The crystal structure of AphB, a virulence gene activator from Vibrio cholerae, reveals residues that influence its response to oxygen and pH

Molecular Microbiology

Volumn 83, Issue 3, 2012, Pages 457-470

  Taylor, Jennifer L ^a,c   de Silva, Rukman S ^a,c   Kovacikova, Gabriela ^b   Lin, Wei ^b   Taylor, Ronald K ^b   Skorupski, Karen ^b   Kull, F Jon ^a  

^a Lamont Doherty Earth Observatory   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAEROBIC GROWTH; APHB GENE; ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE MUTATION; INTRACELLULAR SIGNALING; LIGAND BINDING; MOLECULAR DYNAMICS; NONHUMAN; OXYGEN CONSUMPTION; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DNA BINDING; PROTEIN DOMAIN; RESIDUE ANALYSIS; STRUCTURE ANALYSIS; TRANSCRIPTION REGULATION; VIBRIO CHOLERAE; X RAY CRYSTALLOGRAPHY;

BACTERIAL PROTEINS; CLONING, MOLECULAR; DNA MUTATIONAL ANALYSIS; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN-ION CONCENTRATION; MUTATION; OXYGEN; PROTEIN STRUCTURE, QUATERNARY; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; VIBRIO CHOLERAE;

VIBRIO CHOLERAE;

EID: 84856061400     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07919.x     Document Type: Article

References (60)

1. Abuaita, B.H., and Withey, J.H. (2009) Bicarbonate induces Vibrio cholerae virulence gene expression by enhancing ToxT activity. Infect Immun 77: 4111-4120.
2. Adams, P., Afonine, P., and Bunkoczi, G. (2010) phenix: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr D66: 213-221.
3. Afonine, P., Grosse-Kunstleve, R., and Adams, P.D. (2005) The Phenix refinement framework. CCP4 newsletter July, Contribution 8.
4. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
5. Aravind, L., Anantharaman, V., Balaji, S., Babu, M.M., and Iyer, L.M. (2005) The many faces of the helix-turn-helix domain: transcription regulation and beyond. FEMS Microbiol Rev 29: 231-262.
6. Carroll, P., Tashima, K., and Rogers, M. (1997) Phase variation in tcpH modulates expression of the ToxR regulon in Vibrio cholerae. Mol Microbiol 25: 1099-1111.
7. Champion, G.A., Neely, M.N., Brennan, M.A., and DiRita, V.J. (1997) A branch in the ToxR regulatory cascade of Vibrio cholerae revealed by characterization of toxT mutant strains. Mol Microbiol 23: 323-331.
8. Chatterjee, A., Dutta, P.K., and Chowdhury, R. (2007) Effect of fatty acids and cholesterol present in bile on expression of virulence factors and motility of Vibrio cholerae. Infect Immun 75: 1946-1953.
9. De Silva, R.S., Kovacikova, G., Lin, W., Taylor, R.K., Skorupski, K., and Kull, F.J. (2005) Crystal structure of the virulence gene activator AphA from Vibrio cholerae reveals it is a novel member of the winged helix transcription factor superfamily. J Biol Chem 280: 13779-13783.
10. DeLano, W. (2002) The PyMOL Molecular Graphics System. San Carlos, CA: DeLano Scientific.
11. Devesse, L., Smirnova, I., Lönneborg, R., Kapp, U., Brzezinski, P., Leonard, G.A., and Dian, C. (2011) Crystal structures of the DntR inducer binding domains in complex with salicylate offer insights into the activation of LysR-type transcriptional regulators. Mol Microbiol 81: 354-367.
12. Ding, Y., and Waldor, M.K. (2003) Deletion of a Vibrio cholerae ClC channel results in acid sensitivity and enhanced intestinal colonization. Infect Immun 71: 4197-4200.
13. DiRita, V.J., Parsot, C., Jander, G., and Mekalanos, J.J. (1991) Regulatory cascade controls virulence in Vibrio cholerae. Proc Natl Acad Sci USA 88: 5403-5407.
14. Dutzler, R. (2006) The ClC family of chloride channels and transporters. Curr Opin Struct Biol 16: 439-446.
15. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr D60: 2126-2132.
16. Ezezika, O.C., Haddad, S., Clark, T.J., Neidle, E.L., and Momany, C. (2007) Distinct effector-binding sites enable synergistic transcriptional activation by BenM, a LysR-type regulator. J Mol Biol 367: 616-629.
17. Häse, C.C., and Mekalanos, J.J. (1998) TcpP protein is a positive regulator of virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci USA 95: 730-734.
18. Higgins, D.E., and DiRita, V.J. (1994) Transcriptional control of toxT, a regulatory gene in the ToxR regulon of Vibrio cholerae. Mol Microbiol 14: 17-29.
19. Higgins, D.E., Nazareno, E., and DiRita, V.J. (1992) The virulence gene activator ToxT from Vibrio cholerae is a member of the AraC family of transcriptional activators. J Bacteriol 174: 6974-6980.
20. Kabsch, W. (2010) XDS. Acta Crystallogr D Biol Crystallogr D66: 125-132.
21. Karaolis, D.K., Johnson, J.A., Bailey, C.C., Boedeker, E.C., Kaper, J.B., and Reeves, P.R. (1998) A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains. Proc Natl Acad Sci USA 95: 3134-3139.
22. Kovacikova, G., and Skorupski, K. (1999) A Vibrio cholerae LysR homolog, AphB, cooperates with AphA at the tcpPH promoter to activate expression of the ToxR virulence cascade. J Bacteriol 181: 4250-4256.
23. Kovacikova, G., and Skorupski, K. (2001) Overlapping binding sites for the virulence gene regulators AphA, AphB and cAMP-CRP at the Vibrio cholerae tcpPH promoter. Mol Microbiol 41: 393-407.
24. Kovacikova, G., Lin, W., and Skorupski, K. (2004) Vibrio cholerae AphA uses a novel mechanism for virulence gene activation that involves interaction with the LysR-type regulator AphB at the tcpPH promoter. Mol Microbiol 53: 129-142.
25. Kovacikova, G., Lin, W., and Skorupski, K. (2005) Dual regulation of genes involved in acetoin biosynthesis and motility/biofilm formation by the virulence activator AphA and the acetate-responsive LysR-type regulator AlsR in Vibrio cholerae. Mol Microbiol 57: 420-433.
26. Kovacikova, G., Lin, W., and Skorupski, K. (2010) The LysR-type virulence activator AphB regulates the expression of genes in Vibrio cholerae in response to low pH and anaerobiosis. J Bacteriol 192: 4181-4191.
27. Krukonis, E.S., Yu, R.R., and DiRita, V.J. (2000) The Vibrio cholerae ToxR/TcpP/ToxT virulence cascade: distinct roles for two membrane-localized transcriptional activators on a single promoter. Mol Microbiol 38: 67-84.
28. Kullik, I., Stevens, J., Toledano, M.B., and Storz, G. (1995) Mutational analysis of the redox-sensitive transcriptional regulator OxyR: regions important for DNA binding and multimerization. J Bacteriol 177: 1285-1291.
29. Lang, G.H., and Ogawa, N. (2009) Mutational analysis of the inducer recognition sites of the LysR-type transcriptional regulator TfdT of Burkholderia sp. NK8. Appl Microbiol Biotechnol 83: 1085-1094.
30. Laskowski, R.A. (1995) surfnet: a program for visualizing molecular surfaces, cavities and intermolecular interactions. J Mol Graph 13: 323-330.
31. Liu, Z., Yang, M., Peterfreund, G.L., Tsou, A.M., Selamoglu, N., Daldal, F., etal. (2011) Vibrio cholerae anaerobic induction of virulence gene expression is controlled by thiol-based switches of virulence regulator AphB. Proc Natl Acad Sci USA 108: 810-815.
32. Lochowska, A., Iwanicka-Nowicka, R., Plochocka, D., and Hryniewicz, M.M. (2001) Functional dissection of the LysR-type CysB transcriptional regulator. Regions important for DNA binding, inducer response, oligomerization, and positive control. J Biol Chem 276: 2098-2107.
33. Lowden, M.J., Skorupski, K., Pellegrini, M., Chiorazzo, M.G., Taylor, R.K., and Kull, F.J. (2010) Structure of Vibrio cholerae ToxT reveals a mechanism for fatty acid regulation of virulence genes. Proc Natl Acad Sci USA 107: 2860-2865.
34. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C., and Read, R.J. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
35. Maddocks, S.E., and Oyston, P.C.F. (2008) Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology 154: 3609-3623.
36. Marrero, K., Sánchez, A., Rodríguez-Ulloa, A., González, L.J., Castellanos-Serra, L., Paz-Lago, D., etal. (2009) Anaerobic growth promotes synthesis of colonization factors encoded at the Vibrio pathogenicity island in Vibrio cholerae El Tor. Res Microbiol 160: 48-56.
37. Matson, J.S., Withey, J.H., and DiRita, V.J. (2007) Regulatory networks controlling Vibrio cholerae virulence gene expression. Infect Immun 75: 5542-5549.
38. Merrell, D.S., and Camilli, A. (1999) The cadA gene of Vibrio cholerae is induced during infection and plays a role in acid tolerance. Mol Microbiol 34: 836-849.
39. Merrell, D.S., and Camilli, A. (2000) Regulation of Vibrio cholerae genes required for acid tolerance by a member of the 'ToxR-like' family of transcriptional regulators. J Bacteriol 182: 5342-5350.
40. Merritt, E. (2006a) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr D Biol Crystallogr D62: 439-450.
41. Merritt, E. (2006b) TLSMD web server for the generation of multi-group TLS models. J Appl Crystallogr 39: 109-111.
42. Miller, J. (1972) Experiments in Molecular Genetics. New York: Cold Spring Harbor Laboratory, pp. 352-355.
43. Miller, V.L., Taylor, R.K., and Mekalanos, J.J. (1987) Cholera toxin transcriptional activator toxR is a transmembrane DNA binding protein. Cell 48: 271-279.
44. Monferrer, D., Tralau, T., Kertesz, M.A., Dix, I., Solà, M., and Usón, I. (2010) Structural studies on the full-length LysR-type regulator TsaR from Comamonas testosteroni T-2 reveal a novel open conformation of the tetrameric LTTR fold. Mol Microbiol 75: 1199-1214.
45. Muraoka, S., Okumura, R., Ogawa, N., Nonaka, T., Miyashita, K., and Senda, T. (2003) Crystal structure of a full-length LysR-type transcriptional regulator, CbnR: unusual combination of two subunit forms and molecular bases for causing and changing DNA bend. J Mol Biol 328: 555-566.
46. 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 D53: 240-255.
47. Perrakis, A., Morris, R., and Lamzin, V.S. (1999) Automated protein model building combined with iterative structure refinement. Nat Struct Biol 6: 458-463.
48. Pratt, J.T., Ismail, A.M., and Camilli, A. (2010) PhoB regulates both environmental and virulence gene expression in Vibrio cholerae. Mol Microbiol 77: 1595-1605.
49. Ruangprasert, A., Craven, S.H., Neidle, E.L., and Momany, C. (2010) Full-length structures of BenM and two variants reveal different oligomerization schemes for LysR-type transcriptional regulators. J Mol Biol 404: 568-586.
50. Sainsbury, S., Lane, L.A., Ren, J., Gilbert, R.J., Saunders, N.J., Robinson, C.V., etal. (2009) The structure of CrgA from Neisseria meningitidis reveals a new octameric assembly state for LysR transcriptional regulators. Nucleic Acids Res 37: 4545-4558.
51. Schell, M.A. (1993) Molecular biology of the LysR family of transcriptional regulators. Annu Rev Microbiol 47: 597-626.
52. Skorupski, K., and Taylor, R.K. (1999) A new level in the Vibrio cholerae ToxR virulence cascade: AphA is required for transcriptional activation of the tcpPH operon. Mol Microbiol 31: 763-771.
53. Stec, E., Witkowska-Zimny, M., Hryniewicz, M.M., Neumann, P., Wilkinson, A.J., Brzozowski, A.M., etal. (2006) Structural basis of the sulphate starvation response in E. coli: crystal structure and mutational analysis of the cofactor-binding domain of the Cbl transcriptional regulator. J Mol Biol 364: 309-322.
54. Studier, F.W. (2005) Protein production by auto-induction in high-density shaking cultures. Protein Expr Purif 41: 207-234.
55. Tan, K., Xu, X., Cui, H., Chin, S., Savchenko, A., Edwards, A., and Joachimiak, A. (2010) The crystal structure of a possible transcription regulator protein from Sinorhizobium meliloti 1021.
56. Taylor, R.K., Miller, V.L., Furlong, D.B., and Mekalanos, J.J. (1987) Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc Natl Acad Sci USA 84: 2833-2837.
57. Terwilliger, T.C. (2003) Automated main-chain model building by template matching and iterative fragment extension. Acta Crystallogr D Biol Crystallogr 59: 38-44.
58. Terwilliger, T.C., Grosse-Kunstleve, R.W., Afonine, P.V., Moriarty, N.W., Zwart, P.H., Hung, L.W., etal. (2008) Iterative model building, structure refinement and density modification with the phenix AutoBuild wizard. Acta Crystallogr D Biol Crystallogr D64: 61-69.
59. Waldor, M.K., and Mekalanos, J.J. (1996) Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272: 1910-1914.
60. Zhou, X., Lou, Z., Fu, S., Yang, A., Shen, H., Li, Z., etal. (2010) Crystal structure of ArgP from Mycobacterium tuberculosis confirms two distinct conformations of full-length LysR transcriptional regulators and reveals its function in DNA binding and transcriptional regulation. J Mol Biol 396: 1012-1024.