Methylation of histone H3K23 blocks DNA damage in pericentric heterochromatin during meiosis

eLife

Volumn 2014, Issue 3, 2014, Pages

  Papazyan, Romeo ^a,g   Voronina, Ekaterina ^a,h   Chapman, Jessica R ^b,i   Luperchio, Teresa R ^a   Gilbert, Tonya M ^a   Meier, Elizabeth ^a   Mackintosh, Samuel G ^c   Shabanowitz, Jeffrey ^b   Tackett, Alan J ^c   Reddy, Karen L ^a   Coyne, Robert S ^d   Hunt, Donald F ^b,e   Liu, Yifan ^f   Taverna, Sean D ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^d J CRAIG VENTER INSTITUTE   (United States)

^e UNIVERSITY OF VIRGINIA   (United States)

^f UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^g UNIVERSITY OF PENNSYLVANIA   (United States)

^h UNIVERSITY OF MONTANA   (United States)

ⁱ NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE METHYLTRANSFERASE; TRANSCRIPTION FACTOR EZH2; HETEROCHROMATIN; HISTONE; HISTONE LYSINE METHYLTRANSFERASE; PROTOZOAL DNA; PROTOZOAL PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DNA DAMAGE; DOUBLE STRANDED DNA BREAK; ENZYME LINKED IMMUNOSORBENT ASSAY; GAIN OF FUNCTION MUTATION; HETEROCHROMATIN; HISTONE MODIFICATION; HUMAN; IMMUNOFLUORESCENCE TEST; LOSS OF FUNCTION MUTATION; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MEIOSIS; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; TETRAHYMENA THERMOPHILA; UPREGULATION; WESTERN BLOTTING; AMINO ACID SEQUENCE; CHEMISTRY; DEFICIENCY; GENE DELETION; GENETICS; GERMLINE MICRONUCLEUS; METABOLISM; METHYLATION; MOLECULAR GENETICS; PROTEIN PROCESSING; SEQUENCE ALIGNMENT;

CAENORHABDITIS ELEGANS; TETRAHYMENA; TETRAHYMENA THERMOPHILA;

AMINO ACID SEQUENCE; DNA BREAKS, DOUBLE-STRANDED; DNA, PROTOZOAN; GENE DELETION; HETEROCHROMATIN; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; MEIOSIS; METHYLATION; MICRONUCLEUS, GERMLINE; MOLECULAR SEQUENCE DATA; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTOZOAN PROTEINS; SEQUENCE ALIGNMENT; TETRAHYMENA THERMOPHILA;

EID: 84922571319     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.02996     Document Type: Article

References (81)

1. Alabert C, Groth A. 2012. Chromatin replication and epigenome maintenance. Nature Reviews Molecular Cell Biology13:153–167. doi: 10.1038/nrm3288.
2. Allis CD, Bowen JK, Abraham GN, Glover C V, Gorovsky MA. 1980. Proteolytic processing of histone H3 in chromatin: a physiologically regulated event in Tetrahymena micronuclei. Cell20:55–64. doi: 10.1016/0092-8674(80)90234-2.
3. Aronica L, Bednenko J, Noto T, DeSouza LV, Siu KW, Loidl J, Pearlman RE, Gorovsky MA, Mochizuki K. 2008. Study of an RNA helicase implicates small RNA-noncoding RNA interactions in programmed DNA elimination in Tetrahymena. Genes & Development22:2228–2241. doi: 10.1101/gad.481908.
4. Bannister AJ, Zegerman P, Partridge J F, Miska EA, Thomas JO, Allshire RC, Kouzarides T. 2001. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature410:120–124. doi: 10.1038/35065138.
5. Bender LB, Cao R, Zhang Y, Strome S. 2004. The MES-2/MES-3/MES-6 complex and regulation of histone H3methylation in C. elegans. Current Biology14:1639–1643. doi: 10.1016/j.cub.2004.08.062.
6. Brachet E, Sommermeyer V, Borde V. 2012. Interplay between modifcations of chromatin and meiotic recombination hotspots. Biology of the Cell104:51–69. doi: 10.1111/boc.201100113.
7. Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics77:71–94.
8. Bruns PJ, Cassidy-Hanley D. 2000. Biolistic transformation of macro- and micronuclei. Methods in Cell Biology62:501–512. doi: 10.1016/S0091-679X(08)61553-8.
9. Byrum SD, Taverna SD, Tackett AJ. 2013. Purifcation of a specifc native genomic locus for proteomic analysis. Nucleic Acids Research41:e195. doi: 10.1093/nar/gkt822.
10. Cervantes MD, Xi X, Vermaak D, Yao MC, Malik HS. 2006. The CNA1 histone of the ciliate Tetrahymenathermophila is essential for chromosome segregation in the germline micronucleus. Molecular Biology of the Cell17:485–497. doi: 10.1091/mbc.E05-07-0698.
11. Chalker DL. 2008. Dynamic nuclear reorganization during genome remodeling of Tetrahymena. Biochimica et Biophysica Acta1783:2130–2136. doi: 10.1016/j.bbamcr.2008.07.012.
12. Chung PH, Yao MC. 2012. Tetrahymena thermophila JMJD3 homolog regulates H3K27 methylation and nucleardifferentiation. Eukaryotic Cell 11:601–614. doi: 10.1128/EC.05290-11.
13. Colaiacovo MP, MacQueen AJ, Martinez-Perez E, McDonald K, Adamo A, La Volpe A, Villeneuve AM. 2003. Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Developmental Cell5:463–474. doi: 10.1016/S1534-5807(03)00232-6.
14. Coon JJ, Ueberheide B, Syka JE, Dryhurst DD, Ausio J, Shabanowitz J, Hunt D F. 2005. Protein identifcation using sequential ion/ion reactions and tandem mass spectrometry. Proceedings of the National Academy of Sciences of USA102:9463–9468. doi: 10.1073/pnas.0503189102.
15. Crittenden SL, Troemel ER, Evans TC, Kimble J. 1994. GLP-1 is localized to the mitotic region of the C. elegans germ line. Development120:2901–2911.
16. Dernburg AF, Sedat JW, Hawley RS. 1996. Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell86:135–146. doi: 10.1016/S0092-8674(00)80084-7.
17. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F, Xue C, Marinov GK, Khatun J, Williams BA, Zaleski C, Rozowsky J, Röder M, Kokocinski F, Abdelhamid RF, Alioto T, Antoshechkin I, Baer MT, Bar NS, Batut P, Bell K, Bell I, Chakrabortty S, Chen X, Chrast J, Curado J, Derrien T, Drenkow J, Dumais E, Dumais J, Duttagupta R, Falconnet E, Fastuca M, Fejes-Toth K, Ferreira P, Foissac S, Fullwood MJ, Gao H, Gonzalez D, Gordon A, Gunawardena H, Howald C, Jha S, Johnson R, Kapranov P, King B, Kingswood C, Luo OJ, Park E, Persaud K, Preall JB, Ribeca P, Risk B, Robyr D, Sammeth M, Schaffer L, See LH, Shahab A, Skancke J, Suzuki AM, Takahashi H, Tilgner H, Trout D, Walters N, Wang H, Wrobel J, Yu Y, Ruan X, Hayashizaki Y, Harrow J, Gerstein M, Hubbard T, Reymond A, Antonarakis SE, Hannon G, Giddings MC, Ruan Y, Wold B, Carninci P, Guigó R, Gingeras TR. 2012. Landscape of transcription in humancells. Nature489:101–108. doi: 10.1038/nature11233.
18. Duncan EM, Muratore-Schroeder TL, Cook RG, Garcia BA, Shabanowitz J, Hunt DF, Allis CD. 2008. Cathepsin L proteolytically processes histone H3 during mouse embryonic stem cell differentiation. Cell135:284–294. doi: 10.1016/j.cell.2008.09.055.
19. Gao S, Xiong J, Zhang C, Berquist BR, Yang R, Zhao M, Molascon AJ, Kwiatkowski SY, Yuan D, Qin Z, Wen J, Kapler GM, Andrews PC, Miao W, Liu Y. 2013. Impaired replication elongation in Tetrahymena mutants deficient in histone H3 Lys 27 monomethylation. Genes & Development27:1662–1679. doi: 10.1101/gad.218966.113.
20. Garcia BA, Hake SB, Diaz RL, Kauer M, Morris SA, Recht J, Shabanowitz J, Mishra N, Strahl BD, Allis CD, Hunt D F. 2007a. Organismal differences in post-translational modifcations in histones H3 and H4. The Journal of Biological Chemistry282:7641–7655. doi: 10.1074/jbc.M607900200.
21. Garcia BA, Pesavento JJ, Mizzen CA, Kelleher NL. 2007b. Pervasive combinatorial modifcation of histone H3 in human cells. Nature Methods4:487–489. doi: 10.1038/nmeth1052.
22. Gaydos LJ, Rechtsteiner A, Egelhofer TA, Carroll CR, Strome S. 2012. Antagonism between MES-4 and Polycomb repressive complex 2 promotes appropriate gene expression in C. elegans germ cells. Cell Reports2:1169–1177. doi: 10.1016/j.celrep.2012.09.019.
23. Geer LY, Markey S P, Kowalak JA, Wagner L, Xu M, Maynard DM, Yang X, Shi W, Bryant SH. 2004. Open massspectrometry search algorithm. Journal of Proteome Research3:958–964. doi: 10.1021/pr0499491.
24. Gerton JL, DeRisi J, Shroff R, Lichten M, Brown PO, Petes TD. 2000. Global mapping of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences of USA97:11383–11390. doi: 10.1073/pnas.97.21.11383.
25. Gorovsky MA, Yao MC, Keevert JB, Pleger GL. 1975. Isolation of micro- and macronuclei of Tetrahymena pyriformis. Methods in Cell Biology9:311–327. doi: 10.1016/S0091-679X(08)60080-1.
26. Gu SG, Pak J, Guang S, Maniar JM, Kennedy S, Fire A. 2012. Amplifcation of siRNA in Caenorhabditis elegans generates a transgenerational sequence-targeted histone H3 lysine 9 methylation footprint. Nature Genetics44:157–164. doi: 10.1038/ng.1039.
27. Hamilton EP, Orias E. 2000. Genetic crosses: setting up crosses, testing progeny, and isolating phenotypicassortants. Methods in Cell Biology62:219–228. doi: 10.1016/S0091-679X(08)61532-0.
28. Harlow E, Lane D. 1988. Antibodies: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
29. Heitz E. 1928. Das Heterochromatin der Moose. Jahrbücher für Wissenschaftliche Botanik69:762–818.
30. Jacobs SA, Harp JM, Devarakonda S, Kim Y, Rastinejad F, Khorasanizadeh S. 2002. The active site of the SETdomain is constructed on a knot. Nature Structural Biology9:833–838. doi: 10.1038/nsb861.
31. 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. The EMBO Journal20:5232–5241. doi: 10.1093/emboj/20.18.5232.
32. James TC, Eissenberg JC, Craig C, Dietrich V, Hobson A, Elgin SC. 1989. Distribution patterns of HP1, a heterochromatin-associated nonhistone chromosomal protein of Drosophila. European Journal of Cell Biology50:170–180.
33. Jeppesen P, Turner BM. 1993. The inactive X chromosome in female mammals is distinguished by a lack of histone H4 acetylation, a cytogenetic marker for gene expression. Cell74:281–289. doi: 10.1016/0092-8674(93)90419-Q.
34. Kelly WG, Schaner CE, Dernburg AF, Lee MH, Kim SK, Villeneuve AM, Reinke V. 2002. X-chromosome silencing inthe germline of C. elegans. Development129:479–492.
35. Kim JA, Kruhlak M, Dotiwala F, Nussenzweig A, Haber JE. 2007. Heterochromatin is refractory to gamma-H2AX modification in yeast and mammals. The Journal of Cell Biology178:209–218. doi: 10.1083/jcb.200612031.
36. Kimble J, Crittenden SL. 2007. Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in Caenorhabditis elegans. Annual Review of Cell and Developmental Biology23:405–433. doi: 10.1146/annurev.cellbio.23.090506.123326.
37. Kota SK, Feil R. 2010. Epigenetic transitions in germ cell development and meiosis. Developmental Cell19:675–686. doi: 10.1016/j.devcel.2010.10.009.
38. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature227:680–685. doi: 10.1038/227680a0.
39. Lichten M, de Massy B. 2011. The impressionistic landscape of meiotic recombination. Cell147:267–270. doi: 10.1016/j.cell.2011.09.038.
40. Liu H, Galka M, Iberg A, Wang Z, Li L, Voss C, Jiang X, Lajoie G, Huang Z, Bedford MT, Li SS. 2010. Systematic identification of methyllysine-driven interactions for histone and nonhistone targets. Journal of Proteome Research9:5827–5836. doi: 10.1021/pr100597b.
41. Liu Y, Taverna SD, Muratore TL, Shabanowitz J, Hunt DF, Allis CD. 2007. RNAi-dependent H3K27 methylation is required for heterochromatin formation and DNA elimination in Tetrahymena. Genes & Development21:1530–1545. doi: 10.1101/gad.1544207.
42. Loidl J, Scherthan H. 2004. Organization and pairing of meiotic chromosomes in the ciliate Tetrahymena thermophila. Journal of Cell Science117:5791–5801. doi: 10.1242/jcs.01504.
43. Lukas J, Lukas C, Bartek J. 2011. More than just a focus: the chromatin response to DNA damage and its role ingenome integrity maintenance. Nature Cell Biology13:1161–1169. doi: 10.1038/ncb2344.
44. Maddox PS, Hyndman F, Monen J, Oegema K, Desai A. 2007. Functional genomics identifes a Myb domain-containing protein family required for assembly of CENP-A chromatin. The Journal of Cell Biology176:757–763. doi: 10.1083/jcb.200701065.
45. Madireddi MT, Davis MC, Allis CD. 1994. Identification of a novel polypeptide involved in the formation of DNA-containing vesicles during macronuclear development in Tetrahymena. Developmental Biology165:418–431. doi: 10.1006/dbio.1994.1264.
46. Martindale DW, Allis CD, Bruns PJ. 1982. Conjugation in Tetrahymena thermophila. A temporal analysis of cytological stages. Experimental Cell Research140:227–236. doi: 10.1016/0014-4827(82)90172-0.
47. Mikesh LM, Ueberheide B, Chi A, Coon JJ, Syka JEP, Shabanowitz J, Hunt DF. 2006. The utility of ETD mass spectrometry in proteomics analysis. Biochimica et Biophysica Acta1764:1811–1822. doi: 10.1016/j.bbapap.2006.10.003.
48. Mochizuki K, Fine NA, Fujisawa T, Gorovsky MA. 2002. Analysis of a piwi-related gene implicates small RNAs ingenome rearrangement in Tetrahymena. Cell110:689–699. doi: 10.1016/S0092-8674(02)00909-1.
49. Mochizuki K, Novatchkova M, Loidl J. 2008. DNA double-strand breaks, but not crossovers, are required for the reorganization of meiotic nuclei in Tetrahymena. Journal of Cell Science121:2148–2158. doi: 10.1242/jcs.031799.
50. Moore KE, Carlson SM, Camp ND, Cheung P, James RG, Chua KF, Wolf-Yadlin A, Gozani O. 2013. A general molecular affinity strategy for global detection and proteomic analysis of lysine methylation. Molecular Cell50:444–456. doi: 10.1016/j.molcel.2013.03.005.
51. Motl JA, Chalker DL. 2011. Zygotic expression of the doublestranded RNA binding motif protein Drb2p is required for DNA elimination in the ciliate Tetrahymena thermophila. Eukaryotic Cell10:1648–1659. doi: 10.1128/EC.05216-11.
52. Nightingale KP, Gendreizig S, White DA, Bradbury C, Hollfelder F, Turner BM. 2007. Cross-talk between histone modifcations in response to histone deacetylase inhibitors: MLL4 links histone H3 acetylation and histone H3K4 methylation. The Journal of Biological Chemistry7:4408–4416. doi: 10.1074/jbc.M606773200.
53. Peng JC, Karpen GH. 2009. Heterochromatic genome stability requires regulators of histone H3 K9 methylation. PLOS Genetics5:e1000435. doi: 10.1371/journal.pgen.1000435.
54. Peters AH, O'Carroll D, Scherthan H, Mechtler K, Sauer S, Schofer C, Weipoltshammer K, Pagani M, Lachner M, Kohlmaier A, Opravil S, Doyle M, Sibilia M, Jenuwein T. 2001. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell107:323–337. doi: 10.1016/S0092-8674(01)00542-6.
55. Prigent C, Dimitrov S. 2003. Phosphorylation of serine 10 in histone H3, what for? Journal of Cell Science116:3677–3685. doi: 10.1242/jcs.00735.
56. Reddy KL, Zullo JM, Bertolino E, Singh H. 2008. Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature452:243–247. doi: 10.1038/nature06727.
57. Ruthenburg AJ, Li H, Patel DJ, Allis CD. 2007. Multivalent engagement of chromatin modifcations by linked binding modules. Nature Reviews Molecular Cell Biology8:983–994. doi: 10.1038/nrm2298.
58. Schoeberl UE, Kurth HM, Noto T, Mochizuki K. 2012. Biased transcription and selective degradation of small RNAs shape the pattern of DNA elimination in Tetrahymena. Genes & Development26:1729–1742. doi: 10.1101/gad.196493.112.
59. Shechter D, Dormann HL, Allis CD, Hake SB. 2007. Extraction, purifcation and analysis of histones. Nature Protocols2:1445–1457. doi: 10.1038/nprot.2007.202.
60. Simon JA, Kingston RE. 2009. Mechanisms of polycomb gene silencing: knowns and unknowns. Nature Reviews Molecular Cell Biology10:697–708. doi: 10.1038/nrm2763.
61. Sobel RE, Cook RG, Perry CA, Annunziato AT, Allis CD. 1995. Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proceedings of the National Academy of Sciences of USA4:1237–1241. doi: 10.1073/pnas.92.4.1237.
62. Song X, Gjoneska E, Ren Q, Taverna SD, Allis CD, Gorovsky MA. 2007. Phosphorylation of the SQ H2A.X motif is required for proper meiosis and mitosis in Tetrahymena thermophila. Molecular and Cellular Biology27:2648–2660. doi: 10.1128/MCB.01910-06.
63. Strahl BD, Ohba R, Cook RG, Allis CD. 1999. Methylation of histone H3 at lysine 4 is highly conserved and correlates with transcriptionally active nuclei in Tetrahymena. Proceedings of the National Academy of Sciences of USA21:14967–14972. doi: 10.1073/pnas.96.26.14967.
64. Strahl BD, Allis CD. 2000. The language of covalent histone modifcations. Nature403:41–45. doi: 10.1038/47412.
65. Sugai T, Hiwatashi K. 1974. Cytologic and autoradiographic studies of the micronucleus at meiotic prophase in Tetrahymena pyriformis. The Journal of Protozoology21:542–548. doi: 10.1111/j.1550-7408.1974.tb03695.x.
66. Sweet MT, Allis CD. 2006. Isolation and purification of Tetrahymena nuclei. CSH Protocols2006:doi: 10.1101/pdb.prot4500.
67. Tackett AJ, Dilworth DJ, Davey MJ, O'Donnell MD, Aitchison JD, Rout M P, Chait BT. 2005. Proteomic and genomic characterization of chromatin complexes at a boundary. The Journal of Cell Biology169:35–47. doi: 10.1083/jcb.200502104.
68. Taverna SD, Coyne RS, Allis CD. 2002. Methylation of histone H3 at lysine 9 targets programmed DNA elimination in Tetrahymena. Cell110:701–711. doi: 10.1016/S0092-8674(02)00941-8.
69. Taverna SD, Li H, Ruthenburg AJ, Allis CD, Patel DJ. 2007a. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nature Structural & Molecular Biology14:1025–1040. doi: 10.1038/nsmb1338.
70. Taverna SD, Ueberheide BM, Liu Y, Tackett AJ, Diaz RL, Shabanowitz J, Chait BT, Hunt D F, Allis CD. 2007b. Long-distance combinatorial linkage between methylation and acetylation on histone H3 N termini. Proceedings of the National Academy of Sciences of USA 104:2086–2091. doi: 10.1073/pnas.0610993104.
71. Thomas CE, Kelleher NL, Mizzen CA. 2006. Mass spectrometric characterization of human histone H3: a bird'seye view. Journal of Proteome Research5:240–247. doi: 10.1021/pr050266a.
72. Timmons L, Fire A. 1998. Specific interference by ingested dsRNA. Nature395:854. doi: 10.1038/27579.
73. Turner BM. 2000. Histone acetylation and an epigenetic code. Bioessays 22:836–845. doi: 10.1002/1521-1878(200009)22:9<836::AID-BIES9>3.0.CO;2-X.
74. Vavra KJ, Allis CD, Gorovsky MA. 1982. Regulation of histone acetylation in Tetrahymena macro- and micronuclei. The Journal of Biological Chemistry257:2591–2598.
75. Waterborg JH. 1990. Sequence analysis of acetylation and methylation in two histone H3 variants of alfalfa. The Journal of Biological Chemistry265:17157–17161.
76. Wei Y, Mizzen CA, Cook RG, Gorovsky MA, Allis CD. 1998. Phosphorylation of histone H3 at serine 10 is correlated with chromosome condensation during mitosis and meiosis in Tetrahymena. Proceedings of the National Academy of Sciences of USA95:7480–7484. doi: 10.1073/pnas.95.13.7480.
77. Wells JM, Ellingson JL, Catt DM, Berger PJ, Karrer KM. 1994. A small family of elements with long inverted repeats is located near sites of developmentally regulated DNA rearrangement in Tetrahymena thermophila. Molecular and Cellular Biology14:5939–5949. doi: 10.1128/MCB.14.9.5939.
78. Wenkert D, Allis CD. 1984. Timing of the appearance of macronuclear-specific histone variant hv1 and gene expression in developing new macronuclei of Tetrahymena thermophila. The Journal of Cell Biology98:2107–2117. doi: 10.1083/jcb.98.6.2107.
79. Wu S, Hu YC, Liu H, Shi Y. 2009. Loss of YY1 impacts the heterochromatic state and meiotic double-strand breaksduring mouse spermatogenesis. Molecular and Cellular Biology29:6245–6256. doi: 10.1128/MCB.00679-09.
80. Yamada S, Ohta K, Yamada T. 2013. Acetylated Histone H3K9 is associated with meiotic recombination hotspots, and plays a role in recombination redundantly with other factors including the H3K4 methylase Set1 in fission yeast. Nucleic Acids Research41:3504–3517. doi: 10.1093/nar/gkt049.
81. Young NL, DiMaggio PA, Plazas-Mayorca MD, Baliban RC, Floudas CA, Garcia BA. 2009. High throughput characterization of combinatorial histone codes. Molecular & Cellular Proteomics8:2266–2284. doi: 10.1074/mcp.M900238-MCP200.