The activity of the histone chaperone yeast Asf1 in the assembly and disassembly of histone H3/H4-DNA complexes

Nucleic Acids Research

Volumn 39, Issue 13, 2011, Pages 5449-5458

  Donham, Douglas C ^a   Scorgie, Jean K ^a   Churchill, Mair E A ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISILENCING FUNCTION 1 PROTEIN; CHAPERONE; DIMER; HISTONE H3; HISTONE H4; TETRAMER; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CHROMATIN ASSEMBLY AND DISASSEMBLY; COMPLEX FORMATION; CONTROLLED STUDY; DNA PROTEIN COMPLEX; DNA SEQUENCE; IONIC STRENGTH; NUCLEOSOME; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN PROCESSING; SACCHAROMYCES CEREVISIAE; XENOPUS LAEVIS;

ANIMALS; CELL CYCLE PROTEINS; DNA; HISTONES; HMGB1 PROTEIN; MOLECULAR CHAPERONES; NUCLEOSOMES; SACCHAROMYCES CEREVISIAE PROTEINS; XENOPUS LAEVIS;

SACCHAROMYCES CEREVISIAE;

EID: 80052247642     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr097     Document Type: Article

References (77)

1. Kornberg, R.D. (1977) Structure of chromatin. Annu. Rev. Biochem., 46, 931-954.
2. Jorcano, J.L. and Ruiz-Carrillo, A. (1979) H3.H4 tetramer directs DNA and core histone octamer assembly in the nucleosome core particle. Biochemistry, 18, 768-774.
3. Luger, K., Mader, A.W., Richmond, R.K., Sargent, D.F. and Richmond, T.J. (1997) Crystal structure of the nucleosome core particle at 2.8A resolution. Nature, 389, 251-260. (Pubitemid 27406632)
4. Clapier, C.R. and Cairns, B.R. (2009) The biology of chromatin remodeling complexes. Annu. Rev. Biochem., 78, 273-304.
5. Ransom, M., Dennehey, B.K. and Tyler, J.K. (2010) Chaperoning histones during DNA replication and repair. Cell, 140, 183-195.
6. Akey, C.W. and Luger, K. (2003) Histone chaperones and nucleosome assembly. Curr. Opin. Struct. Biol., 13, 6-14. (Pubitemid 36170249)
7. Park, Y.J. and Luger, K. (2008) Histone chaperones in nucleosome eviction and histone exchange. Curr. Opin. Struct. Biol., 18, 282-289.
8. Eitoku, M., Sato, L., Senda, T. and Horikoshi, M. (2008) Histone chaperones: 30 years from isolation to elucidation of the mechanisms of nucleosome assembly and disassembly. Cell. Mol. Life Sci., 65, 414-444. (Pubitemid 351214651)
9. Das, C., Tyler, J.K. and Churchill, M.E.A. (2010) The histone shuffle: histone chaperones in an energetic dance. Trends Biochem. Sci., 35, 476-489.
10. Le, S., Davis, C., Konopka, J.B. and Sternglanz, R. (1997) Two new S-phase-specific genes from Saccharomyces cerevisiae. Yeast, 13, 1029-1042. (Pubitemid 27368513)
11. Singer, M.S., Kahana, A., Wolf, A.J., Meisinger, L.L., Peterson, S.E., Goggin, C., Mahowald, M. and Gottschling, D.E. (1998) Identification of high-copy disruptors of telomeric silencing in Saccharomyces cerevisiae. Genetics, 150, 613-632. (Pubitemid 28463040)
12. Sutton, A., Bucaria, J., Osley, M.A. and Sternglanz, R. (2001) Yeast ASF1 protein is required for cell cycle regulation of histone gene transcription. Genetics, 158, 587-596. (Pubitemid 32552299)
13. Sharp, J.A., Fouts, E.T., Krawitz, D.C. and Kaufman, P.D. (2001) Yeast histone deposition protein Asf1p requires Hir proteins and PCNA for heterochromatic silencing. Curr. Biol., 11, 463-473. (Pubitemid 32305025)
14. Adkins, M.W., Howar, S.R. and Tyler, J.K. (2004) Chromatin disassembly mediated by the histone chaperone Asf1 is essential for transcriptional activation of the yeast PHO5 and PHO8 genes. Mol. Cell, 14, 657-666. (Pubitemid 38739087)
15. Adkins, M.W. and Tyler, J.K. (2004) The histone chaperone Asf1p mediates global chromatin disassembly in vivo. J. Biol. Chem., 279, 52069-52074. (Pubitemid 39656578)
16. Ramey, C.J., Howar, S., Adkins, M., Linger, J., Spicer, J. and Tyler, J.K. (2004) Activation of the DNA damage checkpoint in yeast lacking the histone chaperone anti-silencing function 1. Mol. Cell. Biol., 24, 10313-10327. (Pubitemid 39507869)
17. Recht, J., Tsubota, T., Tanny, J.C., Diaz, R.L., Berger, J.M., Zhang, X., Garcia, B.A., Shabanowitz, J., Burlingame, A.L., Hunt, D.F. et al. (2006) Histone chaperone Asf1 is required for histone H3 lysine 56 acetylation, a modification associated with S phase in mitosis and meiosis. Proc. Natl Acad. Sci. USA, 103, 6988-6993.
18. Sanematsu, F., Takami, Y., Barman, H.K., Fukagawa, T., Ono, T., Shibahara, K. and Nakayama, T. (2006) Asf1 is required for viability and chromatin assembly during DNA replication in vertebrate cells. J. Biol. Chem., 281, 13817-13827. (Pubitemid 43855297)
19. Schwabish, M.A. and Struhl, K. (2006) Asf1 mediates histone eviction and deposition during elongation by RNA polymerase II. Mol. Cell, 22, 415-422.
20. Nakatani, Y., Ray-Gallet, D., Quivy, J.P., Tagami, H. and Almouzni, G. (2004) Two distinct nucleosome assembly pathways: dependent or independent of DNA synthesis promoted by histone H3.1 and H3.3 complexes. Cold Spring Harb. Symp. Quant. Biol., 69, 273-280. (Pubitemid 41056564)
21. Tyler, J.K., Adams, C.R., Chen, S.R., Kobayashi, R., Kamakaka, R.T. and Kadonaga, J.T. (1999) The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature, 402, 555-560.
22. Munakata, T., Adachi, N., Yokoyama, N., Kuzuhara, T. and Horikoshi, M. (2000) A human homologue of yeast antisilencing factor has histone chaperone activity. Genes Cells, 5, 221-233. (Pubitemid 30227844)
23. Tagami, H., Ray-Gallet, D., Almouzni, G. and Nakatani, Y. (2004) Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell, 116, 51-61. (Pubitemid 38156183)
24. Groth, A., Ray-Gallet, D., Quivy, J.P., Lukas, J., Bartek, J. and Almouzni, G. (2005) Human Asf1 regulates the flow of S phase histones during replicational stress. Mol. Cell, 17, 301-311. (Pubitemid 40138623)
25. Tamburini, B.A., Carson, J.J., Adkins, M.W. and Tyler, J.K. (2005) Functional conservation and specialization among eukaryotic anti-silencing function 1 histone chaperones. Eukaryot. Cell, 4, 1583-1590. (Pubitemid 41339113)
26. English, C.M., Adkins, M.W., Carson, J.J., Churchill, M.E. and Tyler, J.K. (2006) Structural basis for the histone chaperone activity of Asf1. Cell, 127, 495-508. (Pubitemid 44647420)
27. English, C.M., Maluf, N.K., Tripet, B., Churchill, M.E. and Tyler, J.K. (2005) ASF1 binds to a heterodimer of histones H3 and H4: a two-step mechanism for the assembly of the H3-H4 heterotetramer on DNA. Biochemistry, 44, 13673-13682. (Pubitemid 41507448)
28. Natsume, R., Eitoku, M., Akai, Y., Sano, N., Horikoshi, M. and Senda, T. (2007) Structure and function of the histone chaperone CIA/ASF1 complexed with histones H3 and H4. Nature, 446, 338-341. (Pubitemid 46437114)
29. Korber, P., Barbaric, S., Luckenbach, T., Schmid, A., Schermer, U.J., Blaschke, D. and Horz, W. (2006) The histone chaperone Asf1 increases the rate of histone eviction at the yeast PHO5 and PHO8 promoters. J. Biol. Chem., 281, 5539-5545. (Pubitemid 43847649)
30. Kim, H.J., Seol, J.H., Han, J.W., Youn, H.D. and Cho, E.J. (2007) Histone chaperones regulate histone exchange during transcription. EMBO J., 26, 4467-4474.
31. Williams, S.K. and Tyler, J.K. (2007) Transcriptional regulation by chromatin disassembly and reassembly. Curr. Opin. Genet. Dev., 17, 88-93. (Pubitemid 46551714)
32. Andrews, A.J., Chen, X., Zevin, A., Stargell, L.A. and Luger, K. (2010) The histone chaperone Nap1 promotes nucleosome assembly by eliminating nonnucleosomal histone DNA interactions. Mol. Cell, 37, 834-842.
33. Andrews, A.J., Downing, G., Brown, K., Park, Y.J. and Luger, K. (2008) A thermodynamic model for Nap1-histone interactions. J. Biol. Chem., 283, 32412-32418.
34. Thastrom, A., Lowary, P.T., Widlund, H.R., Cao, H., Kubista, M. and Widom, J. (1999) Sequence motifs and free energies of selected natural and non-natural nucleosome positioning DNA sequences. J. Mol. Biol., 288, 213-229. (Pubitemid 29209873)
35. Neumann, H., Hancock, S.M., Buning, R., Routh, A., Chapman, L., Somers, J., Owen-Hughes, T., van Noort, J., Rhodes, D. and Chin, J.W. (2009) A method for genetically installing site-specific acetylation in recombinant histones defines the effects of H3 K56 acetylation. Mol. Cell, 36, 153-163.
36. Das, C., Lucia, M.S., Hansen, K.C. and Tyler, J.K. (2009) CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature, 459, 113-117.
37. Williams, S.K., Truong, D. and Tyler, J.K. (2008) Acetylation in the globular core of histone H3 on lysine-56 promotes chromatin disassembly during transcriptional activation. Proc. Natl Acad. Sci. USA, 105, 9000-9005.
38. Lavelle, C. and Prunell, A. (2007) Chromatin polymorphism and the nucleosome superfamily: a genealogy. Cell Cycle, 6, 2113-2119. (Pubitemid 47450410)
39. Zlatanova, J., Bishop, T.C., Victor, J.M., Jackson, V. and van Holde, K. (2009) The nucleosome family: dynamic and growing. Structure, 17, 160-171.
40. Luger, K., Rechsteiner, T.J. and Richmond, T.J. (1999) Expression and purification of recombinant histones and nucleosome reconstitution. Method. Mol. Biol., 119, 1-16.
41. Dyer, P.N., Edayathumangalam, R.S., White, C.L., Bao, Y., Chakravarthy, S., Muthurajan, U.M. and Luger, K. (2004) Reconstitution of nucleosome core particles from recombinant histones and DNA. Methods Enzymol., 375, 23-44. (Pubitemid 38124858)
42. Roemer, S.C., Adelman, J., Churchill, M.E. and Edwards, D.P. (2008) Mechanism of high-mobility group protein B enhancement of progesterone receptor sequence-specific DNA binding. Nucleic Acids Res., 36, 3655-3666. (Pubitemid 351917529)
43. Lowary, P.T. and Widom, J. (1998) New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol., 276, 19-42. (Pubitemid 28085408)
44. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J., 78, 1606-1619. (Pubitemid 30141584)
45. Vistica, J., Dam, J., Balbo, A., Yikilmaz, E., Mariuzza, R.A., Rouault, T.A. and Schuck, P. (2004) Sedimentation equilibrium analysis of protein interactions with global implicit mass conservation constraints and systematic noise decomposition. Anal. Biochem., 326, 234-256. (Pubitemid 38293385)
46. Park, Y.J., Dyer, P.N., Tremethick, D.J. and Luger, K. (2004) A new fluorescence resonance energy transfer approach demonstrates that the histone variant H2AZ stabilizes the histone octamer within the nucleosome. J. Biol. Chem., 279, 24274-24282. (Pubitemid 38725289)
47. Alilat, M., Sivolob, A., Revet, B. and Prunell, A. (1999) Nucleosome dynamics. Protein and DNA contributions in the chiral transition of the tetrasome, the histone (H3-H4)2 tetramer-DNA particle. J. Mol. Biol., 291, 815-841. (Pubitemid 29403615)
48. Jackson, V. (1995) Preferential binding of histones H3 and H4 to highly positively coiled DNA. Biochemistry, 34, 10607-10619.
49. Somers, J. and Owen-Hughes, T. (2009) Mutations to the histone H3 alpha N region selectively alter the outcome of ATP-dependent nucleosome-remodelling reactions. Nucleic Acids Res., 37, 2504-2513.
50. Panetta, G., Buttinelli, M., Flaus, A., Richmond, T.J. and Rhodes, D. (1998) Differential nucleosome positioning on Xenopus oocyte and somatic 5S RNA genes determines both TFIIIA and H1 binding: a mechanism for selective H1 repression. J. Mol. Biol., 282, 683-697. (Pubitemid 28428861)
51. Peterson, S., Danowit, R., Wunsch, A. and Jackson, V. (2007) NAP1 catalyzes the formation of either positive or negative supercoils on DNA on basis of the dimer-tetramer equilibrium of histones H3/H4. Biochemistry, 46, 8634-8646. (Pubitemid 47106114)
52. Korber, P. and Horz, W. (2004) In vitro assembly of the characteristic chromatin organization at the yeast PHO5 promoter by a replication-independent extract system. J. Biol. Chem., 279, 35113-35120. (Pubitemid 39318148)
53. Rufiange, A., Jacques, P.E., Bhat, W., Robert, F. and Nourani, A. (2007) Genome-wide replication-independent histone H3 exchange occurs predominantly at promoters and implicates H3 K56 acetylation and Asf1. Mol. Cell, 27, 393-405. (Pubitemid 47135636)
54. Takahata, S., Yu, Y. and Stillman, D.J. (2009) FACT and Asf1 regulate nucleosome dynamics and coactivator binding at the HO promoter. Mol. Cell, 34, 405-415.
55. Bianchi, M.E. and Beltrame, M. (1998) Flexing DNA: HMG-box proteins and their partners. Am. J. Hum. Genet., 63, 1573-1577. (Pubitemid 30415718)
56. Thomas, J.O. and Travers, A.A. (2001) HMG1 and 2, and related 'architectural' DNA-binding proteins. Trends Biochem. Sci., 26, 167-174. (Pubitemid 32197576)
57. Travers, A. (2000) Recognition of distorted DNA structures by HMG domains. Curr. Opin. Struct. Biol., 10, 102-109. (Pubitemid 30099334)
58. Schroter, H. and Bode, J. (1982) The binding sites for large and small high-mobility-group (HMG) proteins. Studies on HMG-nucleosome interactions in vitro. Eur. J. Biochem., 127, 429-436.
59. Nightingale, K., Dimitrov, S., Reeves, R. and Wolffe, A.P. (1996) Evidence for a shared structural role for HMG1 and linker histones B4 and H1 in organizing chromatin. EMBO J., 15, 548-561. (Pubitemid 26044568)
60. An, W., van Holde, K. and Zlatanova, J. (1998) The non-histone chromatin protein HMG1 protects linker DNA on the side opposite to that protected by linker histones. J. Biol. Chem., 273, 26289-26291. (Pubitemid 28471628)
61. Karantza, V., Freire, E. and Moudrianakis, E.N. (1996) Thermodynamic studies of the core histones: pH and ionic strength effects on the stability of the (H3-H4)/(H3-H4)2 system. Biochemistry, 35, 2037-2046. (Pubitemid 26062654)
62. Banks, D.D. and Gloss, L.M. (2004) Folding mechanism of the (H3-H4)2 histone tetramer of the core nucleosome. Protein Sci., 13, 1304-1316. (Pubitemid 38526095)
63. Banks, D.D. and Gloss, L.M. (2003) Equilibrium folding of the core histones: the H3-H4 tetramer is less stable than the H2A-H2B dimer. Biochemistry, 42, 6827-6839. (Pubitemid 36666123)
64. Mazurkiewicz, J., Kepert, J.F. and Rippe, K. (2006) On the mechanism of nucleosome assembly by histone chaperone NAP1. J. Biol. Chem., 281, 16462-16472.
65. Mousson, F., Lautrette, A., Thuret, J.Y., Agez, M., Courbeyrette, R., Amigues, B., Becker, E., Neumann, J.M., Guerois, R., Mann, C. et al. (2005) Structural basis for the interaction of Asf1 with histone H3 and its functional implications. Proc. Natl Acad. Sci. USA, 102, 5975-5980. (Pubitemid 40594240)
66. Baxevanis, A.D., Godfrey, J.E. and Moudrianakis, E.N. (1991) Associative behavior of the histone (H3-H4)2 tetramer: dependence on ionic environment. Biochemistry, 30, 8817-8823.
67. Bowman, A., Ward, R., El-Mkami, H., Owen-Hughes, T. and Norman, D.G. (2010) Probing the (H3-H4)2 histone tetramer structure using pulsed EPR spectroscopy combined with site-directed spin labelling. Nucleic Acids Res., 38, 695-707.
68. Barman, H.K., Takami, Y., Nishijima, H., Shibahara, K., Sanematsu, F. and Nakayama, T. (2008) Histone acetyltransferase-1 regulates integrity of cytosolic histone H3-H4 containing complex. Biochem. Biophys. Res. Commun., 373, 624-630.
69. Benson, L.J., Gu, Y., Yakovleva, T., Tong, K., Barrows, C., Strack, C.L., Cook, R.G., Mizzen, C.A. and Annunziato, A.T. (2006) Modifications of H3 and H4 during chromatin replication, nucleosome assembly, and histone exchange. J. Biol. Chem., 281, 9287-9296. (Pubitemid 43864644)
70. Han, J., Zhou, H., Li, Z., Xu, R.M. and Zhang, Z. (2007) Acetylation of lysine 56 of histone H3 catalyzed by RTT109 and regulated by ASF1 is required for replisome integrity. J. Biol. Chem., 282, 28587-28596. (Pubitemid 47606001)
71. Fillingham, J., Recht, J., Silva, A.C., Suter, B., Emili, A., Stagljar, I., Krogan, N.J., Allis, C.D., Keogh, M.C. and Greenblatt, J.F. (2008) Chaperone control of the activity and specificity of the histone H3 acetyltransferase Rtt109. Mol. Cell. Biol., 28, 4342-4353. (Pubitemid 351904956)
72. Jasencakova, Z., Scharf, A.N., Ask, K., Corpet, A., Imhof, A., Almouzni, G. and Groth, A. (2010) Replication stress interferes with histone recycling and predeposition marking of new histones. Mol. Cell, 37, 736-743.
73. Schneider, J., Bajwa, P., Johnson, F.C., Bhaumik, S.R. and Shilatifard, A. (2006) Rtt109 is required for proper H3K56 acetylation: a chromatin mark associated with the elongating RNA polymerase II. J. Biol. Chem., 281, 37270-37274. (Pubitemid 46042030)
74. Adkins, M.W., Carson, J.J., English, C.M., Ramey, C.J. and Tyler, J.K. (2007) The histone chaperone anti-silencing function 1 stimulates the acetylation of newly synthesized histone H3 in S-phase. J. Biol. Chem., 282, 1334-1340. (Pubitemid 47076518)
75. Mello, J.A., Sillje, H.H., Roche, D.M., Kirschner, D.B., Nigg, E.A. and Almouzni, G. (2002) Human Asf1 and CAF-1 interact and synergize in a repair-coupled nucleosome assembly pathway. EMBO Rep., 3, 329-334. (Pubitemid 34467602)
76. Green, E.M., Antczak, A.J., Bailey, A.O., Franco, A.A., Wu, K.J., Yates, J.R. III and Kaufman, P.D. (2005) Replication-independent histone deposition by the HIR complex and Asf1. Curr. Biol., 15, 2044-2049. (Pubitemid 41654629)
77. Li, Q., Zhou, H., Wurtele, H., Davies, B., Horazdovsky, B., Verreault, A. and Zhang, Z. (2008) Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell, 134, 244-255. (Pubitemid 352010333)