Biosynthesis of the Urease Metallocenter

Journal of Biological Chemistry - Tập 288 - Trang 13178-13185 - 2013
Mark A. Farrugia1, Lee Macomber2, Robert P. Hausinger1,2
1Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan, 48824
2Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan 48824

Tài liệu tham khảo

Scott, 2002, Mechanisms of acid resistance due to the urease system of Helicobacter pylori, Gastroenterology, 123, 187, 10.1053/gast.2002.34218 Nielubowicz, 2010, Host-pathogen interactions in the urinary tract interaction, Nat. Rev. Urol, 7, 430, 10.1038/nrurol.2010.101 Witte, 2011, Urea metabolism in plants, Plant Sci, 180, 431, 10.1016/j.plantsci.2010.11.010 Bremner, 1995, Recent research on problems in the use of urea as a nitrogen fertilizer, Fertilizer Res, 42, 321, 10.1007/BF00750524 Sumner, 1926, The isolation and crystallization of the enzyme urease, J. Biol. Chem, 69, 435, 10.1016/S0021-9258(18)84560-4 Dixon, 1975, Jack bean urease (EC 3.5.1.5). A metalloenzyme. A simple biological role for nickel?, J. Am. Chem. Soc, 97, 4131, 10.1021/ja00847a045 Carter, 2009, Interplay of metal ions and urease, Metallomics, 1, 207, 10.1039/b903311d Krajewska, 2009, Ureases I. Functional, catalytic and kinetic properties: a review, J. Mol. Catal. B Enzym, 59, 9, 10.1016/j.molcatb.2009.01.003 Zambelli, 2011, Chemistry of Ni2+ in urease: sensing, trafficking, and catalysis, Acc. Chem. Res, 44, 520, 10.1021/ar200041k Jabri, 1995, The crystal structure of urease from Klebsiella aerogenes, Science, 268, 998, 10.1126/science.7754395 Pearson, 1997, Structure of Cys319 variants and acetohydroxamate-inhibited Klebsiella aerogenes urease, Biochemistry, 36, 8164, 10.1021/bi970514j Benini, 1999, A new proposal for urease mechanism based on the crystal structures of the native and inhibited enzyme from Bacillus pasteurii: why urea hydrolysis costs two nickels, Structure, 7, 205, 10.1016/S0969-2126(99)80026-4 Ha, 2001, Supramolecular assembly and acid resistance of Helicobacter pylori urease, Nat. Struct. Biol, 8, 505, 10.1038/88563 Balasubramanian, 2010, Crystal structure of the first plant urease from jack bean: 83 years of journey from its first crystal to molecular structure, J. Mol. Biol, 400, 274, 10.1016/j.jmb.2010.05.009 Estiu, 2006, Catalyzed decomposition of urea. Molecular dynamics simulations of the binding of urea to urease, Biochemistry, 45, 4429, 10.1021/bi052020p Estiu, 2007, Competitive hydrolytic and elimination mechanisms in the urease catalyzed decomposition of urea, J. Phys. Chem. B, 111, 10263, 10.1021/jp072323o Carlsson, 2010, Computational modeling of the mechanism of urease, Bioinorg. Chem. Appl, 2010, 364891, 10.1155/2010/364891 Mulrooney, 1990, Sequence of the Klebsiella aerogenes urease genes and evidence for accessory proteins facilitating nickel incorporation, J. Bacteriol, 172, 5837, 10.1128/jb.172.10.5837-5843.1990 Lee, 1992, Klebsiella aerogenes urease gene cluster: sequence of ureD and demonstration that four accessory genes (ureDureEureFureG) are involved in nickel metallocenter biosynthesis, J. Bacteriol, 174, 4324, 10.1128/jb.174.13.4324-4330.1992 Mobley, 1995, Molecular biology of microbial ureases, Microbiol. Rev, 59, 451, 10.1128/mr.59.3.451-480.1995 Cussac, 1992, Expression of Helicobacter pylori urease genes in Escherichia coli grown under nitrogen-limiting conditions, J. Bacteriol, 174, 2466, 10.1128/jb.174.8.2466-2473.1992 Bacanamwo, 2002, Activation of the urease of Schizosaccharomyces pombe by the UreF accessory protein from soybean, Mol. Genet. Genomics, 268, 525, 10.1007/s00438-002-0769-z Polacco, 2013, Opinion–nickel and urease in plants: still many knowledge gaps, Plant Sci, 199–200, 79, 10.1016/j.plantsci.2012.10.010 Park, 1994, In vitro activation of urease apoprotein and role of UreD as a chaperone required for nickel metallocenter assembly, Proc. Natl. Acad. Sci. U.S.A, 91, 3233, 10.1073/pnas.91.8.3233 Fong, 2011, Assembly of the preactivation complex for urease maturation in Helicobacter pylori. Crystal structure of the UreF-UreH protein complex, J. Biol. Chem, 286, 43241, 10.1074/jbc.M111.296830 Carter, 2010, Characterization of Klebsiella aerogenes urease accessory protein UreD in fusion with the maltose binding protein, J. Bacteriol, 192, 2294, 10.1128/JB.01426-09 Wollers, 2010, Iron-sulfur (Fe-S) cluster assembly. The SufBCD complex is a new type of Fe-S scaffold with a flavin redox cofactor, J. Biol. Chem, 285, 23331, 10.1074/jbc.M110.127449 Ligabue-Braun, 2012, Evidence-based docking of the urease activation complex, J. Biomol. Struct. Dyn Quiroz-Valenzuela, 2008, The structure of urease activation complexes examined by flexibility analysis, mutagenesis, and small-angle X-ray scattering, Arch. Biochem. Biophys, 480, 51, 10.1016/j.abb.2008.09.004 Chang, 2004, Chemical cross-linking and mass spectrometric identification of sites of interaction for UreD, UreF, and urease, J. Biol. Chem, 279, 15305, 10.1074/jbc.M312979200 Rain, 2001, The protein-protein interaction map of Helicobacter pylori, Nature, 409, 211, 10.1038/35051615 Voland, 2003, Interactions among the seven Helicobacter pylori proteins encoded by the urease gene cluster, Am. J. Physiol. Gastrointest. Liver Physiol, 284, G96, 10.1152/ajpgi.00160.2002 Park, 1995, Requirement of carbon dioxide for in vitro assembly of the urease nickel metallocenter, Science, 267, 1156, 10.1126/science.7855593 Park, 1996, Metal ion interactions with urease and UreD-urease apoproteins, Biochemistry, 35, 5345, 10.1021/bi952894j Moncrief, 1996, Purification and activation properties of UreD-UreF-urease apoprotein complexes, J. Bacteriol, 178, 5417, 10.1128/jb.178.18.5417-5421.1996 Kim, 1999, Expression of the recombinant Klebsiella aerogenes UreF protein as a MalE fusion, Arch. Pharm. Res, 22, 274, 10.1007/BF02976362 Kim, 2006, The UreEF fusion protein provides a soluble and functional form of the UreF urease accessory protein, J. Bacteriol, 188, 8413, 10.1128/JB.01265-06 Lam, 2010, Crystal structure of a truncated urease accessory protein UreF from Helicobacter pylori, Proteins, 78, 2839, 10.1002/prot.22802 Stingl, 2008, In vivo interactome of Helicobacter pylori urease revealed by tandem affinity purification, Mol. Cell. Proteomics, 7, 2429, 10.1074/mcp.M800160-MCP200 Carter, 2011, Function of UreB in Klebsiella aerogenes urease, Biochemistry, 50, 9296, 10.1021/bi2011064 Salomone-Stagni, 2007, A model-based proposal for the role of UreF as a GTPase-activating protein in the urease active site biosynthesis, Proteins, 68, 749, 10.1002/prot.21472 Boer, 2012, Klebsiella aerogenes UreF: identification of the UreG binding site and role in enhancing the fidelity of urease activation, Biochemistry, 51, 2298, 10.1021/bi3000897 Moncrief, 1997, Characterization of UreG, identification of a UreD-UreF-UreG complex, and evidence suggesting that a nucleotide-binding site in UreG is required for in vivo metallocenter assembly of Klebsiella aerogenes urease, J. Bacteriol, 179, 4081, 10.1128/jb.179.13.4081-4086.1997 Zambelli, 2005, UreG, a chaperone in the urease assembly process, is an intrinsically unstructured GTPase that specifically binds Zn2+, J. Biol. Chem, 280, 4684, 10.1074/jbc.M408483200 Zambelli, 2007, Biochemical studies on Mycobacterium tuberculosis UreG and comparative modeling reveal structural and functional conservation among the bacterial UreG family, Biochemistry, 46, 3171, 10.1021/bi6024676 Zambelli, 2009, Zn2+-linked dimerization of UreG from Helicobacter pylori, a chaperone involved in nickel trafficking and urease activation, Proteins, 74, 222, 10.1002/prot.22205 Real-Guerra, 2012, Biochemical and structural studies on native and recombinant Glycine max UreG: a detailed characterization of a plant urease accessory gene, Plant Mol. Biol, 78, 461, 10.1007/s11103-012-9878-1 Boer, 2010, Mutagenesis of Klebsiella aerogenes UreG to probe nickel binding and interactions with other urease-related proteins, Biochemistry, 49, 5859, 10.1021/bi1004987 Martin-Diaconescu, 2012, Unraveling the Helicobacter pylori UreG zinc binding site using x-ray absorption spectroscopy (XAS) and structural modeling, J. Biol. Inorg. Chem, 17, 353, 10.1007/s00775-011-0857-9 Zambelli, 2012, Insights in the (un)structural organization of Bacillus pasteurii UreG, an intrinsically disordered GTPase enzyme, Mol. Biosyst, 8, 220, 10.1039/C1MB05227F Kaluarachchi, 2010, Microbial nickel proteins, Nat. Prod. Rep, 27, 681, 10.1039/b906688h Higgins, 2012, Specific metal recognition in nickel trafficking, Biochemistry, 51, 7816, 10.1021/bi300981m Gasper, 2006, Structural insights into HypB, a GTP-binding protein that regulates metal binding, J. Biol. Chem, 281, 27492, 10.1074/jbc.M600809200 Soriano, 1999, GTP-dependent activation of urease apoprotein in complex with the UreD, UreF, and UreG accessory proteins, Proc. Natl. Acad. Sci. U.S.A, 96, 11140, 10.1073/pnas.96.20.11140 Mehta, 2003, Roles of conserved nucleotide-binding domains in accessory proteins, HypB and UreG, in the maturation of nickel-enzymes required for efficient Helicobacter pylori colonization, Microb. Pathog, 35, 229, 10.1016/S0882-4010(03)00151-7 Park, 1995, Evidence for the presence of urease apoprotein complexes containing UreD, UreF, and UreG in cells that are competent for in vivo enzyme activation, J. Bacteriol, 177, 1947, 10.1128/jb.177.8.1947-1951.1995 Lee, 1993, Purification and characterization of Klebsiella aerogenes UreE protein: a nickel-binding protein that functions in urease metallocenter assembly, Protein Sci, 2, 1042, 10.1002/pro.5560020617 Musiani, 2004, Nickel trafficking: insights into the fold and function of UreE, a urease metallochaperone, J. Inorg. Biochem, 98, 803, 10.1016/j.jinorgbio.2003.12.012 Brayman, 1996, Purification, characterization, and functional analysis of a truncated Klebsiella aerogenes UreE urease accessory protein lacking the histidine-rich carboxyl terminus, J. Bacteriol, 178, 5410, 10.1128/jb.178.18.5410-5416.1996 Song, 2001, Crystal structure of Klebsiella aerogenes UreE, a nickel-binding metallochaperone for urease activation, J. Biol. Chem, 276, 49359, 10.1074/jbc.M108619200 Grossoehme, 2007, Thermodynamics of Ni2+, Cu2+, and Zn2+ binding to urease metallochaperone UreE, Biochemistry, 46, 10506, 10.1021/bi700171v Colpas, 1999, Identification of metal-binding residues in the Klebsiella aerogenes urease nickel metallochaperone, UreE, Biochemistry, 38, 4078, 10.1021/bi982435t Remaut, 2001, Structural basis for Ni2+ transport and assembly of the urease active site by the metallochaperone UreE from Bacillus pasteurii, J. Biol. Chem, 276, 49365, 10.1074/jbc.M108304200 Banaszak, 2012, Crystallographic and x-ray absorption spectroscopic characterization of Helicobacter pylori UreE bound to Ni2+ and Zn2+ reveals a role for the disordered C-terminal arm in metal trafficking, Biochem. J, 441, 1017, 10.1042/BJ20111659 Shi, 2010, Crystal structures of apo and metal-bound forms of the UreE protein from Helicobacter pylori: role of multiple metal binding sites, Biochemistry, 49, 7080, 10.1021/bi100372h Bellucci, 2009, Helicobacter pylori UreE, a urease accessory protein: specific Ni2+- and Zn2+ -binding properties and interaction with its cognate UreG, Biochem. J, 422, 91, 10.1042/BJ20090434 Soriano, 2000, UreE stimulation of GTP-dependent urease activation in the UreD-UreF-UreG-urease apoprotein complex, Biochemistry, 39, 12435, 10.1021/bi001296o Sebbane, 2002, Genes encoding specific nickel transport systems flank the chromosomal urease locus of pathogenic Yersiniae, J. Bacteriol, 184, 5706, 10.1128/JB.184.20.5706-5713.2002 Bossé, 2001, Novel genes affecting urease activity in Actinobacillus pleuropneumoniae, J. Bacteriol, 183, 1242, 10.1128/JB.183.4.1242-1247.2001 Maeda, 1994, Cloning, sequencing, and expression of thermophilic Bacillus sp. strain TB-90 urease gene complex in Escherichia coli, J. Bacteriol, 176, 432, 10.1128/jb.176.2.432-442.1994 Rodionov, 2006, Comparative and functional genomic analysis of prokaryotic nickel and cobalt uptake transporters: evidence for a novel group of ATP-binding cassette transporters, J. Bacteriol, 188, 317, 10.1128/JB.188.1.317-327.2006 Mulrooney, 2003, Nickel uptake and utilization by microorganisms, FEMS Microbiol. Rev, 27, 239, 10.1016/S0168-6445(03)00042-1 Bauerfeind, 1996, Allelic exchange mutagenesis of nixA in Helicobacter pylori results in reduced nickel transport and urease activity, Infect. Immun, 64, 2877, 10.1128/iai.64.7.2877-2880.1996 Hendricks, 1997, Helicobacter pylori ABC transporter: effect of allelic exchange mutagenesis on urease activity, J. Bacteriol, 179, 5892, 10.1128/jb.179.18.5892-5902.1997 Davis, 2006, Helicobacter pylori HP1512 is a nickel-responsive NikR-regulated outer membrane protein, Infect. Immun, 74, 6811, 10.1128/IAI.01188-06 Schauer, 2007, Novel nickel transport mechanism across the bacterial outer membrane energized by the TonB/ExbB/ExbD machinery, Mol. Microbiol, 63, 1054, 10.1111/j.1365-2958.2006.05578.x Olson, 2001, Requirement of nickel metabolism proteins HypA and HypB for full activity of both hydrogenase and urease in Helicobacter pylori, Mol. Microbiol, 39, 176, 10.1046/j.1365-2958.2001.02244.x Benoit, 2012, Helicobacter pylori hydrogenase accessory protein HypA and urease accessory protein UreG compete with each other for UreE recognition, Biochim. Biophys. Acta, 1820, 1519, 10.1016/j.bbagen.2012.06.002 Mizuki, 2004, Ureases of extreme halophiles of the genus Haloarcula with a unique structure of gene cluster, Biosci. Biotechnol. Biochem, 68, 397, 10.1271/bbb.68.397 Kim, 2005, Biosynthesis of active Bacillus subtilis urease in the absence of known urease accessory proteins, J. Bacteriol, 187, 7150, 10.1128/JB.187.20.7150-7154.2005 O'Toole, 2010, Comparative genomics and proteomics of Helicobacter mustelae, an ulcerogenic and carcinogenic gastric pathogen, BMC Genomics, 11, 164, 10.1186/1471-2164-11-164 Strugatsky, 2013, Structure of the proton-gated urea channel from the gastric pathogen Helicobacter pylori, Nature, 493, 255, 10.1038/nature11684 Stoof, 2008, Inverse nickel-responsive regulation of two urease enzymes in the gastric pathogen Helicobacter mustelae, Environ. Microbiol, 10, 2586, 10.1111/j.1462-2920.2008.01681.x Carter, 2011, Iron-containing urease in a pathogenic bacterium, Proc. Natl. Acad. Sci. U.S.A, 108, 13095, 10.1073/pnas.1106915108 Carter, 2012, Apoprotein isolation and activation, and vibrational structure of the Helicobacter mustelae iron urease, J. Inorg. Biochem, 111, 195, 10.1016/j.jinorgbio.2011.10.016