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. 1994 Jan 15;13(2):380–390. doi: 10.1002/j.1460-2075.1994.tb06272.x

A histone-binding protein, nucleoplasmin, stimulates transcription factor binding to nucleosomes and factor-induced nucleosome disassembly.

H Chen 1, B Li 1, J L Workman 1
PMCID: PMC394819  PMID: 8313883

Abstract

The binding of a GAL4-AH, USF or Sp1 to nucleosome cores was stimulated by the presence of the histone-binding protein, nucleoplasmin. Stimulation of factor binding by nucleoplasmin was specific for nucleosome reconstituted DNA and was not mimicked by non-specific histone sinks (i.e. polyglutamate or RNA). Upon GAL4-AH binding, nucleoplasmin specifically removed histones H2A and H2B from the nucleosome which enhanced the subsequent loss of the H3/H4 tetramers onto competing DNA. Thus, nucleoplasmin participated in the complete conversion of nucleosome cores to transcription factor-DNA complexes. These data indicate that proteins which bind histones can increase transcription factor binding to nucleosomal DNA and that transcription factor binding can initiate nucleosome disassembly. Similar activities of histone-binding proteins may participate in the displacement of nucleosomes at enhancers and promoters in vivo.

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Selected References

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

  1. 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]
  2. Almouzni G., Clark D. J., Méchali M., Wolffe A. P. Chromatin assembly on replicating DNA in vitro. Nucleic Acids Res. 1990 Oct 11;18(19):5767–5774. doi: 10.1093/nar/18.19.5767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Almouzni G., Méchali M., Wolffe A. P. Transcription complex disruption caused by a transition in chromatin structure. Mol Cell Biol. 1991 Feb;11(2):655–665. doi: 10.1128/mcb.11.2.655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Archer T. K., Cordingley M. G., Wolford R. G., Hager G. L. Transcription factor access is mediated by accurately positioned nucleosomes on the mouse mammary tumor virus promoter. Mol Cell Biol. 1991 Feb;11(2):688–698. doi: 10.1128/mcb.11.2.688. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blau H. M., Baltimore D. Differentiation requires continuous regulation. J Cell Biol. 1991 Mar;112(5):781–783. doi: 10.1083/jcb.112.5.781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Blau H. M. How fixed is the differentiated state? Lessons from heterokaryons. Trends Genet. 1989 Aug;5(8):268–272. doi: 10.1016/0168-9525(89)90100-5. [DOI] [PubMed] [Google Scholar]
  7. Clark D. J., Felsenfeld G. A nucleosome core is transferred out of the path of a transcribing polymerase. Cell. 1992 Oct 2;71(1):11–22. doi: 10.1016/0092-8674(92)90262-b. [DOI] [PubMed] [Google Scholar]
  8. Cotten M., Chalkley R. Purification of a novel, nucleoplasmin-like protein from somatic nuclei. EMBO J. 1987 Dec 20;6(13):3945–3954. doi: 10.1002/j.1460-2075.1987.tb02736.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Croston G. E., Laybourn P. J., Paranjape S. M., Kadonaga J. T. Mechanism of transcriptional antirepression by GAL4-VP16. Genes Dev. 1992 Dec;6(12A):2270–2281. doi: 10.1101/gad.6.12a.2270. [DOI] [PubMed] [Google Scholar]
  10. Dilworth S. M., Black S. J., Laskey R. A. Two complexes that contain histones are required for nucleosome assembly in vitro: role of nucleoplasmin and N1 in Xenopus egg extracts. Cell. 1987 Dec 24;51(6):1009–1018. doi: 10.1016/0092-8674(87)90587-3. [DOI] [PubMed] [Google Scholar]
  11. Earnshaw W. C., Honda B. M., Laskey R. A., Thomas J. O. Assembly of nucleosomes: the reaction involving X. laevis nucleoplasmin. Cell. 1980 Sep;21(2):373–383. doi: 10.1016/0092-8674(80)90474-2. [DOI] [PubMed] [Google Scholar]
  12. Elgin S. C. Chromatin structure and gene activity. Curr Opin Cell Biol. 1990 Jun;2(3):437–445. doi: 10.1016/0955-0674(90)90125-x. [DOI] [PubMed] [Google Scholar]
  13. Elgin S. C. The formation and function of DNase I hypersensitive sites in the process of gene activation. J Biol Chem. 1988 Dec 25;263(36):19259–19262. [PubMed] [Google Scholar]
  14. 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]
  15. Gross D. S., Garrard W. T. Nuclease hypersensitive sites in chromatin. Annu Rev Biochem. 1988;57:159–197. doi: 10.1146/annurev.bi.57.070188.001111. [DOI] [PubMed] [Google Scholar]
  16. Gruss C., Sogo J. M. Chromatin replication. Bioessays. 1992 Jan;14(1):1–8. doi: 10.1002/bies.950140102. [DOI] [PubMed] [Google Scholar]
  17. Hirschhorn J. N., Brown S. A., Clark C. D., Winston F. Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure. Genes Dev. 1992 Dec;6(12A):2288–2298. doi: 10.1101/gad.6.12a.2288. [DOI] [PubMed] [Google Scholar]
  18. Ishimi Y., Hirosumi J., Sato W., Sugasawa K., Yokota S., Hanaoka F., Yamada M. Purification and initial characterization of a protein which facilitates assembly of nucleosome-like structure from mammalian cells. Eur J Biochem. 1984 Aug 1;142(3):431–439. doi: 10.1111/j.1432-1033.1984.tb08305.x. [DOI] [PubMed] [Google Scholar]
  19. Ishimi Y., Yasuda H., Hirosumi J., Hanaoka F., Yamada M. A protein which facilitates assembly of nucleosome-like structures in vitro in mammalian cells. J Biochem. 1983 Sep;94(3):735–744. doi: 10.1093/oxfordjournals.jbchem.a134414. [DOI] [PubMed] [Google Scholar]
  20. Kerppola T. K., Curran T. Fos-Jun heterodimers and Jun homodimers bend DNA in opposite orientations: implications for transcription factor cooperativity. Cell. 1991 Jul 26;66(2):317–326. doi: 10.1016/0092-8674(91)90621-5. [DOI] [PubMed] [Google Scholar]
  21. Kleinschmidt J. A., Fortkamp E., Krohne G., Zentgraf H., Franke W. W. Co-existence of two different types of soluble histone complexes in nuclei of Xenopus laevis oocytes. J Biol Chem. 1985 Jan 25;260(2):1166–1176. [PubMed] [Google Scholar]
  22. Kleinschmidt J. A., Franke W. W. Soluble acidic complexes containing histones H3 and H4 in nuclei of Xenopus laevis oocytes. Cell. 1982 Jul;29(3):799–809. doi: 10.1016/0092-8674(82)90442-1. [DOI] [PubMed] [Google Scholar]
  23. Kleinschmidt J. A., Seiter A., Zentgraf H. Nucleosome assembly in vitro: separate histone transfer and synergistic interaction of native histone complexes purified from nuclei of Xenopus laevis oocytes. EMBO J. 1990 Apr;9(4):1309–1318. doi: 10.1002/j.1460-2075.1990.tb08240.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kornberg R. D., Lorch Y. Chromatin structure and transcription. Annu Rev Cell Biol. 1992;8:563–587. doi: 10.1146/annurev.cb.08.110192.003023. [DOI] [PubMed] [Google Scholar]
  25. Kornberg R. D., Lorch Y. Irresistible force meets immovable object: transcription and the nucleosome. Cell. 1991 Nov 29;67(5):833–836. doi: 10.1016/0092-8674(91)90354-2. [DOI] [PubMed] [Google Scholar]
  26. Ladiges W. C., Raff R. F., Brown S., Deeg H. J., Storb R. The canine major histocompatibility complex. Supertypic specificities defined by the primed lymphocyte test (PLT). Immunogenetics. 1984;19(4):359–365. doi: 10.1007/BF00345410. [DOI] [PubMed] [Google Scholar]
  27. Laskey R. A., Earnshaw W. C. Nucleosome assembly. Nature. 1980 Aug 21;286(5775):763–767. doi: 10.1038/286763a0. [DOI] [PubMed] [Google Scholar]
  28. Laskey R. A., Honda B. M., Mills A. D., Finch J. T. Nucleosomes are assembled by an acidic protein which binds histones and transfers them to DNA. Nature. 1978 Oct 5;275(5679):416–420. doi: 10.1038/275416a0. [DOI] [PubMed] [Google Scholar]
  29. Lee D. Y., Hayes J. J., Pruss D., Wolffe A. P. A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell. 1993 Jan 15;72(1):73–84. doi: 10.1016/0092-8674(93)90051-q. [DOI] [PubMed] [Google Scholar]
  30. Lin Y. S., Carey M. F., Ptashne M., Green M. R. GAL4 derivatives function alone and synergistically with mammalian activators in vitro. Cell. 1988 Aug 26;54(5):659–664. doi: 10.1016/s0092-8674(88)80010-2. [DOI] [PubMed] [Google Scholar]
  31. Majumder S., Miranda M., DePamphilis M. L. Analysis of gene expression in mouse preimplantation embryos demonstrates that the primary role of enhancers is to relieve repression of promoters. EMBO J. 1993 Mar;12(3):1131–1140. doi: 10.1002/j.1460-2075.1993.tb05754.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Moreau N., Angelier N., Bonnanfant-Jais M. L., Gounon P., Kubisz P. Association of nucleoplasmin with transcription products as revealed by immunolocalization in the amphibian oocyte. J Cell Biol. 1986 Sep;103(3):683–690. doi: 10.1083/jcb.103.3.683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Perlmann T. Glucocorticoid receptor DNA-binding specificity is increased by the organization of DNA in nucleosomes. Proc Natl Acad Sci U S A. 1992 May 1;89(9):3884–3888. doi: 10.1073/pnas.89.9.3884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Perlmann T., Wrange O. Inhibition of chromatin assembly in Xenopus oocytes correlates with derepression of the mouse mammary tumor virus promoter. Mol Cell Biol. 1991 Oct;11(10):5259–5265. doi: 10.1128/mcb.11.10.5259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Perlmann T., Wrange O. Specific glucocorticoid receptor binding to DNA reconstituted in a nucleosome. EMBO J. 1988 Oct;7(10):3073–3079. doi: 10.1002/j.1460-2075.1988.tb03172.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Peterson C. L., Herskowitz I. Characterization of the yeast SWI1, SWI2, and SWI3 genes, which encode a global activator of transcription. Cell. 1992 Feb 7;68(3):573–583. doi: 10.1016/0092-8674(92)90192-f. [DOI] [PubMed] [Google Scholar]
  37. Philpott A., Leno G. H., Laskey R. A. Sperm decondensation in Xenopus egg cytoplasm is mediated by nucleoplasmin. Cell. 1991 May 17;65(4):569–578. doi: 10.1016/0092-8674(91)90089-h. [DOI] [PubMed] [Google Scholar]
  38. Philpott A., Leno G. H. Nucleoplasmin remodels sperm chromatin in Xenopus egg extracts. Cell. 1992 May 29;69(5):759–767. doi: 10.1016/0092-8674(92)90288-n. [DOI] [PubMed] [Google Scholar]
  39. Piña B., Brüggemeier U., Beato M. Nucleosome positioning modulates accessibility of regulatory proteins to the mouse mammary tumor virus promoter. Cell. 1990 Mar 9;60(5):719–731. doi: 10.1016/0092-8674(90)90087-u. [DOI] [PubMed] [Google Scholar]
  40. Pognonec P., Kato H., Sumimoto H., Kretzschmar M., Roeder R. G. A quick procedure for purification of functional recombinant proteins over-expressed in E.coli. Nucleic Acids Res. 1991 Dec 11;19(23):6650–6650. doi: 10.1093/nar/19.23.6650. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Pognonec P., Roeder R. G. Recombinant 43-kDa USF binds to DNA and activates transcription in a manner indistinguishable from that of natural 43/44-kDa USF. Mol Cell Biol. 1991 Oct;11(10):5125–5136. doi: 10.1128/mcb.11.10.5125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Reik A., Schütz G., Stewart A. F. Glucocorticoids are required for establishment and maintenance of an alteration in chromatin structure: induction leads to a reversible disruption of nucleosomes over an enhancer. EMBO J. 1991 Sep;10(9):2569–2576. doi: 10.1002/j.1460-2075.1991.tb07797.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Rhodes D., Laskey R. A. Assembly of nucleosomes and chromatin in vitro. Methods Enzymol. 1989;170:575–585. doi: 10.1016/0076-6879(89)70065-3. [DOI] [PubMed] [Google Scholar]
  44. Rhodes D. Structural analysis of a triple complex between the histone octamer, a Xenopus gene for 5S RNA and transcription factor IIIA. EMBO J. 1985 Dec 16;4(13A):3473–3482. doi: 10.1002/j.1460-2075.1985.tb04106.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Richard-Foy H., Hager G. L. Sequence-specific positioning of nucleosomes over the steroid-inducible MMTV promoter. EMBO J. 1987 Aug;6(8):2321–2328. doi: 10.1002/j.1460-2075.1987.tb02507.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Ruiz-Carrillo A., Jorcano J. L., Eder G., Lurz R. In vitro core particle and nucleosome assembly at physiological ionic strength. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3284–3288. doi: 10.1073/pnas.76.7.3284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Sapp M., Worcel A. Purification and mechanism of action of a nucleosome assembly factor from Xenopus oocytes. J Biol Chem. 1990 Jun 5;265(16):9357–9365. [PubMed] [Google Scholar]
  48. Schmid A., Fascher K. D., Hörz W. Nucleosome disruption at the yeast PHO5 promoter upon PHO5 induction occurs in the absence of DNA replication. Cell. 1992 Nov 27;71(5):853–864. doi: 10.1016/0092-8674(92)90560-y. [DOI] [PubMed] [Google Scholar]
  49. Sealy L., Burgess R. R., Cotten M., Chalkley R. Purification of Xenopus egg nucleoplasmin and its use in chromatin assembly in vitro. Methods Enzymol. 1989;170:612–630. doi: 10.1016/0076-6879(89)70068-9. [DOI] [PubMed] [Google Scholar]
  50. Smith S., Stillman B. Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell. 1989 Jul 14;58(1):15–25. doi: 10.1016/0092-8674(89)90398-x. [DOI] [PubMed] [Google Scholar]
  51. Smith S., Stillman B. Stepwise assembly of chromatin during DNA replication in vitro. EMBO J. 1991 Apr;10(4):971–980. doi: 10.1002/j.1460-2075.1991.tb08031.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Stein A., Mitchell M. Generation of different nucleosome spacing periodicities in vitro. Possible origin of cell type specificity. J Mol Biol. 1988 Oct 20;203(4):1029–1043. doi: 10.1016/0022-2836(88)90127-1. [DOI] [PubMed] [Google Scholar]
  53. Svaren J., Chalkley R. The structure and assembly of active chromatin. Trends Genet. 1990 Feb;6(2):52–56. doi: 10.1016/0168-9525(90)90074-g. [DOI] [PubMed] [Google Scholar]
  54. Svaren J., Hörz W. Histones, nucleosomes and transcription. Curr Opin Genet Dev. 1993 Apr;3(2):219–225. doi: 10.1016/0959-437x(93)90026-l. [DOI] [PubMed] [Google Scholar]
  55. Taylor I. C., Workman J. L., Schuetz T. J., Kingston R. E. Facilitated binding of GAL4 and heat shock factor to nucleosomal templates: differential function of DNA-binding domains. Genes Dev. 1991 Jul;5(7):1285–1298. doi: 10.1101/gad.5.7.1285. [DOI] [PubMed] [Google Scholar]
  56. Winston F., Carlson M. Yeast SNF/SWI transcriptional activators and the SPT/SIN chromatin connection. Trends Genet. 1992 Nov;8(11):387–391. doi: 10.1016/0168-9525(92)90300-s. [DOI] [PubMed] [Google Scholar]
  57. Wolffe A. P. Implications of DNA replication for eukaryotic gene expression. J Cell Sci. 1991 Jun;99(Pt 2):201–206. doi: 10.1242/jcs.99.2.201. [DOI] [PubMed] [Google Scholar]
  58. Workman J. L., Buchman A. R. Multiple functions of nucleosomes and regulatory factors in transcription. Trends Biochem Sci. 1993 Mar;18(3):90–95. doi: 10.1016/0968-0004(93)90160-o. [DOI] [PubMed] [Google Scholar]
  59. Workman J. L., Kingston R. E. Nucleosome core displacement in vitro via a metastable transcription factor-nucleosome complex. Science. 1992 Dec 11;258(5089):1780–1784. doi: 10.1126/science.1465613. [DOI] [PubMed] [Google Scholar]
  60. Workman J. L., Taylor I. C., Kingston R. E., Roeder R. G. Control of class II gene transcription during in vitro nucleosome assembly. Methods Cell Biol. 1991;35:419–447. doi: 10.1016/s0091-679x(08)60582-8. [DOI] [PubMed] [Google Scholar]
  61. Wray W., Boulikas T., Wray V. P., Hancock R. Silver staining of proteins in polyacrylamide gels. Anal Biochem. 1981 Nov 15;118(1):197–203. doi: 10.1016/0003-2697(81)90179-2. [DOI] [PubMed] [Google Scholar]
  62. Zaret K. S., Yamamoto K. R. Reversible and persistent changes in chromatin structure accompany activation of a glucocorticoid-dependent enhancer element. Cell. 1984 Aug;38(1):29–38. doi: 10.1016/0092-8674(84)90523-3. [DOI] [PubMed] [Google Scholar]
  63. Zucker K., Worcel A. The histone H3/H4.N1 complex supplemented with histone H2A-H2B dimers and DNA topoisomerase I forms nucleosomes on circular DNA under physiological conditions. J Biol Chem. 1990 Aug 25;265(24):14487–14496. [PubMed] [Google Scholar]

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