Dual histone H3 methylation marks at lysines 9 and 27 required for interaction with CHROMOMENTHYLASE3

EMBO Journal

Volumn 23, Issue 21, 2004, Pages 4286-4296

  Lindroth, Anders M ^a,g   Shultis, David ^b   Jasencakova, Zuzana ^c,h   Fuchs, Jörg ^c   Johnson, Lianna ^a   Schubert, Daniel ^d   Patnaik, Debasis ^e   Pradhan, Sriharsa ^e   Goodrich, Justin ^d   Schubert, Ingo ^c   Jenuwein, Thomas ^f   Khorasanizadeh, Sepideh ^b   Jacobsen, Steven E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^c LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

^e NEW ENGLAND BIOLABS   (United States)

^f RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^g Program on Infrastructure Policy   (United States)

^h INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

Author keywords

Chromodomain; DNA methylation; Histone code; Histone methylation

Indexed keywords

CHROMOMETHYLASE 3; DNA METHYLTRANSFERASE; HISTONE H3; LYSINE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARABIDOPSIS; ARTICLE; CHROMODOMAIN; CMT3 GENE; DNA METHYLATION; ENHANCER REGION; EPIGENETICS; GENE; GENE SILENCING; H3K27 GENE; H3K9 GENE; HETEROCHROMATIN; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; KYP GENE; METHYLATION; MODEL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; LYSINE; METHYLATION; METHYLTRANSFERASES; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; SEQUENCE ALIGNMENT; SITE-SPECIFIC DNA METHYLTRANSFERASE (CYTOSINE-SPECIFIC);

ARABIDOPSIS; EMBRYOPHYTA;

EID: 9144260620     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600428     Document Type: Article

References (67)

1. Aufsatz W, Mette MF, van der Winden J, Matzke AJ, Matzke M (2002) RNA-directed DNA methylation in Arabidopsis. Proc Natl Acad Sci USA 99: 16499-16506
2. Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, Allshire RC, Kouzarides T (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410: 120-124
3. Bartee L, Malagnac F, Bender J (2001) Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene. Genes Dev 15: 1753-1758
4. Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427: 164-167
5. Callebaut I, Courvalin JC, Mornon JP (1999) The BAH (bromo-adjacent homology) domain: a link between DNA methylation, replication and transcriptional regulation. FEBS Lett 446: 189-193
6. Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298: 1039-1043
7. Cao R, Zhang Y (2004) The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr Opin Genet Dev 14: 155-164
8. Cao X, Jacobsen SE (2002) Role of the Arabidopsis DRM methyl-transferases in de novo DNA methylation and gene silencing. Curr Biol 12: 1138-1144
9. Chan SW, Zilberman D, Xie Z, Johansen LK, Carrington JC, Jacobsen SE (2004) RNA silencing genes control de novo DNA methylation. Science 303: 1336
10. Chanvivattana Y, Bishopp A, Schubert D, Stock C, Moon YH, Sung ZR, Goodrich J (2004) Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development, (in press)
11. Czermin B, Melfi R, McCabe D, Seitz V, Imhof A, Pirrotta V (2002) Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111: 185-196
12. Dutnall RN (2003) Cracking the histone code: one, two, three methyls, you're out!. Mol Cell 12: 3-4
13. Elgin SC, Grewal SI (2003) Heterochromatin: silence is golden. Curr Biol 13: R895-R898
14. Fischle W, Wang Y, Allis CD (2003a) Histone and chromatin cross-talk. Curr Opin Cell Biol 15: 172-183
15. Fischle W, Wang Y, Jacobs SA, Kim Y, Allis CD, Khorasanizadeh S (2003b) Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev 17: 1870-1881
16. Freitag M, Hickey PC, Khlafallah TK, Read ND, Selker EU (2004) HP1 is essential for DNA methylation in neurospora. Mol Cell 13: 427-434
17. Gaudin V, Libault M, Pouteau S, Juul T, Zhao G, Lefebvre D, Grandjean O (2001) Mutations in LIKE HETEROCHROMATIN PROTEIN 1 affect flowering time and plant architecture in Arabidopsis. Development 128: 4847-4858
18. Goodrich J, Puangsomlee P, Martin M, Long D, Meyerowitz EM, Coupland G (1997) A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386: 44-51
19. Grewal SIS, Elgin SCR (2002) Heterochromatin: new possibilities for the inheritance of structure. Curr Opin Genet Dev 12: 178-187
20. Hall IM, Shankaranarayana GD, Noma K, Ayoub N, Cohen A, Grewal SI (2002) Establishment and maintenance of a heterochromatin domain. Science 297: 2232-2237
21. Henikoff S, Comai L (1998) A DNA methyltransferase homolog with a chromodomain exists in multiple polymorphic forms in Arabidopsis. Genetics 149: 307-318
22. Hsieh TF, Hakim O, Ohad N, Fischer RL (2003) From flour to flower: how Polycomb group proteins influence multiple aspects of plant development. Trends Plant Sci 8: 439-445
23. Jackson JP, Johnson L, Jasencakova Z, Zhang X, PerezBurgos L, Singh PB, Cheng X, Schubert I, Jenuwein T, Jacobsen SE (2004) Dimethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in Arabidopsis thaliana. Chromosoma 112: 308-315
24. Jackson JP, Lindroth AM, Cao X, Jacobsen SE (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416: 556-560
25. Jacobs SA, Fischle W, Khorasanizadeh S (2004) Assays for the determination of structure and dynamics of the interaction of the chromodomain with histone peptides. Methods Enzymol 376: 131-148
26. Jacobs SA, Khorasanizadeh S (2002) Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail. Science 295: 2080-2083
27. Jacobs SA, Taverna SD, Zhang Y, Briggs SD, Li J, Eissenberg JC, Allis CD, Khorasanizadeh S (2001) Specificity of the HP1 chromo domain for the methylated N-terminus of histone H3. EMBO J 20: 5232-5241
28. Jasencakova Z, Soppe WJ, Meister A, Gernand D, Turner BM, Schubert I (2003) Histone modifications in Arabidopsis-high methylation of H3 lysine 9 is dispensable for constitutive heterochromatin. Plant J 33: 471-480
29. Johnson L, Cao X, Jacobsen S (2002) Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Curr Biol 12: 1360-1367
30. Jones L, Ratcliff F, Baulcombe DC (2001) RNA-directed transcriptional gene silencing in plants can be inherited independently of the RNA trigger and requires Met1 for maintenance. Curr Biol 11: 747-757
31. Kinoshita T, Harada JJ, Goldberg RB, Fischer RL (2001) Polycomb repression of flowering during early plant development. Proc Natl Acad Sci USA 98: 14156-14161
32. Kinoshita T, Yadegari R, Harada JJ, Goldberg RB, Fischer RL (1999) Imprinting of the MEDEA polycomb gene in the Arabidopsis endosperm. Plant Cell 11: 1945-1952
33. Kotake T, Takada S, Nakahigashi K, Onto M, Goto K (2003) Arabidopsis TERMINAL FLOWER 2 gene encodes a heterochromatin protein 1 homolog and represses both FLOWERING LOCUS T to regulate flowering time and several floral homeotic genes. Plant Cell Physiol 44: 555-564
34. Kuzmichev A, Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D (2002) Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev 16: 2893-2905
35. Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410: 116-120
36. Larsson AS, Landberg K, Meeks-Wagner DR (1998) The TERMINAL FLOWER2 (TFL2) gene controls the reproductive transition and meristem identity in Arabidopsis thaliana. Genetics 149: 597-605
37. Lehnertz B, Ueda Y, Derijck AA, Braunschweig U, Perez-Burgos L, Kubicek S, Chen T, Li E, Jenuwein T, Peters AH (2003) Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr Biol 13: 1192-1200
38. Lindroth AM, Cao X, Jackson JP, Zilberman D, McCallum CM, Henikoff S, Jacobsen SE (2001) Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292: 2077-2080
39. Malagnac F, Bartee L, Bender J (2002) An Arabidopsis SET domain protein required for maintenance but not establishment of DNA methylation. EMBO J 21: 6842-6852
40. Melquist S, Bender J (2003) Transcription from an upstream promoter controls methylation signaling from an inverted repeat of endogenous genes in Arabidopsis. Genes Dev 17: 2036-2047
41. Min J, Zhang Y, Xu RM (2003) Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Genes Dev 17: 1823-1828
42. Moon YH, Chen L, Pan RL, Chang HS, Zhu T, Maffeo DM, Sung ZR (2003) EMF genes maintain vegetative development by repressing the flower program in Arabidopsis. Plant Cell 15: 681-693
43. Muller J, Hart CM, Francis NJ, Vargas ML, Sengupta A, Wild B, Miller EL, O'Connor MB, Kingston RE, Simon JA (2002) Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111: 197-208
44. Nakayama J, Rice JC, Strahl BD, Allis CD, Grewal SI (2001) Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292: 110-113
45. Nielsen PR, Nietlispach D, Mott HR, Callaghan J, Bannister A, Kouzarides T, Murzin AG, Murzina NV, Laue ED (2002) Structure of the HP1 chromodomain bound to histone H3 methylated at lysine 9. Nature 416: 103-107
46. Okamoto I, Otte AP, Allis CD, Reinberg D, Heard E (2004) Epigenetic dynamics of imprinted X inactivation during early mouse development. Science 303: 644-649
47. Papa CM, Springer NM, Muszynski MG, Meeley R, Kaeppler SM (2001) Maize chromomethylase Zea methyltransferase2 is required for CpNpG methylation. Plant Cell 13: 1919-1928
48. Perez-Burgos L, Peters AH, Opravil S, Kauer M, Mechtler K, Jenuwein T (2004) Generation and characterization of methyl-lysine histone antibodies. Methods Enzymol 376: 234-254
49. Peters AH, Kubicek S, Mechtler K, O'Sullivan RJ, Derijck AA, Perez-Burgos L, Kohlmaier A, Opravil S, Tachibana M, Shinkai Y, Martens JH, Jenuwein T (2003) Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol Cell 12: 1577-1589
50. Plath K, Fang J, Mlynarczyk-Evans SK, Cao R, Worringer KA, Wang H, de la Cruz CC, Otte AP, Panning B, Zhang Y (2003) Role of histone H3 lysine 27 methylation in X inactivation. Science 300: 131-135
51. Reyes JC, Grossniklaus U (2003) Diverse functions of Polycomb group proteins during plant development. Semin Cell Dev Biol 14: 77-84
52. Rice JC, Briggs SD, Ueberheide B, Barber CM, Shabanowitz J, Hunt DF, Shinkai Y, Allis CD (2003) Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol Cell 12: 1591-1598
53. Rougeulle C, Chaumeil J, Sarma K, Allis CD, Reinberg D, Avner P, Heard E (2004) Differential histone H3 Lys-9 and Lys-27 methylation profiles on the X chromosome. Mol Cell Biol 24: 5475-5484
54. Schotta G, Ebert A, Krauss V, Fischer A, Hoffmann J, Rea S, Jenuwein T, Dorn R, Reuter G (2002) Central role of Drosophila SU (VAR) 3-9 in histone H3-K9 methylation and heterochromatic gene silencing. EMBO J 21: 1121-1131
55. Soppe WJ, Jacobsen SE, Alonso-Blanco C, Jackson JP, Kakutani T, Koornneef M, Peeters AJ (2000) The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene. Mol Cell 6: 791-802
56. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403: 41-45
57. Sung S, Amasino RM (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427: 159-164
58. Tachibana M, Sugimoto K, Fukushima T, Shinkai Y (2001) Set domain-containing protein, G9a, is a novel lysine-preferring mammalian histone methyltransferase with hyperactivity and specific selectivity to lysines 9 and 27 of histone H3. J Biol Chem 276: 25309-25317
59. Tachibana M, Sugimoto K, Nozaki M, Ueda J, Ohta T, Ohki M, Fukuda M, Takeda N, Niida H, Kato H, Shinkai Y (2002) G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev 16: 1779-1791
60. Takada S, Goto K (2003) Terminal flower2, an Arabidopsis homolog of heterochromatin protein1, counteracts the activation of flowering locus T by constans in the vascular tissues of leaves to regulate flowering time. Plant Cell 15: 2856-2865
61. Tamaru H, Selker EU (2001) A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414: 277-283
62. Tamaru H, Zhang X, McMillen D, Singh PB, Nakayama J, Grewal SI, Allis CD, Cheng X, Selker EU (2003) Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa. Nat Genet 34: 75-79
63. Tariq M, Paszkowski J (2004) DNA and histone methylation in plants. Trends Genet 20: 244-251
64. Thiru A, Nietlispach D, Mott HR, Okuwaki M, Lyon D, Nielsen PR, Hirshberg M, Verreault A, Murzina NV, Laue ED (2004) Structural basis of HP1/PXVXL motif peptide interactions and HP1 localisation to heterochromatin. EMBO J 23: 489-499
65. Turner BM (2000) Histone acetylation and an epigenetic code. BioEssays 22: 836-845
66. Yoshida N, Yanai Y, Chen L, Kato Y, Hiratsuka J, Miwa T, Sung ZR, Takahashi S (2001) EMBRYONIC FLOWER2, a novel polycomb group protein homolog, mediates shoot development and flowering in Arabidopsis. Plant Cell 13: 2471-2481
67. Zilberman D, Cao X, Jacobsen SE (2003) ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299: 716-719