RNAs undergo phase transitions with lower critical solution temperatures.
Journal
Nature chemistry
ISSN: 1755-4349
Titre abrégé: Nat Chem
Pays: England
ID NLM: 101499734
Informations de publication
Date de publication:
Dec 2023
Dec 2023
Historique:
received:
19
10
2022
accepted:
19
09
2023
medline:
6
12
2023
pubmed:
7
11
2023
entrez:
6
11
2023
Statut:
ppublish
Résumé
Co-phase separation of RNAs and RNA-binding proteins drives the biogenesis of ribonucleoprotein granules. RNAs can also undergo phase transitions in the absence of proteins. However, the physicochemical driving forces of protein-free, RNA-driven phase transitions remain unclear. Here we report that various types of RNA undergo phase separation with system-specific lower critical solution temperatures. This entropically driven phase separation is an intrinsic feature of the phosphate backbone that requires Mg
Identifiants
pubmed: 37932412
doi: 10.1038/s41557-023-01353-4
pii: 10.1038/s41557-023-01353-4
doi:
Substances chimiques
RNA
63231-63-0
RNA, Catalytic
0
RNA-Binding Proteins
0
Phosphates
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1693-1704Subventions
Organisme : NIGMS NIH HHS
ID : R35 GM138186
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM138186
Pays : United States
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Brangwynne, C. P. et al. Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science 324, 1729–1732 (2009).
pubmed: 19460965
doi: 10.1126/science.1172046
Molliex, A. et al. Phase separation by low complexity domains promotes stress granule assembly and drives pathological fibrillization. Cell 163, 123–133 (2015).
pubmed: 26406374
pmcid: 5149108
doi: 10.1016/j.cell.2015.09.015
Li, P. et al. Phase transitions in the assembly of multivalent signalling proteins. Nature 483, 336–340 (2012).
pubmed: 22398450
pmcid: 3343696
doi: 10.1038/nature10879
Berry, J., Weber, S. C., Vaidya, N., Haataja, M. & Brangwynne, C. P. RNA transcription modulates phase transition-driven nuclear body assembly. Proc. Natl Acad. Sci. USA 112, E5237–E5245 (2015).
pubmed: 26351690
pmcid: 4586886
doi: 10.1073/pnas.1509317112
Woodruff, J. B. et al. The centrosome is a selective condensate that nucleates microtubules by concentrating tubulin. Cell 169, 1066–1077 (2017).
Zeng, M. et al. Phase transition in postsynaptic densities underlies formation of synaptic complexes and synaptic plasticity. Cell 166, 1163–1175 (2016).
Jiang, H. et al. Phase transition of spindle-associated protein regulate spindle apparatus assembly. Cell 163, 108–122 (2015).
pubmed: 26388440
pmcid: 4607269
doi: 10.1016/j.cell.2015.08.010
Patel, A. et al. A liquid-to-solid phase transition of the ALS protein FUS accelerated by disease mutation. Cell 162, 1066–1077 (2015).
pubmed: 26317470
doi: 10.1016/j.cell.2015.07.047
Martin, E. W. et al. Valence and patterning of aromatic residues determine the phase behavior of prion-like domains. Science 367, 694–699 (2020).
pubmed: 32029630
pmcid: 7297187
doi: 10.1126/science.aaw8653
Dzuricky, M., Rogers, B. A., Shahid, A., Cremer, P. S. & Chilkoti, A. De novo engineering of intracellular condensates using artificial disordered proteins. Nat. Chem. 12, 814–825 (2020).
pubmed: 32747754
pmcid: 8281385
doi: 10.1038/s41557-020-0511-7
Shin, Y. et al. Spatiotemporal control of intracellular phase transitions using light-activated optoDroplets. Cell 168, 159–171 (2017).
Nakamura, H. et al. Intracellular production of hydrogels and synthetic RNA granules by multivalent molecular interactions. Nat. Mater. 17, 79–89 (2018).
pubmed: 29115293
doi: 10.1038/nmat5006
Zhao, E. M. et al. Light-based control of metabolic flux through assembly of synthetic organelles. Nat. Chem. Biol. 15, 589–597 (2019).
pubmed: 31086330
pmcid: 6755918
doi: 10.1038/s41589-019-0284-8
Wang, J. et al. A molecular grammar governing the driving forces for phase separation of prion-like RNA binding proteins. Cell 174, 688–699 (2018).
Lin, Y.-H., Forman-Kay, J. D. & Chan, H. S. Sequence-specific polyampholyte phase separation in membraneless organelles. Phys. Rev. Lett. 117, 178101 (2016).
pubmed: 27824447
doi: 10.1103/PhysRevLett.117.178101
Alshareedah, I., Moosa, M. M., Raju, M., Potoyan, D. A. & Banerjee, P. R. Phase transition of RNA−protein complexes into ordered hollow condensates. Proc. Natl Acad. Sci. USA 117, 15650–15658 (2020).
pubmed: 32571937
pmcid: 7354941
doi: 10.1073/pnas.1922365117
Garcia-Jove Navarro, M. et al. RNA is a critical element for the sizing and the composition of phase-separated RNA–protein condensates. Nat. Commun. 10, 3230 (2019).
pubmed: 31324804
pmcid: 6642089
doi: 10.1038/s41467-019-11241-6
Roden, C. & Gladfelter, A. S. RNA contributions to the form and function of biomolecular condensates. Nat. Rev. Mol. Cell Biol. 22, 183–195 (2021).
pubmed: 32632317
doi: 10.1038/s41580-020-0264-6
Tauber, D., Tauber, G. & Parker, R. Mechanisms and regulation of RNA condensation in RNP granule formation. Trends Biochem. Sci. 45, 764–778 (2020).
pubmed: 32475683
pmcid: 7211619
doi: 10.1016/j.tibs.2020.05.002
Banerjee, P. R., Milin, A. N., Moosa, M. M., Onuchic, P. L. & Deniz, A. A. Reentrant phase transition drives dynamic substructure formation in ribonucleoprotein droplets. Angew. Chem. 129, 11512–11517 (2017).
doi: 10.1002/ange.201703191
Eisenberg, H. & Felsenfeld, G. Studies of the temperature-dependent conformation and phase separation of polyriboadenylic acid solutions at neutral pH. J. Mol. Biol. 30, 17–37 (1967).
pubmed: 6077933
doi: 10.1016/0022-2836(67)90240-9
Pullara, P., Alshareedah, I. & Banerjee, P. R. Temperature-dependent reentrant phase transition of RNA–polycation mixtures. Soft Matter 18, 1342–1349 (2022).
pubmed: 34984429
pmcid: 8854377
doi: 10.1039/D1SM01557E
Van Treeck, B. et al. RNA self-assembly contributes to stress granule formation and defining the stress granule transcriptome. Proc. Natl Acad. Sci. USA 115, 2734–2739 (2018).
pubmed: 29483269
pmcid: 5856561
doi: 10.1073/pnas.1800038115
Boeynaems, S. et al. Spontaneous driving forces give rise to protein−RNA condensates with coexisting phases and complex material properties. Proc. Natl Acad. Sci. USA 116, 7889–7898 (2019).
pubmed: 30926670
pmcid: 6475405
doi: 10.1073/pnas.1821038116
Jain, A. & Vale, R. D. RNA phase transitions in repeat expansion disorders. Nature 546, 243–247 (2017).
pubmed: 28562589
pmcid: 5555642
doi: 10.1038/nature22386
Fay, M. M. & Anderson, P. J. The role of RNA in biological phase separations. J. Mol. Biol. 430, 4685–4701 (2018).
pubmed: 29753780
pmcid: 6204303
doi: 10.1016/j.jmb.2018.05.003
Guo, Q., Shi, X. & Wang, X. RNA and liquid–liquid phase separation. Noncoding RNA Res. 6, 92–99 (2021).
pubmed: 33997539
pmcid: 8111091
doi: 10.1016/j.ncrna.2021.04.003
Polymenidou, M. The RNA face of phase separation. Science 360, 859–860 (2018).
pubmed: 29798872
doi: 10.1126/science.aat8028
Saha, S. & Hyman, A. A. RNA gets in phase. J. Cell Biol. 216, 2235–2237 (2017).
pubmed: 28667121
pmcid: 5551722
doi: 10.1083/jcb.201706034
Weber, S. C. & Brangwynne, C. P. Getting RNA and protein in phase. Cell 149, 1188–1191 (2012).
pubmed: 22682242
doi: 10.1016/j.cell.2012.05.022
Ma, Y. et al. Nucleobase clustering contributes to the formation and hollowing of repeat-expansion RNA condensate. J. Am. Chem. Soc. 144, 4716–4720 (2022).
pubmed: 35179357
doi: 10.1021/jacs.1c12085
Poudyal, R. R., Sieg, J. P., Portz, B., Keating, C. D. & Bevilacqua, P. C. RNA sequence and structure control assembly and function of RNA condensates. RNA 27, 1589–1601 (2021).
pubmed: 34551999
pmcid: 8594466
doi: 10.1261/rna.078875.121
Tolokh, I. S. et al. Why double-stranded RNA resists condensation. Nucleic Acids Res. 42, 10823–10831 (2014).
pubmed: 25123663
pmcid: 4176364
doi: 10.1093/nar/gku756
Fay, M. M., Anderson, P. J. & Ivanov, P. ALS/FTD-associated C9ORF72 repeat RNA promotes phase transitions in vitro and in cells. Cell Reports 21, 3573–3584 (2017).
pubmed: 29262335
doi: 10.1016/j.celrep.2017.11.093
Gatchel, J. R. & Zoghbi, H. Y. Diseases of unstable repeat expansion: mechanisms and common principles. Nat. Rev. Genet. 6, 743–755 (2005).
pubmed: 16205714
doi: 10.1038/nrg1691
Zhang, Y. et al. G-quadruplex structures trigger RNA phase separation. Nucleic Acids Res. 47, 11746–11754 (2019).
pubmed: 31722410
pmcid: 7145655
Choi, J.-M., Hyman, A. A. & Pappu, R. V. Generalized models for bond percolation transitions of associative polymers. Phys. Rev. E 102, 042403 (2020).
pubmed: 33212590
doi: 10.1103/PhysRevE.102.042403
Choi, J.-M., Holehouse, A. S. & Pappu, R. V. Physical principles underlying the complex biology of intracellular phase transitions. Annu. Rev. Biophys. 49, 107–133 (2020).
pubmed: 32004090
doi: 10.1146/annurev-biophys-121219-081629
Futscher, M. H., Philipp, M., Müller-Buschbaum, P. & Schulte, A. The role of backbone hydration of poly(N-isopropyl acrylamide) across the volume phase transition compared to its monomer. Sci. Rep. 7, 17012 (2017).
pubmed: 29208941
pmcid: 5717149
doi: 10.1038/s41598-017-17272-7
Halperin, A., Kröger, M. & Winnik, F. M. Poly(N-isopropylacrylamide) phase diagrams: fifty years of research. Angew. Chem. Int. Ed. 54, 15342–15367 (2015).
doi: 10.1002/anie.201506663
Tanaka, F. Theoretical study of molecular association and thermoreversible gelation in polymers. Polym. J. 34, 479–509 (2002).
doi: 10.1295/polymj.34.479
Tanaka, F. In Molecular Gels: Materials with Self-Assembled Fibrillar Networks (eds. R.G. Weiss and P. Terech) 17–78 (Springer, 2006).
Tanaka, F. Polymer Physics: Applications to Molecular Association and Thermoreversible Gelation (Cambridge Univ. Press, 2011).
doi: 10.1017/CBO9780511975691
Rubinstein, M. & Dobrynin, A. V. Solutions of associative polymers. Trends in Polymer Science 5, 181–186 (1997).
Mittag, T. & Pappu, R. V. A conceptual framework for understanding phase separation and addressing open questions and challenges. Mol. Cell 82, 2201–2214 (2022).
Su, X. et al. Phase separation of signaling molecules promotes T cell receptor signal transduction. Science 352, 595–599 (2016).
pubmed: 27056844
pmcid: 4892427
doi: 10.1126/science.aad9964
Bhandari, K., Cotten, M. A., Kim, J., Rosen, M. K. & Schmit, J. D. Structure–function properties in disordered condensates. J. Phys. Chem. B 125, 467–476 (2021).
pubmed: 33395293
pmcid: 8194388
doi: 10.1021/acs.jpcb.0c11057
Bevilacqua, P. C., Williams, A. M., Chou, H.-L. & Assmann, S. M. RNA multimerization as an organizing force for liquid–liquid phase separation. RNA 28, 16–26 (2022).
pubmed: 34706977
pmcid: 8675289
doi: 10.1261/rna.078999.121
Johansson, J. et al. An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell 110, 551–561 (2002).
pubmed: 12230973
doi: 10.1016/S0092-8674(02)00905-4
Puglisi, J. D. & Tinoco, I. Jr. In Methods in Enzymology (eds. J.E. Dahlberg and J.N. Abelson) Vol. 180, 304–325 (Elsevier, 1989).
Tinoco, I. Jr & Bustamante, C. How RNA folds. J. Mol. Biol. 293, 271–281 (1999).
pubmed: 10550208
doi: 10.1006/jmbi.1999.3001
Vicens, Q. & Kieft, J. S. Thoughts on how to think (and talk) about RNA structure. Proc. Natl Acad. Sci. USA 119, e2112677119 (2022).
pubmed: 35439059
pmcid: 9169933
doi: 10.1073/pnas.2112677119
Wienken, C. J., Baaske, P., Duhr, S. & Braun, D. Thermophoretic melting curves quantify the conformation and stability of RNA and DNA. Nucleic Acids Res. 39, e52 (2011).
pubmed: 21297115
pmcid: 3082908
doi: 10.1093/nar/gkr035
Flory, P. J. Thermodynamics of high polymer solutions. J. Chem. Phys. 10, 51–61 (1942).
doi: 10.1063/1.1723621
Huggins, M. L. Solutions of long chain compounds. J. Chem. Phys. 9, 440 (1941).
doi: 10.1063/1.1750930
Ranganathan, S. & Shakhnovich, E. I. Dynamic metastable long-living droplets formed by sticker-spacer proteins. Elife 9, e56159 (2020).
pubmed: 32484438
pmcid: 7360371
doi: 10.7554/eLife.56159
Roberts, S. et al. Injectable tissue integrating networks from recombinant polypeptides with tunable order. Nat. Mater. 17, 1154–1163 (2018).
pubmed: 30323334
pmcid: 6329288
doi: 10.1038/s41563-018-0182-6
Onuchic, P. L., Milin, A. N., Alshareedah, I., Deniz, A. A. & Banerjee, P. R. Divalent cations can control a switch-like behavior in heterotypic and homotypic RNA coacervates. Sci. Rep. 9, 12161 (2019).
pubmed: 31434954
pmcid: 6704260
doi: 10.1038/s41598-019-48457-x
Merindol, R., Loescher, S., Samanta, A. & Walther, A. Pathway-controlled formation of mesostructured all-DNA colloids and superstructures. Nat. Nanotechnol. 13, 730–738 (2018).
pubmed: 29941888
pmcid: 6082344
doi: 10.1038/s41565-018-0168-1
Ruff, K. M., Roberts, S., Chilkoti, A. & Pappu, R. V. Advances in understanding stimulus-responsive phase behavior of intrinsically disordered protein polymers. J. Mol. Biol. 430, 4619–4635 (2018).
pubmed: 29949750
doi: 10.1016/j.jmb.2018.06.031
Ellis, K. J. & Morrison, J. F. In Methods in Enzymology (ed. D.L. Purich) Vol. 87, 405–426 (Elsevier, 1982).
Zeng, X., Holehouse, A. S., Chilkoti, A., Mittag, T. & Pappu, R. V. Connecting coil-to-globule transitions to full phase diagrams for intrinsically disordered proteins. Biophys. J. 119, 402–418 (2020).
pubmed: 32619404
pmcid: 7376131
doi: 10.1016/j.bpj.2020.06.014
Zeng, X. et al. Design of intrinsically disordered proteins that undergo phase transitions with lower critical solution temperatures. APL Mater. 9, 021119 (2021).
doi: 10.1063/5.0037438
Amin, A. N., Lin, Y.-H., Das, S. & Chan, H. S. Analytical theory for sequence-specific binary fuzzy complexes of charged intrinsically disordered proteins. J. Phys. Chem. B 124, 6709–6720 (2020).
pubmed: 32639157
doi: 10.1021/acs.jpcb.0c04575
Dignon, G. L., Zheng, W., Best, R. B., Kim, Y. C. & Mittal, J. Relation between single-molecule properties and phase behavior of intrinsically disordered proteins. Proc. Natl Acad. Sci. USA 115, 9929–9934 (2018).
pubmed: 30217894
pmcid: 6176625
doi: 10.1073/pnas.1804177115
Lin, Y.-H. & Chan, H. S. Phase separation and single-chain compactness of charged disordered proteins are strongly correlated. Biophys. J. 112, 2043–2046 (2017).
pubmed: 28483149
pmcid: 5448239
doi: 10.1016/j.bpj.2017.04.021
May, S., Iglič, A., Reščič, J., Maset, S. & Bohinc, K. Bridging like-charged macroions through long divalent rodlike ions. J. Phys. Chem. B 112, 1685–1692 (2008).
pubmed: 18205341
doi: 10.1021/jp073355e
Fossat, M. J., Zeng, X. & Pappu, R. V. Uncovering differences in hydration free energies and structures for model compound mimics of charged side chains of amino acids. J. Phys. Chem. B 125, 4148–4161 (2021).
pubmed: 33877835
pmcid: 8154595
doi: 10.1021/acs.jpcb.1c01073
Zeng, X., Ruff, K. M. & Pappu, R. V. Competing interactions give rise to two-state behavior and switch-like transitions in charge-rich intrinsically disordered proteins. Proc. Natl Acad. Sci. USA 119, e2200559119 (2022).
pubmed: 35512095
pmcid: 9171777
doi: 10.1073/pnas.2200559119
Nguyen, H. T., Hori, N. & Thirumalai, D. Condensates in RNA repeat sequences are heterogeneously organized and exhibit reptation dynamics. Nat. Chem. 14, 775–785 (2022).
Harmon, T. S., Holehouse, A. S., Rosen, M. K. & Pappu, R. V. Intrinsically disordered linkers determine the interplay between phase separation and gelation in multivalent proteins. Elife 6, e30294 (2017).
pubmed: 29091028
pmcid: 5703641
doi: 10.7554/eLife.30294
Rubinstein, M. & Semenov, A. N. Thermoreversible gelation in solutions of associating polymers. 2. Linear dynamics. Macromolecules 31, 1386–1397 (1998).
doi: 10.1021/ma970617+
Phan, H.-D., Lai, L. B., Zahurancik, W. J. & Gopalan, V. The many faces of RNA-based RNase P, an RNA-world relic. Trends Biochem. Sci. 46, 976–991 (2021).
pubmed: 34511335
pmcid: 8595784
doi: 10.1016/j.tibs.2021.07.005
Gopalan, V., Vioque, A. & Altman, S. RNase P: variations and uses. J. Biol. Chem. 277, 6759–6762 (2002).
pubmed: 11741968
doi: 10.1074/jbc.R100067200
Guerrier-Takada, C., Gardiner, K., Marsh, T., Pace, N. & Altman, S. The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 35, 849–857 (1983).
pubmed: 6197186
doi: 10.1016/0092-8674(83)90117-4
Cho, I.-M., Lai, L. B., Susanti, D., Mukhopadhyay, B. & Gopalan, V. Ribosomal protein L7Ae is a subunit of archaeal RNase P. Proc. Natl Acad. Sci. USA 107, 14573–14578 (2010).
pubmed: 20675586
pmcid: 2930468
doi: 10.1073/pnas.1005556107
Phan, H.-D. et al. Elucidation of structure–function relationships in Methanocaldococcus jannaschii RNase P, a multi-subunit catalytic ribonucleoprotein. Nucleic Acids Res. 50, 8154–8167 (2022).
pubmed: 35848927
pmcid: 9371926
doi: 10.1093/nar/gkac595
Pulukkunat, D. K. & Gopalan, V. Studies on Methanocaldococcus jannaschii RNase P reveal insights into the roles of RNA and protein cofactors in RNase P catalysis. Nucleic Acids Res. 36, 4172–4180 (2008).
pubmed: 18558617
pmcid: 2475606
doi: 10.1093/nar/gkn360
Tsai, H.-Y., Pulukkunat, D. K., Woznick, W. K. & Gopalan, V. Functional reconstitution and characterization of Pyrococcus furiosus RNase P. Proc. Natl Acad. Sci. USA 103, 16147–16152 (2006).
pubmed: 17053064
pmcid: 1637551
doi: 10.1073/pnas.0608000103
Wan, F. et al. Cryo-electron microscopy structure of an archaeal ribonuclease P holoenzyme. Nat. Commun. 10, 2617 (2019).
pubmed: 31197137
pmcid: 6565675
doi: 10.1038/s41467-019-10496-3
Marathe, I. A. et al. Protein cofactors and substrate influence Mg
pubmed: 34387688
pmcid: 8450104
doi: 10.1093/nar/gkab655
Loughrey, D., Watters, K. E., Settle, A. H. & Lucks, J. B. SHAPE-Seq 2.0: systematic optimization and extension of high-throughput chemical probing of RNA secondary structure with next generation sequencing. Nucleic Acids Res. 42, e165 (2014).
pubmed: 25303992
pmcid: 4245970
doi: 10.1093/nar/gku909
Denesyuk, N. A. & Thirumalai, D. Coarse-grained model for predicting RNA folding thermodynamics. J. Phys. Chem. B 117, 4901–4911 (2013).
pubmed: 23527587
doi: 10.1021/jp401087x
Buchmueller, K. L. & Weeks, K. M. Tris-borate is a poor counterion for RNA: a cautionary tale for RNA folding studies. Nucleic Acids Res. 32, e184 (2004).
pubmed: 15601995
pmcid: 545480
doi: 10.1093/nar/gnh182
Iglesias-Artola, J. M. et al. Charge-density reduction promotes ribozyme activity in RNA–peptide coacervates via RNA fluidization and magnesium partitioning. Nat. Chem. 14, 407–416 (2022).
pubmed: 35165426
pmcid: 8979813
doi: 10.1038/s41557-022-00890-8
Poudyal, R. R. et al. Template-directed RNA polymerization and enhanced ribozyme catalysis inside membraneless compartments formed by coacervates. Nat. Commun. 10, 490 (2019).
pubmed: 30700721
pmcid: 6353945
doi: 10.1038/s41467-019-08353-4
Higgs, P. G. & Lehman, N. The RNA World: molecular cooperation at the origins of life. Nat. Rev. Genet. 16, 7–17 (2015).
pubmed: 25385129
doi: 10.1038/nrg3841
Drobot, B. et al. Compartmentalised RNA catalysis in membrane-free coacervate protocells. Nat. Commun. 9, 3643 (2018).
pubmed: 30194374
pmcid: 6128941
doi: 10.1038/s41467-018-06072-w
Wiedner, H. J. & Giudice, J. It’s not just a phase: function and characteristics of RNA-binding proteins in phase separation. Nat. Struct. Mol. Biol. 28, 465–473 (2021).
pubmed: 34099940
doi: 10.1038/s41594-021-00601-w
Van Treeck, B. & Parker, R. Emerging roles for intermolecular RNA–RNA interactions in RNP assemblies. Cell 174, 791–802 (2018).
pubmed: 30096311
pmcid: 6200146
doi: 10.1016/j.cell.2018.07.023
Cheng, Y. et al. Increased Alu RNA processing in Alzheimer brains is linked to gene expression changes. EMBO Rep. 22, e52255 (2021).
pubmed: 33645898
pmcid: 8097388
doi: 10.15252/embr.202052255
Lin, C.-L. G. et al. Aberrant RNA processing in a neurodegenerative disease: the cause for absent EAAT2, a glutamate transporter, in amyotrophic lateral sclerosis. Neuron 20, 589–602 (1998).
pubmed: 9539131
doi: 10.1016/S0896-6273(00)80997-6
Tank, E. M. et al. Abnormal RNA stability in amyotrophic lateral sclerosis. Nat. Commun. 9, 2845 (2018).
pubmed: 30030424
pmcid: 6054632
doi: 10.1038/s41467-018-05049-z
Tsai, H.-Y., Lai, L. B. & Gopalan, V. A modified pBluescript-based vector for facile cloning and transcription of RNAs. Anal. Biochem. 303, 214–217 (2002).
pubmed: 11950224
doi: 10.1006/abio.2001.5567
Taylor, N. O., Wei, M.-T., Stone, H. A. & Brangwynne, C. P. Quantifying dynamics in phase-separated condensates using fluorescence recovery after photobleaching. Biophys. J. 117, 1285–1300 (2019).
pubmed: 31540706
pmcid: 6818185
doi: 10.1016/j.bpj.2019.08.030
Sousa da Silva, A. W. & Vranken, W. F. ACPYPE—antechamber Python parser interface. BMC Res. Notes 5, 367 (2012).
pubmed: 22824207
pmcid: 3461484
doi: 10.1186/1756-0500-5-367
Vanquelef, E. et al. R.E.D. Server: a web service for deriving RESP and ESP charges and building force field libraries for new molecules and molecular fragments. Nucleic Acids Res. 39, W511–W517 (2011).
pubmed: 21609950
pmcid: 3125739
doi: 10.1093/nar/gkr288
Bayly, C. I., Cieplak, P., Cornell, W. & Kollman, P. A. A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: the RESP model. J. Phys. Chem. 97, 10269–10280 (1993).
doi: 10.1021/j100142a004
Duan, Y. et al. A point‐charge force field for molecular mechanics simulations of proteins based on condensed‐phase quantum mechanical calculations. J. Comput. Chem. 24, 1999–2012 (2003).
pubmed: 14531054
doi: 10.1002/jcc.10349
Lee, C., Yang, W. & Parr, R. G. Development of the Colle–Salvetti correlation-energy formula into a functional of the electron density. Phys. Rev. B 37, 785 (1988).
doi: 10.1103/PhysRevB.37.785
Becke, A. D. Density‐functional thermochemistry. III. The role of exact exchange. J. Chem. Phys. 98, 5648–5652 (1993).
doi: 10.1063/1.464913
Kendall, R. A., Dunning, T. H. Jr & Harrison, R. J. Electron affinities of the first‐row atoms revisited. Systematic basis sets and wave functions. J. Chem. Phys. 96, 6796–6806 (1992).
doi: 10.1063/1.462569
Steinbrecher, T., Latzer, J. & Case, D. Revised AMBER parameters for bioorganic phosphates. J. Chem. Theory Comput. 8, 4405–4412 (2012).
pubmed: 23264757
pmcid: 3524595
doi: 10.1021/ct300613v
Bergonzo, C. & Cheatham, T. E. III Improved force field parameters lead to a better description of RNA structure. J. Chem. Theory Comput. 11, 3969–3972 (2015).
pubmed: 26575892
doi: 10.1021/acs.jctc.5b00444
Grotz, K. K., Cruz-León, S. & Schwierz, N. Optimized magnesium force field parameters for biomolecular simulations with accurate solvation, ion-binding, and water-exchange properties. J. Chem. Theory Comput. 17, 2530–2540 (2021).
pubmed: 33720710
pmcid: 8047801
doi: 10.1021/acs.jctc.0c01281
Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W. & Klein, M. L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926–935 (1983).
doi: 10.1063/1.445869
Abraham, M. J. et al. GROMACS: high performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX 1, 19–25 (2015).
doi: 10.1016/j.softx.2015.06.001
Páll, S., Abraham, M. J., Kutzner, C., Hess, B. & Lindahl, E. Tackling exascale software challenges in molecular dynamics simulations with GROMACS. In International Conference on Exascale Applications and Software 2014 (eds. S. Markidis and E. Laure) 3–27 (Springer, 2014).
GROMACS 2021 manual. GROMACS development team https://doi.org/10.5281/zenodo.4457591 (2021).
Bussi, G., Donadio, D. & Parrinello, M. Canonical sampling through velocity rescaling. J. Chem. Phys. 126, 014101 (2007).
pubmed: 17212484
doi: 10.1063/1.2408420
Parrinello, M. & Rahman, A. Polymorphic transitions in single crystals: a new molecular dynamics method. J. Appl. Phys. 52, 7182–7190 (1981).
doi: 10.1063/1.328693
Nosé, S. & Klein, M. Constant pressure molecular dynamics for molecular systems. Mol. Phys. 50, 1055–1076 (1983).
doi: 10.1080/00268978300102851
Darden, T., York, D. & Pedersen, L. Particle mesh Ewald: an N⋅ log (N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089–10092 (1993).
doi: 10.1063/1.464397
Essmann, U. et al. A smooth particle mesh Ewald method. J. Chem. Phys. 103, 8577–8593 (1995).
doi: 10.1063/1.470117
Hess, B., Bekker, H., Berendsen, H. J. & Fraaije, J. G. LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem. 18, 1463–1472 (1997).
doi: 10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.0.CO;2-H
Zgarbová, M. et al. Refinement of the Cornell et al. nucleic acids force field based on reference quantum chemical calculations of glycosidic torsion profiles. J. Chem. Theory Comput. 7, 2886–2902 (2011).
pubmed: 21921995
pmcid: 3171997
doi: 10.1021/ct200162x
Ferrenberg, A. M. & Swendsen, R. H. Optimized Monte Carlo data analysis. Comput. Phys. 3, 101–104 (1989).
doi: 10.1063/1.4822862
Gallicchio, E., Andrec, M., Felts, A. K. & Levy, R. M. Temperature weighted histogram analysis method, replica exchange, and transition paths. J. Phys. Chem. B 109, 6722–6731 (2005).
pubmed: 16851756
doi: 10.1021/jp045294f