Metastasis tumor antigen 2 (MTA2) is involved in proper imprinted expression of H19 and Peg3 during mouse preimplantation development

Biology of Reproduction

Volumn 83, Issue 6, 2010, Pages 1027-1035

  Ma, Pengpeng ^a   Lin, Shu ^b   Bartolomei, Marisa S ^a   Schultz, Richard M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

DNA methylation; Embryo; Genomic imprinting; H19; MTA; NuRD complex; Peg3; RNAi

Indexed keywords

CHROMODOMAIN HELICASE DNA BINDING PROTEIN 4; DNA BINDING PROTEIN; HELICASE; HISTONE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; METASTASIS TUMOR ANTIGEN 2; METHYL BINDING CPG BINDING DOMAIN PROTEIN 3; PROTEIN SNRPN; REPRESSOR PROTEIN; RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DNA METHYLATION; EMBRYO; FEMALE; GENE; GENETIC TRANSCRIPTION; GENOME IMPRINTING; H19 GENE; MALE; METAPHASE CHROMOSOME; MOUSE; NONHUMAN; NUCLEOSOME; OOCYTE MATURATION; PEG3 GENE; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; RNA INTERFERENCE;

ANIMALS; BLASTOCYST; CELLS, CULTURED; DNA METHYLATION; EMBRYO CULTURE TECHNIQUES; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE SILENCING; GENES, REPORTER; GENOMIC IMPRINTING; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MI-2 NUCLEOSOME REMODELING AND DEACETYLASE COMPLEX; MICE; MICE, INBRED C57BL; MUTAGENESIS; OOCYTES; OOGENESIS; REPRESSOR PROTEINS; RNA INTERFERENCE; RNA, UNTRANSLATED; TRANS-ACTIVATORS; ZYGOTE;

EID: 78649935610     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.110.086397     Document Type: Article

References (56)

1. Wang GG, Allis CD, Chi P. Chromatin remodeling and cancer, part II: ATP-dependent chromatin remodeling. Trends Mol Med 2007; 13:373-380. (Pubitemid 47385382)
2. Denslow SA, Wade PA. The human Mi-2/NuRD complex and gene regulation. Oncogene 2007; 26:5433-5438.
3. Humphrey GW, Wang Y, Russanova VR, Hirai T, Qin J, Nakatani Y, Howard BH. Stable histone deacetylase complexes distinguished by the presence of SANT domain proteins CoREST/kiaa0071 and Mta-L1. J Biol Chem 2001; 276:6817-6824.
4. Tong JK, Hassig CA, Schnitzler GR, Kingston RE, Schreiber SL. Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex. Nature 1998; 395:917-921.
5. Wade PA, Gegonne A, Jones PL, Ballestar E, Aubry F, Wolffe AP. Mi-2 complex couples DNA methylation to chromatin remodelling and histone deacetylation. Nat Genet 1999; 23:62-66.
6. Xue Y, Wong J, Moreno GT, Young MK, Cote J, Wang W. NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Mol Cell 1998; 2:851-861.
7. Zhang Y, LeRoy G, Seelig HP, Lane WS, Reinberg D. The dermatomyositis-specific autoantigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities. Cell 1998; 95:279-289.
8. Ahringer J. NuRD and SIN3 histone deacetylase complexes in development. Trends Genet 2000; 16:351-356.
9. McDonel P, Costello I, Hendrich B. Keeping things quiet: roles of NuRD and Sin3 co-repressor complexes during mammalian development. Int J Biochem Cell Biol 2009; 41:108-116.
10. Zhang Y, Iratni R, Erdjument-Bromage H, Tempst P, Reinberg D. Histone deacetylases and SAP18, a novel polypeptide, are components of a human Sin3 complex. Cell 1997; 89:357-364.
11. Knoepfler PS, Eisenman RN. Sin meets NuRD and other tails of repression. Cell 1999; 99:447-450.
12. Feng Q, Zhang Y. The NuRD complex: linking histone modification to nucleosome remodeling. Curr Top Microbiol Immunol 2003; 274:269-290.
13. Feng Q, Zhang Y. The MeCP1 complex represses transcription through preferential binding, remodeling, and deacetylating methylated nucleosomes. Genes Dev 2001; 15:827-832.
14. Hendrich B, Bird A. Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol Cell Biol 1998; 18:6538-6547.
15. Le Guezennec X, Vermeulen M, Brinkman AB, Hoeijmakers WA, Cohen A, Lasonder E, Stunnenberg HG. MBD2/NuRD and MBD3/NuRD, two distinct complexes with different biochemical and functional properties. Mol Cell Biol 2006; 26:843-851.
16. Manavathi B, Kumar R. Metastasis tumor antigens, an emerging family of multifaceted master coregulators. J Biol Chem 2007; 282:1529-1533.
17. Kumar R, Wang RA, Bagheri-Yarmand R. Emerging roles of MTA family members in human cancers. Semin Oncol 2003; 30:30-37.
18. Fujita N, Jaye DL, Kajita M, Geigerman C, Moreno CS, Wade PA. MTA3, a Mi-2/NuRD complex subunit, regulates an invasive growth pathway in breast cancer. Cell 2003; 113:207-219.
19. Toh Y, Oki E, Oda S, Tokunaga E, Ohno S, Maehara Y, Nicolson GL, Sugimachi K. Overexpression of the MTA1 gene in gastrointestinal carcinomas: correlation with invasion and metastasis. Int J Cancer 1997; 74:459-463.
20. Zhang H, Singh RR, Talukder AH, Kumar R. Metastatic tumor antigen 3 is a direct corepressor of the Wnt4 pathway. Genes Dev 2006; 20:2943-2948.
21. Lu X, Kovalev GI, Chang H, Kallin E, Knudsen G, Xia L, Mishra N, Ruiz P, Li E, Su L, Zhang Y. Inactivation of NuRD component Mta2 causes abnormal T cell activation and lupus-like autoimmune disease in mice. J Biol Chem 2008; 283:13825-13833.
22. Bowen NJ, Fujita N, Kajita M, Wade PA. Mi-2/NuRD: multiple complexes for many purposes. Biochim Biophys Acta 2004; 1677:52-57.
23. Fujita N, Kajita M, Taysavang P, Wade PA. Hormonal regulation of metastasis-associated protein 3 transcription in breast cancer cells. Mol Endocrinol 2004; 18:2937-2949.
24. Wang Y, Zhang H, Chen Y, Sun Y, Yang F, Yu W, Liang J, Sun L, Yang X, Shi L, Li R, Li Y, et al. LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer. Cell 2009; 138:660-672.
25. Yao YL, Yang WM. The metastasis-associated proteins 1 and 2 form distinct protein complexes with histone deacetylase activity. J Biol Chem 2003; 278:42560-42568.
26. Ideraabdullah FY, Vigneau S, Bartolomei MS. Genomic imprinting mechanisms in mammals. Mutat Res 2008; 647:77-85.
27. Verona RI, Mann MR, Bartolomei MS. Genomic imprinting: intricacies of epigenetic regulation in clusters. Annu Rev Cell Dev Biol 2003; 19:237-259.
28. Bartolomei MS. Genomic imprinting: employing and avoiding epigenetic processes. Genes Dev 2009; 23:2124-2133.
29. Ma P, Schultz RM. Histone deacetylase 1 (HDAC1) regulates histone acetylation, development, and gene expression in preimplantation mouse embryos. Dev Biol 2008; 319:110-120.
30. Greciano PG, Goday C. Methylation of histone H3 at Lys4 differs between paternal and maternal chromosomes in Sciara ocellaris germline development. J Cell Sci 2006; 119:4667-4677.
31. Li E, Beard C, Jaenisch R. Role for DNA methylation in genomic imprinting. Nature 1993; 366:362-365.
32. Yamasaki-Ishizaki Y, Kayashima T, Mapendano CK, Soejima H, Ohta T, Masuzaki H, Kinoshita A, Urano T, Yoshiura K, Matsumoto N, Ishimaru T, Mukai T, et al. Role of DNA methylation and histone H3 lysine 27 methylation in tissue-specific imprinting of mouse Grb10. Mol Cell Biol 2007; 27:732-742.
33. Reese KJ, Lin S, Verona RI, Schultz RM, Bartolomei MS. Maintenance of paternal methylation and repression of the imprinted H19 gene requires MBD3. PLoS Genet 2007; 3:e137.
34. Temeles GL, Ram PT, Rothstein JL, Schultz RM. Expression patterns of novel genes during mouse preimplantation embryogenesis. Mol Reprod Dev 1994; 37:121-129.
35. Mann MR, Chung YG, Nolen LD, Verona RI, Latham KE, Bartolomei MS. Disruption of imprinted gene methylation and expression in cloned preimplantation stage mouse embryos. Biol Reprod 2003; 69:902-914.
36. Schultz RM, Montgomery RR, Belanoff JR. Regulation of mouse oocyte meiotic maturation: implication of a decrease in oocyte cAMP and protein dephosphorylation in commitment to resume meiosis. Dev Biol 1983; 97: 264-273.
37. Whitten WK. Nutrient requirements for the culture of preimplantation mouse embryo in vitro. Adv Biosci 1971; 6:129-139.
38. Chatot CL, Ziomek CA, Bavister BD, Lewis JL, Torres I. An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro. J Reprod Fertil 1989; 86:679-688.
39. Ho Y, Wigglesworth K, Eppig JE, Schultz RM. Preimplantation development of mouse embryos in KSOM: augmentation by amino acids and analysis of gene expression. Mol Reprod Dev 1995; 41:232-238.
40. Stein P, Svoboda P, Anger M, Schultz RM. RNAi: mammalian oocytes do it without RNA-dependent RNA polymerase. RNA 2003; 9:187-192.
41. Mann MR, Lee SS, Doherty AS, Verona RI, Nolen LD, Schultz RM, Bartolomei MS. Selective loss of imprinting in the placenta following preimplantation development in culture. Development 2004; 131:3727-3735.
42. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680-685.
43. Tremblay KD, Duran KL, Bartolomei MS. A 5′ 2-kilobase-pair region of the imprinted mouse H19 gene exhibits exclusive paternal methylation throughout development. Mol Cell Biol 1997; 17:4322-4329.
44. Market-Velker BA, Zhang L, Magri LS, Bonvissuto AC, Mann MR. Dual effects of superovulation: loss of maternal and paternal imprinted methylation in a dose-dependent manner. Hum Mol Genet 2010; 19:36-51.
45. Rohde C, Zhang Y, Jurkowski TP, Stamerjohanns H, Reinhardt R, Jeltsch A. Bisulfite sequencing Data Presentation and Compilation (BDPC) web server - a useful tool for DNA methylation analysis. Nucleic Acids Res 2008; 36:e34.
46. Schultz RM. Regulation of zygotic gene activation in the mouse. BioEssays 1993; 15:531-538.
47. Pan H, O'Brien MJ, Wigglesworth K, Eppig JJ, Schultz RM. Transcript profiling during mouse oocyte development and the effect of gonadotropin priming and development in vitro. Dev Biol 2005; 286:493-506.
48. Liang J, Wan M, Zhang Y, Gu P, Xin H, Jung SY, Qin J, Wong J, Cooney AJ, Liu D, Songyang Z. Nanog and Oct4 associate with unique transcriptional repression complexes in embryonic stem cells. Nat Cell Biol 2008; 10:731-739.
49. Kim J, Kim JD. In vivo YY1 knockdown effects on genomic imprinting. Hum Mol Genet 2008; 17:391-401.
50. Kim J, Kollhoff A, Bergmann A, Stubbs L. Methylation-sensitive binding of transcription factor YY1 to an insulator sequence within the paternally expressed imprinted gene, Peg3. Hum Mol Genet 2003; 12:233-245.
51. Kim JD, Hinz AK, Bergmann A, Huang JM, Ovcharenko I, Stubbs L, Kim J. Identification of clustered YY1 binding sites in imprinting control regions. Genome Res 2006; 16:901-911.
52. Kim JD, Yu S, Choo JH, Kim J. Two evolutionarily conserved sequence elements for Peg3/Usp29 transcription. BMC Mol Biol 2008; 9:108.
53. Zhang Y, Ng HH, Erdjument-Bromage H, Tempst P, Bird A, Reinberg D. Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation. Genes Dev 1999; 13:1924-1935.
54. Brunmeir R, Lagger S, Seiser C. Histone deacetylase HDAC1/HDAC2- controlled embryonic development and cell differentiation. Int J Dev Biol 2009; 53:275-289.
55. Kaji K, Caballero IM, MacLeod R, Nichols J, Wilson VA, Hendrich B. The NuRD component Mbd3 is required for pluripotency of embryonic stem cells. Nat Cell Biol 2006; 8:285-292.
56. Szeto IY, Barton SC, Keverne EB, Surani AM. Analysis of imprinted murine Peg3 locus in transgenic mice. Mamm Genome 2004; 15:284-295.