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Science 7 June 1996:
Vol. 272. no. 5267, pp. 1473 - 1476
DOI: 10.1126/science.272.5267.1473
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Reports

Evidence That Spt6p Controls Chromatin Structure by a Direct Interaction with Histones

Alex Bortvin and Fred Winston *

Genetic analysis has implicated SPT6, an essential gene of Saccharomyces cerevisiae, in the control of chromatin structure. Mutations in SPT6 and particular mutations in histone genes are able to overcome transcriptional defects in strains lacking the Snf/Swi protein complex. Here it is shown that an spt6 mutation causes changes in chromatin structure in vivo. In addition, both in vivo and in vitro experiments provide evidence that Spt6p interacts directly with histones and primarily with histone H3. Consistent with these findings, Spt6p is capable of nucleosome assembly in vitro.

Department of Genetics, Harvard Medical School, 200 Longwood Avenue, Boston, MA 02115, USA.
* To whom correspondence should be addressed.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Uncoupling of the Patterns of Chromatin Association of Different Transcription Elongation Factors by a Histone H3 Mutant in Saccharomyces cerevisiae.
A. Lloyd, K. Pratt, E. Siebrasse, M. D. Moran, and A. A. Duina (2009)
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The Iws1:Spt6:CTD complex controls cotranscriptional mRNA biosynthesis and HYPB/Setd2-mediated histone H3K36 methylation.
S. M. Yoh, J. S. Lucas, and K. A. Jones (2008)
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Roles for Ctk1 and Spt6 in Regulating the Different Methylation States of Histone H3 Lysine 36.
M. L. Youdell, K. O. Kizer, E. Kisseleva-Romanova, S. M. Fuchs, E. Duro, B. D. Strahl, and J. Mellor (2008)
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Altered Dosage and Mislocalization of Histone H3 and Cse4p Lead to Chromosome Loss in Saccharomyces cerevisiae.
W.-C. Au, M. J. Crisp, S. Z. DeLuca, O. J. Rando, and M. A. Basrai (2008)
Genetics 179, 263-275
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Spn1 Regulates the Recruitment of Spt6 and the Swi/Snf Complex during Transcriptional Activation by RNA Polymerase II.
L. Zhang, A. G. L. Fletcher, V. Cheung, F. Winston, and L. A. Stargell (2008)
Mol. Cell. Biol. 28, 1393-1403
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P-TEFb Is Critical for the Maturation of RNA Polymerase II into Productive Elongation In Vivo.
Z. Ni, A. Saunders, N. J. Fuda, J. Yao, J.-R. Suarez, W. W. Webb, and J. T. Lis (2008)
Mol. Cell. Biol. 28, 1161-1170
   Abstract »    Full Text »    PDF »
The Spt6 SH2 domain binds Ser2-P RNAPII to direct Iws1-dependent mRNA splicing and export.
S. M. Yoh, H. Cho, L. Pickle, R. M. Evans, and K. A. Jones (2007)
Genes & Dev. 21, 160-174
   Abstract »    Full Text »    PDF »
Global Replication-Independent Histone H4 Exchange in Budding Yeast.
J. Linger and J. K. Tyler (2006)
Eukaryot. Cell 5, 1780-1787
   Abstract »    Full Text »    PDF »
de FACTo Nucleosome Dynamics.
D. Reinberg and R. J. Sims III (2006)
J. Biol. Chem. 281, 23297-23301
   Abstract »    Full Text »    PDF »
Nucleosome displacement in transcription.
J. L. Workman (2006)
Genes & Dev. 20, 2009-2017
   Abstract »    Full Text »    PDF »
Presenilin-Based Genetic Screens in Drosophila melanogaster Identify Novel Notch Pathway Modifiers.
M. B. Mahoney, A. L. Parks, D. A. Ruddy, S. Y. K. Tiong, H. Esengil, A. C. Phan, P. Philandrinos, C. G. Winter, R. Chatterjee, K. Huppert, et al. (2006)
Genetics 172, 2309-2324
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Evidence that Spt2/Sin1, an HMG-Like Factor, Plays Roles in Transcription Elongation, Chromatin Structure, and Genome Stability in Saccharomyces cerevisiae.
A. Nourani, F. Robert, and F. Winston (2006)
Mol. Cell. Biol. 26, 1496-1509
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Identification and Characterization of Elf1, a Conserved Transcription Elongation Factor in Saccharomyces cerevisiae.
D. Prather, N. J. Krogan, A. Emili, J. F. Greenblatt, and F. Winston (2005)
Mol. Cell. Biol. 25, 10122-10135
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Partial Depletion of Histone H4 Increases Homologous Recombination-Mediated Genetic Instability.
F. Prado and A. Aguilera (2005)
Mol. Cell. Biol. 25, 1526-1536
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The Histone Chaperone TAF-I/SET/INHAT Is Required for Transcription In Vitro of Chromatin Templates.
M. J. Gamble, H. Erdjument-Bromage, P. Tempst, L. P. Freedman, and R. P. Fisher (2005)
Mol. Cell. Biol. 25, 797-807
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Interaction between Transcription Elongation Factors and mRNA 3'-End Formation at the Saccharomyces cerevisiae GAL10-GAL7 Locus.
C. D. Kaplan, M. J. Holland, and F. Winston (2005)
J. Biol. Chem. 280, 913-922
   Abstract »    Full Text »    PDF »
Evidence for Eviction and Rapid Deposition of Histones upon Transcriptional Elongation by RNA Polymerase II.
M. A. Schwabish and K. Struhl (2004)
Mol. Cell. Biol. 24, 10111-10117
   Abstract »    Full Text »    PDF »
Elongation by RNA polymerase II: the short and long of it.
R. J. Sims III, R. Belotserkovskaya, and D. Reinberg (2004)
Genes & Dev. 18, 2437-2468
   Abstract »    Full Text »    PDF »
Human Spt6 Stimulates Transcription Elongation by RNA Polymerase II In Vitro.
M. Endoh, W. Zhu, J. Hasegawa, H. Watanabe, D.-K. Kim, M. Aida, N. Inukai, T. Narita, T. Yamada, A. Furuya, et al. (2004)
Mol. Cell. Biol. 24, 3324-3336
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Bur1 Kinase Is Required for Efficient Transcription Elongation by RNA Polymerase II.
M.-C. Keogh, V. Podolny, and S. Buratowski (2003)
Mol. Cell. Biol. 23, 7005-7018
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Involvement of Nucleocytoplasmic Shuttling of Yeast Nap1 in Mitotic Progression.
M. Miyaji-Yamaguchi, K. Kato, R. Nakano, T. Akashi, A. Kikuchi, and K. Nagata (2003)
Mol. Cell. Biol. 23, 6672-6684
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Transcription Initiation Factor IID-interactive Histone Chaperone CIA-II Implicated in Mammalian Spermatogenesis.
T. Umehara and M. Horikoshi (2003)
J. Biol. Chem. 278, 35660-35667
   Abstract »    Full Text »    PDF »
Tracking FACT and the RNA Polymerase II Elongation Complex Through Chromatin in Vivo.
A. Saunders, J. Werner, E. D. Andrulis, T. Nakayama, S. Hirose, D. Reinberg, and J. T. Lis (2003)
Science 301, 1094-1096
   Abstract »    Full Text »    PDF »
Transcription Elongation Factors Repress Transcription Initiation from Cryptic Sites.
C. D. Kaplan, L. Laprade, and F. Winston (2003)
Science 301, 1096-1099
   Abstract »    Full Text »    PDF »
Multiple Roles for Saccharomyces cerevisiae Histone H2A in Telomere Position Effect, Spt Phenotypes and Double-Strand-Break Repair.
H. R. Wyatt, H. Liaw, G. R. Green, and A. J. Lustig (2003)
Genetics 164, 47-64
   Abstract »    Full Text »    PDF »
Dual Roles for Spt5 in Pre-mRNA Processing and Transcription Elongation Revealed by Identification of Spt5-Associated Proteins.
D. L. Lindstrom, S. L. Squazzo, N. Muster, T. A. Burckin, K. C. Wachter, C. A. Emigh, J. A. McCleery, J. R. Yates III, and G. A. Hartzog (2003)
Mol. Cell. Biol. 23, 1368-1378
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Defects in SPT16 or POB3 (yFACT) in Saccharomyces cerevisiae Cause Dependence on the Hir/Hpc Pathway: Polymerase Passage May Degrade Chromatin Structure.
T. Formosa, S. Ruone, M. D. Adams, A. E. Olsen, P. Eriksson, Y. Yu, A. R. Rhoades, P. D. Kaufman, and D. J. Stillman (2002)
Genetics 162, 1557-1571
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SPN1, a Conserved Gene Identified by Suppression of a Postrecruitment-Defective Yeast TATA-Binding Protein Mutant.
J. A. Fischbeck, S. M. Kraemer, and L. A. Stargell (2002)
Genetics 162, 1605-1616
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Novel domains and orthologues of eukaryotic transcription elongation factors.
C. P. Ponting (2002)
Nucleic Acids Res. 30, 3643-3652
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dELL is an essential RNA polymerase II elongation factor with a general role in development.
J. C. Eissenberg, J. Ma, M. A. Gerber, A. Christensen, J. A. Kennison, and A. Shilatifard (2002)
PNAS 99, 9894-9899
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Identification and characterization of CIA/ASF1 as an interactor of bromodomains associated with TFIID.
T. Chimura, T. Kuzuhara, and M. Horikoshi (2002)
PNAS 99, 9334-9339
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The elongation factors Pandora/Spt6 and Foggy/Spt5 promote transcription in the zebrafish embryo.
B. R. Keegan, J. L. Feldman, D. H. Lee, D. S. Koos, R. K. Ho, D. Y. R. Stainier, and D. Yelon (2002)
Development 129, 1623-1632
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Genetic Regulation of Cardiac Patterning in Zebrafish.
D. YELON, J.L. FELDMAN, and B.R. KEEGAN (2002)
Cold Spring Harb Symp Quant Biol 67, 19-26
   Abstract »    PDF »
Systematic Identification of Novel Protein Domain Families Associated with Nuclear Functions.
T. Doerks, R. R. Copley, J. Schultz, C. P. Ponting, and P. Bork (2002)
Genome Res. 12, 47-56
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Glucocorticoid Receptor Activation of the Ikappa Balpha Promoter within Chromatin.
B. J. Deroo and T. K. Archer (2001)
Mol. Biol. Cell 12, 3365-3374
   Abstract »    Full Text »    PDF »
Deletion of the CSB homolog, RAD26, yields Spt- strains with proficient transcription-coupled repair.
S. M. Gregory and K. S. Sweder (2001)
Nucleic Acids Res. 29, 3080-3086
   Abstract »    Full Text »    PDF »
Yeast spt6-140 Mutation, Affecting Chromatin and Transcription, Preferentially Increases Recombination in Which Rad51p-Mediated Strand Exchange Is Dispensable.
F. Malagon and A. Aguilera (2001)
Genetics 158, 597-611
   Abstract »    Full Text »    PDF »
A Bipartite Yeast SSRP1 Analog Comprised of Pob3 and Nhp6 Proteins Modulates Transcription.
N. K. Brewster, G. C. Johnston, and R. A. Singer (2001)
Mol. Cell. Biol. 21, 3491-3502
   Abstract »    Full Text »
Spt5 and Spt6 are associated with active transcription and have characteristics of general elongation factors in D. melanogaster.
C. D. Kaplan, J. R. Morris, C.-t. Wu, and F. Winston (2000)
Genes & Dev. 14, 2623-2634
   Abstract »    Full Text »
High-resolution localization of Drosophila Spt5 and Spt6 at heat shock genes in vivo: roles in promoter proximal pausing and transcription elongation.
E. D. Andrulis, E. Guzmán, P. Döring, J. Werner, and J. T. Lis (2000)
Genes & Dev. 14, 2635-2649
   Abstract »    Full Text »
Synthetic Lethal Interactions Suggest a Role for the Saccharomyces cerevisiae Rtf1 Protein in Transcription Elongation.
P. J. Costa and K. M. Arndt (2000)
Genetics 156, 535-547
   Abstract »    Full Text »
Functional Interaction between Pleiotropic Transactivator pUL69 of Human Cytomegalovirus and the Human Homolog of Yeast Chromatin Regulatory Protein SPT6.
M. Winkler, T. aus dem Siepen, and T. Stamminger (2000)
J. Virol. 74, 8053-8064
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Genetic Interactions between TFIIS and the Swi-Snf Chromatin-Remodeling Complex.
J. K. Davie and C. M. Kane (2000)
Mol. Cell. Biol. 20, 5960-5973
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Histone-Histone Interactions and Centromere Function.
L. Glowczewski, P. Yang, T. Kalashnikova, M. S. Santisteban, and M. M. Smith (2000)
Mol. Cell. Biol. 20, 5700-5711
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Functional Interaction of CCR4-NOT Proteins With TATAA-Binding Protein (TBP) and Its Associated Factors in Yeast.
V. Badarinarayana, Y.-C. Chiang, and C. L. Denis (2000)
Genetics 155, 1045-1054
   Abstract »    Full Text »
Domains in the SPT5 Protein That Modulate Its Transcriptional Regulatory Properties.
D. Ivanov, Y. T. Kwak, J. Guo, and R. B. Gaynor (2000)
Mol. Cell. Biol. 20, 2970-2983
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Nuclear Hormone Receptor Coregulators In Action: Diversity For Shared Tasks.
D. Robyr, A. P. Wolffe, and W. Wahli (2000)
Mol. Endocrinol. 14, 329-347
   Full Text »
CAF-1 and the inheritance of chromatin states: at the crossroads of DNA replication and repair.
P Ridgway and G Almouzni (2000)
J. Cell Sci. 113, 2647-2658
   Abstract »    PDF »
The Nuclear Actin-related Protein of Saccharomyces cerevisiae, Act3p/Arp4, Interacts with Core Histones.
M. Harata, Y. Oma, S. Mizuno, Y. W. Jiang, D. J. Stillman, and U. Wintersberger (1999)
Mol. Biol. Cell 10, 2595-2605
   Abstract »    Full Text »
Histone modification governs the cell cycle regulation of a replication-independent chromatin assembly pathway in Saccharomyces cerevisiae.
B. A. Altheim and M. C. Schultz (1999)
PNAS 96, 1345-1350
   Abstract »    Full Text »    PDF »
Follicle-Stimulating Hormone Promotes Histone H3 Phosphorylation on Serine-10.
D. A. DeManno, J. E. Cottom, M. P. Kline, C. A. Peters, E. T. Maizels, and M. Hunzicker-Dunn (1999)
Mol. Endocrinol. 13, 91-105
   Abstract »    Full Text »
The Yeast Protein Complex Containing Cdc68 and Pob3 Mediates Core-Promoter Repression Through the Cdc68 N-Terminal Domain.
D. R. H. Evans, N. K. Brewster, Q. Xu, A. Rowley, B. A. Altheim, G. C. Johnston, and R. A. Singer (1998)
Genetics 150, 1393-1405
   Abstract »    Full Text »
Sth1p, a Saccharomyces cerevisiae Snf2p/Swi2p Homolog, Is an Essential ATPase in RSC and Differs From Snf/Swi in Its Interactions With Histones and Chromatin-Associated Proteins.
J. Du, I. Nasir, B. K. Benton, M. P. Kladde, and B. C. Laurent (1998)
Genetics 150, 987-1005
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Core Histones and HIRIP3, a Novel Histone-Binding Protein, Directly Interact with WD Repeat Protein HIRA.
S. Lorain, J.-P. Quivy, F. Monier-Gavelle, C. Scamps, Y. Lécluse, G. Almouzni, and M. Lipinski (1998)
Mol. Cell. Biol. 18, 5546-5556
   Abstract »    Full Text »
Characterization of the CP Complex, an Abundant Dimer of Cdc68 and Pob3 Proteins That Regulates Yeast Transcriptional Activation and Chromatin Repression.
N. K. Brewster, G. C. Johnston, and R. A. Singer (1998)
J. Biol. Chem. 273, 21972-21979
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Nuclear Proteins Nut1p and Nut2p Cooperate To Negatively Regulate a Swi4p-Dependent lacZ Reporter Gene in Saccharomyces cerevisiae.
R. K. Tabtiang and I. Herskowitz (1998)
Mol. Cell. Biol. 18, 4707-4718
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Molecular Genetics of the RNA Polymerase II General Transcriptional Machinery.
M. Hampsey (1998)
Microbiol. Mol. Biol. Rev. 62, 465-503
   Abstract »    Full Text »    PDF »
DSIF, a novel transcription elongation factor that regulates RNA polymerase II processivity, is composed of human Spt4 and Spt5 homologs.
T. Wada, T. Takagi, Y. Yamaguchi, A. Ferdous, T. Imai, S. Hirose, S. Sugimoto, K. Yano, G. A. Hartzog, F. Winston, et al. (1998)
Genes & Dev. 12, 343-356
   Abstract »    Full Text »
Evidence that Spt4, Spt5, and Spt6 control transcription elongation by RNA polymerase II in Saccharomyces cerevisiae.
G. A. Hartzog, T. Wada, H. Handa, and F. Winston (1998)
Genes & Dev. 12, 357-369
   Abstract »    Full Text »
The SAGA of Spt Proteins and Transcriptional Analysis in Yeast: Past, Present, and Future.
F. WINSTON and P. SUDARSANAM (1998)
Cold Spring Harb Symp Quant Biol 63, 553-562
   Abstract »    PDF »
Regena (Rga), a Drosophila Homolog of the Global Negative Transcriptional Regulator CDC36 (NOT2) from Yeast, Modifies Gene Expression and Suppresses Position Effect Variegation.
(1998)
Genetics 148, 317-330
Factors Affecting Saccharomyces cerevisiae ADH2 Chromatin Remodeling and Transcription.
L. Verdone, F. Cesari, C. L. Denis, E. Di Mauro, and M. Caserta (1997)
J. Biol. Chem. 272, 30828-30834
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Estrogen-Dependent Transcriptional Activation and Vitellogenin Gene Memory.
R. S. Edinger, E. Mambo, and M. I. Evans (1997)
Mol. Endocrinol. 11, 1985-1993
   Abstract »    Full Text »    PDF »
The Groucho/Transducin-like Enhancer of split Transcriptional Repressors Interact with the Genetically Defined Amino-terminal Silencing Domain of Histone H3.
A. Palaparti, A. Baratz, and S. Stifani (1997)
J. Biol. Chem. 272, 26604-26610
   Abstract »    Full Text »    PDF »
Glc7p Protein Phosphatase Inhibits Expression of Glutamine-Fructose-6-phosphate Transaminase from GFA1.
J. Zheng, M. Khalil, and J. F. Cannon (2000)
J. Biol. Chem. 275, 18070-18078
   Abstract »    Full Text »    PDF »


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