Insight into the mechanism of nucleosome reorganization from histone mutants that suppress defects in the FACT histone chaperone

Genetics

Volumn 188, Issue 4, 2011, Pages 835-846

  McCullough, Laura ^a   Rawlins, Robert ^a   Olsen, Aileen ^a   Xin, Hua ^a   Stillman, David J ^a   Formosa, Tim ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; DIMER; FLUORESCENT DYE; GENOMIC DNA; HISTONE H2A; HISTONE H2B; PROTEIN SPT11; PROTEIN SPT16; PROTEIN SUBUNIT; RIBONUCLEOTIDE REDUCTASE; SACCHAROMYCES CEREVISIAE PROTEIN; TETRAMER; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA REPLICATION; FUNGAL STRAIN; GEL MOBILITY SHIFT ASSAY; GENE DELETION; GENE DUPLICATION; GENE LOCUS; GENE MUTATION; GENE REPLICATION; GENETIC TRANSCRIPTION; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; MOLECULAR DYNAMICS; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOSOME; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PURIFICATION; SACCHAROMYCES CEREVISIAE; WILD TYPE;

DNA-BINDING PROTEINS; ENDONUCLEASES; GENE EXPRESSION REGULATION, FUNGAL; GENE ORDER; HIGH MOBILITY GROUP PROTEINS; HISTONE CHAPERONES; HISTONES; MODELS, MOLECULAR; MUTANT PROTEINS; MUTATION; NUCLEOSOMES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTIONAL ELONGATION FACTORS;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 80051520840     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.111.128769     Document Type: Article

References (44)

1. Ahn, S. H., W. L. Cheung, J. Y. Hsu, R. L. Diaz, M. M. Smith, et al., 2005 Sterile 20 kinase phosphorylates histone H2B at serine 10 during hydrogen peroxide-induced apoptosis in S. cerevisiae. Cell 120: 25-36.
2. Belotserkovskaya, R., S. Oh, V. A. Bondarenko, G. Orphanides, V. M. Studitsky, et al., 2003 FACT facilitates transcriptiondependent nucleosome alteration. Science 301: 1090-1093.
3. Biswas, D., Y. Yu, M. Prall, T. Formosa, and D. J. Stillman, 2005 The yeast FACT complex has a role in transcriptional initiation. Mol. Cell. Biol. 25: 5812-5822.
4. Biswas, D., R. Dutta-Biswas, D. Mitra, Y. Shibata, B. D. Strahl, et al., 2006 Opposing roles for Set2 and yFACT in regulating TBP binding at promoters. EMBO J. 25: 4479-4489.
5. Biswas, D., S. Takahata, H. Xin, R. Dutta-Biswas, Y. Yu. et al., 2008 A role for Chd1 and Set2 in negatively regulating DNA replication in Saccharomyces cerevisiae. Genetics 178: 649-659.
6. Boeke, J. D., J. Trueheart, G. Natsoulis, and G. R. Fink, 1987 5-Fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol. 154: 164-175.
7. Brewster, N. K., G. C. Johnston, and R. A. Singer, 2001 A bipartite yeast SSRP1 analog comprised of Pob3 and Nhp6 proteins modulates transcription. Mol. Cell. Biol. 21: 3491-3502.
8. Christianson, T. W., R. S. Sikorski, M. Dante, J. H. Shero, and P. Hieter, 1992 Multifunctional yeast high-copy-number shuttle vectors. Gene 110: 119-122.
9. Clapier, C. R., and B. R. Cairns, 2009 The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 78: 273-304.
10. Clark-Adams, C. D., D. Norris, M. A. Osley, J. S. Fassler, and F. Winston, 1988 Changes in histone gene dosage alter transcription in yeast. Genes Dev. 2: 150-159.
11. David, L., W. Huber, M. Granovskaia, J. Toedling, C. J. Palm, et al., 2006 A high-resolution map of transcription in the yeast genome. Proc. Natl. Acad. Sci. USA 103: 5320-5325.
12. Dollard, C., S. L. Ricupero-Hovasse, G. Natsoulis, J. D. Boeke, and F. Winston, 1994 SPT10 and SPT21 are required for transcription of particular histone genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 14: 5223-5228.
13. Duina, A. A., A. Rufiange, J. Bracey, J. Hall, A. Nourani, et al., 2007 Evidence that the localization of the elongation factor Spt16 across transcribed genes is dependent upon histone H3 integrity in Saccharomyces cerevisiae. Genetics 177: 101-112.
14. Flaus, A., C. Rencurel, H. Ferreira, N. Wiechens and T. Owen- Hughes, 2004 Sin mutations alter inherent nucleosome mobility. EMBO J. 23: 343-353.
15. Formosa, T., 2008 FACT and the reorganized nucleosome. Mol. Biosyst. 4: 1085-1093.
16. Formosa, T., P. Eriksson, J. Wittmeyer, J. Ginn, Y. Yu, et al., 2001 Spt16-Pob3 and the HMG protein Nhp6 combine to form the nucleosome-binding factor SPN. EMBO J. 20: 3506-3517.
17. Formosa, T., S. Ruone, M. D. Adams, A. E. Olsen, P. Eriksson, et al., 2002 Defects in SPT16 or POB3 (yFACT) in Saccharomyces cerevisiae cause dependence on the Hir/Hpc pathway: polymerase passage may degrade chromatin structure. Genetics 162: 1557-1571.
18. Hainer, S. J., J. A. Pruneski, R. D. Mitchell, R. M. Monteverde, and J. A. Martens, 2010 Intergenic transcription causes repression by directing nucleosome assembly. Genes Dev. 25: 29-40.
19. Hess, D., and F. Winston, 2005 Evidence that Spt10 and Spt21 of Saccharomyces cerevisiae play distinct roles in vivo and functionally interact with MCB-binding factor, SCB-binding factor and Snf1. Genetics 170: 87-94.
20. Jamai, A., A. Puglisi, and M. Strubin, 2009 Histone chaperone spt16 promotes redeposition of the original h3-h4 histones evicted by elongating RNA polymerase. Mol. Cell 35: 377-383.
21. Kaplan, C. D., L. Laprade, and F. Winston, 2003 Transcription elongation factors repress transcription initiation from cryptic sites. Science 301: 1096-1099.
22. Libuda, D. E., and F. Winston, 2006 Amplification of histone genes by circular chromosome formation in Saccharomyces cerevisiae. Nature 443: 1003-1007.
23. Lolas, I. B., K. Himanen, J. T. Gronlund, C. Lynggaard, A. Houben, et al., 2010 The transcript elongation factor FACT affects Arabidopsis vegetative and reproductive development and genetically interacts with HUB1/2. Plant J. 61: 686-697.
24. Lycan, D., G. Mikesell, M. Bunger, and L. Breeden, 1994 Differential effects of Cdc68 on cell cycle-regulated promoters in Saccharomyces cerevisiae. Mol. Cell. Biol. 14: 7455-7465.
25. Malone, E. A., C. D. Clark, A. Chiang, and F. Winston, 1991 Mutation in SPT16/CDC68 suppress cis- and trans-acting mutations that affect promoter function in Saccharomyces cerevisiae. Mol. Cell. Biol. 11: 5710-5717.
26. Norris, D., and M. A. Osley, 1987 The two gene pairs encoding H2A and H2B play different roles in the Saccharomyces cerevisiae life cycle. Mol. Cell. Biol. 7: 3473-3481.
27. O'Donnell, A. F., N. K. Brewster, J. Kurniawan, L. V. Minard, G. C. Johnston, et al., 2004 Domain organization of the yeast histone chaperone FACT: the conserved N-terminal domain of FACT subunit Spt16 mediates recovery from replication stress. Nucleic Acids Res. 32: 5894-5906.
28. O'Donnell, A. F., J. R. Stevens, R. Kepkay, C. A. Barnes, G. C. Johnston, et al., 2009 New mutant versions of yeast FACT subunit Spt16 affect cell integrity. Mol. Genet. Genomics 282: 487-502.
29. Orphanides, G., G. LeRoy, C.-H. Chang, D. S. Luse, and D. Reinberg, 1998 FACT, a factor that facilitates transcript elongation through nucleosomes. Cell 92: 105-116.
30. Osley, M. A., 1991 The regulation of histone synthesis in the cell cycle. Annu. Rev. Biochem. 60: 827-861.
31. Osley, M. A., and D. Lycan, 1987 Trans-acting regulatory mutations that alter transcription of Saccharomyces cerevisiae histone genes. Mol. Cell. Biol. 7: 4204-4210.
32. Reinberg, D., and R. J. Sims III, 2006 de FACTo nucleosome dynamics. J. Biol. Chem. 281: 23297-23301.
33. Rhoades, A. R., S. Ruone, and T. Formosa, 2004 Structural features of nucleosomes reorganized by yeast FACT and its HMG box component, Nhp6. Mol. Cell. Biol. 24: 3907-3917.
34. Rowley, A., R. A. Singer, and G. Johnston, 1991 CDC68, a yeast gene that affects regulation of cell proliferation and transcription, encodes a protein with a highly acidic carboxyl terminus. Mol. Cell. Biol. 11: 5718-5726.
35. Ruone, S., A. R. Rhoades, and T. Formosa, 2003 Multiple Nhp6 molecules are required to recruit Spt16-Pob3 to form yFACT complexes and reorganize nucleosomes. J. Biol. Chem. 278: 45288-45295.
36. Sikorski, R. S., and P. Hieter, 1989 A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.
37. Simchen, G., F. Winston, C. A. Styles, and G. R. Fink, 1984 Tymediated gene expression of the LYS2 and HIS4 genes of Saccharomyces cerevisiae is controlled by the same SPT genes. Proc. Natl. Acad. Sci. USA 81: 2431-2434.
38. Toulmay, A., and R. Schneiter, 2006 A two-step method for the introduction of single or multiple defined point mutations into the genome of Saccharomyces cerevisiae. Yeast 23: 825-831.
39. VanDemark, A. P., M. Blanksma, E. Ferris, A. Heroux, C. P. Hill, et al., 2006 The structure of the yFACT Pob3-M domain, its interaction with the DNA replication factor RPA, and a potential role in nucleosome deposition. Mol. Cell 22: 363-374.
40. VanDemark, A. P., H. Xin, L. McCullough, R. Rawlins, S. Bentley, et al., 2008 Structural and functional analysis of the Spt16p N-terminal domain reveals overlapping roles of yFACT subunits. J. Biol. Chem. 283: 5058-5068.
41. White, C. L., R. K. Suto, and K. Luger, 2001 Structure of the yeast nucleosome core particle reveals fundamental changes in internucleosome interactions. EMBO J. 20: 5207-5218.
42. Winkler, D. D., and K. Luger, 2011 The histone chaperone FACT: structural insights and mechanisms for nucleosome reorganization. J. Biol. Chem. 286: 18369-18374.
43. Xin, H., S. Takahata, M. Blanksma, L. McCullough, D. J. Stillman, et al., 2009 yFACT induces global accessibility of nucleosomal DNA without H2A-H2B displacement. Mol. Cell 35: 365-376.
44. Xu, H., U. J. Kim, T. Schuster, and M. Grunstein, 1992 Identification of a new set of cell cycle-regulatory genes that regulate S-phase transcription of histone genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 12: 5249-5259.