Molecular characterization of the interaction of sialic acid with the periplasmic binding protein from Haemophilus ducreyi
Abstract
The primary role of bacterial periplasmic binding proteins is sequestration of essential metabolites present at a low concentration in the periplasm and making them available for active transporters that transfer these ligands into the bacterial cell. The periplasmic binding proteins (SiaPs) from the tripartite ATP-independent periplasmic (TRAP) transport system that transports mammalian host–derived sialic acids have been well studied from different pathogenic bacteria, including Haemophilus influenzae, Fusobacterium nucleatum, Pasteurella multocida, and Vibrio cholerae. SiaPs bind the sialic acid N-acetylneuraminic acid (Neu5Ac) with nanomolar affinity by forming electrostatic and hydrogen-bonding interactions. Here, we report the crystal structure of a periplasmic binding protein (SatA) of the ATP-binding cassette (ABC) transport system from the pathogenic bacterium Haemophilus ducreyi. The structure of Hd-SatA in the native form and sialic acid–bound forms (with Neu5Ac and N-glycolylneuraminic acid (Neu5Gc)), determined to 2.2, 1.5, and 2.5 Å resolutions, respectively, revealed a ligand-binding site that is very different from those of the SiaPs of the TRAP transport system. A structural comparison along with thermodynamic studies suggested that similar affinities are achieved in the two classes of proteins through distinct mechanisms, one enthalpically driven and the other entropically driven. In summary, our structural and thermodynamic characterization of Hd-SatA revealsmore »
- Authors:
-
- Inst. for Stem Cell Biology and Regenerative Medicine, Bangalore (India); Univ. of Trans-Disciplinary Health Sciences and Technology (TDU), Bangalore (India)
- Univ. of Iowa, Iowa City, IA (United States)
- Inst. for Stem Cell Biology and Regenerative Medicine, Bangalore (India)
- The Ohio State Univ., Columbus, OH (United States)
- Publication Date:
- Research Org.:
- Argonne National Lab. (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1545842
- Resource Type:
- Journal Article: Accepted Manuscript
- Journal Name:
- Journal of Biological Chemistry
- Additional Journal Information:
- Journal Volume: 293; Journal Issue: 52; Journal ID: ISSN 0021-9258
- Publisher:
- American Society for Biochemistry and Molecular Biology
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; crystal structure; isothermal titration calorimetry (ITC); ABC transporter; energetics; sugar transport; enthalpy entropy; nutrient sequestration; sialic acid; virulence; Haemophilus ducreyi; periplasmic binding protein
Citation Formats
Gangi Setty, Thanuja, Mowers, Jonathan C., Hobbs, Aaron G., Maiya, Shubha P., Syed, Sanaa, Munson, Robert S., Apicella, Michael A., and Subramanian, Ramaswamy. Molecular characterization of the interaction of sialic acid with the periplasmic binding protein from Haemophilus ducreyi. United States: N. p., 2018.
Web. doi:10.1074/jbc.RA118.005151.
Gangi Setty, Thanuja, Mowers, Jonathan C., Hobbs, Aaron G., Maiya, Shubha P., Syed, Sanaa, Munson, Robert S., Apicella, Michael A., & Subramanian, Ramaswamy. Molecular characterization of the interaction of sialic acid with the periplasmic binding protein from Haemophilus ducreyi. United States. https://doi.org/10.1074/jbc.RA118.005151
Gangi Setty, Thanuja, Mowers, Jonathan C., Hobbs, Aaron G., Maiya, Shubha P., Syed, Sanaa, Munson, Robert S., Apicella, Michael A., and Subramanian, Ramaswamy. 2018.
"Molecular characterization of the interaction of sialic acid with the periplasmic binding protein from Haemophilus ducreyi". United States. https://doi.org/10.1074/jbc.RA118.005151. https://www.osti.gov/servlets/purl/1545842.
@article{osti_1545842,
title = {Molecular characterization of the interaction of sialic acid with the periplasmic binding protein from Haemophilus ducreyi},
author = {Gangi Setty, Thanuja and Mowers, Jonathan C. and Hobbs, Aaron G. and Maiya, Shubha P. and Syed, Sanaa and Munson, Robert S. and Apicella, Michael A. and Subramanian, Ramaswamy},
abstractNote = {The primary role of bacterial periplasmic binding proteins is sequestration of essential metabolites present at a low concentration in the periplasm and making them available for active transporters that transfer these ligands into the bacterial cell. The periplasmic binding proteins (SiaPs) from the tripartite ATP-independent periplasmic (TRAP) transport system that transports mammalian host–derived sialic acids have been well studied from different pathogenic bacteria, including Haemophilus influenzae, Fusobacterium nucleatum, Pasteurella multocida, and Vibrio cholerae. SiaPs bind the sialic acid N-acetylneuraminic acid (Neu5Ac) with nanomolar affinity by forming electrostatic and hydrogen-bonding interactions. Here, we report the crystal structure of a periplasmic binding protein (SatA) of the ATP-binding cassette (ABC) transport system from the pathogenic bacterium Haemophilus ducreyi. The structure of Hd-SatA in the native form and sialic acid–bound forms (with Neu5Ac and N-glycolylneuraminic acid (Neu5Gc)), determined to 2.2, 1.5, and 2.5 Å resolutions, respectively, revealed a ligand-binding site that is very different from those of the SiaPs of the TRAP transport system. A structural comparison along with thermodynamic studies suggested that similar affinities are achieved in the two classes of proteins through distinct mechanisms, one enthalpically driven and the other entropically driven. In summary, our structural and thermodynamic characterization of Hd-SatA reveals that it binds sialic acids with nanomolar affinity and that this binding is an entropically driven process. This information is important for future structure-based drug design against this pathogen and related bacteria.},
doi = {10.1074/jbc.RA118.005151},
url = {https://www.osti.gov/biblio/1545842},
journal = {Journal of Biological Chemistry},
issn = {0021-9258},
number = 52,
volume = 293,
place = {United States},
year = {Fri Oct 12 00:00:00 EDT 2018},
month = {Fri Oct 12 00:00:00 EDT 2018}
}
Web of Science
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