Kinetic characterization of Vibrio cholerae ApbE: Substrate specificity and regulatory mechanisms

Fang, Xuan; Liang, Pingdong; Raba, Daniel Alexander; Rosas-Lemus, Mónica; Chakravarthy, Srinivas; Tuz, Karina; Juárez, Oscar; Permyakov, Eugene A.

doi:10.1371/journal.pone.0186805

Title: Kinetic characterization of Vibrio cholerae ApbE: Substrate specificity and regulatory mechanisms

Journal Article · Tue Oct 24 00:00:00 EDT 2017 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0186805· OSTI ID:1410114

Fang, Xuan; Liang, Pingdong; Raba, Daniel Alexander; Rosas-Lemus, Mónica; Chakravarthy, Srinivas; Tuz, Karina;

; Permyakov, Eugene A.

ApbE is a member of a novel family of flavin transferases that incorporates flavin mononucleotide (FMN) to subunits of diverse respiratory complexes, which fulfill important homeostatic functions. In this work a detailed characterization of Vibrio cholerae ApbE physiologic activity, substrate specificity and pH dependency was carried out. The data obtained show novel characteristics of the regulation and function of this family. For instance, our experiments indicate that divalent cations are essential for ApbE function, and that the selectivity depends largely on size and the coordination sphere of the cation. Our data also show that ApbE regulation by pH, ADP and potassium is an important mechanism that enhances the adaptation, survival and colonization of V. cholerae in the small intestine. Moreover, studies of the pH-dependency of the activity show that the reaction is favored under alkaline conditions, with a pKa of 8.4. These studies, together with sequence and structure analysis allowed us to identify His257, which is absolutely conserved in the family, as a candidate for the residue whose deprotonation controls the activity. Remarkably, the mutant H257G abolished the flavin transfer activity, strongly indicating that this residue plays an important role in the catalytic mechanism of ApbE.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: National Institutes of Health (NIH)

OSTI ID:: 1410114

Journal Information:: PLoS ONE, Vol. 12, Issue 10; ISSN 1932-6203

Publisher:: Public Library of Science

Country of Publication:: United States

Language:: ENGLISH

References (67)

Effect of multidrug-efflux transporter genes on dipeptide resistance and overproduction in Escherichia coli: Dipeptide transporters Hayashi, Mikiro; Tabata, Kazuhiko; Yagasaki, Makoto FEMS Microbiology Letters, Vol. 304, Issue 1 https://doi.org/10.1111/j.1574-6968.2009.01879.x	journal	February 2010
Three-dimensional structure of p-cresol methylhydroxylase (flavocytochrome c) from Pseudomonas putida at 3.0-.ANG. resolution Mathews, F. Scott; Chen, Zhi Wei; Bellamy, Henry D. Biochemistry, Vol. 30, Issue 1 https://doi.org/10.1021/bi00215a034	journal	January 1991
Recent progress in the Na+-translocating NADH-quinone reductase from the marine Vibrio alginolyticus Hayashi, Maki; Nakayama, Yuji; Unemoto, Tsutomu Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1505, Issue 1 https://doi.org/10.1016/S0005-2728(00)00275-9	journal	May 2001
The Na ⁺ /e ⁻ stoichiometry of the Na ⁺ -motive NADH : quinone oxidoreductase in Vibrio alginolyticus Bogachev, Alexander V.; Murtazina, Rachilya A.; Skulachev, Vladimir P. FEBS Letters, Vol. 409, Issue 3 https://doi.org/10.1016/s0014-5793(97)00536-x	journal	June 1997
Infrared Spectroscopic Evidence of a Redox-Dependent Conformational Change Involving Ion Binding Residue NqrB-D397 in the Na ⁺ -Pumping NADH:Quinone Oxidoreductase from Vibrio cholerae Neehaul, Yashvin; Juárez, Oscar; Barquera, Blanca Biochemistry, Vol. 52, Issue 18 https://doi.org/10.1021/bi4000386	journal	April 2013
An essential role for UshA in processing of extracellular flavin electron shuttles by Shewanella oneidensis: Flavin processing by UshA in S. oneidensis Covington, Elizabeth D.; Gelbmann, Christopher B.; Kotloski, Nicholas J. Molecular Microbiology, Vol. 78, Issue 2 https://doi.org/10.1111/j.1365-2958.2010.07353.x	journal	September 2010
Molecular insights into the enzymatic diversity of flavin-trafficking protein (Ftp; formerly ApbE) in flavoprotein biogenesis in the bacterial periplasm Deka, Ranjit K.; Brautigam, Chad A.; Liu, Wei Z. MicrobiologyOpen, Vol. 5, Issue 1 https://doi.org/10.1002/mbo3.306	journal	December 2015
Urocanate reductase: identification of a novel anaerobic respiratory pathway in Shewanella oneidensis MR-1 : Urocanate reductase of Bogachev, Alexander V.; Bertsova, Yulia V.; Bloch, Dmitry A. Molecular Microbiology, Vol. 86, Issue 6 https://doi.org/10.1111/mmi.12067	journal	November 2012
The flavinyl transferase ApbE of Pseudomonas stutzeri matures the NosR protein required for nitrous oxide reduction Zhang, Lin; Trncik, Christian; Andrade, Susana L. A. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1858, Issue 2 https://doi.org/10.1016/j.bbabio.2016.11.008	journal	February 2017
Covalent Flavinylation Is Essential for Efficient Redox Catalysis in Vanillyl-alcohol Oxidase Fraaije, Marco W.; van den Heuvel, Robert H. H.; van Berkel, Willem J. H. Journal of Biological Chemistry, Vol. 274, Issue 50 https://doi.org/10.1074/jbc.274.50.35514	journal	December 1999
Mechanism of Flavin Mononucleotide Cofactor Binding to the Desulfovibrio vulgaris Flavodoxin. 1. Kinetic Evidence for Cooperative Effects Associated with the Binding of Inorganic Phosphate and the 5‘-Phosphate Moiety of the Cofactor ^† Murray, Tracey Arnold; Swenson, Richard P. Biochemistry, Vol. 42, Issue 8 https://doi.org/10.1021/bi026967s	journal	March 2003
Covalent attachment of flavin adenine dinucleotide (FAD) and flavin mononucleotide (FMN) to enzymes: The current state of affairs Mewies, Martin; McIntire, William S.; Scrutton, Nigel S. Protein Science, Vol. 7, Issue 1 https://doi.org/10.1002/pro.5560070102	journal	January 1998
Covalently bound flavin in the NqrB and NqrC subunits of Na ⁺ -translocating NADH-quinone reductase from Vibrio alginolyticus Nakayama, Yuji; Yasui, Mikako; Sugahara, Kazuya FEBS Letters, Vol. 474, Issue 2-3 https://doi.org/10.1016/S0014-5793(00)01595-7	journal	May 2000
Purification and Characterization of the Recombinant Na ⁺ -Translocating NADH:Quinone Oxidoreductase from Vibrio cholerae ^† Barquera, Blanca; Hellwig, Petra; Zhou, Weidong Biochemistry, Vol. 41, Issue 11 https://doi.org/10.1021/bi011873o	journal	March 2002
Analysis of the structural consensus of the zinc coordination centers of metalloprotein structures Patel, Kirti; Kumar, Anil; Durani, Susheel Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1774, Issue 10 https://doi.org/10.1016/j.bbapap.2007.07.010	journal	October 2007
Sodium Ion Cycle in Bacterial Pathogens: Evidence from Cross-Genome Comparisons Hase, C. C.; Fedorova, N. D.; Galperin, M. Y. Microbiology and Molecular Biology Reviews, Vol. 65, Issue 3 https://doi.org/10.1128/MMBR.65.3.353-370.2001	journal	September 2001
NIH Image to ImageJ: 25 years of image analysis Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W. Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2089	journal	June 2012
Large shifts in pKa values of lysine residues buried inside a protein Isom, D. G.; Castaneda, C. A.; Cannon, B. R. Proceedings of the National Academy of Sciences, Vol. 108, Issue 13 https://doi.org/10.1073/pnas.1010750108	journal	March 2011
Acid Residues in the Transmembrane Helices of the Na ⁺ -Pumping NADH:Quinone Oxidoreductase from Vibrio cholerae Involved in Sodium Translocation Juárez, Oscar; Athearn, Kathleen; Gillespie, Portia Biochemistry, Vol. 48, Issue 40 https://doi.org/10.1021/bi900845y	journal	October 2009
Membrane proteins, lipids and detergents: not just a soap opera Seddon, Annela M.; Curnow, Paul; Booth, Paula J. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1666, Issue 1-2 https://doi.org/10.1016/j.bbamem.2004.04.011	journal	November 2004
Effects of changes in membrane sodium flux on virulence gene expression in Vibrio cholerae Hase, C. C.; Mekalanos, J. J. Proceedings of the National Academy of Sciences, Vol. 96, Issue 6 https://doi.org/10.1073/pnas.96.6.3183	journal	March 1999
Insights into the mechanism of electron transfer and sodium translocation of the Na+-pumping NADH:quinone oxidoreductase Juárez, Oscar; Barquera, Blanca Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 10 https://doi.org/10.1016/j.bbabio.2012.03.017	journal	October 2012
The TP0796 Lipoprotein of Treponema pallidum Is a Bimetal-dependent FAD Pyrophosphatase with a Potential Role in Flavin Homeostasis Deka, Ranjit K.; Brautigam, Chad A.; Liu, Wei Z. Journal of Biological Chemistry, Vol. 288, Issue 16 https://doi.org/10.1074/jbc.M113.449975	journal	February 2013
Dissecting the Energetics of the Apoflavodoxin-FMN Complex Lostao, Anabel; El Harrous, Mohamed; Daoudi, Fatna Journal of Biological Chemistry, Vol. 275, Issue 13 https://doi.org/10.1074/jbc.275.13.9518	journal	March 2000
YeeO from Escherichia coli exports flavins McAnulty, Michael J.; Wood, Thomas K. Bioengineered, Vol. 5, Issue 6 https://doi.org/10.4161/21655979.2014.969173	journal	November 2014
Functional Domains of NosR, a Novel Transmembrane Iron-Sulfur Flavoprotein Necessary for Nitrous Oxide Respiration Wunsch, P.; Zumft, W. G. Journal of Bacteriology, Vol. 187, Issue 6 https://doi.org/10.1128/jb.187.6.1992-2001.2005	journal	March 2005
FMN is covalently attached to a threonine residue in the NqrB and NqrC subunits of Na ⁺ -translocating NADH-quinone reductase from Vibrio alginolyticus Hayashi, Maki; Nakayama, Yuji; Yasui, Mikako FEBS Letters, Vol. 488, Issue 1-2 https://doi.org/10.1016/s0014-5793(00)02404-2	journal	January 2001
Two-Dimensional NMR-Studies of the Flavin Binding Site of Desulfovibrio vulgaris Flavodoxin in Its Threex States Peelen, S.; Vervoort, J. Archives of Biochemistry and Biophysics, Vol. 314, Issue 2 https://doi.org/10.1006/abbi.1994.1445	journal	November 1994
Coordination geometries of selected transition metal ions (Co2+, Ni2+, Cu2+, Zn2+, Cd2+, and Hg2+) in metalloproteins Rulı́šek, Lubomı́r; Vondrášek, Jiřı́ Journal of Inorganic Biochemistry, Vol. 71, Issue 3-4 https://doi.org/10.1016/S0162-0134(98)10042-9	journal	September 1998
Crystal structure of the ApbE protein (TM1553) from Thermotoga maritima at 1.58 Å resolution Han, Gye Won; Sri Krishna, S.; Schwarzenbacher, Robert Proteins: Structure, Function, and Bioinformatics, Vol. 64, Issue 4 https://doi.org/10.1002/prot.20950	journal	June 2006
Sodium-translocating NADH:quinone oxidoreductase as a redox-driven ion pump Verkhovsky, Michael I.; Bogachev, Alexander V. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 6-7 https://doi.org/10.1016/j.bbabio.2009.12.020	journal	June 2010
Chlamydia: Old Ideas Crushed, New Mysteries Bared Hatch, Thomas Science, Vol. 282, Issue 5389 https://doi.org/10.1126/science.282.5389.638	journal	October 1998
Role of exopolysaccharide, the rugose phenotype and VpsR in the pathogenesis of epidemic Vibrio cholerae Rashid, Mohammed H.; Rajanna, Chythanya; Zhang, Dalin FEMS Microbiology Letters, Vol. 230, Issue 1 https://doi.org/10.1016/s0378-1097(03)00879-6	journal	January 2004
The Kinetic Reaction Mechanism of the Vibrio cholerae Sodium-dependent NADH Dehydrogenase Tuz, Karina; Mezic, Katherine G.; Xu, Tianhao Journal of Biological Chemistry, Vol. 290, Issue 33 https://doi.org/10.1074/jbc.M115.658773	journal	May 2015
Biochemical Evidence That Berberine Bridge Enzyme Belongs to a Novel Family of Flavoproteins Containing a Bi-covalently Attached FAD Cofactor Winkler, Andreas; Hartner, Franz; Kutchan, Toni M. Journal of Biological Chemistry, Vol. 281, Issue 30 https://doi.org/10.1074/jbc.M603267200	journal	May 2006
Alternative Pyrimidine Biosynthesis Protein ApbE Is a Flavin Transferase Catalyzing Covalent Attachment of FMN to a Threonine Residue in Bacterial Flavoproteins Bertsova, Yulia V.; Fadeeva, Maria S.; Kostyrko, Vitaly A. Journal of Biological Chemistry, Vol. 288, Issue 20 https://doi.org/10.1074/jbc.m113.455402	journal	April 2013
What’s in a covalent bond?: On the role and formation of covalently bound flavin cofactors Heuts, Dominic P. H. M.; Scrutton, Nigel S.; McIntire, William S. FEBS Journal, Vol. 276, Issue 13 https://doi.org/10.1111/j.1742-4658.2009.07053.x	journal	June 2009
Studies on Succinate Dehydrogenase. 8alpha-Histidyl-FAD as the Active Center of Succinate Dehydrogenase Walker, Wolfram H.; Singer, Thomas P.; Ghisla, Sandro European Journal of Biochemistry, Vol. 26, Issue 2 https://doi.org/10.1111/j.1432-1033.1972.tb01766.x	journal	March 1972
Crystal Structure of 6-Hydroxy-d-nicotine Oxidase from Arthrobacter nicotinovorans Koetter, Jochen W. A.; Schulz, Georg E. Journal of Molecular Biology, Vol. 352, Issue 2 https://doi.org/10.1016/j.jmb.2005.07.041	journal	September 2005
Origin and Evolution of the Sodium -Pumping NADH: Ubiquinone Oxidoreductase Reyes-Prieto, Adrian; Barquera, Blanca; Juárez, Oscar PLoS ONE, Vol. 9, Issue 5 https://doi.org/10.1371/journal.pone.0096696	journal	May 2014
The Binding of Riboflavin-5'-Phosphate in a Flavoprotein: Flavodoxin at 2.0-A Resolution Watenpaugh, K. D.; Sieker, L. C.; Jensen, L. H. Proceedings of the National Academy of Sciences, Vol. 70, Issue 12 https://doi.org/10.1073/pnas.70.12.3857	journal	December 1973
TcpP protein is a positive regulator of virulence gene expression in Vibrio cholerae Hase, C. C.; Mekalanos, J. J. Proceedings of the National Academy of Sciences, Vol. 95, Issue 2 https://doi.org/10.1073/pnas.95.2.730	journal	January 1998
Optical absorption of divalent metal tungstates: Correlation between the band-gap energy and the cation ionic radius Lacomba-Perales, R.; Ruiz-Fuertes, J.; Errandonea, D. arXiv https://doi.org/10.48550/arxiv.0807.2115	text	January 2008
A Periplasmic Location Is Essential for the Role of the ApbE Lipoprotein in Thiamine Synthesis in Salmonella typhimurium Beck, Brian J.; Downs, Diana M. Journal of Bacteriology, Vol. 181, Issue 23 https://doi.org/10.1128/JB.181.23.7285-7290.1999	journal	December 1999
Multidrug efflux transporters in the MATE family Kuroda, Teruo; Tsuchiya, Tomofusa Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1794, Issue 5 https://doi.org/10.1016/j.bbapap.2008.11.012	journal	May 2009
Acid-Base Disturbances in Gastrointestinal Disease Gennari, F. John; Weise, Wolfgang J. Clinical Journal of the American Society of Nephrology, Vol. 3, Issue 6 https://doi.org/10.2215/cjn.02450508	journal	October 2008
Aspartic Acid 397 in Subunit B of the Na ⁺ -pumping NADH:Quinone Oxidoreductase from Vibrio cholerae Forms Part of a Sodium-binding Site, Is Involved in Cation Selectivity, and Affects Cation-binding Site Cooperativity Shea, Michael E.; Juárez, Oscar; Cho, Jonathan Journal of Biological Chemistry, Vol. 288, Issue 43 https://doi.org/10.1074/jbc.m113.510776	journal	September 2013
Cell Vacuolation Caused by Vibrio cholerae Hemolysin Figueroa-Arredondo, P.; Heuser, J. E.; Akopyants, N. S. Infection and Immunity, Vol. 69, Issue 3 https://doi.org/10.1128/iai.69.3.1613-1624.2001	journal	March 2001
The complete general secretory pathway in gram-negative bacteria Pugsley, A. P. Microbiological Reviews, Vol. 57, Issue 1 https://doi.org/10.1128/mr.57.1.50-108.1993	journal	March 1993
Crystal Structure of Glucooligosaccharide Oxidase from Acremonium strictum : A NOVEL FLAVINYLATION OF 6-S-CYSTEINYL, 8α-N1-HISTIDYL FAD Huang, Chun-Hsiang; Lai, Wen-Lin; Lee, Meng-Hwan Journal of Biological Chemistry, Vol. 280, Issue 46 https://doi.org/10.1074/jbc.M506078200	journal	September 2005
Generating disulfides enzymatically: Reaction products and electron acceptors of the endoplasmic reticulum thiol oxidase Ero1p Gross, E.; Sevier, C. S.; Heldman, N. Proceedings of the National Academy of Sciences, Vol. 103, Issue 2 https://doi.org/10.1073/pnas.0506448103	journal	January 2006
The apbE Gene Encodes a Lipoprotein Involved in Thiamine Synthesis in Salmonella typhimurium Beck, Brian J.; Downs, Diana M. Journal of Bacteriology, Vol. 180, Issue 4 https://doi.org/10.1128/JB.180.4.885-891.1998	journal	February 1998
A novel pH- and time-based multi-unit potential colonic drug delivery system. I. Development Gupta, Vishal K.; Beckert, Thomas E.; Price, James C. International Journal of Pharmaceutics, Vol. 213, Issue 1-2 https://doi.org/10.1016/s0378-5173(00)00649-9	journal	February 2001
Expression and mutagenesis of the NqrC subunit of the NQR respiratory Na ⁺ pump from Vibrio cholerae with covalently attached FMN Barquera, Blanca; Häse, Claudia C.; Gennis, Robert B. FEBS Letters, Vol. 492, Issue 1-2 https://doi.org/10.1016/s0014-5793(01)02224-4	journal	March 2001
Covalent Binding of Flavins to RnfG and RnfD in the Rnf Complex from Vibrio cholerae ^† Backiel, Julianne; Zagorevski, Dmitri V.; Wang, Zhenyu Biochemistry, Vol. 47, Issue 43 https://doi.org/10.1021/bi800920j	journal	October 2008
The complete general secretory pathway in gram-negative bacteria. Pugsley, A. P. Microbiological Reviews, Vol. 57, Issue 1 https://doi.org/10.1128/MMBR.57.1.50-108.1993	journal	January 1993
Structure of the Flavocoenzyme of Two Homologous Amine Oxidases: Monomeric Sarcosine Oxidase and N -Methyltryptophan Oxidase ^† Wagner, Mary Ann; Khanna, Peeyush; Jorns, Marilyn Schuman Biochemistry, Vol. 38, Issue 17 https://doi.org/10.1021/bi982955o	journal	April 1999
Mechanisms of flavoprotein-catalyzed reactions Ghisla, Sandro; Massey, Vincent European Journal of Biochemistry, Vol. 181, Issue 1 https://doi.org/10.1111/j.1432-1033.1989.tb14688.x	journal	April 1989
Structure of the V. cholerae Na+-pumping NADH:quinone oxidoreductase Steuber, Julia; Vohl, Georg; Casutt, Marco S. Nature, Vol. 516, Issue 7529 https://doi.org/10.1038/nature14003	journal	December 2014
Entero-Cytolysin (EC) from Vibrio cholerae Non-01 (Some Properties and Pore-Forming Activity) Zitzer, A. O.; Nakisbekov, N. O.; Li, A. V. Zentralblatt für Bakteriologie, Vol. 279, Issue 4 https://doi.org/10.1016/S0934-8840(11)80421-4	journal	November 1993
The origin of the sodium-dependent NADH oxidation by the respiratory chain of Klebsiella pneumoniae Bertsova, Yulia V.; Bogachev, Alexander V. FEBS Letters, Vol. 563, Issue 1-3 https://doi.org/10.1016/s0014-5793(04)00312-6	journal	April 2004
Role of sodium bioenergetics in Vibrio cholerae Häse, Claudia C.; Barquera, Blanca Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1505, Issue 1 https://doi.org/10.1016/s0005-2728(00)00286-3	journal	May 2001
FAD Binding by ApbE Protein from Salmonella enterica: a New Class of FAD-Binding Proteins Boyd, J. M.; Endrizzi, J. A.; Hamilton, T. L. Journal of Bacteriology, Vol. 193, Issue 4 https://doi.org/10.1128/jb.00730-10	journal	December 2010
Genome Sequence of an Obligate Intracellular Pathogen of Humans: Chlamydia trachomatis Stephens, R. S. Science, Vol. 282, Issue 5389 https://doi.org/10.1126/science.282.5389.754	journal	October 1998
Metallobiochemistry of magnesium. Coordination complexes with biological substrates: site specificity, kinetics and thermodynamics of binding, and implications for activity Cowan, J. A. Inorganic Chemistry, Vol. 30, Issue 13 https://doi.org/10.1021/ic00013a008	journal	June 1991
Flavin Electron Shuttles Dominate Extracellular Electron Transfer by Shewanella oneidensis Kotloski, Nicholas J.; Gralnick, Jeffrey A. mBio, Vol. 4, Issue 1 https://doi.org/10.1128/mBio.00553-12	journal	January 2013
Structure of the covalently bound coenzyme of trimethylamine dehydrogenase. Evidence for a 6-substituted flavin. Steenkamp, D. J.; McIntire, W.; Kenney, W. C. Journal of Biological Chemistry, Vol. 253, Issue 8 https://doi.org/10.1016/S0021-9258(17)40896-9	journal	April 1978

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