Substitutions in the Amino-Terminal tail of Neurospora histone H3 have varied effects on DNA methylation

PLoS Genetics

Volumn 7, Issue 12, 2011, Pages

  Adhvaryu, Keyur K ^a,b   Berge, Emanuela ^a,c   Tamaru, Hisashi ^a,d   Freitag, Michael ^a,e   Selker, Eric U ^a  

^a UNIVERSITY OF OREGON   (United States)

^b YORK UNIVERSITY   (Canada)

^c Invitrogen   (United States)

^d GREGOR MENDEL INSTITUTE OF MOLECULAR PLANT BIOLOGY   (Austria)

^e OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 5; GENOMIC DNA; HISTONE H3; UNCLASSIFIED DRUG; AMINO ACID; HISTONE; HISTONE LYSINE METHYLTRANSFERASE; HISTONE METHYLTRANSFERASE; LYSINE;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; DNA METHYLATION; FUNGAL STRAIN; GENE FREQUENCY; GENE MUTATION; HISTONE PHOSPHORYLATION; IN VIVO STUDY; MICROSCOPY; MOLECULAR DYNAMICS; NEUROSPORA; NONHUMAN; PROCESS OPTIMIZATION; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SOUTHERN BLOTTING; VALIDATION PROCESS; WESTERN BLOTTING; WILD TYPE; ACETYLATION; CHEMISTRY; EUCHROMATIN; GENETICS; HETEROCHROMATIN; LETHAL GENE; METABOLISM; MUTATION; NEUROSPORA CRASSA; PHOSPHORYLATION; RECESSIVE GENE;

EUKARYOTA; NEUROSPORA; NEUROSPORA CRASSA;

ACETYLATION; AMINO ACID SUBSTITUTION; AMINO ACIDS; DNA METHYLATION; EUCHROMATIN; GENES, LETHAL; GENES, RECESSIVE; HETEROCHROMATIN; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; LYSINE; MUTATION; NEUROSPORA CRASSA; PHOSPHORYLATION;

EID: 84855272671     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002423     Document Type: Article

References (81)

1. Campos E, Reinberg, Danny, (2009) Histones: Annotating Chromatin. Annu Rev Genet 43.
2. Malik HS, Henikoff S, (2003) Phylogenomics of the nucleosome. Nat Struct Biol 10: 882-891.
3. Woudt LP, Pastink A, Kempers-Veenstra AE, Jansen AE, Mager WH, et al. (1983) The genes coding for histone H3 and H4 in Neurospora crassa are unique and contain intervening sequences. Nucleic Acids Res 11: 5347-5360.
4. Hays SM, Swanson J, Selker EU, (2002) Identification and characterization of the genes encoding the core histones and histone variants of Neurospora crassa. Genetics 160: 961-973.
5. Smith MM, Santisteban MS, (1998) Genetic dissection of histone function. Methods 15: 269-281.
6. Nakanishi S, Sanderson BW, Delventhal KM, Bradford WD, Staehling-Hampton K, et al. (2008) A comprehensive library of histone mutants identifies nucleosomal residues required for H3K4 methylation. Nat Struct Mol Biol 15: 881-888.
7. Dai J, Hyland EM, Yuan DS, Huang H, Bader JS, et al. (2008) Probing nucleosome function: a highly versatile library of synthetic histone H3 and H4 mutants. Cell 134: 1066-1078.
8. Matsubara K, Sano N, Umehara T, Horikoshi M, (2007) Global analysis of functional surfaces of core histones with comprehensive point mutants. Genes Cells 12: 13-33.
9. Mellone BG, Ball L, Suka N, Grunstein MR, Partridge JF, et al. (2003) Centromere silencing and function in fission yeast is governed by the amino terminus of histone H3. Curr Biol 13: 1748-1757.
10. Kouzarides T, (2007) Chromatin modifications and their function. Cell 128: 693-705.
11. Luco RF, Pan Q, Tominaga K, Blencowe BJ, Pereira-Smith OM, et al. (2010) Regulation of alternative splicing by histone modifications. Science 327: 996-1000.
12. Megee PC, Morgan BA, Mittman BA, Smith MM, (1990) Genetic analysis of histone H4: essential role of lysines subject to reversible acetylation. Science 247: 841-845.
13. Xiong L, Adhvaryu KK, Selker EU, Wang Y, (2010) Mapping of lysine methylation and acetylation in core histones of Neurospora crassa. Biochemistry 49: 5236-5243.
14. Tamaru H, Selker EU, (2001) A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414: 277-283.
15. Tamaru H, Zhang X, McMillen D, Singh PB, Nakayama J, et al. (2003) Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa. Nat Genet 34: 75-79.
16. Selker EU, (1990) Premeiotic instability of repeated sequences in Neurospora crassa. Annu Rev Genet 24: 579-613.
17. Galagan JE, Selker EU, (2004) RIP: the evolutionary cost of genome defense. Trends Genet 20: 417-423.
18. Selker EU, Tountas NA, Cross SH, Margolin BS, Murphy JG, et al. (2003) The methylated component of the Neurospora crassa genome. Nature 422: 893-897.
19. Lewis ZA, Honda S, Khlafallah TK, Jeffress JK, Freitag M, et al. (2009) Relics of repeat-induced point mutation direct heterochromatin formation in Neurospora crassa. Genome Res 19: 427-437.
20. Freitag M, Hickey PC, Khlafallah TK, Read ND, Selker EU, (2004) HP1 is essential for DNA methylation in Neurospora. Mol Cell 13: 427-434.
21. Honda S, Selker EU, (2008) Direct interaction between DNA methyltransferase DIM-2 and HP1 is required for DNA methylation in Neurospora. Mol Cell Biol 28: 6044-6055.
22. Kouzminova EA, Selker EU, (2001) Dim-2 encodes a DNA-methyltransferase responsible for all known cytosine methylation in Neurospora. EMBO Journal 20: 4309-4323.
23. 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.
24. Jacobs SA, Taverna SD, Zhang Y, Briggs SD, Li J, et al. (2001) Specificity of the HP1 chromo domain for the methylated N-terminus of histone H3. Embo J 20: 5232-5241.
25. Lewis ZA, Adhvaryu KK, Honda S, Shiver AL, Selker EU, (2010) Identification of DIM-7, a protein required to target the DIM-5 H3 methyltransferase to chromatin. Proc Natl Acad Sci U S A.
26. Lewis ZA, Adhvaryu KK, Honda S, Shiver AL, Knip M, et al. (2010) DNA Methylation and Normal Chromosome Behavior in Neurospora Depend on Five Components of a Histone Methyltransferase Complex, DCDC. PLoS Genet 6: e1001196 doi:10.1371/journal.pgen.1001196.
27. Jacobs SA, Khorasanizadeh S, (2002) Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail. Science 295: 2080-2083.
28. Adhvaryu KK, Selker EU, (2008) Protein phosphatase PP1 is required for normal DNA methylation in Neurospora. Genes Dev 22: 3391-3396.
29. Ebbs ML, Bender J, (2006) Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell 18: 1166-1176.
30. Jackson JP, Lindroth AM, Cao X, Jacobsen SE, (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416: 556-560.
31. Jackson JP, Johnson L, Jasencakova Z, Zhang X, PerezBurgos L, et al. (2004) Dimethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in Arabidopsis thaliana. Chromosoma 112: 308-315.
32. Lehnertz B, Ueda Y, Derijck AA, Braunschweig U, Perez-Burgos L, et al. (2003) Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr Biol 13: 1192-1200.
33. Zhang X, Yang Z, Khan SI, Horton JR, Tamaru H, et al. (2003) Structural basis for the product specificity of histone lysine methyltransferases. Mol Cell 12: 177-185.
34. Irelan JT, Selker EU, (1997) Cytosine methylation associated with repeat-induced point mutation causes epigenetic gene silencing in Neurospora crassa. Genetics 146: 509-523.
35. Rea S, Eisenhaber F, O'Carroll D, Strahl BD, Sun ZW, et al. (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406: 593-599.
36. 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.
37. Schultz DC, Ayyanathan K, Negorev D, Maul GG, Rauscher FJ 3rd, (2002) 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 16: 919-932.
38. Smith KM, Dobosy JR, Reifsnyder JE, Rountree MR, Anderson DC, et al. (2010) H2B- and H3-specific Histone Deacetylases are Required for DNA Methylation in Neurospora crassa. Genetics.
39. Canzio D, Chang EY, Shankar S, Kuchenbecker KM, Simon MD, et al. (2011) Chromodomain-mediated oligomerization of HP1 suggests a nucleosome-bridging mechanism for heterochromatin assembly. Mol Cell 41: 67-81.
40. Xhemalce B, Kouzarides T, (2010) A chromodomain switch mediated by histone H3 Lys 4 acetylation regulates heterochromatin assembly. Genes Dev 24: 647-652.
41. Casas-Mollano JA, Jeong BR, Xu J, Moriyama H, Cerutti H, (2008) The MUT9p kinase phosphorylates histone H3 threonine 3 and is necessary for heritable epigenetic silencing in Chlamydomonas. Proc Natl Acad Sci U S A 105: 6486-6491.
42. Shimada M, Niida H, Zineldeen DH, Tagami H, Tanaka M, et al. (2008) Chk1 is a histone H3 threonine 11 kinase that regulates DNA damage-induced transcriptional repression. Cell 132: 221-232.
43. Metzger E, Yin N, Wissmann M, Kunowska N, Fischer K, et al. (2008) Phosphorylation of histone H3 at threonine 11 establishes a novel chromatin mark for transcriptional regulation. Nat Cell Biol 10: 53-60.
44. Dunn KL, Davie JR, (2005) Stimulation of the Ras-MAPK pathway leads to independent phosphorylation of histone H3 on serine 10 and 28. Oncogene 24: 3492-3502.
45. Metzger E, Imhof A, Patel D, Kahl P, Hoffmeyer K, et al. (2010) Phosphorylation of histone H3T6 by PKCbeta(I) controls demethylation at histone H3K4. Nature 464: 792-796.
46. Kelly AE, Ghenoiu C, Xue JZ, Zierhut C, Kimura H, et al. (2010) Survivin reads phosphorylated histone H3 threonine 3 to activate the mitotic kinase Aurora B. Science 330: 235-239.
47. Wang F, Dai J, Daum JR, Niedzialkowska E, Banerjee B, et al. (2010) Histone H3 Thr-3 phosphorylation by Haspin positions Aurora B at centromeres in mitosis. Science 330: 231-235.
48. Houben A, Demidov D, Rutten T, Scheidtmann KH, (2005) Novel phosphorylation of histone H3 at threonine 11 that temporally correlates with condensation of mitotic and meiotic chromosomes in plant cells. Cytogenet Genome Res 109: 148-155.
49. Rathert P, Zhang X, Freund C, Cheng X, Jeltsch A, (2008) Analysis of the substrate specificity of the Dim-5 histone lysine methyltransferase using peptide arrays. Chem Biol 15: 5-11.
50. Yamada T, Fischle W, Sugiyama T, Allis CD, Grewal SI, (2005) The nucleation and maintenance of heterochromatin by a histone deacetylase in fission yeast. Mol Cell 20: 173-185.
51. Chen ES, Zhang K, Nicolas E, Cam HP, Zofall M, et al. (2008) Cell cycle control of centromeric repeat transcription and heterochromatin assembly. Nature 451: 734-737.
52. Zhang K, Mosch K, Fischle W, Grewal SI, (2008) Roles of the Clr4 methyltransferase complex in nucleation, spreading and maintenance of heterochromatin. Nat Struct Mol Biol 15: 381-388.
53. Nicolas E, Yamada T, Cam HP, Fitzgerald PC, Kobayashi R, et al. (2007) Distinct roles of HDAC complexes in promoter silencing, antisense suppression and DNA damage protection. Nat Struct Mol Biol 14: 372-380.
54. Motamedi MR, Hong EJ, Li X, Gerber S, Denison C, et al. (2008) HP1 proteins form distinct complexes and mediate heterochromatic gene silencing by nonoverlapping mechanisms. Mol Cell 32: 778-790.
55. Sugiyama T, Cam HP, Sugiyama R, Noma K, Zofall M, et al. (2007) SHREC, an effector complex for heterochromatic transcriptional silencing. Cell 128: 491-504.
56. Bedford MT, Clarke SG, (2009) Protein arginine methylation in mammals: who, what, and why. Mol Cell 33: 1-13.
57. Kirmizis A, Santos-Rosa H, Penkett CJ, Singer MA, Vermeulen M, et al. (2007) Arginine methylation at histone H3R2 controls deposition of H3K4 trimethylation. Nature 449: 928-932.
58. Guccione E, Bassi C, Casadio F, Martinato F, Cesaroni M, et al. (2007) Methylation of histone H3R2 by PRMT6 and H3K4 by an MLL complex are mutually exclusive. Nature 449: 933-937.
59. Kirmizis A, Santos-Rosa H, Penkett CJ, Singer MA, Green RD, et al. (2009) Distinct transcriptional outputs associated with mono- and dimethylated histone H3 arginine 2. Nat Struct Mol Biol 16: 449-451.
60. Chin HG, Pradhan M, Esteve PO, Patnaik D, Evans TC Jr, et al. (2005) Sequence specificity and role of proximal amino acids of the histone H3 tail on catalysis of murine G9A lysine 9 histone H3 methyltransferase. Biochemistry 44: 12998-13006.
61. Eskeland R, Czermin B, Boeke J, Bonaldi T, Regula JT, et al. (2004) The N-terminus of Drosophila SU(VAR)3-9 mediates dimerization and regulates its methyltransferase activity. Biochemistry 43: 3740-3749.
62. Rudolph T, Yonezawa M, Lein S, Heidrich K, Kubicek S, et al. (2007) Heterochromatin formation in Drosophila is initiated through active removal of H3K4 methylation by the LSD1 homolog SU(VAR)3-3. Mol Cell 26: 103-115.
63. Li F, Huarte M, Zaratiegui M, Vaughn MW, Shi Y, et al. (2008) Lid2 is required for coordinating H3K4 and H3K9 methylation of heterochromatin and euchromatin. Cell 135: 272-283.
64. Ooi SKT, Qiu C, Bernstein E, Li K, Jia D, et al. (2007) DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448: 714-717.
65. Butler JS, Lee JH, Skalnik DG, (2008) CFP1 interacts with DNMT1 independently of association with the Setd1 Histone H3K4 methyltransferase complexes. DNA Cell Biol 27: 533-543.
66. Thomson JP, Skene PJ, Selfridge J, Clouaire T, Guy J, et al. (2010) CpG islands influence chromatin structure via the CpG-binding protein Cfp1. Nature 464: 1082-1086.
67. Davis RH, De Serres FJ, (1970) Genetic and microbiological research techniques for Neurospora crassa. Meth Enzymol 17A: 47-143.
68. Perkins DD, (1986) Hints and precautions for the care, feeding and breeding of Neurospora. Fungal Genetics Newsl 33: 35-41.
69. Davis RH, (2000) Neurospora: Contributions of a Model Organism Oxford University Press.
70. Irelan J, Miao V, Selker EU, (1993) Small scale DNA preps for Neurospora crassa. Fungal Genetics Newsletter 40: 24.
71. Oakley BR, Rinehart JE, Mitchell BL, Oakley CE, Carmona C, et al. (1987) Cloning, mapping and molecular analysis of the pyrG (orotidine- 5′-phosphate decarboxylase) gene of Aspergillus nidulans. Gene 61: 385-399.
72. Southern EM, (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98: 503-517.
73. Feinberg AP, Vogelstein B, (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity (I). Anal Biochem 132: 6-13.
74. Selker EU, Stevens JN, (1987) Signal for DNA methylation associated with tandem duplication in Neurospora crassa. Mol Cell Biol 7: 1032-1038.
75. Zhang X, Tamaru H, Khan S, Horton J, Keefe L, et al. (2002) Structure of the Neurospora SET Domain Protein DIM-5, a Histone H3 Lysine Methyltransferase. Cell 111: 117-127.
76. Baum JA, Giles NH, (1986) DNase I hypersensitive sites within the inducible qa gene cluster of Neurospora crassa. Proc Natl Acad Sci U S A 83: 6533-6537.
77. Turner BM, (2005) Reading signals on the nucleosome with a new nomenclature for modified histones. Nat Struct Mol Biol 12: 110-112.
78. Hickey PC, Jacobson D, Read ND, Louise Glass NL, (2002) Live-cell imaging of vegetative hyphal fusion in Neurospora crassa. Fungal Genet Biol 37: 109-119.
79. Abramoff MD, Magelhaes PJ, Ram SJ, (2004) Image Processing with ImageJ. Biophotonics International 11: 36-42.
80. Nelson CJ, Santos-Rosa H, Kouzarides T, (2006) Proline isomerization of histone H3 regulates lysine methylation and gene expression. Cell 126: 905-916.
81. Duncan EM, Muratore-Schroeder TL, Cook RG, Garcia BA, Shabanowitz J, et al. (2008) Cathepsin L proteolytically processes histone H3 during mouse embryonic stem cell differentiation. Cell 135: 284-294.