Release of linker histone from the nucleosome driven by polyelectrolyte competition with a disordered protein.
Journal
Nature chemistry
ISSN: 1755-4349
Titre abrégé: Nat Chem
Pays: England
ID NLM: 101499734
Informations de publication
Date de publication:
02 2022
02 2022
Historique:
received:
22
08
2020
accepted:
19
10
2021
pubmed:
8
1
2022
medline:
23
2
2022
entrez:
7
1
2022
Statut:
ppublish
Résumé
Highly charged intrinsically disordered proteins are essential regulators of chromatin structure and transcriptional activity. Here we identify a surprising mechanism of molecular competition that relies on the pronounced dynamical disorder present in these polyelectrolytes and their complexes. The highly positively charged human linker histone H1.0 (H1) binds to nucleosomes with ultrahigh affinity, implying residence times incompatible with efficient biological regulation. However, we show that the disordered regions of H1 retain their large-amplitude dynamics when bound to the nucleosome, which enables the highly negatively charged and disordered histone chaperone prothymosin α to efficiently invade the H1-nucleosome complex and displace H1 via a competitive substitution mechanism, vastly accelerating H1 dissociation. By integrating experiments and simulations, we establish a molecular model that rationalizes the remarkable kinetics of this process structurally and dynamically. Given the abundance of polyelectrolyte sequences in the nuclear proteome, this mechanism is likely to be widespread in cellular regulation.
Identifiants
pubmed: 34992286
doi: 10.1038/s41557-021-00839-3
pii: 10.1038/s41557-021-00839-3
doi:
Substances chimiques
Histones
0
Intrinsically Disordered Proteins
0
Nucleosomes
0
Polyelectrolytes
0
Types de publication
Journal Article
Research Support, N.I.H., Intramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
224-231Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Habchi, J., Tompa, P., Longhi, S. & Uversky, V. N. Introducing protein intrinsic disorder. Chem. Rev. 114, 6561–6588 (2014).
pubmed: 24739139
doi: 10.1021/cr400514h
Watson, M. & Stott, K. Disordered domains in chromatin-binding proteins. Essays Biochem. 63, 147–156 (2019).
pubmed: 30940742
doi: 10.1042/EBC20180068
Wright, P. E. & Dyson, H. J. Intrinsically disordered proteins in cellular signalling and regulation. Nat. Rev. Mol. Cell Biol. 16, 18–29 (2014).
doi: 10.1038/nrm3920
Fuxreiter, M. et al. Malleable machines take shape in eukaryotic transcriptional regulation. Nat. Chem. Biol. 4, 728–737 (2008).
pubmed: 19008886
pmcid: 2921704
doi: 10.1038/nchembio.127
Vuzman, D. & Levy, Y. Intrinsically disordered regions as affinity tuners in protein–DNA interactions. Mol. Biosyst. 8, 47–57 (2012).
pubmed: 21918774
doi: 10.1039/C1MB05273J
Borgia, A. et al. Extreme disorder in an ultrahigh-affinity protein complex. Nature 555, 61–66 (2018).
pubmed: 29466338
pmcid: 6264893
doi: 10.1038/nature25762
Turner, A. L. et al. Highly disordered histone H1–DNA model complexes and their condensates. Proc. Natl Acad. Sci. USA 115, 11964–11969 (2018).
Srivastava, S. & Tirrell, M. V. Polyelectrolyte complexation. Adv. Chem. Phys. 161, 499–544 (2016).
van der Gucht, J., Spruijt, E., Lemmers, M. & Cohen Stuart, M. A. Polyelectrolyte complexes: bulk phases and colloidal systems. J. Colloid Interface Sci. 361, 407–422 (2011).
pubmed: 21705008
doi: 10.1016/j.jcis.2011.05.080
Gibbs, E. B. & Kriwacki, R. W. Linker histones as liquid-like glue for chromatin. Proc. Natl Acad. Sci. USA 115, 11868–11870 (2018).
pubmed: 30389709
pmcid: 6255204
doi: 10.1073/pnas.1816936115
Larson, A. G. et al. Liquid droplet formation by HP1α suggests a role for phase separation in heterochromatin. Nature 547, 236–240 (2017).
pubmed: 28636604
pmcid: 5606208
doi: 10.1038/nature22822
Schuler, B. et al. Binding without folding – the biomolecular function of disordered polyelectrolyte complexes. Curr. Opin. Struct. Biol. 60, 66–76 (2019).
pubmed: 31874413
doi: 10.1016/j.sbi.2019.12.006
Korolev, N., Allahverdi, A., Lyubartsev, A. P. & Nordenskiold, L. The polyelectrolyte properties of chromatin. Soft Matter 8, 9322–9333 (2012).
doi: 10.1039/c2sm25662b
Hergeth, S. P. & Schneider, R. The H1 linker histones: multifunctional proteins beyond the nucleosomal core particle. EMBO Rep. 16, 1439–1453 (2015).
pubmed: 26474902
pmcid: 4641498
doi: 10.15252/embr.201540749
Cutter, A. R. & Hayes, J. J. A brief review of nucleosome structure. FEBS Lett. 589, 2914–2922 (2015).
pubmed: 25980611
pmcid: 4598263
doi: 10.1016/j.febslet.2015.05.016
Öztürk, M. A., De, M., Cojocaru, V. & Wade, R. C. Chromatosome structure and dynamics from molecular simulations. Annu. Rev. Phys. Chem. 71, 101–119 (2020).
pubmed: 32017651
doi: 10.1146/annurev-physchem-071119-040043
Willcockson, M. A. et al. H1 histones control the epigenetic landscape by local chromatin compaction. Nature 589, 293–298 (2021).
pubmed: 33299182
doi: 10.1038/s41586-020-3032-z
Gibson, B. A. et al. Organization of chromatin by intrinsic and regulated phase separation. Cell 179, 470–484, e421 (2019).
pubmed: 31543265
pmcid: 6778041
doi: 10.1016/j.cell.2019.08.037
Flanagan, T. W. & Brown, D. T. Molecular dynamics of histone H1. Biochim. Biophys. Acta 1859, 468–475 (2016).
pubmed: 26454113
doi: 10.1016/j.bbagrm.2015.10.005
George, E. M. & Brown, D. T. Prothymosin α is a component of a linker histone chaperone. FEBS Lett. 584, 2833–2836 (2010).
pubmed: 20434447
pmcid: 2891112
doi: 10.1016/j.febslet.2010.04.065
Gomez-Marquez, J. & Rodríguez, P. Prothymosin α is a chromatin-remodelling protein in mammalian cells. Biochem. J. 333, 1–3 (1998).
pubmed: 9639554
pmcid: 1219547
doi: 10.1042/bj3330001
Karetsou, Z. et al. Prothymosin α modulates the interaction of histone H1 with chromatin. Nucleic Acids Res. 26, 3111–3118 (1998).
pubmed: 9628907
pmcid: 147683
doi: 10.1093/nar/26.13.3111
Peng, B. & Muthukumar, M. Modeling competitive substitution in a polyelectrolyte complex. J. Chem. Phys. 143, 243133 (2015).
pubmed: 26723618
pmcid: 4662678
doi: 10.1063/1.4936256
Mao, A. H., Crick, S. L., Vitalis, A., Chicoine, C. L. & Pappu, R. V. Net charge per residue modulates conformational ensembles of intrinsically disordered proteins. Proc. Natl Acad. Sci. USA 107, 8183–8188 (2010).
pubmed: 20404210
pmcid: 2889596
doi: 10.1073/pnas.0911107107
Müller-Späth, S. et al. Charge interactions can dominate the dimensions of intrinsically disordered proteins. Proc. Natl Acad. Sci. USA 107, 14609–14614 (2010).
pubmed: 20639465
pmcid: 2930438
doi: 10.1073/pnas.1001743107
Lowary, P. T. & Widom, J. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 276, 19–42 (1998).
pubmed: 9514715
doi: 10.1006/jmbi.1997.1494
Fang, H., Clark, D. J. & Hayes, J. J. DNA and nucleosomes direct distinct folding of a linker histone H1 C-terminal domain. Nucleic Acids Res. 40, 1475–1484 (2012).
pubmed: 22021384
doi: 10.1093/nar/gkr866
White, A. E., Hieb, A. R. & Luger, K. A quantitative investigation of linker histone interactions with nucleosomes and chromatin. Sci. Rep. 6, 19122 (2016).
pubmed: 26750377
pmcid: 4707517
doi: 10.1038/srep19122
Bednar, J. et al. Structure and dynamics of a 197 bp nucleosome in complex with linker histone H1. Mol. Cell 66, 384–397.e8 (2017).
pubmed: 28475873
pmcid: 5508712
doi: 10.1016/j.molcel.2017.04.012
Sridhar, A. et al. Emergence of chromatin hierarchical loops from protein disorder and nucleosome asymmetry. Proc. Natl Acad. Sci. USA 117, 7216–7224 (2020).
Syed, S. H. et al. Single-base resolution mapping of H1–nucleosome interactions and 3D organization of the nucleosome. Proc. Natl Acad. Sci. USA 107, 9620–9625 (2010).
pubmed: 20457934
pmcid: 2906896
doi: 10.1073/pnas.1000309107
Record, M. T. Jr, Anderson, C. F. & Lohman, T. M. Thermodynamic analysis of ion effects on the binding and conformational equilibria of proteins and nucleic acids: the roles of ion association or release, screening, and ion effects on water activity. Q. Rev. Biophys. 11, 103–178 (1978).
pubmed: 353875
doi: 10.1017/S003358350000202X
Anderson, C. F. & Record, M. T. Jr. Salt-nucleic acid interactions. Annu. Rev. Phys. Chem. 46, 657–700 (1995).
pubmed: 7495482
doi: 10.1146/annurev.pc.46.100195.003301
Brown, D. T., Izard, T. & Misteli, T. Mapping the interaction surface of linker histone H1
pubmed: 16462749
pmcid: 1868459
doi: 10.1038/nsmb1050
Gansen, A. et al. High precision FRET studies reveal reversible transitions in nucleosomes between microseconds and minutes. Nat. Commun. 9, 4628 (2018).
pubmed: 30401903
pmcid: 6219519
doi: 10.1038/s41467-018-06758-1
Gansen, A. et al. Nucleosome disassembly intermediates characterized by single-molecule FRET. Proc. Natl Acad. Sci. USA 106, 15308–15313 (2009).
pubmed: 19706432
pmcid: 2741247
doi: 10.1073/pnas.0903005106
Gopich, I. V. & Szabo, A. Decoding the pattern of photon colors in single-molecule FRET. J. Phys. Chem. B 113, 10965–10973 (2009).
pubmed: 19588948
pmcid: 2802060
doi: 10.1021/jp903671p
Lever, M. A., Th’ng, J. P., Sun, X. & Hendzel, M. J. Rapid exchange of histone H1.1 on chromatin in living human cells. Nature 408, 873–876 (2000).
pubmed: 11130728
doi: 10.1038/35048603
Misteli, T., Gunjan, A., Hock, R., Bustin, M. & Brown, D. T. Dynamic binding of histone H1 to chromatin in living cells. Nature 408, 877–881 (2000).
pubmed: 11130729
doi: 10.1038/35048610
Bednar, J., Hamiche, A. & Dimitrov, S. H1–nucleosome interactions and their functional implications. Biochim. Biophys. Acta 1859, 436–443 (2015).
pubmed: 26477489
doi: 10.1016/j.bbagrm.2015.10.012
Bryan, L. C. et al. Single-molecule kinetic analysis of HP1-chromatin binding reveals a dynamic network of histone modification and DNA interactions. Nucleic Acids Res. 45, 10504–10517 (2017).
pubmed: 28985346
pmcid: 5737501
doi: 10.1093/nar/gkx697
Papamarcaki, T. & Tsolas, O. Prothymosin α binds to histone H1 in vitro. FEBS Lett. 345, 71–75 (1994).
pubmed: 8194604
doi: 10.1016/0014-5793(94)00439-0
Sottini, A. et al. Polyelectrolyte interactions enable rapid association and dissociation in high-affinity disordered protein complexes. Nat. Commun. 11, 5736 (2020).
pubmed: 33184256
pmcid: 7661507
doi: 10.1038/s41467-020-18859-x
Haritos, A. A., Salvin, S. B., Blacher, R., Stein, S. & Horecker, B. L. Parathymosin alpha: a peptide from rat tissues with structural homology to prothymosin alpha. Proc. Natl Acad. Sci. USA 82, 1050–1053 (1985).
pubmed: 3856246
pmcid: 397191
doi: 10.1073/pnas.82.4.1050
Chen, T. Y., Cheng, Y. S., Huang, P. S. & Chen, P. Facilitated unbinding via multivalency-enabled ternary complexes: new paradigm for protein–DNA interactions. Acc. Chem. Res. 51, 860–868 (2018).
pubmed: 29368512
pmcid: 5904000
doi: 10.1021/acs.accounts.7b00541
Gibb, B. et al. Concentration-dependent exchange of replication protein A on single-stranded DNA revealed by single-molecule imaging. PLoS ONE 9, e87922 (2014).
pubmed: 24498402
pmcid: 3912175
doi: 10.1371/journal.pone.0087922
Kamar, R. I. et al. Facilitated dissociation of transcription factors from single DNA binding sites. Proc. Natl Acad. Sci. USA 114, E3251–E3257 (2017).
pubmed: 28364020
pmcid: 5402408
doi: 10.1073/pnas.1701884114
Lewis, J. S. et al. Single-molecule visualization of fast polymerase turnover in the bacterial replisome. eLife 6, e23932 (2017).
pubmed: 28432790
pmcid: 5419744
doi: 10.7554/eLife.23932
Potoyan, D. A., Zheng, W. H., Komives, E. A. & Wolynes, P. G. Molecular stripping in the NF-κB/IκB/DNA genetic regulatory network. Proc. Natl Acad. Sci. USA 113, 110–115 (2016).
pubmed: 26699500
doi: 10.1073/pnas.1520483112
Wu, H., Dalal, Y. & Papoian, G. A. Binding dynamics of disordered linker histone H1 with a nucleosomal particle. J. Mol. Biol. 433, 166881 (2021).
pubmed: 33617899
doi: 10.1016/j.jmb.2021.166881
Fang, H., Wei, S., Lee, T. H. & Hayes, J. J. Chromatin structure-dependent conformations of the H1 CTD. Nucleic Acids Res. 44, 9131–9141 (2016).
pubmed: 27365050
pmcid: 5100576
Soranno, A. et al. Quantifying internal friction in unfolded and intrinsically disordered proteins with single-molecule spectroscopy. Proc. Natl Acad. Sci. USA 109, 17800–17806 (2012).
pubmed: 22492978
pmcid: 3497802
doi: 10.1073/pnas.1117368109
Nettels, D., Gopich, I. V., Hoffmann, A. & Schuler, B. Ultrafast dynamics of protein collapse from single-molecule photon statistics. Proc. Natl. Acad. Sci. USA 104, 2655–2660 (2007).
pubmed: 17301233
pmcid: 1815237
doi: 10.1073/pnas.0611093104
Kenzaki, H. & Takada, S. Partial unwrapping and histone tail dynamics in nucleosome revealed by coarse-grained molecular simulations. PLoS Comput. Biol. 11, e1004443 (2015).
pubmed: 26262925
pmcid: 4532510
doi: 10.1371/journal.pcbi.1004443
Zhang, B., Zheng, W., Papoian, G. A. & Wolynes, P. G. Exploring the free energy landscape of nucleosomes. J. Am. Chem. Soc. 138, 8126–8133 (2016).
pubmed: 27300314
doi: 10.1021/jacs.6b02893
Holmstrom, E. D., Liu, Z. W., Nettels, D., Best, R. B. & Schuler, B. Disordered RNA chaperones can enhance nucleic acid folding via local charge screening. Nat. Commun. 10, 245 (2019).
doi: 10.1038/s41467-019-10356-0
Korolev, N., Fan, Y., Lyubartsev, A. P. & Nordenskiold, L. Modelling chromatin structure and dynamics: status and prospects. Curr. Opin. Struct. Biol. 22, 151–159 (2012).
pubmed: 22305428
doi: 10.1016/j.sbi.2012.01.006
Lu, X., Hamkalo, B., Parseghian, M. H. & Hansen, J. C. Chromatin condensing functions of the linker histone C-terminal domain are mediated by specific amino acid composition and intrinsic protein disorder. Biochemistry 48, 164–172 (2009).
pubmed: 19072710
doi: 10.1021/bi801636y
Shoemaker, B. A., Portman, J. J. & Wolynes, P. G. Speeding molecular recognition by using the folding funnel: the fly-casting mechanism. Proc. Natl Acad. Sci. USA 97, 8868–8873 (2000).
pubmed: 10908673
pmcid: 16787
doi: 10.1073/pnas.160259697
Vareli, K., Tsolas, O. & Frangou-Lazaridis, M. Regulation of prothymosin α during the cell cycle. Eur. J. Biochem. 238, 799–806 (1996).
pubmed: 8706683
doi: 10.1111/j.1432-1033.1996.0799w.x
Wang, S. et al. Linker histone defines structure and self-association behaviour of the 177 bp human chromatosome. Sci. Rep. 11, 380 (2021).
pubmed: 33432055
pmcid: 7801413
doi: 10.1038/s41598-020-79654-8
Catez, F., Ueda, T. & Bustin, M. Determinants of histone H1 mobility and chromatin binding in living cells. Nat. Struct. Mol. Biol. 13, 305–310 (2006).
pubmed: 16715048
pmcid: 3730444
doi: 10.1038/nsmb1077
Annalisa, I. & Robert, S. The role of linker histone H1 modifications in the regulation of gene expression and chromatin dynamics. Biochim. Biophys. Acta 1859, 486–495 (2015).
Privalov, P. L., Dragan, A. I. & Crane-Robinson, C. Interpreting protein/DNA interactions: distinguishing specific from non-specific and electrostatic from non-electrostatic components. Nucleic Acids Res. 39, 2483–2491 (2011).
pubmed: 21071403
doi: 10.1093/nar/gkq984
Shakya, A., Park, S., Rana, N. & King, J. T. Liquid-liquid phase separation of histone proteins in cells: role in chromatin organization. Biophys. J. 118, 753–764 (2020).
pubmed: 31952807
doi: 10.1016/j.bpj.2019.12.022
Scott, K. A., Steward, A., Fowler, S. B. & Clarke, J. Titin; a multidomain protein that behaves as the sum of its parts. J. Mol. Biol. 315, 819–829 (2002).
pubmed: 11812150
doi: 10.1006/jmbi.2001.5260
Kilic, S., Bachmann, A. L., Bryan, L. C. & Fierz, B. Multivalency governs HP1α association dynamics with the silent chromatin state. Nat. Commun. 6, 7313 (2015).
pubmed: 26084584
doi: 10.1038/ncomms8313
Lowary, P. T. & Widom, J. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 276, 19–42 (1998).
pubmed: 9514715
doi: 10.1006/jmbi.1997.1494
Dyer, P. N. et al. Reconstitution of Nnucleosome core particles from recombinant histones and DNA. Methods Enzymol. 375, 23–44 (2004).
pubmed: 14870657
doi: 10.1016/S0076-6879(03)75002-2
Müller, B. K., Zaychikov, E., Bräuchle, C. & Lamb, D. C. Pulsed interleaved excitation. Biophys. J. 89, 3508–3522 (2005).
pubmed: 16113120
pmcid: 1366845
doi: 10.1529/biophysj.105.064766
Klehs, K. et al. Increasing the brightness of cyanine fluorophores for single-molecule and superresolution imaging. ChemPhysChem 15, 637–641 (2014).
pubmed: 24376142
doi: 10.1002/cphc.201300874
Aitken, C. E., Marshall, R. A. & Puglisi, J. D. An oxygen scavenging system for improvement of dye stability in single-molecule fluorescence experiments. Biophys. J. 94, 1826–1835 (2008).
pubmed: 17921203
pmcid: 2242739
doi: 10.1529/biophysj.107.117689
Ha, T. & Tinnefeld, P. Photophysics of fluorescence probes for single-molecule biophysics and super-resolution imaging. Ann. Rev. Phys. Chem. 63, 595–617 (2012).
Schuler, B. Application of single molecule Förster resonance energy transfer to protein folding. Methods Mol. Biol. 350, 115–138 (2007).
pubmed: 16957321
Nettels, D., Gopich, I. V., Hoffmann, A. & Schuler, B. Ultrafast dynamics of protein collapse from single-molecule photon statistics. Proc. Natl Acad. Sci. USA 104, 2655–2660 (2007).
pubmed: 17301233
pmcid: 1815237
doi: 10.1073/pnas.0611093104
Gopich, I. V., Nettels, D., Schuler, B. & Szabo, A. Protein dynamics from single-molecule fluorescence intensity correlation functions. J. Chem. Phys. 131, 095102 (2009).
pubmed: 19739874
pmcid: 2766399
doi: 10.1063/1.3212597
Holmstrom, E. D. et al. Accurate transfer efficiencies, distance distributions, and ensembles of unfolded and intrinsically disordered proteins from single-molecule FRET. Methods Enzymol. 611, 287–325 (2018).
pubmed: 30471690
pmcid: 8018263
doi: 10.1016/bs.mie.2018.09.030
Zheng, W. et al. Inferring properties of disordered chains from FRET transfer efficiencies. J. Chem. Phys. 148, 123329 (2018).
pubmed: 29604882
pmcid: 5812746
doi: 10.1063/1.5006954
Gopich, I. V. & Szabo, A. Theory of the energy transfer efficiency and fluorescence lifetime distribution in single-molecule FRET. Proc. Natl Acad. Sci. USA 109, 7747–7752 (2012).
pubmed: 22550169
pmcid: 3356627
doi: 10.1073/pnas.1205120109
Sisamakis, E., Valeri, A., Kalinin, S., Rothwell, P. J. & Seidel, C. A. M. Accurate single-molecule FRET studies using multiparameter fluorescence detection. Methods Enzymol. 475, 455–514 (2010).
pubmed: 20627168
doi: 10.1016/S0076-6879(10)75018-7
Hellenkamp, B. et al. Precision and accuracy of single-molecule FRET measurements—a multi-laboratory benchmark study. Nat. Methods 15, 669–676 (2018).
pubmed: 30171252
pmcid: 6121742
doi: 10.1038/s41592-018-0085-0
Zosel, F., Mercadante, D., Nettels, D. & Schuler, B. A proline switch explains kinetic heterogeneity in a coupled folding and binding reaction. Nat. Commun. 9, 3332 (2018).
pubmed: 30127362
pmcid: 6102232
doi: 10.1038/s41467-018-05725-0
Chung, H. S. et al. Extracting rate coefficients from single-molecule photon trajectories and FRET efficiency histograms for a fast-folding protein. J. Phys. Chem. A 115, 3642–3656 (2011).
pubmed: 20509636
doi: 10.1021/jp1009669
Viterbi, A. J. Error bounds for convolutional codes and an asymptotically optimum decoding algorithm. IEEE Trans. Inf. Theory 13, 260–269 (1967).
doi: 10.1109/TIT.1967.1054010
Karanicolas, J. & Brooks, C. L. III The origins of asymmetry in the folding transition states of protein L and protein G. Protein Sci. 11, 2351–2361 (2002).
pubmed: 12237457
pmcid: 2373711
doi: 10.1110/ps.0205402
Kim, Y. C. & Hummer, G. Coarse-grained models for simulations of multiprotein complexes: application to ubiquitin binding. J. Mol. Biol. 375, 1416–1433 (2008).
pubmed: 18083189
doi: 10.1016/j.jmb.2007.11.063
Yakovchuk, P., Protozanova, E. & Frank-Kamenetskii, M. D. Base-stacking and base-pairing contributions into thermal stability of the DNA double helix. Nucleic Acids Res. 34, 564–574 (2006).
pubmed: 16449200
pmcid: 1360284
doi: 10.1093/nar/gkj454
Zhou, B. R. et al. Structural insights into the histone H1–nucleosome complex. Proc. Natl Acad. Sci. USA 110, 19390–19395 (2013).
pubmed: 24218562
pmcid: 3845106
doi: 10.1073/pnas.1314905110
Zhou, Y. B., Gerchman, S. E., Ramakrishnan, V., Travers, A. & Muyldermans, S. Position and orientation of the globular domain of linker histone H5 on the nucleosome. Nature 395, 402–405 (1998).
pubmed: 9759733
doi: 10.1038/26521
Berendsen, H. J. C., van der Spoel, D. & van Drunen, R. GROMACS: a message-passing parallel molecular dynamics implementation. Comp. Phys. Comm. 91, 43–56 (1995).
doi: 10.1016/0010-4655(95)00042-E
van der Spoel, D. et al. GROMACS: fast, flexible, and free. J. Comput. Chem. 26, 1701–1718 (2005).
doi: 10.1002/jcc.20291
Aznauryan, M. et al. Comprehensive structural and dynamical view of an unfolded protein from the combination of single-molecule FRET, NMR, and SAXS. Proc. Natl Acad. Sci. USA 113, E5389–E5398 (2016).
pubmed: 27566405
pmcid: 5027429
doi: 10.1073/pnas.1607193113
Lin, L. I. A concordance correlation coefficient to evaluate reproducibility. Biometrics 45, 255–268 (1989).
pubmed: 2720055
doi: 10.2307/2532051
Tribello, G. A., Bonomi, M., Branduardi, D., Camilloni, C. & Bussi, G. Plumed 2: new feathers for an old bird. Comput. Phys. Commun. 185, 604–613 (2014).
doi: 10.1016/j.cpc.2013.09.018
Sugita, Y., Kitao, A. & Okamoto, Y. Multidimensional replica-exchange method for free-energy calculations. J. Chem. Phys. 113, 6042–6051 (2000).
doi: 10.1063/1.1308516
Kumar, S., Rosenberg, J. M., Bouzida, D., Swendsen, R. H. & Kollman, P. A. The weighted histogram analysis method for free-energy calculations on biomolecules. I. The method. J. Comp. Chem. 13, 1011–1021 (1992).
doi: 10.1002/jcc.540130812
Shoup, D. & Szabo, A. Role of diffusion in ligand binding to macromolecules and cell-bound receptors. Biophys. J. 40, 33–39 (1982).
pubmed: 7139033
pmcid: 1328970
doi: 10.1016/S0006-3495(82)84455-X