A novel signal transduction protein: Combination of solute binding and tandem PAS-like sensor domains in one polypeptide chain
Abstract
The tandem Per-Arnt-Sim (PAS) like sensors are commonly found in signal transduction proteins. The periplasmic solute binding protein (SBP) domains are found ubiquitously and are generally involved in solute transport. These domains are widely observed as parts of separate proteins but not within the same polypeptide chain. We report the structural and biochemical characterization of the extracellular ligand-binding receptor, Dret_0059 from Desulfohalobium retbaense DSM 5692, an organism isolated from the Retba salt lake in Senegal. The structure of Dret_0059 consists of a novel combination of SBP and TPAS sensor domains. The N-terminal region forms an SBP domain and the C-terminal region folds into a tandem PAS-like domain structure. A ketoleucine moiety is bound to the SBP, whereas a cytosine molecule is bound in the distal PAS domain of the TPAS. The differential scanning flourimetry studies in solution support the ligands observed in the crystal structure. There are only two other proteins with this structural architecture in the non-redundant sequence data base and we predict that they too bind the same substrates. There is significant interaction between the SBP and TPAS domains, and it is quite conceivable that the binding of one ligand will have an effect on the binding ofmore »
- Authors:
-
- Argonne National Lab. (ANL), Argonne, IL (United States)
- Argonne National Lab. (ANL), Argonne, IL (United States); Univ. of Chicago, Chicago, IL (United States)
- Publication Date:
- Research Org.:
- Argonne National Lab. (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- National Institutes of Health (NIH); National Institute of General Medical Sciences; USDOE
- OSTI Identifier:
- 1353039
- Grant/Contract Number:
- AC02-06CH11357
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Protein Science
- Additional Journal Information:
- Journal Volume: 26; Journal Issue: 4; Journal ID: ISSN 0961-8368
- Publisher:
- The Protein Society
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; KIC; Ketoleucine; cytosine; receptor; signal transduction; solute binding protein; tandem PAS-like sensor; ligand-binding protein; protein fold; structure
Citation Formats
Wu, R., Wilton, R., Cuff, M. E., Endres, M., Babnigg, G., Edirisinghe, J. N., Henry, C. S., Joachimiak, A., Schiffer, M., and Pokkuluri, P. R. A novel signal transduction protein: Combination of solute binding and tandem PAS-like sensor domains in one polypeptide chain. United States: N. p., 2017.
Web. doi:10.1002/pro.3134.
Wu, R., Wilton, R., Cuff, M. E., Endres, M., Babnigg, G., Edirisinghe, J. N., Henry, C. S., Joachimiak, A., Schiffer, M., & Pokkuluri, P. R. A novel signal transduction protein: Combination of solute binding and tandem PAS-like sensor domains in one polypeptide chain. United States. https://doi.org/10.1002/pro.3134
Wu, R., Wilton, R., Cuff, M. E., Endres, M., Babnigg, G., Edirisinghe, J. N., Henry, C. S., Joachimiak, A., Schiffer, M., and Pokkuluri, P. R. Tue .
"A novel signal transduction protein: Combination of solute binding and tandem PAS-like sensor domains in one polypeptide chain". United States. https://doi.org/10.1002/pro.3134. https://www.osti.gov/servlets/purl/1353039.
@article{osti_1353039,
title = {A novel signal transduction protein: Combination of solute binding and tandem PAS-like sensor domains in one polypeptide chain},
author = {Wu, R. and Wilton, R. and Cuff, M. E. and Endres, M. and Babnigg, G. and Edirisinghe, J. N. and Henry, C. S. and Joachimiak, A. and Schiffer, M. and Pokkuluri, P. R.},
abstractNote = {The tandem Per-Arnt-Sim (PAS) like sensors are commonly found in signal transduction proteins. The periplasmic solute binding protein (SBP) domains are found ubiquitously and are generally involved in solute transport. These domains are widely observed as parts of separate proteins but not within the same polypeptide chain. We report the structural and biochemical characterization of the extracellular ligand-binding receptor, Dret_0059 from Desulfohalobium retbaense DSM 5692, an organism isolated from the Retba salt lake in Senegal. The structure of Dret_0059 consists of a novel combination of SBP and TPAS sensor domains. The N-terminal region forms an SBP domain and the C-terminal region folds into a tandem PAS-like domain structure. A ketoleucine moiety is bound to the SBP, whereas a cytosine molecule is bound in the distal PAS domain of the TPAS. The differential scanning flourimetry studies in solution support the ligands observed in the crystal structure. There are only two other proteins with this structural architecture in the non-redundant sequence data base and we predict that they too bind the same substrates. There is significant interaction between the SBP and TPAS domains, and it is quite conceivable that the binding of one ligand will have an effect on the binding of the other. Our attempts to remove the ligands bound to the protein during expression were not successful, therefore, it is not clear what the relative affects are. The genomic context of this receptor does not contain any protein components expected for transport function, hence, we suggest that Dret_0059 is likely involved in signal transduction and not in solute transport.},
doi = {10.1002/pro.3134},
journal = {Protein Science},
number = 4,
volume = 26,
place = {United States},
year = {Tue Feb 07 00:00:00 EST 2017},
month = {Tue Feb 07 00:00:00 EST 2017}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 1 work
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
The venus flytrap of periplasmic binding proteins: An ancient protein module present in multiple drug receptors
journal, June 1999
- Felder, Christian B.; Graul, Richard C.; Lee, Alan Y.
- AAPS PharmSci, Vol. 1, Issue 2
Ligand-Free and -Bound Structures of the Binding Protein (LivJ) of the Escherichia coli ABC Leucine/Isoleucine/Valine Transport System: Trajectory and Dynamics of the Interdomain Rotation and Ligand Specificity †
journal, May 2005
- Trakhanov, Sergei; Vyas, Nand K.; Luecke, Hartmut
- Biochemistry, Vol. 44, Issue 17
Extracytoplasmic PAS-Like Domains Are Common in Signal Transduction Proteins
journal, December 2009
- Chang, C.; Tesar, C.; Gu, M.
- Journal of Bacteriology, Vol. 192, Issue 4
Structural characterization and modeling of the Borrelia burgdorferi hybrid histidine kinase Hk1 periplasmic sensor: A system for sensing small molecules associated with tick feeding
journal, October 2015
- Bauer, William J.; Luthra, Amit; Zhu, Guangyu
- Journal of Structural Biology, Vol. 192, Issue 1
Crystal structure of a histidine kinase sensor domain with similarity to periplasmic binding proteins
journal, October 2009
- Cheung, Jonah; Le-Khac, Matthew; Hendrickson, Wayne A.
- Proteins: Structure, Function, and Bioinformatics, Vol. 77, Issue 1
Characterization of Transport Proteins for Aromatic Compounds Derived from Lignin: Benzoate Derivative Binding Proteins
journal, November 2012
- Michalska, Karolina; Chang, Changsoo; Mack, Jamey C.
- Journal of Molecular Biology, Vol. 423, Issue 4
Experimental Strategies for Functional Annotation and Metabolism Discovery: Targeted Screening of Solute Binding Proteins and Unbiased Panning of Metabolomes
journal, January 2015
- Vetting, Matthew W.; Al-Obaidi, Nawar; Zhao, Suwen
- Biochemistry, Vol. 54, Issue 3
Condition-Dependent Transcriptome Reveals High-Level Regulatory Architecture in Bacillus subtilis
journal, March 2012
- Nicolas, P.; Mader, U.; Dervyn, E.
- Science, Vol. 335, Issue 6072
High-throughput generation, optimization and analysis of genome-scale metabolic models
journal, August 2010
- Henry, Christopher S.; DeJongh, Matthew; Best, Aaron A.
- Nature Biotechnology, Vol. 28, Issue 9
Dali server: conservation mapping in 3D
journal, May 2010
- Holm, Liisa; Rosenstr�m, P�ivi
- Nucleic Acids Research, Vol. 38, Issue suppl_2
HKL -3000: the integration of data reduction and structure solution – from diffraction images to an initial model in minutes
journal, July 2006
- Minor, Wladek; Cymborowski, Marcin; Otwinowski, Zbyszek
- Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 8
RegPrecise: a database of curated genomic inferences of transcriptional regulatory interactions in prokaryotes
journal, October 2009
- Novichkov, Pavel S.; Laikova, Olga N.; Novichkova, Elena S.
- Nucleic Acids Research, Vol. 38, Issue suppl_1
Complete genome sequence of Desulfohalobium retbaense type strain (HR100T)
journal, January 2010
- Spring, Stefan; Nolan, Matt; Lapidus, Alla
- Standards in Genomic Sciences, Vol. 2, Issue 1
The PAS fold: A redefinition of the PAS domain based upon structural prediction
journal, March 2004
- Hefti, Marco H.; Françoijs, Kees-Jan; de Vries, Sacco C.
- European Journal of Biochemistry, Vol. 271, Issue 6
Chemical screening methods to identify ligands that promote protein stability, protein crystallization, and structure determination
journal, October 2006
- Vedadi, M.; Niesen, F. H.; Allali-Hassani, A.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 43
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
Coot model-building tools for molecular graphics
journal, November 2004
- Emsley, Paul; Cowtan, Kevin
- Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
Culturable diversity of lithotrophic haloalkaliphilic sulfate-reducing bacteria in soda lakes and the description of Desulfonatronum thioautotrophicum sp. nov., Desulfonatronum thiosulfatophilum sp. nov., Desulfonatronovibrio thiodismutans sp. nov., and Desulfonatronovibrio magnus sp. nov.
journal, April 2011
- Sorokin, D. Y.; Tourova, T. P.; Kolganova, T. V.
- Extremophiles, Vol. 15, Issue 3
KEGG: Kyoto Encyclopedia of Genes and Genomes
journal, January 2000
- Kanehisa, Minoru; Goto, Susumu
- Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30
Nature of the protein universe
journal, June 2009
- Levitt, M.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 27
Thermofluor-based high-throughput stability optimization of proteins for structural studies
journal, October 2006
- Ericsson, Ulrika B.; Hallberg, B. Martin; DeTitta, George T.
- Analytical Biochemistry, Vol. 357, Issue 2
REFMAC 5 for the refinement of macromolecular crystal structures
journal, March 2011
- Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A.
- Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
The crystal structure of the tandem-PAS sensing domain of Campylobacter jejuni chemoreceptor Tlp1 suggests indirect mechanism of ligand recognition
journal, May 2016
- Machuca, Mayra A.; Liu, Yu C.; Beckham, Simone A.
- Journal of Structural Biology, Vol. 194, Issue 2
FFAS03: a server for profile-profile sequence alignments
journal, July 2005
- Jaroszewski, L.; Rychlewski, L.; Li, Z.
- Nucleic Acids Research, Vol. 33, Issue Web Server
Ligand-Induced Asymmetry in Histidine Sensor Kinase Complex Regulates Quorum Sensing
journal, September 2006
- Neiditch, Matthew B.; Federle, Michael J.; Pompeani, Audra J.
- Cell, Vol. 126, Issue 6
Functional Assignment of Solute-Binding Proteins of ABC Transporters Using a Fluorescence-Based Thermal Shift Assay †
journal, December 2008
- Giuliani, Sarah E.; Frank, Ashley M.; Collart, Frank R.
- Biochemistry, Vol. 47, Issue 52
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
Atomic structure and specificity of bacterial periplasmic receptors for active transport and chemotaxis: variation of common themes
journal, April 1996
- Quiocho, Florante A.; Ledvina, Polly S.
- Molecular Microbiology, Vol. 20, Issue 1
High-throughput protein purification and quality assessment for crystallization
journal, September 2011
- Kim, Youngchang; Babnigg, Gyorgy; Jedrzejczak, Robert
- Methods, Vol. 55, Issue 1
A structural classification of substrate-binding proteins
journal, April 2010
- Berntsson, Ronnie P. -A.; Smits, Sander H. J.; Schmitt, Lutz
- FEBS Letters, Vol. 584, Issue 12
DBTBS: a database of transcriptional regulation in Bacillus subtilis containing upstream intergenic conservation information
journal, October 2007
- Sierro, Nicolas; Makita, Yuko; de Hoon, Michiel
- Nucleic Acids Research, Vol. 36, Issue suppl_1
Structures and Solution Properties of Two Novel Periplasmic Sensor Domains with c-Type Heme from Chemotaxis Proteins of Geobacter sulfurreducens: Implications for Signal Transduction
journal, April 2008
- Pokkuluri, P. R.; Pessanha, M.; Londer, Y. Y.
- Journal of Molecular Biology, Vol. 377, Issue 5
The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability
journal, September 2007
- Niesen, Frank H.; Berglund, Helena; Vedadi, Masoud
- Nature Protocols, Vol. 2, Issue 9
Computing and Applying Atomic Regulons to Understand Gene Expression and Regulation
journal, November 2016
- Faria, José P.; Davis, James J.; Edirisinghe, Janaka N.
- Frontiers in Microbiology, Vol. 7
Structural Characterization of the Predominant Family of Histidine Kinase Sensor Domains
journal, July 2010
- Zhang, Zhen; Hendrickson, Wayne A.
- Journal of Molecular Biology, Vol. 400, Issue 3
Chemotaxis to Pyrimidines and Identification of a Cytosine Chemoreceptor in Pseudomonas putida
journal, February 2009
- Liu, X.; Wood, P. L.; Parales, J. V.
- Journal of Bacteriology, Vol. 191, Issue 9
Automation of protein purification for structural genomics
journal, March 2004
- Kim, Youngchang; Dementieva, Irina; Zhou, Min
- Journal of Structural and Functional Genomics, Vol. 5, Issue 1/2
Desulfonatronobacter acidivorans gen. nov., sp. nov. and Desulfobulbus alkaliphilus sp. nov., haloalkaliphilic heterotrophic sulfate-reducing bacteria from soda lakes
journal, October 2011
- Sorokin, D. Y.; Tourova, T. P.; Panteleeva, A. N.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 62, Issue Pt 9
Molecular mechanism of the Escherichia coli maltose transporter
journal, August 2013
- Chen, Jue
- Current Opinion in Structural Biology, Vol. 23, Issue 4
RegulonDB version 7.0: transcriptional regulation of Escherichia coli K-12 integrated within genetic sensory response units (Gensor Units)
journal, November 2010
- Gama-Castro, S.; Salgado, H.; Peralta-Gil, M.
- Nucleic Acids Research, Vol. 39, Issue Database
The RAST Server: Rapid Annotations using Subsystems Technology
journal, January 2008
- Aziz, Ramy K.; Bartels, Daniela; Best, Aaron A.
- BMC Genomics, Vol. 9, Issue 1, Article No. 75
Insight into the sporulation phosphorelay: Crystal structure of the sensor domain of Bacillus subtilis histidine kinase, KinD : The Crystal Structure of the KinD Sensor Domain
journal, March 2013
- Wu, R.; Gu, M.; Wilton, R.
- Protein Science, Vol. 22, Issue 5