Abstract
The Drosophila nucleosome remodeling factor NURF utilizes the energy of ATP hydrolysis to perturb the structure of nucleosomes and facilitate binding of transcription factors. The ATPase activity of purified NURF is stimulated significantly more by nucleosomes than by naked DNA or histones alone, suggesting that NURF is able to recognize specific features of the nucleosome. Here, we show that the interaction between NURF and nucleosomes is impaired by proteolytic removal of the N-terminal histone tails and by chemical cross-linking of nucleosomal histones. The ATPase activity of NURF is also competitively inhibited by each of the four Drosophila histone tails expressed as GST fusion proteins. A similar inhibition is observed for a histone H4 tail substituted with glutamine at four conserved, acetylatable lysines. These findings indicate a novel role for the flexible histone tails in chromatin remodeling by NURF, and this role may, in part, be independent of histone acetylation.
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- Adams C. C., Workman J. L. Nucleosome displacement in transcription. Cell. 1993 Feb 12;72(3):305–308. doi: 10.1016/0092-8674(93)90109-4. [DOI] [PubMed] [Google Scholar]
- Arents G., Burlingame R. W., Wang B. C., Love W. E., Moudrianakis E. N. 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. doi: 10.1073/pnas.88.22.10148. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ausio J., Dong F., van Holde K. E. Use of selectively trypsinized nucleosome core particles to analyze the role of the histone "tails" in the stabilization of the nucleosome. J Mol Biol. 1989 Apr 5;206(3):451–463. doi: 10.1016/0022-2836(89)90493-2. [DOI] [PubMed] [Google Scholar]
- Ausio J., van Holde K. E. Histone hyperacetylation: its effects on nucleosome conformation and stability. Biochemistry. 1986 Mar 25;25(6):1421–1428. doi: 10.1021/bi00354a035. [DOI] [PubMed] [Google Scholar]
- Becker P. B., Wu C. Cell-free system for assembly of transcriptionally repressed chromatin from Drosophila embryos. Mol Cell Biol. 1992 May;12(5):2241–2249. doi: 10.1128/mcb.12.5.2241. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bonner W. M., West M. H., Stedman J. D. Two-dimensional gel analysis of histones in acid extracts of nuclei, cells, and tissues. Eur J Biochem. 1980 Aug;109(1):17–23. doi: 10.1111/j.1432-1033.1980.tb04762.x. [DOI] [PubMed] [Google Scholar]
- Cairns B. R., Kim Y. J., Sayre M. H., Laurent B. C., Kornberg R. D. A multisubunit complex containing the SWI1/ADR6, SWI2/SNF2, SWI3, SNF5, and SNF6 gene products isolated from yeast. Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1950–1954. doi: 10.1073/pnas.91.5.1950. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carlson M., Laurent B. C. The SNF/SWI family of global transcriptional activators. Curr Opin Cell Biol. 1994 Jun;6(3):396–402. doi: 10.1016/0955-0674(94)90032-9. [DOI] [PubMed] [Google Scholar]
- Chen H., Li B., Workman J. L. A histone-binding protein, nucleoplasmin, stimulates transcription factor binding to nucleosomes and factor-induced nucleosome disassembly. EMBO J. 1994 Jan 15;13(2):380–390. doi: 10.1002/j.1460-2075.1994.tb06272.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Côté J., Quinn J., Workman J. L., Peterson C. L. Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex. Science. 1994 Jul 1;265(5168):53–60. doi: 10.1126/science.8016655. [DOI] [PubMed] [Google Scholar]
- Durrin L. K., Mann R. K., Kayne P. S., Grunstein M. Yeast histone H4 N-terminal sequence is required for promoter activation in vivo. Cell. 1991 Jun 14;65(6):1023–1031. doi: 10.1016/0092-8674(91)90554-c. [DOI] [PubMed] [Google Scholar]
- Edmondson D. G., Smith M. M., Roth S. Y. Repression domain of the yeast global repressor Tup1 interacts directly with histones H3 and H4. Genes Dev. 1996 May 15;10(10):1247–1259. doi: 10.1101/gad.10.10.1247. [DOI] [PubMed] [Google Scholar]
- Felsenfeld G. Chromatin as an essential part of the transcriptional mechanism. Nature. 1992 Jan 16;355(6357):219–224. doi: 10.1038/355219a0. [DOI] [PubMed] [Google Scholar]
- Georgel P., Demeler B., Terpening C., Paule M. R., van Holde K. E. Binding of the RNA polymerase I transcription complex to its promoter can modify positioning of downstream nucleosomes assembled in vitro. J Biol Chem. 1993 Jan 25;268(3):1947–1954. [PubMed] [Google Scholar]
- Grunstein M., Hecht A., Fisher-Adams G., Wan J., Mann R. K., Strahl-Bolsinger S., Laroche T., Gasser S. The regulation of euchromatin and heterochromatin by histones in yeast. J Cell Sci Suppl. 1995;19:29–36. doi: 10.1242/jcs.1995.supplement_19.4. [DOI] [PubMed] [Google Scholar]
- Hecht A., Laroche T., Strahl-Bolsinger S., Gasser S. M., Grunstein M. Histone H3 and H4 N-termini interact with SIR3 and SIR4 proteins: a molecular model for the formation of heterochromatin in yeast. Cell. 1995 Feb 24;80(4):583–592. doi: 10.1016/0092-8674(95)90512-x. [DOI] [PubMed] [Google Scholar]
- Imbalzano A. N., Kwon H., Green M. R., Kingston R. E. Facilitated binding of TATA-binding protein to nucleosomal DNA. Nature. 1994 Aug 11;370(6489):481–485. doi: 10.1038/370481a0. [DOI] [PubMed] [Google Scholar]
- Juan L. J., Utley R. T., Adams C. C., Vettese-Dadey M., Workman J. L. Differential repression of transcription factor binding by histone H1 is regulated by the core histone amino termini. EMBO J. 1994 Dec 15;13(24):6031–6040. doi: 10.1002/j.1460-2075.1994.tb06949.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Loidl P. Histone acetylation: facts and questions. Chromosoma. 1994 Dec;103(7):441–449. doi: 10.1007/BF00337382. [DOI] [PubMed] [Google Scholar]
- Megee P. C., Morgan B. A., Mittman B. A., Smith M. M. Genetic analysis of histone H4: essential role of lysines subject to reversible acetylation. Science. 1990 Feb 16;247(4944):841–845. doi: 10.1126/science.2106160. [DOI] [PubMed] [Google Scholar]
- Moudrianakis E. N., Arents G. Structure of the histone octamer core of the nucleosome and its potential interactions with DNA. Cold Spring Harb Symp Quant Biol. 1993;58:273–279. doi: 10.1101/sqb.1993.058.01.032. [DOI] [PubMed] [Google Scholar]
- Neubauer B., Hörz W. Analysis of nucleosome positioning by in vitro reconstitution. Methods Enzymol. 1989;170:630–644. doi: 10.1016/0076-6879(89)70069-0. [DOI] [PubMed] [Google Scholar]
- Owen-Hughes T., Utley R. T., Côté J., Peterson C. L., Workman J. L. Persistent site-specific remodeling of a nucleosome array by transient action of the SWI/SNF complex. Science. 1996 Jul 26;273(5274):513–516. doi: 10.1126/science.273.5274.513. [DOI] [PubMed] [Google Scholar]
- Panyutin I. G., Biswas I., Hsieh P. A pivotal role for the structure of the Holliday junction in DNA branch migration. EMBO J. 1995 Apr 18;14(8):1819–1826. doi: 10.1002/j.1460-2075.1995.tb07170.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Park E. C., Szostak J. W. 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. doi: 10.1128/mcb.10.9.4932. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Patterton D., Wolffe A. P. Developmental roles for chromatin and chromosomal structure. Dev Biol. 1996 Jan 10;173(1):2–13. doi: 10.1006/dbio.1996.0002. [DOI] [PubMed] [Google Scholar]
- Peterson C. L., Dingwall A., Scott M. P. Five SWI/SNF gene products are components of a large multisubunit complex required for transcriptional enhancement. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):2905–2908. doi: 10.1073/pnas.91.8.2905. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Puerta C., Hernández F., López-Alarcón L., Palacián E. Acetylation of histone H2A.H2B dimers facilitates transcription. Biochem Biophys Res Commun. 1995 May 16;210(2):409–416. doi: 10.1006/bbrc.1995.1676. [DOI] [PubMed] [Google Scholar]
- Quinn J., Fyrberg A. M., Ganster R. W., Schmidt M. C., Peterson C. L. DNA-binding properties of the yeast SWI/SNF complex. Nature. 1996 Feb 29;379(6568):844–847. doi: 10.1038/379844a0. [DOI] [PubMed] [Google Scholar]
- Richmond T. J., Finch J. T., Rushton B., Rhodes D., Klug A. Structure of the nucleosome core particle at 7 A resolution. Nature. 1984 Oct 11;311(5986):532–537. doi: 10.1038/311532a0. [DOI] [PubMed] [Google Scholar]
- Richmond T. J., Rechsteiner T., Luger K. Studies of nucleosome structure. Cold Spring Harb Symp Quant Biol. 1993;58:265–272. doi: 10.1101/sqb.1993.058.01.031. [DOI] [PubMed] [Google Scholar]
- Simon R. H., Felsenfeld G. A new procedure for purifying histone pairs H2A + H2B and H3 + H4 from chromatin using hydroxylapatite. Nucleic Acids Res. 1979 Feb;6(2):689–696. doi: 10.1093/nar/6.2.689. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smith D. B., Johnson K. S. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene. 1988 Jul 15;67(1):31–40. doi: 10.1016/0378-1119(88)90005-4. [DOI] [PubMed] [Google Scholar]
- Suda M., Iwai K. Identification of suberimidate cross-linking sites of four histone sequences in H1-depleted chromatin. Histone arrangement in nucleosome core. J Biochem. 1979 Dec;86(6):1659–1670. doi: 10.1093/oxfordjournals.jbchem.a132686. [DOI] [PubMed] [Google Scholar]
- Taunton J., Hassig C. A., Schreiber S. L. A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p. Science. 1996 Apr 19;272(5260):408–411. doi: 10.1126/science.272.5260.408. [DOI] [PubMed] [Google Scholar]
- Thomas J. O. Chemical cross-linking of histones. Methods Enzymol. 1989;170:549–571. doi: 10.1016/0076-6879(89)70064-1. [DOI] [PubMed] [Google Scholar]
- Thomas J. O., Kornberg R. D. The study of histone--histone associations by chemical cross-linking. Methods Cell Biol. 1978;18:429–440. [PubMed] [Google Scholar]
- Thompson J. S., Hecht A., Grunstein M. Histones and the regulation of heterochromatin in yeast. Cold Spring Harb Symp Quant Biol. 1993;58:247–256. doi: 10.1101/sqb.1993.058.01.029. [DOI] [PubMed] [Google Scholar]
- Tsukiyama T., Becker P. B., Wu C. ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor. Nature. 1994 Feb 10;367(6463):525–532. doi: 10.1038/367525a0. [DOI] [PubMed] [Google Scholar]
- Tsukiyama T., Wu C. Purification and properties of an ATP-dependent nucleosome remodeling factor. Cell. 1995 Dec 15;83(6):1011–1020. doi: 10.1016/0092-8674(95)90216-3. [DOI] [PubMed] [Google Scholar]
- Vettese-Dadey M., Grant P. A., Hebbes T. R., Crane- Robinson C., Allis C. D., Workman J. L. Acetylation of histone H4 plays a primary role in enhancing transcription factor binding to nucleosomal DNA in vitro. EMBO J. 1996 May 15;15(10):2508–2518. [PMC free article] [PubMed] [Google Scholar]
- Vettese-Dadey M., Walter P., Chen H., Juan L. J., Workman J. L. Role of the histone amino termini in facilitated binding of a transcription factor, GAL4-AH, to nucleosome cores. Mol Cell Biol. 1994 Feb;14(2):970–981. doi: 10.1128/mcb.14.2.970. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wolffe A. P., Pruss D. Targeting chromatin disruption: Transcription regulators that acetylate histones. Cell. 1996 Mar 22;84(6):817–819. doi: 10.1016/s0092-8674(00)81059-4. [DOI] [PubMed] [Google Scholar]