Periplasmic Binding Protein Dimer Has a Second Allosteric Event Tied to Ligand Binding

Li, Le; Ghimire-Rijal, Sudipa; Lucas, Sarah L.; Stanley, Christopher B.; Wright, Edward; Agarwal, Pratul K.; Myles, Dean A.; Cuneo, Matthew J.

doi:10.1021/acs.biochem.7b00657

Title: Periplasmic Binding Protein Dimer Has a Second Allosteric Event Tied to Ligand Binding

Journal Article · Wed Sep 06 00:00:00 EDT 2017 · Biochemistry

DOI:https://doi.org/10.1021/acs.biochem.7b00657· OSTI ID:1407759

^[1]; Ghimire-Rijal, Sudipa ^[1]; Lucas, Sarah L. ^[2];

^[1]; Wright, Edward ^[3];

^[4]; Myles, Dean A. ^[1];

^[1]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); North Carolina State Univ., Raleigh, NC (United States)
Univ. of Tennessee, Knoxville, TN (United States)
Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Here, the ligand-induced conformational changes of periplasmic binding proteins (PBP) play a key role in the acquisition of metabolites in ATP binding cassette (ABC) transport systems. This conformational change allows for differential recognition of the ligand occupancy of the PBP by the ABC transporter. This minimizes futile ATP hydrolysis in the transporter, a phenomenon in which ATP hydrolysis is not coupled to metabolite transport. In many systems, the PBP conformational change is insufficient at eliminating futile ATP hydrolysis. Here we identify an additional state of the PBP that is also allosterically regulated by the ligand. Ligand binding to the homodimeric apo PBP leads to a tightening of the interface alpha-helices so that the hydrogen bonding pattern shifts to that of a 3₁₀ helix, in-turn altering the contacts and the dynamics of the protein interface so that the monomer exists in the presence of ligand.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1407759

Journal Information:: Biochemistry, Vol. 56, Issue 40; ISSN 0006-2960

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 12 works

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References (49)

MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes Davis, I. W.; Murray, L. W.; Richardson, J. S. Nucleic Acids Research, Vol. 32, Issue Web Server https://doi.org/10.1093/nar/gkh398	journal	July 2004
Structure of an ABC transporter in complex with its binding protein Hollenstein, Kaspar; Frei, Dominik C.; Locher, Kaspar P. Nature, Vol. 446, Issue 7132 https://doi.org/10.1038/nature05626	journal	February 2007
ABC transporters: one, two or four extracytoplasmic substrate-binding sites? van der Heide, T.; Poolman, B. EMBO reports, Vol. 3, Issue 10 https://doi.org/10.1093/embo-reports/kvf201	journal	October 2002
Ligand-induced conformational changes in a thermophilic ribose-binding protein Cuneo, Matthew J.; Beese, Lorena S.; Hellinga, Homme W. BMC Structural Biology, Vol. 8, Issue 1 https://doi.org/10.1186/1472-6807-8-50	journal	January 2008
Liganded and Unliganded Receptors Interact with Equal Affinity with the Membrane Complex of Periplasmic Permeases, a Subfamily of Traffic ATPases Ames, Giovanna Ferro-Luzzi; Liu, Cheng Eureka; Joshi, Anil K. Journal of Biological Chemistry, Vol. 271, Issue 24 https://doi.org/10.1074/jbc.271.24.14264	journal	June 1996
Absolute calibration of small-angle neutron scattering data Wignall, G. D.; Bates, F. S. Journal of Applied Crystallography, Vol. 20, Issue 1 https://doi.org/10.1107/S0021889887087181	journal	February 1987
CRYSOL – a Program to Evaluate X-ray Solution Scattering of Biological Macromolecules from Atomic Coordinates Svergun, D.; Barberato, C.; Koch, M. H. J. Journal of Applied Crystallography, Vol. 28, Issue 6 https://doi.org/10.1107/S0021889895007047	journal	December 1995
Determination of the regularization parameter in indirect-transform methods using perceptual criteria Svergun, D. I. Journal of Applied Crystallography, Vol. 25, Issue 4, p. 495-503 https://doi.org/10.1107/S0021889892001663	journal	August 1992
The Amber biomolecular simulation programs Case, David A.; Cheatham, Thomas E.; Darden, Tom Journal of Computational Chemistry, Vol. 26, Issue 16 https://doi.org/10.1002/jcc.20290	journal	January 2005
Allostery: an illustrated definition for the ‘second secret of life’ Fenton, Aron W. Trends in Biochemical Sciences, Vol. 33, Issue 9 https://doi.org/10.1016/j.tibs.2008.05.009	journal	September 2008
The Allosteric Regulatory Mechanism of the Escherichia coli MetNI Methionine ATP Binding Cassette (ABC) Transporter Yang, Janet G.; Rees, Douglas C. Journal of Biological Chemistry, Vol. 290, Issue 14 https://doi.org/10.1074/jbc.M114.603365	journal	February 2015
Cis/trans isomerization in HIV-1 capsid protein catalyzed by cyclophilin A: Insights from computational and theoretical studies Agarwal, Pratul K. Proteins: Structure, Function, and Bioinformatics, Vol. 56, Issue 3 https://doi.org/10.1002/prot.20135	journal	May 2004
PRIMUS: a Windows PC-based system for small-angle scattering data analysis Konarev, Petr V.; Volkov, Vladimir V.; Sokolova, Anna V. Journal of Applied Crystallography, Vol. 36, Issue 5, p. 1277-1282 https://doi.org/10.1107/S0021889803012779	journal	September 2003
The High-Affinity E. coli Methionine ABC Transporter: Structure and Allosteric Regulation Kadaba, N. S.; Kaiser, J. T.; Johnson, E. Science, Vol. 321, Issue 5886 https://doi.org/10.1126/science.1157987	journal	July 2008
Structural Analysis of a Periplasmic Binding Protein in the Tripartite ATP-independent Transporter Family Reveals a Tetrameric Assembly That May Have a Role in Ligand Transport Cuneo, Matthew J.; Changela, Anita; Miklos, Aleksandr E. Journal of Biological Chemistry, Vol. 283, Issue 47 https://doi.org/10.1074/jbc.M803595200	journal	August 2008
Conformational Changes of Three Periplasmic Receptors for Bacterial Chemotaxis and Transport: The Maltose-, Glucose/Galactose- and Ribose-binding Proteins. Shilton, Brian H.; Flocco, Maria M.; Nilsson, Martin Journal of Molecular Biology, Vol. 264, Issue 2 https://doi.org/10.1006/jmbi.1996.0645	journal	November 1996
Structure and mechanism of ATP-binding cassette transporters Locher, Kaspar P. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 364, Issue 1514 https://doi.org/10.1098/rstb.2008.0125	journal	October 2008
Protein dynamics explain the allosteric behaviors of hemoglobin Yonetani, Takashi; Laberge, Monique Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1784, Issue 9 https://doi.org/10.1016/j.bbapap.2008.04.025	journal	September 2008
Robust and convenient analysis of protein thermal and chemical stability: Robust and Convenient Analysis of Protein Stability Niklasson, Markus; Andresen, Cecilia; Helander, Sara Protein Science, Vol. 24, Issue 12 https://doi.org/10.1002/pro.2809	journal	October 2015
Size-Distribution Analysis of Macromolecules by Sedimentation Velocity Ultracentrifugation and Lamm Equation Modeling Schuck, Peter Biophysical Journal, Vol. 78, Issue 3 https://doi.org/10.1016/S0006-3495(00)76713-0	journal	March 2000
Evidence for lateral gene transfer between Archaea and Bacteria from genome sequence of Thermotoga maritima Nelson, Karen E.; Clayton, Rebecca A.; Gill, Steven R. Nature, Vol. 399, Issue 6734 https://doi.org/10.1038/20601	journal	May 1999
The extended Q -range small-angle neutron scattering diffractometer at the SNS Zhao, J. K.; Gao, C. Y.; Liu, D. Journal of Applied Crystallography, Vol. 43, Issue 5 https://doi.org/10.1107/S002188981002217X	journal	July 2010
Aspartate and maltose-binding protein interact with adjacent sites in the Tar chemotactic signal transducer of Escherichia coli Gardina, P.; Conway, C.; Kossman, M. Journal of Bacteriology, Vol. 174, Issue 5 https://doi.org/10.1128/jb.174.5.1528-1536.1992	journal	March 1992
Molecular details of ligand selectivity determinants in a promiscuous β-glucan periplasmic binding protein Munshi, Parthapratim; Stanley, Christopher B.; Ghimire-Rijal, Sudipa BMC Structural Biology, Vol. 13, Issue 1 https://doi.org/10.1186/1472-6807-13-18	journal	January 2013
Inference of Macromolecular Assemblies from Crystalline State Krissinel, Evgeny; Henrick, Kim Journal of Molecular Biology, Vol. 372, Issue 3 https://doi.org/10.1016/j.jmb.2007.05.022	journal	September 2007
Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors Brejc, KatjuS̆a; van Dijk, Willem J.; Klaassen, Remco V. Nature, Vol. 411, Issue 6835 https://doi.org/10.1038/35077011	journal	May 2001
Crystal Structure of the Maltose Transporter in a Pretranslocation Intermediate State Oldham, M. L.; Chen, J. Science, Vol. 332, Issue 6034 https://doi.org/10.1126/science.1200767	journal	May 2011
Evolutionarily Conserved Linkage between Enzyme Fold, Flexibility, and Catalysis Ramanathan, Arvind; Agarwal, Pratul K. PLoS Biology, Vol. 9, Issue 11 https://doi.org/10.1371/journal.pbio.1001193	journal	November 2011
Mechanism of maltose transport in Escherichia coli: transmembrane signaling by periplasmic binding proteins. Davidson, A. L.; Shuman, H. A.; Nikaido, H. Proceedings of the National Academy of Sciences, Vol. 89, Issue 6 https://doi.org/10.1073/pnas.89.6.2360	journal	March 1992
Crystallographic evidence of a large ligand-induced hinge-twist motion between the two domains of the maltodextrin binding protein involved in active transport and chemotaxis Sharff, Andrew J.; Rodseth, Lynn E.; Spurlino, John C. Biochemistry, Vol. 31, Issue 44 https://doi.org/10.1021/bi00159a003	journal	November 1992
Allosteric crosstalk between peptide-binding, transport, and ATP hydrolysis of the ABC transporter TAP Gorbulev, S.; Abele, R.; Tampe, R. Proceedings of the National Academy of Sciences, Vol. 98, Issue 7 https://doi.org/10.1073/pnas.061467898	journal	March 2001
Computational Identification of Slow Conformational Fluctuations in Proteins Ramanathan, Arvind; Agarwal, Pratul K. The Journal of Physical Chemistry B, Vol. 113, Issue 52 https://doi.org/10.1021/jp9077213	journal	December 2009
Multiple open forms of ribose-binding protein trace the path of its conformational change Björkman, A. Joakim; Mowbray, Sherry L. Journal of Molecular Biology, Vol. 279, Issue 3 https://doi.org/10.1006/jmbi.1998.1785	journal	June 1998
Crystal structures of an Extracytoplasmic Solute Receptor from a TRAP transporter in its open and closed forms reveal a helix-swapped dimer requiring a cation for α-keto acid binding Gonin, Sophie; Arnoux, Pascal; Pierru, Bénédicte BMC Structural Biology, Vol. 7, Issue 1 https://doi.org/10.1186/1472-6807-7-11	journal	January 2007
Duplication of Genes in an ATP-binding Cassette Transport System Increases Dynamic Range While Maintaining Ligand Specificity Ghimire-Rijal, Sudipa; Lu, Xun; Myles, Dean A. Journal of Biological Chemistry, Vol. 289, Issue 43 https://doi.org/10.1074/jbc.M114.590992	journal	October 2014
Amino acid transport in thermophiles: characterization of an arginine-binding protein in Thermotoga maritima Luchansky, Matthew S.; Der, Bryan S.; D’Auria, Sabato Mol. BioSyst., Vol. 6, Issue 1 https://doi.org/10.1039/B908412F	journal	January 2009
Crystal structure of a catalytic intermediate of the maltose transporter Oldham, Michael L.; Khare, Dheeraj; Quiocho, Florante A. Nature, Vol. 450, Issue 7169 https://doi.org/10.1038/nature06264	journal	November 2007
A reciprocating twin-channel model for ABC transporters Jones, Peter M.; George, Anthony M. Quarterly Reviews of Biophysics, Vol. 47, Issue 3 https://doi.org/10.1017/S0033583514000031	journal	April 2014
The structure of Escherichia coli BtuF and binding to its cognate ATP binding cassette transporter Borths, E. L.; Locher, K. P.; Lee, A. T. Proceedings of the National Academy of Sciences, Vol. 99, Issue 26 https://doi.org/10.1073/pnas.262659699	journal	December 2002
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Stimulation of the Maltose Transporter ATPase by Unliganded Maltose Binding Protein Gould, Alister D.; Telmer, Patrick G.; Shilton, Brian H. Biochemistry, Vol. 48, Issue 33 https://doi.org/10.1021/bi9007066	journal	August 2009
Trapping open and closed forms of FitE-A group III periplasmic binding protein Shi, Rong; Proteau, Ariane; Wagner, John Proteins: Structure, Function, and Bioinformatics, Vol. 75, Issue 3 https://doi.org/10.1002/prot.22272	journal	May 2009
The Protein Data Bank Berman, H. M. Nucleic Acids Research, Vol. 28, Issue 1 https://doi.org/10.1093/nar/28.1.235	journal	January 2000
Full engagement of liganded maltose-binding protein stabilizes a semi-open ATP-binding cassette dimer in the maltose transporter: Maltose-bound MBP stabilizes a semi-open ABC dimer Alvarez, Frances Joan D.; Orelle, Cédric; Huang, Yan Molecular Microbiology, Vol. 98, Issue 5 https://doi.org/10.1111/mmi.13165	journal	September 2015
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Stability of yeast iso-1-ferricytochrome c as a function of pH and temperature Cohen, David S.; Pielak, Gary J. Protein Science, Vol. 3, Issue 8 https://doi.org/10.1002/pro.5560030811	journal	August 1994
Binding protein-independent histidine permease mutants. Uncoupling of ATP hydrolysis from transmembrane signaling. Petronilli, V.; Ames, G. F. Journal of Biological Chemistry, Vol. 266, Issue 25 https://doi.org/10.1016/S0021-9258(18)55294-7	journal	September 1991
Leucine/isoleucine/valine-binding protein contracts upon binding of ligand Olah, G. A.; Trakhanov, S.; Trewhella, J. Journal of Biological Chemistry, Vol. 268, Issue 22 https://doi.org/10.1016/S0021-9258(19)85411-X	journal	August 1993
Dependence of maltose transport and chemotaxis on the amount of maltose-binding protein. Manson, M. D.; Boos, W.; Bassford, P. J. Journal of Biological Chemistry, Vol. 260, Issue 17 https://doi.org/10.1016/S0021-9258(17)39299-2	journal	August 1985

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