Dynamic intramolecular regulation of the histone chaperone nucleoplasmin controls histone binding and release

Warren, Christopher; Matsui, Tsutomu; Karp, Jerome M.; Onikubo, Takashi; Cahill, Sean; Brenowitz, Michael; Cowburn, David; Girvin, Mark; Shechter, David

doi:10.1038/s41467-017-02308-3

Title: Dynamic intramolecular regulation of the histone chaperone nucleoplasmin controls histone binding and release

Journal Article · Wed Dec 20 00:00:00 EST 2017 · Nature Communications

DOI:https://doi.org/10.1038/s41467-017-02308-3· OSTI ID:1420044

Warren, Christopher ^[1]; Matsui, Tsutomu ^[2]; Karp, Jerome M. ^[1]; Onikubo, Takashi ^[3]; Cahill, Sean ^[1]; Brenowitz, Michael ^[1];

^[1]; Girvin, Mark ^[1]; Shechter, David ^[1]

Albert Einstein College of Medicine, Bronx, NY (United States)
Stanford Univ., Menlo Park, CA (United States)
Albert Einstein College of Medicine, Bronx, NY (United States); Rockefeller Univ., New York, NY (United States)

Here, nucleoplasmin (Npm) is a highly conserved histone chaperone responsible for the maternal storage and zygotic release of histones H2A/H2B. Npm contains a pentameric N-terminal core domain and an intrinsically disordered C-terminal tail domain. Though intrinsically disordered regions are common among histone chaperones, their roles in histone binding and chaperoning remain unclear. Using an NMR-based approach, here we demonstrate that the Xenopus laevis Npm tail domain controls the binding of histones at its largest acidic stretch (A2) via direct competition with both the C-terminal basic stretch and basic nuclear localization signal. NMR and small-angle X-ray scattering (SAXS) structural analyses allowed us to construct models of both the tail domain and the pentameric complex. Functional analyses demonstrate that these competitive intramolecular interactions negatively regulate Npm histone chaperone activity in vitro. Together these data establish a potentially generalizable mechanism of histone chaperone regulation via dynamic and specific intramolecular shielding of histone interaction sites.

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Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1420044

Journal Information:: Nature Communications, Vol. 8, Issue 1; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 16 works

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References (67)

The Crystal Structure of Nucleoplasmin-Core Dutta, Shuchismita; Akey, Ildikó V.; Dingwall, Colin Molecular Cell, Vol. 8, Issue 4 https://doi.org/10.1016/S1097-2765(01)00354-9	journal	October 2001
Roles of NPM2 in Chromatin and Nucleolar Organization in Oocytes and Embryos Burns, K. H. Science, Vol. 300, Issue 5619 https://doi.org/10.1126/science.1081813	journal	April 2003
Structural insight into how the human helicase subunit MCM2 may act as a histone chaperone together with ASF1 at the replication fork Richet, Nicolas; Liu, Danni; Legrand, Pierre Nucleic Acids Research, Vol. 43, Issue 3 https://doi.org/10.1093/nar/gkv021	journal	January 2015
Histone chaperones in nucleosome eviction and histone exchange Park, Young-Jun; Luger, Karolin Current Opinion in Structural Biology, Vol. 18, Issue 3 https://doi.org/10.1016/j.sbi.2008.04.003	journal	June 2008
Developmentally Regulated Post-translational Modification of Nucleoplasmin Controls Histone Sequestration and Deposition Onikubo, Takashi; Nicklay, Joshua J.; Xing, Li Cell Reports, Vol. 10, Issue 10 https://doi.org/10.1016/j.celrep.2015.02.038	journal	March 2015
Reconstitution of mitotic chromatids with a minimum set of purified factors Shintomi, Keishi; Takahashi, Tatsuro S.; Hirano, Tatsuya Nature Cell Biology, Vol. 17, Issue 8 https://doi.org/10.1038/ncb3187	journal	June 2015
DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering Franke, Daniel; Svergun, Dmitri I. Journal of Applied Crystallography, Vol. 42, Issue 2, p. 342-346 https://doi.org/10.1107/S0021889809000338	journal	January 2009
Two complexes that contain histones are required for nucleosome assembly in vitro: Role of nucleoplasmin and N1 in Xenopus egg extracts Dilworth, Stephen M.; Black, Susan J.; Laskey, Ronald A. Cell, Vol. 51, Issue 6 https://doi.org/10.1016/0092-8674(87)90587-3	journal	December 1987
The Amber biomolecular simulation programs Case, David A.; Cheatham, Thomas E.; Darden, Tom Journal of Computational Chemistry, Vol. 26, Issue 16 https://doi.org/10.1002/jcc.20290	journal	January 2005
Determination of the regularization parameter in indirect-transform methods using perceptual criteria Svergun, D. I. Journal of Applied Crystallography, Vol. 25, Issue 4, p. 495-503 https://doi.org/10.1107/S0021889892001663	journal	August 1992
Preferential Binding of the Histone (H3-H4) ₂ Tetramer by NAP1 Is Mediated by the Amino-terminal Histone Tails McBryant, Steven J.; Park, Young-Jun; Abernathy, Stephanie M. Journal of Biological Chemistry, Vol. 278, Issue 45 https://doi.org/10.1074/jbc.M305636200	journal	August 2003
Nucleosomes are assembled by an acidic protein which binds histones and transfers them to DNA Laskey, R. A.; Honda, B. M.; Mills, A. D. Nature, Vol. 275, Issue 5679 https://doi.org/10.1038/275416a0	journal	October 1978
A Mechanism for Histone Chaperoning Activity of Nucleoplasmin: Thermodynamic and Structural Models Taneva, Stefka G.; Bañuelos, Sonia; Falces, Jorge Journal of Molecular Biology, Vol. 393, Issue 2 https://doi.org/10.1016/j.jmb.2009.08.005	journal	October 2009
Ensemble Approach for NMR Structure Refinement against ¹ H Paramagnetic Relaxation Enhancement Data Arising from a Flexible Paramagnetic Group Attached to a Macromolecule Iwahara, Junji; Schwieters, Charles D.; Clore, G. Marius Journal of the American Chemical Society, Vol. 126, Issue 18 https://doi.org/10.1021/ja031580d	journal	May 2004
Chromatin assembly: Cooperation between histone chaperones and ATP-dependent nucleosome remodeling machines Tyler, Jessica K. European Journal of Biochemistry, Vol. 269, Issue 9 https://doi.org/10.1046/j.1432-1033.2002.02890.x	journal	April 2002
Massive phosphorylation distinguishes Xenopus laevis nucleoplasmin isolated from oocytes or unfertilized eggs Cotten, Matt; Sealy, Linda; Chalkley, Roger Biochemistry, Vol. 25, Issue 18 https://doi.org/10.1021/bi00366a014	journal	September 1986
New insights into nucleosome and chromatin structure: an ordered state or a disordered affair? Luger, Karolin; Dechassa, Mekonnen L.; Tremethick, David J. Nature Reviews Molecular Cell Biology, Vol. 13, Issue 7 https://doi.org/10.1038/nrm3382	journal	June 2012
ANP32E is a histone chaperone that removes H2A.Z from chromatin Obri, Arnaud; Ouararhni, Khalid; Papin, Christophe Nature, Vol. 505, Issue 7485 https://doi.org/10.1038/nature12922	journal	January 2014
Fly Fishing for Histones: Catch and Release by Histone Chaperone Intrinsically Disordered Regions and Acidic Stretches Warren, Christopher; Shechter, David Journal of Molecular Biology, Vol. 429, Issue 16 https://doi.org/10.1016/j.jmb.2017.06.005	journal	August 2017
Sensitivity of secondary structure propensities to sequence differences between α- and γ-synuclein: Implications for fibrillation Marsh, Joseph A.; Singh, Vinay K.; Jia, Zongchao Protein Science, Vol. 15, Issue 12 https://doi.org/10.1110/ps.062465306	journal	December 2006
The Xplor-NIH NMR molecular structure determination package Schwieters, Charles D.; Kuszewski, John J.; Tjandra, Nico Journal of Magnetic Resonance, Vol. 160, Issue 1 https://doi.org/10.1016/S1090-7807(02)00014-9	journal	January 2003
Mutation of the small acidic tract A1 drastically reduces nucleoplasmin activity Salvany, Lara; Chiva, Manel; Arnan, Carme FEBS Letters, Vol. 576, Issue 3 https://doi.org/10.1016/j.febslet.2004.07.095	journal	September 2004
Kinetic Advantage of Intrinsically Disordered Proteins in Coupled Folding–Binding Process: A Critical Assessment of the “Fly-Casting” Mechanism Huang, Yongqi; Liu, Zhirong Journal of Molecular Biology, Vol. 393, Issue 5 https://doi.org/10.1016/j.jmb.2009.09.010	journal	November 2009
Two surfaces on the histone chaperone Rtt106 mediate histone binding, replication, and silencing Zunder, R. M.; Antczak, A. J.; Berger, J. M. Proceedings of the National Academy of Sciences, Vol. 109, Issue 3 https://doi.org/10.1073/pnas.1119095109	journal	December 2011
The human histone chaperone sNASP interacts with linker and core histones through distinct mechanisms Wang, H.; Ge, Z.; Walsh, S. T. R. Nucleic Acids Research, Vol. 40, Issue 2 https://doi.org/10.1093/nar/gkr781	journal	September 2011
NMR Characterization of Long-Range Order in Intrinsically Disordered Proteins Salmon, Loïc; Nodet, Gabrielle; Ozenne, Valéry Journal of the American Chemical Society, Vol. 132, Issue 24 https://doi.org/10.1021/ja101645g	journal	June 2010
A Quantitative Characterization of Nucleoplasmin/Histone Complexes Reveals Chaperone Versatility Fernández-Rivero, Noelia; Franco, Aitor; Velázquez-Campoy, Adrian Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep32114	journal	August 2016
Crystal structure of the nucleosome core particle at 2.8 Å resolution Luger, Karolin; Mäder, Armin W.; Richmond, Robin K. Nature, Vol. 389, Issue 6648 https://doi.org/10.1038/38444	journal	September 1997
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
The histone shuffle: histone chaperones in an energetic dance Das, Chandrima; Tyler, Jessica K.; Churchill, Mair E. A. Trends in Biochemical Sciences, Vol. 35, Issue 9 https://doi.org/10.1016/j.tibs.2010.04.001	journal	September 2010
Probabilistic Interaction Network of Evidence Algorithm and its Application to Complete Labeling of Peak Lists from Protein NMR Spectroscopy Bahrami, Arash; Assadi, Amir H.; Markley, John L. PLoS Computational Biology, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pcbi.1000307	journal	March 2009
Estimation of Protein Secondary Structure from Circular Dichroism Spectra: Comparison of CONTIN, SELCON, and CDSSTR Methods with an Expanded Reference Set Sreerama, Narasimha; Woody, Robert W. Analytical Biochemistry, Vol. 287, Issue 2, p. 252-260 https://doi.org/10.1006/abio.2000.4880	journal	December 2000
Structural Basis of the pH-Dependent Assembly of a Botulinum Neurotoxin Complex Matsui, Tsutomu; Gu, Shenyan; Lam, Kwok-ho Journal of Molecular Biology, Vol. 426, Issue 22 https://doi.org/10.1016/j.jmb.2014.09.009	journal	November 2014
Flexible-meccano: a tool for the generation of explicit ensemble descriptions of intrinsically disordered proteins and their associated experimental observables Ozenne, V.; Bauer, F.; Salmon, L. Bioinformatics, Vol. 28, Issue 11 https://doi.org/10.1093/bioinformatics/bts172	journal	May 2012
Quantitative Characterization of Configurational Space Sampled by HIV-1 Nucleocapsid Using Solution NMR, X-ray Scattering and Protein Engineering Deshmukh, Lalit; Schwieters, Charles D.; Grishaev, Alexander ChemPhysChem, Vol. 17, Issue 11 https://doi.org/10.1002/cphc.201600212	journal	March 2016
Activation Mechanism of the Nuclear Chaperone Nucleoplasmin: Role of the Core Domain Bañuelos, Sonia; Hierro, Aitor; Arizmendi, Jesús M. Journal of Molecular Biology, Vol. 334, Issue 3 https://doi.org/10.1016/j.jmb.2003.09.067	journal	November 2003
Histone chaperones in nucleosome assembly and human disease Burgess, Rebecca J.; Zhang, Zhiguo Nature Structural & Molecular Biology, Vol. 20, Issue 1 https://doi.org/10.1038/nsmb.2461	journal	January 2013
Particle mesh Ewald: An N ⋅log( N ) method for Ewald sums in large systems Darden, Tom; York, Darrin; Pedersen, Lee The Journal of Chemical Physics, Vol. 98, Issue 12 https://doi.org/10.1063/1.464397	journal	June 1993
The intrinsically disordered distal face of nucleoplasmin recognizes distinct oligomerization states of histones Ramos, I.; Fernandez-Rivero, N.; Arranz, R. Nucleic Acids Research, Vol. 42, Issue 2 https://doi.org/10.1093/nar/gkt899	journal	October 2013
Histone transfer among chaperones Liu, Wallace H.; Churchill, Mair E. A. Biochemical Society Transactions, Vol. 40, Issue 2 https://doi.org/10.1042/BST20110737	journal	March 2012
Intrinsically disordered regions of nucleophosmin/B23 regulate its RNA binding activity through their inter- and intra-molecular association Hisaoka, M.; Nagata, K.; Okuwaki, M. Nucleic Acids Research, Vol. 42, Issue 2 https://doi.org/10.1093/nar/gkt897	journal	October 2013
Protein fold determined by paramagnetic magic-angle spinning solid-state NMR spectroscopy Sengupta, Ishita; Nadaud, Philippe S.; Helmus, Jonathan J. Nature Chemistry, Vol. 4, Issue 5 https://doi.org/10.1038/nchem.1299	journal	March 2012
The Catalytic Subunit of the SWR1 Remodeler Is a Histone Chaperone for the H2A.Z-H2B Dimer Hong, Jingjun; Feng, Hanqiao; Wang, Feng Molecular Cell, Vol. 53, Issue 3 https://doi.org/10.1016/j.molcel.2014.01.010	journal	February 2014
New developments in the ATSAS program package for small-angle scattering data analysis Petoukhov, Maxim V.; Franke, Daniel; Shkumatov, Alexander V. Journal of Applied Crystallography, Vol. 45, Issue 2 https://doi.org/10.1107/S0021889812007662	journal	March 2012
Comparative Protein Structure Modeling Using MODELLER Eswar, Narayanan; Webb, Ben; Marti-Renom, Marc A. Current Protocols in Protein Science, Vol. 50, Issue 1 https://doi.org/10.1002/0471140864.ps0209s50	journal	November 2007
The Histone Chaperone Nap1 Promotes Nucleosome Assembly by Eliminating Nonnucleosomal Histone DNA Interactions Andrews, Andrew J.; Chen, Xu; Zevin, Alexander Molecular Cell, Vol. 37, Issue 6 https://doi.org/10.1016/j.molcel.2010.01.037	journal	March 2010
Glutamylation of Nap1 modulates histone H1 dynamics and chromosome condensation in Xenopus Miller, Kelly E.; Heald, Rebecca The Journal of Cell Biology, Vol. 209, Issue 2 https://doi.org/10.1083/jcb.201412097	journal	April 2015
Prediction and Functional Analysis of Native Disorder in Proteins from the Three Kingdoms of Life Ward, J. J.; Sodhi, J. S.; McGuffin, L. J. Journal of Molecular Biology, Vol. 337, Issue 3 https://doi.org/10.1016/j.jmb.2004.02.002	journal	March 2004
C-terminal acidic domain of histone chaperone human NAP1 is an efficient binding assistant for histone H2A-H2B, but not H3-H4 Ohtomo, Hideaki; Akashi, Satoko; Moriwaki, Yoshihito Genes to Cells, Vol. 21, Issue 3 https://doi.org/10.1111/gtc.12339	journal	February 2016
NMR structure of chaperone Chz1 complexed with histones H2A.Z-H2B Zhou, Zheng; Feng, Hanqiao; Hansen, D. Flemming Nature Structural & Molecular Biology, Vol. 15, Issue 8 https://doi.org/10.1038/nsmb.1465	journal	July 2008
Intrinsically disordered proteins: a 10-year recap Tompa, Peter Trends in Biochemical Sciences, Vol. 37, Issue 12 https://doi.org/10.1016/j.tibs.2012.08.004	journal	December 2012
FACT Disrupts Nucleosome Structure by Binding H2A-H2B with Conserved Peptide Motifs Kemble, David J.; McCullough, Laura L.; Whitby, Frank G. Molecular Cell, Vol. 60, Issue 2 https://doi.org/10.1016/j.molcel.2015.09.008	journal	October 2015
The CCPN data model for NMR spectroscopy: Development of a software pipeline Vranken, Wim F.; Boucher, Wayne; Stevens, Tim J. Proteins: Structure, Function, and Bioinformatics, Vol. 59, Issue 4 https://doi.org/10.1002/prot.20449	journal	April 2005
Assembly of nucleosomes: the reaction involving X. laevis nucleoplasmin Earnshaw, William C.; Honda, Barry M.; Laskey, Ronald A. Cell, Vol. 21, Issue 2 https://doi.org/10.1016/0092-8674(80)90474-2	journal	September 1980
Chaperone Nap1 Shields Histone Surfaces Used in a Nucleosome and Can Put H2A-H2B in an Unconventional Tetrameric Form D’Arcy, Sheena; Martin, Kyle W.; Panchenko, Tanya Molecular Cell, Vol. 51, Issue 5 https://doi.org/10.1016/j.molcel.2013.07.015	journal	September 2013
Electrostatic Interactions at the C-Terminal Domain of Nucleoplasmin Modulate Its Chromatin Decondensation Activity ^† Hierro, Aitor; Arizmendi, Jesús M.; Bañuelos, Sonia Biochemistry, Vol. 41, Issue 20 https://doi.org/10.1021/bi020002r	journal	May 2002
Water Dispersion Interactions Strongly Influence Simulated Structural Properties of Disordered Protein States Piana, Stefano; Donchev, Alexander G.; Robustelli, Paul The Journal of Physical Chemistry B, Vol. 119, Issue 16 https://doi.org/10.1021/jp508971m	journal	April 2015
Architectures of Whole-Module and Bimodular Proteins from the 6-Deoxyerythronolide B Synthase Edwards, Andrea L.; Matsui, Tsutomu; Weiss, Thomas M. Journal of Molecular Biology, Vol. 426, Issue 11 https://doi.org/10.1016/j.jmb.2014.03.015	journal	May 2014
Improved side-chain torsion potentials for the Amber ff99SB protein force field Lindorff-Larsen, Kresten; Piana, Stefano; Palmo, Kim Proteins: Structure, Function, and Bioinformatics https://doi.org/10.1002/prot.22711	journal	January 2010
Cac1 WHD and PIP domains have distinct roles in replisome progression and genomic stability Tsirkas, Ioannis; Dovrat, Daniel; Lei, Yang Current Genetics, Vol. 67, Issue 1 https://doi.org/10.1007/s00294-020-01113-8	journal	October 2020
Nucleoplasmin Binds Histone H2A-H2B Dimers through Its Distal Face Ramos, Isbaal; Martín-Benito, Jaime; Finn, Ron Journal of Biological Chemistry, Vol. 285, Issue 44 https://doi.org/10.1074/jbc.m110.150664	journal	August 2010
Interaction of Nucleoplasmin with Core Histones Arnan, Carme; Saperas, Núria; Prieto, Cèlia Journal of Biological Chemistry, Vol. 278, Issue 33 https://doi.org/10.1074/jbc.m305560200	journal	June 2003
Phosphorylation of Both Nucleoplasmin Domains Is Required for Activation of Its Chromatin Decondensation Activity Bañuelos, Sonia; Omaetxebarria, Miren J.; Ramos, Isbaal Journal of Biological Chemistry, Vol. 282, Issue 29 https://doi.org/10.1074/jbc.m702842200	journal	May 2007
Polyglutamylation Is a Post-translational Modification with a Broad Range of Substrates van Dijk, Juliette; Miro, Julie; Strub, Jean-Marc Journal of Biological Chemistry, Vol. 283, Issue 7 https://doi.org/10.1074/jbc.m705813200	journal	November 2007
An integrated high-throughput data acquisition system for biological solution X-ray scattering studies Martel, Anne; Liu, Ping; Weiss, Thomas M. Journal of Synchrotron Radiation, Vol. 19, Issue 3 https://doi.org/10.1107/s0909049512008072	journal	March 2012
Ambiguity assessment of small-angle scattering curves from monodisperse systems Petoukhov, Maxim V.; Svergun, Dmitri I. Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 5 https://doi.org/10.1107/s1399004715002576	journal	April 2015
DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering Franke, D.; Svergun, D. I. Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/phppubdb-11993	text	January 2009

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