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EcoSal Plus

Domain 2: Cell Architecture and Growth

Regulation of Fimbrial Expression

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  • Authors: Ian Blomfield1, and Marjan van der Woude2
  • Editors: Michael S. Donenberg3, Andreas J. Bäumler4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Biosciences, University of Kent, Canterbury, Kent CT2 7NJ, United Kingdom; 2: Department of Biology and the Hull York Medical School, IIU Area 12, University of York, P.O. Box 373, York YO10 5YW, United Kingdom; 3: University of Maryland, School of Medicine, Baltimore, MD; 4: University of California, Davis, Davis, CA
  • Received 16 April 2007 Accepted 13 June 2007 Published 13 September 2007
  • Address correspondence to Marjan van der Woude mvdw1@york.ac.uk.
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  • Abstract:

    Fimbria-mediated interaction with the host elicits both innate and adaptive immune responses, and thus their expression may not always be beneficial in vivo. Furthermore, the metabolic drain of producing fimbriae is significant. It is not surprising, therefore, to find that fimbrial production in and is under extensive environmental regulation. In many instances, fimbrial expression is regulated by phase variation, in which individual cells are capable of switching between fimbriate and afimbriate states to produce a mixed population. Mechanisms of phase variation vary considerably between different fimbriae and involve both genetic and epigenetic processes. Notwithstanding this, fimbrial expression is also sometimes controlled at the posttranscriptional level. In this chapter, we review key features of the regulation of fimbrial gene expression in and . The occurrence and distribution of fimbrial operons vary significantly among pathovars and even among the many serovars. Therefore, general principles are presented on the basis of detailed discussion of paradigms that have been extensively studied, including Pap, type 1 fimbriae, and curli. The roles of operon specific regulators like FimB or CsgD and of global regulatory proteins like Lrp, CpxR, and the histone-like proteins H-NS and IHF are reviewed as are the roles of sRNAs and of signalling nucleotide cyclic-di-GMP. Individual examples are discussed in detail to illustrate how the regulatory factors cooperate to allow tight control of expression of single operons. Molecular networks that allow coordinated expression between multiple fimbrial operons and with flagella in a single isolate are also presented. This chapter illustrates how adhesin expression is controlled, and the model systems also illustrate general regulatory principles germane to our overall understanding of bacterial gene regulation.

  • Citation: Blomfield I, van der Woude M. 2007. Regulation of Fimbrial Expression, EcoSal Plus 2007; doi:10.1128/ecosal.2.4.2.2

Key Concept Ranking

Gene Expression and Regulation
1.1768343
DNA Synthesis
0.7875565
Transcription Start Site
0.58142775
Type 1 Fimbriae
0.505555
Outer Membrane Proteins
0.46025127
Gene Expression
0.4293491
1.1768343

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ecosal.2.4.2.2.citations
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/content/journal/ecosalplus/10.1128/ecosal.2.4.2.2
2007-09-13
2017-03-29

Abstract:

Fimbria-mediated interaction with the host elicits both innate and adaptive immune responses, and thus their expression may not always be beneficial in vivo. Furthermore, the metabolic drain of producing fimbriae is significant. It is not surprising, therefore, to find that fimbrial production in and is under extensive environmental regulation. In many instances, fimbrial expression is regulated by phase variation, in which individual cells are capable of switching between fimbriate and afimbriate states to produce a mixed population. Mechanisms of phase variation vary considerably between different fimbriae and involve both genetic and epigenetic processes. Notwithstanding this, fimbrial expression is also sometimes controlled at the posttranscriptional level. In this chapter, we review key features of the regulation of fimbrial gene expression in and . The occurrence and distribution of fimbrial operons vary significantly among pathovars and even among the many serovars. Therefore, general principles are presented on the basis of detailed discussion of paradigms that have been extensively studied, including Pap, type 1 fimbriae, and curli. The roles of operon specific regulators like FimB or CsgD and of global regulatory proteins like Lrp, CpxR, and the histone-like proteins H-NS and IHF are reviewed as are the roles of sRNAs and of signalling nucleotide cyclic-di-GMP. Individual examples are discussed in detail to illustrate how the regulatory factors cooperate to allow tight control of expression of single operons. Molecular networks that allow coordinated expression between multiple fimbrial operons and with flagella in a single isolate are also presented. This chapter illustrates how adhesin expression is controlled, and the model systems also illustrate general regulatory principles germane to our overall understanding of bacterial gene regulation.

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Figures

Image of Figure 1
Figure 1

The labels describe the (epi)genetic state of transcription of the operon, whereas the lines depict fimbrial levels. In the first generation (G1), a phase switch from “off” to “on” occurs after DNA replication to produce both on and off daughter cells. After generations (Gn), a few on-phase cells have switched off and vice versa. A lower density of lines indicates fewer fimbriae as a result of the switch to a genetic off phase in combination with the dilution of preexisting structures. See the text for further details.

Citation: Blomfield I, van der Woude M. 2007. Regulation of Fimbrial Expression, EcoSal Plus 2007; doi:10.1128/ecosal.2.4.2.2
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Image of Figure 2
Figure 2

Genes are depicted as shaded rectangles, regulatory proteins and RNA polymerase are indicated by unshaded symbols, regulatory soluble RNA is shown as short wavy lines, and transcripts of operons are represented by long wavy lines with arrows. A direct mode of action of a regulatory factor is denoted by an unshaded arrow, and an unknown mode is represented by a striped arrow. Positive and negative effects are indicated by the symbols + and −. See the text for environmental signals that are incorporated through these factors, for differences in , and for additional details. The cartoon is not to scale.

Citation: Blomfield I, van der Woude M. 2007. Regulation of Fimbrial Expression, EcoSal Plus 2007; doi:10.1128/ecosal.2.4.2.2
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Image of Figure 3
Figure 3

and are transcribed as separate transcription units in a clockwise direction as indicated. The divergently transcribed gene, which shares several regulatory elements with ( Fig. 5 ), is transcribed in a counterclockwise direction. The invertible element, , shown in the on orientation, is delineated by large arrows. transcription extends into .

Citation: Blomfield I, van der Woude M. 2007. Regulation of Fimbrial Expression, EcoSal Plus 2007; doi:10.1128/ecosal.2.4.2.2
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Figure 4

The invertible element is demarcated by 9-bp inverted repeats (IRL and IRR). Both FimB and FimE (listed as FimR) catalyze inversion from on to off, although off-to-on inversion is catalyzed primarily by FimB. Like other site-specific recombinases, FimB and FimE bind to recognition sites that flank the sites of strand cleavage and exchange. Lrp binds to three sites and IHF binds to one site (site 2) within the invertible element. IHF binds to an additional site (site 1) between and IRL. The start site for mRNA, indicated by the double arrow, overlaps the internal recombinase binding sites at IRR in the on orientation. The direction of transcription is indicated by arrows. Leucine and alanine stimulate the inversion by promoting the selective loss of Lrp from site 3, forming a nucleoprotein complex with IHF that presumably favors the inversion reaction.

Citation: Blomfield I, van der Woude M. 2007. Regulation of Fimbrial Expression, EcoSal Plus 2007; doi:10.1128/ecosal.2.4.2.2
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Figure 5

and are transcribed from divergent promoters (P) in the directions indicated by the arrows. Regulators bind to operator sequences, termed (NanR), , (NagC), and (IHF), situated far upstream of the promoter, to activate the transcription of the recombinase gene. IHF, which facilitates the cooperative binding of NagC to and , is expected to produce a hairpin-like bend in the DNA midway between the two NagC operator sites (not shown). The binding of NanR to prevents the methylation of the Dam site GATC, whereas the binding of NagC to and , as well as IHF binding to , is necessary for the methylation protection of GATC. Methylation protection at GATC and GATC appears to alternate, presumably reflecting alternate binding of NanR (upper panel) and NagC (lower panel) to their operator sites. However, IHF binding is presumed to be invariable. Mutations in and have a lesser effect (small +) on expression than those in or or (large +). coincides with the −10 region of the promoter, and expression is repressed by both NanR and NagC. NagC binding occludes a Crp site (not shown) thought to activate the promoter. and are hence coordinately controlled, with suppressed by both Neu5Ac and GlcNAc and stimulated. In the absence of either NeuAc or GlcNAc, the expression of is presumably inhibited alternately by NagC and NanR (indicated by dashed arrows).

Citation: Blomfield I, van der Woude M. 2007. Regulation of Fimbrial Expression, EcoSal Plus 2007; doi:10.1128/ecosal.2.4.2.2
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Figure 6

The transition phase is indicated by brackets, and open vertical arrows depict rounds of DNA replication. Solid horizontal arrows represent the and promoters. Also shown are the two Dam (pentagon) target sequences in this region, GATC and GATC, that are methylated (M-GATC), hemimethylated (HM-GATC), or unmethylated (UM-GATC). See the text for explanation. The regulatory proteins PapB, CAP, and Lrp and the Lrp-PapI complex are shown; see the text for the role of other regulatory factors, including CpxAR and H-NS. Activation, repression, and targets of regulation are depicted by +, −, and open arrows, respectively. The cartoon is not to scale.

Citation: Blomfield I, van der Woude M. 2007. Regulation of Fimbrial Expression, EcoSal Plus 2007; doi:10.1128/ecosal.2.4.2.2
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