Transcriptional regulation, metal binding properties and structure of Pden1597, an unusual zinc transport protein from Paracoccus denitrificans
Abstract
Here, ATP-binding cassette (ABC) transporters of the cluster 9 family are ubiquitous among bacteria and essential for acquiring Zn2+ and Mn2+ from the environment or, in the case of pathogens, from the host. These rely on a substrate-binding protein (SBP) to coordinate the relevant metal with high affinity and specificity and subsequently release it to a membrane permease for translocation into the cytoplasm. Although a number of cluster 9 SBP structures have been determined, the structural attributes conferring Zn2+ or Mn2+ specificity remain ambiguous. Here we describe the gene expression profile, in vitro metal binding properties, and crystal structure of a new cluster 9 SBP from Paracoccus denitrificans we have called AztC. Although all of our results strongly indicate Zn2+ over Mn2+ specificity, the Zn2+ ion is coordinated by a conserved Asp residue only observed to date as a metal ligand in Mn2+-specific SBPs. The unusual sequence properties of this protein are shared among close homologues, including members from the human pathogens Klebsiella pneumonia and Enterobacter aerogenes, and would seem to suggest a subclass of Zn2+-specific transporters among the cluster 9 family. In any case, the unusual coordination environment of AztC expands the already considerable range of those available tomore »
- Authors:
-
- New Mexico State Univ., Las Cruces, NM (United States)
- Publication Date:
- Research Org.:
- Univ. of California, Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1347699
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Biological Chemistry
- Additional Journal Information:
- Journal Volume: 290; Journal Issue: 19; 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; ABC transporter; manganese; metal homeostasis; metalloprotein; transcription regulation; zinc
Citation Formats
Handali, Melody, Neupane, Durga P., Roychowdhury, Hridindu, and Yukl, Erik T. Transcriptional regulation, metal binding properties and structure of Pden1597, an unusual zinc transport protein from Paracoccus denitrificans. United States: N. p., 2015.
Web. doi:10.1074/jbc.m115.645853.
Handali, Melody, Neupane, Durga P., Roychowdhury, Hridindu, & Yukl, Erik T. Transcriptional regulation, metal binding properties and structure of Pden1597, an unusual zinc transport protein from Paracoccus denitrificans. United States. https://doi.org/10.1074/jbc.m115.645853
Handali, Melody, Neupane, Durga P., Roychowdhury, Hridindu, and Yukl, Erik T. Wed .
"Transcriptional regulation, metal binding properties and structure of Pden1597, an unusual zinc transport protein from Paracoccus denitrificans". United States. https://doi.org/10.1074/jbc.m115.645853. https://www.osti.gov/servlets/purl/1347699.
@article{osti_1347699,
title = {Transcriptional regulation, metal binding properties and structure of Pden1597, an unusual zinc transport protein from Paracoccus denitrificans},
author = {Handali, Melody and Neupane, Durga P. and Roychowdhury, Hridindu and Yukl, Erik T.},
abstractNote = {Here, ATP-binding cassette (ABC) transporters of the cluster 9 family are ubiquitous among bacteria and essential for acquiring Zn2+ and Mn2+ from the environment or, in the case of pathogens, from the host. These rely on a substrate-binding protein (SBP) to coordinate the relevant metal with high affinity and specificity and subsequently release it to a membrane permease for translocation into the cytoplasm. Although a number of cluster 9 SBP structures have been determined, the structural attributes conferring Zn2+ or Mn2+ specificity remain ambiguous. Here we describe the gene expression profile, in vitro metal binding properties, and crystal structure of a new cluster 9 SBP from Paracoccus denitrificans we have called AztC. Although all of our results strongly indicate Zn2+ over Mn2+ specificity, the Zn2+ ion is coordinated by a conserved Asp residue only observed to date as a metal ligand in Mn2+-specific SBPs. The unusual sequence properties of this protein are shared among close homologues, including members from the human pathogens Klebsiella pneumonia and Enterobacter aerogenes, and would seem to suggest a subclass of Zn2+-specific transporters among the cluster 9 family. In any case, the unusual coordination environment of AztC expands the already considerable range of those available to Zn2+-specific SBPs and highlights the presence of a His-rich loop as the most reliable indicator of Zn2+ specificity.},
doi = {10.1074/jbc.m115.645853},
journal = {Journal of Biological Chemistry},
number = 19,
volume = 290,
place = {United States},
year = {Wed Mar 18 00:00:00 EDT 2015},
month = {Wed Mar 18 00:00:00 EDT 2015}
}
Web of Science
Works referenced in this record:
Apo, Zn2+-bound and Mn2+-bound structures reveal ligand-binding properties of SitA from the pathogen Staphylococcus pseudintermedius
journal, November 2014
- Abate, Francesca; Malito, Enrico; Cozzi, Roberta
- Bioscience Reports, Vol. 34, Issue 6
High-Affinity Zn2+ Uptake System ZnuABC Is Required for Bacterial Zinc Homeostasis in Intracellular Environments and Contributes to the Virulence of Salmonella enterica
journal, October 2007
- Ammendola, Serena; Pasquali, Paolo; Pistoia, Claudia
- Infection and Immunity, Vol. 75, Issue 12
Metal Binding Studies and EPR Spectroscopy of the Manganese Transport Regulator MntR †
journal, December 2006
- Golynskiy, Misha V.; Gunderson, William A.; Hendrich, Michael P.
- Biochemistry, Vol. 45, Issue 51
MntABC and MntH Contribute to Systemic Staphylococcus aureus Infection by Competing with Calprotectin for Nutrient Manganese
journal, July 2013
- Kehl-Fie, Thomas E.; Zhang, Yaofang; Moore, Jessica L.
- Infection and Immunity, Vol. 81, Issue 9
The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague
journal, April 1999
- Bearden, Scott W.; Perry, Robert D.
- Molecular Microbiology, Vol. 32, Issue 2
Structure and metal binding properties of ZnuA, a periplasmic zinc transporter from Escherichia coli
journal, November 2007
- Yatsunyk, Liliya A.; Easton, J. Allen; Kim, Lydia R.
- JBIC Journal of Biological Inorganic Chemistry, Vol. 13, Issue 2
Conserved Aspartic Acid 714 in Transmembrane Segment 8 of the ZntA Subgroup of P 1B -Type ATPases Is a Metal-Binding Residue †
journal, May 2006
- Dutta, Sabari J.; Liu, Junbo; Hou, Zhanjun
- Biochemistry, Vol. 45, Issue 18
Arginine 116 stabilizes the entrance to the metal ion-binding site of the MntC protein
journal, February 2013
- Kanteev, Margarita; Adir, Noam
- Acta Crystallographica Section F Structural Biology and Crystallization Communications, Vol. 69, Issue 3
SignalP 4.0: discriminating signal peptides from transmembrane regions
journal, September 2011
- Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar
- Nature Methods, Vol. 8, Issue 10
Imperfect coordination chemistry facilitates metal ion release in the Psa permease
journal, November 2013
- Couñago, Rafael M.; Ween, Miranda P.; Begg, Stephanie L.
- Nature Chemical Biology, Vol. 10, Issue 1
Crystal Structure and Metal Binding Properties of the Lipoprotein MtsA, Responsible for Iron Transport in Streptococcus pyogenes
journal, July 2009
- Sun, Xuesong; Baker, Heather M.; Ge, Ruiguang
- Biochemistry, Vol. 48, Issue 26
Structural Analysis of ABC-family Periplasmic Zinc Binding Protein Provides New Insights Into Mechanism of Ligand Uptake and Release
journal, April 2007
- Chandra, Beeram Ravi; Yogavel, M.; Sharma, Amit
- Journal of Molecular Biology, Vol. 367, Issue 4
Possible Regulatory Role for the Histidine-Rich Loop in the Zinc Transport Protein, ZnuA † , ‡
journal, July 2007
- Wei, Baoxian; Randich, Amelia M.; Bhattacharyya-Pakrasi, Maitrayee
- Biochemistry, Vol. 46, Issue 30
Insight into the Interaction of Metal Ions with TroA from Streptococcus suis
journal, May 2011
- Zheng, Beiwen; Zhang, Qiangmin; Gao, Jia
- PLoS ONE, Vol. 6, Issue 5
Structural Determinants of Metal Specificity in the Zinc Transport Protein ZnuA from Synechocystis 6803
journal, November 2003
- Banerjee, Soojay; Wei, Baoxian; Bhattacharyya-Pakrasi, Maitrayee
- Journal of Molecular Biology, Vol. 333, Issue 5
TroA of Streptococcus suis Is Required for Manganese Acquisition and Full Virulence
journal, July 2011
- Schreur, P. J. W.; Rebel, J. M. J.; Smits, M. A.
- Journal of Bacteriology, Vol. 193, Issue 19
Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria.
journal, January 1993
- Tam, R.; Saier, M. H.
- Microbiological Reviews, Vol. 57, Issue 2
Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria
journal, June 1993
- Tam, R.; Saier, M. H.
- Microbiological Reviews, Vol. 57, Issue 2
In vivo characterization of the psa genes from Streptococcus pneumoniae in multiple models of infection
journal, May 2002
- Marra, Andrea; Lawson, Stacey; Asundi, Jyoti S.
- Microbiology, Vol. 148, Issue 5
In-gel digestion for mass spectrometric characterization of proteins and proteomes
journal, December 2006
- Shevchenko, Andrej; Tomas, Henrik; Havli, Jan
- Nature Protocols, Vol. 1, Issue 6
Use of the amicyanin signal sequence for efficient periplasmic expression in E. coli of a human antibody light chain variable domain
journal, April 2015
- Dow, Brian A.; Tatulian, Suren A.; Davidson, Victor L.
- Protein Expression and Purification, Vol. 108
Copper control of bacterial nitrous oxide emission and its impact on vitamin B12-dependent metabolism
journal, November 2013
- Sullivan, M. J.; Gates, A. J.; Appia-Ayme, C.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 49
Metals in proteins: correlation between the metal-ion type, coordination number and the amino-acid residues involved in the coordination
journal, February 2008
- Dokmanić, Ivan; Šikić, Mile; Tomić, Sanja
- Acta Crystallographica Section D Biological Crystallography, Vol. 64, Issue 3
The general transition metal (Tro) and Zn 2+ (Znu) transporters in Treponema pallidum : analysis of metal specificities and expression profiles
journal, July 2007
- Desrosiers, Daniel C.; Sun, Yong Cheng; Zaidi, Akbar A.
- Molecular Microbiology, Vol. 65, Issue 1
Metal-Binding Affinity of the Transmembrane Site in ZntA: Implications for Metal Selectivity †
journal, January 2006
- Liu, Junbo; Dutta, Sabari J.; Stemmler, Ann J.
- Biochemistry, Vol. 45, Issue 3
Metal-Binding Characteristics of the Amino-Terminal Domain of ZntA: Binding of Lead Is Different Compared to Cadmium and Zinc †
journal, April 2005
- Liu, Junbo; Stemmler, Ann J.; Fatima, Juhi
- Biochemistry, Vol. 44, Issue 13
The adc locus, which affects competence for genetic transformation in Streptococcus pneumoniae, encodes an ABC transporter with a putative lipoprotein homologous to a family of streptococcal adhesins
journal, February 1997
- Dintilhac, A.; Claverys, J. -P.
- Research in Microbiology, Vol. 148, Issue 2
The Phenix software for automated determination of macromolecular structures
journal, September 2011
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Methods, Vol. 55, Issue 1
A Molecular Mechanism for Bacterial Susceptibility to Zinc
journal, November 2011
- McDevitt, Christopher A.; Ogunniyi, Abiodun D.; Valkov, Eugene
- PLoS Pathogens, Vol. 7, Issue 11
Iron, copper, zinc, and manganese transport and regulation in pathogenic Enterobacteria: correlations between strains, site of infection and the relative importance of the different metal transport systems for virulence
journal, January 2013
- Porcheron, Gaëlle; Garénaux, Amélie; Proulx, Julie
- Frontiers in Cellular and Infection Microbiology, Vol. 3
The crystal structure of pneumococcal surface antigen PsaA reveals a metal-binding site and a novel structure for a putative ABC-type binding protein
journal, December 1998
- Lawrence, Michael C.; Pilling, Patricia A.; Epa, V. Chandana
- Structure, Vol. 6, Issue 12
MauG, a Novel Diheme Protein Required for Tryptophan Tryptophylquinone Biogenesis †
journal, June 2003
- Wang, Yongting; Graichen, M. Elizabeth; Liu, Aimin
- Biochemistry, Vol. 42, Issue 24
Three-Dimensional Structure and Biophysical Characterization of Staphylococcus aureus Cell Surface Antigen–Manganese Transporter MntC
journal, September 2013
- Gribenko, Alexey; Mosyak, Lidia; Ghosh, Sharmistha
- Journal of Molecular Biology, Vol. 425, Issue 18
Femtomolar Sensitivity of Metalloregulatory Proteins Controlling Zinc Homeostasis
journal, June 2001
- Outten, C. E.
- Science, Vol. 292, Issue 5526
The solute-binding component of a putative Mn(II) ABC transporter (MntA) is a novel Bacillus anthracis virulence determinant: Role of MntA in anthrax pathogenesis
journal, September 2005
- Gat, Orit; Mendelson, Itai; Chitlaru, Theodor
- Molecular Microbiology, Vol. 58, Issue 2
Spectroscopic Determination of Tryptophan and Tyrosine in Proteins *
journal, July 1967
- Edelhoch, Harold
- Biochemistry, Vol. 6, Issue 7
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 MntC Crystal Structure Suggests that Import of Mn2+ in Cyanobacteria is Redox Controlled
journal, May 2005
- Rukhman, Valeria; Anati, Rina; Melamed-Frank, Meira
- Journal of Molecular Biology, Vol. 348, Issue 4
Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens
journal, February 2013
- Damo, S. M.; Kehl-Fie, T. E.; Sugitani, N.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 10
The Zinc-Responsive Regulator Zur Controls a Zinc Uptake System and Some Ribosomal Proteins in Streptomyces coelicolor A3(2)
journal, April 2007
- Shin, Jung-Ho; Oh, So-Young; Kim, Soon-Jong
- Journal of Bacteriology, Vol. 189, Issue 11
Structural changes in a cryo-cooled protein crystal owing to radiation damage
journal, March 2000
- Burmeister, Wilhelm Pascal
- Acta Crystallographica Section D Biological Crystallography, Vol. 56, Issue 3
A new family of high-affinity ABC manganese and zinc permeases
journal, April 2001
- Claverys, Jean-Pierre
- Research in Microbiology, Vol. 152, Issue 3-4
Calprotectin-Mediated Zinc Chelation as a Biostatic Mechanism in Host Defence
journal, November 1995
- Clohessy, P. A.; Golden, B. E.
- Scandinavian Journal of Immunology, Vol. 42, Issue 5
The Crystal Structure of Zn(II)-Free Treponema pallidum TroA, a Periplasmic Metal-Binding Protein, Reveals a Closed Conformation
journal, April 2002
- Lee, Yong-Hwan; Dorwart, Michael R.; Hazlett, Karsten R. O.
- Journal of Bacteriology, Vol. 184, Issue 8
Bacterial ATP-driven transporters of transition metals: physiological roles, mechanisms of action, and roles in bacterial virulence
journal, January 2011
- Klein, Joshua S.; Lewinson, Oded
- Metallomics, Vol. 3, Issue 11
The X-ray Structure of the Zinc Transporter ZnuA from Salmonella enterica Discloses a Unique Triad of Zinc-Coordinating Histidines
journal, June 2011
- Ilari, Andrea; Alaleona, Flaminia; Petrarca, Patrizia
- Journal of Molecular Biology, Vol. 409, Issue 4
Crystal Structure of the Zinc-binding Transport Protein ZnuA from Escherichia coli Reveals an Unexpected Variation in Metal Coordination
journal, May 2007
- Li, Hua; Jogl, Gerwald
- Journal of Molecular Biology, Vol. 368, Issue 5
Program DYNAFIT for the Analysis of Enzyme Kinetic Data: Application to HIV Proteinase
journal, June 1996
- Kuzmič, Petr
- Analytical Biochemistry, Vol. 237, Issue 2
Metal Ion Binding and Coordination Geometry for Wild Type and Mutants of Metallo-β-lactamase from Bacillus cereus 569/H/9 (BcII) : A COMBINED THERMODYNAMIC, KINETIC, AND SPECTROSCOPIC APPROACH
journal, September 2001
- de Seny, Dominique; Heinz, Uwe; Wommer, Sandra
- Journal of Biological Chemistry, Vol. 276, Issue 48
Severe Zinc Depletion of Escherichia coli: ROLES FOR HIGH AFFINITY ZINC BINDING BY ZinT, ZINC TRANSPORT AND ZINC-INDEPENDENT PROTEINS
journal, April 2009
- Graham, Alison I.; Hunt, Stuart; Stokes, Sarah L.
- Journal of Biological Chemistry, Vol. 284, Issue 27
A deliberate approach to screening for initial crystallization conditions of biological macromolecules
journal, April 2003
- Luft, Joseph R.; Collins, Robert J.; Fehrman, Nancy A.
- Journal of Structural Biology, Vol. 142, Issue 1
Phaser crystallographic software
journal, July 2007
- McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D.
- Journal of Applied Crystallography, Vol. 40, Issue 4
Metal ions in biological catalysis: from enzyme databases to general principles
journal, July 2008
- Andreini, Claudia; Bertini, Ivano; Cavallaro, Gabriele
- JBIC Journal of Biological Inorganic Chemistry, Vol. 13, Issue 8
Works referencing / citing this record:
Crystal structures of AztD provide mechanistic insights into direct zinc transfer between proteins
journal, August 2019
- Neupane, Durga Prasad; Fullam, Stephanie Hope; Chacón, Kelly Natalia
- Communications Biology, Vol. 2, Issue 1
Crystal structures of AztD provide mechanistic insights into direct zinc transfer between proteins
journal, August 2019
- Neupane, Durga Prasad; Fullam, Stephanie Hope; Chacón, Kelly Natalia
- Communications Biology, Vol. 2, Issue 1
Two ABC Transporters and a Periplasmic Metallochaperone Participate in Zinc Acquisition in Paracoccus denitrificans
journal, October 2018
- Neupane, Durga P.; Kumar, Santosh; Yukl, Erik T.
- Biochemistry, Vol. 58, Issue 2
In silico Study of Iron, Zinc and Copper Binding Proteins of Pseudomonas syringae pv. lapsa: Emphasis on Secreted Metalloproteins
journal, August 2018
- Sharma, Ankita; Sharma, Dixit; Verma, Shailender K.
- Frontiers in Microbiology, Vol. 9