Dual roles of F123 in protein homodimerization and inhibitor binding to biotin protein ligase from Staphylococcus aureus

Molecular Microbiology

Volumn 91, Issue 1, 2014, Pages 110-120

  Soares da Costa, Tatiana P ^a,d   Yap, Min Y ^b   Perugini, Matthew A ^c   Wallace, John C ^a   Abell, Andrew D ^a   Wilce, Matthew C J ^b   Polyak, Steven W ^a   Booker, Grant W ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c LA TROBE UNIVERSITY   (Australia)

^d CHARLES STURT UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; BACTERIAL PROTEIN; BIOTIN; BIOTIN PROTEIN LIGASE; PROTEIN F123; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; BIRA PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; LIGAND; LIGASE; PHENYLALANINE; REPRESSOR PROTEIN;

ARTICLE; BIOTINYLATION; CONTROLLED STUDY; DIMERIZATION; DISSOCIATION; DNA BINDING; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME KINETICS; HYDROGEN BOND; HYDROPHOBICITY; LIGAND BINDING; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; STAPHYLOCOCCUS AUREUS; SURFACE PLASMON RESONANCE; ULTRACENTRIFUGATION; X RAY CRYSTALLOGRAPHY; ANTAGONISTS AND INHIBITORS; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN CONFORMATION; PROTEIN MOTIF; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; SMALL ANGLE SCATTERING; X RAY DIFFRACTION;

ESCHERICHIA COLI; STAPHYLOCOCCUS AUREUS;

AMINO ACID MOTIFS; BACTERIAL PROTEINS; BINDING SITES; BIOTIN; CARBON-NITROGEN LIGASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; LIGANDS; LIGASES; MODELS, MOLECULAR; PHENYLALANINE; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; REPRESSOR PROTEINS; SCATTERING, SMALL ANGLE; STAPHYLOCOCCUS AUREUS; SURFACE PLASMON RESONANCE; X-RAY DIFFRACTION;

EID: 84891160473     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12446     Document Type: Article

References (46)

1. Bagautdinov, B., Kuroishi, C., Sugahara, M., and Kunishima, N. (2005) Crystal structures of biotin protein ligase from Pyrococcus horikoshii OT3 and its complexes: structural basis of biotin activation. J Mol Biol 353: 322-333.
2. Barker, D.F., and Campbell, A.M. (1981) Genetic and biochemical characterisation of the birA gene and its product : evidence for a direct role of biotin holoenzyme synthetase in repression of the biotin operon in Escherichia coli. J Mol Biol 146: 469-492.
3. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilising the principle of protein-dye binding. Anal Biochem 72: 248-254.
4. Brown, P.H., Cronan, J.E., Grotli, M., and Beckett, D. (2004) The biotin repressor: modulation of allostery by corepressor analogs. J Mol Biol 337: 857-869.
5. Burgess, B.R., Dobson, R.C., Bailey, M.F., Atkinson, S.C., Griffin, M.D., Jameson, G.B., etal. (2008) Structure and evolution of a novel dimeric enzyme from a clinically important bacterial pathogen. J Biol Chem 283: 27598-27603.
6. Chakravartty, V., and Cronan, J.E. (2012) Altered regulation of Escherichia coli biotin biosynthesis in BirA superrepressor mutant strains. J Bacteriol 194: 1113-1126.
7. Chapman-Smith, A., Mulhern, T.D., Whelan, F., Cronan, J.E., Jr., and Wallace, J.C. (2001) The C-terminal domain of biotin protein ligase from E. coli is required for catalytic activity. Protein Sci 10: 2608-2617.
8. Duckworth, B.P., Geders, T.W., Tiwari, D., Boshoff, H.I., Sibbald, P.A., Barry, C.E., 3rd, etal. (2011) Bisubstrate adenylation inhibitors of biotin protein ligase from Mycobacterium tuberculosis. Chem Biol 18: 1432-1441.
9. Eisenstein, E., and Beckett, D. (1999) Dimerization of the Escherichia coli biotin repressor: corepressor function in protein assembly. Biochemistry 38: 13077-13084.
10. Gupta, V., Gupta, R.K., Khare, G., Salunke, D.M., Surolia, A., and Tyagi, A.K. (2010) Structural ordering of disordered ligand-binding loops of biotin protein ligase into active conformations as a consequence of dehydration. PLoS ONE 5: e9222.
11. Ingaramo, M., and Beckett, D. (2009) Distinct amino termini of two human HCS isoforms influence biotin acceptor substrate recognition. J Biol Chem 284: 30862-30870.
12. Kwon, K., and Beckett, D. (2000) Function of a conserved sequence motif in biotin holoenzyme synthetases. Protein Sci 9: 1530-1539.
13. Kwon, K., Streaker, E.D., and Beckett, D. (2002) Binding specificity and the ligand dissociation process in the E. coli biotin holoenzyme synthetase. Protein Sci 11: 558-570.
14. Laue, T.M., Shah, B., Ridgeway, T.M., and Pelletier, S.L. (1992) Computer-aided interpretation of sedimentation data for proteins. In Analytical Ultracentrifugation in Biochemistry and Polymer Science. Harding, S.E., Rowe, A.J., and Horton, J.C. (eds). Cambridge: Royal Society of Chemistry, pp. 90-125.
15. Mayende, L., Swift, R.D., Bailey, L.M., Soares da Costa, T.P., Wallace, J.C., Booker, G.W., and Polyak, S.W. (2012) A novel molecular mechanism to explain biotin-unresponsive holocarboxylase synthetase deficiency. J Mol Med (Berl) 90: 81-88.
16. Pendini, N.R., Bailey, L.M., Booker, G.W., Wilce, M.C., Wallace, J.C., and Polyak, S.W. (2008a) Microbial biotin protein ligases aid in understanding holocarboxylase synthetase deficiency. Biochim Biophys Acta 1784: 973-982.
17. Pendini, N.R., Polyak, S.W., Booker, G.W., Wallace, J.C., and Wilce, M.C. (2008b) Purification, crystallization and preliminary crystallographic analysis of biotin protein ligase from Staphylococcus aureus. Acta Crystallogr Sect F Struct Biol Cryst Commun 64: 520-523.
18. Pendini, N.R., Yap, M.Y., Polyak, S.W., Cowieson, N.P., Abell, A., Booker, G.W., etal. (2013) Structural characterization of Staphylococcus aureus biotin protein ligase and interaction partners: an antibiotic target. Protein Sci 22: 762-773.
19. Perugini, M.A., Schuck, P., and Howlett, G.J. (2000) Self-association of human apolipoprotein E3 and E4 in the presence and absence of phospholipid. J Biol Chem 275: 36758-36765.
20. Perugini, M.A., Schuck, P., and Howlett, G.J. (2002) Differences in the binding capacity of human apolipoprotein E3 and E4 to size-fractionated lipid emulsions. Eur J Biochem 269: 5939-5949.
21. Polyak, S.W., Chapman-Smith, A., Brautigan, P.J., and Wallace, J.C. (1999) Biotin protein ligase from Saccharomyces cerevisiae. The N-terminal domain is required for complete activity. J Biol Chem 274: 32847-32854.
22. Polyak, S.W., Bailey, L.M., Azhar, A., and Booker, G.W. (2012) Biotin (Vitamin H or B7). In Micronutrients: Sources, Properties and Health Benefits. Betancourt, A.I., and Gaitan, H.F. (eds). New York: Nova Science Publishers, pp. 65-94.
23. Prakash, O., and Eisenberg, M.A. (1979) Biotinyl 5′-adenylate: corepressor role in the regulation of the biotin genes of Escherichia coli K-12. Proc Natl Acad Sci USA 76: 5592-5595.
24. Purushothaman, S., Gupta, G., Srivastava, R., Ramu, V.G., and Surolia, A. (2008) Ligand specificity of group I biotin protein ligase of Mycobacterium tuberculosis. PLoS ONE 3: e2320.
25. Rodionov, D.A., Mironov, A.A., and Gelfand, M.S. (2002) Conservation of the biotin regulon and the BirA regulatory signal in Eubacteria and Archaea. Genome Res 12: 1507-1516.
26. Schneidman-Duhovny, D., Hammel, M., and Sali, A. (2010) FoXS: a web server for rapid computation and fitting of SAXS profiles. Nucleic Acids Res 38: W540-W544.
27. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys J 78: 1606-1619.
28. Schuck, P., Perugini, M.A., Gonzales, N.R., Howlett, G.J., and Schubert, D. (2002) Size-distribution analysis of proteins by analytical ultracentrifugation: strategies and application to model systems. Biophys J 82: 1096-1111.
29. Soares da Costa, T.P., Tieu, W., Yap, M.Y., Pendini, N.R., Polyak, S.W., Sejer Pedersen, D., etal. (2012a) Selective inhibition of Biotin protein ligase from Staphylococcus aureus. J Biol Chem 287: 17823-17832.
30. Soares da Costa, T.P., Tieu, W., Yap, M.Y., Zvarec, O., Bell, J., Turnidge, J.D., etal. (2012b) Biotin analogues with antibacterial activity are potent inhibitors of Biotin protein ligase. ACS Med Chem Lett 3: 509-514.
31. Solbiati, J., and Cronan, J.E. (2010) The switch regulating transcription of the Escherichia coli biotin operon does not require extensive protein-protein interactions. Chem Biol 17: 11-17.
32. Streaker, E.D., and Beckett, D. (2003) Coupling of protein assembly and DNA binding: biotin repressor dimerization precedes biotin operator binding. J Mol Biol 325: 937-948.
33. Streaker, E.D., Gupta, A., and Beckett, D. (2002) The biotin repressor: thermodynamic coupling of corepressor binding, protein assembly, and sequence-specific DNA binding. Biochemistry 41: 14263-14271.
34. Tieu, W., Soares da Costa, T.P., Yap, M.Y., Keeling, K.L., Wilce, M.C.J., Wallace, J.C., etal. (2013) Optimising in situ click chemistry: the screening and identification of biotin protein ligase inhibitors. Chem Sci 4: 3533-3537.
35. Tron, C.M., McNae, I.W., Nutley, M., Clarke, D.J., Cooper, A., Walkinshaw, M.D., etal. (2009) Structural and functional studies of the biotin protein ligase from Aquifex aeolicus reveal a critical role for a conserved residue in target specificity. J Mol Biol 387: 129-146.
36. Vistica, J., Dam, J., Balbo, A., Yikilmaz, E., Mariuzza, R.A., Rouault, T.A., and Schuck, P. (2004) Sedimentation equilibrium analysis of protein interactions with global implicit mass conservation constraints and systematic noise decomposition. Anal Biochem 326: 234-256.
37. Volkov, V.V., and Svergun, D.I. (2003) Uniqueness of ab initio shape determination in small-angle scattering. J Appl Cryst 36: 860-864.
38. Voss, J.E., Scally, S.W., Taylor, N.L., Atkinson, S.C., Griffin, M.D., Hutton, C.A., etal. (2010) Substrate-mediated stabilization of a tetrameric drug target reveals Achilles heel in anthrax. J Biol Chem 285: 5188-5195.
39. Weaver, L.H., Kwon, K., Beckett, D., and Matthews, B.W. (2001a) Competing protein:protein interactions are proposed to control the biological switch of the E coli biotin repressor. Protein Sci 10: 2618-2622.
40. Weaver, L.H., Kwon, K., Beckett, D., and Matthews, B.W. (2001b) Corepressor-induced organization and assembly of the biotin repressor: a model for allosteric activation of a transcriptional regulator. Proc Natl Acad Sci USA 98: 6045-6050.
41. Wilson, K.P., Shewchuk, L.M., Brennan, R.G., Otsuka, A.J., and Matthews, B.W. (1992) Escherichia coli biotin holoenzyme synthetase/bio repressor crystal structure delineates the biotin- and DNA-binding domains. Proc Natl Acad Sci USA 89: 9257-9261.
42. Wood, Z.A., Weaver, L.H., Brown, P.H., Beckett, D., and Matthews, B.W. (2006) Co-repressor induced order and biotin repressor dimerization: a case for divergent followed by convergent evolution. J Mol Biol 357: 509-523.
43. Xu, Y., and Beckett, D. (1994) Kinetics of biotinyl-5′-adenylate synthesis catalyzed by the Escherichia coli repressor of biotin biosynthesis and the stability of the enzyme-product complex. Biochemistry 33: 7354-7360.
44. Xu, Y., Johnson, C.R., and Beckett, D. (1996) Thermodynamic analysis of small ligand binding to the Escherichia coli repressor of biotin biosynthesis. Biochemistry 35: 5509-5517.
45. Zhao, H., and Beckett, D. (2008) Kinetic partitioning between alternative protein-protein interactions controls a transcriptional switch. J Mol Biol 380: 223-236.
46. Zhao, H., Naganathan, S., and Beckett, D. (2009) Thermodynamic and structural investigation of bispecificity in protein-protein interactions. J Mol Biol 389: 336-348.