{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T13:37:51Z","timestamp":1790861871091,"version":"4.1.0"},"reference-count":45,"publisher":"Portland Press Ltd.","issue":"3","content-domain":{"domain":["portlandpress.com"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2012,2,1]]},"abstract":"<jats:p>The survival and growth of the pathogen Helicobacter pylori in the gastric acidic environment is ensured by the activity of urease, an enzyme containing two essential Ni2+ ions in the active site. The metallo-chaperone UreE facilitates in vivo Ni2+ insertion into the apoenzyme. Crystals of apo-HpUreE (H. pylori UreE) and its Ni2+- and Zn2+-bound forms were obtained from protein solutions in the absence and presence of the metal ions. The crystal structures of the homodimeric protein, determined at 2.00 \u00c5 (apo), 1.59 \u00c5 (Ni2+) and 2.52 \u00c5 (Zn2+) resolution, show the conserved proximal and solvent-exposed His102 residues from two adjacent monomers invariably involved in metal binding. The C-terminal regions of the apoprotein are disordered in the crystal, but acquire significant ordering in the presence of the metal ions due to the binding of His152. The analysis of X-ray absorption spectral data obtained using solutions of Ni2+- and Zn2+-bound HpUreE provided accurate information of the metal-ion environment in the absence of solid-state effects. These results reveal the role of the histidine residues at the protein C-terminus in metal-ion binding, and the mutual influence of protein framework and metal-ion stereo-electronic properties in establishing co-ordination number and geometry leading to metal selectivity.<\/jats:p>","DOI":"10.1042\/bj20111659","type":"journal-article","created":{"date-parts":[[2011,10,21]],"date-time":"2011-10-21T08:19:45Z","timestamp":1319185185000},"page":"1017-1035","update-policy":"https:\/\/doi.org\/10.1042\/crossmark_policy","source":"Crossref","is-referenced-by-count":62,"title":["Crystallographic and X-ray absorption spectroscopic characterization of <i>Helicobacter pylori<\/i> UreE bound to Ni2+ and Zn2+ reveals a role for the disordered C-terminal arm in metal trafficking"],"prefix":"10.1042","volume":"441","author":[{"given":"Katarzyna","family":"Banaszak","sequence":"first","affiliation":[{"name":"Institute of Bioorganic Chemistry, Polish Academy of Sciences, Noskowskiego 12\/14, 61-704 Poznan, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vlad","family":"Martin-Diaconescu","sequence":"additional","affiliation":[{"name":"Department of Chemistry, University of Massachusetts, Amherst, MA 01003, U.S.A."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Matteo","family":"Bellucci","sequence":"additional","affiliation":[{"name":"Laboratory of Bioinorganic Chemistry, Department of Agro-Environmental Science and Technology, University of Bologna, Viale G. Fanin 40, 40127 Bologna, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Barbara","family":"Zambelli","sequence":"additional","affiliation":[{"name":"Laboratory of Bioinorganic Chemistry, Department of Agro-Environmental Science and Technology, University of Bologna, Viale G. Fanin 40, 40127 Bologna, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wojciech","family":"Rypniewski","sequence":"additional","affiliation":[{"name":"Institute of Bioorganic Chemistry, Polish Academy of Sciences, Noskowskiego 12\/14, 61-704 Poznan, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael\u00a0J.","family":"Maroney","sequence":"additional","affiliation":[{"name":"Department of Chemistry, University of Massachusetts, Amherst, MA 01003, U.S.A."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stefano","family":"Ciurli","sequence":"additional","affiliation":[{"name":"Laboratory of Bioinorganic Chemistry, Department of Agro-Environmental Science and Technology, University of Bologna, Viale G. Fanin 40, 40127 Bologna, Italy"},{"name":"Center for Magnetic Resonance (CERM), University of Florence, Via Luigi Sacconi 6, I-50019 Sesto Fiorentino, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"288","published-online":{"date-parts":[[2012,1,16]]},"reference":[{"key":"2021112215392614000_B1","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1039\/b903311d","article-title":"Interplay of metal ions and urease","volume":"1","author":"Carter","year":"2009","journal-title":"Metallomics"},{"key":"2021112215392614000_B2","doi-asserted-by":"crossref","first-page":"520","DOI":"10.1021\/ar200041k","article-title":"Chemistry of Ni2+ in urease: sensing, trafficking, and catalysis","volume":"44","author":"Zambelli","year":"2011","journal-title":"Acc. Chem. Res."},{"key":"2021112215392614000_B3","doi-asserted-by":"crossref","first-page":"10828","DOI":"10.1021\/ja0525399","article-title":"The burden borne by urease","volume":"127","author":"Callahan","year":"2005","journal-title":"J. Am. Chem. Soc."},{"key":"2021112215392614000_B4","doi-asserted-by":"crossref","first-page":"998","DOI":"10.1126\/science.7754395","article-title":"The crystal structure of urease from Klebsiella aerogenes","volume":"268","author":"Jabri","year":"1995","journal-title":"Science"},{"key":"2021112215392614000_B5","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1016\/S0969-2126(99)80026-4","article-title":"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","volume":"7","author":"Benini","year":"1999","journal-title":"Structure"},{"key":"2021112215392614000_B6","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1038\/88563","article-title":"Supramolecular assembly and acid resistance of Helicobacter pylori urease","volume":"8","author":"Ha","year":"2001","journal-title":"Nat. Struct. Biol."},{"key":"2021112215392614000_B7","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1016\/j.jmb.2010.05.009","article-title":"Crystal structure of the first plant urease from jack bean: 83\u00a0years of journey from its first crystal to molecular structure","volume":"400","author":"Balasubramanian","year":"2010","journal-title":"J. Mol. Biol."},{"key":"2021112215392614000_B8","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1002\/9780470028131.ch14","article-title":"Chaperones of nickel metabolism","volume-title":"Nickel and its Surprising Impact in Nature","author":"Quiroz","year":"2007"},{"key":"2021112215392614000_B9","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1128\/mr.53.1.85-108.1989","article-title":"Microbial urease: significance, regulation and molecular characterization","volume":"53","author":"Mobley","year":"1989","journal-title":"Microbiol. Rev."},{"key":"2021112215392614000_B10","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1128\/mr.59.3.451-480.1995","article-title":"Molecular biology of microbial ureases","volume":"59","author":"Mobley","year":"1995","journal-title":"Microbiol. Rev."},{"key":"2021112215392614000_B11","doi-asserted-by":"crossref","first-page":"5345","DOI":"10.1021\/bi952894j","article-title":"Metal ion interactions with urease and UreD\u2013urease apoproteins","volume":"35","author":"Park","year":"1996","journal-title":"Biochemistry"},{"key":"2021112215392614000_B12","doi-asserted-by":"crossref","first-page":"1156","DOI":"10.1126\/science.7855593","article-title":"Requirement of carbon dioxide for in vitro assembly of the urease nickel metallocenter","volume":"267","author":"Park","year":"1995","journal-title":"Science"},{"key":"2021112215392614000_B13","doi-asserted-by":"crossref","first-page":"12435","DOI":"10.1021\/bi001296o","article-title":"UreE stimulation of GTP-dependent urease activation in the UreD\u2013UreF\u2013UreG\u2013urease apoprotein complex","volume":"39","author":"Soriano","year":"2000","journal-title":"Biochemistry"},{"key":"2021112215392614000_B14","doi-asserted-by":"crossref","first-page":"4324","DOI":"10.1128\/jb.174.13.4324-4330.1992","article-title":"Klebsiella aerogenes urease gene cluster: sequence of ureD and demonstration that four accessory genes (ureD, ureE, ureF, ureG) are involved in nickel metallocenter biosynthesis","volume":"174","author":"Lee","year":"1992","journal-title":"J. Bacteriol."},{"key":"2021112215392614000_B15","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1042\/BJ20090434","article-title":"Helicobacter pylori UreE, a urease accessory protein: specific Ni2+ and Zn2+ binding properties and interaction with its cognate UreG","volume":"422","author":"Bellucci","year":"2009","journal-title":"Biochem. J."},{"key":"2021112215392614000_B16","doi-asserted-by":"crossref","first-page":"5859","DOI":"10.1021\/bi1004987","article-title":"Mutagenesis of Klebsiella aerogenes UreG to probe nickel binding and interactions with other urease-related proteins","volume":"49","author":"Boer","year":"2010","journal-title":"Biochemistry"},{"key":"2021112215392614000_B17","doi-asserted-by":"crossref","first-page":"49359","DOI":"10.1074\/jbc.M108619200","article-title":"Crystal structure of Klebsiella aerogenes UreE, a nickel-binding metallochaperone for urease activation","volume":"276","author":"Song","year":"2001","journal-title":"J. Biol. Chem."},{"key":"2021112215392614000_B18","doi-asserted-by":"crossref","first-page":"49365","DOI":"10.1074\/jbc.M108304200","article-title":"Structural basis for Ni2+ transport and assembly of the urease active site by the metallochaperone UreE from Bacillus pasteurii","volume":"276","author":"Remaut","year":"2001","journal-title":"J. Biol. Chem."},{"key":"2021112215392614000_B19","doi-asserted-by":"crossref","first-page":"7080","DOI":"10.1021\/bi100372h","article-title":"Crystal structures of apo and metal-bound forms of the UreE protein from Helicobacter pylori: role of multiple metal binding sites","volume":"49","author":"Shi","year":"2010","journal-title":"Biochemistry"},{"key":"2021112215392614000_B20","doi-asserted-by":"crossref","first-page":"4787","DOI":"10.1128\/JB.185.16.4787-4795.2003","article-title":"Dependence of Helicobacter pylori urease activity on the nickel-sequestering ability of the UreE accessory protein","volume":"185","author":"Benoit","year":"2003","journal-title":"J. Bacteriol."},{"key":"2021112215392614000_B21","doi-asserted-by":"crossref","first-page":"1042","DOI":"10.1002\/pro.5560020617","article-title":"Purification and characterization of Klebsiella aerogenes UreE protein: a nickel binding protein that functions in urease metallocenter assembly","volume":"2","author":"Lee","year":"1993","journal-title":"Protein Sci."},{"key":"2021112215392614000_B22","doi-asserted-by":"crossref","first-page":"6495","DOI":"10.1021\/bi0601003","article-title":"The nickel site of Bacillus pasteurii UreE, a urease metallo-chaperone, as revealed by metal-binding studies and X-ray absorption spectroscopy","volume":"45","author":"Stola","year":"2006","journal-title":"Biochemistry"},{"key":"2021112215392614000_B23","doi-asserted-by":"crossref","first-page":"803","DOI":"10.1016\/j.jinorgbio.2003.12.012","article-title":"Nickel trafficking: insights into the fold and function of UreE, a urease metallochaperone","volume":"98","author":"Musiani","year":"2004","journal-title":"J. Inorg. Biochem."},{"key":"2021112215392614000_B24","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1016\/S0076-6879(97)76066-X","article-title":"Processing of X-ray diffraction data collected in oscillation mode","volume":"276","author":"Otwinowski","year":"1997","journal-title":"Methods Enzymol."},{"key":"2021112215392614000_B25","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1107\/S0907444905001307","article-title":"Auto-Rickshaw: an automated crystal structure determination platform as an efficient tool for the validation of an X-ray diffraction experiment","volume":"61","author":"Panjikar","year":"2005","journal-title":"Acta Crystallogr. Sect. D Biol. Crystallogr."},{"key":"2021112215392614000_B26","doi-asserted-by":"crossref","first-page":"1772","DOI":"10.1107\/S0907444902011678","article-title":"Substructure solution with SHELXD","volume":"58","author":"Schneider","year":"2002","journal-title":"Acta Crystallogr. Sect. D Biol. Crystallogr."},{"key":"2021112215392614000_B27","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1016\/S0076-6879(97)76073-7","article-title":"Maximum-likelihood heavy-atom parameter refinement for the MIR and MAD methods","volume":"276","author":"de la Fortelle","year":"1997","journal-title":"Methods Enzymol."},{"key":"2021112215392614000_B28","first-page":"34","article-title":"An automated procedure for phase improvement by density modification. Joint CCP4 ESF-EACBM Newsl","volume":"31","author":"Cowtan","year":"1994","journal-title":"Protein Crystallogr."},{"key":"2021112215392614000_B29","doi-asserted-by":"crossref","first-page":"965","DOI":"10.1107\/S0907444900005072","article-title":"Maximum-likelihood density modification","volume":"56","author":"Terwilliger","year":"2000","journal-title":"Acta Crystallogr. Sect. D Biol. Crystallogr."},{"key":"2021112215392614000_B30","doi-asserted-by":"crossref","first-page":"458","DOI":"10.1038\/8263","article-title":"Automated protein model building combined with iterative structure refinement","volume":"6","author":"Perrakis","year":"1999","journal-title":"Nat. Struct. Biol."},{"key":"2021112215392614000_B31","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1107\/S090904950302394X","article-title":"Breaking good resolutions with ARP\/wARP","volume":"11","author":"Morris","year":"2004","journal-title":"J. Synchrotron Radiat."},{"key":"2021112215392614000_B32","doi-asserted-by":"crossref","first-page":"658","DOI":"10.1107\/S0021889807021206","article-title":"Phaser crystallographic software","volume":"40","author":"McCoy","year":"2007","journal-title":"J. Appl. Crystallogr."},{"key":"2021112215392614000_B33","doi-asserted-by":"crossref","first-page":"760","DOI":"10.1107\/S0907444994003112","article-title":"The CCP4 suite: programs for protein crystallography","volume":"50","author":"Collaborative Computational Project, Number 4","year":"1994","journal-title":"Acta Crystallogr. Sect. D Biol. Crystallogr."},{"key":"2021112215392614000_B34","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1524\/zkri.217.12.644.20662","article-title":"Macromolecular phasing with SHELXE","volume":"217","author":"Sheldrick","year":"2002","journal-title":"Z. Kristallogr."},{"key":"2021112215392614000_B35","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1107\/S0907444996012255","article-title":"Refinement of macromolecular structures by the maximum-likelihood method","volume":"53","author":"Murshudov","year":"1997","journal-title":"Acta Crystallogr. Sect. D Biol. Crystallogr."},{"key":"2021112215392614000_B36","doi-asserted-by":"crossref","first-page":"1011","DOI":"10.1238\/Physica.Topical.115a01011","article-title":"Sixpack: a graphical user interface for XAS analysis using IFEFFIT","volume":"T115","author":"Webb","year":"2005","journal-title":"Physica Scripta"},{"key":"2021112215392614000_B37","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1107\/S0909049505012719","article-title":"ATHENA, ARTEMIS, HEPHAESTUS: data analysis for X-ray absorption spectroscopy using IFEFFIT","volume":"12","author":"Ravel","year":"2005","journal-title":"J. Synchrotron Radiat."},{"key":"2021112215392614000_B38","doi-asserted-by":"crossref","first-page":"2995","DOI":"10.1103\/PhysRevB.52.2995","article-title":"Multiple scattering calculations of x-ray absorption spectra","volume":"52","author":"Zabinsky","year":"1995","journal-title":"Phys. Rev. B"},{"key":"2021112215392614000_B39","doi-asserted-by":"crossref","first-page":"96","DOI":"10.1107\/S0909049500016290","article-title":"EXAFS analysis using FEFF and FEFFIT","volume":"8","author":"Newville","year":"2001","journal-title":"J. Synchrotron Radiat."},{"key":"2021112215392614000_B40","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1107\/S0108767391001071","article-title":"Accurate bond and angle parameters for X-ray protein structure refinement","volume":"47","author":"Engh","year":"1991","journal-title":"Acta Crystallogr. Sect. A Found. Crystallogr."},{"key":"2021112215392614000_B41","doi-asserted-by":"crossref","first-page":"23120","DOI":"10.1016\/S0021-9258(18)54471-9","article-title":"Copper K-extended X-ray absorption fine structure studies of oxidized and reduced dopamine \u03b2-hydroxylase. Confirmation of a sulfur ligand to copper(I) in the reduced enzyme","volume":"266","author":"Blackburn","year":"1991","journal-title":"J. Biol. Chem."},{"key":"2021112215392614000_B42","doi-asserted-by":"crossref","first-page":"4809","DOI":"10.1021\/bi015814m","article-title":"Unraveling the substrate\u2013metal binding site of ferrochelatase: an X-ray absorption spectroscopic study","volume":"41","author":"Ferreira","year":"2002","journal-title":"Biochemistry"},{"key":"2021112215392614000_B43","doi-asserted-by":"crossref","first-page":"920","DOI":"10.1021\/ic00005a010","article-title":"X-ray spectroscopic studies of nickel complexes, with application to the structure of nickel sites in hydrogenases","volume":"30","author":"Colpas","year":"1991","journal-title":"Inorg. Chem."},{"key":"2021112215392614000_B44","doi-asserted-by":"crossref","first-page":"2564","DOI":"10.1021\/bi9721344","article-title":"X-ray absorption spectroscopy of a new zinc site in the Fur protein from Escherichia coli","volume":"37","author":"Jacquamet","year":"1998","journal-title":"Biochemistry"},{"key":"2021112215392614000_B45","doi-asserted-by":"crossref","first-page":"7157","DOI":"10.1021\/ja00257a042","article-title":"X-ray absorption spectroscopy of metal\u2013histidine coordination in metalloproteins. Exact simulation of the EXAFS of tetrakis(imidazole)copper(II) nitrate and other copper\u2013imidazole complexes by the use of a multiple-scattering treatment","volume":"109","author":"Strange","year":"1987","journal-title":"J. Am. Chem. Soc."}],"container-title":["Biochemical Journal"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/portlandpress.com\/biochemj\/article-pdf\/441\/3\/1017\/670538\/bj4411017.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/portlandpress.com\/biochemj\/article-pdf\/441\/3\/1017\/670538\/bj4411017.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,11,22]],"date-time":"2021-11-22T21:45:59Z","timestamp":1637617559000},"score":1,"resource":{"primary":{"URL":"https:\/\/portlandpress.com\/biochemj\/article\/441\/3\/1017\/46208\/Crystallographic-and-X-ray-absorption"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2012,1,16]]},"references-count":45,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2012,2,1]]}},"URL":"https:\/\/doi.org\/10.1042\/bj20111659","relation":{},"ISSN":["0264-6021","1470-8728"],"issn-type":[{"value":"0264-6021","type":"print"},{"value":"1470-8728","type":"electronic"}],"subject":[],"published":{"date-parts":[[2012,1,16]]}}}