Single-Molecular Dissection of Liquid-Liquid Phase Transitions.


Journal

Journal of the American Chemical Society
ISSN: 1520-5126
Titre abrégé: J Am Chem Soc
Pays: United States
ID NLM: 7503056

Informations de publication

Date de publication:
09 08 2023
Historique:
pmc-release: 09 08 2024
medline: 10 8 2023
pubmed: 26 7 2023
entrez: 26 7 2023
Statut: ppublish

Résumé

Interaction between peptides and nucleic acids is a ubiquitous process that drives many cellular functions, such as replications, transcriptions, and translations. Recently, this interaction has been found in liquid-liquid phase separation (LLPS), a process responsible for the formation of newly discovered membraneless organelles with a variety of biological functions inside cells. In this work, we studied the molecular interaction between the poly-l-lysine (PLL) peptide and nucleic acids during the early stage of an LLPS process at the single-molecule level using optical tweezers. By monitoring the mechanical tension of individual nucleic acid templates upon PLL addition, we revealed a multistage LLPS process mediated by the long-range interactions between nucleic acids and polyelectrolytes. By varying different types (ssDNA, ssRNA, and dsDNA) and sequences (A-, T-, G-, or U-rich) of nucleic acids, we pieced together transition diagrams of the PLL-nucleic acid condensates from which we concluded that the propensity to form rigid nucleic acid-PLL complexes reduces the condensate formation during the LLPS process. We anticipate that these results are instrumental in understanding the transition mechanism of LLPS condensates, which allows new strategies to interfere with the biological functions of LLPS condensates inside cells.

Identifiants

pubmed: 37494702
doi: 10.1021/jacs.3c03812
pmc: PMC10528544
mid: NIHMS1920975
doi:

Substances chimiques

RNA 63231-63-0
Polyelectrolytes 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

17143-17150

Subventions

Organisme : NCI NIH HHS
ID : R01 CA236350
Pays : United States

Références

Biochem Pharmacol. 2006 Feb 28;71(5):702-10
pubmed: 16376306
Soft Matter. 2010 Jul 21;6(14):3232-3236
pubmed: 21544267
Science. 1996 Feb 9;271(5250):795-9
pubmed: 8628994
Nat Rev Mol Cell Biol. 2017 May;18(5):285-298
pubmed: 28225081
Science. 2017 Sep 22;357(6357):
pubmed: 28935776
Annu Rev Cell Dev Biol. 2014;30:39-58
pubmed: 25288112
Biochim Biophys Acta Gene Regul Mech. 2020 Dec;1863(12):194641
pubmed: 33017669
Biochemistry. 2004 Dec 28;43(51):15996-6010
pubmed: 15609994
Mol Pharm. 2014 Oct 6;11(10):3395-408
pubmed: 25157701
Nucleic Acids Res. 2016 Sep 30;44(17):8417-24
pubmed: 27288442
Nature. 2012 Mar 07;483(7389):336-40
pubmed: 22398450
Dev Cell. 2020 Oct 12;55(1):30-44
pubmed: 32726575
Angew Chem Int Ed Engl. 2022 Jun 7;61(23):e202113156
pubmed: 35320624
Biophys J. 1995 Oct;69(4):1528-35
pubmed: 8534823
Nat Commun. 2022 Oct 1;13(1):5771
pubmed: 36182948
Biophys J. 2011 Apr 20;100(8):2006-15
pubmed: 21504737
Nat Rev Mol Cell Biol. 2021 Mar;22(3):183-195
pubmed: 32632317
J Am Chem Soc. 2018 Feb 7;140(5):1632-1638
pubmed: 29314832
Acc Chem Res. 2016 Nov 15;49(11):2540-2550
pubmed: 27797171
Biophys J. 2018 Nov 20;115(10):1840-1847
pubmed: 30342746
J Am Chem Soc. 2021 Jul 7;143(26):9849-9857
pubmed: 34152774
Soft Matter. 2017 Nov 1;13(42):7740-7752
pubmed: 29043368
Nature. 2017 Jul 13;547(7662):236-240
pubmed: 28636604
Biophys J. 2010 May 19;98(9):1902-10
pubmed: 20441754
Chem Soc Rev. 2014 May 21;43(10):3324-41
pubmed: 24643375
Nat Commun. 2020 Feb 4;11(1):695
pubmed: 32019927
Cell. 2019 Oct 3;179(2):470-484.e21
pubmed: 31543265
Adv Mater. 2022 Jun;34(25):e2103828
pubmed: 34436789
Mol Cell. 2022 Jul 7;82(13):2415-2426.e5
pubmed: 35477005
J Biol Chem. 2020 Sep 25;295(39):13419-13431
pubmed: 32699013
Proc Natl Acad Sci U S A. 1997 Jun 10;94(12):6185-90
pubmed: 9177192
J Am Chem Soc. 2023 Feb 1;145(4):2375-2385
pubmed: 36689740
Microb Cell. 2014 Apr;1(4):137-139
pubmed: 25279376
Phys Rev Lett. 2006 Mar 24;96(11):118301
pubmed: 16605879
Nat Commun. 2019 Jul 19;10(1):3230
pubmed: 31324804
Angew Chem Int Ed Engl. 2019 Apr 1;58(15):4858-4862
pubmed: 30762296
Mol Cell. 2015 Oct 15;60(2):208-19
pubmed: 26412307
Elife. 2014 Oct 16;3:
pubmed: 25321392
Nat Commun. 2019 Jul 2;10(1):2909
pubmed: 31266957
Trends Genet. 2021 Apr;37(4):337-354
pubmed: 33020022
Phys Rev Lett. 2003 Jan 10;90(1):018102
pubmed: 12570651
Nat Rev Immunol. 2022 Mar;22(3):188-199
pubmed: 34230650
Nat Rev Mol Cell Biol. 2021 Mar;22(3):215-235
pubmed: 33169001
Cold Spring Harb Symp Quant Biol. 2019;84:21-30
pubmed: 32295929
Biophys J. 2020 Feb 4;118(3):753-764
pubmed: 31952807
Int J Mol Sci. 2021 Sep 24;22(19):
pubmed: 34638607
Biol Direct. 2012 Jan 20;7:4
pubmed: 22264281
Phys Rev E Stat Nonlin Soft Matter Phys. 2004 Aug;70(2 Pt 1):020902
pubmed: 15447472
Nucleic Acids Res. 2022 Jul 22;50(13):7247-7259
pubmed: 35801856
J Am Chem Soc. 1996 Feb 21;118(7):1587-1594
pubmed: 20830216
Biophys J. 2000 Apr;78(4):1965-78
pubmed: 10733975
Nat Methods. 2012 Jul;9(7):671-5
pubmed: 22930834
Elife. 2022 Jan 31;11:
pubmed: 35098921
Biomacromolecules. 2022 Nov 14;23(11):4795-4803
pubmed: 36322676
J Am Chem Soc. 1995 Jul 1;117(29):7818-7819
pubmed: 27524830
J Mol Biol. 2018 Nov 2;430(23):4685-4701
pubmed: 29753780

Auteurs

Pravin Pokhrel (P)

Department of Chemistry and Biochemistry, Kent State University, Kent, Ohio 44242, United States.

Sagun Jonchhe (S)

Department of Chemistry and Biochemistry, Kent State University, Kent, Ohio 44242, United States.

Wei Pan (W)

Department of Chemistry and Biochemistry, Kent State University, Kent, Ohio 44242, United States.

Hanbin Mao (H)

Department of Chemistry and Biochemistry, Kent State University, Kent, Ohio 44242, United States.

Articles similaires

Humans RNA, Circular Exosomes Cell Proliferation Epithelial-Mesenchymal Transition
DNA Methylation Humans DNA Animals Machine Learning
Cryoelectron Microscopy Models, Molecular RNA DNA Nucleic Acid Conformation
Phonons Titanium Oxides Zirconium Calcium Compounds

Classifications MeSH