Periplasmic Binding Protein Dimer Has a Second Allosteric Event Tied to Ligand Binding
Abstract
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.
- Authors:
-
- 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)
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1407759
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Biochemistry
- Additional Journal Information:
- Journal Volume: 56; Journal Issue: 40; Journal ID: ISSN 0006-2960
- Publisher:
- American Chemical Society (ACS)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Li, Le, Ghimire-Rijal, Sudipa, Lucas, Sarah L., Stanley, Christopher B., Wright, Edward, Agarwal, Pratul K., Myles, Dean A., and Cuneo, Matthew J. Periplasmic Binding Protein Dimer Has a Second Allosteric Event Tied to Ligand Binding. United States: N. p., 2017.
Web. doi:10.1021/acs.biochem.7b00657.
Li, Le, Ghimire-Rijal, Sudipa, Lucas, Sarah L., Stanley, Christopher B., Wright, Edward, Agarwal, Pratul K., Myles, Dean A., & Cuneo, Matthew J. Periplasmic Binding Protein Dimer Has a Second Allosteric Event Tied to Ligand Binding. United States. https://doi.org/10.1021/acs.biochem.7b00657
Li, Le, Ghimire-Rijal, Sudipa, Lucas, Sarah L., Stanley, Christopher B., Wright, Edward, Agarwal, Pratul K., Myles, Dean A., and Cuneo, Matthew J. Wed .
"Periplasmic Binding Protein Dimer Has a Second Allosteric Event Tied to Ligand Binding". United States. https://doi.org/10.1021/acs.biochem.7b00657. https://www.osti.gov/servlets/purl/1407759.
@article{osti_1407759,
title = {Periplasmic Binding Protein Dimer Has a Second Allosteric Event Tied to Ligand Binding},
author = {Li, Le and Ghimire-Rijal, Sudipa and Lucas, Sarah L. and Stanley, Christopher B. and Wright, Edward and Agarwal, Pratul K. and Myles, Dean A. and Cuneo, Matthew J.},
abstractNote = {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.},
doi = {10.1021/acs.biochem.7b00657},
journal = {Biochemistry},
number = 40,
volume = 56,
place = {United States},
year = {Wed Sep 06 00:00:00 EDT 2017},
month = {Wed Sep 06 00:00:00 EDT 2017}
}
Web of Science
Works referenced in this record:
MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes
journal, July 2004
- Davis, I. W.; Murray, L. W.; Richardson, J. S.
- Nucleic Acids Research, Vol. 32, Issue Web Server
Structure of an ABC transporter in complex with its binding protein
journal, February 2007
- Hollenstein, Kaspar; Frei, Dominik C.; Locher, Kaspar P.
- Nature, Vol. 446, Issue 7132
ABC transporters: one, two or four extracytoplasmic substrate-binding sites?
journal, October 2002
- van der Heide, T.; Poolman, B.
- EMBO reports, Vol. 3, Issue 10
Ligand-induced conformational changes in a thermophilic ribose-binding protein
journal, January 2008
- Cuneo, Matthew J.; Beese, Lorena S.; Hellinga, Homme W.
- BMC Structural Biology, Vol. 8, Issue 1
Liganded and Unliganded Receptors Interact with Equal Affinity with the Membrane Complex of Periplasmic Permeases, a Subfamily of Traffic ATPases
journal, June 1996
- Ames, Giovanna Ferro-Luzzi; Liu, Cheng Eureka; Joshi, Anil K.
- Journal of Biological Chemistry, Vol. 271, Issue 24
Absolute calibration of small-angle neutron scattering data
journal, February 1987
- Wignall, G. D.; Bates, F. S.
- Journal of Applied Crystallography, Vol. 20, Issue 1
CRYSOL – a Program to Evaluate X-ray Solution Scattering of Biological Macromolecules from Atomic Coordinates
journal, December 1995
- Svergun, D.; Barberato, C.; Koch, M. H. J.
- Journal of Applied Crystallography, Vol. 28, Issue 6
Determination of the regularization parameter in indirect-transform methods using perceptual criteria
journal, August 1992
- Svergun, D. I.
- Journal of Applied Crystallography, Vol. 25, Issue 4, p. 495-503
The Amber biomolecular simulation programs
journal, January 2005
- Case, David A.; Cheatham, Thomas E.; Darden, Tom
- Journal of Computational Chemistry, Vol. 26, Issue 16
Allostery: an illustrated definition for the ‘second secret of life’
journal, September 2008
- Fenton, Aron W.
- Trends in Biochemical Sciences, Vol. 33, Issue 9
The Allosteric Regulatory Mechanism of the Escherichia coli MetNI Methionine ATP Binding Cassette (ABC) Transporter
journal, February 2015
- Yang, Janet G.; Rees, Douglas C.
- Journal of Biological Chemistry, Vol. 290, Issue 14
Cis/trans isomerization in HIV-1 capsid protein catalyzed by cyclophilin A: Insights from computational and theoretical studies
journal, May 2004
- Agarwal, Pratul K.
- Proteins: Structure, Function, and Bioinformatics, Vol. 56, Issue 3
PRIMUS: a Windows PC-based system for small-angle scattering data analysis
journal, September 2003
- Konarev, Petr V.; Volkov, Vladimir V.; Sokolova, Anna V.
- Journal of Applied Crystallography, Vol. 36, Issue 5, p. 1277-1282
The High-Affinity E. coli Methionine ABC Transporter: Structure and Allosteric Regulation
journal, July 2008
- Kadaba, N. S.; Kaiser, J. T.; Johnson, E.
- Science, Vol. 321, Issue 5886
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
journal, August 2008
- Cuneo, Matthew J.; Changela, Anita; Miklos, Aleksandr E.
- Journal of Biological Chemistry, Vol. 283, Issue 47
Conformational Changes of Three Periplasmic Receptors for Bacterial Chemotaxis and Transport: The Maltose-, Glucose/Galactose- and Ribose-binding Proteins.
journal, November 1996
- Shilton, Brian H.; Flocco, Maria M.; Nilsson, Martin
- Journal of Molecular Biology, Vol. 264, Issue 2
Structure and mechanism of ATP-binding cassette transporters
journal, October 2008
- Locher, Kaspar P.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 364, Issue 1514
Protein dynamics explain the allosteric behaviors of hemoglobin
journal, September 2008
- Yonetani, Takashi; Laberge, Monique
- Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1784, Issue 9
Robust and convenient analysis of protein thermal and chemical stability: Robust and Convenient Analysis of Protein Stability
journal, October 2015
- Niklasson, Markus; Andresen, Cecilia; Helander, Sara
- Protein Science, Vol. 24, Issue 12
Size-Distribution Analysis of Macromolecules by Sedimentation Velocity Ultracentrifugation and Lamm Equation Modeling
journal, March 2000
- Schuck, Peter
- Biophysical Journal, Vol. 78, Issue 3
Evidence for lateral gene transfer between Archaea and Bacteria from genome sequence of Thermotoga maritima
journal, May 1999
- Nelson, Karen E.; Clayton, Rebecca A.; Gill, Steven R.
- Nature, Vol. 399, Issue 6734
The extended Q -range small-angle neutron scattering diffractometer at the SNS
journal, July 2010
- Zhao, J. K.; Gao, C. Y.; Liu, D.
- Journal of Applied Crystallography, Vol. 43, Issue 5
Aspartate and maltose-binding protein interact with adjacent sites in the Tar chemotactic signal transducer of Escherichia coli
journal, March 1992
- Gardina, P.; Conway, C.; Kossman, M.
- Journal of Bacteriology, Vol. 174, Issue 5
Molecular details of ligand selectivity determinants in a promiscuous β-glucan periplasmic binding protein
journal, January 2013
- Munshi, Parthapratim; Stanley, Christopher B.; Ghimire-Rijal, Sudipa
- BMC Structural Biology, Vol. 13, Issue 1
Inference of Macromolecular Assemblies from Crystalline State
journal, September 2007
- Krissinel, Evgeny; Henrick, Kim
- Journal of Molecular Biology, Vol. 372, Issue 3
Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors
journal, May 2001
- Brejc, KatjuS̆a; van Dijk, Willem J.; Klaassen, Remco V.
- Nature, Vol. 411, Issue 6835
Crystal Structure of the Maltose Transporter in a Pretranslocation Intermediate State
journal, May 2011
- Oldham, M. L.; Chen, J.
- Science, Vol. 332, Issue 6034
Evolutionarily Conserved Linkage between Enzyme Fold, Flexibility, and Catalysis
journal, November 2011
- Ramanathan, Arvind; Agarwal, Pratul K.
- PLoS Biology, Vol. 9, Issue 11
Mechanism of maltose transport in Escherichia coli: transmembrane signaling by periplasmic binding proteins.
journal, March 1992
- Davidson, A. L.; Shuman, H. A.; Nikaido, H.
- Proceedings of the National Academy of Sciences, Vol. 89, Issue 6
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
journal, November 1992
- Sharff, Andrew J.; Rodseth, Lynn E.; Spurlino, John C.
- Biochemistry, Vol. 31, Issue 44
Allosteric crosstalk between peptide-binding, transport, and ATP hydrolysis of the ABC transporter TAP
journal, March 2001
- Gorbulev, S.; Abele, R.; Tampe, R.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 7
Computational Identification of Slow Conformational Fluctuations in Proteins
journal, December 2009
- Ramanathan, Arvind; Agarwal, Pratul K.
- The Journal of Physical Chemistry B, Vol. 113, Issue 52
Multiple open forms of ribose-binding protein trace the path of its conformational change
journal, June 1998
- Björkman, A. Joakim; Mowbray, Sherry L.
- Journal of Molecular Biology, Vol. 279, Issue 3
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
journal, January 2007
- Gonin, Sophie; Arnoux, Pascal; Pierru, Bénédicte
- BMC Structural Biology, Vol. 7, Issue 1
Duplication of Genes in an ATP-binding Cassette Transport System Increases Dynamic Range While Maintaining Ligand Specificity
journal, October 2014
- Ghimire-Rijal, Sudipa; Lu, Xun; Myles, Dean A.
- Journal of Biological Chemistry, Vol. 289, Issue 43
Amino acid transport in thermophiles: characterization of an arginine-binding protein in Thermotoga maritima
journal, January 2009
- Luchansky, Matthew S.; Der, Bryan S.; D’Auria, Sabato
- Mol. BioSyst., Vol. 6, Issue 1
Crystal structure of a catalytic intermediate of the maltose transporter
journal, November 2007
- Oldham, Michael L.; Khare, Dheeraj; Quiocho, Florante A.
- Nature, Vol. 450, Issue 7169
A reciprocating twin-channel model for ABC transporters
journal, April 2014
- Jones, Peter M.; George, Anthony M.
- Quarterly Reviews of Biophysics, Vol. 47, Issue 3
The structure of Escherichia coli BtuF and binding to its cognate ATP binding cassette transporter
journal, December 2002
- Borths, E. L.; Locher, K. P.; Lee, A. T.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 26
PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
Stimulation of the Maltose Transporter ATPase by Unliganded Maltose Binding Protein
journal, August 2009
- Gould, Alister D.; Telmer, Patrick G.; Shilton, Brian H.
- Biochemistry, Vol. 48, Issue 33
Trapping open and closed forms of FitE-A group III periplasmic binding protein
journal, May 2009
- Shi, Rong; Proteau, Ariane; Wagner, John
- Proteins: Structure, Function, and Bioinformatics, Vol. 75, Issue 3
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
journal, September 2015
- Alvarez, Frances Joan D.; Orelle, Cédric; Huang, Yan
- Molecular Microbiology, Vol. 98, Issue 5
[20] Processing of X-ray diffraction data collected in oscillation mode
book, January 1997
- Otwinowski, Zbyszek; Minor, Wladek
- Macromolecular Crystallography Part A, 307-326
Stability of yeast iso-1-ferricytochrome c as a function of pH and temperature
journal, August 1994
- Cohen, David S.; Pielak, Gary J.
- Protein Science, Vol. 3, Issue 8
Binding protein-independent histidine permease mutants. Uncoupling of ATP hydrolysis from transmembrane signaling.
journal, September 1991
- Petronilli, V.; Ames, G. F.
- Journal of Biological Chemistry, Vol. 266, Issue 25
Leucine/isoleucine/valine-binding protein contracts upon binding of ligand
journal, August 1993
- Olah, G. A.; Trakhanov, S.; Trewhella, J.
- Journal of Biological Chemistry, Vol. 268, Issue 22
Dependence of maltose transport and chemotaxis on the amount of maltose-binding protein.
journal, August 1985
- Manson, M. D.; Boos, W.; Bassford, P. J.
- Journal of Biological Chemistry, Vol. 260, Issue 17
Works referencing / citing this record:
Nucleotide substrate binding characterization in human pancreatic-type ribonucleases
journal, August 2019
- Bafna, Khushboo; Narayanan, Chitra; Chennubhotla, S. Chakra
- PLOS ONE, Vol. 14, Issue 8
Nucleotide substrate binding characterization in human pancreatic-type ribonucleases
journal, August 2019
- Bafna, Khushboo; Narayanan, Chitra; Chennubhotla, S. Chakra
- PLOS ONE, Vol. 14, Issue 8