Allosteric Communications between Domains Modulate the Activity of Matrix Metalloprotease-1.
Journal
Biophysical journal
ISSN: 1542-0086
Titre abrégé: Biophys J
Pays: United States
ID NLM: 0370626
Informations de publication
Date de publication:
21 07 2020
21 07 2020
Historique:
received:
11
12
2019
revised:
30
05
2020
accepted:
09
06
2020
pubmed:
26
6
2020
medline:
15
5
2021
entrez:
26
6
2020
Statut:
ppublish
Résumé
An understanding of the structure-dynamics relationship is essential for understanding how a protein works. Prior research has shown that the activity of a protein correlates with intradomain dynamics occurring at picosecond to millisecond timescales. However, the correlation between interdomain dynamics and the function of a protein is poorly understood. Here, we show that communications between the catalytic and hemopexin domains of matrix metalloprotease-1 (MMP1) on type 1 collagen fibrils correlate with its activity. Using single-molecule Förster resonance energy transfer, we identified functionally relevant open conformations in which the two MMP1 domains are well separated, which were significantly absent for catalytically inactive point mutant (E219Q) of MMP1 and could be modulated by an inhibitor or an enhancer of activity. The observed relevance of open conformations resolves the debate about the roles of open and closed MMP1 structures in function. We fitted the histograms of single-molecule Förster resonance energy transfer values to a sum of two Gaussians and the autocorrelations to an exponential and power law. We used a two-state Poisson process to describe the dynamics and calculate the kinetic rates from the fit parameters. All-atom and coarse-grained simulations reproduced some of the experimental features and revealed substrate-dependent MMP1 dynamics. Our results suggest that an interdomain separation facilitates opening up the catalytic pocket so that the collagen chains come closer to the MMP1 active site. Coordination of functional conformations at different parts of MMP1 occurs via allosteric communications that can take place via interactions mediated by collagen even if the linker between the domains is absent. Modeling dynamics as a Poisson process enables connecting the picosecond timescales of molecular dynamics simulations with the millisecond timescales of single-molecule measurements. Water-soluble MMP1 interacting with water-insoluble collagen fibrils poses challenges for biochemical studies that the single-molecule tracking can overcome for other insoluble substrates. Interdomain communications are likely important for multidomain proteins.
Identifiants
pubmed: 32585130
pii: S0006-3495(20)30484-7
doi: 10.1016/j.bpj.2020.06.010
pmc: PMC7376139
pii:
doi:
Substances chimiques
Proteins
0
Matrix Metalloproteinase 1
EC 3.4.24.7
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
360-374Informations de copyright
Copyright © 2020 Biophysical Society. Published by Elsevier Inc. All rights reserved.
Références
Nat Chem Biol. 2009 Nov;5(11):789-96
pubmed: 19841628
Proc Natl Acad Sci U S A. 2014 Oct 7;111(40):E4148-55
pubmed: 25246591
Phys Rev E Stat Nonlin Soft Matter Phys. 2006 Feb;73(2 Pt 1):022102
pubmed: 16605373
Proc Natl Acad Sci U S A. 2007 Nov 27;104(48):18964-9
pubmed: 18029448
Nat Methods. 2006 Nov;3(11):891-3
pubmed: 17013382
Hum Genomics. 2010 Feb;4(3):194-201
pubmed: 20368140
J Vasc Surg. 2001 Nov;34(5):930-8
pubmed: 11700497
J Biol Chem. 1992 Mar 5;267(7):4583-91
pubmed: 1311314
J Vasc Surg. 1996 Jul;24(1):127-33
pubmed: 8691515
Biophys J. 2001 Jan;80(1):505-15
pubmed: 11159421
Methods Enzymol. 2000;319:20-8
pubmed: 10907495
Chem Soc Rev. 2014 Feb 21;43(4):1057-75
pubmed: 24141280
J Mol Biol. 2002 May 24;319(1):173-81
pubmed: 12051944
J Periodontal Res. 1984 Nov;19(6):651-5
pubmed: 6098638
Proteins. 2004 Nov 15;57(3):433-43
pubmed: 15382234
FEBS Lett. 2001 Aug 17;503(2-3):158-62
pubmed: 11513874
Anal Biochem. 2004 May 15;328(2):166-73
pubmed: 15113693
Protein Expr Purif. 2018 Aug;148:59-67
pubmed: 29626520
Curr Biol. 2012 Jun 19;22(12):1047-56
pubmed: 22578418
Proc Natl Acad Sci U S A. 2009 Oct 13;106(41):17359-64
pubmed: 19805169
Phys Rev A Gen Phys. 1985 Mar;31(3):1695-1697
pubmed: 9895674
J Am Chem Soc. 2012 Feb 1;134(4):2100-10
pubmed: 22239621
J Microsc. 2017 Jun;266(3):298-306
pubmed: 28328030
Mol Biotechnol. 2002 Sep;22(1):51-86
pubmed: 12353914
J Biomol Struct Dyn. 2017 Feb;35(3):564-573
pubmed: 26886688
Proteins. 2008 Mar;70(4):1154-61
pubmed: 17932911
Genome Biol. 2002 Jul 25;3(8):RESEARCH0040
pubmed: 12186647
RSC Adv. 2016 Jan 1;6(28):23223-23232
pubmed: 26998255
Int J Biochem Cell Biol. 2006;38(7):1050-62
pubmed: 16446111
Proc Natl Acad Sci U S A. 2008 Feb 26;105(8):2824-9
pubmed: 18287018
Matrix Biol. 2015 Oct;48:78-88
pubmed: 26049074
J Biol Chem. 2011 Dec 30;286(52):45073-82
pubmed: 22030392
Chem Rev. 2006 May;106(5):1624-71
pubmed: 16683748
Nat Rev Mol Cell Biol. 2007 Mar;8(3):221-33
pubmed: 17318226
Q Rev Biophys. 2011 Feb;44(1):123-51
pubmed: 21108866
Proc Natl Acad Sci U S A. 1958 Feb;44(2):98-104
pubmed: 16590179
Nature. 2007 Dec 6;450(7171):913-6
pubmed: 18026087
Proc Natl Acad Sci U S A. 2016 Jul 26;113(30):8436-41
pubmed: 27402741
Bioinformatics. 2006 Nov 1;22(21):2619-27
pubmed: 16928735
J Biol Chem. 2009 May 8;284(19):12821-8
pubmed: 19282283
Biomech Model Mechanobiol. 2019 Dec;18(6):1809-1819
pubmed: 31161353
J Biol Chem. 2013 Oct 18;288(42):30659-71
pubmed: 24025334
J Am Chem Soc. 2009 Apr 15;131(14):5018-9
pubmed: 19301868
Proc Natl Acad Sci U S A. 2002 Feb 5;99(3):1314-8
pubmed: 11805290
EMBO J. 2004 Aug 4;23(15):3020-30
pubmed: 15257288
Int J Exp Pathol. 2017 Feb;98(1):4-16
pubmed: 28508516
Proc Natl Acad Sci U S A. 2010 Apr 27;107(17):E71; author reply E72
pubmed: 20424124
Bioinformatics. 2015 May 1;31(9):1487-9
pubmed: 25568280
Phys Rev Lett. 1993 Jun 7;70(23):3584-3587
pubmed: 10053911
Methods Mol Biol. 2012;914:285-317
pubmed: 22976035
Nat Mater. 2002 Oct;1(2):77-9
pubmed: 12618812
J Phys Chem B. 2018 May 31;122(21):5316-5326
pubmed: 29161042
Bone. 1998 Jan;22(1):33-8
pubmed: 9437511
Proc Natl Acad Sci U S A. 2012 Jul 31;109(31):12461-6
pubmed: 22761315
J Mol Biol. 2009 Jan 9;385(1):312-29
pubmed: 18952103
Proc Natl Acad Sci U S A. 2007 Jan 30;104(5):1528-33
pubmed: 17251351
Brain Res. 1999 Sep 18;842(1):92-100
pubmed: 10526099
Biophys Chem. 2016 Nov;218:42-46
pubmed: 27648753
Surg Today. 1997;27(4):302-4
pubmed: 9086544
J Mol Biol. 1965 May;12:88-118
pubmed: 14343300
Sci Rep. 2019 Dec 11;9(1):18785
pubmed: 31827179
J Leukoc Biol. 2007 Apr;81(4):870-92
pubmed: 17185359
Matrix Biol. 1998 Dec;17(8-9):657-65
pubmed: 9923658
Science. 2004 Oct 1;306(5693):108-11
pubmed: 15459390
Biochem J. 1989 Oct 1;263(1):201-6
pubmed: 2557822
J Cereb Blood Flow Metab. 2000 Dec;20(12):1681-9
pubmed: 11129784