The C terminus of the histone chaperone Asf1 cross-links to histone H3 in yeast and promotes interaction with histones H3 and H4

Molecular and Cellular Biology

Volumn 33, Issue 3, 2013, Pages 605-621

  Dennehey, Briana K ^a   Noone, Seth ^b,c   Liu, Wallace H ^b   Smith, Luke ^b   Churchill, Mair E A ^b   Tyler, Jessica K ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

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

^c NATIONAL RENEWABLE ENERGY LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CHAPERONE; CHECKPOINT KINASE 2; FUNGAL PROTEIN; HISTONE H3; HISTONE H4;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CROSS LINKING; IMMUNOPRECIPITATION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE; YEAST;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CELL CYCLE PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; HISTONES; HUMANS; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; POINT MUTATION; PROTEIN INTERACTION MAPPING; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT;

EID: 84873054485     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01053-12     Document Type: Article

References (61)

1. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ. 1997. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389:251-260.
2. Ransom M, Dennehey BK, Tyler JK. 2010. Chaperoning histones during DNA replication and repair. Cell 140:183-195.
3. Le S, Davis C, Konopka JB, Sternglanz R. 1997. Two new S-phasespecific genes from Saccharomyces cerevisiae. Yeast 13:1029-1042.
4. Singer MS, Kahana A, Wolf AJ, Meisinger LL, Peterson SE, Goggin C, Mahowald M, Gottschling DE. 1998. Identification of high-copy disruptors of telomeric silencing in Saccharomyces cerevisiae. Genetics 150:613-632.
5. Tyler JK, Adams CR, Chen SR, Kobayashi R, Kamakaka RT, Kadonaga JT. 1999. The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature 402:555-560.
6. Adkins MW, Howar SR, Tyler JK. 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.
7. English CM, Adkins MW, Carson JJ, Churchill ME, Tyler JK. 2006. Structural basis for the histone chaperone activity of Asf1. Cell 127:495-508.
8. Natsume R, Eitoku M, Akai Y, Sano N, Horikoshi M, Senda T. 2007. Structure and function of the histone chaperone CIA/ASF1 complexed with histones H3 and H4. Nature 446:338-341.
9. Tyler JK, Collins KA, Prasad-Sinha J, Amiott E, Bulger M, Harte PJ, Kobayashi R, Kadonaga JT. 2001. Interaction between the Drosophila CAF-1 and ASF1 chromatin assembly factors. Mol. Cell Biol. 21:6574-6584.
10. Green EM, Antczak AJ, Bailey AO, Franco AA, Wu KJ, Yates JR, III, Kaufman PD. 2005. Replication-independent histone deposition by the HIR complex and Asf1. Curr. Biol. 15:2044-2049.
11. Emili A, Schieltz DM, Yates JR, III, Hartwell LH. 2001. Dynamic interaction of DNA damage checkpoint protein Rad53 with chromatin assembly factor Asf1. Mol. Cell 7:13-20.
12. Jiao Y, Seeger K, Lautrette A, Gaubert A, Mousson F, Guerois R, Mann C, Ochsenbein F. 2012. Surprising complexity of the Asf1 histone chaperone- Rad53 kinase interaction. Proc. Natl. Acad. Sci. U. S. A. 109:2866-2871.
13. Schwartz MF, Lee SJ, Duong JK, Eminaga S, Stern DF. 2003. FHA domain-mediated DNA checkpoint regulation of Rad53. Cell Cycle 2:384-396.
14. Sillje HH, Nigg EA. 2001. Identification of human Asf1 chromatin assembly factors as substrates of Tousled-like kinases. Curr. Biol. 11:1068-1073.
15. Daganzo SM, Erzberger JP, Lam WM, Skordalakes E, Zhang R, Franco AA, Brill SJ, Adams PD, Berger JM, Kaufman PD. 2003. Structure and function of the conserved core of histone deposition protein Asf1. Curr. Biol. 13:2148-2158.
16. Mousson F, Lautrette A, Thuret JY, Agez M, Courbeyrette R, Amigues B, Becker E, Neumann JM, Guerois R, Mann C, Ochsenbein F. 2005. Structural basis for the interaction of Asf1 with histone H3 and its functional implications. Proc. Natl. Acad. Sci. U. S. A. 102:5975-5980.
17. Padmanabhan B, Kataoka K, Adachi N, Horikoshi M. 2002. Purification, crystallization and preliminary X-ray diffraction analysis of yeast nucleosome-assembly factor Cia1p. Acta Crystallogr. D 58:1876-1878.
18. Umehara T, Chimura T, Ichikawa N, Horikoshi M. 2002. Polyanionic stretch-deleted histone chaperone cia1/Asf1p is functional both in vivo and in vitro. Genes Cells 7:59-73.
19. Franco AA, Lam WM, Burgers PM, Kaufman PD. 2005. Histone deposition protein Asf1 maintains DNA replisome integrity and interacts with replication factor C. Genes Dev. 19:1365-1375.
20. Minard LV, Williams JS, Walker AC, Schultz MC. 2011. Transcriptional regulation by Asf1: new mechanistic insights from studies of the DNA damage response to replication stress. J. Biol. Chem. 286:7082-7092.
21. Tamburini BA, Carson JJ, Linger JG, Tyler JK. 2006. Dominant mutants of the Saccharomyces cerevisiae ASF1 histone chaperone bypass the need for CAF-1 in transcriptional silencing by altering histone and Sir protein recruitment. Genetics 173:599-610.
22. Tamburini BA, Carson JJ, Adkins MW, Tyler JK. 2005. Functional conservation and specialization among eukaryotic anti-silencing function 1 histone chaperones. Eukaryot. Cell 4:1583-1590.
23. Pilyugin M, Demmers J, Verrijzer CP, Karch F, Moshkin YM. 2009. Phosphorylation-mediated control of histone chaperone ASF1 levels by Tousled-like kinases. PLoS One 4:e8328. doi:10.1371/journal.pone.0008328.
24. Chen CC, Carson JJ, Feser J, Tamburini B, Zabaronick S, Linger J, Tyler JK. 2008. Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 134:231-243.
25. Smolka MB, Albuquerque CP, Chen S-H, Schmidt KH, Wei XX, Kolodner RD, Zhou H. 2005. Dynamic changes in protein-protein interaction and protein phosphorylation probed with amine-reactive isotope tag. Mol. Cell. Proteomics 4:1358-1369.
26. Longtine MS, McKenzie A, III, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953-961.
27. Funakoshi M, Hochstrasser M. 2009. Small epitope-linker modules for PCR-based C-terminal tagging in Saccharomyces cerevisiae. Yeast 26:185-192.
28. Sikorski RS, Hieter P. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19-27.
29. Hyland EM, Cosgrove MS, Molina H, Wang D, Pandey A, Cottee RJ, Boeke JD. 2005. Insights into the role of histone H3 and histone H4 core modifiable residues in Saccharomyces cerevisiae. Mol. Cell. Biol. 25:10060-10070.
30. Ryu Y, Schultz PG. 2006. Efficient incorporation of unnatural amino acids into proteins in Escherichia coli. Nat. Methods 3:263-265.
31. English CM, Maluf NK, Tripet B, Churchill ME, Tyler JK. 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.
32. Chen H-T, Warfield L, Hahn S. 2007. The positions of TFIIF and TFIIE in theRNApolymerase II transcription preinitiation complex. Nat. Struct. Mol. Biol. 14:696-703.
33. Mann RK, Grunstein M. 1992. Histone H3 N-terminal mutations allow hyperactivation of the yeast GAL1 gene in vivo. EMBO J. 11:3297-3306.
34. Guthrie C, Fink GR. 1991. Guide to yeast genetics and molecular biology. Methods Enzymol. 194:1-863.
35. Chavez MS, Scorgie JK, Dennehey BK, Noone SM, Tyler JK, Churchill ME. 2012. The conformational flexibility of the C-terminus of histone H4 promotes histone octamer and nucleosome stability and yeast viability. Epigenetics Chromatin 5:5.
36. Donham DC, II, Scorgie JK, Churchill MEA. 2011. The activity of the histone chaperone yeast Asf1 in the assembly and disassembly of histone H3/H4-DNA complexes. Nucleic Acids Res. 39:5449-5458.
37. Luger K, Rechsteiner TJ, Richmond TJ. 1999. Expression and purification of recombinant histones and nucleosome reconstitution. Methods Mol. Biol. 119:1-16.
38. Chalkley RJ, Baker PR, Huang L, Hansen KC, Allen NP, Rexach M, Burlingame AL. 2005. Comprehensive analysis of a multidimensional liquid chromatography mass spectrometry dataset acquired on a quadrupole selecting, quadrupole collision cell, time-of-flight mass spectrometer. II. New developments in Protein Prospector allow for reliable and comprehensive automatic analysis of large datasets. Mol. Cell. Proteomics 4:1194-1204.
39. Chin JW, Cropp TA, Anderson JC, Mukherji M, Zhang Z, Schultz PG. 2003. An expanded eukaryotic genetic code. Science 301:964-967.
40. Tong AHY, Boone C. 2006. Synthetic genetic array analysis in Saccharomyces cerevisiae. Methods Mol. Biol. 313:171-192.
41. Pont-Kingdon G. 1994. Construction of chimeric molecules by a two-step recombinant PCR method. Biotechniques 16:1010-1011.
42. Sarkar G, Sommer SS. 1990. The "megaprimer" method of site-directed mutagenesis. Biotechniques 8:404-407.
43. Kinoshita E, Kinoshita-Kikuta E, Takiyama K, Koike T. 2006. Phosphate- binding tag, a new tool to visualize phosphorylated proteins. Mol. Cell. Proteomics 5:749-757.
44. Hellman U, Wernstedt C, Gonez J, Heldin CH. 1995. Improvement of an "in-gel" digestion procedure for the micropreparation of internal protein fragments for amino acid sequencing. Anal. Biochem. 224:451-455.
45. Rosenfeld J, Capdevielle J, Guillemot JC, Ferrara P. 1992. In-gel digestion of proteins for internal sequence analysis after one- or twodimensional gel electrophoresis. Anal. Biochem. 203:173-179.
46. Chalkley RJ, Baker PR, Hansen KC, Medzihradszky KF, Allen NP, Rexach M, Burlingame AL. 2005. Comprehensive analysis of a multidimensional liquid chromatography mass spectrometry dataset acquired on a quadrupole selecting, quadrupole collision cell, time-of-flight mass spectrometer. I. How much of the data is theoretically interpretable by search engines? Mol. Cell. Proteomics 4:1189-1193.
47. Rossmann MP, Luo W, Tsaponina O, Chabes A, Stillman B. 2011. A common telomeric gene silencing assay is affected by nucleotide metabolism. Mol. Cell 42:127-136.
48. Huang L-Y, Umanah G, Hauser M, Son C, Arshava B, Naider F, Becker JM. 2008. Unnatural amino acid replacement in a yeastGprotein-coupled receptor in its native environment. Biochemistry 47:5638-5648.
49. Mohibullah N, Hahn S. 2008. Site-specific cross-linking of TBP in vivo and in vitro reveals a direct functional interaction with the SAGA subunit Spt3. Genes Dev. 22:2994-3006.
50. Wittelsberger A, Mierke DF, Rosenblatt M. 2008. Mapping ligandreceptor interfaces: approaching the resolution limit of benzophenonebased photoaffinity scanning. Chem. Biol. Drug Des. 71:380-383.
51. Scorgie JK, Donham DC, III, Churchill ME. 2012. Analysis of histone chaperone antisilencing function 1 interactions. Methods Enzymol. 512: 223-241.
52. Johnston M, Riles L, Hegemann JH. 2002. Gene disruption. Methods Enzymol. 350:290-315.
53. Burgess RJ, Zhou H, Han J, Zhang Z. 2010. A role for Gcn5 in replication- coupled nucleosome assembly. Mol. Cell 37:469-480.
54. Li Q, Zhou H, Wurtele H, Davies B, Horazdovsky B, Verreault A, Zhang Z. 2008. Acetylation of histone H3 lysine 56 regulates replicationcoupled nucleosome assembly. Cell 134:244-255.
55. Zhang R, Poustovoitov MV, Ye X, Santos HA, Chen W, Daganzo SM, Erzberger JP, Serebriiskii IG, Canutescu AA, Dunbrack RL, Pehrson JR, Berger JM, Kaufman PD, Adams PD. 2005. Formation of MacroH2Acontaining senescence-associated heterochromatin foci and senescence driven by ASF1a and HIRA. Dev. Cell 8:19-30.
56. Kaufman PD, Cohen JL, Osley MA. 1998. Hir proteins are required for position-dependent gene silencing in Saccharomyces cerevisiae in the absence of chromatin assembly factor I. Mol. Cell. Biol. 18:4793-4806.
57. Kaufman PD, Kobayashi R, Stillman B. 1997. Ultraviolet radiation sensitivity and reduction of telomeric silencing in Saccharomyces cerevisiae cells lacking chromatin assembly factor-I. Genes Dev. 11:345-357.
58. Tang Y, Poustovoitov MV, Zhao K, Garfinkel M, Canutescu A, Dunbrack R, Adams PD, Marmorstein R. 2006. Structure of a human ASF1a- HIRA complex and insights into specificity of histone chaperone complex assembly. Nat. Struct. Mol. Biol. 13:921-929.
59. Malay AD, Umehara T, Matsubara-Malay K, Padmanabhan B, Yokoyama S. 2008. Crystal structures of fission yeast histone chaperone Asf1 complexed with the Hip1 B-domain or the Cac2 C terminus. J. Biol. Chem. 283:14022-14031.
60. Singh RK, Kabbaj M-HM, Paik J, Gunjan A. 2009. Histone levels are regulated by phosphorylation and ubiquitylation-dependent proteolysis. Nat. Cell Biol. 11:925-933.
61. Gupta SK, Kececioglu JD, Schaffer AA. 1995. Improving the practical space and time efficiency of the shortest-paths approach to sum-of-pairs multiple sequence alignment. J. Comput. Biol. 2:459-472.