Imperfect coordination chemistry facilitates metal ion release in the Psa permease

Nature Chemical Biology

Volumn 10, Issue 1, 2014, Pages 35-41

  Couñago, Rafael M ^a   Ween, Miranda P ^b   Begg, Stephanie L ^b   Bajaj, Megha ^a   Zuegg, Johannes ^a   O'Mara, Megan L ^a   Cooper, Matthew A ^a   McEwan, Alastair G ^a   Paton, James C ^b   Kobe, Bostjan ^a   McDevitt, Christopher A ^b  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; COORDINATION COMPOUND; DIVALENT CATION; MANGANESE; PERMEASE; PSA PROTEIN; TRANSITION ELEMENT; UNCLASSIFIED DRUG; ZINC ION;

ARTICLE; CONFORMATIONAL TRANSITION; ENZYME SUBSTRATE COMPLEX; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; STREPTOCOCCUS PNEUMONIAE;

BINDING SITES; CATIONS; MEMBRANE TRANSPORT PROTEINS; METALS; MODELS, MOLECULAR; STREPTOCOCCUS PNEUMONIAE;

BACTERIA (MICROORGANISMS); STREPTOCOCCUS PNEUMONIAE;

EID: 84890982990     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1382     Document Type: Article

References (45)

1. Papp-Wallace, K.M. & Maguire, M.E. Manganese transport and the role of manganese in virulence. Annu. Rev. Microbiol. 60, 187-209(2006). (Pubitemid 44627946)
2. Gat, O. et al. The solute-binding component of a putative Mn(ii) ABC transporter (MntA) is a novel Bacillus anthracis virulence determinant. Mol. Microbiol. 58, 533-551(2005). (Pubitemid 41476167)
3. Berry, A.M. & Paton, J.C. Sequence heterogeneity of PsaA, a 37-kilodalton putative adhesin essential for virulence of Streptococcus pneumoniae. Infect. Immun. 64, 5255-5262(1996). (Pubitemid 26403989)
4. Yesilkaya, H. et al. Role of manganese-containing superoxide dismutase in oxidative stress and virulence of Streptococcus pneumoniae. Infect. Immun. 68, 2819-2826(2000). (Pubitemid 30253861)
5. Janulczyk, R., Ricci, S. & Bjorck, L. MtsABC is important for manganese and iron transport, oxidative stress resistance, and virulence of Streptococcus pyogenes. Infect. Immun. 71, 2656-2664(2003). (Pubitemid 36519881)
6. Horsburgh, M.J. et al. MntR modulates expression of the PerR regulon and superoxide resistance in Staphylococcus aureus through control of manganese uptake. Mol. Microbiol. 44, 1269-1286(2002). (Pubitemid 34595758)
7. Ogunniyi, A.D. et al. Central role of manganese in regulation of stress responses, physiology, and metabolism in Streptococcus pneumoniae. J. Bacteriol. 192, 4489-4497(2010).
8. Archibald, F.S. & Fridovich, I. Manganese and defenses against oxygen toxicity in Lactobacillus plantarum. J. Bacteriol. 145, 442-451(1981). (Pubitemid 11140325)
9. Sobota, J.M. & Imlay, J.A. Iron enzyme ribulose-5-phosphate 3-epimerase in Escherichia coli is rapidly damaged by hydrogen peroxide but can be protected by manganese. Proc. Natl. Acad. Sci. USA 108, 5402-5407(2011).
10. Aguirre, J.D. & Culotta, V.C. Battles with iron: manganese in oxidative stress protection. J. Biol. Chem. 287, 13541-13548(2012).
11. Wu, H.J. et al. Manganese regulation of virulence factors and oxidative stress resistance in Neisseria gonorrhoeae. J. Proteomics 73, 899-916(2010).
12. Keele, B.B. Jr., McCord, J.M. & Fridovich, I. Superoxide dismutase from Escherichia coli B. A new manganese-containing enzyme. J. Biol. Chem. 245, 6176-6181(1970).
13. Andreini, C., Bertini, I., Cavallaro, G., Holliday, G.L. & Thornton, J.M. Metal ions in biological catalysis: from enzyme databases to general principles. J. Biol. Inorg. Chem. 13, 1205-1218(2008).
14. Dintilhac, A., Alloing, G., Granadel, C. & Claverys, J.P. Competence and virulence of Streptococcus pneumoniae: Adc and PsaA mutants exhibit a requirement for Zn and Mn resulting from inactivation of putative ABC metal permeases. Mol. Microbiol. 25, 727-739(1997). (Pubitemid 27394570)
15. McAllister, L.J. et al. Molecular analysis of the psa permease complex of Streptococcus pneumoniae. Mol. Microbiol. 53, 889-901(2004). (Pubitemid 39036967)
16. Marra, A., Lawson, S., Asundi, J.S., Brigham, D. & Hromockyj, A.E. In vivo characterization of the psa genes from Streptococcus pneumoniae in multiple models of infection. Microbiology 148, 1483-1491(2002). (Pubitemid 34567226)
17. McDevitt, C.A. et al. A molecular mechanism for bacterial susceptibility to zinc. PLoS Pathog. 7, e1002357(2011).
18. Lawrence, M.C. et al. The crystal structure of pneumococcal surface antigen PsaA reveals a metal-binding site and a novel structure for a putative ABC-type binding protein. Structure 6, 1553-1561(1998). (Pubitemid 29000532)
19. Berntsson, R.P., Smits, S.H., Schmitt, L., Slotboom, D.J. & Poolman, B. A structural classification of substrate-binding proteins. FEBS Lett. 584, 2606-2617(2010).
20. Woo, J.S., Zeltina, A., Goetz, B.A. & Locher, K.P. X-ray structure of the Yersinia pestis heme transporter HmuUV. Nat. Struct. Mol. Biol. 19, 1310-1315(2012).
21. Korkhov, V.M., Mireku, S.A. & Locher, K.P. Structure of AMP-PNP-bound vitamin B12 transporter BtuCD-F. Nature 490, 367-372(2012).
22. Quiocho, F.A. & Ledvina, P.S. Atomic structure and specificity of bacterial periplasmic receptors for active transport and chemotaxis: variation of common themes. Mol. Microbiol. 20, 17-25(1996). (Pubitemid 26126045)
23. Mao, B., Pear, M.R., McCammon, J.A. & Quiocho, F.A. Hinge-bending in l-arabinose-binding protein. The "Venus's-flytrap" model. J. Biol. Chem. 257, 1131-1133(1982).
24. Felder, C.B., Graul, R.C., Lee, A.Y., Merkle, H.P. & Sadee, W. The Venus flytrap of periplasmic binding proteins: an ancient protein module present in multiple drug receptors. AAPS PharmSci 1, E2(1999).
25. Lee, Y.H., Deka, R.K., Norgard, M.V., Radolf, J.D. & Hasemann, C.A. Treponema pallidum TroA is a periplasmic zinc-binding protein with a helical backbone. Nat. Struct. Biol. 6, 628-633(1999). (Pubitemid 29318950)
26. Ilari, A., Alaleona, F., Petrarca, P., Battistoni, A. & Chiancone, E. The X-ray structure of the zinc transporter ZnuA from Salmonella enterica discloses a unique triad of zinc-coordinating histidines. J. Mol. Biol. 409, 630-641(2011).
27. Wei, B., Randich, A.M., Bhattacharyya-Pakrasi, M., Pakrasi, H.B. & Smith, T.J. Possible regulatory role for the histidine-rich loop in the zinc transport protein, ZnuA. Biochemistry 46, 8734-8743(2007). (Pubitemid 47204439)
28. Yatsunyk, L.A. et al. Structure and metal binding properties of ZnuA, a periplasmic zinc transporter from Escherichia coli. J. Biol. Inorg. Chem. 13, 271-288(2008).
29. Lee, Y.H. et al. The crystal structure of Zn(ii)-free Treponema pallidum TroA, a periplasmic metal-binding protein, reveals a closed conformation. J. Bacteriol. 184, 2300-2304(2002).
30. Couñago, R.M., McDevitt, C.A., Ween, M.P. & Kobe, B. Prokaryotic substrate-binding proteins as targets for antimicrobial therapies. Curr. Drug Targets 13, 1400-1410(2012).
31. Waldron, K.J., Rutherford, J.C., Ford, D. & Robinson, N.J. Metalloproteins and metal sensing. Nature 460, 823-830(2009).
32. Ma, Z., Jacobsen, F.E. & Giedroc, D.P. Coordination chemistry of bacterial metal transport and sensing. Chem. Rev. 109, 4644-4681(2009).
33. Irving, H. & Williams, R.J.P. Order of stability of metal complexes. Nature 162, 746-747(1948).
34. Harding, M.M. Small revisions to predicted distances around metal sites in proteins. Acta Crystallogr. D Biol. Crystallogr. 62, 678-682(2006). (Pubitemid 43806647)
35. Fraústo da Silva, J.J.R.F. & Williams, R.J.P. The Biological Chemistry of the Elements: the Inorganic Chemistry of Life 2nd edn. (Oxford University Press, New York, 2001).
36. Giedroc, D.P. & Arunkumar, A.I. Metal sensor proteins: nature's metalloregulated allosteric switches. Dalton Trans. 3107-3120(2007). (Pubitemid 47117766)
37. Sun, X. et al. Crystal structure and metal binding properties of the lipoprotein MtsA, responsible for iron transport in Streptococcus pyogenes. Biochemistry 48, 6184-6190(2009).
38. Rukhman, V., Anati, R., Melamed-Frank, M. & Adir, N. The MntC crystal structure suggests that import of Mn2+ in cyanobacteria is redox controlled. J. Mol. Biol. 348, 961-969(2005). (Pubitemid 40552796)
39. Banerjee, S., Wei, B., Bhattacharyya-Pakrasi, M., Pakrasi, H.B. & Smith, T.J. Structural determinants of metal specificity in the zinc transport protein ZnuA from Synechocystis 6803. J. Mol. Biol. 333, 1061-1069(2003). (Pubitemid 37324505)
40. Huckle, J.W., Morby, A.P., Turner, J.S. & Robinson, N.J. Isolation of a prokaryotic metallothionein locus and analysis of transcriptional control by trace metal ions. Mol. Microbiol. 7, 177-187(1993). (Pubitemid 23036180)
41. Cavet, J.S. et al. A nickel-cobalt-sensing ArsR-SmtB family repressor. Contributions of cytosol and effector binding sites to metal selectivity. J. Biol. Chem. 277, 38441-38448(2002). (Pubitemid 35154701)
42. Turner, J.S., Glands, P.D., Samson, A.C. & Robinson, N.J. Zn2+-sensing by the cyanobacterial metallothionein repressor SmtB: different motifs mediate metal-induced protein-DNA dissociation. Nucleic Acids Res. 24, 3714-3721(1996). (Pubitemid 26335379)
43. Pennella, M.A., Shokes, J.E., Cosper, N.J., Scott, R.A. & Giedroc, D.P. Structural elements of metal selectivity in metal sensor proteins. Proc. Natl. Acad. Sci. USA 100, 3713-3718(2003). (Pubitemid 36418097)
44. Golynskiy, M.V., Gunderson, W.A., Hendrich, M.P. & Cohen, S.M. Metal binding studies and EPR spectroscopy of the manganese transport regulator MntR. Biochemistry 45, 15359-15372(2006). (Pubitemid 46032461)
45. Mills, S.A. & Marletta, M.A. Metal binding characteristics and role of iron oxidation in the ferric uptake regulator from Escherichia coli. Biochemistry 44, 13553-13559(2005). (Pubitemid 41443682)