Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin

Current Biology

Volumn 13, Issue 14, 2003, Pages 1192-1200

  Lehnertz, Bernhard ^a,c   Ueda, Yoshihide ^b   Derijck, Alwin A H A ^a,d   Braunschweig, Ulrich ^a   Perez Burgos, Laura ^a   Kubicek, Stefan ^a   Chen, Taiping ^b   Li, En ^b   Jenuwein, Thomas ^a   Peters, Antoine H F M ^a  

^a RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS THALIANA; MAMMALIA; NEUROSPORA CRASSA;

EID: 10744230544     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0960-9822(03)00432-9     Document Type: Article

References (41)

1. Bird, A. (2002). DNA methylation patterns and epigenetic memory. Genes Dev. 16, 6-21.
2. Robertson, K.D., and Wollfe, A.P. (2000). DNA methylation in health and disease. Nat. Rev. Genet. 1, 11-19.
3. Okano, M., Bell, D.W., Haber, D.A., and Li, E. (1999). DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247-257.
4. Li, E., Bestor, T.H., and Jaenisch, R. (1992). Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915-926.
5. Lei, H., Oh, S.P., Okano, M., Juttermann, R., Goss, K.A., Jaenisch, R., and Li, E. (1996). De novo DNA cytosine methyltransferase activities in mouse embryonic stem cells. Development 122, 3195-3205.
6. Yoder, J.A., Soman, N.S., Verdine, G.L., and Bestor, T.H. (1997). DNA (cytosine-5)-methyltransferases in mouse cells and tissues. Studies with a mechanism-based probe. J. Mol. Biol. 270, 385-395.
7. Okano, M., Xie, S., and Li, E. (1998). Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat. Genet. 19, 219-220.
8. Jeddeloh, J.A., Stokes, T.L., and Richards, E.J. (1999). Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat. Genet. 22, 94-97.
9. Gibbons, R.J., McDowell, T.L., Raman, S., O'Rourke, D.M., Garrick, D., Ayyub, H., and Higgs, D.R. (2000). Mutations in ATRX, encoding a SWI/SNF-like protein, cause diverse changes in the pattern of DNA methylation. Nat. Genet. 24, 368-371.
10. Dennis, K., Fan, T., Geiman, T., Yan, Q., and Muegge, K. (2001). Lsh, a member of the SNF2 family, is required for genome-wide methylation. Genes Dev. 15, 2940-2944.
11. Gendrel, A.V., Lippman, Z., Yordan, C., Colot, V., and Martienssen, R. (2002). Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science 20, 20.
12. Tamaru, H., and Selker, E.U. (2001). A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414, 277-283.
13. Jackson, J.P., Lindroth, A.M., Cao, X., and Jacobsen, S.E. (2002). Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416, 556-560.
14. 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.
15. Peters, A.H.F.M., O'Carroll, D., Scherthan, H., Mechtler, K., Sauer, S., Schofer, C., Weipoltshammer, K., Pagani, M., Lachner, M., Kohlmaier, A., et al. (2001). Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107, 323-337.
16. Bannister, A.J., Zegerman, P., Partridge, J.F., Miska, E.A., Thomas, J.O., Allshire, R.C., and Kouzarides, T. (2001). Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410, 120-124.
17. Lachner, M., O'Carroll, D., Rea, S., Mechtler, K., and Jenuwein, T. (2001). Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410, 116-120.
18. Nakayama, J., Rice, J.C., Strahl, B.D., Allis, C.D., and Grewal, S.I. (2001). Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292, 110-113.
19. Nan, X., Campoy, F.J., and Bird, A. (1997). MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin. Cell 88, 471-481.
20. Chen, T., Ueda, Y., Xie, S., and Li, E. (2002). A novel Dnmt3a isoform produced from an alternative promoter localizes to euchromatin and its expression correlates with active de novo methylation. J. Biol. Chem. 277, 38746-38754.
21. Bachman, K.E., Rountree, M.R., and Baylin, S.B. (2001). Dnmt3a and Dnmt3b are transcriptional repressors that exhibit unique localization properties to heterochromatin. J. Biol. Chem. 276, 32282-32287.
22. Nan, X., Tate, P., Li, E., and Bird, A. (1996). DNA methylation specifies chromosomal localization of MeCP2. Mol. Cell. Biol. 16, 414-421.
23. Kalitis, P., and Choo, K.H.A. (1997). Centromere DNA of higher eukaryotes. In The Centromere, K.H.A. Choo, ed. (New York: Oxford University Press), pp. 97-142.
24. Vissel, B., and Choo, K.H.A. (1989). Mouse major (gamma) satellite DNA is highly conserved and organized into extremely long tandem arrays: implications for recombination between nonhomologous chromosomes. Genomics 5, 407-414.
25. Volpe, T.A., Kidner, C., Hall, I.M., Teng, G., Grewal, S.I., and Martienssen, R.A. (2002). Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297, 1833-1837.
26. Hall, I.M., Shankaranarayana, G.D., Noma, K., Ayoub, N., Cohen, A., and Grewal, S.I. (2002). Establishment and maintenance of a heterochromatin domain. Science 297, 2232-2237.
27. Partridge, J.F., Scott, K.S., Bannister, A.J., Kouzarides, T., and Allshire, R.C. (2002). cis-acting DNA from fission yeast centre-meres mediates histone H3 methylation and recruitment of silencing factors and cohesin to an ectopic site. Curr. Biol. 12, 1652-1660.
28. Xu, G.L., Bestor, T.H., Bourc'his, D., Hsieh, C.L., Tommerup, N., Bugge, M., Hulten, M., Qu, X., Russo, J.J., and Viegas-Pequignot, E. (1999). Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 402, 187-191.
29. Chuang, L.S., Ian, H.I., Koh, T.W., Ng, H.H., Xu, G., and Li, B.F. (1997). Human DNA-(cytosine-5) methyltransferase-PCNA complex as a target for p21WAF1. Science 277, 1996-2000.
30. Rountree, M.R., Bachman, K.E., and Baylin, S.B. (2000). DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nat. Genet. 5, 269-277.
31. Johnson, L., Cao, X., and Jacobsen, S. (2002). Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Curr. Biol. 12, 1360-1367.
32. Nguyen, C.T., Weisenberger, D.J., Velicescu, M., Gonzales, F.A., Lin, J.C., Liang, G., and Jones, P.A. (2002). Histone H3-lysine 9 methylation is associated with aberrant gene silencing in cancer cells and is rapidly reversed by 5-aza-2′-deoxycytidine. Cancer Res. 62, 6456-6461.
33. Fahrner, J.A., Eguchi, S., Herman, J.G., and Baylin, S.B. (2002). Dependence of histone modifications and gene expression on DNA hypermethylation in cancer. Cancer Res. 62, 7213-7218.
34. Kondo, Y., Shen, L., and Issa, J.P. (2003). Critical role of histone methylation in tumor suppressor gene silencing in colorectal cancer. Mol. Cell. Biol. 23, 206-215.
35. Ahmad, K., and Henikoff, S. (2002). The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol. Cell 9, 1191-1200.
36. Nan, X., Ng, H.H., Johnson, C.A., Laherty, C.D., Turner, B.M., Eisenman, R.N., and Bird, A. (1998). Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393, 386-389.
37. Jones, P.L., Veenstra, G.J., Wade, P.A., Vermaak, D., Kass, S.U., Landsberger, N., Strouboulis, J., and Wolffe, A.P. (1998). Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat. Genet. 19, 187-191.
38. 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. Bioh Chem. 278, 4035-4040.
39. Melcher, M., Schmid, M., Aagaard, L., Selenko, P., Laible, G., and Jenuwein, T. (2000). Structure-function analysis of SUV39H1 reveals a dominant role in heterochromatin organization, chromosome segregation, and mitotic progression. Mol. Cell. Biol. 20, 3728-3741.
40. O'Carroll, D., Scherthan, H., Peters, A.H.F.M., Opravil, S., Haynes, A.R., Laibie, G., Rea, S., Schmid, M., Lebersorger, A., Jerratsch, M., et al. (2000). Isolation and characterization of Suv39h2, a second histone H3 methyltransferase gene that displays testis-specific expression. Mol. Cell. Biol. 20, 9423-9433.
41. Chapman, V., Forrester, L., Sanford, J., Hastie, N., and Rossant, J. (1984). Cell lineage-specific undermethylation of mouse repetitive DNA. Nature 307, 284-286.