Arabidopsis MBD proteins show different binding specificities and nuclear localization

Plant Molecular Biology

Volumn 53, Issue 5, 2003, Pages 755-771

  Scebba, Francesca ^a   Bernacchia, Giovanni ^b   De Bastiani, Morena ^b   Evangelista, Monica ^a   Cantoni, Rita Maria ^c   Cella, Rino ^c   Locci, Maria Tereasa ^d   Pitto, Letizia ^a  

^a INSTITUTE OF CLINICAL PHYSIOLOGY   (Italy)

^b UNIVERSITY OF FERRARA   (Italy)

^c UNIVERSITY OF PAVIA   (Italy)

^d UNIVERSITY OF PISA   (Italy)

Author keywords

Arabidopsis thaliana; DNA binding proteins; GFP tagged proteins; Symmetric and asymmetric methylation

Indexed keywords

ALKYLATION; CROPS; DATA REDUCTION; DNA; ENZYMES; ESCHERICHIA COLI; MOLECULAR BIOLOGY;

HOMOLOGY; METHYLATION;

PLANTS (BOTANY);

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA; ESCHERICHIA COLI; MAMMALIA; VERTEBRATA; ZEA MAYS;

EID: 1942506630     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:PLAN.0000019118.56822.a9     Document Type: Article

References (73)

1. Ballestar, E. and Wolffe, A.P. 2001. Methyl-CpG-binding proteins. Targeting specific gene repression. Eur. J. Biochem. 268: 1-6.
2. Ballestar, E., Pile, L.A., Wassarman, D.A., Wolffe, A.P. and Wade, P.A. 2001. A Drosophila MBD family member is a transcriptional corepressor associated with specific genes. Eur. J. Biochem. 268: 5397-406.
3. Bartels, D. and Thompson, R.D. 1993. The characterization of cDNA clones coding for wheat storage proteins. Nucl. Acids Res 11: 2961-2978.
4. Baylin, S.B., Esteller, M., Rountree, M.R., Bachman, K.E., Schuebel, K. and Herman, J.G. 2001. Aberrant patterns of DNA methylation, chromatin formation and gene expression in cancer. Hum. Mol. Genet. 10: 687-692.
5. Bellacosa, A., Cicchillitti, L., Schepis, F., Riccio, A., Yeung, A.T., Matsumoto, Y., Golemis, E.A., Genuardi, M. and Neri, G. 1999. MED1, a novel human methyl-CpG-binding endonuclease, interacts with DNA mismatch repair protein MLH1. Proc. Natl. Acad. Sci. USA 96: 3969-3974.
6. Ben-Hattar, J., Beard, P. and Jiricny, J. 1989. Cytosine methylation in CTF and Sp1 recognition sites of an HSV tk promoter: effects on transcription in vivo and on factor binding in vitro. Nucl. Acids Res 17: 10179-10190.
7. Berg, A., Meza, T.J., Mahic, M., Thorstensen, T., Kristiansen, K. and Aalen, R.B. 2003. Ten members of the Arabidopsis gene family encoding methyl-CpG-binding domain proteins are transcriptionally active and at least one, AtMBD11, is crucial for normal development. Nucl. Acids Res 31: 5291-5304.
8. Bird, A.P. and Wolffe, A.P. 1999. Methylation-induced repression-belts, braces, and chromatin. Cell 99: 451-454.
9. Campanero, M.R., Armstrong, M.I. and Flemington, E.K. 2000. CpG methylation as a mechanism for the regulation of E2F activity. Proc. Natl. Acad. Sci. USA 97: 6481-6486.
10. Chen, Z.J. and Pikaard, C.S. 1997. Epigenetic silencing of RNA polymerase I transcription: a role for DNA methylation and histone modification in nucleolar dominance. Genes Dev. 11: 2124-2136.
11. Chomczynski, P. and Sacchi, N. 1987. Single step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162: 156-159.
12. Di Fiore, B., Palena, A., Felsani, A., Palitti, F., Caruso, M. and Lavia, P. 1999. Cytosine methylation trasforms an E2F site in the retinoblastoma gene promoter into a binding site for the general repressor methylcytosine-binding protein 2 (MeCP2). Nucl. Acids Res 27: 2852-2859.
13. Dieguez, M.J., Bellotto, M., Afsar, K., Mittelsten Scheid, O. and Paszkowski, J. 1997. Methylation of cytosines in nonconventional methylation acceptor sites can contribute to reduced gene expression. Mol. Gen. Genet. 253: 581-588.
14. Doyle, J.J. and Doyle, J.L. 1990. Isolation of plant DNA from fresh tissue. Focus 12: 13-15.
15. Ehrlich, K. 1993. Characterization of DBPm, a plant protein that binds to DNA containing 5-methylcytosine. Biochim. Biophys. Acta 1172: 108-116.
16. Fraga, M.F., Ballestar, E., Montoya, G., Taysavang, P., Wade, P.A. and Esteller, M. 2003. The affinity of different MBD proteins for a specific methylated locus depends on their intrinsic binding properties. Nucl. Acids Res 31: 1765-1774.
17. Fujita, N., Takebayashi, S., Okomura, K., Kudo, S., Chiba, T., Saya, H. and Nakao, M. 1999. Methylation-mediated transcriptional silencing in euchromatin by methyl-CpG binding protein MBD1 isoforms. Mol. Cell Biol. 19: 6415-6426.
18. Fuks, F., Hurd, P.J., Wolf, D., Nan, X., Bird, A.P. and Kouzarides, T. 2003. The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J. Biol. Chem. 278: 4035-4040.
19. Gendrel, A.V., Lippman, Z., Yordan, C., Colot, V. and Martienssen, R.A. 2002. Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science 297: 1871-1873.
20. Grafstrom, R.H., Yuan, R. and Hamilton, D.L. 1985. The characteristics of DNA methylation in an in vitro DNA synthesizing system from mouse fibroblasts. Nucl. Acids Res 13: 2827-2842.
21. Gruenbaum, Y., Naveh-Many, T., Cedar, H. and Razin, A. 1981. Sequence specificity of methylation in higher plant DNA. Nature 292: 860-862.
22. Haseloff, J. and Amos, B. 1995. GFP in plants. Trends Genet 11: 328-329.
23. Hendrich, B. and Bird, A. 1998. Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol. Cell Biol. 18: 6538-6547.
24. Hendrich, B., Guy, J., Ramsahoye, B., Wilson, V.A. and Bird, A. 2001. Closely related proteins MBD2 and MBD3 play distinctive but interacting roles in mouse development. Genes Dev. 15:710-723.
25. Hendrich, B. and Tweedie, S. 2003. The methyl-CpG binding domain and the evolving role of DNA methylation in animals. Trends Genet. 19: 269-277.
26. Holler, M., Westin, G., Jiricny, J. and Schaffner, W. 1988. Sp1 transcription factor binds DNA and activates transcription even when the binding site is CpG methylated. Genes Dev. 2: 1127-1135.
27. Inamdar, N.M., Ehrlich, K.C. and Ehrlich, M. 1991. CpG methylation inhibits binding of several sequence-specific DNA-binding proteins from pea, wheat, soybean and cauliflower. Plant Mol. Biol. 17: 111-123.
28. Jacobsen S.E. and Meyerowitz, E.M. 1997. Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science 277: 1100-1103.
29. Jeddeloh, J.A., Stokes, T.L. and Richards, E.J. 1999. Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nature Genet. 22: 94-97.
30. Jenuwein, T. and Allis, C.D. 2001. Translating the histone code. Science 293: 1074-1080.
31. Kaludov, N.K. and Wolffe, A.P. 2000. MeCP2 driven transcriptional repression in vitro: selectivity for methylated DNA, action at a distance and contacts with the basal transcription machinery. Nucl. Acids Res. 28: 1921-1928.
32. Kang, H.G., Fang, Y. and Singh, K.B. 1999. A glucocorticoid-inducible transcription system causes severe growth defects in Arabidopsis and induces defense-related genes. Plant J. 20: 127-133.
33. Levine, A., Cantoni, G.L. and Razin, A. 1991. Inhibition of promoter activity by methylation: Possible involvement of protein mediators. Proc. Natl. Acad. Sci. USA 88: 6515-6518.
34. Lewis, J.D., Meehan, R.R., Henzel, W.J., Maurer-Fogy, I., Jeppesen, P., Klein, F. and Bird, A. 1992. Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA. Cell 69: 905-914.
35. Lindroth, A.M., Cao, X., Jackson, J.P., Zilberman, D., McCallum, C.M., Henikoff, S. and Jacobsen, S.E. 2001. Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292: 2077-2080.
36. Luff, B., Pawlowski, L. and Bender, J. 1999. An inverted repeat triggers cytosine methylation of identical sequences in Arabidopsis. Mol. Cell 3: 505-511.
37. Mariconti, L., Pellegrini, B., Cantoni, R., Stevens, R., Bergounioux, C., Cella, R. and Albani, D. 2002. The E2F Family of transcription factors from Arabidopsis thaliana. J. Biol. Chem. 277: 9911-9919.
38. Meehan, R.R., Lewi, J.D., McKay, S., Kleiner, E.L. and Bird, A.P. 1989. Identification of a mammalian protein that binds specifically to DNA containing methylated CpGs. Cell 58: 499-507.
39. Nan, X., Meehan, R.R. and Bird, A. 1993. Dissection of the methyl-CpG binding domain from the chromosomal protein MeCP2. Nucl. Acids Res. 21: 4886-4892.
40. Nan, X., Tate, P., Li, E. and Bird, A. 1996. DNA methylation specify chromosomal localization of MeCP2. Mol. Cell Biol. 16: 414-421.
41. Nyce, J., Liu, L. and Jones, P.A. 1986. Variable effects of DNA-synthesis inhibitors upon DNA methylation in mammalian cells. Nucl. Acids Res. 14: 4353-4367.
42. Oakeley, E.J. and Jost, J.P. 1996. Non-symmetrical cytosine methylation in tobacco pollen DNA. Plant Mol. Biol. 31: 927-930.
43. Ohki, I., Shimotake, N., Fujita, N., Jee, J., Ikegam, T., Nakao, M. and Shirakawa, M. 2001. Solution structure of the methyl-CpG binding domain of human MBD1 in complex with methylated DNA. Cell 105: 487-497.
44. Papa, C.M., Springer, N.M., Muszynski, M.G., Meeley, R. and Kaeppler, S.M. 2001. Maize chromomethylase Zea methyltransferase2 is required for CpNpG methylation. Plant Cell 13: 1919-1928.
45. Pikaard, C.S. and Lawrence, R.J. 2002. Uniting the paths to gene silencing. Nature Genet. 32: 340-341.
46. Pitto, L., Cernilogar, F., Evangelista, M., Miarelli, C., Lombardi, L. and Rocchi P. 2000. Characterization of carrot nuclear proteins that exhibit specific binding affinity towards conventional and non-conventional DNA methylation. Plant Mol. Biol. 44: 659-673.
47. Podestà, A., Castiglione, M.R., Avanzi, S. and Montagnoli, G. 1993. Molecular geometry of antigen binding by a monoclonal antibody against 5-methylcytidine. Int. J. Biochem. 25: 929-933.
48. Pradhan, S., Urwin, N.A.R., Jenkins, G.I. and Adams, R.L.P. 1999. Effect of CWG methylation on expression of plant genes. Biochem. J. 341:473-476.
49. Ramsahoye, B.H., Biniszkiewicz, D., Lyko, F., Clark, V., Bird, A.P. and Jaenisch, R. 2000. Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. Proc. Natl. Acad. Sci. USA 97: 5237-5242.
50. Razin, A. and Kafri, T. 1994. DNA methylation from embryo to adult. Prog. Nucl. Acid Res. Mol. Biol. 48: 53-81.
51. Rein, T., DePamphilis, M.L. and Zorbas, H. 1998. Identifying 5-methylcytosine and related modifications in DNA genomes. Nucl. Acids Res. 26: 2255-2264.
52. Rice, J.C. and Allis, C.D. 2001. Code of silence. Nature 414: 258-261.
53. Riggs, A.D. and Pfeifer, G.P. 1992. X-chromosome inactivation and cell memory. Trends Genet. 8: 169-174.
54. Robertson, K.D. 2001. DNA methylation, methyltransferases, and cancer. Oncogene 20: 3139-3155.
55. Robertson, K.D. 2002. DNA methylation and chromatin-unraveling the tangled web. Oncogene 21: 5361-5379.
56. Roloff, T.C., Ropers, H.H. and Nuber, U.A. 2003. Comparative study of methyl-CpG-binding domain proteins. BMC Genomics 4: 1-9.
57. Rossi, V., Motto, M. and Pellegrini, L. 1997. Analysis of the methylation pattern of the maize opaque-2 (O2) promoter and in vitro binding studies indicate that the O2 B-Zip protein and other endosperm factors can bind to methylated target sequences. J. Biol. Chem. 272: 13758-13765.
58. Santoro, R., Li, J., and Grummt, I. 2002. The nucleolar remodelling complex NoRC mediates heterochromatin formation and silencing of ribosomal gene transcription. Nature Genet. 32: 393-396.
59. Sturaro, M. and Viotti, A. 2001. Methylation of the Opaque2 box in zein genes is parent-dependent and affects O2 DNA binding activity in vitro. Plant Mol. Biol. 46: 549-560.
60. Szyroki, A., Ivashikina, N., Dietrich, P., Roelfsema, M.R.G., Ache, P., Reintanz, B., Decken, R., Godde, M., Felle, H., Steinmeyer, R., Palme, K. and Hedrich, H. 2001. KAT1 is not essential for stomatal opening. Proc. Natl. Acad. Sci. USA 98: 2917-2921.
61. ten Lohuis, M., Galliano, H., Heidmann, I. and Meyer, P. 1995. Treatment with propionic and butyric acid enhances expression variegation and promoter methylation in plant transgenes. Biol. Chem. Hoppe-Seyler 376: 311-320.
62. Tian, L. and Chen, Z.J. 2001. Blocking histone deacetylation in Arabidopsis induces pleiotropic effects on plant gene regulation and development. Proc. Natl. Acad. Sci. USA 98: 200-205.
63. von Arnim, A.G., Deng, X.W. and Stacey, M.G. 1998. Cloning vectors for the expression of green fluorescent protein fusion proteins in transgenic plants. Gene 221: 35-43.
64. Wade, P.A. 2001a. Methyl CpG binding proteins: coupling chromatin architecture to gene regulation. Oncogene 20: 3166-3173.
65. Wade, P.A. 2001b. Methyl CpG-binding proteins and transcriptional repression. Bioessays 23: 1131-1137.
66. Wade, P.A., Gegonne, A., Jones, P.L., Ballestar, E., Aubry, F. and Wolffe, A.P. 1999. Mi-2 complex couples DNA methylation to chromatin remodelling and histone deacetylation. Nature Genet. 23: 62-66.
67. Wade, P.A. and Wolffe, A.P. 2001. ReCoGnizing methylated DNA. Nature Struct. Biol. 8: 575-577.
68. Weih, F., Nitsch, D., Reik, A., Schütz, G. and Becker, P.B. 1991. Analysis of CpG methylation and genomic footprinting at the tyrosine aminotransferase gene: DNA methylation alone is not sufficient to prevent protein binding in vivo. EMBO J. 10: 2559-2567.
69. Zemach, A. and Grafi, G. 2003. Characterization of Arabidopsis thaliana methyl-CpG-binding domain (MBD) proteins. Plant J. 34: 565-572.
70. Zhang, D.L., Ehrlich, K.C., Supakar, P.C. and Ehrlich, M. 1989. A plant DNA-binding protein that recognizes 5-methylcytosine residues. Mol. Cell Biol. 9: 1351-1356.
71. Zhang, Y., Ng, H.H., Erdjument-Bromage, H., Tempst, P., Bird, A. and Reinberg, D. 1999. Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation. Genes Dev. 13: 1924-1935.
72. Zhang, Z. and Gurr, S.J. 2000. Walking into the unknown: a 'step down' PCR-based technique leading to the direct sequence analysis of flanking genomic DNA. Gene 253: 145-150.
73. Zhou, Y., Magill, C.W., Magill, J.M. and Newton, R.J. 1998. An apparent case of nonsymmetrical and sustained strand-specific hemimethylation in the Dc8 gene of carrot. Genome 41: 23-33.