Water molecules mediate zinc mobility in the bacterial zinc diffusion channel ZIPB
Abstract
Regulated ion diffusion across biological membranes is vital for cell function. In a nanoscale ion channel, the active role of discrete water molecules in modulating hydrodynamic behaviors of individual ions is poorly understood because of the technical challenge of tracking water molecules through the channel. Here we report the results of a hydroxyl radical footprinting analysis of the zinc-selective channel ZIPB from the Gram-negative bacterium, Bordetella bronchiseptica Irradiating ZIPB by microsecond X-ray pulses activated water molecules to form covalent hydroxyl radical adducts at nearby residues, which were identified by bottom-up proteomics to detect residues that interact either with zinc or water in response to zinc binding. We found a series of residues exhibiting reciprocal changes in water accessibility attributed to alternating zinc and water binding. Mapping these residues to the previously reported crystal structure of ZIPB, we identified a water-reactive pathway that superimposed on a zinc translocation pathway consisting of two binuclear metal centers and an interim zinc-binding site. The cotranslocation of zinc and water suggested that pore-lining residues undergo a mode switch between zinc coordination and water binding to confer zinc mobility. The unprecedented details of water-mediated zinc transport identified here highlight an essential role of solvated waters inmore »
- Authors:
-
[2]
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Johns Hopkins Univ., Baltimore, MD (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1582337
- Grant/Contract Number:
- AC02-05CH11231; 5R01DK108599
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Biological Chemistry
- Additional Journal Information:
- Journal Volume: 294; Journal Issue: 36; Journal ID: ISSN 0021-9258
- Publisher:
- American Society for Biochemistry and Molecular Biology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Gupta, Sayan, Merriman, Chengfeng, Petzold, Christopher J., Ralston, Corie Y., and Fu, Dax. Water molecules mediate zinc mobility in the bacterial zinc diffusion channel ZIPB. United States: N. p., 2019.
Web. doi:10.1074/jbc.ra119.009239.
Gupta, Sayan, Merriman, Chengfeng, Petzold, Christopher J., Ralston, Corie Y., & Fu, Dax. Water molecules mediate zinc mobility in the bacterial zinc diffusion channel ZIPB. United States. doi:https://doi.org/10.1074/jbc.ra119.009239
Gupta, Sayan, Merriman, Chengfeng, Petzold, Christopher J., Ralston, Corie Y., and Fu, Dax. Thu .
"Water molecules mediate zinc mobility in the bacterial zinc diffusion channel ZIPB". United States. doi:https://doi.org/10.1074/jbc.ra119.009239. https://www.osti.gov/servlets/purl/1582337.
@article{osti_1582337,
title = {Water molecules mediate zinc mobility in the bacterial zinc diffusion channel ZIPB},
author = {Gupta, Sayan and Merriman, Chengfeng and Petzold, Christopher J. and Ralston, Corie Y. and Fu, Dax},
abstractNote = {Regulated ion diffusion across biological membranes is vital for cell function. In a nanoscale ion channel, the active role of discrete water molecules in modulating hydrodynamic behaviors of individual ions is poorly understood because of the technical challenge of tracking water molecules through the channel. Here we report the results of a hydroxyl radical footprinting analysis of the zinc-selective channel ZIPB from the Gram-negative bacterium, Bordetella bronchiseptica Irradiating ZIPB by microsecond X-ray pulses activated water molecules to form covalent hydroxyl radical adducts at nearby residues, which were identified by bottom-up proteomics to detect residues that interact either with zinc or water in response to zinc binding. We found a series of residues exhibiting reciprocal changes in water accessibility attributed to alternating zinc and water binding. Mapping these residues to the previously reported crystal structure of ZIPB, we identified a water-reactive pathway that superimposed on a zinc translocation pathway consisting of two binuclear metal centers and an interim zinc-binding site. The cotranslocation of zinc and water suggested that pore-lining residues undergo a mode switch between zinc coordination and water binding to confer zinc mobility. The unprecedented details of water-mediated zinc transport identified here highlight an essential role of solvated waters in driving zinc coordination dynamics and transmembrane crossing.},
doi = {10.1074/jbc.ra119.009239},
journal = {Journal of Biological Chemistry},
number = 36,
volume = 294,
place = {United States},
year = {2019},
month = {7}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 2 works
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:
Computation and Functional Studies Provide a Model for the Structure of the Zinc Transporter hZIP4
journal, May 2015
- Antala, Sagar; Ovchinnikov, Sergey; Kamisetty, Hetunandan
- Journal of Biological Chemistry, Vol. 290, Issue 29
Standard Flow Liquid Chromatography for Shotgun Proteomics in Bioenergy Research
journal, April 2015
- González Fernández-Niño, Susana M.; Smith-Moritz, A. Michelle; Chan, Leanne Jade G.
- Frontiers in Bioengineering and Biotechnology, Vol. 3
Structure of the Zinc Transporter YiiP
journal, September 2007
- Lu, M.; Fu, D.
- Science, Vol. 317, Issue 5845
Secondary Reactions and Strategies To Improve Quantitative Protein Footprinting
journal, May 2005
- Xu, Guozhong; Kiselar, Janna; He, Qin
- Analytical Chemistry, Vol. 77, Issue 10
Zinc coordination, function, and structure of zinc enzymes and other proteins
journal, June 1990
- Vallee, Bert L.; Auld, David S.
- Biochemistry, Vol. 29, Issue 24
Ion selectivity in channels and transporters
journal, April 2011
- Roux, Benoît; Bernèche, Simon; Egwolf, Bernhard
- The Journal of General Physiology, Vol. 137, Issue 5
New perspectives of zinc coordination environments in proteins
journal, June 2012
- Maret, Wolfgang
- Journal of Inorganic Biochemistry, Vol. 111
Crystal structures of a ZIP zinc transporter reveal a binuclear metal center in the transport pathway
journal, August 2017
- Zhang, Tuo; Liu, Jian; Fellner, Matthias
- Science Advances, Vol. 3, Issue 8
Complementary Structural Mass Spectrometry Techniques Reveal Local Dynamics in Functionally Important Regions of a Metastable Serpin
journal, January 2008
- Zheng, Xiaojing; Wintrode, Patrick L.; Chance, Mark R.
- Structure, Vol. 16, Issue 1
Reassessment of the Transport Mechanism of the Human Zinc Transporter SLC39A2
journal, May 2018
- Franz, Marie C.; Pujol-Giménez, Jonai; Montalbetti, Nicolas
- Biochemistry, Vol. 57, Issue 26
Buried water molecules in helical transmembrane proteins
journal, February 2008
- Renthal, Robert
- Protein Science, Vol. 17, Issue 2
Femtomolar Sensitivity of Metalloregulatory Proteins Controlling Zinc Homeostasis
journal, June 2001
- Outten, C. E.
- Science, Vol. 292, Issue 5526
Synchrotron X-ray footprinting as a method to visualize water in proteins
journal, July 2016
- Gupta, Sayan; Feng, Jun; Chan, Leanne Jade G.
- Journal of Synchrotron Radiation, Vol. 23, Issue 5
Unraveling the structural elements of pH sensitivity and substrate binding in the human zinc transporter SLC39A2 (ZIP2)
journal, March 2019
- Gyimesi, Gergely; Albano, Giuseppe; Fuster, Daniel G.
- Journal of Biological Chemistry, Vol. 294, Issue 20
Affinity gradients drive copper to cellular destinations
journal, May 2010
- Banci, Lucia; Bertini, Ivano; Ciofi-Baffoni, Simone
- Nature, Vol. 465, Issue 7298
Selective Electrodiffusion of Zinc Ions in a Zrt-, Irt-like Protein, ZIPB
journal, September 2010
- Lin, Wei; Chai, Jin; Love, James
- Journal of Biological Chemistry, Vol. 285, Issue 50
Structure and dynamics of protein waters revealed by radiolysis and mass spectrometry
journal, August 2012
- Gupta, S.; D'Mello, R.; Chance, M. R.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 37
Conformational Changes During the Gating of a Potassium Channel Revealed by Structural Mass Spectrometry
journal, July 2010
- Gupta, Sayan; Bavro, Vassiliy N.; D'Mello, Rhijuta
- Structure, Vol. 18, Issue 7
Hydroxyl Radical-Mediated Modification of Proteins as Probes for Structural Proteomics
journal, August 2007
- Xu, Guozhong; Chance, Mark R.
- Chemical Reviews, Vol. 107, Issue 8
Recovery from slow inactivation in K+ channels is controlled by water molecules
journal, July 2013
- Ostmeyer, Jared; Chakrapani, Sudha; Pan, Albert C.
- Nature, Vol. 501, Issue 7465
Metallochaperones, an Intracellular Shuttle Service for Metal Ions
journal, May 2000
- O'Halloran, Thomas V.; Culotta, Valeria Cizewski
- Journal of Biological Chemistry, Vol. 275, Issue 33
Development of a microsecond X-ray protein footprinting facility at the Advanced Light Source
journal, May 2014
- Gupta, Sayan; Celestre, Richard; Petzold, Christopher J.
- Journal of Synchrotron Radiation, Vol. 21, Issue 4
Visualizing the kinetic power stroke that drives proton-coupled zinc(ii) transport
journal, June 2014
- Gupta, Sayan; Chai, Jin; Cheng, Jie
- Nature, Vol. 512, Issue 7512
Structural waters define a functional channel mediating activation of the GPCR, rhodopsin
journal, August 2009
- Angel, T. E.; Gupta, S.; Jastrzebska, B.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 34
The SLC39 family of zinc transporters
journal, April 2013
- Jeong, Jeeyon; Eide, David J.
- Molecular Aspects of Medicine, Vol. 34, Issue 2-3
Coordination Dynamics of Zinc in Proteins
journal, October 2009
- Maret, Wolfgang; Li, Yuan
- Chemical Reviews, Vol. 109, Issue 10
Counting the Zinc-Proteins Encoded in the Human Genome
journal, January 2006
- Andreini, Claudia; Banci, Lucia; Bertini, Ivano
- Journal of Proteome Research, Vol. 5, Issue 1
Three-dimensional structure of the human copper transporter hCTR1
journal, February 2009
- De Feo, C. J.; Aller, S. G.; Siluvai, G. S.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 11