Identification of Bordetella Pertussis Regulatory Sequences Required for Transcriptional Activation of the FhaB Gene and Autoregulation of the BvgAS Operon

Overview

Journal J Bacteriol

Publisher American Society for Microbiology

Specialty Microbiology

Date 1991 Apr 1

PMID 2007557

Citations 51

Authors

C R Roy

S Falkow

Affiliations

Soon will be listed here.

Abstract

Transcription of numerous virulence genes in Bordetella pertussis is positively regulated by the products of the bvgAS genes. In this study a series of lacZYA fusions containing deletions in either the fhaB or bvgA promoter regions was used to identify cis-acting regulatory regions required for bvg activation of these two genes. Gel retardation and DNase I protection analyses have shown that specific protein-DNA interactions occur at these regulatory regions and that these interactions require the transcriptional activator protein BvgA. The regulatory regions found upstream of fhaB and bvgA which are involved in protein binding both contain the sequence TTTCCTA. This sequence is part of an inverted repeat upstream of fhaB and a direct repeat upstream of bvgA. Homologous repeats are not apparent upstream of other bvg-activated genes, such as ptx and cyaA. These data suggest that the mechanism for transcriptional regulation of the other bvg-activated genes is complex and may require regulatory factors in addition to the bvgAS gene products.

Citing Articles

Interference of flagellar rotation up-regulates the expression of small RNA contributing to infection.

Hiramatsu Y, Nishida T, Nugraha D, Osada-Oka M, Nakane D, Imada K Sci Adv. 2022; 8(51):eade8971.

PMID: 36542710 PMC: 9770993. DOI: 10.1126/sciadv.ade8971.

Multiple weak interactions between BvgA~P and ptx promoter DNA strongly activate transcription of pertussis toxin genes in Bordetella pertussis.

Chen Q, Boucher P, Stibitz S PLoS Pathog. 2020; 16(5):e1008500.

PMID: 32401811 PMC: 7250471. DOI: 10.1371/journal.ppat.1008500.

Pertussis: Microbiology, Disease, Treatment, and Prevention.

Kilgore P, Salim A, Zervos M, Schmitt H Clin Microbiol Rev. 2016; 29(3):449-86.

PMID: 27029594 PMC: 4861987. DOI: 10.1128/CMR.00083-15.

Polymorphisms influencing expression of dermonecrotic toxin in Bordetella bronchiseptica.

Okada K, Abe H, Ike F, Ogura Y, Hayashi T, Fukui-Miyazaki A PLoS One. 2015; 10(2):e0116604.

PMID: 25642712 PMC: 4314077. DOI: 10.1371/journal.pone.0116604.

Evidence for a role of the polysaccharide capsule transport proteins in pertussis pathogenesis.

Hoo R, Lam J, Huot L, Pant A, Li R, Hot D PLoS One. 2014; 9(12):e115243.

PMID: 25501560 PMC: 4264864. DOI: 10.1371/journal.pone.0115243.

References

Roy C, Miller J, Falkow S . The bvgA gene of Bordetella pertussis encodes a transcriptional activator required for coordinate regulation of several virulence genes. J Bacteriol. 1989; 171(11):6338-44. PMC: 210508. DOI: 10.1128/jb.171.11.6338-6344.1989. View

Melton A, Weiss A . Environmental regulation of expression of virulence determinants in Bordetella pertussis. J Bacteriol. 1989; 171(11):6206-12. PMC: 210490. DOI: 10.1128/jb.171.11.6206-6212.1989. View

Laoide B, Ullmann A . Virulence dependent and independent regulation of the Bordetella pertussis cya operon. EMBO J. 1990; 9(4):999-1005. PMC: 551769. DOI: 10.1002/j.1460-2075.1990.tb08202.x. View

Roy C, Miller J, Falkow S . Autogenous regulation of the Bordetella pertussis bvgABC operon. Proc Natl Acad Sci U S A. 1990; 87(10):3763-7. PMC: 53983. DOI: 10.1073/pnas.87.10.3763. View

Scarlato V, Prugnola A, Arico B, Rappuoli R . Positive transcriptional feedback at the bvg locus controls expression of virulence factors in Bordetella pertussis. Proc Natl Acad Sci U S A. 1990; 87(17):6753-7. PMC: 54615. DOI: 10.1073/pnas.87.17.6753. View

Lacey B . Antigenic modulation of Bordetella pertussis. J Hyg (Lond). 1960; 58:57-93. PMC: 2134314. DOI: 10.1017/s0022172400038134. View

Galas D, Schmitz A . DNAse footprinting: a simple method for the detection of protein-DNA binding specificity. Nucleic Acids Res. 1978; 5(9):3157-70. PMC: 342238. DOI: 10.1093/nar/5.9.3157. View

Garner M, Revzin A . A gel electrophoresis method for quantifying the binding of proteins to specific DNA regions: application to components of the Escherichia coli lactose operon regulatory system. Nucleic Acids Res. 1981; 9(13):3047-60. PMC: 327330. DOI: 10.1093/nar/9.13.3047. View

Weiss A, Hewlett E, Myers G, Falkow S . Tn5-induced mutations affecting virulence factors of Bordetella pertussis. Infect Immun. 1983; 42(1):33-41. PMC: 264520. DOI: 10.1128/iai.42.1.33-41.1983. View

10.

Weiss A, Falkow S . Genetic analysis of phase change in Bordetella pertussis. Infect Immun. 1984; 43(1):263-9. PMC: 263420. DOI: 10.1128/iai.43.1.263-269.1984. View

11.

Tabor S, Richardson C . A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc Natl Acad Sci U S A. 1985; 82(4):1074-8. PMC: 397196. DOI: 10.1073/pnas.82.4.1074. View

12.

Nixon B, Ronson C, Ausubel F . Two-component regulatory systems responsive to environmental stimuli share strongly conserved domains with the nitrogen assimilation regulatory genes ntrB and ntrC. Proc Natl Acad Sci U S A. 1986; 83(20):7850-4. PMC: 386820. DOI: 10.1073/pnas.83.20.7850. View

13.

Stibitz S, Black W, Falkow S . The construction of a cloning vector designed for gene replacement in Bordetella pertussis. Gene. 1986; 50(1-3):133-40. DOI: 10.1016/0378-1119(86)90318-5. View

14.

Simons R, Houman F, Kleckner N . Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene. 1987; 53(1):85-96. DOI: 10.1016/0378-1119(87)90095-3. View

15.

Gross R, Rappuoli R . Positive regulation of pertussis toxin expression. Proc Natl Acad Sci U S A. 1988; 85(11):3913-7. PMC: 280330. DOI: 10.1073/pnas.85.11.3913. View

16.

Stibitz S, Weiss A, Falkow S . Genetic analysis of a region of the Bordetella pertussis chromosome encoding filamentous hemagglutinin and the pleiotropic regulatory locus vir. J Bacteriol. 1988; 170(7):2904-13. PMC: 211228. DOI: 10.1128/jb.170.7.2904-2913.1988. View

17.

Dower W, Miller J, Ragsdale C . High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res. 1988; 16(13):6127-45. PMC: 336852. DOI: 10.1093/nar/16.13.6127. View

18.

Knapp S, Mekalanos J . Two trans-acting regulatory genes (vir and mod) control antigenic modulation in Bordetella pertussis. J Bacteriol. 1988; 170(11):5059-66. PMC: 211571. DOI: 10.1128/jb.170.11.5059-5066.1988. View

19.

Stibitz S, AARONSON W, Monack D, Falkow S . Phase variation in Bordetella pertussis by frameshift mutation in a gene for a novel two-component system. Nature. 1989; 338(6212):266-9. DOI: 10.1038/338266a0. View

20.

Relman D, Domenighini M, Tuomanen E, Rappuoli R, Falkow S . Filamentous hemagglutinin of Bordetella pertussis: nucleotide sequence and crucial role in adherence. Proc Natl Acad Sci U S A. 1989; 86(8):2637-41. PMC: 286972. DOI: 10.1073/pnas.86.8.2637. View