Structural organization of bacterial ureases
Keywords:
urease, sub-unit organization, quaternary structure, accessory proteinsAbstract
This brief review concerns the basic principles of structural organization of multi-subunit bacterial ureases and formation of their quaternary structure. Urease is a nickel-containing enzyme (urea amidohydrolase, ЕС 3.5.1.5) that catalyses the hydrolysis of urea to get ammonia and carbamate which then decomposes with water to get ammonia and carbon dioxide. Urease is produced by bacteria, fungi, yeast and plants. On the basis of similarities in amino acid sequences, ureases assumed to have a similar structure and conservative catalytic mechanism. Within past two decades bacterial ureases have gained much attention in research field as a virulence factor in human and animal infections. The first crystal structure of urease has been determined for that from Klebsiella aerogenes. The native enzyme consists of three subunits, UreA (α-chain), UreB (β-chain) and UreC (γ-chain), and contains four structural domains: two in α-chain (α-domain 1 and α-domain-2), one in β- and one in γ-chain. These three chains form a T-shaped heterotrimer αβγ. Three αβγ heterotrimers form quaternary complex (αβγ)3. In case of Helicobacter pilori, the analogous trimers of corresponding dimeric subunits (αβ)3 form tetrameric structure ((αβ)3)4 in which four trimers are situated at the vertexes of the regular triangle pyramid. Active center is located in α-domain 1 and contains two atoms of nickel coordinated by residues His134, His136, carboxylated Lys217, His 246, His272 and Asp360, as well as residues involved in binding (His219) and catalysis (His320). Active site is capped by a flap that controls substrate ingress to and product egress from the dinickel center. Urease requires accessory proteins (UreD, UreF, UreG and UreE) for the correct assembly of their Ni-containing metallocenters. The accessory proteins UreD, UreF, and UreG sequentially bind to the apoprotein (UreABC)3 to finally form (UreABC-UreDFG)3 activation complex. UreE metallochaperone delivers nickel ions to this complex, UreE and (UreDFG)3 are then released from the activated enzyme. An understanding of structural organization of bacterial ureases is the necessary factor in the studies of structure-function relationships of these enzymes, mechanisms of their enzyme and non-enzyme activity, in design of new safe and efficient enzyme inhibitors aimed to struggle with infectious diseases promoted by urease activity.
References
Mobley, H. L. T. Molecular biology of microbial ureases [Text] / H. T. Mobley, M. D. Island, R. P. Hausinger // Microbiol. Rev. – 1995. – Vol. 59, N 3. - P. 451–480.
Mobley, H. L. T. Microbial ureases: significance, regulation, and molecular characterization [Text] / H. L. T. Mobley, R. P. Hausinger // Microbiol. Rev. – 1989. – Vol. 53, N 1. – P. 85–108.
Suzuki, K. Urease-producing species of intestinal anaerobes and their activities [Text] / K. Suzuki, Y. Benno, T. Mitsuoka, S. Takebe, K. Kobashi, J. Hase // Appl. Environ. Microb. - 1979. – Vol. 37, N 3. - P. 379-382.
Murchan, S. Emergence, spread, and characterization of phage variants of epidemic methicillin-resistant Staphylococcus aureus 16 in England and Wales [Text] / S. Murchan, H. M. Aucken, G. L. O’Neill,.M. Ganner, B. D. Cookson // J. Clin. Microbiol. – 2004. – Vol. 42, N 11. – P. 5154-5160.
Jin, M. Development of a large-scale HPLC-based purification for the urease from Staphylococcus leei and determination of subunit structure [Text] / M. Jin, W. Rosario, E. Watler, D.H. Calhoun // Protein Expr. Purif. – 2004. – Vol. 34, N 1. – P. 111-117.
Clemens, D.L. Purification, characterization, and genetic analysis of Mycobacterium tuberculosis urease, a potentially critical determinant of host-pathogen interaction [Text] / D. L. Clemens, B.-Y. Lee, M. A. Horwitz // J. Bacteriol. – 1995. – Vol. 177, N 19. – P. 5644-5652.
Dupuy, B. Clostridium perfringens urease genes are plasmid borne [Text] / B. Dupuy, G. Daube, M. R. Popoff, S. T. Cole // Infect. Immun. – 1997. – Vol. 65, N 6. – P. 2313-2320.
Futagami, S. Systemic and local immune responses against Helicobacter pylori urease in patients with chronic gastritis: distinct IgA and IgG productive sites [Text] / S. Futagami, H. Takahashi, Y. Norose, M. Kobayashi, M. // Gut. – 1998. – Vol. 43, N 2. – P. 168-175.
Nakano, M. Association of the urease gene with enterohemorrhagic Escherichia coli strains irrespective of their serogroups [Text] / M. Nakano, T. Iida, M. Ohnishi, K. Kurokawa, A. Takahashi, T. Tsukamoto, T. Yasunaga, T. Hayashi, T. Honda // J. Clin. Microbiol. – 2001. – Vol. 39, N 12. – P. 4541-4543.
Orth, D. Prevalence, structure and expression of urease genes in Shiga toxin-producing Escherichia coli from humans and the environment [Text] / D. Orth, K. Grif, M. P. Dierich, R. Wurzner // Int. J. Hyg. Environ.-Health. – 2006. – Vol. 209, N 6. – P. 513-520.
Konieczna, I. Bacterial ureases and its role in long-lasting human diseases [Text] / I. Konieczna, P. Zarnowiec, M. Kwinkowski, et al. // Curr. Protein. Pept. Sci. – 2012. – Vol. 13. – P. 789-806.
Sirko, A. Plant ureases: roles and regulation [Text] / A. Sirko, R. Brodzik // Acta Biochim. Pol. – 2000. – Vol. 47, N 4. – P. 1189-1195.
Tange, Y. Identification of the ure1+ gene encoding urease in fission yeast [Text] / Y. Tange, O. Niwa // Curr. Genet. – 1997. – Vol. 32, N 3. – P. 244-246.
Zonia, L.E. Essential role of urease in germination of nitrogen-limited Arabidopsis thaliana seeds [Text] / L. E. Zonia, N. E. Stebbins, J. C. Polacco // Plant Physiol. – 1995. – Vol. 107, N 4. – P. 1097-1103.
Pedrozo, H.A. A mechanism of adaptation to hypergravity in the statocyst of Aplysia californica [Text] / H. A. Pedrozo, Z. Schwartz, M. Luther, D. D. Dean, B. D. Boyan, M. L. Wiederhold // Hear Res. – 1996. – Vol. 102, N 1-2. – P. 51-62.
McLean, R. J. C. The ecology and pathogenicity of urease-producing bacteria in the urinary tract [Text] / R. J. C. McLean, J. C. Nickel, K.-J. Cheng, J. W. Costerton // CRC Crit. Rev. Microbiol. – 1988. – Vol. 16, N 1. – P. 37–79.
Visek, W. J., Effects of urea hydrolysis on cell life-span and metabolism [] / W. J. Visek // Fed. Proc. Fed. Am. Soc. Exp. Biol. – 1972. – Vol. 31. – P. 1178-1193.
Visek, W. J. Ammonia: its effects on biological systems, metabolic hormones and reproduction [Text] / W. J. Visek // J. Dairy Sci. – 1984. – Vol. 67, N 3. – P. 481-498.
Follmer, C. Ureases as a target for the treatment of gastric and urinary infections [Text] / C. Folmer // J. Clin. Pathol. – 2010. – Vol. 63, N 5. – P. 424-430.
Burne, R. A. Bacterial ureases in infectious diseases [Text] / R. A. Burne, Y.-Y. M. Chen // Microbes and Infection. – 2000. – Vol. 2. – P. 533−542.
Collins, C. M. Bacterial ureases: structure, regulation of expression and role in pathogenesis [Text] / M. Collins and S. E. F. D’Orazio // Mol. Microbiol. – 1993. – Vol. 9, N 5. P. 907–913.
Carlini, C. R. Ureases as multifunctional toxic proteins: A review [Text] / C. R. Carlini, R. Ligabue-Braun // Toxicon. – 2016. – Vol. 110. – P. 90-109.
Modolo, L. V. An overview on the potential of natural products as urease inhibitors: a review [Text] / L. V. Modolo, A. X. de Souza, L. P. Horta, D. P. Araujo, A. de Fatima // J. Adv. Res. – 2015. – Vol. 6. – P. 35-44.
Wöhler, F. Ueber künstliche bildung des harnstoffs [Text] / F. Wöhler // Ann. Phys. Chem. – 1828. – Vol. 12. – P. 253-256.
Balasubramanian, A. Crystal structure of the first plant urease from jack bean: 83 years of journey from its first crystal to molecular structure [Text] / A. Balasubramanian, K, Ponnuraj // J. Mol. Biol. – 2010. Vol. 400. – P. 274–283.
Summner, J. B. The isolation and crystallization of the enzyme urease [Text] / J. B. Sumner // J. Biol. Chem. – 1926. – Vol. 69. – P. 435–441.
Фёршт, Э. Структура и механизм действия ферментов [Текст] / Под ред. Б. И. Курганова. – М. : Мир, 1980. – 432 с.
Бландел, Т. Кристаллография белка [Текст] / Под Ред. Ю. Т. Стручкова. - М. : Мир, 1979. – 622 с.
Dixon, N. E. 1975. Jack bean urease (EC 3.5.1.5). A metalloenzyme. A simple biological role for nickel? [Text] / N. E. Dixon, C. Gazzola, R. L. Blakeley, B. Zerner. // J. Am. Chem. Soc. – 1975. – Vol. 97. – P. 4131–4133.
Ragsdale, S. W. Nickel-based Enzyme Systems [Text] / S.W. Ragsdale
// J. Biol. Chem. – 2009. – Vol. 284, N 28. – P. 18571–18575.
Carter, E. L. Interplay of metal ions and urease [Text] / E. L. Carter, N. Flugga, J. L. Boer, S. B. Mulrooney, R. P. Hausinger // Metallomics. – 2009. – Vol. 1. – P. 207-221.
Boer, J. L. Nickel-dependent metalloenzymes [Text] / J. L. Boer, S. B. Mulrooney, R. P. Hausinger // Arch. Biochem. Biophys. – 2014. – Vol. 544. – P. 142-152.
Krajewska, B. Ureases I. Functional, catalytic and kinetic properties: a review [Text] / J. Mol. Catal. B Enzym . – 2009. – Vol. 59, N 1-3. – P. 9–21.
Ligabue-Braun, R. 3-to-1: unraveling structural transitions in ureases [Text] / R. Ligabue-Braun, F. C. Andreis, H. Verli, C. R. Carlini // Naturwissenschaften. – 2013. – Vol. 100. – P. 459–467.
Jabri, E. The crystal structure of urease from Klebsiella aerogenes [Text] / E. Jabri, M. B. Carr, R. P. Hausinger, P. A. Karplus // Science. – 1995. – Vol. 268, N 5213. – P. 998-1004.
Karplus, P.A. 70 years of crystalline urease: what have we learned? [Text] / P. A. Karplus, M. F. Pearson, R. P. Hausinger // Acc. Chem. Res. – 1997. – Vol. 30. – P. 330-337.
Habel, J. E. Structure of Rv1848 (UreA), the Mycobacterium tuberculosis urease gamma subunit [Text] / J. E. Habel, E. H. Bursey, B. S. Rho, et al. // Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. – 2010. – Vol. 66, N 7. – P. 781-786.
Rjberts, B. P. Wide-open flaps are key to urease activity [Text] / B. P. Roberts, B. R. Miller, A. E. Roitberg, R. M. Merz // J. Am. Chem. Soc. – 2012. – Vol. 134. – P. 9934–9937.
Macomber, L. Reduction urease activity by interaction with the flap covering the active site [Text] / L. Macomber, M. S. Minkara, R. P. Hausinger, K. M. Merz // J. Chem. Inf. Model. – 2015. – Vol. 55, N 2. – P. 354-361.
Ha, N.-C. Supramolecular assembly and acid resistance of Helicobacter pylori urease [Text] / N.-C. Ha, S.-T. Oh, J. Y. Sung, et al. // Nature Struct. Biol. - 2001. – Vol. 8. – P. 505-509.
Carter, E. L. Iron-containing urease in a pathogenic bacterium [Text] / E. L. Carter, D. E. Tronrud, S. R. Taber, P. A. Karplus, R. P. Hausinger // P. Natl. Acad. Sci. USA. – 2011. – Vol. 108. – P. 13095-13099.
Follmer, C. Canatoxin, a toxic protein from jack beans (Сanavalia ensiformis), is a variant from of urease (EC 3.5.1.5): Biological effects of urease independent of its ureolitic activity [Text] / Biochem. J. – 2001. – Vol. 360, N 1. – P. 217-224.
Zambelli, B. Chemistry of Ni2+ in urease: Sensing, trafficking, and catalysis [Text] / Accounts Chem. Res. – 2011. – Vol. 44. – P. 520-530.
Farrugia1, M. A. Analysis of a soluble (UreD:UreF:UreG)2 accessory protein complex and its interactions with Klebsiella aerogenes urease by Mass Spectrometry [Text] / M. A. Farrugia1, L. Han, Y. Zhong, J. L. Boer, B. T. Ruotolo, R. P. Hausinger // J. Am. Soc. Mass. Spectrom. – 2013. – Vol. 24, N 9. – P. 1328–1337.
Ligabue-Braun, R. Evidence-based docking of the urease activation complex [Text] / R. Ligabue-Braun, R. Real-Guerra, C. R. Carlini, H. Verli // J. Biomol. Struct. Dyn. – 2013. - Vol. 31, N 8. – P. 854–861.
Quiroz-Valenzuela, S. The structure of urease activation complexes examined by flexibility analysis, mutagenesis, and small-angle X-ray scattering./ S. Quiroz-Valenzuela, S. C. Sukuru, R. P. Hausinger, L. A. Kuhn, W. T. Heller // Arch. Biochem. Biophys. – 2008. – Vol. 480, 51–57.
Fong, Y. H. Structure of UreG/UreF/UreH complex reveals how urease accessory proteins facilitate maturation of Helicobacter pylori urease [Text] / Y. H. Fong, H. C. Wonh, M. H. Yuen, P. H. Lau et al. // PLoS Biol. – 2013. – Vol. 11, N 10. – P. 1-16.
Quiroz-Valenzuela, S. The structure of urease activation complexes examined by flexibility analysis, mutagenesis, and small-angle X-ray scattering [Text] / S. Quiroz-Valenzuela, S. C. K. Sukuru, R. P. Hausinger, A. L. A. Kuhn, W. T. Helle // Arch. Biochem. Biophys. – 2008. – Vol. 480, N 1. – P. 51–57.
Downloads
How to Cite
Issue
Section
License
Copyright (c) 2020 Annals of Mechnikov's Institute
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 Unported License.
