The pentameric nucleoplasmin fold is present in Drosophila FKBP39 and a large number of chromatin-related proteins

Article English OPEN
Edlich-Muth, Christian ; Artero, Jean-Baptiste ; Callow, Phil ; Przewloka, Marcin ; Watson, Aleksandra A. ; Zhang, Wei ; Glover, David M ; Debski, Janusz ; Dadlez, Michal ; Round, Adam R. ; Forsyth, V. Trevor ; Laue, Ernest D. (2015)
  • Publisher: Elsevier
  • Journal: volume 427, issue 10, pages 1,949-1,963 (issn: 0022-2836, eissn: 1089-8638)
  • Related identifiers: doi: 10.1016/j.jmb.2015.03.010, pmc: PMC4414354
  • Subject: Molecular Biology | Q1 | NOE, nuclear Overhauser enhancement | structure determination | histone chaperone | Article | NMR | nucleoplasmin | SAXS, small-angle X-ray scattering | HSQC, heteronuclear single quantum coherence | FKBP | SANS, small-angle neutron scattering | PPI, peptidyl proline isomerase

Nucleoplasmin is a histone chaperone that consists of a pentameric N-terminal domain and an unstructured C-terminal tail. The pentameric core domain, a doughnut-like structure with a central pore, is only found in the nucleoplasmin family. Here, we report the first structure of a nucleoplasmin-like domain (NPL) from the unrelated Drosophila protein, FKBP39, and we present evidence that this protein associates with chromatin. Furthermore, we show that two other chromatin proteins, Arabidopsis thaliana histone deacetylase type 2 (HD2) and Saccharomyces cerevisiae Fpr4, share the NPL fold and form pentamers, or a dimer of pentamers in the case of HD2. Thus, we propose a new family of proteins that share the pentameric nucleoplasmin-like NPL domain and are found in protists, fungi, plants and animals. [Image - see article] We are grateful to Gunter Stier for providing the vector; Michael Nilges, Oleg Fedorov, Benjamin Bardiaux, Stefanie Hartmann and Wolfgang Rieping for helpful discussions; and Daniel Nietlispach for NMR expertise. We thank Renato Paro for generously providing us with an anti-FKBP39 antibody. We would like to thank the Wellcome Trust for financial support (grant 082010/Z/07/Z). V.T.F. and E.D.L. acknowledge support from Engineering and Physical Sciences Research Council under grants GR/R99393/01 and EP/C015452/1 for the creation of the Deuteration Laboratory platform operating within the Grenoble Partnership for Structural Biology. V.T.F. also acknowledges support from the European Union under contract RII3-CT-2003-505925. J.B.A. acknowledges the provision of a postdoctoral fellowship held at Keele University. M.R.P. and D.M.G. were supported by the Medical Research Council and Cancer Research UK grants to D.M.G. A.A.W. is a recipient of a Wellcome Trust Fellowship092441/Z/10/Z. J.D. and M.D. were supported by the Harmonia 5 Grant 2013/10/M/NZ2/00298 from the Polish National Science Center. The authors would like to thank the Institut Laue-Langevin (ILL), the European Synchrotron Radiation Facility (ESRF) and the European Molecular Biology Laboratory Hamburg outstation (EMBL-HH) for the provision of beamtime and access to the experimental facilities of D22, ID14eh3 and X33 respectively. We would also like to thank the local contacts at all the facilities for providing assistance in using the beam lines. This is the final version of the article. It first appeared from Elsevier via
  • References (55)
    55 references, page 1 of 6

    [1] Frehlick LJ, Eirin-Lopez JM, Ausio J. New insights into the nucleophosmin/nucleoplasmin family of nuclear chaperones. Bioessays 2007;29:49-59.

    [2] Philpott A, Leno GH, Laskey RA. Sperm decondensation in Xenopus egg cytoplasm is mediated by nucleoplasmin. Cell 1991;65:569-78.

    [3] Betthauser JM, Pfister-Genskow M, Xu H, Golueke PJ, Lacson JC, Koppang RW, et al. Nucleoplasmin facilitates reprogramming and in vivo development of bovine nuclear transfer embryos. Mol Reprod Dev 2006;73:977-86.

    [4] Tamada H, Van Thuan N, Reed P, Nelson D, Katoku-Kikyo N, Wudel J, et al. Chromatin decondensation and nuclear reprogramming by nucleoplasmin. Mol Cell Biol 2006;26: 1259-71.

    [5] Dutta S, Akey IV, Dingwall C, Hartman KL, Laue T, Nolte RT, et al. The crystal structure of nucleoplasmin-core: implications for histone binding and nucleosome assembly. Mol Cell 2001;8:841-53.

    [6] Ramos I, Martin-Benito J, Finn R, Bretana L, Aloria K, Arizmendi JM, et al. Nucleoplasmin binds histone H2A-H2B dimers through its distal face. J Biol Chem 2010;285:33771-8.

    [7] Brosch G, Lusser A, Goralik-Schramel M, Loidl P. Purification and characterization of a high molecular weight histone deacetylase complex (HD2) of maize embryos. Biochemistry 1996;35:15907-14.

    [8] Dangl M, Brosch G, Haas H, Loidl P, Lusser A. Comparative analysis of HD2 type histone deacetylases in higher plants. Planta 2001;213:280-5.

    [9] Kolle D, Brosch G, Lechner T, Pipal A, Helliger W, Taplick J, et al. Different types of maize histone deacetylases are distinguished by a highly complex substrate and site specificity. Biochemistry 1999;38:6769-73.

    [10] Lusser A, Brosch G, Loidl A, Haas H, Loidl P. Identification of maize histone deacetylase HD2 as an acidic nucleolar phosphoprotein. Science 1997;277:88-91.

  • Related Research Results (1)
  • Bioentities (2)
    1k5j Protein Data Bank
    1kj5 Protein Data Bank
  • Metrics
    No metrics available