WXG100 protein superfamily consists of three subfamilies and exhibits an α-helical C-terminal conserved residue pattern

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Poulsen, Christian ^a,e   Panjikar, Santosh ^a,c,d   Holton, Simon J ^a,f   Wilmanns, Matthias ^a   Song, Young Hwa ^a,b  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b UNIVERSITY OF LÜBECK   (Germany)

^c AUSTRALIAN SYNCHROTRON   (Australia)

^d MONASH UNIVERSITY   (Australia)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

^f BAYER PHARMA AG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CULTURE FILTRATE PROTEIN 10; EARLY SECRETORY ANTIGENIC TARGET 6; HETERODIMER; HOMODIMER; OLIGOMER; PROTEIN ESXA; PROTEIN WXG100; T LYMPHOCYTE ANTIGEN; UNCLASSIFIED DRUG; BIOPOLYMER;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BIOINFORMATICS; CARBOXY TERMINAL SEQUENCE; GENETIC CONSERVATION; OPERON; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN SECRETION; PROTEIN STRUCTURE; SAGESXA GENE; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; STREPTOCOCCUS AGALACTIAE; STRUCTURE ANALYSIS; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; MYCOBACTERIUM TUBERCULOSIS; NUCLEOTIDE SEQUENCE; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BIOPOLYMERS; CONSERVED SEQUENCE; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM TUBERCULOSIS; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84896294684     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0089313     Document Type: Article

References (49)

1. Finlay BB, Falkow S (1997) Common themes in microbial pathogenicity revisited. Microbiol Mol Biol Rev 61: 136-169. (Pubitemid 27283798)
2. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537-544. (Pubitemid 28319235)
3. Brodin P, Majlessi L, Marsollier L, de Jonge MI, Bottai D, et al. (2006) Dissection of ESAT-6 system 1 of Mycobacterium tuberculosis and impact on immunogenicity and virulence. Infect Immun 74: 88-98. (Pubitemid 43023062)
4. McLaughlin B, Chon JS, MacGurn JA, Carlsson F, Cheng TL, et al. (2007) A mycobacterium ESX-1-secreted virulence factor with unique requirements for export. PLoS Pathog 3: e105.
5. Bitter W, Houben EN, Bottai D, Brodin P, Brown EJ, et al. (2009) Systematic genetic nomenclature for type VII secretion systems. PLoS Pathog 5: e1000507.
6. Pallen MJ (2002) The ESAT-6/WXG100 superfamily - and a new Gram-positive secretion system? Trends Microbiol 10: 209-212.
7. Garufi G, Butler E, Missiakas D (2008) ESAT-6-like protein secretion in Bacillus anthracis. J Bacteriol 190: 7004-7011.
8. Burts M, Williams W, DeBord K, Missiakas D (2005) EsxA and EsxB are secreted by an ESAT-6-like system that is required for the pathogenesis of Staphylococcus aureus infections. Proc Natl Acad Sci U S A 102: 1169-1174. (Pubitemid 40170744)
9. Daleke MH, Ummels R, Bawono P, Heringa J, Vandenbroucke-Grauls CM, et al. (2012) General secretion signal for the mycobacterial type VII secretion pathway. Proc Natl Acad Sci U S A 109: 11342-11347.
10. Abdallah A, Gey van Pittius N, Champion P, Cox J, Luirink J, et al. (2007) Type VII secretion-mycobacteria show the way. Nat Rev Microbiol 5: 883-891.
11. Renshaw PS, Lightbody KL, Veverka V, Muskett FW, Kelly G, et al. (2005) Structure and function of the complex formed by the tuberculosis virulence factors CFP-10 and ESAT-6. Embo J 24: 2491-2498. (Pubitemid 41076306)
12. Sundaramoorthy R, Fyfe PK, Hunter WN (2008) Structure of Staphylococcus aureus EsxA suggests a contribution to virulence by action as a transport chaperone and/or adaptor protein. J Mol Biol 383: 603-614.
13. Poulsen C, Holton S, Geerlof A, Wilmanns M, Song Y (2010) Stoichiometric protein complex formation and over-expression using the prokaryotic native operon structure. FEBS Lett 584: 669-674.
14. Champion PA, Stanley SA, Champion MM, Brown EJ, Cox JS (2006) C-terminal signal sequence promotes virulence factor secretion in Mycobacterium tuberculosis. Science 313: 1632-1636. (Pubitemid 44414036)
15. Fortune SM, Jaeger A, Sarracino DA, Chase MR, Sassetti CM, et al. (2005) Mutually dependent secretion of proteins required for mycobacterial virulence. Proc Natl Acad Sci U S A 102: 10676-10681. (Pubitemid 41061613)
16. Shukla A, Pallen M, Anthony M, White SA (2010) The homodimeric GBS1074 from Streptococcus agalactiae. Acta Crystallogr Sect F Struct Biol Cryst Commun 66: 1421-1425.
17. Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, et al. (2009) A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462: 1056-1060.
18. Frickey T, Lupas A (2004) CLANS: a Java application for visualizing protein families based on pairwise similarity. Bioinformatics 20: 3702-3704. (Pubitemid 40136822)
19. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755. (Pubitemid 32851390)
20. Biegert A, Mayer C, Remmert M, Soding J, Lupas AN (2006) The MPI Bioinformatics Toolkit for protein sequence analysis. Nucleic Acids Res 34: W335-339. (Pubitemid 44529789)
21. Teutschbein J, Schumann G, Mollmann U, Grabley S, Cole ST, et al. (2009) A protein linkage map of the ESAT-6 secretion system 1 (ESX-1) of Mycobacterium tuberculosis. Microbiol Res 164: 253-259.
22. Daugelat S, Kowall J, Mattow J, Bumann D, Winter R, et al. (2003) The RD1 proteins of Mycobacterium tuberculosis: expression in Mycobacterium smegmatis and biochemical characterization. Microbes Infect 5: 1082-1095. (Pubitemid 37211469)
23. Singh A, Mai D, Kumar A, Steyn AJ (2006) Dissecting virulence pathways of Mycobacterium tuberculosis through protein-protein association. Proc Natl Acad Sci U S A 103: 11346-11351. (Pubitemid 44156520)
24. Renshaw PS, Panagiotidou P, Whelan A, Gordon SV, Hewinson RG, et al. (2002) Conclusive evidence that the major T-cell antigens of the Mycobacterium tuberculosis complex ESAT-6 and CFP-10 form a tight, 1:1 complex and characterization of the structural properties of ESAT-6, CFP-10, and the ESAT-6*CFP-10 complex. Implications for pathogenesis and virulence. J Biol Chem 277: 21598-21603. (Pubitemid 34952307)
25. Sutcliffe IC (2011) New insights into the distribution of WXG100 protein secretion systems. Antonie Van Leeuwenhoek 99: 127-131.
26. Gey van Pittius NC, Sampson SL, Lee H, Kim Y, van Helden PD, et al. (2006) Evolution and expansion of the Mycobacterium tuberculosis PE and PPE multigene families and their association with the duplication of the ESAT-6 (esx) gene cluster regions. BMC Evol Biol 6: 95.
27. Bern M, Goldberg D (2005) Automatic selection of representative proteins for bacterial phylogeny. BMC Evol Biol 5: 34.
28. Lightbody KL, Ilghari D, Waters LC, Carey G, Bailey MA, et al. (2008) Molecular features governing the stability and specificity of functional complex formation by Mycobacterium tuberculosis CFP-10/ESAT-6 family proteins. J Biol Chem 283: 17681-17690.
29. Anderson M, Aly KA, Chen YH, Missiakas D (2013) Secretion of atypical protein substrates by the ESAT-6 Secretion System of Staphylococcus aureus. Mol Microbiol 90: 734-743.
30. Ize B, Palmer T (2006) Microbiology. Mycobacteria's export strategy. Science 313: 1583-1584.
31. Kabsch W Xds. Acta Crystallogr D Biol Crystallogr 66: 125-132.
32. McCoy AJ (2007) Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr D Biol Crystallogr 63: 32-41.
33. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, et al. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 58: 1948-1954. (Pubitemid 35337293)
34. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132. (Pubitemid 41742764)
35. Panjikar S, Parthasarathy V, Lamzin VS, Weiss MS, Tucker PA (2005) Auto-Rickshaw: an automated crystal structure determination platform as an efficient tool for the validation of an X-ray diffraction experiment. Acta Crystallogr D Biol Crystallogr 61: 449-457. (Pubitemid 43934605)
36. Dodson EJ, Winn M, Ralph A (1997) Collaborative Computational Project, number 4: providing programs for protein crystallography. Methods Enzymol 277: 620-633. (Pubitemid 27390943)
37. Sheldrick GM (2008) A short history of SHELX. Acta Crystallogr A 64: 112-122.
38. Schneider TR (2002) A genetic algorithm for the identification of conformationally invariant regions in protein molecules. Acta Crystallogr D Biol Crystallogr 58: 195-208.
39. Hoa Q (2004) Abs: a program to determine absolute configuration and evaluate anomalous scatterer substructure. Journal of Applied Crystallography 37: 498-499.
40. Terwilliger T (2004) SOLVE and RESOLVE: automated structure solution, density modification and model building. J Synchrotron Radiat 11: 49-52.
41. Panjikar S, Parthasarathy V, Lamzin VS, Weiss MS, Tucker PA (2009) On the combination of molecular replacement and single-wavelength anomalous diffraction phasing for automated structure determination. Acta Crystallogr D Biol Crystallogr 65: 1089-1097.
42. Perrakis A, Harkiolaki M, Wilson KS, Lamzin VS (2001) ARP/wARP and molecular replacement. Acta Crystallogr D Biol Crystallogr 57: 1445-1450. (Pubitemid 36117195)
43. Kirschner A, Frishman D (2008) Prediction of beta-turns and beta-turn types by a novel bidirectional Elman-type recurrent neural network with multiple output layers (MOLEBRNN). Gene 422: 22-29.
44. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948. (Pubitemid 350162903)
45. Abascal F, Valencia A (2002) Clustering of proximal sequence space for the identification of protein families. Bioinformatics 18: 908-921. (Pubitemid 34846473)
46. Harrington ED, Singh AH, Doerks T, Letunic I, von Mering C, et al. (2007) Quantitative assessment of protein function prediction from metagenomics shotgun sequences. Proc Natl Acad Sci U S A 104: 13913-13918. (Pubitemid 350003312)
47. Roback P, Beard J, Baumann D, Gille C, Henry K, et al. (2007) A predicted operon map for Mycobacterium tuberculosis. Nucleic Acids Res 35: 5085-5095. (Pubitemid 47394193)
48. Brunger AT, Adams PD (2002) Molecular dynamics applied to X-ray structure refinement. Acc Chem Res 35: 404-412.
49. Ramachandran GN (1963) Protein Structure and Crystallography. Science 141: 288-291.