Local frustration determines loop opening during the catalytic cycle of an oxidoreductase

Local structural frustration, the existence of mutually exclusive competing interactions, may explain why some proteins are dynamic while others are rigid. Frustration is thought to underpin biomolecular recognition and the flexibility of protein-binding sites. Here, we show how a small chemical mod...

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Published ineLife Vol. 9
Main Authors Stelzl, Lukas S, Mavridou, Despoina Ai, Saridakis, Emmanuel, Gonzalez, Diego, Baldwin, Andrew J, Ferguson, Stuart J, Sansom, Mark Sp, Redfield, Christina
Format Journal Article
LanguageEnglish
Published England eLife Science Publications, Ltd 22.06.2020
eLife Sciences Publications Ltd
eLife Sciences Publications, Ltd
Subjects
Catalysis
Catalytic Domain
Chemical bonds
Chemical modification
Computational and Systems Biology
Cycling
Cysteine
Cysteine - metabolism
Cystine
Escherichia coli - metabolism
Escherichia coli Proteins - metabolism
Experiments
Frustration
Immunoglobulins
local frustration
molecular dynamics
NMR
Oxidation
Oxidation-Reduction
Oxidoreductase
Oxidoreductases - metabolism
Periplasm
Periplasm - metabolism
Periplasmic Proteins - metabolism
Protein Binding
protein dynamics
Protein structure
Proteins
Structural Biology and Molecular Biophysics
Sulfhydryl Compounds - metabolism
Thiols
computational biology
systems biology
NMR
protein dynamics
local frustration
structural biology
molecular biophysics
molecular dynamics
oxidoreductase
E. coli
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Abstract Local structural frustration, the existence of mutually exclusive competing interactions, may explain why some proteins are dynamic while others are rigid. Frustration is thought to underpin biomolecular recognition and the flexibility of protein-binding sites. Here, we show how a small chemical modification, the oxidation of two cysteine thiols to a disulfide bond, during the catalytic cycle of the N-terminal domain of the key bacterial oxidoreductase DsbD (nDsbD), introduces frustration ultimately influencing protein function. In oxidized nDsbD, local frustration disrupts the packing of the protective cap-loop region against the active site allowing loop opening. By contrast, in reduced nDsbD the cap loop is rigid, always protecting the active-site thiols from the oxidizing environment of the periplasm. Our results point toward an intricate coupling between the dynamics of the active-site cysteines and of the cap loop which modulates the association reactions of nDsbD with its partners resulting in optimized protein function.
AbstractList Local structural frustration, the existence of mutually exclusive competing interactions, may explain why some proteins are dynamic while others are rigid. Frustration is thought to underpin biomolecular recognition and the flexibility of protein-binding sites. Here, we show how a small chemical modification, the oxidation of two cysteine thiols to a disulfide bond, during the catalytic cycle of the N-terminal domain of the key bacterial oxidoreductase DsbD (nDsbD), introduces frustration ultimately influencing protein function. In oxidized nDsbD, local frustration disrupts the packing of the protective cap-loop region against the active site allowing loop opening. By contrast, in reduced nDsbD the cap loop is rigid, always protecting the active-site thiols from the oxidizing environment of the periplasm. Our results point toward an intricate coupling between the dynamics of the active-site cysteines and of the cap loop which modulates the association reactions of nDsbD with its partners resulting in optimized protein function.
Audience Academic
Author Stelzl, Lukas S
Ferguson, Stuart J
Sansom, Mark Sp
Redfield, Christina
Mavridou, Despoina Ai
Saridakis, Emmanuel
Gonzalez, Diego
Baldwin, Andrew J
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  surname: Redfield
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  organization: Department of Biochemistry, University of Oxford, Oxford, United Kingdom
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Cites_doi 10.1017/S0033583514000092
10.1002/jcc.21787
10.1038/nature05858
10.1073/pnas.1018980108
10.1021/bi0603064
10.1002/cbic.201300193
10.1021/ja00381a009
10.1021/ja2017703
10.1073/pnas.0709915104
10.1021/jacs.6b09460
10.1371/journal.pcbi.1002704
10.1021/bi016038l
10.1016/j.jmb.2006.12.033
10.1016/j.bpj.2014.06.025
10.1073/pnas.1217306110
10.7554/eLife.17505
10.1021/jp973084f
10.1073/pnas.1819859116
10.1063/1.2408420
10.1021/ct400654r
10.1038/sj.emboj.7600178
10.1016/0263-7855(96)00018-5
10.1038/s41467-017-01163-6
10.1126/science.1157092
10.1016/j.sbi.2017.09.006
10.1021/ja983961a
10.1038/s41467-019-08557-8
10.1016/0022-2836(92)90136-8
10.1093/nar/gks447
10.1089/ars.2012.4864
10.1006/jmre.1998.1361
10.1107/S0907444909052925
10.1016/j.jmb.2007.04.038
10.1021/bi00449a003
10.1007/BF00197809
10.1107/S0907444996012255
10.1074/jbc.RA118.004847
10.1093/nar/gkq453
10.1093/emboj/cdf489
10.4324/9780203809075
10.1038/nchembio.232
10.1007/s12104-011-9347-9
10.1074/jbc.M111.236141
10.1006/jmbi.1994.0073
10.1007/s10858-013-9741-y
10.1002/jcc.20291
10.1038/nchembio.238
10.1080/00268979200100511
10.1002/jcc.20065
10.1016/j.jmb.2011.07.017
10.1093/nar/gkh340
10.1073/pnas.1815431116
10.1038/s41929-019-0307-6
10.1007/s10858-016-0060-y
10.1021/ja9815733
10.1007/s00018-006-6055-1
10.1021/ja300265w
10.1126/science.1179557
10.1063/1.470117
10.1021/ja206442c
10.1063/1.328693
10.1107/S0907444910007493
10.1021/ct700200b
10.1007/s10858-018-0166-5
10.1371/journal.pone.0009490
10.1021/ct900549r
10.1021/ja0367389
10.1073/pnas.1216597110
10.1021/jacs.6b08744
10.1016/0009-2614(90)85567-V
10.1074/jbc.M805963200
10.1073/pnas.0804221105
10.1016/S0076-6879(97)76066-X
10.1016/j.str.2005.04.014
10.7554/eLife.32764
10.1089/ars.2012.4962
10.1021/ja00381a010
10.1021/ja0207089
10.1021/ja971639e
10.1002/prot.20449
10.1021/ja003447g
10.1126/science.1187409
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Keywords computational biology
systems biology
NMR
protein dynamics
local frustration
structural biology
molecular biophysics
molecular dynamics
oxidoreductase
E. coli
Language English
License 2020, Stelzl et al.
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Department of Theoretical Biophysics, Max Planck Institute of Biophysics, Frankfurt, Germany.
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References MacKerell (bib42) 1998; 102
Nielsen (bib52) 2018; 70
Price (bib62) 2010; 5
Peters (bib61) 2012; 8
Delaglio (bib17) 1995; 6
Ferreiro (bib26) 2014; 47
Baldwin (bib5) 2011; 133
Zhang (bib84) 2016; 138
Sugase (bib78) 2007; 447
Denoncin (bib18) 2013; 19
Shaw (bib69) 2010; 330
Wang (bib82) 2016; 5
Stirnimann (bib76) 2005; 13
Adams (bib2) 2010; 66
Lange (bib38) 2008; 320
Chandrasekhar (bib13) 1992; 226
Fersht (bib28) 1984
Danielsson (bib15) 2013; 110
Michaud-Agrawal (bib49) 2011; 32
Palmer (bib57) 1992; 75
Olsson (bib53) 2017; 139
Skrynnikov (bib72) 2002; 124
Boehr (bib8) 2009; 5
Lipari (bib40) 1982; 104
Smith (bib74) 2018; 293
Mavridou (bib46) 2009; 284
Robustelli (bib63) 2012; 134
Robustelli (bib64) 2013; 9
Depuydt (bib19) 2009; 326
Grey (bib31) 2003; 125
Rozhkova (bib65) 2004; 23
Mulder (bib50) 2001; 123
Vallurupalli (bib79) 2008; 105
Pan (bib58) 2019; 116
Loria (bib41) 1999; 121
Van Der Spoel (bib80) 2005; 26
Essmann (bib23) 1995; 103
Skinner (bib71) 2016; 66
Haebel (bib32) 2002; 21
Ferreiro (bib25) 2011; 108
Ferreiro (bib27) 2018; 48
Freiberger (bib29) 2019; 116
Bjelkmar (bib7) 2010; 6
Zhou (bib85) 2014; 107
Emsley (bib22) 2010; 66
Ottiger (bib55) 1998; 131
Mavridou (bib47) 2011; 286
Stiller (bib75) 2019; 2
Goulding (bib30) 2002; 41
Sekhar (bib68) 2018; 7
Stirnimann (bib77) 2006; 63
Boyd (bib10) 1998; 120
Murshudov (bib51) 1997; 53
Paul (bib60) 2017; 8
Ferreiro (bib24) 2007; 104
Cho (bib14) 2013; 18
Jenik (bib36) 2012; 40
Parrinello (bib59) 1981; 52
Hess (bib34) 2008; 4
Rozhkova (bib66) 2007; 367
Schmidt (bib67) 2006; 45
Baldwin (bib4) 2011; 413
Hekkelman (bib33) 2010; 38
Otwinowski (bib56) 1997; 276
Smith (bib73) 2013; 14
Ottiger (bib54) 1997; 119
Xue (bib83) 2012; 134
Mackerell (bib43) 2004; 25
Vranken (bib81) 2005; 59
Bussi (bib12) 2007; 126
Alderson (bib3) 2019; 10
Brunger (bib11) 1992
Shen (bib70) 2013; 56
Baldwin (bib6) 2009; 5
Das (bib16) 2013; 110
Mandel (bib44) 1995; 246
Kay (bib37) 1989; 28
Dill (bib20) 2010
Boyd (bib9) 1990; 175
Lipari (bib39) 1982; 104
Abragam (bib1) 1961
Edgar (bib21) 2004; 32
Mavridou (bib45) 2007; 370
Mavridou (bib48) 2012; 6
Humphrey (bib35) 1996; 14
References_xml – volume: 47
  start-page: 285
  year: 2014
  ident: bib26
  article-title: Frustration in biomolecules
  publication-title: Quarterly Reviews of Biophysics
  doi: 10.1017/S0033583514000092
  contributor:
    fullname: Ferreiro
– volume: 32
  start-page: 2319
  year: 2011
  ident: bib49
  article-title: MDAnalysis: a toolkit for the analysis of molecular dynamics simulations
  publication-title: Journal of Computational Chemistry
  doi: 10.1002/jcc.21787
  contributor:
    fullname: Michaud-Agrawal
– volume: 447
  start-page: 1021
  year: 2007
  ident: bib78
  article-title: Mechanism of coupled folding and binding of an intrinsically disordered protein
  publication-title: Nature
  doi: 10.1038/nature05858
  contributor:
    fullname: Sugase
– volume: 108
  start-page: 3499
  year: 2011
  ident: bib25
  article-title: On the role of frustration in the energy landscapes of allosteric proteins
  publication-title: PNAS
  doi: 10.1073/pnas.1018980108
  contributor:
    fullname: Ferreiro
– volume: 45
  start-page: 7429
  year: 2006
  ident: bib67
  article-title: Allosteric disulfide bonds
  publication-title: Biochemistry
  doi: 10.1021/bi0603064
  contributor:
    fullname: Schmidt
– volume: 14
  start-page: 1780
  year: 2013
  ident: bib73
  article-title: The dynamics of lysozyme from bacteriophage lambda in solution probed by NMR and MD simulations
  publication-title: ChemBioChem
  doi: 10.1002/cbic.201300193
  contributor:
    fullname: Smith
– volume: 104
  start-page: 4546
  year: 1982
  ident: bib39
  article-title: Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. theory and range of validity
  publication-title: Journal of the American Chemical Society
  doi: 10.1021/ja00381a009
  contributor:
    fullname: Lipari
– volume-title: Enzyme Structure and Mechanism
  year: 1984
  ident: bib28
  contributor:
    fullname: Fersht
– volume: 133
  start-page: 14160
  year: 2011
  ident: bib5
  article-title: Metastability of native proteins and the phenomenon of amyloid formation
  publication-title: Journal of the American Chemical Society
  doi: 10.1021/ja2017703
  contributor:
    fullname: Baldwin
– volume: 104
  start-page: 19819
  year: 2007
  ident: bib24
  article-title: Localizing frustration in native proteins and protein assemblies
  publication-title: PNAS
  doi: 10.1073/pnas.0709915104
  contributor:
    fullname: Ferreiro
– volume: 139
  start-page: 200
  year: 2017
  ident: bib53
  article-title: Mechanistic models of chemical exchange induced relaxation in protein NMR
  publication-title: Journal of the American Chemical Society
  doi: 10.1021/jacs.6b09460
  contributor:
    fullname: Olsson
– volume: 8
  year: 2012
  ident: bib61
  article-title: Ubiquitin dynamics in complexes reveal molecular recognition mechanisms beyond induced fit and conformational selection
  publication-title: PLOS Computational Biology
  doi: 10.1371/journal.pcbi.1002704
  contributor:
    fullname: Peters
– volume: 41
  start-page: 6920
  year: 2002
  ident: bib30
  article-title: Thiol-disulfide exchange in an immunoglobulin-like fold: structure of the N-terminal domain of DsbD
  publication-title: Biochemistry-Us
  doi: 10.1021/bi016038l
  contributor:
    fullname: Goulding
– volume: 367
  start-page: 1162
  year: 2007
  ident: bib66
  article-title: Kinetics of the intramolecular disulfide exchange between the periplasmic domains of DsbD
  publication-title: Journal of Molecular Biology
  doi: 10.1016/j.jmb.2006.12.033
  contributor:
    fullname: Rozhkova
– volume: 107
  start-page: 672
  year: 2014
  ident: bib85
  article-title: Identification of allosteric disulfides from prestress analysis
  publication-title: Biophysical Journal
  doi: 10.1016/j.bpj.2014.06.025
  contributor:
    fullname: Zhou
– volume: 110
  start-page: 3829
  year: 2013
  ident: bib15
  article-title: Global structural motions from the strain of a single hydrogen bond
  publication-title: PNAS
  doi: 10.1073/pnas.1217306110
  contributor:
    fullname: Danielsson
– volume: 5
  year: 2016
  ident: bib82
  article-title: Mapping transiently formed and sparsely populated conformations on a complex energy landscape
  publication-title: eLife
  doi: 10.7554/eLife.17505
  contributor:
    fullname: Wang
– volume: 102
  start-page: 3586
  year: 1998
  ident: bib42
  article-title: All-atom empirical potential for molecular modeling and dynamics studies of proteins
  publication-title: The Journal of Physical Chemistry B
  doi: 10.1021/jp973084f
  contributor:
    fullname: MacKerell
– volume: 116
  start-page: 4037
  year: 2019
  ident: bib29
  article-title: Local frustration around enzyme active sites
  publication-title: PNAS
  doi: 10.1073/pnas.1819859116
  contributor:
    fullname: Freiberger
– volume: 126
  year: 2007
  ident: bib12
  article-title: Canonical sampling through velocity rescaling
  publication-title: The Journal of Chemical Physics
  doi: 10.1063/1.2408420
  contributor:
    fullname: Bussi
– volume: 9
  start-page: 5190
  year: 2013
  ident: bib64
  article-title: Conformational dynamics of the partially disordered yeast transcription factor GCN4
  publication-title: Journal of Chemical Theory and Computation
  doi: 10.1021/ct400654r
  contributor:
    fullname: Robustelli
– volume: 23
  start-page: 1709
  year: 2004
  ident: bib65
  article-title: Structural basis and kinetics of inter- and intramolecular disulfide exchange in the redox catalyst DsbD
  publication-title: The EMBO Journal
  doi: 10.1038/sj.emboj.7600178
  contributor:
    fullname: Rozhkova
– volume: 14
  start-page: 33
  year: 1996
  ident: bib35
  article-title: VMD: visual molecular dynamics
  publication-title: Journal of Molecular Graphics
  doi: 10.1016/0263-7855(96)00018-5
  contributor:
    fullname: Humphrey
– volume: 8
  year: 2017
  ident: bib60
  article-title: Protein-peptide association kinetics beyond the seconds timescale from atomistic simulations
  publication-title: Nature Communications
  doi: 10.1038/s41467-017-01163-6
  contributor:
    fullname: Paul
– volume: 320
  start-page: 1471
  year: 2008
  ident: bib38
  article-title: Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution
  publication-title: Science
  doi: 10.1126/science.1157092
  contributor:
    fullname: Lange
– volume: 48
  start-page: 68
  year: 2018
  ident: bib27
  article-title: Frustration, function and folding
  publication-title: Current Opinion in Structural Biology
  doi: 10.1016/j.sbi.2017.09.006
  contributor:
    fullname: Ferreiro
– volume: 121
  start-page: 2331
  year: 1999
  ident: bib41
  article-title: A Relaxation-Compensated carr−purcell−meiboom−gill sequence for characterizing chemical exchange by NMR spectroscopy
  publication-title: Journal of the American Chemical Society
  doi: 10.1021/ja983961a
  contributor:
    fullname: Loria
– volume: 10
  year: 2019
  ident: bib3
  article-title: Local unfolding of the HSP27 monomer regulates chaperone activity
  publication-title: Nature Communications
  doi: 10.1038/s41467-019-08557-8
  contributor:
    fullname: Alderson
– volume: 226
  start-page: 239
  year: 1992
  ident: bib13
  article-title: A 500 ps molecular dynamics simulation study of interleukin-1 beta in water correlation with nuclear magnetic resonance spectroscopy and crystallography
  publication-title: Journal of Molecular Biology
  doi: 10.1016/0022-2836(92)90136-8
  contributor:
    fullname: Chandrasekhar
– volume: 40
  start-page: W348
  year: 2012
  ident: bib36
  article-title: Protein frustratometer: a tool to localize energetic frustration in protein molecules
  publication-title: Nucleic Acids Research
  doi: 10.1093/nar/gks447
  contributor:
    fullname: Jenik
– volume: 19
  start-page: 63
  year: 2013
  ident: bib18
  article-title: Disulfide bond formation in the bacterial periplasm: major achievements and challenges ahead
  publication-title: Antioxidants & Redox Signaling
  doi: 10.1089/ars.2012.4864
  contributor:
    fullname: Denoncin
– volume: 131
  start-page: 373
  year: 1998
  ident: bib55
  article-title: Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra
  publication-title: Journal of Magnetic Resonance
  doi: 10.1006/jmre.1998.1361
  contributor:
    fullname: Ottiger
– volume: 66
  start-page: 213
  year: 2010
  ident: bib2
  article-title: PHENIX: a comprehensive Python-based system for macromolecular structure solution
  publication-title: Acta Crystallographica Section D Biological Crystallography
  doi: 10.1107/S0907444909052925
  contributor:
    fullname: Adams
– volume: 370
  start-page: 643
  year: 2007
  ident: bib45
  article-title: Active-site properties of the oxidized and reduced C-terminal domain of DsbD obtained by NMR spectroscopy
  publication-title: Journal of Molecular Biology
  doi: 10.1016/j.jmb.2007.04.038
  contributor:
    fullname: Mavridou
– volume: 28
  start-page: 8972
  year: 1989
  ident: bib37
  article-title: Backbone dynamics of proteins as studied by 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease
  publication-title: Biochemistry
  doi: 10.1021/bi00449a003
  contributor:
    fullname: Kay
– volume: 6
  start-page: 277
  year: 1995
  ident: bib17
  article-title: NMRPipe: a multidimensional spectral processing system based on UNIX pipes
  publication-title: Journal of Biomolecular NMR
  doi: 10.1007/BF00197809
  contributor:
    fullname: Delaglio
– volume: 53
  start-page: 240
  year: 1997
  ident: bib51
  article-title: Refinement of macromolecular structures by the maximum-likelihood method
  publication-title: Acta Crystallographica Section D Biological Crystallography
  doi: 10.1107/S0907444996012255
  contributor:
    fullname: Murshudov
– volume: 293
  start-page: 16559
  year: 2018
  ident: bib74
  article-title: Structural and biochemical insights into the disulfide reductase mechanism of DsbD, an essential enzyme for neisserial pathogens
  publication-title: Journal of Biological Chemistry
  doi: 10.1074/jbc.RA118.004847
  contributor:
    fullname: Smith
– volume: 38
  start-page: W719
  year: 2010
  ident: bib33
  article-title: WIWS: a protein structure bioinformatics web service collection
  publication-title: Nucleic Acids Research
  doi: 10.1093/nar/gkq453
  contributor:
    fullname: Hekkelman
– volume: 21
  start-page: 4774
  year: 2002
  ident: bib32
  article-title: The disulfide bond isomerase DsbC is activated by an immunoglobulin-fold thiol oxidoreductase: crystal structure of the DsbC-DsbDalpha complex
  publication-title: The EMBO Journal
  doi: 10.1093/emboj/cdf489
  contributor:
    fullname: Haebel
– volume-title: Molecular Driving Forces: Statistical Thermodynamics in Biology, Chemistry, Physics and Nanoscience
  year: 2010
  ident: bib20
  doi: 10.4324/9780203809075
  contributor:
    fullname: Dill
– volume: 5
  start-page: 789
  year: 2009
  ident: bib8
  article-title: The role of dynamic conformational ensembles in biomolecular recognition
  publication-title: Nature Chemical Biology
  doi: 10.1038/nchembio.232
  contributor:
    fullname: Boehr
– volume: 6
  start-page: 163
  year: 2012
  ident: bib48
  article-title: 1h, 13C and 15N resonance assignments for the oxidized and reduced states of the N-terminal domain of DsbD from Escherichia coli
  publication-title: Biomolecular NMR Assignments
  doi: 10.1007/s12104-011-9347-9
  contributor:
    fullname: Mavridou
– volume: 286
  start-page: 24943
  year: 2011
  ident: bib47
  article-title: Oxidation state-dependent protein-protein interactions in disulfide cascades
  publication-title: Journal of Biological Chemistry
  doi: 10.1074/jbc.M111.236141
  contributor:
    fullname: Mavridou
– volume: 246
  start-page: 144
  year: 1995
  ident: bib44
  article-title: Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme
  publication-title: Journal of Molecular Biology
  doi: 10.1006/jmbi.1994.0073
  contributor:
    fullname: Mandel
– volume: 56
  start-page: 227
  year: 2013
  ident: bib70
  article-title: Protein backbone and sidechain torsion angles predicted from NMR chemical shifts using artificial neural networks
  publication-title: Journal of Biomolecular NMR
  doi: 10.1007/s10858-013-9741-y
  contributor:
    fullname: Shen
– volume: 26
  start-page: 1701
  year: 2005
  ident: bib80
  article-title: GROMACS: fast, flexible, and free
  publication-title: Journal of Computational Chemistry
  doi: 10.1002/jcc.20291
  contributor:
    fullname: Van Der Spoel
– volume: 5
  start-page: 808
  year: 2009
  ident: bib6
  article-title: NMR spectroscopy brings invisible protein states into focus
  publication-title: Nature Chemical Biology
  doi: 10.1038/nchembio.238
  contributor:
    fullname: Baldwin
– volume: 75
  start-page: 699
  year: 1992
  ident: bib57
  article-title: Suppression of the effects of cross-correlation between dipolar and anisotropic chemical shift relaxation mechanisms in the measurement of spin-spin relaxation rates
  publication-title: Molecular Physics
  doi: 10.1080/00268979200100511
  contributor:
    fullname: Palmer
– volume: 25
  start-page: 1400
  year: 2004
  ident: bib43
  article-title: Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations
  publication-title: Journal of Computational Chemistry
  doi: 10.1002/jcc.20065
  contributor:
    fullname: Mackerell
– volume: 413
  start-page: 310
  year: 2011
  ident: bib4
  article-title: Quaternary dynamics of αB-crystallin as a direct consequence of localised tertiary fluctuations in the C-terminus
  publication-title: Journal of Molecular Biology
  doi: 10.1016/j.jmb.2011.07.017
  contributor:
    fullname: Baldwin
– volume: 32
  start-page: 1792
  year: 2004
  ident: bib21
  article-title: MUSCLE: multiple sequence alignment with high accuracy and high throughput
  publication-title: Nucleic Acids Research
  doi: 10.1093/nar/gkh340
  contributor:
    fullname: Edgar
– volume: 116
  start-page: 4244
  year: 2019
  ident: bib58
  article-title: Atomic-level characterization of protein-protein association
  publication-title: PNAS
  doi: 10.1073/pnas.1815431116
  contributor:
    fullname: Pan
– volume: 2
  start-page: 726
  year: 2019
  ident: bib75
  article-title: Probing the transition state in enzyme catalysis by High-Pressure NMR dynamics
  publication-title: Nature Catalysis
  doi: 10.1038/s41929-019-0307-6
  contributor:
    fullname: Stiller
– volume: 66
  start-page: 111
  year: 2016
  ident: bib71
  article-title: CcpNmr AnalysisAssign: a flexible platform for integrated NMR analysis
  publication-title: Journal of Biomolecular NMR
  doi: 10.1007/s10858-016-0060-y
  contributor:
    fullname: Skinner
– volume: 120
  start-page: 9692
  year: 1998
  ident: bib10
  article-title: Defining the orientation of the 15N shielding tensor using 15N NMR relaxation data for a protein in solution
  publication-title: Journal of the American Chemical Society
  doi: 10.1021/ja9815733
  contributor:
    fullname: Boyd
– volume: 63
  start-page: 1642
  year: 2006
  ident: bib77
  article-title: nDsbD: a redox interaction hub in the Escherichia coli periplasm
  publication-title: Cellular and Molecular Life Sciences
  doi: 10.1007/s00018-006-6055-1
  contributor:
    fullname: Stirnimann
– volume: 134
  start-page: 6365
  year: 2012
  ident: bib63
  article-title: Interpreting protein structural dynamics from NMR chemical shifts
  publication-title: Journal of the American Chemical Society
  doi: 10.1021/ja300265w
  contributor:
    fullname: Robustelli
– volume: 326
  start-page: 1109
  year: 2009
  ident: bib19
  article-title: A periplasmic reducing system protects single cysteine residues from oxidation
  publication-title: Science
  doi: 10.1126/science.1179557
  contributor:
    fullname: Depuydt
– volume: 103
  start-page: 8577
  year: 1995
  ident: bib23
  article-title: A smooth particle mesh ewald method
  publication-title: The Journal of Chemical Physics
  doi: 10.1063/1.470117
  contributor:
    fullname: Essmann
– volume: 134
  start-page: 2555
  year: 2012
  ident: bib83
  article-title: Microsecond time-scale conformational exchange in proteins: using long molecular dynamics trajectory to simulate NMR relaxation dispersion data
  publication-title: Journal of the American Chemical Society
  doi: 10.1021/ja206442c
  contributor:
    fullname: Xue
– volume: 52
  start-page: 7182
  year: 1981
  ident: bib59
  article-title: Polymorphic transitions in single crystals: a new molecular dynamics method
  publication-title: Journal of Applied Physics
  doi: 10.1063/1.328693
  contributor:
    fullname: Parrinello
– volume: 66
  start-page: 486
  year: 2010
  ident: bib22
  article-title: Features and development of coot
  publication-title: Acta Crystallographica. Section D, Biological Crystallography
  doi: 10.1107/S0907444910007493
  contributor:
    fullname: Emsley
– volume: 4
  start-page: 116
  year: 2008
  ident: bib34
  article-title: P-LINCS: A Parallel Linear Constraint Solver for Molecular Simulation
  publication-title: Journal of Chemical Theory and Computation
  doi: 10.1021/ct700200b
  contributor:
    fullname: Hess
– volume: 70
  start-page: 141
  year: 2018
  ident: bib52
  article-title: POTENCI: prediction of temperature, neighbor and pH-corrected chemical shifts for intrinsically disordered proteins
  publication-title: Journal of Biomolecular NMR
  doi: 10.1007/s10858-018-0166-5
  contributor:
    fullname: Nielsen
– volume: 5
  year: 2010
  ident: bib62
  article-title: FastTree 2--approximately maximum-likelihood trees for large alignments
  publication-title: PLOS ONE
  doi: 10.1371/journal.pone.0009490
  contributor:
    fullname: Price
– volume: 6
  start-page: 459
  year: 2010
  ident: bib7
  article-title: Implementation of the CHARMM force field in GROMACS: analysis of protein stability effects from correction maps, virtual interaction sites, and water models
  publication-title: Journal of Chemical Theory and Computation
  doi: 10.1021/ct900549r
  contributor:
    fullname: Bjelkmar
– volume: 125
  start-page: 14324
  year: 2003
  ident: bib31
  article-title: Disulfide bond isomerization in basic pancreatic trypsin inhibitor: multisite chemical exchange quantified by CPMG relaxation dispersion and chemical shift modeling
  publication-title: Journal of the American Chemical Society
  doi: 10.1021/ja0367389
  contributor:
    fullname: Grey
– volume: 110
  start-page: 3871
  year: 2013
  ident: bib16
  article-title: SOD1 exhibits allosteric frustration to facilitate metal binding affinity
  publication-title: PNAS
  doi: 10.1073/pnas.1216597110
  contributor:
    fullname: Das
– volume: 138
  start-page: 14066
  year: 2016
  ident: bib84
  article-title: HIV-1 capsid function is regulated by dynamics: quantitative Atomic-Resolution insights by integrating Magic-Angle-Spinning NMR, QM/MM, and MD
  publication-title: Journal of the American Chemical Society
  doi: 10.1021/jacs.6b08744
  contributor:
    fullname: Zhang
– volume-title: X-PLOR Version 3.1: A System for X-Ray Crystallography and NMR
  year: 1992
  ident: bib11
  contributor:
    fullname: Brunger
– volume: 175
  start-page: 477
  year: 1990
  ident: bib9
  article-title: Influence of cross-correlation between dipolar and anisotropic chemical shift relaxation mechanisms upon longitudinal relaxation rates of 15N in macromolecules
  publication-title: Chemical Physics Letters
  doi: 10.1016/0009-2614(90)85567-V
  contributor:
    fullname: Boyd
– volume: 284
  start-page: 3219
  year: 2009
  ident: bib46
  article-title: Control of periplasmic interdomain thiol:disulfide exchange in the transmembrane oxidoreductase DsbD
  publication-title: Journal of Biological Chemistry
  doi: 10.1074/jbc.M805963200
  contributor:
    fullname: Mavridou
– volume: 105
  start-page: 11766
  year: 2008
  ident: bib79
  article-title: Structures of invisible, excited protein states by relaxation dispersion NMR spectroscopy
  publication-title: PNAS
  doi: 10.1073/pnas.0804221105
  contributor:
    fullname: Vallurupalli
– volume: 276
  start-page: 307
  year: 1997
  ident: bib56
  article-title: Processing of X-ray diffraction data collected in oscillation mode
  publication-title: Methods in Enzymology
  doi: 10.1016/S0076-6879(97)76066-X
  contributor:
    fullname: Otwinowski
– volume: 13
  start-page: 985
  year: 2005
  ident: bib76
  article-title: Structural basis and kinetics of DsbD-Dependent cytochrome c Maturation
  publication-title: Structure
  doi: 10.1016/j.str.2005.04.014
  contributor:
    fullname: Stirnimann
– volume: 7
  year: 2018
  ident: bib68
  article-title: Conserved conformational selection mechanism of Hsp70 chaperone-substrate interactions
  publication-title: eLife
  doi: 10.7554/eLife.32764
  contributor:
    fullname: Sekhar
– volume: 18
  start-page: 1690
  year: 2013
  ident: bib14
  article-title: Many roles of the bacterial envelope reducing pathways
  publication-title: Antioxidants & Redox Signaling
  doi: 10.1089/ars.2012.4962
  contributor:
    fullname: Cho
– volume: 104
  start-page: 4559
  year: 1982
  ident: bib40
  article-title: Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. analysis of experimental results
  publication-title: Journal of the American Chemical Society
  doi: 10.1021/ja00381a010
  contributor:
    fullname: Lipari
– volume: 124
  start-page: 12352
  year: 2002
  ident: bib72
  article-title: Reconstructing NMR spectra of “Invisible” Excited Protein States Using HSQC and HMQC Experiments
  publication-title: Journal of the American Chemical Society
  doi: 10.1021/ja0207089
  contributor:
    fullname: Skrynnikov
– volume-title: The Principles of Nuclear Magnetism, the International Series of Monographs on Physics
  year: 1961
  ident: bib1
  contributor:
    fullname: Abragam
– volume: 119
  start-page: 9825
  year: 1997
  ident: bib54
  article-title: Magnetic Field Dependent Amide 15 N Chemical Shifts in a Protein−DNA Complex Resulting from Magnetic Ordering in Solution
  publication-title: Journal of the American Chemical Society
  doi: 10.1021/ja971639e
  contributor:
    fullname: Ottiger
– volume: 59
  start-page: 687
  year: 2005
  ident: bib81
  article-title: The CCPN data model for NMR spectroscopy: development of a software pipeline
  publication-title: Proteins: Structure, Function, and Bioinformatics
  doi: 10.1002/prot.20449
  contributor:
    fullname: Vranken
– volume: 123
  start-page: 967
  year: 2001
  ident: bib50
  article-title: Measurement of slow (micros-ms) time scale dynamics in protein side chains by (15)N relaxation dispersion NMR spectroscopy: application to asn and gln residues in a cavity mutant of T4 lysozyme
  publication-title: Journal of the American Chemical Society
  doi: 10.1021/ja003447g
  contributor:
    fullname: Mulder
– volume: 330
  start-page: 341
  year: 2010
  ident: bib69
  article-title: Atomic-level characterization of the structural dynamics of proteins
  publication-title: Science
  doi: 10.1126/science.1187409
  contributor:
    fullname: Shaw
SSID ssj0000748819
Score 2.3628407
Snippet Local structural frustration, the existence of mutually exclusive competing interactions, may explain why some proteins are dynamic while others are rigid....
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SubjectTerms Catalysis
Catalytic Domain
Chemical bonds
Chemical modification
Computational and Systems Biology
Cycling
Cysteine
Cysteine - metabolism
Cystine
Escherichia coli - metabolism
Escherichia coli Proteins - metabolism
Experiments
Frustration
Immunoglobulins
local frustration
molecular dynamics
NMR
Oxidation
Oxidation-Reduction
Oxidoreductase
Oxidoreductases - metabolism
Periplasm
Periplasm - metabolism
Periplasmic Proteins - metabolism
Protein Binding
protein dynamics
Protein structure
Proteins
Structural Biology and Molecular Biophysics
Sulfhydryl Compounds - metabolism
Thiols
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Title Local frustration determines loop opening during the catalytic cycle of an oxidoreductase
URI https://www.ncbi.nlm.nih.gov/pubmed/32568066
https://www.proquest.com/docview/2429406670
https://search.proquest.com/docview/2415832162
https://pubmed.ncbi.nlm.nih.gov/PMC7347389
https://doaj.org/article/91b2903dba754d03b967a55ca869e844
Volume 9
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