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Chapter 21 : Bordetella pertussis BvgAS Virulence Control System

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Abstract:

During infection of a suitable host, adheres to ciliated epithelial cells and expresses several toxins responsible for both local damage and systemic effects. In 1960, Lacey reported that altering growth conditions affected the expression of several antigens. Further analysis and extension of this work demonstrated that chlorate and sulfate anions, nicotinic acid derivatives, and low temperature can reversibly down-regulate expression of virulence factors by . In vivo signals that may promote phenotypic modulation and the mechanism through which modulators interact with BvgAS to regulate its function are not known. Autophosphorylation of the cytoplasmic portion of BvgS (‘BvgS) and phosphotransfer to BvgA have been demonstrated using an in vitro phosphorylation assay. As expected, mutation of the proposed primary site of autophosphorylation, His-729 in the transmitter, abolishes activity in vivo and autophosphorylation in vitro. Phosphotransfer to BvgA from BvgS can be uncoupled from BvgS autophosphorylation by mutations in BvgS. Identification of additional Bvg-phase genes and their functional roles in will further our understanding of virulence gene regulation as it relates to pathogenesis. Pathogenesis of begins with ; characterization of the mechanisms by which BvgAS senses and responds to changing environments is essential for understanding .

Citation: Uhl M, Miller J. 1995. Bordetella pertussis BvgAS Virulence Control System, p 333-349. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch21

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Figures

Image of FIGURE 1
FIGURE 1

Selected features of the BvgA and BvgS proteins ( ). Shaded boxes depict regions sharing sequence similarity to two-component systems. The consensus ATP binding motif (ATP) and amino acids conserved among two-component systems are shown for BvgS: His-729 (H729), Asp-1023 (D1023), and Lys-1080 (K1080). Selected amino acids conserved among receivers are also noted for BvgA: Asp-54 (D54) and Lys-104 (K104). Proposed hydrophobic transmembrane sequences (TM) and A/P-rich regions in BvgS and the helix-turn-helix motif in BvgA (HTH) are noted.

Citation: Uhl M, Miller J. 1995. Bordetella pertussis BvgAS Virulence Control System, p 333-349. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch21
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Image of FIGURE 2
FIGURE 2

Alignment of the conserved histidine region in the C termini of BvgS family members. Alignments of a small portion of the C-terminus domain are shown with consensus amino acids noted for matches in six of the eight amino acids sequences. Consensus abbreviations are Ψ for hydrophobic amino acid and + for positively charged amino acid. Amino acid numbering is noted for BvgS, with the conserved histidine in bold. The location of the consensus sequence in the C terminus is shown, with the transmitter and receiver domains included for comparison. BvgS family members are LemA of pv. ; BarA, ArcB, and EvgS of ; RpfC of pv. ; and RteA of ( ). Sequences were aligned with the PILEUP program from the Genetics Computer Group sequence analysis software package. The consensus motif has also been noticed by others ( ).

Citation: Uhl M, Miller J. 1995. Bordetella pertussis BvgAS Virulence Control System, p 333-349. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch21
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Image of FIGURE 3
FIGURE 3

Model for activation of the and loci ( ). Transcription of the operon initiates in the Bvg phase from the P promoter. In the Bvg phase, following activation of BvgAS, BvgA (A) is able to direct RNA polymerase (RNAP) to activate transcription of the and loci at the P and promoters. Relative levels of transcription are represented by arrow thickness. Locations of inverted and direct repeats in the and intergenic regions are illustrated by small numbered arrows, and the sequences comprising these repeats are listed below. Two additional Bvg-phase promoters, P and P, have also been identified and are discussed in the text ( ).

Citation: Uhl M, Miller J. 1995. Bordetella pertussis BvgAS Virulence Control System, p 333-349. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch21
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Image of FIGURE 4
FIGURE 4

Sensory transduction mutations in the BvgS linker region ( ). The structure of the BvgS protein is indicated. Abbreviations: TM, transmembrane region; T, transmitter; A/P1, AP-rich sequence AAPPAAATAATP; R, receiver; A/P2, AALPTPPSPQAAAPA; C, C-terminal region. The amino acid sequence of the linker region is shown along with substitutions resulting from the constitutive mutations in (Bvg, insensitive to modulation). Phenotypes of BvgS wild-type and mutations (; Δ366P; Δ366P) in an reporter system are shown.

Citation: Uhl M, Miller J. 1995. Bordetella pertussis BvgAS Virulence Control System, p 333-349. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch21
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Image of FIGURE 5
FIGURE 5

In vitro activity of ′BvgS and mutant derivatives. Wild-type ′BvgS and mutant derivatives were phosphorylated in the absence (lanes 1 to 8) or presence (lanes 9 to 16) of BvgA. Lanes 1 and 9, wild-type ′BvgS; lanes 2 and 10, ′BvgS H729Q; lanes 3 and 11, ′BvgS D1023N; lanes 4 and 12, ′BvgS K1080R; lanes 5 and 13, ′BvgS K1080M; lanes 6 and 14, ′BvgS Δ59R; lanes 7 and 15, ′BvgS Ω1051; lanes 8 and 16, ′BvgS Δ15C. Locations of ′BvgS and BvgA are marked with arrows. Adapted from , with permission.

Citation: Uhl M, Miller J. 1995. Bordetella pertussis BvgAS Virulence Control System, p 333-349. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch21
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Image of FIGURE 6
FIGURE 6

Hypothetical model for steps involved in BvgAS signal transduction ( ). After multimerization of BvgS, signal inputs (low temperature, nicotinic acid, MgSO) regulate activity of the protein. BvgS in a conformationally “active” state is able to autophosphorylate at His-729 of the transmitter. After autophosphorylation, the BvgS transmitter intramolecularly transfers to Asp-1023 in the receiver. The BvgS C terminus is also phosphorylated subsequent to receiver phosphorylation ( ). BvgA is phosphorylated by BvgS in a phosphotransfer reaction. Phosphorylated BvgA is able to activate transcription of virulence genes, and initial reports indicate this is through increased affinity for DNA (Boucher et al., 1994). Autophosphorylation and phosphotransfer have been demonstrated for BvgA and BvgS. Mutations that alter the proposed site of autophosphorylation (H→Q) or remove the receiver or C terminus (ΔR, ΔC) prevent autophosphorylation. Both Asp-1023 (D→N) and Lys-1080 (K→R) are necessary for phosphotransfer to BvgA, and Asp-1023 is required for transphosphorylation of the BvgS C terminus ( , and unpublished data). BvgS signal-insensitive muutations, such as , are proposed to lock the protein into an active conformation ( ). Multimerization of BvgS has been suggested by intermolecular complementation of BvgS mutations ( ).

Citation: Uhl M, Miller J. 1995. Bordetella pertussis BvgAS Virulence Control System, p 333-349. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch21
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Tables

Generic image for table
TABLE 1

BvgA and BvgS mutations and phenotypes in vivo and in vitro

Citation: Uhl M, Miller J. 1995. Bordetella pertussis BvgAS Virulence Control System, p 333-349. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch21

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