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Title: Structural insights into the mechanism of oxidative activation of heme-free H-NOX from Vibrio cholerae

Abstract

Bacterial heme nitric oxide/oxygen (H-NOX) domains are nitric oxide (NO) or oxygen sensors. This activity is mediated through binding of the ligand to a heme cofactor. However, H-NOX from Vibrio cholerae (Vc H-NOX) can be easily purified in a heme-free state that is capable of reversibly responding to oxidation, suggesting a heme-independent function as a redox sensor. This occurs by oxidation of Cys residues at a zinc-binding site conserved in a subset of H-NOX homologs. Remarkably, zinc is not lost from the protein upon oxidation, although its ligation environment is significantly altered. Using a combination of computational and experimental approaches, we have characterized localized structural changes that accompany the formation of specific disulfide bonds between Cys residues upon oxidation. Furthermore, the larger-scale structural changes accompanying oxidation appear to mimic those changes observed upon NO binding to the heme-bound form. Thus, Vc H-NOX and its homologs may act as both redox and NO sensors by completely separate mechanisms.

Authors:
 [1];  [2];  [3];  [1]; ORCiD logo [1]
  1. New Mexico State Univ., Las Cruces, NM (United States). Dept. of Chemistry and Biochemistry
  2. Reed College, Portland, OR (United States). Dept. of Chemistry
  3. New Mexico State Univ., Las Cruces, NM (United States). Dept. of Plant and Environmental Sciences
Publication Date:
Research Org.:
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1624989
Grant/Contract Number:  
AC02-76SF00515
Resource Type:
Accepted Manuscript
Journal Name:
Biochemical Journal
Additional Journal Information:
Journal Volume: 477; Journal Issue: 6; Journal ID: ISSN 0264-6021
Publisher:
Biochemical Society
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Biochemistry & Molecular Biology; disulphide bonds; redox signalling; zinc; Computational Biology; Molecular Bases of Health & Disease; Signaling

Citation Formats

Mukhopadhyay, Roma, Chacón, Kelly N., Jarvis, Jacqueline M., Talipov, Marat R., and Yukl, Erik T.. Structural insights into the mechanism of oxidative activation of heme-free H-NOX from Vibrio cholerae. United States: N. p., 2020. Web. doi:10.1042/bcj20200124.
Mukhopadhyay, Roma, Chacón, Kelly N., Jarvis, Jacqueline M., Talipov, Marat R., & Yukl, Erik T.. Structural insights into the mechanism of oxidative activation of heme-free H-NOX from Vibrio cholerae. United States. https://doi.org/10.1042/bcj20200124
Mukhopadhyay, Roma, Chacón, Kelly N., Jarvis, Jacqueline M., Talipov, Marat R., and Yukl, Erik T.. Mon . "Structural insights into the mechanism of oxidative activation of heme-free H-NOX from Vibrio cholerae". United States. https://doi.org/10.1042/bcj20200124. https://www.osti.gov/servlets/purl/1624989.
@article{osti_1624989,
title = {Structural insights into the mechanism of oxidative activation of heme-free H-NOX from Vibrio cholerae},
author = {Mukhopadhyay, Roma and Chacón, Kelly N. and Jarvis, Jacqueline M. and Talipov, Marat R. and Yukl, Erik T.},
abstractNote = {Bacterial heme nitric oxide/oxygen (H-NOX) domains are nitric oxide (NO) or oxygen sensors. This activity is mediated through binding of the ligand to a heme cofactor. However, H-NOX from Vibrio cholerae (Vc H-NOX) can be easily purified in a heme-free state that is capable of reversibly responding to oxidation, suggesting a heme-independent function as a redox sensor. This occurs by oxidation of Cys residues at a zinc-binding site conserved in a subset of H-NOX homologs. Remarkably, zinc is not lost from the protein upon oxidation, although its ligation environment is significantly altered. Using a combination of computational and experimental approaches, we have characterized localized structural changes that accompany the formation of specific disulfide bonds between Cys residues upon oxidation. Furthermore, the larger-scale structural changes accompanying oxidation appear to mimic those changes observed upon NO binding to the heme-bound form. Thus, Vc H-NOX and its homologs may act as both redox and NO sensors by completely separate mechanisms.},
doi = {10.1042/bcj20200124},
journal = {Biochemical Journal},
number = 6,
volume = 477,
place = {United States},
year = {2020},
month = {3}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Figures / Tables:

Figure 1 Figure 1: Conservation of zinc binding sites among H-NOX homologues. (A) Sequence similarity network including 599 sequences filtered such that only edges associated with E-values less than 10−47 are included in the network. Sequences are represented by rectangles colored according to class. (B) Multiple sequence alignment of three representative sequencesmore » from each group in (A). Putative zinc-binding residues are highlighted in yellow. Species names are abbreviated as follows: (Group 1) Calg, Cellulophaga algiola; Rsli, Runella slithyformis; Mext, Methylobacterium extorquans; (Group 2) Vcho, Vibrio cholerae; Sone, Shewanella oneidensis; Lpne, Legionella pneumophila; (Group 3) Msp, Mycobacterium sp.; Cvib, Caulobacter vibrioides; Psp, Pseudomonas sp. DY-1; (Group 4) Vhar, Vibrio harveyi; Vnig, Vibrio nigripulchritudo; Psan, Photobacterium sanguinicancri. (C) Zinc coordination environment in a Vc H-NOX homology model. Each of the residues in the figure has been mutated to Ala and those indicated by asterisks result in insoluble protein.« less

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Works referenced in this record:

Shewanella oneidensis MR-1 H-NOX Regulation of a Histidine Kinase by Nitric Oxide
journal, December 2007

  • Price, Mark S.; Chao, Lily Y.; Marletta, Michael A.
  • Biochemistry, Vol. 46, Issue 48
  • DOI: 10.1021/bi7019035

Definition of molecular orbitals in fragment molecular orbital method
journal, September 2002


Nonphysical sampling distributions in Monte Carlo free-energy estimation: Umbrella sampling
journal, February 1977


Enzyme Function Initiative-Enzyme Similarity Tool (EFI-EST): A web tool for generating protein sequence similarity networks
journal, August 2015

  • Gerlt, John A.; Bouvier, Jason T.; Davidson, Daniel B.
  • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1854, Issue 8
  • DOI: 10.1016/j.bbapap.2015.04.015

The polarizable continuum model (PCM) interfaced with the fragment molecular orbital method (FMO)
journal, January 2006

  • Fedorov, Dmitri G.; Kitaura, Kazuo; Li, Hui
  • Journal of Computational Chemistry, Vol. 27, Issue 8
  • DOI: 10.1002/jcc.20406

Algorithm improvements for molecular dynamics simulations
journal, January 2011

  • Larsson, Per; Hess, Berk; Lindahl, Erik
  • WIREs Computational Molecular Science, Vol. 1, Issue 1
  • DOI: 10.1002/wcms.3

The Amber biomolecular simulation programs
journal, January 2005

  • Case, David A.; Cheatham, Thomas E.; Darden, Tom
  • Journal of Computational Chemistry, Vol. 26, Issue 16
  • DOI: 10.1002/jcc.20290

The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling
journal, November 2005


Nitric Oxide Regulation of Cyclic di-GMP Synthesis and Hydrolysis in Shewanella woodyi
journal, February 2012

  • Liu, Niu; Xu, Yueming; Hossain, Sajjad
  • Biochemistry, Vol. 51, Issue 10
  • DOI: 10.1021/bi201753f

Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes
journal, March 1977

  • Ryckaert, Jean-Paul; Ciccotti, Giovanni; Berendsen, Herman J. C.
  • Journal of Computational Physics, Vol. 23, Issue 3
  • DOI: 10.1016/0021-9991(77)90098-5

A structural basis for H-NOX signaling in Shewanella oneidensis by trapping a histidine kinase inhibitory conformation
journal, November 2009

  • Erbil, W. K.; Price, M. S.; Wemmer, D. E.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 47
  • DOI: 10.1073/pnas.0911645106

H-NOX regulation of c-di-GMP metabolism and biofilm formation in Legionella pneumophila: H-NOX regulation of biofilms
journal, July 2010


Routine Microsecond Molecular Dynamics Simulations with AMBER on GPUs. 2. Explicit Solvent Particle Mesh Ewald
journal, August 2013

  • Salomon-Ferrer, Romelia; Götz, Andreas W.; Poole, Duncan
  • Journal of Chemical Theory and Computation, Vol. 9, Issue 9
  • DOI: 10.1021/ct400314y

Comparison of simple potential functions for simulating liquid water
journal, July 1983

  • Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D.
  • The Journal of Chemical Physics, Vol. 79, Issue 2
  • DOI: 10.1063/1.445869

Role of Vibrio polysaccharide (vps) genes in VPS production, biofilm formation and Vibrio cholerae pathogenesis
journal, September 2010

  • Fong, Jiunn C. N.; Syed, Khalid A.; Klose, Karl E.
  • Microbiology, Vol. 156, Issue 9
  • DOI: 10.1099/mic.0.040196-0

Routine Microsecond Molecular Dynamics Simulations with AMBER on GPUs. 1. Generalized Born
journal, April 2012

  • Götz, Andreas W.; Williamson, Mark J.; Xu, Dong
  • Journal of Chemical Theory and Computation, Vol. 8, Issue 5
  • DOI: 10.1021/ct200909j

Structural insights into the molecular mechanism of H-NOX activation: Molecular Mechanism of H-NOX Activation
journal, February 2010

  • Olea, Charles; Herzik, Mark A.; Kuriyan, John
  • Protein Science, Vol. 19, Issue 4
  • DOI: 10.1002/pro.357

Structural and Functional Evidence Indicates Selective Oxygen Signaling in Caldanaerobacter subterraneus H-NOX
journal, June 2016

  • Hespen, Charles W.; Bruegger, Joel J.; Phillips-Piro, Christine M.
  • ACS Chemical Biology, Vol. 11, Issue 8
  • DOI: 10.1021/acschembio.6b00431

Discovery of a Nitric Oxide Responsive Quorum Sensing Circuit in Vibrio harveyi
journal, May 2012

  • Henares, Bernadette M.; Higgins, Kate E.; Boon, Elizabeth M.
  • ACS Chemical Biology, Vol. 7, Issue 8
  • DOI: 10.1021/cb300215t

Mapping the H-NOX/HK Binding Interface in Vibrio cholerae by Hydrogen/Deuterium Exchange Mass Spectrometry
journal, February 2018


Electron Transfer Dissociation (ETD) of Peptides Containing Intrachain Disulfide Bonds
journal, December 2011

  • Cole, Scott R.; Ma, Xiaoxiao; Zhang, Xinrong
  • Journal of The American Society for Mass Spectrometry, Vol. 23, Issue 2
  • DOI: 10.1007/s13361-011-0300-z

UCSF Chimera?A visualization system for exploratory research and analysis
journal, January 2004

  • Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C.
  • Journal of Computational Chemistry, Vol. 25, Issue 13
  • DOI: 10.1002/jcc.20084

Parametrized Models of Aqueous Free Energies of Solvation Based on Pairwise Descreening of Solute Atomic Charges from a Dielectric Medium
journal, January 1996

  • Hawkins, Gregory D.; Cramer, Christopher J.; Truhlar, Donald G.
  • The Journal of Physical Chemistry, Vol. 100, Issue 51
  • DOI: 10.1021/jp961710n

Direct mass spectrometric characterization of disulfide linkages
journal, March 2018


H-NOX-mediated nitric oxide sensing modulates symbiotic colonization by Vibrio fischeri
journal, April 2010

  • Wang, Y.; Dufour, Y. S.; Carlson, H. K.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 18
  • DOI: 10.1073/pnas.1003571107

ACEMD: Accelerating Biomolecular Dynamics in the Microsecond Time Scale
journal, May 2009

  • Harvey, M. J.; Giupponi, G.; Fabritiis, G. De
  • Journal of Chemical Theory and Computation, Vol. 5, Issue 6
  • DOI: 10.1021/ct9000685

Long-Time-Step Molecular Dynamics through Hydrogen Mass Repartitioning
journal, March 2015

  • Hopkins, Chad W.; Le Grand, Scott; Walker, Ross C.
  • Journal of Chemical Theory and Computation, Vol. 11, Issue 4
  • DOI: 10.1021/ct5010406

A rapid, exact, curved-wave theory for EXAFS calculations. II. The multiple-scattering contributions
journal, April 1986


Transmissibility of cholera: In vivo-formed biofilms and their relationship to infectivity and persistence in the environment
journal, April 2006

  • Faruque, S. M.; Biswas, K.; Udden, S. M. N.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 16
  • DOI: 10.1073/pnas.0601277103

Structural insights into the role of iron–histidine bond cleavage in nitric oxide-induced activation of H-NOX gas sensor proteins
journal, September 2014

  • Herzik, Mark A.; Jonnalagadda, Rohan; Kuriyan, John
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 40
  • DOI: 10.1073/pnas.1416936111

Simple Approach to Assign Disulfide Connectivity Using Extracted Ion Chromatograms of Electron Transfer Dissociation Spectra
journal, December 2012

  • Clark, Daniel F.; Go, Eden P.; Desaire, Heather
  • Analytical Chemistry, Vol. 85, Issue 2
  • DOI: 10.1021/ac303124w

Probing the Function of Heme Distortion in the H-NOX Family
journal, November 2008

  • Olea, Charles; Boon, Elizabeth M.; Pellicena, Patricia
  • ACS Chemical Biology, Vol. 3, Issue 11
  • DOI: 10.1021/cb800185h

The utility of ETD mass spectrometry in proteomic analysis
journal, December 2006

  • Mikesh, Leann M.; Ueberheide, Beatrix; Chi, An
  • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1764, Issue 12
  • DOI: 10.1016/j.bbapap.2006.10.003

Stimulation of biofilm formation by oxidative stress in Campylobacter jejuni under aerobic conditions
journal, May 2016


Increased Levels of Inflammatory Mediators in Children and Adults Infected with Vibrio cholerae O1 and O139
journal, March 2002


General atomic and molecular electronic structure system
journal, November 1993

  • Schmidt, Michael W.; Baldridge, Kim K.; Boatz, Jerry A.
  • Journal of Computational Chemistry, Vol. 14, Issue 11, p. 1347-1363
  • DOI: 10.1002/jcc.540141112

ff14SB: Improving the Accuracy of Protein Side Chain and Backbone Parameters from ff99SB
journal, July 2015

  • Maier, James A.; Martinez, Carmenza; Kasavajhala, Koushik
  • Journal of Chemical Theory and Computation, Vol. 11, Issue 8
  • DOI: 10.1021/acs.jctc.5b00255

Effect of reducing disulfide-containing proteins on electrospray ionization mass spectra
journal, April 1990

  • Loo, Joseph A.; Edmonds, Charles G.; Udseth, Harold R.
  • Analytical Chemistry, Vol. 62, Issue 7
  • DOI: 10.1021/ac00206a009

Self-limiting nature of seasonal cholera epidemics: Role of host-mediated amplification of phage
journal, April 2005

  • Faruque, S. M.; Islam, M. J.; Ahmad, Q. S.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 17
  • DOI: 10.1073/pnas.0502069102

Pairwise solute descreening of solute charges from a dielectric medium
journal, November 1995

  • Hawkins, Gregory D.; Cramer, Christopher J.; Truhlar, Donald G.
  • Chemical Physics Letters, Vol. 246, Issue 1-2
  • DOI: 10.1016/0009-2614(95)01082-K

THE weighted histogram analysis method for free-energy calculations on biomolecules. I. The method
journal, October 1992

  • Kumar, Shankar; Rosenberg, John M.; Bouzida, Djamal
  • Journal of Computational Chemistry, Vol. 13, Issue 8
  • DOI: 10.1002/jcc.540130812

Determination of the transcriptome of Vibrio cholerae during intraintestinal growth and midexponential phase in vitro
journal, January 2003

  • Xu, Q.; Dziejman, M.; Mekalanos, J. J.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 3
  • DOI: 10.1073/pnas.0337479100

A rapid, exact curved-wave theory for EXAFS calculations
journal, January 1984

  • Gurman, S. J.; Binsted, N.; Ross, I.
  • Journal of Physics C: Solid State Physics, Vol. 17, Issue 1
  • DOI: 10.1088/0022-3719/17/1/019

Vibrio cholerae Infection of Drosophila melanogaster Mimics the Human Disease Cholera
journal, September 2005


Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
journal, November 2003


‘Democratized’ genomic enzymology web tools for functional assignment
journal, December 2018


Spatially selective colonization of the arthropod intestine through activation of Vibrio cholerae biofilm formation
journal, November 2011

  • Purdy, A. E.; Watnick, P. I.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 49
  • DOI: 10.1073/pnas.1111530108

Structural Insight into H‐NOX Gas Sensing and Cognate Signaling Protein Regulation
journal, November 2018


Nitric Oxide-Induced Conformational Changes Govern H-NOX and Histidine Kinase Interaction and Regulation in Shewanella oneidensis
journal, February 2017


Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega
journal, January 2011

  • Sievers, Fabian; Wilm, Andreas; Dineen, David
  • Molecular Systems Biology, Vol. 7, Issue 1
  • DOI: 10.1038/msb.2011.75

Ligand specificity of H-NOX domains: from sGC to bacterial NO sensors
journal, April 2005


Nitric Oxide Modulates Bacterial Biofilm Formation through a Multicomponent Cyclic-di-GMP Signaling Network
journal, May 2012


Pair interaction energy decomposition analysis
journal, January 2006

  • Fedorov, Dmitri G.; Kitaura, Kazuo
  • Journal of Computational Chemistry, Vol. 28, Issue 1
  • DOI: 10.1002/jcc.20496

Role of the W07-toxin on Vibrio cholerae-induced diarrhoea
journal, January 2004

  • Bhattacharyya, Shalmoli; Ghosh, Sujata; Shant, Jasleen
  • Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1670, Issue 1
  • DOI: 10.1016/j.bbagen.2003.10.016

Crystal structure of an oxygen-binding heme domain related to soluble guanylate cyclases
journal, August 2004

  • Pellicena, P.; Karow, D. S.; Boon, E. M.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 35
  • DOI: 10.1073/pnas.0405188101

Mass Spectrometric Determination of Disulfide Linkages in Recombinant Therapeutic Proteins Using Online LC−MS with Electron-Transfer Dissociation
journal, January 2009

  • Wu, Shiaw-Lin; Jiang, Haitao; Lu, Qiaozhen
  • Analytical Chemistry, Vol. 81, Issue 1
  • DOI: 10.1021/ac801560k

A smooth particle mesh Ewald method
journal, November 1995

  • Essmann, Ulrich; Perera, Lalith; Berkowitz, Max L.
  • The Journal of Chemical Physics, Vol. 103, Issue 19
  • DOI: 10.1063/1.470117

Theoretical study of intramolecular interaction energies during dynamics simulations of oligopeptides by the fragment molecular orbital-Hamiltonian algorithm method
journal, March 2005

  • Ishimoto, Takayoshi; Tokiwa, Hiroaki; Teramae, Hiroyuki
  • The Journal of Chemical Physics, Vol. 122, Issue 9
  • DOI: 10.1063/1.1857481

Jalview Version 2--a multiple sequence alignment editor and analysis workbench
journal, January 2009


VMD: Visual molecular dynamics
journal, February 1996


Structural Insight into H‐NOX Gas Sensing and Cognate Signaling Protein Regulation
journal, November 2018


The Amber biomolecular simulation programs
journal, January 2005

  • Case, David A.; Cheatham, Thomas E.; Darden, Tom
  • Journal of Computational Chemistry, Vol. 26, Issue 16
  • DOI: 10.1002/jcc.20290

The polarizable continuum model (PCM) interfaced with the fragment molecular orbital method (FMO)
journal, January 2006

  • Fedorov, Dmitri G.; Kitaura, Kazuo; Li, Hui
  • Journal of Computational Chemistry, Vol. 27, Issue 8
  • DOI: 10.1002/jcc.20406

Pair interaction energy decomposition analysis
journal, January 2006

  • Fedorov, Dmitri G.; Kitaura, Kazuo
  • Journal of Computational Chemistry, Vol. 28, Issue 1
  • DOI: 10.1002/jcc.20496

Structural insights into the molecular mechanism of H-NOX activation: Molecular Mechanism of H-NOX Activation
journal, February 2010

  • Olea, Charles; Herzik, Mark A.; Kuriyan, John
  • Protein Science, Vol. 19, Issue 4
  • DOI: 10.1002/pro.357

Algorithm improvements for molecular dynamics simulations
journal, January 2011

  • Larsson, Per; Hess, Berk; Lindahl, Erik
  • WIREs Computational Molecular Science, Vol. 1, Issue 1
  • DOI: 10.1002/wcms.3

Computational Study of Methionine Methylation Process Catalyzed by SETD3
journal, April 2022

  • Zhao, Yuan-Yuan; Deng, Hao; Rahman, Adua
  • Interdisciplinary Sciences: Computational Life Sciences, Vol. 14, Issue 4
  • DOI: 10.1007/s12539-022-00516-0

Electron Transfer Dissociation (ETD) of Peptides Containing Intrachain Disulfide Bonds
journal, December 2011

  • Cole, Scott R.; Ma, Xiaoxiao; Zhang, Xinrong
  • Journal of The American Society for Mass Spectrometry, Vol. 23, Issue 2
  • DOI: 10.1007/s13361-011-0300-z

Nonphysical sampling distributions in Monte Carlo free-energy estimation: Umbrella sampling
journal, February 1977


Role of the W07-toxin on Vibrio cholerae-induced diarrhoea
journal, January 2004

  • Bhattacharyya, Shalmoli; Ghosh, Sujata; Shant, Jasleen
  • Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1670, Issue 1
  • DOI: 10.1016/j.bbagen.2003.10.016

Enzyme Function Initiative-Enzyme Similarity Tool (EFI-EST): A web tool for generating protein sequence similarity networks
journal, August 2015

  • Gerlt, John A.; Bouvier, Jason T.; Davidson, Daniel B.
  • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1854, Issue 8
  • DOI: 10.1016/j.bbapap.2015.04.015

‘Democratized’ genomic enzymology web tools for functional assignment
journal, December 2018


Nitric Oxide Modulates Bacterial Biofilm Formation through a Multicomponent Cyclic-di-GMP Signaling Network
journal, May 2012


Electron capture dissociation of gaseous multiply charged ions by Fourier-transform ion cyclotron resonance
journal, March 2001

  • McLafferty, Fred W.; Horn, David M.; Breuker, Kathrin
  • Journal of the American Society for Mass Spectrometry, Vol. 12, Issue 3
  • DOI: 10.1016/s1044-0305(00)00223-3

Effect of reducing disulfide-containing proteins on electrospray ionization mass spectra
journal, April 1990

  • Loo, Joseph A.; Edmonds, Charles G.; Udseth, Harold R.
  • Analytical Chemistry, Vol. 62, Issue 7
  • DOI: 10.1021/ac00206a009

Nitric Oxide-Induced Conformational Changes Govern H-NOX and Histidine Kinase Interaction and Regulation in Shewanella oneidensis
journal, February 2017


ff14SB: Improving the Accuracy of Protein Side Chain and Backbone Parameters from ff99SB
journal, July 2015

  • Maier, James A.; Martinez, Carmenza; Kasavajhala, Koushik
  • Journal of Chemical Theory and Computation, Vol. 11, Issue 8
  • DOI: 10.1021/acs.jctc.5b00255

Structural and Functional Evidence Indicates Selective Oxygen Signaling in Caldanaerobacter subterraneus H-NOX
journal, June 2016

  • Hespen, Charles W.; Bruegger, Joel J.; Phillips-Piro, Christine M.
  • ACS Chemical Biology, Vol. 11, Issue 8
  • DOI: 10.1021/acschembio.6b00431

Shewanella oneidensis MR-1 H-NOX Regulation of a Histidine Kinase by Nitric Oxide
journal, December 2007

  • Price, Mark S.; Chao, Lily Y.; Marletta, Michael A.
  • Biochemistry, Vol. 46, Issue 48
  • DOI: 10.1021/bi7019035

Discovery of a Nitric Oxide Responsive Quorum Sensing Circuit in Vibrio harveyi
journal, May 2012

  • Henares, Bernadette M.; Higgins, Kate E.; Boon, Elizabeth M.
  • ACS Chemical Biology, Vol. 7, Issue 8
  • DOI: 10.1021/cb300215t

Probing the Function of Heme Distortion in the H-NOX Family
journal, November 2008

  • Olea, Charles; Boon, Elizabeth M.; Pellicena, Patricia
  • ACS Chemical Biology, Vol. 3, Issue 11
  • DOI: 10.1021/cb800185h

Routine Microsecond Molecular Dynamics Simulations with AMBER on GPUs. 2. Explicit Solvent Particle Mesh Ewald
journal, August 2013

  • Salomon-Ferrer, Romelia; Götz, Andreas W.; Poole, Duncan
  • Journal of Chemical Theory and Computation, Vol. 9, Issue 9
  • DOI: 10.1021/ct400314y

Long-Time-Step Molecular Dynamics through Hydrogen Mass Repartitioning
journal, March 2015

  • Hopkins, Chad W.; Le Grand, Scott; Walker, Ross C.
  • Journal of Chemical Theory and Computation, Vol. 11, Issue 4
  • DOI: 10.1021/ct5010406

ACEMD: Accelerating Biomolecular Dynamics in the Microsecond Time Scale
journal, May 2009

  • Harvey, M. J.; Giupponi, G.; Fabritiis, G. De
  • Journal of Chemical Theory and Computation, Vol. 5, Issue 6
  • DOI: 10.1021/ct9000685

Parametrized Models of Aqueous Free Energies of Solvation Based on Pairwise Descreening of Solute Atomic Charges from a Dielectric Medium
journal, January 1996

  • Hawkins, Gregory D.; Cramer, Christopher J.; Truhlar, Donald G.
  • The Journal of Physical Chemistry, Vol. 100, Issue 51
  • DOI: 10.1021/jp961710n

Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega
journal, January 2011

  • Sievers, Fabian; Wilm, Andreas; Dineen, David
  • Molecular Systems Biology, Vol. 7, Issue 1
  • DOI: 10.1038/msb.2011.75

Evolution of the murine gut resistome following broad-spectrum antibiotic treatment
journal, April 2022


Comparative transcriptomic analysis reveals conserved programmes underpinning organogenesis and reproduction in land plants
journal, July 2021


Stepwise gating of the Sec61 protein-conducting channel by Sec63 and Sec62
journal, January 2021

  • Itskanov, Samuel; Kuo, Katie M.; Gumbart, James C.
  • Nature Structural & Molecular Biology, Vol. 28, Issue 2
  • DOI: 10.1038/s41594-020-00541-x

Theoretical study of intramolecular interaction energies during dynamics simulations of oligopeptides by the fragment molecular orbital-Hamiltonian algorithm method
journal, March 2005

  • Ishimoto, Takayoshi; Tokiwa, Hiroaki; Teramae, Hiroyuki
  • The Journal of Chemical Physics, Vol. 122, Issue 9
  • DOI: 10.1063/1.1857481

Determination of the transcriptome of Vibrio cholerae during intraintestinal growth and midexponential phase in vitro
journal, January 2003

  • Xu, Q.; Dziejman, M.; Mekalanos, J. J.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 3
  • DOI: 10.1073/pnas.0337479100

Crystal structure of an oxygen-binding heme domain related to soluble guanylate cyclases
journal, August 2004

  • Pellicena, P.; Karow, D. S.; Boon, E. M.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 35
  • DOI: 10.1073/pnas.0405188101

Self-limiting nature of seasonal cholera epidemics: Role of host-mediated amplification of phage
journal, April 2005

  • Faruque, S. M.; Islam, M. J.; Ahmad, Q. S.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 17
  • DOI: 10.1073/pnas.0502069102

Transmissibility of cholera: In vivo-formed biofilms and their relationship to infectivity and persistence in the environment
journal, April 2006

  • Faruque, S. M.; Biswas, K.; Udden, S. M. N.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 16
  • DOI: 10.1073/pnas.0601277103

A structural basis for H-NOX signaling in Shewanella oneidensis by trapping a histidine kinase inhibitory conformation
journal, November 2009

  • Erbil, W. K.; Price, M. S.; Wemmer, D. E.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 47
  • DOI: 10.1073/pnas.0911645106

H-NOX-mediated nitric oxide sensing modulates symbiotic colonization by Vibrio fischeri
journal, April 2010

  • Wang, Y.; Dufour, Y. S.; Carlson, H. K.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 18
  • DOI: 10.1073/pnas.1003571107

Heme-independent Redox Sensing by the Heme-Nitric Oxide/Oxygen-binding Protein (H-NOX) from Vibrio cholerae
journal, June 2016

  • Mukhopadyay, Roma; Sudasinghe, Nilusha; Schaub, Tanner
  • Journal of Biological Chemistry, Vol. 291, Issue 34
  • DOI: 10.1074/jbc.m116.733337

Oxidant Sensing by Reversible Disulfide Bond Formation
journal, July 2013

  • Cremers, Claudia M.; Jakob, Ursula
  • Journal of Biological Chemistry, Vol. 288, Issue 37
  • DOI: 10.1074/jbc.r113.462929

Direct mass spectrometric characterization of disulfide linkages
journal, March 2018


A rapid, exact curved-wave theory for EXAFS calculations
journal, January 1984

  • Gurman, S. J.; Binsted, N.; Ross, I.
  • Journal of Physics C: Solid State Physics, Vol. 17, Issue 1
  • DOI: 10.1088/0022-3719/17/1/019

The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling
journal, November 2005


Role of Vibrio polysaccharide (vps) genes in VPS production, biofilm formation and Vibrio cholerae pathogenesis
journal, September 2010

  • Fong, Jiunn C. N.; Syed, Khalid A.; Klose, Karl E.
  • Microbiology, Vol. 156, Issue 9
  • DOI: 10.1099/mic.0.040196-0

State-of-the-Art Analysis of Whole X-ray Absorption Spectra
journal, July 1996


Increased Levels of Inflammatory Mediators in Children and Adults Infected with Vibrio cholerae O1 and O139
journal, March 2002


Comparative Proteomic Analysis Reveals Activation of Mucosal Innate Immune Signaling Pathways during Cholera
journal, January 2015

  • Ellis, Crystal N.; LaRocque, Regina C.; Uddin, Taher
  • Infection and Immunity, Vol. 83, Issue 3
  • DOI: 10.1128/iai.02765-14

Environmental and Genetic Determinants of Biofilm Formation in Paracoccus denitrificans
journal, September 2017


Vibrio cholerae Infection of Drosophila melanogaster Mimics the Human Disease Cholera
journal, September 2005


Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.