Structure–function studies of histone H3/H4 tetramer maintenance during transcription by chaperone Spt2

Genes and Development

Volumn 29, Issue 12, 2015, Pages 1326-1340

  Chen, Shoudeng ^a   Rufiange, Anne ^b   Huang, Hongda ^a   Rajashankar, Kanagalaghatta R ^c,d   Nourani, Amine ^b   Patel, Dinshaw J ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b UNIVERSITÉ LAVAL   (Canada)

^c ARGONNE NATIONAL LABORATORY   (United States)

^d Department of Obstetrics Gynecology   (United States)

Author keywords

Epigenetics; H3; H4 tetramer; Histone chaperone; Histone maintenance; Spt2; Spurious transcription; Transcription elongation

Indexed keywords

CHAPERONE; HISTONE H3; HISTONE H4; HUMAN SUPPRESSOR OF TY INSERTIONS 2 CHAPERONE; RNA POLYMERASE; TETRAMER; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; HISTONE; INORGANIC SALT; MULTIPROTEIN COMPLEX; NONHISTONE PROTEIN; NUCLEOSOME; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEIN; SPT2 PROTEIN, HUMAN; SPT2 PROTEIN, S CEREVISIAE;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CHROMATIN STRUCTURE; COMPLEX FORMATION; CONTROLLED STUDY; CROSS LINKING; CRYSTAL STRUCTURE; HUMAN; HYDROGEN BOND; ISOTHERMAL TITRATION CALORIMETRY; LIGHT SCATTERING; MOLECULAR WEIGHT; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; STOICHIOMETRY; STRUCTURE ACTIVITY RELATION; CHEMICAL STRUCTURE; CHEMISTRY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PROTEIN QUATERNARY STRUCTURE; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE;

CHROMOSOMAL PROTEINS, NON-HISTONE; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; HISTONE CHAPERONES; HISTONES; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; NUCLEOSOMES; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN STRUCTURE, QUATERNARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SALTS; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSCRIPTION, GENETIC;

EID: 84933514672     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.261115.115     Document Type: Article

References (39)

1. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-KunstleveRW, et al. 2010. Phenix: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221.
2. Annunziato AT. 2005. Split decision: what happens to nucleosomesduringDNAreplication? J BiolChem280:12065-12068.
3. Avvakumov N, Nourani A, Cote J. 2011. Histone chaperones: modulators of chromatin marks. Mol Cell 41: 502-514.
4. Banks DD, Gloss LM. 2003. Equilibrium folding of the core histones: the H3-H4 tetramer is less stable than the H2A-H2B dimer. Biochemistry 42: 6827-6839.
5. Belotserkovskaya R, Oh S, Bondarenko VA, Orphanides G, Studitsky VM, Reinberg D. 2003. FACT facilitates transcription-dependent nucleosome alteration. Science 301: 1090-1093.
6. BhatW, Boutin G, Rufiange A, Nourani A. 2013. Casein kinase 2 associates with the yeast chromatin reassembly factor Spt2/ Sin1 to regulate its function in the repression of spurious transcription. Mol Cell Biol 33: 4198-4211.
7. Bowman A, Ward R,Wiechens N, Singh V, El-Mkami H, Norman DG,Owen-Hughes T. 2011. The histone chaperones Nap1 and Vps75 bind histones H3 and H4 in a tetrameric conformation. Mol Cell 41: 398-408.
8. Cheung V, Chua G, Batada NN, Landry CR, Michnick SW, Hughes TR, Winston F. 2008. Chromatin-and transcriptionrelated factors repress transcription from within coding regions throughout the Saccharomyces cerevisiae genome. PLoS Biol 6: e277.
9. Dion MF, Kaplan T, Kim M, Buratowski S, Friedman N, Rando OJ. 2007. Dynamics of replication-independent histone turnover in budding yeast. Science 315: 1405-1408.
10. Dyer PN, Edayathumangalam RS, White CL, Bao Y, Chakravarthy S, Muthurajan UM, Luger K. 2004. Reconstitution of nucleosome core particles from recombinant histones and DNA. Methods Enzymol 375: 23-44.
11. Elsasser SJ, Huang H, Lewis PW, Chin JW, Allis CD, Patel DJ. 2012. DAXX envelops a histone H3. 3-H4 dimer for H3. 3-specific recognition. Nature 491: 560-565.
12. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486-501.
13. English CM, Adkins MW, Carson JJ, Churchill ME, Tyler JK. 2006. Structural basis for the histone chaperone activity of Asf1. Cell 127: 495-508.
14. Jamai A, Puglisi A, Strubin M. 2009. Histone chaperone spt16 promotes redeposition of the original h3-h4 histones evicted by elongating RNA polymerase. Mol Cell 35: 377-383.
15. Kaplan CD, Laprade L, Winston F. 2003. Transcription elongation factors repress transcription initiation from cryptic sites. Science 301: 1096-1099.
16. Katan-Khaykovich Y, Struhl K. 2011. Splitting of H3-H4 tetramers at transcriptionally active genes undergoing dynamic histone exchange. Proc Natl Acad Sci 108: 1296-1301.
17. Kimura H, Cook PR. 2001. Kinetics of core histones in living human cells: little exchange of H3 and H4 and some rapid exchange of H2B. J Cell Biol 153: 1341-1353.
18. Kireeva ML, Walter W, Tchernajenko V, Bondarenko V, Kashlev M, Studitsky VM. 2002. Nucleosome remodeling induced by RNA polymerase II: loss of the H2A/H2B dimer during transcription. Mol Cell 9: 541-552.
19. KrugerW, Peterson CL, Sil A, Coburn C, Arents G, Moudrianakis EN, Herskowitz I. 1995. Amino acid substitutions in the structured domains of histones H3 and H4 partially relieve the requirement of the yeast SWI/SNF complex for transcription. Genes Dev 9: 2770-2779.
20. Liu CP, Xiong C,Wang M, Yu Z, Yang N, Chen P, Zhang Z, Li G, Xu RM. 2012. Structure of the variant histone H3. 3-H4 heterodimer in complex with its chaperone DAXX. Nat Struct Mol Biol 19: 1287-1292.
21. 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.
22. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
23. Murshudov GN, Vagin AA, Dodson EJ. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
24. 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.
25. Nourani A, Robert F, Winston F. 2006. Evidence that Spt2/Sin1, an HMG-like factor, plays roles in transcription elongation, chromatin structure, and genome stability in Saccharomyces cerevisiae. Mol Cell Biol 26: 1496-1509.
26. Orphanides G,Wu WH, Lane WS, Hampsey M, Reinberg D. 1999. The chromatin-specific transcription elongation factor FACT comprises human SPT16 and SSRP1 proteins. Nature 400: 284-288.
27. Osakabe A, Tachiwana H, Takaku M, Hori T, Obuse C, Kimura H, Fukagawa T, Kurumizaka H. 2013. Vertebrate Spt2 is a novel nucleolar histone chaperone that assists in ribosomal DNA transcription. J Cell Sci 126: 1323-1332.
28. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol, 276: 307-326.
29. Rufiange A, Jacques PE, Bhat W, Robert F, 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.
30. Sheldrick GM. 2010. Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr D Biol Crystallogr 66: 479-485.
31. Simchen G, Winston F, Styles CA, Fink GR. 1984. Ty-mediated gene expression of the LYS2 and HIS4 genes of Saccharomyces cerevisiae is controlled by the same SPT genes. Proc Natl Acad Sci 81: 2431-2434.
32. Smolle M, Workman JL. 2013. Transcription-associated histone modifications and cryptic transcription. Biochim Biophys Acta 1829: 84-97.
33. Sternberg PW, Stern MJ, Clark I, Herskowitz I. 1987. Activation of the yeast HO gene by release from multiple negative controls. Cell 48: 567-577.
34. Thebault P, Boutin G, Bhat W, Rufiange A, Martens J, Nourani A. 2011. Transcription regulation by the noncoding RNA SRG1 requires Spt2-dependent chromatin deposition in the wake of RNA polymerase II. Mol Cell Biol 31: 1288-1300.
35. Thiriet C, Hayes JJ. 2005. Replication-independent core histone dynamics at transcriptionally active loci in vivo. Genes Dev 19: 677-682.
36. Vagin A, Teplyakov A. 2010. Molecular replacement with MOLREP. Acta Crystallogr D Biol Crystallogr 66: 22-25.
37. Winston F, Chaleff DT, Valent B, Fink GR. 1984. Mutation affecting TY-mediated expression of the HIS4 gene of Saccharomyces cerevisiae. Genetics 107: 179-197.
38. Winston F, Dollard C, Ricupero-Hovasse SL. 1995. Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11: 53-55.
39. Xu M, Long C, Chen X, Huang C, Chen S, Zhu B. 2010. Partitioning of histone H3-H4 tetramers during DNA replication-dependent chromatin assembly. Science 328: 94-98.