Driving forces of the complex formation between highly charged disordered proteins.
intrinsically disordered proteins
polyelectrolyte complexation
protein binding
single-molecule spectroscopy
Journal
Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876
Informations de publication
Date de publication:
10 10 2023
10 10 2023
Historique:
pmc-release:
05
04
2024
medline:
9
10
2023
pubmed:
5
10
2023
entrez:
5
10
2023
Statut:
ppublish
Résumé
Highly disordered complexes between oppositely charged intrinsically disordered proteins present a new paradigm of biomolecular interactions. Here, we investigate the driving forces of such interactions for the example of the highly positively charged linker histone H1 and its highly negatively charged chaperone, prothymosin α (ProTα). Temperature-dependent single-molecule Förster resonance energy transfer (FRET) experiments and isothermal titration calorimetry reveal ProTα-H1 binding to be enthalpically unfavorable, and salt-dependent affinity measurements suggest counterion release entropy to be an important thermodynamic driving force. Using single-molecule FRET, we also identify ternary complexes between ProTα and H1 in addition to the heterodimer at equilibrium and show how they contribute to the thermodynamics observed in ensemble experiments. Finally, we explain the observed thermodynamics quantitatively with a mean-field polyelectrolyte theory that treats counterion release explicitly. ProTα-H1 complex formation resembles the interactions between synthetic polyelectrolytes, and the underlying principles are likely to be of broad relevance for interactions between charged biomolecules in general.
Identifiants
pubmed: 37796987
doi: 10.1073/pnas.2304036120
pmc: PMC10576128
doi:
Substances chimiques
Polyelectrolytes
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2304036120Références
Annu Rev Biophys. 2023 May 9;52:433-462
pubmed: 36750251
Proc Natl Acad Sci U S A. 2010 Aug 17;107(33):14609-14
pubmed: 20639465
J Chem Phys. 2004 May 15;120(19):9343-50
pubmed: 15267872
J Mol Recognit. 2010 Mar-Apr;23(2):105-16
pubmed: 19585546
Bioinformatics. 2018 Jun 15;34(12):2053-2060
pubmed: 29365182
Proc Natl Acad Sci U S A. 2017 Sep 12;114(37):9882-9887
pubmed: 28847960
Trends Biochem Sci. 2008 Jan;33(1):2-8
pubmed: 18054235
J Am Chem Soc. 2018 Nov 14;140(45):15319-15328
pubmed: 30351015
Proc Natl Acad Sci U S A. 2008 Nov 18;105(46):17772-7
pubmed: 19008353
Nat Commun. 2020 Nov 12;11(1):5736
pubmed: 33184256
Proc Natl Acad Sci U S A. 2017 Jun 20;114(25):6563-6568
pubmed: 28584100
Annu Rev Phys Chem. 1995;46:657-700
pubmed: 7495482
Annu Rev Biophys. 2015;44:53-75
pubmed: 25747592
J Mol Biol. 1997 Nov 14;273(5):1048-60
pubmed: 9367790
Curr Opin Biomed Eng. 2019 Dec;12:8-17
pubmed: 31989063
Nat Chem. 2022 Feb;14(2):224-231
pubmed: 34992286
Proc Natl Acad Sci U S A. 2022 Jul 12;119(28):e2202222119
pubmed: 35787038
Nat Commun. 2021 Jul 23;12(1):4513
pubmed: 34301955
Adv Mater. 2015 Apr 17;27(15):2420-32
pubmed: 25771881
Annu Rev Phys Chem. 2020 Apr 20;71:391-414
pubmed: 32097582
Nat Commun. 2019 Aug 6;10(1):3435
pubmed: 31387991
Angew Chem Int Ed Engl. 2021 Feb 19;60(8):3882-3904
pubmed: 32589355
J Am Chem Soc. 2018 Feb 7;140(5):1632-1638
pubmed: 29314832
J Biol Chem. 2002 Dec 27;277(52):50676-82
pubmed: 12379649
J Am Chem Soc. 2016 Jan 27;138(3):980-90
pubmed: 26771205
ACS Cent Sci. 2018 May 23;4(5):638-644
pubmed: 29806011
Nucleic Acids Res. 2017 May 19;45(9):e66
pubmed: 28034955
J Mol Biol. 2008 Mar 14;377(1):9-27
pubmed: 18237740
Phys Chem Chem Phys. 2020 Oct 28;22(41):23952-23985
pubmed: 33073810
Nat Commun. 2015 Jan 14;6:6052
pubmed: 25586861
Biochemistry. 2018 May 1;57(17):2470-2477
pubmed: 29569441
Angew Chem Int Ed Engl. 2019 Mar 26;58(14):4720-4724
pubmed: 30703278
Macromolecules. 2017 Dec 26;50(24):9528-9560
pubmed: 29296029
Proc Natl Acad Sci U S A. 2019 Sep 24;116(39):19506-19512
pubmed: 31488718
Biochemistry. 1988 Jan 12;27(1):456-71
pubmed: 3280021
J Am Chem Soc. 2021 Sep 15;143(36):14540-14550
pubmed: 34473923
ACS Nano. 2012 Jul 24;6(7):6174-84
pubmed: 22670686
Cell. 2015 Oct 22;163(3):734-45
pubmed: 26456112
Adv Colloid Interface Sci. 2011 Sep 14;167(1-2):2-11
pubmed: 21377640
Protein Sci. 2019 Jun;28(6):1095-1105
pubmed: 30968464
FEBS Lett. 2010 Jul 2;584(13):2833-6
pubmed: 20434447
Curr Opin Struct Biol. 2020 Feb;60:66-76
pubmed: 31874413
Soft Matter. 2015 Aug 7;11(29):5889-97
pubmed: 26112168
J Chem Phys. 2023 May 28;158(20):
pubmed: 37226994
Methods Cell Biol. 2008;84:79-113
pubmed: 17964929
Biochemistry. 2006 Jun 6;45(22):6873-88
pubmed: 16734424
FEBS Lett. 2015 Sep 14;589(19 Pt A):2433-40
pubmed: 26073260
Nat Commun. 2019 Jun 5;10(1):2453
pubmed: 31165735
EMBO J. 1995 Mar 15;14(6):1257-63
pubmed: 7720716
Biophys J. 2021 Dec 21;120(24):5438-5453
pubmed: 34826385
J Biol Chem. 1995 Mar 17;270(11):5818-22
pubmed: 7890711
Macromolecules. 2010 Mar 9;43(5):2574-2581
pubmed: 21052522
Proc Natl Acad Sci U S A. 2022 Sep 6;119(36):e2209975119
pubmed: 36037377
Methods Enzymol. 2010;472:179-204
pubmed: 20580965
Soft Matter. 2017 Oct 11;13(39):7001-7012
pubmed: 28840212
Mol Cell. 2016 Jul 7;63(1):72-85
pubmed: 27392146
Biophys Chem. 2005 Apr 1;115(2-3):89-97
pubmed: 15752588
Nat Commun. 2017 Nov 2;8(1):1273
pubmed: 29097695
J Colloid Interface Sci. 2011 Sep 15;361(2):407-22
pubmed: 21705008
Q Rev Biophys. 1978 May;11(2):103-78
pubmed: 353875
J Chem Phys. 2006 Apr 21;124(15):154902
pubmed: 16674260
Langmuir. 2012 Nov 13;28(45):15947-57
pubmed: 23083137
Adv Protein Chem. 1998;51:281-353
pubmed: 9615173
Chem Rev. 1997 Aug 5;97(5):1233-1250
pubmed: 11851449
Curr Opin Struct Biol. 2009 Feb;19(1):31-8
pubmed: 19157855
Chem Rev. 2016 Jun 8;116(11):6424-62
pubmed: 26922996
Angew Chem Int Ed Engl. 2017 Jan 24;56(5):1269-1272
pubmed: 28026092
Nucleic Acids Res. 2011 Apr;39(7):2483-91
pubmed: 21071403
Mol Biosyst. 2012 Jan;8(1):97-104
pubmed: 21874205
Biophys J. 2012 Nov 21;103(10):2203-14
pubmed: 23200054
J Mol Biol. 1992 Nov 5;228(1):252-64
pubmed: 1447786
Proc Natl Acad Sci U S A. 2014 Apr 8;111(14):5213-8
pubmed: 24706910
Curr Opin Struct Biol. 2020 Feb;60:1-6
pubmed: 31629249
Biochemistry. 2006 Apr 25;45(16):5190-205
pubmed: 16618108
Acc Chem Res. 2018 Apr 17;51(4):860-868
pubmed: 29368512
Proc Natl Acad Sci U S A. 2022 Jun 28;119(26):e2120456119
pubmed: 35727975
Nature. 2018 Mar 1;555(7694):61-66
pubmed: 29466338
FEBS J. 2005 Oct;272(20):5129-48
pubmed: 16218947
Proc Natl Acad Sci U S A. 2013 Aug 13;110(33):13392-7
pubmed: 23901099
J Biomol Struct Dyn. 1998 Oct;16(2):461-76
pubmed: 9833682
J Phys Chem B. 2021 Apr 29;125(16):4148-4161
pubmed: 33877835
J Chem Phys. 2018 Oct 28;149(16):163308
pubmed: 30384692
Proc Natl Acad Sci U S A. 2009 Dec 8;106(49):20740-5
pubmed: 19933333
Proc Natl Acad Sci U S A. 2018 Nov 20;115(47):11964-11969
pubmed: 30301810
Annu Rev Biochem. 2014;83:813-41
pubmed: 24606136
Methods Enzymol. 2010;475:455-514
pubmed: 20627168
J Chem Phys. 2015 Dec 28;143(24):243133
pubmed: 26723618
Biochemistry. 2018 Dec 4;57(48):6645-6648
pubmed: 30430826
Soft Matter. 2014 Dec 21;10(47):9496-505
pubmed: 25347132
Nature. 2023 Jul;619(7971):876-883
pubmed: 37468629
J Chem Phys. 2023 Jan 7;158(1):014904
pubmed: 36610965
Adv Colloid Interface Sci. 2017 Jan;239:2-16
pubmed: 27161661
J Chem Phys. 2015 Aug 28;143(8):085101
pubmed: 26328871