Machine learning coarse-grained potentials of protein thermodynamics.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
15 09 2023
Historique:
received: 02 06 2023
accepted: 29 08 2023
medline: 18 9 2023
pubmed: 16 9 2023
entrez: 15 9 2023
Statut: epublish

Résumé

A generalized understanding of protein dynamics is an unsolved scientific problem, the solution of which is critical to the interpretation of the structure-function relationships that govern essential biological processes. Here, we approach this problem by constructing coarse-grained molecular potentials based on artificial neural networks and grounded in statistical mechanics. For training, we build a unique dataset of unbiased all-atom molecular dynamics simulations of approximately 9 ms for twelve different proteins with multiple secondary structure arrangements. The coarse-grained models are capable of accelerating the dynamics by more than three orders of magnitude while preserving the thermodynamics of the systems. Coarse-grained simulations identify relevant structural states in the ensemble with comparable energetics to the all-atom systems. Furthermore, we show that a single coarse-grained potential can integrate all twelve proteins and can capture experimental structural features of mutated proteins. These results indicate that machine learning coarse-grained potentials could provide a feasible approach to simulate and understand protein dynamics.

Identifiants

pubmed: 37714883
doi: 10.1038/s41467-023-41343-1
pii: 10.1038/s41467-023-41343-1
pmc: PMC10504246
doi:

Substances chimiques

Ataxia Telangiectasia Mutated Proteins EC 2.7.11.1

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

5739

Informations de copyright

© 2023. Springer Nature Limited.

Références

J Chem Phys. 2020 May 21;152(19):194106
pubmed: 33687259
J Phys Chem B. 2005 Feb 24;109(7):2469-73
pubmed: 16851243
Proc Natl Acad Sci U S A. 2005 Jul 19;102(29):10141-6
pubmed: 16006532
Nature. 2021 Aug;596(7873):583-589
pubmed: 34265844
Nature. 2005 Nov 3;438(7064):117-21
pubmed: 16267559
J Chem Theory Comput. 2009 Jun 9;5(6):1632-9
pubmed: 26609855
J Chem Theory Comput. 2019 Apr 9;15(4):2719-2733
pubmed: 30810317
J Chem Phys. 2013 Sep 7;139(9):090901
pubmed: 24028092
J Chem Theory Comput. 2016 Apr 12;12(4):1845-52
pubmed: 26949976
J Chem Theory Comput. 2013 Apr 9;9(4):2000-2009
pubmed: 23750122
J Chem Phys. 2018 Jul 21;149(3):034101
pubmed: 30037247
J Chem Theory Comput. 2020 Jul 14;16(7):4685-4693
pubmed: 32539384
J Chem Theory Comput. 2008 May;4(5):819-34
pubmed: 26621095
Nat Commun. 2021 Nov 25;12(1):6884
pubmed: 34824254
Phys Rev Lett. 2012 Feb 3;108(5):058301
pubmed: 22400967
J Comput Chem. 1999 Jun;20(8):786-798
pubmed: 35619462
Chem Sci. 2017 Apr 1;8(4):3192-3203
pubmed: 28507695
Annu Rev Biophys. 2013;42:73-93
pubmed: 23451897
Nat Chem. 2017 Oct;9(10):1005-1011
pubmed: 28937668
Nat Struct Biol. 2000 Aug;7(8):669-73
pubmed: 10932252
Curr Opin Struct Biol. 2004 Feb;14(1):76-88
pubmed: 15102453
J Chem Phys. 2022 Sep 14;157(10):104102
pubmed: 36109216
ACS Cent Sci. 2019 May 22;5(5):755-767
pubmed: 31139712
J Chem Phys. 2015 Dec 28;143(24):243104
pubmed: 26723589
Nature. 2007 Dec 13;450(7172):964-72
pubmed: 18075575
J Chem Phys. 2011 May 7;134(17):174105
pubmed: 21548671
J Chem Phys. 2004 Jul 1;121(1):415-25
pubmed: 15260562
J Chem Theory Comput. 2021 Apr 13;17(4):2355-2363
pubmed: 33729795
Science. 2021 Aug 20;373(6557):871-876
pubmed: 34282049
J Chem Theory Comput. 2019 Jan 8;15(1):448-455
pubmed: 30481453
Proc Natl Acad Sci U S A. 2013 Apr 9;110(15):5915-20
pubmed: 23503848
J Chem Inf Model. 2010 Mar 22;50(3):397-403
pubmed: 20199097
J Chem Theory Comput. 2019 Jun 11;15(6):3678-3693
pubmed: 31042390
Nature. 1975 Feb 27;253(5494):694-8
pubmed: 1167625
Proc Natl Acad Sci U S A. 2020 Sep 29;117(39):24061-24068
pubmed: 32929015
Biophys J. 2008 Feb 1;94(3):726-36
pubmed: 17890394
J Phys Chem B. 2013 Oct 24;117(42):12935-42
pubmed: 23882999
J Mol Biol. 2000 May 19;298(5):937-53
pubmed: 10801360
Nature. 1977 Jun 16;267(5612):585-90
pubmed: 301613
J Chem Phys. 2008 Aug 14;129(6):064107
pubmed: 18715051
Curr Opin Struct Biol. 2001 Apr;11(2):224-30
pubmed: 11297932
J Chem Phys. 2008 Oct 14;129(14):144108
pubmed: 19045135
Nucleic Acids Res. 2003 Jul 1;31(13):3370-4
pubmed: 12824330
J Am Chem Soc. 2018 Feb 21;140(7):2386-2396
pubmed: 29323881
Annu Rev Biochem. 2008;77:363-82
pubmed: 18410248
Science. 2019 Sep 6;365(6457):
pubmed: 31488660
J Chem Phys. 2021 Aug 28;155(8):084101
pubmed: 34470360
Nat Struct Mol Biol. 2004 Feb;11(2):135-41
pubmed: 14730350
J Chem Theory Comput. 2022 Oct 11;18(10):5759-5791
pubmed: 36070494
Phys Rev Lett. 2007 Apr 6;98(14):146401
pubmed: 17501293
Nat Commun. 2023 Sep 15;14(1):5739
pubmed: 37714883
Science. 2011 Oct 28;334(6055):517-20
pubmed: 22034434
Science. 1991 Dec 13;254(5038):1598-603
pubmed: 1749933
Nat Struct Biol. 2002 Sep;9(9):646-52
pubmed: 12198485
J Chem Phys. 2020 Sep 28;153(12):124111
pubmed: 33003742
Curr Opin Struct Biol. 2008 Apr;18(2):154-62
pubmed: 18378442
J Chem Phys. 2020 Oct 28;153(16):164501
pubmed: 33138411
Proc Natl Acad Sci U S A. 2002 Oct 1;99(20):12562-6
pubmed: 12271136
J Chem Phys. 2018 Jun 28;148(24):241722
pubmed: 29960322
Curr Opin Struct Biol. 2004 Feb;14(1):89-95
pubmed: 15102454
Curr Opin Struct Biol. 2023 Apr;79:102533
pubmed: 36731338
PLoS Comput Biol. 2010 Jun 24;6(6):e1000827
pubmed: 20585614
J Chem Theory Comput. 2014 May 13;10(5):2064-9
pubmed: 26580533
J Am Chem Soc. 2004 Jul 14;126(27):8426-32
pubmed: 15237999
J Chem Theory Comput. 2018 Jan 9;14(1):453-460
pubmed: 29207235
J Chem Phys. 2020 Nov 21;153(19):194101
pubmed: 33218238
Acta Biochim Pol. 2004;51(2):349-71
pubmed: 15218533
Biophys J. 2011 May 4;100(9):L47-9
pubmed: 21539772
J Chem Phys. 2019 Jul 28;151(4):044116
pubmed: 31370528
J Chem Phys. 2008 Jun 28;128(24):244114
pubmed: 18601324
Nat Commun. 2021 Dec 14;12(1):7273
pubmed: 34907176
J Phys Chem B. 2012 Jul 26;116(29):8494-503
pubmed: 22545654
J Chem Phys. 2013 Jul 7;139(1):015102
pubmed: 23822324
J Phys Chem B. 2007 Jul 12;111(27):7812-24
pubmed: 17569554
J Chem Phys. 2021 Apr 28;154(16):164113
pubmed: 33940848
Chem Soc Rev. 2013 Aug 21;42(16):6801-22
pubmed: 23708257
Curr Opin Struct Biol. 2008 Feb;18(1):10-5
pubmed: 18160277

Auteurs

Maciej Majewski (M)

Computational Science Laboratory, Universitat Pompeu Fabra, Barcelona Biomedical Research Park (PRBB), Carrer Dr. Aiguader 88, 08003, Barcelona, Spain.
Acellera Labs, Doctor Trueta 183, 08005, Barcelona, Spain.

Adrià Pérez (A)

Computational Science Laboratory, Universitat Pompeu Fabra, Barcelona Biomedical Research Park (PRBB), Carrer Dr. Aiguader 88, 08003, Barcelona, Spain.
Acellera Labs, Doctor Trueta 183, 08005, Barcelona, Spain.

Philipp Thölke (P)

Computational Science Laboratory, Universitat Pompeu Fabra, Barcelona Biomedical Research Park (PRBB), Carrer Dr. Aiguader 88, 08003, Barcelona, Spain.

Stefan Doerr (S)

Acellera Labs, Doctor Trueta 183, 08005, Barcelona, Spain.

Nicholas E Charron (NE)

Department of Physics, Rice University, Houston, TX, 77005, USA.
Center for Theoretical Biological Physics, Rice University, Houston, TX, 77005, USA.
Department of Physics, FU Berlin, Arnimallee 12, 14195, Berlin, Germany.

Toni Giorgino (T)

Biophysics Institute, National Research Council (CNR-IBF), 20133, Milan, Italy.

Brooke E Husic (BE)

Department of Mathematics and Computer Science, FU Berlin, Arnimallee 12, 14195, Berlin, Germany.
Lewis Sigler Institute for Integrative Genomics, Princeton University, Princeton, NJ, 08540, USA.
Princeton Center for Theoretical Science, Princeton University, Princeton, NJ, 08540, USA.
Center for the Physics of Biological Function, Princeton University, Princeton, NJ, 08540, USA.

Cecilia Clementi (C)

Department of Physics, Rice University, Houston, TX, 77005, USA. cecilia.clementi@fu-berlin.de.
Center for Theoretical Biological Physics, Rice University, Houston, TX, 77005, USA. cecilia.clementi@fu-berlin.de.
Department of Physics, FU Berlin, Arnimallee 12, 14195, Berlin, Germany. cecilia.clementi@fu-berlin.de.
Department of Chemistry, Rice University, Houston, TX, 77005, USA. cecilia.clementi@fu-berlin.de.

Frank Noé (F)

Department of Physics, FU Berlin, Arnimallee 12, 14195, Berlin, Germany. frank.noe@fu-berlin.de.
Department of Mathematics and Computer Science, FU Berlin, Arnimallee 12, 14195, Berlin, Germany. frank.noe@fu-berlin.de.
Department of Chemistry, Rice University, Houston, TX, 77005, USA. frank.noe@fu-berlin.de.
Microsoft Research AI4Science, Karl-Liebknecht Str. 32, 10178, Berlin, Germany. frank.noe@fu-berlin.de.

Gianni De Fabritiis (G)

Computational Science Laboratory, Universitat Pompeu Fabra, Barcelona Biomedical Research Park (PRBB), Carrer Dr. Aiguader 88, 08003, Barcelona, Spain. gianni.defabritiis@upf.edu.
Acellera Labs, Doctor Trueta 183, 08005, Barcelona, Spain. gianni.defabritiis@upf.edu.
Institució Catalana de Recerca i Estudis Avançats (ICREA), Passeig Lluis Companys 23, 08010, Barcelona, Spain. gianni.defabritiis@upf.edu.

Articles similaires

Photosynthesis Ribulose-Bisphosphate Carboxylase Carbon Dioxide Molecular Dynamics Simulation Cyanobacteria

Exploring blood-brain barrier passage using atomic weighted vector and machine learning.

Yoan Martínez-López, Paulina Phoobane, Yanaima Jauriga et al.
1.00
Blood-Brain Barrier Machine Learning Humans Support Vector Machine Software

Understanding the role of machine learning in predicting progression of osteoarthritis.

Simone Castagno, Benjamin Gompels, Estelle Strangmark et al.
1.00
Humans Disease Progression Machine Learning Osteoarthritis
Humans Artificial Intelligence Neoplasms Prognosis Image Processing, Computer-Assisted

Classifications MeSH