The conformational flexibility of the C-terminus of histone H4 promotes histone octamer and nucleosome stability and yeast viability

Epigenetics and Chromatin

Volumn 5, Issue 1, 2012, Pages

  Chavez, Myrriah S ^a   Scorgie, Jean K ^b   Dennehey, Briana K ^a   Noone, Seth ^a   Tyler, Jessica K ^a   Churchill, Mair Ea ^b  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Anti silencing function 1 (Asf1); Histone H3 H4; Histone H4; Nucleosome; Saccharomyces cerevisiae

Indexed keywords

HISTONE H3; HISTONE H4; MICROCOCCAL NUCLEASE; OCTAMER TRANSCRIPTION FACTOR;

AMINO ACID SUBSTITUTION; ARTICLE; BIOACCUMULATION; CARBOXY TERMINAL SEQUENCE; CELL CYCLE PROGRESSION; CELL VIABILITY; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTALLIZATION; FLOW CYTOMETRY; FUNGAL STRAIN; GEL MOBILITY SHIFT ASSAY; GEL PERMEATION CHROMATOGRAPHY; IN VITRO STUDY; MOLECULAR DYNAMICS; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOSOME; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION; SUBSTITUTION REACTION; ULTRACENTRIFUGATION;

SACCHAROMYCES CEREVISIAE;

EID: 84866247042     PISSN: None     EISSN: 17568935     Source Type: Journal    
DOI: 10.1186/1756-8935-5-5     Document Type: Article

References (67)

1. Chromatin structure; oligomers of the histones. RD Kornberg, JO Thomas, Science 1974 184 865 868 10.1126/science.184.4139.865 4825888
2. H3.H4 tetramer directs DNA and core histone octamer assembly in the nucleosome core particle. JL Jorcano, A Ruiz-Carrillo, Biochemistry 1979 18 768 774 10.1021/bi00572a005 217424
3. Crystal structure of the nucleosome core particle at 2.8 resolution. K Luger, AW Mader, RK Richmond, DF Sargent, TJ Richmond, Nature 1997 389 251 260 10.1038/38444 9305837 (Pubitemid 27406632)
4. The nucleosome family: dynamic and growing. J Zlatanova, TC Bishop, JM Victor, V Jackson, K van Holde, Structure 2009 17 160 171 10.1016/j.str.2008.12. 016 19217387
5. Chaperoning histones during DNA replication and repair. M Ransom, BK Dennehey, JK Tyler, Cell 2010 140 183 195 10.1016/j.cell.2010.01.004 20141833
6. The role of chromatin during transcription. B Li, M Carey, JL Workman, Cell 2007 128 707 719 10.1016/j.cell.2007.01.015 17320508 (Pubitemid 46273570)
7. The histone shuffle: histone chaperones in an energetic dance. C Das, JK Tyler, MEA Churchill, Trends Biochem Sci 2010 35 476 489 10.1016/j.tibs.2010.04. 001 20444609
8. The biology of chromatin remodeling complexes. CR Clapier, BR Cairns, Annu Rev Biochem 2009 78 273 304 10.1146/annurev.biochem.77.062706.153223 19355820
9. Histone chaperones and nucleosome assembly. CW Akey, K Luger, Curr Opin Struct Biol 2003 13 6 14 10.1016/S0959-440X(03)00002-2 12581654 (Pubitemid 36170249)
10. Histone chaperones in nucleosome eviction and histone exchange. YJ Park, K Luger, Curr Opin Struct Biol 2008 18 282 289 10.1016/j.sbi.2008.04.003 18534842
11. Histone chaperones: 30 years from isolation to elucidation of the mechanisms of nucleosome assembly and disassembly. M Eitoku, L Sato, T Senda, M Horikoshi, Cell Mol Life Sci 2008 65 414 444 10.1007/s00018-007-7305-6 17955179 (Pubitemid 351214651)
12. The RCAF complex mediates chromatin assembly during DNA replication and repair. JK Tyler, CR Adams, SR Chen, R Kobayashi, RT Kamakaka, JT Kadonaga, Nature 1999 402 555 560 10.1038/990147 10591219
13. A human homologue of yeast anti-silencing factor has histone chaperone activity. T Munakata, N Adachi, N Yokoyama, T Kuzuhara, M Horikoshi, Genes Cells 2000 5 221 233 10.1046/j.1365-2443.2000.00319.x 10759893 (Pubitemid 30227844)
14. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. H Tagami, D Ray-Gallet, G Almouzni, Y Nakatani, Cell 2004 116 51 61 10.1016/S0092-8674(03)01064-X 14718166 (Pubitemid 38156183)
15. Human Asf1 regulates the flow of S phase histones during replicational stress. A Groth, D Ray-Gallet, JP Quivy, J Lukas, J Bartek, G Almouzni, Mol Cell 2005 17 301 311 10.1016/j.molcel.2004.12.018 15664198 (Pubitemid 40138623)
16. Functional conservation and specialization among eukaryotic anti-silencing function 1 histone chaperones. BA Tamburini, JJ Carson, MW Adkins, JK Tyler, Eukaryot Cell 2005 4 1583 1590 10.1128/EC.4.9.1583-1590.2005 16151251 (Pubitemid 41339113)
17. ASF1 binds to a heterodimer of histones H3 and H4: a two-step mechanism for the assembly of the H3-H4 heterotetramer on DNA. CM English, NK Maluf, B Tripet, ME Churchill, JK Tyler, Biochemistry 2005 44 13673 13682 10.1021/bi051333h 16229457 (Pubitemid 41507448)
18. The activity of the histone chaperone yeast Asf1 in the assembly and disassembly of histone H3/H4-DNA complexes. DC Donham, JK Scorgie, MEA Churchill, Nucleic Acids Res 2011 39 5449 5458 10.1093/nar/gkr097 21447559
19. Histone chaperone Asf1 is required for histone H3 lysine 56 acetylation, a modification associated with S phase in mitosis and meiosis. J Recht, T Tsubota, JC Tanny, RL Diaz, JM Berger, X Zhang, BA Garcia, J Shabanowitz, AL Burlingame, DF Hunt, PD Kaufman, CD Allis, Proc Natl Acad Sci U S A 2006 103 6988 6993 10.1073/pnas.0601676103 16627621
20. The histone chaperone anti-silencing function 1 stimulates the acetylation of newly synthesized histone H3 in S-phase. MW Adkins, JJ Carson, CM English, CJ Ramey, JK Tyler, J Biol Chem 2007 282 1334 1340 17107956 (Pubitemid 47076518)
21. Acetylation of lysine 56 of histone H3 catalyzed by RTT109 and regulated by ASF1 is required for replisome integrity. J Han, H Zhou, Z Li, RM Xu, Z Zhang, J Biol Chem 2007 282 28587 28596 10.1074/jbc.M702496200 17690098 (Pubitemid 47606001)
22. Histone H3-K56 acetylation is catalyzed by histone chaperone-dependent complexes. T Tsubota, CE Berndsen, JA Erkmann, CL Smith, L Yang, MA Freitas, JM Denu, PD Kaufman, Mol Cell 2007 25 703 712 10.1016/j.molcel.2007.02.006 17320445 (Pubitemid 46341923)
23. Structural basis for the histone chaperone activity of Asf1. CM English, MW Adkins, JJ Carson, ME Churchill, JK Tyler, Cell 2006 127 495 508 10.1016/j.cell.2006.08.047 17081973 (Pubitemid 44647420)
24. Structure and function of the histone chaperone CIA/ASF1 complexed with histones H3 and H4. R Natsume, M Eitoku, Y Akai, N Sano, M Horikoshi, T Senda, Nature 2007 446 338 341 10.1038/nature05613 17293877 (Pubitemid 46437114)
25. How is epigenetic information on chromatin inherited after DNA replication? Y Nakatani, H Tagami, E Shestakova, Ernst Schering Res Found Workshop 2006 57 89 96 10.1007/3-540-37633-X-5 16568950
26. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 resolution. CA Davey, DF Sargent, K Luger, AW Maeder, TJ Richmond, J Mol Biol 2002 319 1097 1113 10.1016/S0022-2836(02)00386-8 12079350 (Pubitemid 34729421)
27. Histone H3 N-terminal mutations allow hyperactivation of the yeast GAL1 genein vivo. RK Mann, M Grunstein, EMBO J 1992 11 3297 3306 1505519
28. All four core histone N-termini contain sequences required for the repression of basal transcription in yeast. F Lenfant, RK Mann, B Thomsen, X Ling, M Grunstein, EMBO J 1996 15 3974 3985 8670902 (Pubitemid 26289807)
29. Yeast histone H3 and H4 amino termini are important for nucleosome assemblyin vivoandin vitro: redundant and position-independent functions in assembly but not in gene regulation. X Ling, TA Harkness, MC Schultz, G Fisher-Adams, M Grunstein, Genes Dev 1996 10 686 699 10.1101/gad.10.6.686 8598296 (Pubitemid 26112423)
30. Continuous histone H2B and transcription-dependent histone H3 exchange in yeast cells outside of replication. A Jamai, RM Imoberdorf, M Strubin, Mol Cell 2007 25 345 355 10.1016/j.molcel.2007.01.019 17289583 (Pubitemid 46199292)
31. Histone H3 Thr 45 phosphorylation is a replication-associated post-translational modification in S. cerevisiae. SP Baker, J Phillips, S Anderson, Q Qiu, J Shabanowitz, MM Smith, JR Yates, DF Hunt, PA Grant, Nat Cell Biol 2010 12 294 298 20139971
32. A conserved patch near the C terminus of histone H4 is required for genome stability in budding yeast. Y Yu, M Srinivasan, S Nakanishi, J Leatherwood, A Shilatifard, R Sternglanz, Mol Cell Biol 2011 31 2311 2325 10.1128/MCB.01432-10 21444721
33. Probing nucleosome function: a highly versatile library of synthetic histone H3 and H4 mutants. J Dai, EM Hyland, DS Yuan, H Huang, JS Bader, JD Boeke, Cell 2008 134 1066 1078 10.1016/j.cell.2008.07.019 18805098
34. A comprehensive library of histone mutants identifies nucleosomal residues required for H3K4 methylation. S Nakanishi, BW Sanderson, KM Delventhal, WD Bradford, K Staehling-Hampton, A Shilatifard, Nat Struct Mol Biol 2008 15 881 888 10.1038/nsmb.1454 18622391
35. Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Q Li, H Zhou, H Wurtele, B Davies, B Horazdovsky, A Verreault, Z Zhang, Cell 2008 134 244 255 10.1016/j.cell.2008.06.018 18662540 (Pubitemid 352010333)
36. Chromatin disassembly mediated by the histone chaperone Asf1 is essential for transcriptional activation of the yeast PHO5 and PHO8 genes. MW Adkins, SR Howar, JK Tyler, Mol Cell 2004 14 657 666 10.1016/j.molcel.2004.05.016 15175160 (Pubitemid 38739087)
37. Reconstitution of nucleosome core particles from recombinant histones and DNA. PN Dyer, RS Edayathumangalam, CL White, Y Bao, S Chakravarthy, UM Muthurajan, K Luger, Methods Enzymol 2004 375 23 44 14870657 (Pubitemid 38124858)
38. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. PT Lowary, J Widom, J Mol Biol 1998 276 19 42 10.1006/jmbi.1997.1494 9514715 (Pubitemid 28085408)
39. The docking domain of histone H2A is required for H1 binding and RSC-mediated nucleosome remodeling. MS Shukla, SH Syed, D Goutte-Gattat, JL Ruichard, F Montel, A Hamiche, AA Travers, C Faivre-Moskalenko, J Bednar, JJ Hayes, D Angelov, S Dimitrov, Nucleic Acids Res 2011 39 2559 2570 10.1093/nar/gkq1174 21131284
40. Nucleosomes containing the histone variant H2A.Bbd organize only 118 base pairs of DNA. Y Bao, K Konesky, YJ Park, S Rosu, PN Dyer, D Rangasamy, DJ Tremethick, PJ Laybourn, K Luger, EMBO J 2004 23 3314 3324 10.1038/sj.emboj. 7600316 15257289 (Pubitemid 39209155)
41. A new fluorescence resonance energy transfer approach demonstrates that the histone variant H2AZ stabilizes the histone octamer within the nucleosome. YJ Park, PN Dyer, DJ Tremethick, K Luger, J Biol Chem 2004 279 24274 24282 10.1074/jbc.M313152200 15020582 (Pubitemid 38725289)
42. ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. T Ito, M Bulger, MJ Pazin, R Kobayashi, JT Kadonaga, Cell 1997 90 145 155 10.1016/S0092-8674(00)80321-9 9230310 (Pubitemid 28009426)
43. The chromatin-remodeling enzyme ACF is an ATP-dependent DNA length sensor that regulates nucleosome spacing. JG Yang, TS Madrid, E Sevastopoulos, GJ Narlikar, Nat Struct Mol Biol 2006 13 1078 1083 10.1038/nsmb1170 17099699 (Pubitemid 44885917)
44. Identification of residues in chromodomain helicase DNA-binding protein 1 (Chd1) required for coupling ATP hydrolysis to nucleosome sliding. A Patel, JN McKnight, P Genzor, GD Bowman, J Biol Chem 2011 286 43984 43993 10.1074/jbc.M111.282970 22039057
45. The histone chaperone Asf1p mediates global chromatin disassemblyin vivo. MW Adkins, JK Tyler, J Biol Chem 2004 279 52069 52074 10.1074/jbc.M406113200 15452122 (Pubitemid 39656578)
46. Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. R Driscoll, A Hudson, SP Jackson, Science 2007 315 649 652 10.1126/science.1135862 17272722 (Pubitemid 46214709)
47. Elevated histone expression promotes life span extension. J Feser, D Truong, C Das, JJ Carson, J Kieft, T Harkness, JK Tyler, Mol Cell 2010 39 724 35 10.1016/j.molcel.2010.08.015 20832724
48. Histone levels are regulated by phosphorylation and ubiquitylation- dependent proteolysis. RK Singh, MH Kabbaj, J Paik, A Gunjan, Nat Cell Biol 2009 11 925 933 10.1038/ncb1903 19578373
49. Sfh1p, a component of a novel chromatin-remodeling complex, is required for cell cycle progression. Y Cao, BR Cairns, RD Kornberg, BC Laurent, Mol Cell Biol 1997 17 3323 3334 9154831 (Pubitemid 27215047)
50. Amino acid substitutions in the structured domains of histones H3 and H4 partially relieve the requirement of the yeast SWI/SNF complex for transcription. W Kruger, CL Peterson, A Sil, C Coburn, G Arents, EN Moudrianakis, I Herskowitz, Genes Dev 1995 9 2770 2779 10.1101/gad.9.22.2770 7590252
51. Sin mutations alter inherent nucleosome mobility. A Flaus, C Rencurel, H Ferreira, N Wiechens, T Owen-Hughes, EMBO J 2004 23 343 353 10.1038/sj.emboj. 7600047 14726954 (Pubitemid 38294499)
52. Crystal structures of histone Sin mutant nucleosomes reveal altered protein-DNA interactions. UM Muthurajan, Y Bao, LJ Forsberg, RS Edayathumangalam, PN Dyer, CL White, K Luger, EMBO J 2004 23 260 271 10.1038/sj.emboj.7600046 14739929 (Pubitemid 38294491)
53. Extremely conserved histone H4 N terminus is dispensable for growth but essential for repressing the silent mating loci in yeast. PS Kayne, UJ Kim, M Han, JR Mullen, F Yoshizaki, M Grunstein, Cell 1988 55 27 39 10.1016/0092-8674(88)90006-2 3048701
54. Histone octamer functionin vivo: mutations in the dimer-tetramer interfaces disrupt both gene activation and repression. MS Santisteban, G Arents, EN Moudrianakis, MM Smith, EMBO J 1997 16 2493 2506 10.1093/emboj/16.9. 2493 9171362 (Pubitemid 27258645)
55. Insight into the mechanism of nucleosome reorganization from histone mutants that suppress defects in the FACT histone chaperone. L McCullough, R Rawlins, A Olsen, H Xin, DJ Stillman, T Formosa, Genetics 2011 188 835 846 10.1534/genetics.111.128769 21625001
56. Global analysis of core histones reveals nucleosomal surfaces required for chromosome bi-orientation. S Kawashima, Y Nakabayashi, K Matsubara, N Sano, T Enomoto, K Tanaka, M Seki, M Horikoshi, EMBO J 2011 30 3353 3367 10.1038/emboj.2011.241 21772248
57. Guide to yeast genetics and molecular biology. C Guthrie, JR Fink, Methods Enzymol 1991 194 1 863 2005781
58. Insights into the role of histone H3 and histone H4 core modifiable residues inSaccharomyces cerevisiae. EM Hyland, MS Cosgrove, H Molina, D Wang, A Pandey, RJ Cottee, JD Boeke, Mol Cell Biol 2005 25 10060 10070 10.1128/MCB.25.22.10060-10070.2005 16260619 (Pubitemid 41572751)
59. Sequence motifs and free energies of selected natural and non-natural nucleosome positioning DNA sequences. A Thastrom, PT Lowary, HR Widlund, H Cao, M Kubista, J Widom, J Mol Biol 1999 288 213 229 10.1006/jmbi.1999.2686 10329138 (Pubitemid 29209873)
60. Likelihood-enhanced fast rotation functions. LC Storoni, AJ McCoy, RJ Read, Acta Crystallogr 2004 D60 432 438 (Pubitemid 41087570)
61. Likelihood-enhanced fast translation functions. AJ McCoy, RW Grosse-Kunstleve, LC Storoni, RJ Read, Acta Crystallogr 2005 D61 458 464 (Pubitemid 43934606)
62. The CCP4 Suite-programs for protein crystallography. S Bailey, Acta Crystallogr 1994 D50 760 763
63. WL DeLano, The PyMOL Molecular Graphics System DeLano Scientific, Palo Alto, CA 2008
64. Structure of the histone chaperone ASF1 bound to the histone H3 C-terminal helix and functional insights. M Agez, J Chen, R Guerois, C van Heijenoort, JY Thuret, C Mann, F Ochsenbein, Structure 2007 15 191 199 10.1016/j.str.2007.01.002 17292837 (Pubitemid 46217867)
65. Elevated histone expression promotes life span extension. J Feser, D Truong, C Das, JJ Carson, J Kieft, T Harkness, JK Tyler, Mol Cell 2010 39 724 735 10.1016/j.molcel.2010.08.015 20832724
66. Preparation of nucleosome core particle from recombinant histones. K Luger, TJ Rechsteiner, TJ Richmond, Methods Enzymol 1999 304 3 19 10372352 (Pubitemid 29268874)
67. Chromatin assemblyin vitrowith purified recombinant ACF and NAP-1. DV Fyodorov, JT Kadonaga, Methods Enzymol 2003 371 499 515 14712724 (Pubitemid 37542753)