- -

New Insight into the Transcarbamylase Family: TheStructure of Putrescine Transcarbamylase, a Key Catalystfor Fermentative Utilization of Agmatine

RiuNet: Institutional repository of the Polithecnic University of Valencia

Share/Send to

Cited by

Statistics

  • Estadisticas de Uso

New Insight into the Transcarbamylase Family: TheStructure of Putrescine Transcarbamylase, a Key Catalystfor Fermentative Utilization of Agmatine

Show simple item record

Files in this item

Thumbnail
Name: Polo, L. M. - New ...
Size: 1.593Mb
Format: PDF
Description: Versión editorial
Open
dc.contributor.author Polo, Luis Mariano es_ES
dc.contributor.author Gil Ortíz, Fernando es_ES
dc.contributor.author Cantin Sanz, Angel es_ES
dc.contributor.author Rubio, Vicente es_ES
dc.date.accessioned 2015-06-09T07:58:34Z
dc.date.available 2015-06-09T07:58:34Z
dc.date.issued 2012-02-20
dc.identifier.issn 1932-6203
dc.identifier.uri http://hdl.handle.net/10251/51405
dc.description.abstract Transcarbamylases reversibly transfer a carbamyl group from carbamylphosphate (CP) to an amine. Although aspartate transcarbamylase and ornithine transcarbamylase (OTC) are well characterized, little was known about putrescine transcarbamylase (PTC), the enzyme that generates CP for ATP production in the fermentative catabolism of agmatine. We demonstrate that PTC (from Enterococcus faecalis), in addition to using putrescine, can utilize L-ornithine as a poor substrate. Crystal structures at 2.5 A˚ and 2.0 A˚ resolutions of PTC bound to its respective bisubstrate analog inhibitors for putrescine and ornithine use, N-(phosphonoacetyl)-putrescine and d-N-(phosphonoacetyl)-L-ornithine, shed light on PTC preference for putrescine. Except for a highly prominent C-terminal helix that projects away and embraces an adjacent subunit, PTC closely resembles OTCs, suggesting recent divergence of the two enzymes. Since differences between the respective 230 and SMG loops of PTC and OTC appeared to account for the differential preference of these enzymes for putrescine and ornithine, we engineered the 230-loop of PTC to make it to resemble the SMG loop of OTCs, increasing the activity with ornithine and greatly decreasing the activity with putrescine. We also examined the role of the C-terminal helix that appears a constant and exclusive PTC trait. The enzyme lacking this helix remained active but the PTC trimer stability appeared decreased, since some of the enzyme eluted as monomers from a gel filtration column. In addition, truncated PTC tended to aggregate to hexamers, as shown both chromatographically and by X-ray crystallography. Therefore, the extra Cterminal helix plays a dual role: it stabilizes the PTC trimer and, by shielding helix 1 of an adjacent subunit, it prevents the supratrimeric oligomerizations of obscure significance observed with some OTCs. Guided by the structural data we identify signature traits that permit easy and unambiguous annotation of PTC sequences. es_ES
dc.description.sponsorship This work was supported by grants BFU2008-05021 of the Spanish Ministry for Science and Prometeo/2009/051 of the Valencian Government. The European Union and the European Molecular Biology Laboratory funded synchrotron visits. LMP was supported by a Consejo Superior de Investigaciones Cientificas-Banco de Santander fellowship and FGO by a JAE-DOC contract of the Consejo Superior de Investigaciones Cientificas. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. en_EN
dc.language Inglés es_ES
dc.publisher Public Library of Science es_ES
dc.relation.ispartof PLoS ONE es_ES
dc.rights Reconocimiento (by) es_ES
dc.title New Insight into the Transcarbamylase Family: TheStructure of Putrescine Transcarbamylase, a Key Catalystfor Fermentative Utilization of Agmatine es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1371/journal.pone.0031528
dc.relation.projectID info:eu-repo/grantAgreement/MICINN//BFU2008-05021/ES/COMPLEJOS MACROMOLECULARES, PLURIEMPLEO E IMPLICACIONES EN ENFERMEDADES RARAS DE LOS MIEMBROS DE LA FAMILIA AMINOACIDO QUINASA/
dc.relation.projectID info:eu-repo/grantAgreement/GVA//PROMETEO09%2F2009%2F051/ES/Genes, proteínas y rutas de señalización en enfermedades raras (Biomeder)/
dc.rights.accessRights Abierto es_ES
dc.contributor.affiliation Universitat Politècnica de València. Instituto Universitario Mixto de Tecnología Química - Institut Universitari Mixt de Tecnologia Química es_ES
dc.description.bibliographicCitation Polo, LM.; Gil Ortíz, F.; Cantin Sanz, A.; Rubio, V. (2012). New Insight into the Transcarbamylase Family: TheStructure of Putrescine Transcarbamylase, a Key Catalystfor Fermentative Utilization of Agmatine. PLoS ONE. 7(2):31528-31543. https://doi.org/10.1371/journal.pone.0031528 es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion http://dx.doi.org/10.1371/journal.pone.0031528 es_ES
dc.description.upvformatpinicio 31528 es_ES
dc.description.upvformatpfin 31543 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 7 es_ES
dc.description.issue 2 es_ES
dc.relation.senia 239823
dc.identifier.pmid 22363663 en_EN
dc.identifier.pmcid PMC3282769 en_EN
dc.contributor.funder Ministerio de Ciencia e Innovación
dc.contributor.funder Generalitat Valenciana
dc.contributor.funder Banco Santander
dc.contributor.funder Consejo Superior de Investigaciones Científicas
dc.contributor.funder European Commission
dc.description.references Keefe, A., & Miller, S. (1995). Are polyphosphates or phosphate esters prebiotic reagents? Journal of Molecular Evolution, 41(6). doi:10.1007/bf00173147 es_ES
dc.description.references Jones, M. E. (1963). Carbamyl Phosphate: Many forms of life use this molecule to synthesize arginine, uracil, and adenosine triphosphate. Science, 140(3574), 1373-1379. doi:10.1126/science.140.3574.1373 es_ES
dc.description.references Kantrowitz, E., & Lipscomb, W. (1988). Escherichia coli aspartate transcarbamylase: the relation between structure and function. Science, 241(4866), 669-674. doi:10.1126/science.3041592 es_ES
dc.description.references Xu, Y., Labedan, B., & Glansdorff, N. (2007). Surprising Arginine Biosynthesis: a Reappraisal of the Enzymology and Evolution of the Pathway in Microorganisms. Microbiology and Molecular Biology Reviews, 71(1), 36-47. doi:10.1128/mmbr.00032-06 es_ES
dc.description.references WARGNIES, B., LAUWERS, N., & STALON, V. (1979). Structure and Properties of the Putrescine Carbamoyltransferase of Streptococcus faecalis. European Journal of Biochemistry, 101(1), 143-152. doi:10.1111/j.1432-1033.1979.tb04226.x es_ES
dc.description.references Llacer, J. L., Polo, L. M., Tavarez, S., Alarcon, B., Hilario, R., & Rubio, V. (2006). The Gene Cluster for Agmatine Catabolism of Enterococcus faecalis: Study of Recombinant Putrescine Transcarbamylase and Agmatine Deiminase and a Snapshot of Agmatine Deiminase Catalyzing Its Reaction. Journal of Bacteriology, 189(4), 1254-1265. doi:10.1128/jb.01216-06 es_ES
dc.description.references Tigier, H., & Grisolia, S. (1965). Induction of carbamyl-P specific oxamate transcarbamylase by parabanic acid in a streptococcus. Biochemical and Biophysical Research Communications, 19(2), 209-214. doi:10.1016/0006-291x(65)90506-1 es_ES
dc.description.references Vander Wauven, C., Simon, J.-P., Slos, P., & Stalon, V. (1986). Control of enzyme synthesis in the oxalurate catabolic pathway of Streptococcus faecalis ATCC 11700: evidence for the existence of a third carbamate kinase. Archives of Microbiology, 145(4), 386-390. doi:10.1007/bf00470876 es_ES
dc.description.references Xi, H., Schneider, B. L., & Reitzer, L. (2000). Purine Catabolism in Escherichia coli and Function of Xanthine Dehydrogenase in Purine Salvage. Journal of Bacteriology, 182(19), 5332-5341. doi:10.1128/jb.182.19.5332-5341.2000 es_ES
dc.description.references Liu, Y., Zeng, L., & Burne, R. A. (2009). AguR Is Required for Induction of the Streptococcus mutans Agmatine Deiminase System by Low pH and Agmatine. Applied and Environmental Microbiology, 75(9), 2629-2637. doi:10.1128/aem.02145-08 es_ES
dc.description.references Chen, J., Jiang, L., Chen, Q., Zhao, H., Luo, X., Chen, X., & Fang, W. (2009). lmo0038 Is Involved in Acid and Heat Stress Responses and Specific for Listeria monocytogenes Lineages I and II, and Listeria ivanovii. Foodborne Pathogens and Disease, 6(3), 365-376. doi:10.1089/fpd.2008.0207 es_ES
dc.description.references Villeret, V., Tricot, C., Stalon, V., & Dideberg, O. (1995). Crystal structure of Pseudomonas aeruginosa catabolic ornithine transcarbamoylase at 3.0-A resolution: a different oligomeric organization in the transcarbamoylase family. Proceedings of the National Academy of Sciences, 92(23), 10762-10766. doi:10.1073/pnas.92.23.10762 es_ES
dc.description.references De las Rivas, B., Fox, G. C., Angulo, I., Ripoll, M. M., Rodríguez, H., Muñoz, R., & Mancheño, J. M. (2009). Crystal Structure of the Hexameric Catabolic Ornithine Transcarbamylase from Lactobacillus hilgardii: Structural Insights into the Oligomeric Assembly and Metal Binding. Journal of Molecular Biology, 393(2), 425-434. doi:10.1016/j.jmb.2009.08.002 es_ES
dc.description.references Liu, Y., & Burne, R. A. (2009). Multiple Two-Component Systems of Streptococcus mutans Regulate Agmatine Deiminase Gene Expression and Stress Tolerance. Journal of Bacteriology, 191(23), 7363-7366. doi:10.1128/jb.01054-09 es_ES
dc.description.references Low, D. E., Keller, N., Barth, A., & Jones, R. N. (2001). Clinical Prevalence, Antimicrobial Susceptibility, and Geographic Resistance Patterns of Enterococci: Results from the SENTRY Antimicrobial Surveillance Program, 1997–1999. Clinical Infectious Diseases, 32(s2), S133-S145. doi:10.1086/320185 es_ES
dc.description.references Griswold, A. R., Chen, Y.-Y. M., & Burne, R. A. (2004). Analysis of an Agmatine Deiminase Gene Cluster in Streptococcus mutans UA159. Journal of Bacteriology, 186(6), 1902-1904. doi:10.1128/jb.186.6.1902-1904.2004 es_ES
dc.description.references Naumoff, D. G., Xu, Y., Glansdorff, N., & Labedan, B. (2004). BMC Genomics, 5(1), 52. doi:10.1186/1471-2164-5-52 es_ES
dc.description.references Villeret, V., Clantin, B., Tricot, C., Legrain, C., Roovers, M., Stalon, V., … Van Beeumen, J. (1998). The crystal structure of Pyrococcus furiosus ornithine carbamoyltransferase reveals a key role for oligomerization in enzyme stability at extremely high temperatures. Proceedings of the National Academy of Sciences, 95(6), 2801-2806. doi:10.1073/pnas.95.6.2801 es_ES
dc.description.references Galkin, A., Kulakova, L., Wu, R., Gong, M., Dunaway-Mariano, D., & Herzberg, O. (2009). X-ray structure and kinetic properties of ornithine transcarbamoylase from the human parasiteGiardia lamblia. Proteins: Structure, Function, and Bioinformatics, 76(4), 1049-1053. doi:10.1002/prot.22469 es_ES
dc.description.references Aoki, Y., Sunaga, H., & Suzuki, K. T. (1988). A cadmium-binding protein in rat liver identified as ornithine carbamoyltransferase. Biochemical Journal, 250(3), 735-742. doi:10.1042/bj2500735 es_ES
dc.description.references Shi, D., Morizono, H., Ha, Y., Aoyagi, M., Tuchman, M., & Allewell, N. M. (1998). 1.85-Å Resolution Crystal Structure of Human Ornithine Transcarbamoylase Complexed withN-Phosphonacetyl-l-ornithine. Journal of Biological Chemistry, 273(51), 34247-34254. doi:10.1074/jbc.273.51.34247 es_ES
dc.description.references Robey, E. A., & Schachman, H. K. (1985). Regeneration of active enzyme by formation of hybrids from inactive derivatives: implications for active sites shared between polypeptide chains of aspartate transcarbamoylase. Proceedings of the National Academy of Sciences, 82(2), 361-365. doi:10.1073/pnas.82.2.361 es_ES
dc.description.references Krissinel, E., & Henrick, K. (2004). Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallographica Section D Biological Crystallography, 60(12), 2256-2268. doi:10.1107/s0907444904026460 es_ES
dc.description.references Labedan, B., Boyen, A., Baetens, M., Charlier, D., Chen, P., Cunin, R., … Zhang, Y.-F. (1999). The Evolutionary History of Carbamoyltransferases: A Complex Set of Paralogous Genes Was Already Present in the Last Universal Common Ancestor. Journal of Molecular Evolution, 49(4), 461-473. doi:10.1007/pl00006569 es_ES
dc.description.references Ha, Y., McCann, M. T., Tuchman, M., & Allewell, N. M. (1997). Substrate-induced conformational change in a trimeric ornithine transcarbamoylase. Proceedings of the National Academy of Sciences, 94(18), 9550-9555. doi:10.1073/pnas.94.18.9550 es_ES
dc.description.references Rulı́šek, L., & Vondrášek, J. (1998). Coordination geometries of selected transition metal ions (Co2+, Ni2+, Cu2+, Zn2+, Cd2+, and Hg2+) in metalloproteins. Journal of Inorganic Biochemistry, 71(3-4), 115-127. doi:10.1016/s0162-0134(98)10042-9 es_ES
dc.description.references Krissinel, E., & Henrick, K. (2007). Inference of Macromolecular Assemblies from Crystalline State. Journal of Molecular Biology, 372(3), 774-797. doi:10.1016/j.jmb.2007.05.022 es_ES
dc.description.references Naumoff, D. G. (2004). The difficulty of annotating genes: the case of putrescine carbamoyltransferase. Microbiology, 150(12), 3908-3911. doi:10.1099/mic.0.27640-0 es_ES
dc.description.references Griswold, A. R., Jameson-Lee, M., & Burne, R. A. (2006). Regulation and Physiologic Significance of the Agmatine Deiminase System of Streptococcus mutans UA159. Journal of Bacteriology, 188(3), 834-841. doi:10.1128/jb.188.3.834-841.2006 es_ES
dc.description.references Kuo, L. C., Miller, A. W., Lee, S., & Kozuma, C. (1988). Site-directed mutagenesis of Escherichia coli ornithine transcarbamoylase: role of arginine-57 in substrate binding and catalysis. Biochemistry, 27(24), 8823-8832. doi:10.1021/bi00424a021 es_ES
dc.description.references Ramón-Maiques, S., Britton, H. G., & Rubio, V. (2002). Molecular Physiology of Phosphoryl Group Transfer from Carbamoyl Phosphate by a Hyperthermophilic Enzyme at Low Temperature†. Biochemistry, 41(12), 3916-3924. doi:10.1021/bi011637d es_ES
dc.description.references Legrain, C., Villeret, V., Roovers, M., Gigot, D., Dideberg, O., Pierard, A., & Glansdorff, N. (1997). Biochemical Characterisation of Ornithine Carbamoyltransferase from Pyrococcus Furiosus. European Journal of Biochemistry, 247(3), 1046-1055. doi:10.1111/j.1432-1033.1997.01046.x es_ES
dc.description.references Clantin, B., Tricot, C., Lonhienne, T., Stalon, V., & Villeret, V. (2001). Probing the role of oligomerization in the high thermal stability ofPyrococcus furiosusornithine carbamoyltransferase by site-specific mutants. European Journal of Biochemistry, 268(14), 3937-3942. doi:10.1046/j.1432-1327.2001.02302.x es_ES
dc.description.references Massant, J., Wouters, J., & Glansdorff, N. (2003). Refined structure ofPyrococcus furiosusornithine carbamoyltransferase at 1.87 A. Acta Crystallographica Section D Biological Crystallography, 59(12), 2140-2149. doi:10.1107/s0907444903019231 es_ES
dc.description.references Zhang, P., Martin, P. D., Purcarea, C., Vaishnav, A., Brunzelle, J. S., Fernando, R., … Edwards, B. F. P. (2009). Dihydroorotase from the HyperthermophileAquifiex aeolicusIs Activated by Stoichiometric Association with Aspartate Transcarbamoylase and Forms a One-Pot Reactor for Pyrimidine Biosynthesis†‡. Biochemistry, 48(4), 766-778. doi:10.1021/bi801831r es_ES
dc.description.references Evans, D. R., Bein, K., Guy, H. I., Liu, X., Molina, J. A., & Zimmermann, B. H. (1993). CAD gene sequence and the domain structure of the mammalian multifunctional protein CAD. Biochemical Society Transactions, 21(1), 186-191. doi:10.1042/bst0210186 es_ES
dc.description.references Kotaka, M., Ren, J., Lockyer, M., Hawkins, A. R., & Stammers, D. K. (2006). Structures of R- and T-stateEscherichia coliAspartokinase III. Journal of Biological Chemistry, 281(42), 31544-31552. doi:10.1074/jbc.m605886200 es_ES
dc.description.references Gileadi, O., Burgess-Brown, N. A., Colebrook, S. M., Berridge, G., Savitsky, P., Smee, C. E. A., … Pantic, N. H. (2008). High Throughput Production of Recombinant Human Proteins for Crystallography. Structural Proteomics, 221-246. doi:10.1007/978-1-60327-058-8_14 es_ES
dc.description.references Goloubinoff, P., Gatenby, A. A., & Lorimer, G. H. (1989). GroE heat-shock proteins promote assembly of foreign prokaryotic ribulose bisphosphate carboxylase oligomers in Escherichia coli. Nature, 337(6202), 44-47. doi:10.1038/337044a0 es_ES
dc.description.references Otwinowski, Z., & Minor, W. (1997). [20] Processing of X-ray diffraction data collected in oscillation mode. Macromolecular Crystallography Part A, 307-326. doi:10.1016/s0076-6879(97)76066-x es_ES
dc.description.references Collaborative Computational Project, Number 4. (1994). The CCP4 suite: programs for protein crystallography. Acta Crystallographica Section D Biological Crystallography, 50(5), 760-763. doi:10.1107/s0907444994003112 es_ES
dc.description.references Murshudov, G. N., Skubák, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., … Vagin, A. A. (2011). REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallographica Section D Biological Crystallography, 67(4), 355-367. doi:10.1107/s0907444911001314 es_ES
dc.description.references Emsley, P., Lohkamp, B., Scott, W. G., & Cowtan, K. (2010). Features and development ofCoot. Acta Crystallographica Section D Biological Crystallography, 66(4), 486-501. doi:10.1107/s0907444910007493 es_ES
dc.description.references Brünger, A. T. (1992). Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature, 355(6359), 472-475. doi:10.1038/355472a0 es_ES
dc.description.references Laskowski, R. A., MacArthur, M. W., Moss, D. S., & Thornton, J. M. (1993). PROCHECK: a program to check the stereochemical quality of protein structures. Journal of Applied Crystallography, 26(2), 283-291. doi:10.1107/s0021889892009944 es_ES
dc.description.references Winn, M. D., Murshudov, G. N., & Papiz, M. Z. (2003). Macromolecular TLS Refinement in REFMAC at Moderate Resolutions. Macromolecular Crystallography, Part D, 300-321. doi:10.1016/s0076-6879(03)74014-2 es_ES
dc.description.references Painter, J., & Merritt, E. A. (2006). TLSMDweb server for the generation of multi-group TLS models. Journal of Applied Crystallography, 39(1), 109-111. doi:10.1107/s0021889805038987 es_ES
dc.description.references Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2), 248-254. doi:10.1016/0003-2697(76)90527-3 es_ES
dc.description.references LAEMMLI, U. K. (1970). Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4. Nature, 227(5259), 680-685. doi:10.1038/227680a0 es_ES
dc.description.references Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22(22), 4673-4680. doi:10.1093/nar/22.22.4673 es_ES


This item appears in the following Collection(s)

Show simple item record