Barrier-to-Autointegration Factor influences specific histone modifications

Rocío de Oca

Paul Andreassen

Katherine Wilson

Additional material

Supplementary PDF file supplied by authors.

Click here to view.^{(1.4M, pdf)}

^{Department of Cell Biology; The Johns Hopkins University School of Medicine; Baltimore, MD USA}

^{Division of Experimental Hematology & Cancer Biology; Cincinnati Children’s Research Foundation; University of Cincinnati College of Medicine; Cincinnati, OH USA}

^{Corresponding author.}

Correspondence to: Katherine L. Wilson; Email: ude.imhj@nosliwlk

Abstract

Defects in the nuclear envelope or nuclear ‘lamina’ networks cause disease and can perturb histone posttranslational (epigenetic) regulation. Barrier-to-Autointegration Factor (BAF) is an essential but enigmatic lamina component that binds lamins, LEM-domain proteins, DNA and histone H3 directly. We report that BAF copurified with nuclease-digested mononucleosomes and associated with modified histones in vivo. BAF overexpression significantly reduced global histone H3 acetylation by 18%. In cells that stably overexpressed BAF 3-fold, silencing mark H3-K27-Me1/3 and active marks H4-K16-Ac and H4-Ac5 decreased significantly. Significant increases were also seen for silencing mark H3-K9-Me3, active marks H3-K4-Me2, H3-K9/K14-Ac and H4-K5-Ac and a mark (H3-K79-Me2) associated with both active and silent chromatin. Other increases (H3-S10-P, H3-S28-P and silencing mark H3-K9-Me2) did not reach statistical significance. BAF overexpression also significantly influenced cell cycle distribution. Moreover, BAF associated in vivo with SET/I2PP2A (protein phosphatase 2A inhibitor; blocks H3 dephosphorylation) and G9a (H3-K9 methyltransferase), but showed no detectable association with HDAC1 or HATs. These findings reveal BAF as a novel epigenetic regulator and are discussed in relation to BAF deficiency phenotypes, which include a hereditary progeria syndrome and loss of pluripotency in embryonic stem cells.

Keywords: Barrier-to-Autointegration Factor, cell cycle, DNA replication, G9a, H3-K9 dimethylation, H3-S10 phosphorylation, Hutchinson-Gilford Progeria Syndrome, Lamina-Associated Domain, nuclear envelope, nucleoskeleton, nucleosome, SET/I2PP2A

Abstract

Click here to view.^{(1.4M, pdf)}

Acknowledgments

We are grateful to P. Traktman (Medical College of Wisconsin) for the 293:BAF and 293:CAT cell lines; R. Stolle for purified BAF; M. J. Eddins and K. Fahie (Johns Hopkins School of Medicine) for chromatography help and M. J. Eddins for Figure 1E. We thank C. Lerin and P. Puigserver (Dana Farber Cancer Institute), I. Celic and J. Boeke (Johns Hopkins School ofMedicine), W. L. Kraus (Cornell), J. Th’ng (Northwestern Ontario Regional Cancer Centre) and C. Slawson and L. Blosser (Johns Hopkins Flow Cytometry Facility) for reagents and advice. We thank W. Gu (Columbia), R. Roeder (Rockefeller), M. R. Stallcup (Univ. Southern California), T. Papamarcaki (Univ. Ioannina) and H. Wang (Univ. Alabama) for constructs and S. Taverna and the Wilson lab for insightful discussions. This work was funded by American Heart Association Predoctoral fellowship 0615601U (R.M.) and National Institutes of Health RO1 GM48646 (K.L.W.).

Acknowledgments

Disclosure of Potential Conflicts of Interest

The authors have declared that no competing interests exist.

Disclosure of Potential Conflicts of Interest

Glossary

Abbreviations:

BAF	Barrier to Autointegration Factor
BrdU	5-Bromo-2’-Deoxyuridine
CBB	Coomassie Brilliant Blue
DMEM	Dulbecco’s modified eagle’s medium
HDAC	histone deacetylase
HGPS	Hutchinson-Gilford progeria syndrome
HP1	heterochromatin protein 1
IP	immunoprecipitation
LADs	Lamina-Associated Domains
LEM	LAP2-Emerin-MAN1
LOCKs	Large Organized Chromatin K9 modifications
NE	nuclear envelope
SET/I2PP2A	protein phosphatase 2A inhibitor
Tet	tetracycline
PARP1	poly(ADP) ribose polymerase 1
PBS	phosphate-buffered saline
PTM	posttranslational modification
RBBP4	retinoblastoma binding protein 4
2X-SB	2X-Sample Buffer

Glossary

Footnotes

Previously published online: www.landesbioscience.com/journals/nucleus/article/17960

Footnotes

References

1. Postnikov Y, Bustin MRegulation of chromatin structure and function by HMGN proteins. Biochim Biophys Acta. 2010;1799:62, 8.[Google Scholar]
2. McBryant SJ, Lu X, Hansen JCMultifunctionality of the linker histones: an emerging role for protein-protein interactions. Cell Res. 2010;20:519–28. doi: 10.1038/cr.2010.35.] [[Google Scholar]
3. Jenuwein T, Allis CDTranslating the histone code. Science. 2001;293:1074–80. doi: 10.1126/science.1063127.] [[PubMed][Google Scholar]
4. Berger SLThe complex language of chromatin regulation during transcription. Nature. 2007;447:407–12. doi: 10.1038/nature05915.] [[PubMed][Google Scholar]
5. Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein TMethylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature. 2001;410:116–20. doi: 10.1038/35065132.] [[PubMed][Google Scholar]
6. Nowak SJ, Corces VGPhosphorylation of histone H3: a balancing act between chromosome condensation and transcriptional activation. Trends Genet. 2004;20:214–20. doi: 10.1016/j.tig.2004.02.007.] [[PubMed][Google Scholar]
7. Dechat T, Pfleghaar K, Sengupta K, Shimi T, Shumaker DK, Solimando L, et al Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev. 2008;22:832–53. doi: 10.1101/gad.1652708.] [[Google Scholar]
8. Wilson KL, Berk JMThe nuclear envelope at a glance. J Cell Sci. 2010;123:1973–8. doi: 10.1242/jcs.019042.] [[Google Scholar]
9. Simon DN, Wilson KLThe nucleoskeleton as a genome-associated dynamic ‘network of networks’ Nat Rev Mol Cell Biol. 2011;12:695–708. doi: 10.1038/nrm3207.] [[PubMed][Google Scholar]
10. Pickersgill H, Kalverda B, de Wit E, Talhout W, Fornerod M, van Steensel BCharacterization of the Drosophila melanogaster genome at the nuclear lamina. Nat Genet. 2006;38:1005–14. doi: 10.1038/ng1852.] [[PubMed][Google Scholar]
11. Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB, Talhout W, et al Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature. 2008;453:948–51. doi: 10.1038/nature06947.] [[PubMed][Google Scholar]
12. Peric-Hupkes D, Meuleman W, Pagie L, Bruggeman SW, Solovei I, Brugman W, et al Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol Cell. 2010;38:603–13. doi: 10.1016/j.molcel.2010.03.016.] [[Google Scholar]
13. Meister P, Towbin BD, Pike BL, Ponti A, Gasser SM. The spatial dynamics of tissue-specific promoters during C. elegans development. Genes Dev. 2010;24:766–82. doi: 10.1101/gad.559610.] [
14. Wilson KL, Foisner RLamin-binding Proteins. Cold Spring Harb Perspect Biol. 2010;2:a000554. doi: 10.1101/cshperspect.a000554.] [[Google Scholar]
15. Prokocimer M, Davidovich M, Nissim-Rafinia M, Wiesel-Motiuk N, Bar D, Barkan R, Meshorer E, Gruenbaum YNuclear lamins: key regulators of nuclear structure and activities. J Cell Mol Med. 2009;13:1059, 85. doi: 10.1111/j.1582-4934.2008.00676.x.] [[Google Scholar]
16. Worman HJ, Fong LG, Muchir A, Young SGLaminopathies and the long strange trip from basic cell biology to therapy. J Clin Invest. 2009;119:1825–36. doi: 10.1172/JCI37679.] [[Google Scholar]
17. Sabatelli P, Lattanzi G, Ognibene A, Columbaro M, Capanni C, Merlini L, et al Nuclear alterations in autosomal-dominant Emery-Dreifuss muscular dystrophy. Muscle Nerve. 2001;24:826–9. doi: 10.1002/mus.1076.] [[PubMed][Google Scholar]
18. Goldman RD, Shumaker DK, Erdos MR, Eriksson M, Goldman AE, Gordon LB, et al Accumulation of mutant lamin A causes progressive changes in nuclear architecture in Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci USA. 2004;101:8963–8. doi: 10.1073/pnas.0402943101.] [[Google Scholar]
19. Columbaro M, Capanni C, Mattioli E, Novelli G, Parnaik VK, Squarzoni S, et al Rescue of heterochromatin organization in Hutchinson-Gilford progeria by drug treatment. Cell Mol Life Sci. 2005;62:2669–78. doi: 10.1007/s00018-005-5318-6.] [[Google Scholar]
20. Scaffidi P, Misteli TReversal of the cellular phenotype in the premature aging disease Hutchinson-Gilford progeria syndrome. Nat Med. 2005;11:440–5. doi: 10.1038/nm1204.] [[Google Scholar]
21. Filesi I, Gullotta F, Lattanzi G, D'Apice MR, Capanni C, Nardone AM, et al Alterations of nuclear envelope and chromatin organization in mandibuloacral dysplasia, a rare form of laminopathy. Physiol Genomics. 2005;23:150–8. doi: 10.1152/physiolgenomics.00060.2005.] [[PubMed][Google Scholar]
22. Shumaker DK, Dechat T, Kohlmaier A, Adam SA, Bozovsky MR, Erdos MR, et al Mutant nuclear lamin A leads to progressive alterations of epigenetic control in premature aging. Proc Natl Acad Sci USA. 2006;103:8703–8. doi: 10.1073/pnas.0602569103.] [[Google Scholar]
23. Margalit A, Brachner A, Gotzmann J, Foisner R, Gruenbaum YBarrier-to-autointegration factor–a BAFfling little protein. Trends Cell Biol. 2007;17:202–8. doi: 10.1016/j.tcb.2007.02.004.] [[PubMed][Google Scholar]
24. Haraguchi T, Koujin T, Segura-Totten M, Lee KK, Matsuoka Y, Yoneda Y, et al BAF is required for emerin assembly into the reforming nuclear envelope. J Cell Sci. 2001;114:4575–85.[PubMed][Google Scholar]
25. Liu J, Lee KK, Segura-Totten M, Neufeld E, Wilson KL, Gruenbaum YMAN1 and emerin have overlapping function(s) essential for chromosome segregation and cell division in Caenorhabditis elegans. Proc Natl Acad Sci USA. 2003;100:4598–603. doi: 10.1073/pnas.0730821100.] [[Google Scholar]
26. Furukawa K, Sugiyama S, Osouda S, Goto H, Inagaki M, Horigome T, et al Barrier-to-autointegration factor plays crucial roles in cell cycle progression and nuclear organization in Drosophila. J Cell Sci. 2003;116:3811–23. doi: 10.1242/jcs.00682.] [[PubMed][Google Scholar]
27. Margalit A, Segura-Totten M, Gruenbaum Y, Wilson KLBarrier-to-autointegration factor is required to segregate and enclose chromosomes within the nuclear envelope and assemble the nuclear lamina. Proc Natl Acad Sci USA. 2005;102:3290–5. doi: 10.1073/pnas.0408364102.] [[Google Scholar]
28. Gorj´ńcz M, Klerkx EP, Galy V, Santarella R, Lopez-Iglesias C, Askjaer P, et al Caenorhabditis elegans BAF-1 and its kinase VRK-1 participate directly in post-mitotic nuclear envelope assembly. EMBO J. 2007;26:132–43. doi: 10.1038/sj.emboj.7601470.] [[Google Scholar]
29. Haraguchi T, Kojidani T, Koujin T, Shimi T, Osakada H, Mori C, et al Live cell imaging and electron microscopy reveal dynamic processes of BAF-directed nuclear envelope assembly. J Cell Sci. 2008;121:2540–54. doi: 10.1242/jcs.033597.] [[PubMed][Google Scholar]
30. Reddy KL, Zullo JM, Bertolino E, Singh HTranscriptional repression mediated by repositioning of genes to the nuclear lamina. Nature. 2008;452:243–7. doi: 10.1038/nature06727.] [[PubMed][Google Scholar]
31. Jiang X, Xia L, Chen D, Yang Y, Huang H, Yang L, et al Otefin, a nuclear membrane protein, determines the fate of germline stem cells in Drosophila via interaction with Smad complexes. Dev Cell. 2008;14:494–506. doi: 10.1016/j.devcel.2008.02.018.] [[PubMed][Google Scholar]
32. Towbin BD, Meister P, Pike BL, Gasser SM. Repetitive transgenes in C. elegans accumulate heterochromatic marks and are sequestered at the nuclear envelope in a copy-number- and lamin-dependent manner. Cold Spring Harb Symp Quant Biol. 2010;75:555–65. doi: 10.1101/sqb.2010.75.041.] [[PubMed]
33. Holaska JM, Lee KK, Kowalski AK, Wilson KLTranscriptional repressor germ cell-less (GCL) and barrier to autointegration factor (BAF) compete for binding to emerin in vitro. J Biol Chem. 2003;278:6969–75. doi: 10.1074/jbc.M208811200.] [[PubMed][Google Scholar]
34. Shimi T, Koujin T, Segura-Totten M, Wilson KL, Haraguchi T, Hiraoka YDynamic interaction between BAF and emerin revealed by FRAP, FLIP and FRET analyses in living HeLa cells. J Struct Biol. 2004;147:31–41. doi: 10.1016/j.jsb.2003.11.013.] [[PubMed][Google Scholar]
35. Margalit A, Neufeld E, Feinstein N, Wilson KL, Podbilewicz B, Gruenbaum Y. Barrier to autointegration factor blocks premature cell fusion and maintains adult muscle integrity in C. elegans. J Cell Biol. 2007;178:661–73. doi: 10.1083/jcb.200704049.] [
36. Zheng R, Ghirlando R, Lee MS, Mizuuchi K, Krause M, Craigie RBarrier-to-autointegration factor (BAF) bridges DNA in a discrete, higher-order nucleoprotein complex. Proc Natl Acad Sci USA. 2000;97:8997–9002. doi: 10.1073/pnas.150240197.] [[Google Scholar]
37. Bradley CM, Ronning DR, Ghirlando R, Craigie R, Dyda FStructural basis for DNA bridging by barrier-to-autointegration factor. Nat Struct Mol Biol. 2005;12:935–6. doi: 10.1038/nsmb989.] [[PubMed][Google Scholar]
38. Skoko D, Li M, Huang Y, Mizuuchi M, Cai M, Bradley CM, et al Barrier-to-autointegration factor (BAF) condenses DNA by looping. Proc Natl Acad Sci USA. 2009;106:16610–5. doi: 10.1073/pnas.0909077106.] [[Google Scholar]
39. Segura-Totten M, Kowalski AK, Craigie R, Wilson KLBarrier-to-autointegration factor: major roles in chromatin decondensation and nuclear assembly. J Cell Biol. 2002;158:475–85. doi: 10.1083/jcb.200202019.] [[Google Scholar]
40. Wang X, Xu S, Rivolta C, Li LY, Peng GH, Swain PK, et al Barrier to autointegration factor interacts with the cone-rod homeobox and represses its transactivation function. J Biol Chem. 2002;277:43288–300. doi: 10.1074/jbc.M207952200.] [[PubMed][Google Scholar]
41. Montes de Oca R, Lee KK, Wilson KLBinding of barrier to autointegration factor (BAF) to histone H3 and selected linker histones including H1.1. J Biol Chem. 2005;280:42252–62. doi: 10.1074/jbc.M509917200.] [[PubMed][Google Scholar]
42. Montes de Oca R, Shoemaker CJ, Gucek M, Cole RN, Wilson KLBarrier-to-autointegration factor proteome reveals chromatin-regulatory partners. PLoS ONE. 2009;4:e7050. doi: 10.1371/journal.pone.0007050.] [[Google Scholar]
43. Cox JL, Mallanna SK, Ormsbee BD, Desler M, Wiebe MS, Rizzino ABanf1 is required to maintain the self-renewal of both mouse and human embryonic stem cells. J Cell Sci. 2011;124:2654–65. doi: 10.1242/jcs.083238.] [[Google Scholar]
44. Puente XS, Quesada V, Osorio FG, Cabanillas R, Cadinanos J, Fraile JM, et al Exome sequencing and functional analysis identifies BANF1 mutation as the cause of a hereditary progeroid syndrome. Am J Hum Genet. 2011;88:650–6. doi: 10.1016/j.ajhg.2011.04.010.] [[Google Scholar]
45. Park YJ, Luger KHistone chaperones in nucleosome eviction and histone exchange. Curr Opin Struct Biol. 2008;18:282–9. doi: 10.1016/j.sbi.2008.04.003.] [[Google Scholar]
46. Kim MY, Mauro S, Gevry N, Lis JT, Kraus WLNAD+-dependent modulation of chromatin structure and transcription by nucleosome binding properties of PARP-1. Cell. 2004;119:803–14. doi: 10.1016/j.cell.2004.11.002.] [[PubMed][Google Scholar]
47. Foltz DR, Jansen LE, Black BE, Bailey AO, Yates JR, 3rd, Cleveland DWThe human CENP-A centromeric nucleosome-associated complex. Nat Cell Biol. 2006;8:458–69. doi: 10.1038/ncb1397.] [[PubMed][Google Scholar]
48. Luger K, Möder AW, Richmond RK, Sargent DF, Richmond TJCrystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 1997;389:251–60. doi: 10.1038/38444.] [[PubMed][Google Scholar]
49. Umland TC, Wei S-Q, Craigie R, Davies DRStructural Basis of DNA Bridging by Barrier-to-Autointegration Factor. Biochemistry. 2000;39:9130–8. doi: 10.1021/bi000572w.] [[PubMed][Google Scholar]
50. Wiebe MS, Traktman PPoxviral B1 kinase overcomes barrier to autointegration factor, a host defense against virus replication. Cell Host Microbe. 2007;1:187–97. doi: 10.1016/j.chom.2007.03.007.] [[Google Scholar]
51. Bolden JE, Peart MJ, Johnstone RWAnticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov. 2006;5:769–84. doi: 10.1038/nrd2133.] [[PubMed][Google Scholar]
52. Haraguchi T, Koujin T, Osakada H, Kojidani T, Mori C, Masuda H, et al Nuclear localization of barrier-to-autointegration factor is correlated with progression of S phase in human cells. J Cell Sci. 2007;120:1967–77. doi: 10.1242/jcs.03461.] [[PubMed][Google Scholar]
53. Andreassen PR, Margolis RLMicrotubule dependency of p34cdc2 inactivation and mitotic exit in mammalian cells. J Cell Biol. 1994;127:789–802. doi: 10.1083/jcb.127.3.789.] [[Google Scholar]
54. Davis FM, Tsao TY, Fowler SK, Rao PNMonoclonal antibodies to mitotic cells. Proc Natl Acad Sci USA. 1983;80:2926–30. doi: 10.1073/pnas.80.10.2926.] [[Google Scholar]
55. Nowak SJ, Pai CY, Corces VGProtein phosphatase 2A activity affects histone H3 phosphorylation and transcription in Drosophila melanogaster. Mol Cell Biol. 2003;23:6129–38. doi: 10.1128/MCB.23.17.6129-6138.2003.] [[Google Scholar]
56. Tachibana M, Sugimoto K, Fukushima T, Shinkai YSet 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. 2001;276:25309–17. doi: 10.1074/jbc.M101914200.] [[PubMed][Google Scholar]
57. Taverna SD, Li H, Ruthenburg AJ, Allis CD, Patel DJHow chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat Struct Mol Biol. 2007;14:1025–40. doi: 10.1038/nsmb1338.] [[Google Scholar]
58. Gant TM, Harris CA, Wilson KLRoles of LAP2 proteins in nuclear assembly and DNA replication: truncated LAP2beta proteins alter lamina assembly, envelope formation, nuclear size and DNA replication efficiency in Xenopus laevis extracts. J Cell Biol. 1999;144:1083–96. doi: 10.1083/jcb.144.6.1083.] [[Google Scholar]
59. Zhou J, Chau C, Deng Z, Stedman W, Lieberman PMEpigenetic control of replication origins. Cell Cycle. 2005;4:889–92. doi: 10.4161/cc.4.7.1823.] [[PubMed][Google Scholar]
60. Cayrou C, Coulombe P, Mechali MProgramming DNA replication origins and chromosome organization. Chromosome Res. 2010;18:137–45. doi: 10.1007/s10577-009-9105-3.] [[PubMed][Google Scholar]
61. Jørgensen S, Elvers I, Trelle MB, Menzel T, Eskildsen M, Jensen ON, et al The histone methyltransferase SET8 is required for S-phase progression. J Cell Biol. 2007;179:1337–45. doi: 10.1083/jcb.200706150.] [[Google Scholar]
62. Tardat M, Murr R, Herceg Z, Sardet C, Julien EPR-Set7-dependent lysine methylation ensures genome replication and stability through S phase. J Cell Biol. 2007;179:1413–26. doi: 10.1083/jcb.200706179.] [[Google Scholar]
63. Li G, Sudlow G, Belmont ASInterphase cell cycle dynamics of a late-replicating, heterochromatic homogeneously staining region: precise choreography of condensation/decondensation and nuclear positioning. J Cell Biol. 1998;140:975–89. doi: 10.1083/jcb.140.5.975.] [[Google Scholar]
64. Widrow RJ, Hansen RS, Kawame H, Gartler SM, Laird CDVery late DNA replication in the human cell cycle. Proc Natl Acad Sci USA. 1998;95:11246–50. doi: 10.1073/pnas.95.19.11246.] [[Google Scholar]
65. Herrera JE, West KL, Schiltz RL, Nakatani Y, Bustin MHistone H1 is a specific repressor of core histone acetylation in chromatin. Mol Cell Biol. 2000;20:523–9. doi: 10.1128/MCB.20.2.523-529.2000.] [[Google Scholar]
66. Lim JH, West KL, Rubinstein Y, Bergel M, Postnikov YV, Bustin MChromosomal protein HMGN1 enhances the acetylation of lysine 14 in histone H3. EMBO J. 2005;24:3038–48. doi: 10.1038/sj.emboj.7600768.] [[Google Scholar]
67. Ueda T, Postnikov YV, Bustin MDistinct domains in high mobility group N variants modulate specific chromatin modifications. J Biol Chem. 2006;281:10182–7. doi: 10.1074/jbc.M600821200.] [[PubMed][Google Scholar]
68. Collins RE, Northrop JP, Horton JR, Lee DY, Zhang X, Stallcup MR, et al The ankyrin repeats of G9a and GLP histone methyltransferases are mono- and dimethyllysine binding modules. Nat Struct Mol Biol. 2008;15:245–50. doi: 10.1038/nsmb.1384.] [[Google Scholar]
69. Rai K, Jafri IF, Chidester S, James SR, Karpf AR, Cairns BR, et al Dnmt3 and G9a cooperate for tissue-specific development in zebrafish. J Biol Chem. 2010;285:4110–21. doi: 10.1074/jbc.M109.073676.] [[Google Scholar]
70. Mamada H, Takahashi N, Taira MInvolvement of an inner nuclear membrane protein, Nemp1, in Xenopus neural development through an interaction with the chromatin protein BAF. Dev Biol. 2009;327:497–507. doi: 10.1016/j.ydbio.2008.12.038.] [[PubMed][Google Scholar]
71. Wen B, Wu H, Shinkai Y, Irizarry RA, Feinberg APLarge histone H3 lysine 9 dimethylated chromatin blocks distinguish differentiated from embryonic stem cells. Nat Genet. 2009;41:246–50. doi: 10.1038/ng.297.] [[Google Scholar]
72. Sims RJ, 3rd, Nishioka K, Reinberg DHistone lysine methylation: a signature for chromatin function. Trends Genet. 2003;19:629–39. doi: 10.1016/j.tig.2003.09.007.] [[PubMed][Google Scholar]
73. Steger DJ, Lefterova MI, Ying L, Stonestrom AJ, Schupp M, Zhuo D, et al DOT1L/KMT4 recruitment and H3K79 methylation are ubiquitously coupled with gene transcription in mammalian cells. Mol Cell Biol. 2008;28:2825–39. doi: 10.1128/MCB.02076-07.] [[Google Scholar]
74. Pegoraro G, Kubben N, Wickert U, Gohler H, Hoffmann K, Misteli TAgeing-related chromatin defects through loss of the NURD complex. Nat Cell Biol. 2009;11:1261–7. doi: 10.1038/ncb1971.] [[Google Scholar]
75. Delbarre E, Tramier M, Coppey-Moisan M, Gaillard C, Courvalin JC, Buendia BThe truncated prelamin A in Hutchinson-Gilford progeria syndrome alters segregation of A-type and B-type lamin homopolymers. Hum Mol Genet. 2006;15:1113–22. doi: 10.1093/hmg/ddl026.] [[PubMed][Google Scholar]
76. Bengtsson L, Wilson KLBarrier-to-autointegration factor phosphorylation on Ser-4 regulates emerin binding to lamin A in vitro and emerin localization in vivo. Mol Biol Cell. 2006;17:1154–63. doi: 10.1091/mbc.E05-04-0356.] [[Google Scholar]
77. Clayton AL, Rose S, Barratt MJ, Mahadevan LCPhosphoacetylation of histone H3 on c-fos- and c-jun-associated nucleosomes upon gene activation. EMBO J. 2000;19:3714–26. doi: 10.1093/emboj/19.14.3714.] [[Google Scholar]
78. Wang AH, Bertos NR, Vezmar M, Pelletier N, Crosato M, Heng HH, et al HDAC4, a human histone deacetylase related to yeast HDA1, is a transcriptional corepressor. Mol Cell Biol. 1999;19:7816–27.[Google Scholar]
79. Andreassen PR, Skoufias DA, Margolis RLAnalysis of the spindle-assembly checkpoint in HeLa cells. Methods Mol Biol. 2004;281:213–25.[PubMed][Google Scholar]