol. Cell. Biol. 2000, 20, 1394–1406.
38. Ohki, I.; Shimotake, N.; Fujita, N.; Jee, J.; Ikegami, T.; Nakao, M.; Shirakawa, M. Solution structure of the methyl-CpG binding domain of human MBD1 in complex with methylated DNA. Cell 2001, 105, 487–497.
39. Luger, K.; Mader, A.W.; Richmond, R.K.; Sargent, D.F.; Richmond, T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 1997, 389, 251–260.
40. Fujita, N.; Takebayashi, S.; Okumura, K.; Kudo, S.; Chiba, T.; Saya, H.; Nakao, M. Methylation-mediated transcriptional silencing in euchromatin by methyl-CpG binding protein MBD1 isoforms. Mol. Cell. Biol. 1999, 19, 6415–6426.
41. Nakao, M.; Matsui, S.; Yamamoto, S.; Okumura, K.; Shirakawa, M.; Fujita, N. Regulation of transcription and chromatin by methyl-CpG binding protein MBD 1. Brain Dev. 2001, 23, S174–S176.
42. Fujita, N.; Shimotake, N.; Ohki, I.; Chiba, T.; Saya, H.; Shirakawa, M.; Nakao, M. Mechanism of transcriptional regulation by methyl-CpG binding protein MBD 1. Mol. Cell. Biol. 2000, 20, 5107–5118.
43. Kafri, T.; Ariel, M.; Brandeis, M.; Shemer, R.; Urven, L.; McCarrey, J.; Cedar, H.; Razin, A. Developmental pattern of gene-specific DNA methylation in the mouse embryo and germ line. Genes Dev. 1992, 6, 705–714.
44. Bird, A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002, 16, 6–21.
45. Baubec, T.; Ivanek, R.; Lienert, F.; Schubeler, D. Methylation-dependent and -independent genomic targeting principles of the MBD protein family. Cell 2013, 153, 480–492.
46. Clouaire, T.; de Las Heras, J.I.; Merusi, C.; Stancheva, I. Recruitment of MBD1 to target genes requires sequence-specific interaction of the MBD domain with methylated DNA. Nucleic Acids Res. 2010, 38, 4620–4634.
47. Baylin, S.B. DNA methylation and gene silencing in cancer. Nat. Clin. Pract. Oncol. 2005, 2, S4–S11.
48. Carone, D.M.; Lawrence, J.B. Heterochromatin instability in cancer: From the Barr body to satellites and the nuclear periphery. Semin. Cancer Biol. 2013, 23, 99–108.
49. Ichimura, T.; Watanabe, S.; Sakamoto, Y.; Aoto, T.; Fujita, N.; Nakao, M. Transcriptional repression and heterochromatin formation by MBD1 and MCAF/AM family proteins. J. Biol. Chem. 2005, 280, 13928–13935.
50. Sarraf, S.A.; Stancheva, I. Methyl-CpG binding protein MBD1 couples histone H3 methylation at lysine 9 by SETDB1 to DNA replication and chromatin assembly. Mol. Cell 2004, 15, 595–605.
51. Hameed, U.F.; Lim, J.; Zhang, Q.; Wasik, M.A.; Yang, D.; Swaminathan, K. Transcriptional repressor domain of MBD1 is intrinsically disordered and interacts with its binding partners in a selective manner. Sci. Rep. 2014, 4, 4896.
52. Minkovsky, A.; Sahakyan, A.; Rankin-Gee, E.; Bonora, G.; Patel, S.; Plath, K. The Mbd1-Atf7ip-Setdb1 pathway contributes to the maintenance of X chromosome inactivation. Epigenet. Chromatin 2014, 7, 12.
53. Lyst, M.J.; Nan, X.; Stancheva, I. Regulation of MBD1-mediated transcriptional repression by SUMO and PIAS proteins. EMBO J. 2006, 25, 5317–5328.
54. Uchimura, Y.; Ichimura, T.; Uwada, J.; Tachibana, T.; Sugahara, S.; Nakao, M.; Saitoh, H. Involvement of SUMO modification in MBD1- and MCAF1-mediated heterochromatin formation. J. Biol. Chem. 2006, 281, 23180–23190.
55. Sakamoto, Y.; Watanabe, S.; Ichimura, T.; Kawasuji, M.; Koseki, H.; Baba, H.; Nakao, M. Overlapping roles of the methylated DNA-binding protein MBD1 and polycomb group proteins in transcriptional repression of HOXA genes and heterochromatin foci formation. J. Biol. Chem. 2007, 282, 16391–16400.
56. Villa, R.; Morey, L.; Raker, V.A.; Buschbeck, M.; Gutierrez, A.; de Santis, F.; Corsaro, M.; Varas, F.; Bossi, D.; Minucci, S.; et al. The methyl-CpG binding protein MBD1 is required for PML-RARα function. Proc. Natl. Acad. Sci. USA 2006, 103, 1400–1405.
57. Watanabe, S.; Ichimura, T.; Fujita, N.; Tsuruzoe, S.; Ohki, I.; Shirakawa, M.; Kawasuji, M.; Nakao, M. Methylated DNA-binding domain 1 and methylpurine-DNA glycosylase link transcriptional repression and DNA repair in chromatin. Proc. Natl. Acad. Sci. USA 2003, 100, 12859–12864.
58. Taby, R.; Issa, J.P. Cancer epigenetics. CA Cancer J. Clin. 2010, 60, 376–392.
59. McGough, J.M.; Yang, D.; Huang, S.; Georgi, D.; Hewitt, S.M.; Rocken, C.; Tanzer, M.; Ebert, M.P.; Liu, K. DNA methylation represses IFN-γ-induced and signal transducer and activator of transcription 1-mediated IFN regulatory factor 8 activation in colon carcinoma cells. Mol. Cancer Res. 2008, 6, 1841–1851.
60. Bernstein, B.E.; Meissner, A.; Lander, E.S. The mammalian epigenome. Cell 2007, 128, 669–681.
61. Meza-Sosa, K.F.; Pedraza-Alva, G.; Perez-Martinez, L. MicroRNAs: Key triggers of neuronal cell fate. Front. Cell. Neurosci. 2014, 8, 175.
62. Lopez-Serra, L.; Ballestar, E.; Fraga, M.F.; Alaminos, M.; Setien, F.; Esteller, M. A profile of methyl-CpG binding domain protein occupancy of hypermethylated promoter CpG islands of tumor suppressor genes in human cancer. Cancer Res. 2006, 66, 8342–8346.
63. Hendrich, B.; Guy, J.; Ramsahoye, B.; Wilson, V.A.; Bird, A. Closely related proteins MBD2 and MBD3 play distinctive but interacting roles in mouse development. Genes Dev. 2001, 15, 710–723.
64. Guy, J.; Hendrich, B.; Holmes, M.; Martin, J.E.; Bird, A. A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat. Genet. 2001, 27, 322–326.
65. Chen, R.Z.; Akbarian, S.; Tudor, M.; Jaenisch, R. Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat. Genet. 2001, 27, 327–331.
66. Lei, H.; Oh, S.P.; Okano, M.; Juttermann, R.; Goss, K.A.; Jaenisch, R.; Li, E. De novo DNA cytosine methyltransferase activities in mouse embryonic stem cells. Development 1996, 122, 3195–3205.
67. Lopez-Serra, L.; Esteller, M. Proteins that bind methylated DNA and human cancer: Reading the wrong words. Br. J. Cancer 2008, 98, 1881–1885.
68. Klose, R.J.; Sarraf, S.A.; Schmiedeberg, L.; McDermott, S.M.; Stancheva, I.; Bird, A.P. DNA binding selectivity of MeCP2 due to a requirement for A/T sequences adjacent to methyl-CpG. Mol. Cell 2005, 19, 667–678.
69. Hendrich, B.; Hardeland, U.; Ng, H.H.; Jiricny, J.; Bird, A. The thymine glycosylase MBD4 can bind to the product of deamination at methylated CpG sites. Nature 1999, 401, 301–304.
70. Fujita, N.; Watanabe, S.; Ichimura, T.; Tsuruzoe, S.; Shinkai, Y.; Tachibana, M.; Chiba, T.; Nakao, M. Methyl-CpG binding domain 1 (MBD1) interacts with the Suv39h1-HP1 heterochromatic complex for DNA methylation-based transcriptional repression. J. Biol. Chem. 2003, 278, 24132–24138.