A topological data analytic approach for discovering biophysical signatures in protein dynamics.


Journal

PLoS computational biology
ISSN: 1553-7358
Titre abrégé: PLoS Comput Biol
Pays: United States
ID NLM: 101238922

Informations de publication

Date de publication:
05 2022
Historique:
received: 31 08 2021
accepted: 22 03 2022
revised: 12 05 2022
pubmed: 3 5 2022
medline: 18 5 2022
entrez: 2 5 2022
Statut: epublish

Résumé

Identifying structural differences among proteins can be a non-trivial task. When contrasting ensembles of protein structures obtained from molecular dynamics simulations, biologically-relevant features can be easily overshadowed by spurious fluctuations. Here, we present SINATRA Pro, a computational pipeline designed to robustly identify topological differences between two sets of protein structures. Algorithmically, SINATRA Pro works by first taking in the 3D atomic coordinates for each protein snapshot and summarizing them according to their underlying topology. Statistically significant topological features are then projected back onto a user-selected representative protein structure, thus facilitating the visual identification of biophysical signatures of different protein ensembles. We assess the ability of SINATRA Pro to detect minute conformational changes in five independent protein systems of varying complexities. In all test cases, SINATRA Pro identifies known structural features that have been validated by previous experimental and computational studies, as well as novel features that are also likely to be biologically-relevant according to the literature. These results highlight SINATRA Pro as a promising method for facilitating the non-trivial task of pattern recognition in trajectories resulting from molecular dynamics simulations, with substantially increased resolution.

Identifiants

pubmed: 35500014
doi: 10.1371/journal.pcbi.1010045
pii: PCOMPBIOL-D-21-01589
pmc: PMC9098046
doi:

Substances chimiques

Proteins 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1010045

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

Nature. 1999 May 20;399(6733):221-9
pubmed: 10353244
Sci Rep. 2018 Dec 18;8(1):17938
pubmed: 30560871
Mol Cell. 2004 Nov 5;16(3):319-30
pubmed: 15525506
J Comput Chem. 2005 Dec;26(16):1701-18
pubmed: 16211538
Biomolecules. 2019 Dec 11;9(12):
pubmed: 31835662
J Comput Chem. 2011 Jul 30;32(10):2319-27
pubmed: 21500218
Proc Natl Acad Sci U S A. 2006 Nov 21;103(47):17783-8
pubmed: 17095602
Annu Rev Biochem. 2000;69:373-98
pubmed: 10966463
Protein Sci. 2021 Jan;30(1):20-30
pubmed: 32734663
Clin Microbiol Infect. 2008 Jan;14 Suppl 1:11-32
pubmed: 18154525
J Chem Phys. 2014 Jul 7;141(1):014111
pubmed: 25005281
J Mol Graph. 1996 Feb;14(1):33-8, 27-8
pubmed: 8744570
Curr Opin Struct Biol. 1999 Jun;9(3):374-82
pubmed: 10361094
Proc Natl Acad Sci U S A. 2021 Oct 12;118(41):
pubmed: 34625491
Org Biomol Chem. 2003 Jan 7;1(1):5-14
pubmed: 12929379
Cell Rep. 2017 Dec 5;21(10):2796-2812
pubmed: 29212027
Proteins. 2021 Dec;89(12):1673-1686
pubmed: 34240477
J Chem Theory Comput. 2016 Jan 12;12(1):281-96
pubmed: 26584231
J Chem Theory Comput. 2015 Aug 11;11(8):3696-713
pubmed: 26574453
Living J Comput Mol Sci. 2018;1(1):
pubmed: 30533602
Nucleic Acids Res. 2000 Jan 1;28(1):235-42
pubmed: 10592235
Science. 2020 Oct 9;370(6513):
pubmed: 33004676
PLoS Comput Biol. 2018 Nov 9;14(11):e1006364
pubmed: 30412578
Ther Clin Risk Manag. 2009 Apr;5(2):281-9
pubmed: 19536317
Biochim Biophys Acta Proteins Proteom. 2017 Nov;1865(11 Pt A):1416-1422
pubmed: 28846854
Neuron. 2018 Sep 19;99(6):1129-1143
pubmed: 30236283
J Biol Chem. 2015 Apr 17;290(16):10382-94
pubmed: 25713062
Med Phys. 2021 Nov;48(11):7043-7051
pubmed: 34587294
Nat Commun. 2013;4:1733
pubmed: 23591900
Nat Rev Cancer. 2013 Aug;13(8):559-71
pubmed: 23842646
Science. 2009 Oct 30;326(5953):688-694
pubmed: 19833920
Biophys J. 2020 Jan 7;118(1):151-161
pubmed: 31711607
Bioinformatics. 2021 Jul 10;:
pubmed: 34247232
Drugs. 1998 Jun;55(6):837-42; discussion 843-4
pubmed: 9617598
Biophys J. 2015 Jul 21;109(2):277-86
pubmed: 26200863
Antimicrob Agents Chemother. 1995 Dec;39(12):2593-601
pubmed: 8592985
Nat Struct Mol Biol. 2008 Oct;15(10):1109-18
pubmed: 18794843
Virology. 1993 Apr;193(2):661-71
pubmed: 7681610
Science. 2015 Feb 20;347(6224):882-6
pubmed: 25700521
J Comput Chem. 2010 May;31(7):1561-3
pubmed: 20017124
Antimicrob Agents Chemother. 2010 Oct;54(10):4253-61
pubmed: 20660676
HIV AIDS (Auckl). 2015 Apr 08;7:95-104
pubmed: 25897264
Ann Appl Stat. 2019 Jun;13(2):958-989
pubmed: 32542104
J Am Stat Assoc. 2018;113(524):1710-1721
pubmed: 30799887
Mediterr J Hematol Infect Dis. 2014 Jan 02;6(1):e2014007
pubmed: 24455116
J Mol Biol. 2009 Jan 9;385(1):312-29
pubmed: 18952103
Genes Cancer. 2012 May;3(5-6):447-54
pubmed: 23226582
Proc Natl Acad Sci U S A. 2009 Jan 6;106(1):139-44
pubmed: 19109437
Genetics. 2015 Oct;201(2):759-68
pubmed: 26219298
Proc Natl Acad Sci U S A. 2006 Jan 24;103(4):915-20
pubmed: 16418268
Structure. 2008 Jun;16(6):906-15
pubmed: 18547523
Front Microbiol. 2019 Oct 24;10:2351
pubmed: 31708880
J Mol Biol. 2008 Aug 1;381(1):102-15
pubmed: 18597780
Acta Crystallogr A. 2005 Jul;61(Pt 4):478-80
pubmed: 15973002
Nat Rev Genet. 2006 May;7(5):337-48
pubmed: 16619049
Biochim Biophys Acta. 2010 Mar;1804(3):440-4
pubmed: 19879387
Proc Natl Acad Sci U S A. 2018 Mar 27;115(13):3386-3391
pubmed: 29531062

Auteurs

Wai Shing Tang (WS)

Department of Physics, Brown University, Providence, Rhode Island, United States of America.

Gabriel Monteiro da Silva (GM)

Department of Molecular and Cell Biology, Brown University, Providence, Rhode Island, United States of America.

Henry Kirveslahti (H)

Department of Statistical Science, Duke University, Durham, North Carolina, United States of America.

Erin Skeens (E)

Department of Molecular and Cell Biology, Brown University, Providence, Rhode Island, United States of America.

Bibo Feng (B)

Department of Chemistry, Brown University, Providence, Rhode Island, United States of America.

Timothy Sudijono (T)

Department of Statistics, Stanford University, Palo Alto, California, United States of America.

Kevin K Yang (KK)

Microsoft Research New England, Cambridge, Massachusetts, United States of America.

Sayan Mukherjee (S)

Department of Statistical Science, Duke University, Durham, North Carolina, United States of America.
Department of Computer Science, Duke University, Durham, North Carolina, United States of America.
Department of Mathematics, Duke University, Durham, North Carolina, United States of America.
Department of Bioinformatics & Biostatistics, Duke University, Durham, North Carolina, United States of America.

Brenda Rubenstein (B)

Department of Chemistry, Brown University, Providence, Rhode Island, United States of America.

Lorin Crawford (L)

Microsoft Research New England, Cambridge, Massachusetts, United States of America.
Department of Biostatistics, Brown University, Providence, Rhode Island, United States of America.
Center for Computational Molecular Biology, Brown University, Providence, Rhode Island, United States of America.

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Classifications MeSH