Identification of a non-basic domain in the histone H4 N-terminus required for repression of the yeast silent mating loci. (original) (raw)

EMBO J. 1992 Jun; 11(6): 2201–2209.

Molecular Biology Institute, University of California, Los Angeles 90024.

Abstract

We have shown previously that a stretch of four charged residues (16-19) at the histone H4 N-terminus is involved in repression of the yeast silent mating loci. One of these residues, Lys16, is a site for acetylation, which may prevent repression of the silent mating loci. In this paper we ask whether other sequences in histone H4, possibly in conjunction with H3 residues, are required for repression. We find that even in combination, the other seven acetylatable lysines in H3 and H4 do not function in repression. In contrast, we have found that an adjacent relatively uncharged domain (residues 21-29) is required for repression and that single amino acid insertions and deletions in this region are extremely detrimental. We propose that the basic and non-basic domains together form a DNA (or protein) induced amphipathic alpha-helix required in the formation of a repressive chromatin structure.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (1.4M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

Allan J, Harborne N, Rau DC, Gould H. Participation of core histone "tails" in the stabilization of the chromatin solenoid. J Cell Biol. 1982 May;93(2):285–297. [PMC free article] [PubMed] [Google Scholar]
Annunziato AT, Frado LL, Seale RL, Woodcock CL. Treatment with sodium butyrate inhibits the complete condensation of interphase chromatin. Chromosoma. 1988;96(2):132–138. [PubMed] [Google Scholar]
Arents G, Burlingame RW, Wang BC, Love WE, Moudrianakis EN. The nucleosomal core histone octamer at 3.1 A resolution: a tripartite protein assembly and a left-handed superhelix. Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10148–10152. [PMC free article] [PubMed] [Google Scholar]
Bradbury EM, Rattle HW. Simple computer-aided approach for the analyses of the nuclear-magnetic-resonance spectra of histones. Fractions F1, Fsa1, F2B, cleaved halves of F2B and F2B-DNA. Eur J Biochem. 1972 May 23;27(2):270–281. [PubMed] [Google Scholar]
Brand AH, Micklem G, Nasmyth K. A yeast silencer contains sequences that can promote autonomous plasmid replication and transcriptional activation. Cell. 1987 Dec 4;51(5):709–719. [PubMed] [Google Scholar]
Buchman AR, Kimmerly WJ, Rine J, Kornberg RD. Two DNA-binding factors recognize specific sequences at silencers, upstream activating sequences, autonomously replicating sequences, and telomeres in Saccharomyces cerevisiae. Mol Cell Biol. 1988 Jan;8(1):210–225. [PMC free article] [PubMed] [Google Scholar]
Cary PD, Crane-Robinson C, Bradbury EM, Dixon GH. Effect of acetylation on the binding of N-terminal peptides of histone H4 to DNA. Eur J Biochem. 1982 Sep;127(1):137–143. [PubMed] [Google Scholar]
Chahal SS, Matthews HR, Bradbury EM. Acetylation of histone H4 and its role in chromatin structure and function. Nature. 1980 Sep 4;287(5777):76–79. [PubMed] [Google Scholar]
Chicoine LG, Schulman IG, Richman R, Cook RG, Allis CD. Nonrandom utilization of acetylation sites in histones isolated from Tetrahymena. Evidence for functionally distinct H4 acetylation sites. J Biol Chem. 1986 Jan 25;261(3):1071–1076. [PubMed] [Google Scholar]
Clark DJ, Hill CS, Martin SR, Thomas JO. Alpha-helix in the carboxy-terminal domains of histones H1 and H5. EMBO J. 1988 Jan;7(1):69–75. [PMC free article] [PubMed] [Google Scholar]
Couppez M, Martin-Ponthieu A, Sautière P. Histone H4 from cuttlefish testis is sequentially acetylated. Comparison with acetylation of calf thymus histone H4. J Biol Chem. 1987 Feb 25;262(6):2854–2860. [PubMed] [Google Scholar]
Cousens LS, Gallwitz D, Alberts BM. Different accessibilities in chromatin to histone acetylase. J Biol Chem. 1979 Mar 10;254(5):1716–1723. [PubMed] [Google Scholar]
Durrin LK, Mann RK, Kayne PS, Grunstein M. Yeast histone H4 N-terminal sequence is required for promoter activation in vivo. Cell. 1991 Jun 14;65(6):1023–1031. [PubMed] [Google Scholar]
Ebralidse KK, Grachev SA, Mirzabekov AD. A highly basic histone H4 domain bound to the sharply bent region of nucleosomal DNA. Nature. 1988 Jan 28;331(6154):365–367. [PubMed] [Google Scholar]
Feldman JB, Hicks JB, Broach JR. Identification of sites required for repression of a silent mating type locus in yeast. J Mol Biol. 1984 Oct 5;178(4):815–834. [PubMed] [Google Scholar]
Gottschling DE, Aparicio OM, Billington BL, Zakian VA. Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell. 1990 Nov 16;63(4):751–762. [PubMed] [Google Scholar]
Hebbes TR, Thorne AW, Crane-Robinson C. A direct link between core histone acetylation and transcriptionally active chromatin. EMBO J. 1988 May;7(5):1395–1402. [PMC free article] [PubMed] [Google Scholar]
Herskowitz I. A regulatory hierarchy for cell specialization in yeast. Nature. 1989 Dec 14;342(6251):749–757. [PubMed] [Google Scholar]
Hill CS, Thomas JO. Core histone-DNA interactions in sea urchin sperm chromatin. The N-terminal tail of H2B interacts with linker DNA. Eur J Biochem. 1990 Jan 12;187(1):145–153. [PubMed] [Google Scholar]
Hill CS, Martin SR, Thomas JO. A stable alpha-helical element in the carboxy-terminal domain of free and chromatin-bound histone H1 from sea urchin sperm. EMBO J. 1989 Sep;8(9):2591–2599. [PMC free article] [PubMed] [Google Scholar]
Johnson LM, Kayne PS, Kahn ES, Grunstein M. Genetic evidence for an interaction between SIR3 and histone H4 in the repression of the silent mating loci in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1990 Aug;87(16):6286–6290. [PMC free article] [PubMed] [Google Scholar]
Kayne PS, Kim UJ, Han M, Mullen JR, Yoshizaki F, Grunstein M. Extremely conserved histone H4 N terminus is dispensable for growth but essential for repressing the silent mating loci in yeast. Cell. 1988 Oct 7;55(1):27–39. [PubMed] [Google Scholar]
Lowary PT, Widom J. Higher-order structure of Saccharomyces cerevisiae chromatin. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8266–8270. [PMC free article] [PubMed] [Google Scholar]
Marvin KW, Yau P, Bradbury EM. Isolation and characterization of acetylated histones H3 and H4 and their assembly into nucleosomes. J Biol Chem. 1990 Nov 15;265(32):19839–19847. [PubMed] [Google Scholar]
McGhee JD, Rau DC, Charney E, Felsenfeld G. Orientation of the nucleosome within the higher order structure of chromatin. Cell. 1980 Nov;22(1 Pt 1):87–96. [PubMed] [Google Scholar]
Megee PC, Morgan BA, Mittman BA, Smith MM. Genetic analysis of histone H4: essential role of lysines subject to reversible acetylation. Science. 1990 Feb 16;247(4944):841–845. [PubMed] [Google Scholar]
Miller AM, Nasmyth KA. Role of DNA replication in the repression of silent mating type loci in yeast. Nature. 1984 Nov 15;312(5991):247–251. [PubMed] [Google Scholar]
Nasmyth KA. The regulation of yeast mating-type chromatin structure by SIR: an action at a distance affecting both transcription and transposition. Cell. 1982 Sep;30(2):567–578. [PubMed] [Google Scholar]
Nasmyth KA, Tatchell K, Hall BD, Astell C, Smith M. A position effect in the control of transcription at yeast mating type loci. Nature. 1981 Jan 22;289(5795):244–250. [PubMed] [Google Scholar]
Norton VG, Imai BS, Yau P, Bradbury EM. Histone acetylation reduces nucleosome core particle linking number change. Cell. 1989 May 5;57(3):449–457. [PubMed] [Google Scholar]
O'Neil KT, Hoess RH, DeGrado WF. Design of DNA-binding peptides based on the leucine zipper motif. Science. 1990 Aug 17;249(4970):774–778. [PubMed] [Google Scholar]
Park EC, Szostak JW. Point mutations in the yeast histone H4 gene prevent silencing of the silent mating type locus HML. Mol Cell Biol. 1990 Sep;10(9):4932–4934. [PMC free article] [PubMed] [Google Scholar]
Ridsdale JA, Hendzel MJ, Delcuve GP, Davie JR. Histone acetylation alters the capacity of the H1 histones to condense transcriptionally active/competent chromatin. J Biol Chem. 1990 Mar 25;265(9):5150–5156. [PubMed] [Google Scholar]
Rine J, Herskowitz I. Four genes responsible for a position effect on expression from HML and HMR in Saccharomyces cerevisiae. Genetics. 1987 May;116(1):9–22. [PMC free article] [PubMed] [Google Scholar]
Sarkar G, Sommer SS. The "megaprimer" method of site-directed mutagenesis. Biotechniques. 1990 Apr;8(4):404–407. [PubMed] [Google Scholar]
Schnell R, Rine J. A position effect on the expression of a tRNA gene mediated by the SIR genes in Saccharomyces cerevisiae. Mol Cell Biol. 1986 Feb;6(2):494–501. [PMC free article] [PubMed] [Google Scholar]
Shore D, Nasmyth K. Purification and cloning of a DNA binding protein from yeast that binds to both silencer and activator elements. Cell. 1987 Dec 4;51(5):721–732. [PubMed] [Google Scholar]
Shuman JD, Vinson CR, McKnight SL. Evidence of changes in protease sensitivity and subunit exchange rate on DNA binding by C/EBP. Science. 1990 Aug 17;249(4970):771–774. [PubMed] [Google Scholar]
Talanian RV, McKnight CJ, Kim PS. Sequence-specific DNA binding by a short peptide dimer. Science. 1990 Aug 17;249(4970):769–771. [PubMed] [Google Scholar]
Thorne AW, Kmiciek D, Mitchelson K, Sautiere P, Crane-Robinson C. Patterns of histone acetylation. Eur J Biochem. 1990 Nov 13;193(3):701–713. [PubMed] [Google Scholar]
Turner BM. Histone acetylation and control of gene expression. J Cell Sci. 1991 May;99(Pt 1):13–20. [PubMed] [Google Scholar]
Vidali G, Boffa LC, Bradbury EM, Allfrey VG. Butyrate suppression of histone deacetylation leads to accumulation of multiacetylated forms of histones H3 and H4 and increased DNase I sensitivity of the associated DNA sequences. Proc Natl Acad Sci U S A. 1978 May;75(5):2239–2243. [PMC free article] [PubMed] [Google Scholar]
Vidali G, Ferrari N, Pfeffer U. Histone acetylation: a step in gene activation. Adv Exp Med Biol. 1988;231:583–596. [PubMed] [Google Scholar]
Weiss MA, Ellenberger T, Wobbe CR, Lee JP, Harrison SC, Struhl K. Folding transition in the DNA-binding domain of GCN4 on specific binding to DNA. Nature. 1990 Oct 11;347(6293):575–578. [PubMed] [Google Scholar]
Whiteway M, Szostak JW. The ARD1 gene of yeast functions in the switch between the mitotic cell cycle and alternative developmental pathways. Cell. 1985 Dec;43(2 Pt 1):483–492. [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group