Skip to main content
OSTI.GOVU.S. Department of Energy Office of Scientific and Technical Information
U.S. Department of Energy
Office of Scientific and Technical Information
 

Molecular details of ligand selectivity determinants in a promiscuous β-glucan periplasmic binding protein

Journal Article · · BMC Structural Biology (Online)
 [1];  [2];  [2];  [2];  [2];  [2]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Neutron Sciences Directorate; Middle Tennessee State Univ., Murfreesboro, TN (United States). Dept. of Chemistry; Shiv Nadar University (India); DOE/OSTI
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Neutron Sciences Directorate
+ Show Author Affiliations
Background: Members of the periplasmic binding protein (PBP) superfamily utilize a highly conserved inter-domain ligand binding site that adapts to specifically bind a chemically diverse range of ligands. This paradigm of PBP ligand binding specificity was recently altered when the structure of the Thermotoga maritima cellobiose-binding protein (tmCBP) was solved. The tmCBP binding site is bipartite, comprising a canonical solvent-excluded region (subsite one), adjacent to a solvent-filled cavity (subsite two) where specific and semi-specific ligand recognition occur, respectively. Results: A molecular level understanding of binding pocket adaptation mechanisms that simultaneously allow both ligand specificity at subsite one and promiscuity at subsite two has potentially important implications in ligand binding and drug design studies. We sought to investigate the determinants of ligand binding selectivity in tmCBP through biophysical characterization of tmCBP in the presence of varying β-glucan oligosaccharides. Crystal structures show that whilst the amino acids that comprise both the tmCBP subsite one and subsite two binding sites remain fixed in conformation regardless of which ligands are present, the rich hydrogen bonding potential of water molecules may facilitate the ordering and the plasticity of this unique PBP binding site. Conclusions: The identification of the roles these water molecules play in ligand recognition suggests potential mechanisms that can be utilized to adapt a single ligand binding site to recognize multiple distinct ligands.
Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Spallation Neutron Source (SNS)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
AC05-00OR22725
OSTI ID:
1626545
Journal Information:
BMC Structural Biology (Online), Journal Name: BMC Structural Biology (Online) Journal Issue: 1 Vol. 13; ISSN 1472-6807
Publisher:
BioMed CentralCopyright Statement
Country of Publication:
United States
Language:
English

References (63)

Stability of yeast iso-1-ferricytochrome c as a function of pH and temperature journal August 1994
Conformational Changes of Three Periplasmic Receptors for Bacterial Chemotaxis and Transport: The Maltose-, Glucose/Galactose- and Ribose-binding Proteins. journal November 1996
The structure of glutamine-binding protein complexed with glutamine at 1.94 Å resolution: comparisons with other amino acid binding proteins journal April 1998
Multiple open forms of ribose-binding protein trace the path of its conformational change journal June 1998
Domain dislocation: a change of core structure in periplasmic binding proteins in their evolutionary history journal February 1999
Structure of d -allose binding protein from Escherichia coli bound to d -allose at 1.8 Å resolution 1 1Edited by A. R. Fersht journal March 1999
A structural classification of substrate-binding proteins journal April 2010
Structural Adaptations that Modulate Monosaccharide, Disaccharide, and Trisaccharide Specificities in Periplasmic Maltose-Binding Proteins journal May 2009
Structure of the Escherichia coli Phosphonate Binding Protein PhnD and Rationally Optimized Phosphonate Biosensors journal December 2011
Regulation of LuxPQ Receptor Activity by the Quorum-Sensing Signal Autoinducer-2 journal May 2005
Periplasmic binding proteins: a versatile superfamily for protein engineering journal August 2004
Classification of a Haemophilus influenzae ABC Transporter HI1470/71 through Its Cognate Molybdate Periplasmic Binding Protein, MolA journal November 2011
Determination of Domain Structure of Proteins from X-Ray Solution Scattering journal June 2001
Identification of the ribose binding protein as the receptor for ribose chemotaxis in Salmonella typhimurium journal October 1974
Stimulation of the Maltose Transporter ATPase by Unliganded Maltose Binding Protein journal August 2009
Crystal Structure of Thiaminase-I from Bacillus t hiaminolyticus at 2.0 Å Resolution † , ‡ journal November 1998
Structure of Haemophilus influenzae Fe+3-binding protein reveals convergent evolution within a superfamily journal November 1997
Mapping the Sinorhizobium meliloti 1021 solute-binding protein-dependent transportome journal November 2006
Slow protein evolutionary rates are dictated by surface-core association journal June 2011
Crystal Structure of PotD, the Primary Receptor of the Polyamine Transport System in Escherichia coli journal April 1996
Crystal Structures of the BtuF Periplasmic-binding Protein for Vitamin B12 Suggest a Functionally Important Reduction in Protein Mobility upon Ligand Binding journal December 2002
Insights into the Conformational Equilibria of Maltose-binding Protein by Analysis of High Affinity Mutants journal June 2003
X-ray Structures of the Leucine-binding Protein Illustrate Conformational Changes and the Basis of Ligand Specificity journal December 2003
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
MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes journal July 2004
Highly thermostable endo-1,3-β -glucanase (laminarinase) Lam A from Thermotoga neapolitana: nucleotide sequence of the gene and characterization of the recombinant gene product journal May 1997
Determination of the regularization parameter in indirect-transform methods using perceptual criteria journal August 1992
Coot model-building tools for molecular graphics journal November 2004
The CCP4 suite programs for protein crystallography journal September 1994
Conformational changes of glucose/galactose-binding protein illuminated by open, unliganded, and ultra-high-resolution ligand-bound structures journal June 2007
The tripartite ATP-independent periplasmic (TRAP) transporters of bacteria and archaea journal August 2001
Crystal structure of lac repressor core tetramer and its implications for DNA looping journal June 1995
Several Archaeal Homologs of Putative Oligopeptide-Binding Proteins Encoded by Thermotoga maritima Bind Sugars journal February 2006
Importance of a Hydrophobic Pocket for Peptide Binding in Lactococcal OppA journal June 2011
Molecular cloning and characterization of genes required for ribose transport and utilization in Escherichia coli K-12. journal January 1984
An Expression-Driven Approach to the Prediction of Carbohydrate Transport and Utilization Regulons in the Hyperthermophilic Bacterium Thermotoga maritima journal November 2005
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
Ligand-induced conformational changes in a thermophilic ribose-binding protein journal January 2008
PHENIX: a comprehensive Python-based system for macromolecular structure solution. text January 2010
Structural basis for a ribofuranosyl binding protein: Insights into the furanose specific transport: Insights into the Furanose Specific Transport journal February 2011
Determination of Domain Structure of Proteins from X-Ray Solution Scattering journal June 2001
Active transport of maltose in Escherichia coli K12. Role of the periplasmic maltose-binding protein and evidence for a substrate recognition site in the cytoplasmic membrane. journal May 1982
[20] Processing of X-ray diffraction data collected in oscillation mode book January 1997
Manipulation of ligand binding affinity by exploitation of conformational coupling journal September 2001
The energetic cost of domain reorientation in maltose-binding protein as studied by NMR and fluorescence spectroscopy journal October 2003
Structural Analysis of Semi-specific Oligosaccharide Recognition by a Cellulose-binding Protein of Thermotoga maritima Reveals Adaptations for Functional Diversification of the Oligopeptide Periplasmic Binding Protein Fold journal November 2009
Hinge-bending Motion of d-Allose-binding Protein from Escherichia coli : THREE OPEN CONFORMATIONS journal February 2002
Crystal Structures of the BtuF Periplasmic-binding Protein for Vitamin B12 Suggest a Functionally Important Reduction in Protein Mobility upon Ligand Binding journal December 2002
Insights into the Conformational Equilibria of Maltose-binding Protein by Analysis of High Affinity Mutants journal June 2003
X-ray Structures of the Leucine-binding Protein Illustrate Conformational Changes and the Basis of Ligand Specificity journal December 2003
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
The Protein Data Bank journal January 2000
LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions journal January 1995
The extended Q -range small-angle neutron scattering diffractometer at the SNS journal July 2010
Absolute calibration of small-angle neutron scattering data journal February 1987
Determination of the regularization parameter in indirect-transform methods using perceptual criteria journal August 1992
Coot model-building tools for molecular graphics journal November 2004
PHENIX: a comprehensive Python-based system for macromolecular structure solution journal January 2010
The CCP4 suite programs for protein crystallography journal September 1994
Tyr702 Is an Important Determinant of Agonist Binding and Domain Closure of the Ligand-Binding Core of GluR2 journal December 2004
Several Archaeal Homologs of Putative Oligopeptide-Binding Proteins Encoded by Thermotoga maritima Bind Sugars journal February 2006
Importance of a Hydrophobic Pocket for Peptide Binding in Lactococcal OppA journal June 2011
An Expression-Driven Approach to the Prediction of Carbohydrate Transport and Utilization Regulons in the Hyperthermophilic Bacterium Thermotoga maritima journal November 2005

Similar Records

Related Subjects

71 CLASSICAL AND QUANTUM MECHANICS
GENERAL PHYSICS
72 PHYSICS OF ELEMENTARY PARTICLES AND FIELDS
ABC transport
Biophysics
Carbohydrate recognition
Laminarin
Ligand specificity
Periplasmic binding protein