Crystal structure of Bacillus anthracis virulence regulator AtxA and effects of phosphorylated histidines on multimerization and activity

Molecular Microbiology

Volumn 95, Issue 3, 2015, Pages 426-441

  Hammerstrom, Troy G ^a   Horton, Lori B ^a   Swick, Michelle C ^a   Joachimiak, Andrzej ^b   Osipiuk, Jerzy ^b   Koehler, Theresa M ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATXA PROTEIN; BACTERIAL PROTEIN; DIMER; HISTIDINE; UNCLASSIFIED DRUG; ATXA PROTEIN, BACILLUS ANTHRACIS; TRANSACTIVATOR PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BACILLUS ANTHRACIS; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; DNA BINDING; DNA BINDING DOMAIN; NONHUMAN; PHOSPHOENOLPYRUVATE CARBOHYDRATE PHOSPHOTRANSFERASE SYSTEM REGULATED DOMAIN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; BACTERIAL CAPSULE; CHEMICAL STRUCTURE; CHEMISTRY; CRYSTALLIZATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; OPERON; PATHOGENICITY; PHOSPHORYLATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; VIRULENCE; X RAY CRYSTALLOGRAPHY;

BACILLUS ANTHRACIS; BACTERIA (MICROORGANISMS);

BACILLUS ANTHRACIS; BACTERIAL CAPSULES; BACTERIAL PROTEINS; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; HISTIDINE; MODELS, MOLECULAR; MUTATION; OPERON; PHOSPHORYLATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; TRANS-ACTIVATORS; VIRULENCE;

EID: 84924590551     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12867     Document Type: Article

References (71)

1. Adams, P.D., Grosse-Kunstleve, R.W., Hung, L.W., Ioerger, T.R., McCoy, A.J., Moriarty, N.W., etal. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 58: 1948-1954.
2. Bartkus, J.M., and Leppla, S.H. (1989) Transcriptional regulation of the protective antigen gene of Bacillus anthracis. Infect Immun 57: 2295-2300.
3. Ben-Zeev, E., Fux, L., Amster-Choder, O., and Eisenstein, M. (2005) Experimental and computational characterization of the dimerization of the PTS-regulation domains of BglG from Escherichia coli. J Mol Biol 347: 693-706.
4. Bera, A.K., Zhu, J., Zalkin, H., and Smith, J.L. (2003) Functional dissection of the Bacillus subtilis pur operator site. J Bacteriol 185: 4099-4109.
5. Bertani, G. (1951) Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 62: 293-300.
6. Bourgogne, A., Drysdale, M., Hilsenbeck, S.G., Peterson, S.N., and Koehler, T.M. (2003) Global effects of virulence gene regulators in a Bacillus anthracis strain with both virulence plasmids. Infect Immun 71: 2736-2743.
7. Cachat, E., Barker, M., Read, T.D., and Priest, F.G. (2008) A Bacillus thuringiensis strain producing a polyglutamate capsule resembling that of Bacillus anthracis. FEMS Microbiol Lett 285: 220-226.
8. Casabon, I., Couture, M., Vaillancourt, K., and Vadeboncoeur, C. (2009) Kinetic studies of HPr, HPr(H15D), HPr(H15E), and HPr(His approximately P) phosphorylation by the Streptococcus salivarius HPr(Ser) kinase/phosphorylase. Biochemistry 48: 10765-10774.
9. Cataldi, A., Fouet, A., and Mock, M. (1992) Regulation of pag gene expression in Bacillus anthracis: use of a pag-lacZ transcriptional fusion. FEMS Microbiol Lett 77: 89-93.
10. Chaffin, D.O., Mentele, L.M., and Rubens, C.E. (2005) Sialylation of Group B streptococcal capsular polysaccharide is mediated by cpsK and is required for optimal capsule polymerization and expression. J Bacteriol 187: 4615-4626.
11. Chiang, C., Bongiorni, C., and Perego, M. (2011) Glucose-dependent activation of Bacillus anthracis toxin gene expression and virulence requires the carbon catabolite protein CcpA. J Bacteriol 193: 52-62.
12. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
13. 2/bicarbonate, affects AtxA synthesis. Infect Immun 65: 2576-2582.
14. Dai, Z., Sirard, J.C., Mock, M., and Koehler, T.M. (1995) The atxA gene product activates transcription of the anthrax toxin genes and is essential for virulence. Mol Microbiol 16: 1171-1181.
15. Dale, J.L., Raynor, M.J., Dwivedi, P., and Koehler, T.M. (2012) cis-Acting elements that control expression of the master virulence regulatory gene atxA in Bacillus anthracis. J Bacteriol 194: 4069-4079.
16. Davis, I.W., Murray, L.W., Richardson, J.S., and Richardson, D.C. (2004) MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes. Nucleic Acids Res 32: W615-W619.
17. Drysdale, M., Bourgogne, A., Hilsenbeck, S.G., and Koehler, T.M. (2004) atxA controls Bacillus anthracis capsule synthesis via acpA and a newly discovered regulator, acpB. J Bacteriol 186: 307-315.
18. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
19. Eschenfeldt, W.H., Makowska-Grzyska, M., Stols, L., Donnelly, M.I., Jedrzejczak, R., and Joachimiak, A. (2013) New LIC vectors for production of proteins from genes containing rare codons. J Struct Funct Genomics 14: 135-144.
20. Fouet, A., and Mock, M. (1996) Differential influence of the two Bacillus anthracis plasmids on regulation of virulence gene expression. Infect Immun 64: 4928-4932.
21. Gorrec, F., Palmer, C.M., Lebon, G., and Warne, T. (2011) Pi sampling: a methodical and flexible approach to initial macromolecular crystallization screening. Acta Crystallogr D Biol Crystallogr 67: 463-470.
22. Graille, M., Zhou, C.Z., Receveur-Brechot, V., Collinet, B., Declerck, N., and van Tilbeurgh, H. (2005) Activation of the LicT transcriptional antiterminator involves a domain swing/lock mechanism provoking massive structural changes. J Biol Chem 280: 14780-14789.
23. Green, B.D., Battisti, L., Koehler, T.M., Thorne, C.B., and Ivins, B.E. (1985) Demonstration of a capsule plasmid in Bacillus anthracis. Infect Immun 49: 291-297.
24. Hadjifrangiskou, M., and Koehler, T.M. (2008) Intrinsic curvature associated with the coordinately regulated anthrax toxin gene promoters. Microbiology 154: 2501-2512.
25. 2-signalling. Mol Microbiol 82: 634-647.
26. Himmel, S., Grosse, C., Wolff, S., Schwiegk, C., and Becker, S. (2012) Structure of the RBD-PRDI fragment of the antiterminator protein GlcT. Acta Crystallograph Sect F Struct Biol Cryst Commun 68: 751-756.
27. Holm, L., and Rosenstrom, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res 38: W545-W549.
28. Hondorp, E.R., and McIver, K.S. (2007) The Mga virulence regulon: infection where the grass is greener. Mol Microbiol 66: 1056-1065.
29. Hondorp, E.R., Hou, S.C., Hempstead, A.D., Hause, L.L., Beckett, D.M., and McIver, K.S. (2012) Characterization of the Group A Streptococcus Mga virulence regulator reveals a role for the C-terminal region in oligomerization and transcriptional activation. Mol Microbiol 83: 953-967.
30. Hondorp, E.R., Hou, S.C., Hause, L.L., Gera, K., Lee, C.E., and McIver, K.S. (2013) PTS phosphorylation of Mga modulates regulon expression and virulence in the Group A Streptococcus. Mol Microbiol 88: 1176-1193.
31. Horton, R.M., Hunt, H.D., Ho, S.N., Pullen, J.K., and Pease, L.R. (1989) Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77: 61-68.
32. Joyet, P., Derkaoui, M., Poncet, S., and Deutscher, J. (2010) Control of Bacillus subtilis mtl operon expression by complex phosphorylation-dependent regulation of the transcriptional activator MtlR. Mol Microbiol 76: 1279-1294.
33. 2 and a trans-acting element activate transcription from one of two promoters. J Bacteriol 176: 586-595.
34. Krissinel, E., and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: 774-797.
35. Laskowski, R.A., Watson, J.D., and Thornton, J.M. (2005) ProFunc: a server for predicting protein function from 3D structure. Nucleic Acids Res 33: W89-W93.
36. Lee, S.G., Krishnan, H.B., and Jez, J.M. (2014) Structural basis for regulation of rhizobial nodulation and symbiosis gene expression by the regulatory protein NolR. Proc Natl Acad Sci USA 111: 6509-6514.
37. Lei, J., Li, L.F., and Su, X.D. (2009) Crystal structures of phosphotransferase system enzymes PtxB (IIB(Asc)) and PtxA (IIA(Asc)) from Streptococcus mutans. J Mol Biol 386: 465-475.
38. McIver, K.S., and Myles, R.L. (2002) Two DNA-binding domains of Mga are required for virulence gene activation in the Group A Streptococcus. Mol Microbiol 43: 1591-1601.
39. McIver, K.S., Heath, A.S., Green, B.D., and Scott, J.R. (1995) Specific binding of the activator Mga to promoter sequences of the emm and scpA genes in the Group A Streptococcus. J Bacteriol 177: 6619-6624.
40. Marrero, R., and Welkos, S.L. (1995) The transformation frequency of plasmids into Bacillus anthracis is affected by adenine methylation. Gene 152: 75-78.
41. Mignot, T., Mock, M., and Fouet, A. (2003) A plasmid-encoded regulator couples the synthesis of toxins and surface structures in Bacillus anthracis. Mol Microbiol 47: 917-927.
42. Minor, W., Cymborowski, M., Otwinowski, Z., and Chruszcz, M. (2006) HKL-3000: the integration of data reduction and structure solution - from diffraction images to an initial model in minutes. Acta Crystallogr D Biol Crystallogr 62: 859-866.
43. Murshudov, G.N., Vagin, A.A., and Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
44. Narayanan, A., Kumar, S., Evrard, A.N., Paul, L.N., and Yernool, D.A. (2014) An asymmetric heterodomain interface stabilizes a response regulator-DNA complex. Nat Commun 5: 3282.
45. Njoroge, J.W., Nguyen, Y., Curtis, M.M., Moreira, C.G., and Sperandio, V. (2012) Virulence meets metabolism: Cra and KdpE gene regulation in enterohemorrhagic Escherichia coli. mBio 3: e00280-12.
46. Pflughoeft, K.J., Sumby, P., and Koehler, T.M. (2011) Bacillus anthracis sin locus and regulation of secreted proteases. J Bacteriol 193: 631-639.
47. Ravel, J., Jiang, L., Stanley, S.T., Wilson, M.R., Decker, R.S., Read, T.D., etal. (2009) The complete genome sequence of Bacillus anthracis Ames 'Ancestor. J Bacteriol 191: 445-446.
48. Ribardo, D.A., and McIver, K.S. (2006) Defining the Mga regulon: comparative transcriptome analysis reveals both direct and indirect regulation by Mga in the Group A Streptococcus. Mol Microbiol 62: 491-508.
49. Rosenbaum, G., Alkire, R.W., Evans, G., Rotella, F.J., Lazarski, K., Zhang, R.G., etal. (2006) The Structural Biology Center 19ID undulator beamline: facility specifications and protein crystallographic results. J Synchrotron Radiat 13: 30-45.
50. Saile, E., and Koehler, T.M. (2002) Control of anthrax toxin gene expression by the transition state regulator abrB. J Bacteriol 184: 370-380.
51. Sambrook, J.R.D. (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
52. Schmalisch, M.H., Bachem, S., and Stulke, J. (2003) Control of the Bacillus subtilis antiterminator protein GlcT by phosphorylation. Elucidation of the phosphorylation chain leading to inactivation of GlcT. J Biol Chem 278: 51108-51115.
53. Schnetz, K., Stulke, J., Gertz, S., Kruger, S., Krieg, M., Hecker, M., and Rak, B. (1996) LicT, a Bacillus subtilis transcriptional antiterminator protein of the BglG family. J Bacteriol 178: 1971-1979.
54. Shuman, S. (1989) Vaccinia DNA topoisomerase I promotes illegitimate recombination in Escherichia coli. Proc Natl Acad Sci USA 86: 3489-3493.
55. Sirard, J.C., Mock, M., and Fouet, A. (1994) The three Bacillus anthracis toxin genes are coordinately regulated by bicarbonate and temperature. J Bacteriol 176: 5188-5192.
56. Sirard, J.C., Guidi-Rontani, C., Fouet, A., and Mock, M. (2000) Characterization of a plasmid region involved in Bacillus anthracis toxin production and pathogenesis. Int J Med Microbiol 290: 313-316.
57. Solano-Collado, V., Lurz, R., Espinosa, M., and Bravo, A. (2013) The pneumococcal MgaSpn virulence transcriptional regulator generates multimeric complexes on linear double-stranded DNA. Nucleic Acids Res 41: 6975-6991.
58. Strauch, M.A., Ballar, P., Rowshan, A.J., and Zoller, K.L. (2005) The DNA-binding specificity of the Bacillus anthracis AbrB protein. Microbiology 151: 1751-1759.
59. Stulke, J., Arnaud, M., Rapoport, G., and Martin-Verstraete, I. (1998) PRD - a protein domain involved in PTS-dependent induction and carbon catabolite repression of catabolic operons in bacteria. Mol Microbiol 28: 865-874.
60. Thorne, C.B., and Belton, F.C. (1957) An agar-diffusion method for titrating Bacillus anthracis immunizing antigen and its application to a study of antigen production. J Gen Microbiol 17: 505-516.
61. van Tilbeurgh, H., Le Coq, D., and Declerck, N. (2001) Crystal structure of an activated form of the PTS regulation domain from the LicT transcriptional antiterminator. EMBO J 20: 3789-3799.
62. Tobisch, S., Stulke, J., and Hecker, M. (1999) Regulation of the lic operon of Bacillus subtilis and characterization of potential phosphorylation sites of the LicR regulator protein by site-directed mutagenesis. J Bacteriol 181: 4995-5003.
63. Tortosa, P., Declerck, N., Dutartre, H., Lindner, C., Deutscher, J., and Le Coq, D. (2001) Sites of positive and negative regulation in the Bacillus subtilis antiterminators LicT and SacY. Mol Microbiol 41: 1381-1393.
64. Tsvetanova, B., Wilson, A.C., Bongiorni, C., Chiang, C., Hoch, J.A., and Perego, M. (2007) Opposing effects of histidine phosphorylation regulate the AtxA virulence transcription factor in Bacillus anthracis. Mol Microbiol 63: 644-655.
65. Walsh, M.A., Dementieva, I., Evans, G., Sanishvili, R., and Joachimiak, A. (1999) Taking MAD to the extreme: ultrafast protein structure determination. Acta Crystallogr D Biol Crystallogr 55: 1168-1173.
66. Welkos, S., Little, S., Friedlander, A., Fritz, D., and Fellows, P. (2001) The role of antibodies to Bacillus anthracis and anthrax toxin components in inhibiting the early stages of infection by anthrax spores. Microbiology 147: 1677-1685.
67. Wenzel, M., and Altenbuchner, J. (2013) The Bacillus subtilis mannose regulator, ManR, a DNA-binding protein regulated by HPr and its cognate PTS transporter ManP. Mol Microbiol 88: 562-576.
68. Wilson, A.C., Hoch, J.A., and Perego, M. (2009) Two small c-type cytochromes affect virulence gene expression in Bacillus anthracis. Mol Microbiol 72: 109-123.
69. Wittekind, M., Reizer, J., Deutscher, J., Saier, M.H., and Klevit, R.E. (1989) Common structural changes accompany the functional inactivation of HPr by seryl phosphorylation or by serine to aspartate substitution. Biochemistry 28: 9908-9912.
70. Yanisch-Perron, C., Vieira, J., and Messing, J. (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33: 103-119.
71. Zdobnov, E.M., and Apweiler, R. (2001) InterProScan - an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17: 847-848.