Structural characterization of Staphylococcus aureus biotin protein ligase and interaction partners: An antibiotic target

Protein Science

Volumn 22, Issue 6, 2013, Pages 762-773

  Pendini, Nicole R ^a,b   Yap, Min Y ^a   Polyak, Steven W ^b   Cowieson, Nathan P ^a   Abell, Andrew ^b   Booker, Grant W ^b   Wallace, John C ^b   Wilce, Jacqueline A ^a   Wilce, Matthew C J ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Bacterial enzyme; Biotin protein ligase; Biotin carboxyl carrier protein; Biotinylation; DNA binding; Small angle X ray scattering

Indexed keywords

BIOTIN; BIOTIN PROTEIN LIGASE; LIGASE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DNA BINDING; HUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REPRESSOR GENE; STAPHYLOCOCCUS AUREUS; SURFACE PROPERTY; X RAY CRYSTALLOGRAPHY;

ACETYL-COA CARBOXYLASE; ADENOSINE MONOPHOSPHATE; AMINO ACID SEQUENCE; BIOTIN; CARBON-NITROGEN LIGASES; CRYSTALLOGRAPHY, X-RAY; FATTY ACID SYNTHASE, TYPE II; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN INTERACTION MAPS; PROTEIN MULTIMERIZATION; SEQUENCE ALIGNMENT; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 84881301516     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2262     Document Type: Article

References (54)

1. Chiang SL, Mekalanos JJ (1998) Use of signaturetagged transposon mutagenesis to identify Vibrio cholerae genes critical for colonization. Mol Microbiol 27:797-805.
2. Lee JM, Zhang S, Saha S, Santa Anna S, Jiang C, Perkins J (2001) RNA expression analysis using an antisense Bacillus subtilis genome array. J Bacteriol 183:7371-7380.
3. Sassetti CM, Rubin EJ (2003) Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci USA 100:12989-12994.
4. Bae T, Banger AK, Wallace A, Glass EM, Aslund F, Schneewind O, Missiakas DM (2004) Staphylococcus aureus virulence genes identified by bursa aurealis mutagenesis and nematode killing. Proc Natl Acad Sci USA 101:12312-12317.
5. Bergman NH, Anderson EC, Swenson EE, Janes BK, Fisher N, Niemeyer MM, Miyoshi AD, Hanna PC (2007) Transcriptional profiling of Bacillus anthracis during infection of host macrophages. Infect Immun 75:3434-3444.
6. Eisenreich W, Dandekar T, Heesemann J, Goebel W (2010) Carbon metabolism of intracellular bacterial pathogens and possible links to virulence. Nat Rev Microbiol 8:401-412.
7. Becher D, Hempel K, Sievers S, Zuhlke D, Pane-Farre J, Otto A, Fuchs S, Albrecht D, Bernhardt J, Engelmann S, Volker U, van Dijl JM, Hecker M (2009) A proteomic view of an important human pathogen-towards the quantification of the entire Staphylococcus aureus proteome. PLoS One 4:e8176.
8. Hecker M, Becher D, Fuchs S, Engelmann S (2010) A proteomic view of cell physiology and virulence of Staphylococcus aureus. Int J Med Microbiol 300:76-87.
9. Pendini NR, Bailey LM, Booker GW, Wilce MC, Wallace JC, Polyak SW (2008) Microbial biotin protein ligases aid in understanding holocarboxylase synthetase deficiency. Biochim Biophys Acta 1784:973-982.
10. Bagautdinov B, Kuroishi C, Sugahara M, 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.
11. Gupta V, Gupta RK, Khare G, Salunke DM, Surolia A, Tyagi AK (2010) Structural ordering of disordered ligand-binding loops of biotin protein ligase into active conformations as a consequence of dehydration. PLoS One 5:e9222.
12. Tron CM, McNae IW, Nutley M, Clarke DJ, Cooper A, Walkinshaw MD, Baxter RL, Campopiano DJ (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.
13. Purushothaman S, Gupta G, Srivastava R, Ramu VG, Surolia A (2008) Ligand specificity of group I biotin protein ligase of Mycobacterium tuberculosis. PLoS One 3:e2320.
14. Abbott J, Beckett D (1993) Cooperative binding of the Escherichia coli repressor of biotin biosynthesis to the biotin operator sequence. Biochemistry 32:9649-9656.
15. Eisenstein E, Beckett D (1999) Dimerization of the Escherichia coli biotin repressor: corepressor function in protein assembly. Biochemistry 38:13077-13084.
16. Beckett D (2009) Biotin sensing at the molecular level. J Nutr 139:167-170.
17. Hassan YI, Moriyama H, Olsen LJ, Bi X, Zempleni J (2009) N-and C-terminal domains in human holocarboxylase synthetase participate in substrate recognition. Mol Genet Metabol 96:183-188.
18. Ingaramo M, Beckett D (2009) Distinct amino termini of two human HCS isoforms influence biotin acceptor substrate recognition. J Biol Chem 284:30862-30870.
19. Mayende L, Swift RD, Bailey LM, Soares da Costa TP, Wallace JC, Booker GW, Polyak SW (2012) A novel molecular mechanism to explain biotin-unresponsive holocarboxylase synthetase deficiency. J Mol Med (Berl) 90:81-88.
20. Deleo FR, Otto M, Kreiswirth BN, Chambers HF (2010) Community-associated meticillin-resistant Staphylococcus aureus. Lancet 375:1557-1568.
21. Turnidge JD, Kotsanas D, Munckhof W, Roberts S, Bennett CM, Nimmo GR, Coombs GW, Murray RJ, Howden B, Johnson PD, Dowling K (2009) Staphylococcus aureus bacteraemia: a major cause of mortality in Australia and New Zealand. Med J Aust 191:368-373.
22. Liu CI, Liu GY, Song Y, Yin F, Hensler ME, Jeng WY, Nizet V, Wang AH, Oldfield E (2008) A cholesterol biosynthesis inhibitor blocks Staphylococcus aureus virulence. Science 319:1391-1394.
23. Heras B, Shouldice SR, Totsika M, Scanlon MJ, Schembri MA, Martin JL (2009) DSB proteins and bacterial pathogenicity. Nat Rev Microbiol 7:215-225.
24. Soares da Costa TP, Tieu W, Yap MY, Pendini NR, Polyak SW, Sejer Pedersen D, Morona R, Turnidge JD, Wallace JC, Wilce MC, Booker GW, Abell AD (2012) Selective inhibition of biotin protein ligase from Staphylococcus aureus. J Biol Chem 287:17823-17832.
25. Rodionov DA, Mironov AA, Gelfand MS (2002) Conservation of the biotin regulon and the BirA regulatory signal in Eubacteria and Archaea. Genome Res 12:1507-1516.
26. Weaver LH, Kwon K, Beckett D, Matthews BW (2001) Competing protein: protein interactions are proposed to control the biological switch of the E. coli biotin repressor. Protein Sci 10:2618-2622.
27. Weaver LH, Kwon K, Beckett D, Matthews BW (2001) 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.
28. Bagautdinov B, Matsuura Y, Bagautdinova S, Kunishima N (2008) Protein biotinylation visualized by a complex structure of biotin protein ligase with a substrate. J Biol Chem 283:14739-14750.
29. Wood ZA, Weaver LH, Brown PH, Beckett D, Matthews BW (2006) Co-repressor induced order and biotin repressor dimerization: a case for divergent followed by convergent evolution. J Mol Biol 357:509-523.
30. Wallace AC, Laskowski RA, Thornton JM (1995) LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng 8:127-134.
31. Noble MEM, Musacchio A, Saraste M, Courtneidge SA, Wierenga RK (1993) Crystal structure of the SH3 domain in human Fyn-comparison of the 3-dimensional structures of SH3 domains in tyrosine kinases and spectrin. EMBO J 12:2617-2624.
32. Soares Da Costa TP, Tieu W, Yap MY, Zvarec OJ, Bell JM, Turnidge JD, Wallace JC, Booker GW, Wilce MC, Abell AD, Polyak SW (2012) Biotin analogues with antibacterial activity are potent inhibitors of biotin protein ligase. ACS Med Chem Lett 3:509-514.
33. Saha RP, Bahadur RP, Pal A, Mandal S, Chakrabarti P (2006) ProFace: a server for the analysis of the physicochemical features of protein-protein interfaces. BMC Struct Biol 6:11.
34. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372:774-797.
35. Schneidman-Duhovny D, Hammel M, Sali A (2010) FoXS: a web server for rapid computation and fitting of SAXS profiles. Nucleic Acids Res 38:Suppl:W540-544.
36. Volkov V, Svergun D (2003) Uniqueness of ab initio shape determination in small-angle scattering. J Appl Crystallogr 36:860-864.
37. Wriggers W, Milligan RA, McCammon JA (1999) Situs: a package for docking crystal structures into low-resolution maps from electron microscopy. J Struct Biol 125:185-195.
38. Campeau E, Gravel RA (2001) Expression in Escherichia coli of N-and C-terminally deleted human holocarboxylase synthetase. Influence of the N-terminus on biotinylation and identification of a minimum functional protein. J Biol Chem 276:12310-12316.
39. Otsuka A, Abelson J (1978) The regulatory region of the biotin operon in Escherichia coli. Nature 276:689-694.
40. Adikaram PR, Beckett D (2012) Functinal versatility of a single protein surface in two protein:protein interactions. J Mol Biol 419:223-233.
41. Bagautdinov B, Matsuura Y, Bagautdinova S, Kunishima N (2008) Protein biotinylation visualized by a complex structure of biotin protein ligase with a substrate. J Biol Chem 283:14739-14750.
42. Pendini NR, Polyak SW, Booker GW, Wallace JC, Wilce MC (2008) Purification, crystallization and preliminary crystallographic analysis of biotin protein ligase from Staphylococcus aureus. Acta Crystallogr Sect F Struct Biol Cryst Commun 64:520-523.
43. Chapman-Smith A, Turner DL, Cronan JE, Morris TW, Wallace JC (1994) Expression, biotinylation and purification of a biotin-domain peptide from the biotin carboxy carrier protein of Escherichia coli acetyl-CoA carboxylase. Biochem J 302:881-887.
44. Leslie AG (1999) Integration of macromolecular diffraction data. Acta Crystallogr D Biol Crystallogr 55:1696-1702.
45. (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50:760-763.
46. Lopez G, Valencia A, Tress ML (2007) Firestar-prediction of functionally important residues using structural templates and alignment reliability. Nucleic Acids Res 35:W573-577.
47. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximumlikelihood method. Acta Crystallogr D Biol Crystallogr 53:240-255.
48. Lovell SC, Davis IW, Arendall WB, 3rd, de Bakker PI, Word JM, Prisant MG, Richardson JS, Richardson DC (2003) Structure validation by Calpha geometry: phi,psi and Cbeta deviation. Proteins 50:437-450.
49. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66:213-221.
50. Konarev P, Volkov V, AV S, Koch M, Svergun D. PRIMUS: a windows PC-based system for small-angle scattering data analysis. J Appl Cryst 36:1277-1282.
51. Franke D, Svergun DI. DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J Appl Cryst 42:342-346.
52. The PyMOL Molecular graphics system (2002) (Version 1.5.0.2 Schrodinger, LLC.).
53. Gouet P, Robert X, Courcelle E (2003) ESPript=ENDscript: extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic Acids Res 31:3320-3323.
54. Humphrey W, Dalke A, Schulten K (1996) VMD- visual molecular dynamics. J Mol Graph 14:33-38.