The Bordetella pertussis model of exquisite gene control by the global transcription factor BvgA

Microbiology (United Kingdom)

Volumn 158, Issue 7, 2012, Pages 1665-1676

  Decker, Kimberly B ^a,c   James, Tamara D ^a   Stibitz, Scott ^b   Hinton, Deborah M ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; BVGA PROTEIN; CYTOSINE; PROTEIN; RNA POLYMERASE; UNCLASSIFIED DRUG;

BACTERIAL VIRULENCE; BASE MISPAIRING; BINDING AFFINITY; BINDING SITE; BORDETELLA PERTUSSIS; DNA BINDING; DNA HELIX; DNA SEQUENCE; ESCHERICHIA COLI; FIM2 GENE; FIM3 GENE; GENE; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENE SEQUENCE; GENETIC VARIABILITY; HELICOBACTER PYLORI; MUTATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; RNA REPLICATION; TRANSCRIPTION INITIATION;

BACTERIAL PROTEINS; BORDETELLA PERTUSSIS; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MODELS, BIOLOGICAL; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN MULTIMERIZATION; TRANSCRIPTION FACTORS;

BACTERIA (MICROORGANISMS); BORDETELLA PERTUSSIS;

EID: 84863647217     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.058941-0     Document Type: Review

References (93)

1. Akerley, B. J., Cotter, P. A. & Miller, J. F. (1995). Ectopic expression of the flagellar regulon alters development of the Bordetella-host interaction. Cell 80, 611-620.
2. Barnard, A., Wolfe, A. & Busby, S. (2004). Regulation at complex bacterial promoters: how bacteria use different promoter organizations to produce different regulatory outcomes. Curr Opin Microbiol 7, 102-108.
3. Baxter, K., Lee, J., Minakhin, L., Severinov, K. & Hinton, D. M. (2006). Mutational analysis of sigma70 region 4 needed for appropriation by the bacteriophage T4 transcription factors AsiA and MotA. J Mol Biol 363, 931-944.
4. Benoff, B., Yang, H., Lawson, C. L., Parkinson, G., Liu, J., Blatter, E., Ebright, Y. W., Berman, H. M. & Ebright, R. H. (2002). Structural basis of transcription activation: the CAP-alpha CTD-DNA complex. Science 297, 1562-1566.
5. 70 is recruited to PhoB promoters. EMBO J 30, 3776-3785.
6. Bonocora, R. P., Caignan, G., Woodrell, C., Werner, M. H. & Hinton, D. M. (2008). A basic/hydrophobic cleft of the T4 activatorMotA interacts with the C-terminus of E. coli sigma70 to activate middle gene transcription. Mol Microbiol 69, 331-343.
7. Bootsma, H. J., Cummings, C. A., Relman, D. A. & Miller, J. F. (2002). Global expression analysis of the Bordetella virulence regulon. National Meeting of the American Society for Microbiology 102, abstract 1572.
8. Bordet, J. & Gengou, O. (1906). Le microbe de la coqueluche. Ann Inst Pasteur (Paris) 20, 731-741.
9. Boucher, P. E. & Stibitz, S. (1995). Synergistic binding of RNA polymerase and BvgA phosphate to the pertussis toxin promoter of Bordetella pertussis. J Bacteriol 177, 6486-6491.
10. Boucher, P. E., Menozzi, F. D. & Locht, C. (1994). The modular architecture of bacterial response regulators. Insights into the activation mechanism of the BvgA transactivator of Bordetella pertussis. J Mol Biol 241, 363-377.
11. Boucher, P. E., Murakami, K., Ishihama, A. & Stibitz, S. (1997). Nature of DNA binding and RNA polymerase interaction of the Bordetella pertussis BvgA transcriptional activator at the fha promoter. J Bacteriol 179, 1755-1763.
12. Boucher, P. E., Yang, M. S., Schmidt, D. M. & Stibitz, S. (2001). Genetic and biochemical analyses of BvgA interaction with the secondary binding region of the fha promoter of Bordetella pertussis. J Bacteriol 183, 536-544.
13. Boucher, P. E., Maris, A. E., Yang, M. S. & Stibitz, S. (2003). The response regulator BvgA and RNA polymerase alpha subunit Cterminal domain bind simultaneously to different faces of the same segment of promoter DNA. Mol Cell 11, 163-173.
14. Bouchez, V., Caro, V., Levillain, E., Guigon, G. & Guiso, N. (2008). Genomic content of Bordetella pertussis clinical isolates circulating in areas of intensive children vaccination. PLoS ONE 3, e2437.
15. Bouchez, V., Brun, D., Cantinelli, T., Dore, G., Njamkepo, E. & Guiso, N. (2009). First report and detailed characterization of B. pertussis isolates not expressing Pertussis Toxin or Pertactin. Vaccine 27, 6034-6041.
16. Brinig, M. M., Cummings, C. A., Sanden, G. N., Stefanelli, P., Lawrence, A. & Relman, D. A. (2006). Significant gene order and expression differences in Bordetella pertussis despite limited gene content variation. J Bacteriol 188, 2375-2382.
17. Browning, D. F. & Busby, S. J. (2004). The regulation of bacterial transcription initiation. Nat Rev Microbiol 2, 57-65.
18. Campbell, E. A., Muzzin, O., Chlenov, M., Sun, J. L., Olson, C. A., Weinman, O., Trester-Zedlitz, M. L. & Darst, S. A. (2002). Structure of the bacterial RNA polymerase promoter specificity sigma subunit. Mol Cell 9, 527-539.
19. Caro, V., Hot, D., Guigon, G., Hubans, C., Arrivé, M., Soubigou, G., Renauld-Mongénie, G., Antoine, R., Locht, C. & other authors (2006). Temporal analysis of French Bordetella pertussis isolates by comparative whole-genome hybridization. Microbes Infect 8, 2228-2235.
20. CDC (1995). Pertussis-United States, January 1992-June 1995. MMWR Morb Mortal Wkly Rep 44, 525-529.
21. CDC (2011). Pertussis (Whooping Cough). Outbreaks. www.cdc.gov/ vaccines/pubs/pinkbook/pert.html
22. Chen, Q., Decker, K. B., Boucher, P. E., Hinton, D. & Stibitz, S. (2010). Novel architectural features of Bordetella pertussis fimbrial subunit promoters and their activation by the global virulence regulator BvgA. Mol Microbiol 77, 1326-1340.
23. Cotter, P. A. & DiRita, V. J. (2000). Bacterial virulence gene regulation: an evolutionary perspective. Annu Rev Microbiol 54, 519-565.
24. Cotter, P. A. & Jones, A. M. (2003). Phosphorelay control of virulence gene expression in Bordetella. Trends Microbiol 11, 367-373.
25. Cotter, P. A. & Miller, J. F. (1994). BvgAS-mediated signal transduction: analysis of phase-locked regulatory mutants of Bordetella bronchiseptica in a rabbit model. Infect Immun 62, 3381-3390.
26. de Melker, H. E., Schellekens, J. F. P., Neppelenbroek, S. E., Mooi, F. R., Rümke, H. C. & Conyn-van Spaendonck, M. A. E. (2000). Reemergence of pertussis in the highly vaccinated population of the Netherlands: observations on surveillance data. Emerg Infect Dis 6, 348-357.
27. Decker, K. B., Chen, Q., Hsieh, M. L., Boucher, P., Stibitz, S. & Hinton, D. M. (2011). Different requirements for σ Region 4 in BvgA activation of the Bordetella pertussis promoters P(fim3) and P(fhaB). J Mol Biol 409, 692-709.
28. Diavatopoulos, D. A., Cummings, C. A., Schouls, L. M., Brinig, M. M., Relman, D. A. & Mooi, F. R. (2005). Bordetella pertussis, the causative agent of whooping cough, evolved from a distinct, human-associated lineage of B. bronchiseptica. PLoS Pathog 1, e45.
29. Dorman, C. J. (1995). 1995 Fleming Lecture. DNA topology and the global control of bacterial gene expression: implications for the regulation of virulence gene expression. Microbiology 141, 1271-1280.
30. Dove, S. L., Darst, S. A. & Hochschild, A. (2003). Region 4 of sigma as a target for transcription regulation. Mol Microbiol 48, 863-874.
31. Dybvig, K. (1993). DNA rearrangements and phenotypic switching in prokaryotes. Mol Microbiol 10, 465-471.
32. Galperin, M. Y. (2010). Diversity of structure and function of response regulator output domains. Curr Opin Microbiol 13, 150-159.
33. Gangarosa, E. J., Galazka, A. M., Wolfe, C. R., Phillips, L. M., Gangarosa, R. E., Miller, E. & Chen, R. T. (1998). Impact of antivaccine movements on pertussis control: the untold story. Lancet 351, 356-361.
34. García San Miguel, L., Quereda, C., Martínez, M., Martín-Dávila, P., Cobo, J. & Guerrero, A. (1998). Bordetella bronchiseptica cavitary pneumonia in a patient with AIDS. Eur J Clin Microbiol Infect Dis 17, 675-676.
35. Geier, D. & Geier, M. (2002). The true story of pertussis vaccination: a sordid legacy? J Hist Med Allied Sci 57, 249-284.
36. Gerlach, G., von Wintzingerode, F., Middendorf, B. & Gross, R. (2001). Evolutionary trends in the genus Bordetella. Microbes Infect 3, 61-72.
37. Geuijen, C. A., Willems, R. J., Bongaerts, M., Top, J., Gielen, H. & Mooi, F. R. (1997). Role of the Bordetella pertussis minor fimbrial subunit, FimD, in colonization of the mouse respiratory tract. Infect Immun 65, 4222-4228.
38. Gogol, E. B., Cummings, C. A., Burns, R. C. & Relman, D. A. (2007). Phase variation and microevolution at homopolymeric tracts in Bordetella pertussis. BMC Genomics 8, 122.
39. Gourse, R. L., Ross, W. & Gaal, T. (2000). UPs and downs in bacterial transcription initiation: the role of the alpha subunit of RNA polymerase in promoter recognition. Mol Microbiol 37, 687-695.
40. Gries, T. J., Kontur, W. S., Capp, M. W., Saecker, R. M. & Record, M. T., Jr (2010). One-step DNA melting in the RNA polymerase cleft opens the initiation bubble to form an unstable open complex. Proc Natl Acad Sci U S A 107, 10418-10423.
41. Gruber, T. M. & Gross, C. A. (2003). Multiple sigma subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol 57, 441-466.
42. Halperin, S. A. (2007). The control of pertussis-2007 and beyond. N Engl J Med 356, 110-113.
43. Heck, D. V., Trus, B. L. & Steven, A. C. (1996). Three-dimensional structure of Bordetella pertussis fimbriae. J Struct Biol 116, 264-269.
44. Heikkinen, E., Kallonen, T., Saarinen, L., Sara, R., King, A. J., Mooi, F. R., Soini, J. T., Mertsola, J. & He, Q. S. (2007). Comparative genomics of Bordetella pertussis reveals progressive gene loss in Finnish strains. PLoS ONE 2, e904.
45. Heikkinen, E., Xing, D. K., Olander, R. M., Hytönen, J., Viljanen, M. K., Mertsola, J. & He, Q. (2008). Bordetella pertussis isolates in Finland: serotype and fimbrial expression. BMC Microbiol 8, 162.
46. Henderson, I. R., Owen, P. & Nataro, J. P. (1999). Molecular switches-the ON and OFF of bacterial phase variation. Mol Microbiol 33, 919-932.
47. Herrou, J., Debrie, A. S., Willery, E., Renauld-Mongénie, G., Locht, C., Mooi, F., Jacob-Dubuisson, F. & Antoine, R. (2009). Molecular evolution of the two-component system BvgAS involved in virulence regulation in Bordetella. PLoS ONE 4, e6996.
48. Hinton, D. M. (2010). Transcriptional control in the prereplicative phase of T4 development. Virol J 7, 289.
49. Hobman, J. L., Wilkie, J. & Brown, N. L. (2005). A design for life: prokaryotic metal-binding MerR family regulators. Biometals 18, 429-436.
50. Hook-Barnard, I. G. & Hinton, D. M. (2007). Transcription initiation by mix and match elements: flexibility for polymerase binding to bacterial promoters. Gene Regul Syst Bio 1, 275-293.
51. Jain, D., Kim, Y., Maxwell, K. L., Beasley, S., Zhang, R., Gussin, G. N., Edwards, A. M. & Darst, S. A. (2005). Crystal structure of bacteriophage lambda cII and its DNA complex. Mol Cell 19, 259-269.
52. Karimova, G. & Ullmann, A. (1997). Characterization of DNA binding sites for the BvgA protein of Bordetella pertussis. J Bacteriol 179, 3790-3792.
53. Karimova, G., Bellalou, J. & Ullmann, A. (1996). Phosphorylationdependent binding of BvgA to the upstream region of the cyaA gene of Bordetella pertussis. Mol Microbiol 20, 489-496.
54. Kerr, J. R. & Matthews, R. C. (2000). Bordetella pertussis infection: pathogenesis, diagnosis, management, and the role of protective immunity. Eur J Clin Microbiol Infect Dis 19, 77-88.
55. Kinnear, S. M., Boucher, P. E., Stibitz, S. & Carbonetti, N. H. (1999). Analysis of BvgA activation of the pertactin gene promoter in Bordetella pertussis. J Bacteriol 181, 5234-5241.
56. Kinnear, S. M., Marques, R. R. & Carbonetti, N. H. (2001). Differential regulation of Bvg-activated virulence factors plays a role in Bordetella pertussis pathogenicity. Infect Immun 69, 1983-1993.
57. R promoter open complexes: characterization of conformational changes by rapid [perturbant] upshift experiments. J Mol Biol 376, 1034-1047.
58. Lacey, B. W. (1960). Antigenic modulation of Bordetella pertussis. J Hyg (Lond) 58, 57-93.
59. Lambert, L. J., Wei, Y., Schirf, V., Demeler, B. & Werner, M. H. (2004). T4 AsiA blocks DNA recognition by remodeling sigma70 region 4. EMBO J 23, 2952-2962.
60. Lawson, C. L., Swigon, D., Murakami, K. S., Darst, S. A., Berman, H. M. & Ebright, R. H. (2004). Catabolite activator protein: DNA binding and transcription activation. Curr Opin Struct Biol 14, 10-20.
61. Levinson, G. & Gutman, G. A. (1987). Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol 4, 203-221.
62. Locht, C., Antoine, R. & Jacob-Dubuisson, F. (2001). Bordetella pertussis, molecular pathogenesis under multiple aspects. Curr Opin Microbiol 4, 82-89.
63. Marques, R. R. & Carbonetti, N. H. (1997). Genetic analysis of pertussis toxin promoter activation in Bordetella pertussis. Mol Microbiol 24, 1215-1224.
64. Marteyn, B., West, N. P., Browning, D. F., Cole, J. A., Shaw, J. G., Palm, F., Mounier, J., Prévost, M. C., Sansonetti, P. & Tang, C. M. (2010). Modulation of Shigella virulence in response to available oxygen in vivo. Nature 465, 355-358.
65. Mattoo, S., Foreman-Wykert, A. K., Cotter, P. A. & Miller, J. F. (2001). Mechanisms of Bordetella pathogenesis. Front Biosci 6, e168-e186.
66. Merkel, T. J., Stibitz, S., Keith, J. M., Leef, M. & Shahin, R. (1998). Contribution of regulation by the bvg locus to respiratory infection of mice by Bordetella pertussis. Infect Immun 66, 4367-4373.
67. Merkel, T. J., Boucher, P. E., Stibitz, S. & Grippe, V. K. (2003). Analysis of bvgR expression in Bordetella pertussis. J Bacteriol 185, 6902-6912.
68. Mooi, F. R., van der Heide, H. G. J., ter Avest, A. R., Welinder, K. G., Livey, I., van der Zeijst, B. A. M. & Gaastra, W. (1987). Characterization of fimbrial subunits from Bordetella species. Microb Pathog 2, 473-484.
69. Mooi, F. R., Jansen, W. H., Brunings, H., Gielen, H., van der Heide, H. G. J., Walvoort, H. C. & Guinee, P. A. M. (1992). Construction and analysis of Bordetella pertussis mutants defective in the production of fimbriae. Microb Pathog 12, 127-135.
70. Mooi, F. R., van Loo, I. H. M., van Gent, M., He, Q., Bart, M. J., Heuvelman, K. J., de Greeff, S. C., Diavatopoulos, D., Teunis, P. & other authors (2009). Bordetella pertussis strains with increased toxin production associated with pertussis resurgence. Emerg Infect Dis 15, 1206-1213.
71. Parkhill, J., Sebaihia, M., Preston, A., Murphy, L. D., Thomson, N., Harris, D. E., Holden, M. T., Churcher, C. M., Bentley, S. D. & other authors (2003). Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 35, 32-40.
72. Proulx, F., Toledano, B., Phan, V., Clermont, M. J., Mariscalco, M. M. & Seidman, E. G. (2002). Circulating granulocyte colony-stimulating factor, C-X-C, and C-C chemokines in children with Escherichia coli O157:H7 associated hemolytic uremic syndrome. Pediatr Res 52, 928-934.
73. Rhen, M. & Dorman, C. J. (2005). Hierarchical gene regulators adapt Salmonella enterica to its host milieus. Int J Med Microbiol 294, 487-502.
74. Riboli, B., Pedroni, P., Cuzzoni, A., Grandi, G. & de Ferra, F. (1991). Expression of Bordetella pertussis fimbrial (fim) genes in Bordetella bronchiseptica: fimX is expressed at a low level and vir-regulated. Microb Pathog 10, 393-403.
75. Roy, C. R. & Falkow, S. (1991). Identification of Bordetella pertussis regulatory sequences required for transcriptional activation of the fhaB gene and autoregulation of the bvgAS operon. J Bacteriol 173, 2385-2392.
76. Saecker, R. M., Tsodikov, O. V., McQuade, K. L., Schlax, P. E., Jr, Capp, M. W. & Record, M. T., Jr (2002). Kinetic studies and structural models of the association of E. coli sigma(70) RNA polymerase with the lambdaP(R) promoter: large scale conformational changes in forming the kinetically significant intermediates. J Mol Biol 319, 649-671.
77. Scarlato, V., Aricó, B., Prugnola, A. & Rappuoli, R. (1991). Sequential activation and environmental regulation of virulence genes in Bordetella pertussis. EMBO J 10, 3971-3975.
78. Seifert, H. S. & So, M. (1988). Genetic mechanisms of bacterial antigenic variation. Microbiol Rev 52, 327-336.
79. Steffen, P. & Ullmann, A. (1998). Hybrid Bordetella pertussis-Escherichia coli RNA polymerases: selectivity of promoter activation. J Bacteriol 180, 1567-1569.
80. Steffen, P., Goyard, S. & Ullmann, A. (1996). Phosphorylated BvgA is sufficient for transcriptional activation of virulence-regulated genes in Bordetella pertussis. EMBO J 15, 102-109.
81. Stibitz, S., Aaronson, W., Monack, D. & Falkow, S. (1989). Phase variation in Bordetella pertussis by frameshift mutation in a gene for a novel two-component system. Nature 338, 266-269.
82. Stock, A. M., Robinson, V. L. & Goudreau, P. N. (2000). Twocomponent signal transduction. Annu Rev Biochem 69, 183-215.
83. Streisinger, G. & Owen, J. (1985). Mechanisms of spontaneous and induced frameshift mutation in bacteriophage T4. Genetics 109, 633-659.
84. Swanson, M. S. & Hammer, B. K. (2000). Legionella pneumophila pathogesesis: a fateful journey from amoebae to macrophages. Annu Rev Microbiol 54, 567-613.
85. Tsang, R. S. W., Lau, A. K. H., Sill, M. L., Halperin, S. A., Van Caeseele, P., Jamieson, F. & Martin, I. E. (2004). Polymorphisms of the fimbria fim3 gene of Bordetella pertussis strains isolated in Canada. J Clin Microbiol 42, 5364-5367.
86. Uhl, M. A. & Miller, J. F. (1996). Integration of multiple domains in a two-component sensor protein: the Bordetella pertussis BvgAS phosphorelay. EMBO J 15, 1028-1036.
87. van Loo, I. H. M., Heuvelman, K. J., King, A. J. & Mooi, F. R. (2002). Multilocus sequence typing of Bordetella pertussis based on surface protein genes. J Clin Microbiol 40, 1994-2001.
88. von Wintzingerode, F., Schattke, A., Siddiqui, R. A., Rösick, U., Göbel, U. B. & Gross, R. (2001). Bordetella petrii sp. nov., isolated from an anaerobic bioreactor, and emended description of the genus Bordetella. Int J Syst Evol Microbiol 51, 1257-1265.
89. Watanabe, S., Kita, A., Kobayashi, K. & Miki, K. (2008). Crystal structure of the [2Fe-2S] oxidative-stress sensor SoxR bound to DNA. Proc Natl Acad Sci U S A 105, 4121-4126.
90. Willems, R., Paul, A., van der Heide, H. G., ter Avest, A. R. & Mooi, F. R. (1990). Fimbrial phase variation in Bordetella pertussis: a novel mechanism for transcriptional regulation. EMBO J 9, 2803-2809.
91. Williams, C. L., Boucher, P. E., Stibitz, S. & Cotter, P. A. (2005). BvgA functions as both an activator and a repressor to control Bvg phase expression of bipA in Bordetella pertussis. Mol Microbiol 56, 175-188.
92. Yang, Z. X., Zhou, Y. N., Yang, Y. & Jin, D. J. (2010). Polyphosphate binds to the principal sigma factor of RNA polymerase during starvation response in Helicobacter pylori. Mol Microbiol 77, 618-627.
93. Zu, T., Manetti, R., Rappuoli, R. & Scarlato, V. (1996). Differential binding of BvgA to two classes of virulence genes of Bordetella pertussis directs promoter selectivity by RNA polymerase. Mol Microbiol 21, 557-565.