Biochemical and structural studies on native and recombinant Glycine max UreG: a detailed characterization of a plant urease accessory protein

Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N (2010) ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res 38:W529–W533. doi:10.1093/nar/gkq399 Barja-Fidalgo C, Guimaraes JA, Carlini CR (1991) Canatoxin, a plant protein, induces insulin release from isolated pancreatic-islets. Endocrinology 128:675–679. doi:10.1210/endo-128-2-675 Becker-Ritt AB, Martinelli AS, Mitidieri S, Feder V, Wassermann GE, Santi L, Vainstein MH, Oliveira JT, Fiuza LM, Pasquali G, Carlini CR (2007) Antifungal activity of plant and bacterial ureases. Toxicon 50:971–983. doi:10.1016/j.toxicon.2007.07.008 Bellucci M, Zambelli B, Musiani F, Turano P, Ciurli S (2009) Helicobacter pylori UreE, a urease accessory protein: specific Ni2+- and Zn2+-binding properties and interaction with its cognate UreG. Biochem J 422:91–100. doi:10.1042/bj20090434 Boer J, Quiroz-valenzuela S, Anderson KL, Hausinger RP (2010) Mutagenesis of Klebsiella aerogenes UreG to probe nickel binding and interactions with other urease-related proteins. Biochemistry 49:5859–5869. doi:10.1021/bi1004987 Brown PH, Cakmak I, Zhang Q (1993) Form and function of zinc plants. In: Robson AD (ed) Zinc in soils and plants: proceedings of the international symposium on “zinc in soils and plants”. Kluwer Academic Publishers, The Netherlands, pp 93–106 Cao FQ, Werner AK, Dahncke K, Romeis T, Liu LH, Witte CP (2010) Identification and characterization of proteins involved in rice urea and arginine catabolism. Plant Physiol 154:98–108. doi:10.1104/pp.110.160929 Carlini CR, Polacco JC (2008) Toxic properties of urease. Crop Sci 48:1665–1672 Casalot L, Rousset M (2001) Maturation of the [NiFe] hydrogenases. Trends Microbiol 9:228–237. doi:10.2135/cropsci2007.10.0576 Colpas GJ, Hausinger RP (2000) In vivo and in vitro kinetics of metal transfer by the Klebsiella aerogenes urease nickel metallochaperone, UreE. J Biol Chem 275:10731–10737. doi:10.1074/jbc.275.15.10731 Cuff JA, Clamp ME, Siddiqui AS, Finlay M, Barton GJ (1998) Jpred: a consensus secondary structure prediction server. Bioinformatics 14:892–893. doi:10.1093/bioinformatics/14.10.892 Dunker AK, Brown CJ, Lawson JD, Iakoucheva LM, Obradovic Z (2002) Intrinsic disorder and protein function. Biochemistry 41:6573–6582. doi:10.1021/bi012159+ Fiske CH, SubbaRow Y (1925) The colorimetric determination of phosphorus. J Biol Chem 66:375–400 Follmer C, Real-Guerra R, Wasserman GE, Olivera-Severo D, Carlini CR (2004) Jack bean, soybean and Bacillus pasteurii ureases: biological effects unrelated to ureolytic activity. Eur J Biochem 271:1357–1363. doi:10.1111/j.1432-1033.2004.04046.x Freyermuth SK, Bacanamwo M, Polacco JC (2000) The soybean Eu3 gene encodes a Ni-binding protein necessary for urease activity. Plant J 21:53–60. doi:10.1046/j.1365-313x.2000.00655.x Fu CL, Olson JW, Maier RJ (1995) HypB Protein of Bradyrhizobium japonicum is a metal-binding GTPase capable of binding 18 divalent nickel ions per dimer. Proc Natl Acad Sci USA 92:2333–2337. doi:10.1073/pnas.92.6.2333 Gasper R, Scrima A, Wittinghofer A (2006) Structural insights into HypB, a GTP-binding protein that regulates metal binding. J Biol Chem 281:27492–27502. doi:10.1074/jbc.M600809200 Glibert PM, Harrison J, Heil C, Seitzinger S (2006) Escalating worldwide use of urea—a global change contributing to coastal eutrophication. Biogeochemistry 77:441–463. doi:10.1007/s10533-005-3070-5 Heredia P, De Las Rivas J (2003) Calcium-dependent conformational change and thermal stability of the isolated PsbO protein detected by FTIR spectroscopy. Biochemistry 42:11383–11831. doi:10.1021/bi034582j Hodge A, Robinson D, Fitter A (2000) Are microorganisms more effective than plants at competing for nitrogen? Trends Plant Sci 5:304–308. doi:10.1016/S1360-1385(00)01656-3 Jaiswal R, Panda D (2009) Differential assembly properties of Escherichia coli FtsZ and Mycobacterium tuberculosis FtsZ: an analysis using divalent calcium. J Biochem 146:733–742. doi:10.1093/jb/mvp120 Konc J, Janezic D (2010) ProBiS algorithm for detection of structurally similar protein binding sites by local structural alignment. Bioinformatics 26:1160–1168. doi:10.1093/bioinformatics/btq100 Laskowski RA, Macarthur MW, Moss DS, Thornton JM (1993) Procheck—a program to check the stereochemical quality of protein structures. J Appl Crystal 26:283–291. doi:10.1107/S0021889892009944 Lee MH, Pankratz HS, Wang S, Scott RA, Finnegan MG, Johnson MK, Ippolito JA, Christianson DW, Hausinger RP (1993) Purification and characterization of Klebsiella aerogenes ureE protein: a nickel-binding protein that function in urease metallocenter assembly. Protein Sci 2:1042–1052. doi:10.1002/pro.5560020617 Lundin B, Thuswaldner S, Shutova T, Eshaghi S, Samuelsson G, Barber L, Andersson B, Spetea C (2007) Subsequent events to GTP binding by the plant PsbO protein: structural changes, GTP hydrolysis and dissociation from the photosystem II complex. Biochim Biophys Acta 1767:500–508. doi:10.1016/j.bbabio.2006.10.009 Maier T, Jacobi A, Sauter M, Bock A (1993) The product of the HypB gene, which is required for nickel incorporation into hydrogenases, is a novel guanine nucleotide-binding protein. J Bacteriol 175:630–635 Marti-Renom MA, Stuart AC, Fiser A, Sanchez R, Melo F, Sali A (2000) Comparative protein structure modeling of genes and genomes. Annu Rev Biophys Biomol Struct 29:291–325. doi:10.1146/annurev.biophys.29.1.291 Mehta N, Benoit S, Maier RJ (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 35:229–234. doi:10.1016/S0882-4010(03)00151-7 Meyer-Bothling LE, Polacco JC (1987) Mutational analysis of the embryo-specific urease locus of soybean. Mol Gen Genet 209:439–444. doi:10.1007/bf00331147 Meyer-Bothling LE, Polacco JC, Cianzio SR (1987) Pleiotropic soybean mutants defective in both urease isoenzymes. Mol Gen Genet 209:432–438. doi:10.1007/bf00331146 Moncrief MB, Hausinger RP (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 179:4081–4086 Mulrooney SB, Hausinger RP (2003) Nickel uptake and utilization by microorganisms. FEMS Microbiol Rev 27:239–261. doi:10.1016/S0168-6445(03)00042-1 Olson JW, Fu C, Maier RJ (1997) The HypB protein from Bradyrhizobium japonicum can store nickel and is required for the nickel-dependent transcriptional regulation of hydrogenase. Mol Microbiol 24:119–128. doi:10.1046/j.1365-2958.1997.3251690.x Polacco JC, Holland MA (1993) Roles of urease in plant cells. Int Rev Cytol 145:65–103 Rey L, Imperial J, Palacios JM, Ruiz-Argueso T (1994) Purification of Rhizobium leguminosarum HypB, a nickel-binding protein required for hydrogenase synthesis. J Bacteriol 176:6066–6073 Shen MY, Sali A (2006) Statistical potential for assessment and prediction of protein structures. Protein Sci 15:2507–2524. doi:10.1110/ps.062416606 Shutova T, Nikitina J, Deikus G, Anderson B, Klimov V, Samuelsson G (2005) Structural dynamics of the manganese-stabilizing protein—effect of pH, calcium, and manganese. Biochemistry 44:15182–15192. doi:10.1021/bi0512750 Soriano A, Hausinger RP (1999) GTP-dependent activation of urease apoprotein in complex with the UreD. Ure F, and Ure G accessory proteins. Proc Natl Acad Sci USA 96:11140–11144. doi:10.1073/pnas.96.20.11140 Soriano A, Colpas GL, Hausinger RP (2000) UreE stimulation of GTP-dependent urease activation in the UreD-UreF-UreG-urease complex. Biochemistry 39:12435–12440. doi:10.1021/bi001296o Sprang SR (1997) G proteins mechanisms: insights from structural analysis. Annu Rev Biochem 66:639–678. doi:10.1146/annurev.biochem.66.1.639 Staniscuaski F, Ferreira-DaSilva CT, Mulinari F, Pires-Alves M, Carlini CR (2005) Insecticidal effects of canatoxin on the cotton stainer bug Dysdercus peruvianus (Hemiptera: Pyrrhocoridae). Toxicon 45:753–760. doi:10.1016/j.toxicon.2005.01.014 Stola M, Musiani F, Mangani S, Turano P, Safarov N, Zambelli B, Ciurli S (2006) The nickel site of Bacillus pasteurii UreE, a urease metallo-chaperone, as revealed by metal-binding studies and X-ray absorption spectroscopy. Biochemistry 45:6495–6509. doi:10.1021/bi0601003 Tompa P (2002) Intrinsically unstructured proteins. Trends Biochem Sci 27:527–533. doi:10.1016/s0968-0004(02)02169-2 Torisky RS, Griffin JD, Yenofsky RL, Polacco JC (1994) A single gene (Eu4) encodes the tissue ubiquitous urease of soybean. Mol Gen Gent 242:404–414. doi:10.1007/BF00281790 Uversky VN (2002) Natively unfolded proteins: a point where biology waits for physics. Protein Sci 11:739–756. doi:10.1110/ps.4210102 Whitmore L, Wallace BA (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res 32:W668–W673. doi:10.1093/nar/gkh371 Whitmore L, Wallace BA (2008) Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases. Biopolymers 89:392–400. doi:10.1002/bip.20853 Witte CP (2011) Urea metabolism in plants. Plant Sci 118:431–438. doi:10.1016/j.plantsci.2010.11.010 Witte CP, Isidore E, Tiller SA, Davies HV, Taylor MA (2001) Functional characterization of urease accessory protein G (ureG) from potato. Plant Mol Biol 45:169–179. doi:10.1023/a:1006429315851 Witte CP, Tiller SA, Taylor MA, Davies HV (2002) Leaf urea metabolism in potato: urease activity profile and patterns of recovery and distribution of N-15 after foliar urea application in wild-type and urease-antisense transgenics. Plant Physiol 128:1129–1136. doi:10.1104/pp.010506 Witte CP, Rosso MG, Romeis T (2005) Identification of three urease accessory proteins that are required for urease activation in Arabidopsis. Plant Physiol 139:1155–1162. doi:10.1104/pp.105.070292 Zambelli B, Stola M, Musiani F, De Vriendt K, Samyn B, Devreese B, Van Beeumen J, Turano P, Dikiy A, Bryant DA, Ciurli S (2005) UreG, a chaperone in the urease assembly process, is an intrinsically unstructured GTPase that specifically binds Zn2+. J Biol Chem 280:4684–4695. doi:10.1074/jbc0M408483200 Zambelli B, Musiani F, Savini M, Tucker P, Ciurli S (2007) Biochemical studies on Mycobacterium tuberculosis UreG and comparative modeling reveal structural and functional conservation among the bacterial UreG family. Biochemistry 46:3171–3182. doi:10.1021/bi6024676 Zambelli B, Turano P, Musiani F, Neyroz P, Ciurli S (2009) Zn2+-linked dimerization of UreG from Helicobacter pylori, a chaperone involved in nickel trafficking and urease activation. Proteins 74:222–239. doi:10.1002/prot.22205 Zambelli B, Musiani F, Benini S, Ciurli S (2011) Chemistry of Ni(2+) in urease: sensing, trafficking, and catalysis. Acc Chem Res. doi:10.1021/ar200041k Zambelli B, Cremades N, Neyroz P, Turano P, Uversky V, Ciurli S (2012) Insights in the (un)structural organization of Bacillus pasteurii UreG, an intrinsically disordered GTPase enzyme. Mol BioSyst 8:220–228. doi:10.1039/c1mb05227f