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Chapter 28 : Methylation-Dependent and Lrp-Dependent Fimbrial Gene Regulation in Escherichia coli

Author: David A. Low1
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Affiliations: 1: David A. Low • Division of Cell Biology and Immunology, Department of Pathology, Room 5B310MC, University of Utah Medical School, Salt Lake City, Utah 84132
Content Type: Monograph
Publication Year: 1994

Category: Microbial Genetics and Molecular Biology; Bacterial Pathogenesis

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Methylation-Dependent and Lrp-Dependent Fimbrial Gene Regulation in Escherichia coli, Page 1 of 2

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Abstract:

The majority of bacterial pathogens and opportunists colonize the mucosal surfaces of their hosts by expressing specific adhesins that bind to host target receptors. Many urinary tract isolates, in particular those that cause kidney infections, contain multiple pyelonephritis-associated pili () operons, each of which is capable of expressing and assembling cell surface fimbriae. Lrp is a regulatory protein that exerts global control over as many as 50 genes in . In some cases, such as , switching, and pilin transcription, Lrp is a positive regulator. In other cases, such as , , and , Lrp acts negatively. Analysis of mutations within regulatory DNA that allow transcription of in the absence of Papl indicates that Papl does not interact with DNA. The regulation of gene expression is complex and involves a variety of factors including Lrp, Dam, CRP, Papl, PapB, and possibly H-NS. In addition, RimJ, the N-terminal acetylase of ribosomal protein S5, may play a role in thermoregulation. As a member of the Lrp regulon, Pap fimbrial regulation is tied to cellular metabolism, although it is not leucine responsive. Under the CRP regulon, Pap fimbrial expression is shut down when rich carbon sources such as glucose are present.

Citation: Low D. 1994. Methylation-Dependent and Lrp-Dependent Fimbrial Gene Regulation in Escherichia coli, p 423-436. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch28

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Gene Expression and Regulation
1.0270822
Type 1 Fimbriae
0.5291601
Transcription Start Site
0.5057696
Aliphatic Amino Acids
0.49982846
Gene Expression
0.46971837
Gene Regulation
0.42957148
DNA
0.42339417
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Methylation-Dependent and Lrp-Dependent Fimbrial Gene Regulation in Escherichia coli
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Citation: Low D. 1994. Methylation-Dependent and Lrp-Dependent Fimbrial Gene Regulation in Escherichia coli, p 423-436. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch28
/content/10.1128/9781555818340.chap28.fig28-1
Figure 1

Methy lation patterns of Pap phase on and phase off cells. The square at the upper left represents binding of Lrp-PapI around the GATC-I site, whereas the oval at the lower right represents binding of Lrp near the GATC-I site. Black dots indicate methyl groups covalently attached to adenosine residues by Dam.

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10.1128/9781555818340/fig28-1.gif
Image of Figure 1
Figure 1

Methy lation patterns of Pap phase on and phase off cells. The square at the upper left represents binding of Lrp-PapI around the GATC-I site, whereas the oval at the lower right represents binding of Lrp near the GATC-I site. Black dots indicate methyl groups covalently attached to adenosine residues by Dam.

Citation: Low D. 1994. Methylation-Dependent and Lrp-Dependent Fimbrial Gene Regulation in Escherichia coli, p 423-436. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch28
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Figure 2

Organization of the regulatory region of the operon. Binding domains for PapB ( ), Lrp and Lrp-PapI ( ), and CRP ( ) as well as the 27-bp inverted repeats containing GATC-I and GATC-II are shown as boxes. Also shown are the transcription start sites of the and transcripts. PapB site 2 overlaps the -10 RNA polymerase recognition site at the promoter.

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10.1128/9781555818340/fig28-2.gif
Image of Figure 2
Figure 2

Organization of the regulatory region of the operon. Binding domains for PapB ( ), Lrp and Lrp-PapI ( ), and CRP ( ) as well as the 27-bp inverted repeats containing GATC-I and GATC-II are shown as boxes. Also shown are the transcription start sites of the and transcripts. PapB site 2 overlaps the -10 RNA polymerase recognition site at the promoter.

Citation: Low D. 1994. Methylation-Dependent and Lrp-Dependent Fimbrial Gene Regulation in Escherichia coli, p 423-436. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch28
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Figure 3

Regulatory regions of four Lrp-regulated fimbrial operons. The organization of the ( ), ( ), ( ), and ( ) fimbrial regulatory regions are shown. Genes sharing sequence similarities with are denoted by dark shading, whereas genes with sequence similarities to are denoted by diagonal stripes. DNA sequences with similarity to the GATC-I box (CGATCTTTTAT) and GATC-II box (AAGATCGT) ( ) are depicted as small open boxes. Transcription start sites are shown by arrows. The insertion sequences within are not drawn to scale. In the operon, ORF 7 overlaps the 3' end of the gene.

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Figure 3

Regulatory regions of four Lrp-regulated fimbrial operons. The organization of the ( ), ( ), ( ), and ( ) fimbrial regulatory regions are shown. Genes sharing sequence similarities with are denoted by dark shading, whereas genes with sequence similarities to are denoted by diagonal stripes. DNA sequences with similarity to the GATC-I box (CGATCTTTTAT) and GATC-II box (AAGATCGT) ( ) are depicted as small open boxes. Transcription start sites are shown by arrows. The insertion sequences within are not drawn to scale. In the operon, ORF 7 overlaps the 3' end of the gene.

Citation: Low D. 1994. Methylation-Dependent and Lrp-Dependent Fimbrial Gene Regulation in Escherichia coli, p 423-436. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch28
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Figure 4

Comparative amino acid analysis of PapI-related DNA sequences. The amino acid sequences of PapI ( ), SfaC ( ), PrsI ( ), DaaF ( ), PefI ( ), and FaeA ( ) are shown. Dashes represent gaps introduced for alignment purposes. On the top row, cons denotes total consensus at a given amino acid position among all six regulatory proteins. Amino acids that are conserved among all six PapI-like proteins are shown in boldface type. Lowercase letters indicate that at least three sequences contain the same amino acid at a single position. Boxed regions show identities between either PefI and DaaF or PefI and FaeA or identities among PefI, DaaF, and FaeA that are not present in PapI, SfaC, or PrsI sequences.

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Figure 4

Comparative amino acid analysis of PapI-related DNA sequences. The amino acid sequences of PapI ( ), SfaC ( ), PrsI ( ), DaaF ( ), PefI ( ), and FaeA ( ) are shown. Dashes represent gaps introduced for alignment purposes. On the top row, cons denotes total consensus at a given amino acid position among all six regulatory proteins. Amino acids that are conserved among all six PapI-like proteins are shown in boldface type. Lowercase letters indicate that at least three sequences contain the same amino acid at a single position. Boxed regions show identities between either PefI and DaaF or PefI and FaeA or identities among PefI, DaaF, and FaeA that are not present in PapI, SfaC, or PrsI sequences.

Citation: Low D. 1994. Methylation-Dependent and Lrp-Dependent Fimbrial Gene Regulation in Escherichia coli, p 423-436. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch28
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Figure 5

Regulatory networks affecting the operon. Large circles represent the operons controlled within each regulatory network or regulon, and numbers denote the various classes of regulatory control. The operons and are members of class 2 since they are controlled by Lrp, CRP, and DNA methylation patterns. The operon belongs to class 3 since it is not regulated by Dam. The and operons ( ) are possible members of class 1, although it is not known if any of these operons are regulated by Lrp or Dam. Finally, my colleagues and I ( ) recently identified a gene located at 77 min on the chromosome; the gene contains a nonmethylated GATC site dependent on the presence of Lrp, possibly a member of class 4.

10.1128/9781555818340/fig28-5_thmb.gif
10.1128/9781555818340/fig28-5.gif
Image of Figure 5
Figure 5

Regulatory networks affecting the operon. Large circles represent the operons controlled within each regulatory network or regulon, and numbers denote the various classes of regulatory control. The operons and are members of class 2 since they are controlled by Lrp, CRP, and DNA methylation patterns. The operon belongs to class 3 since it is not regulated by Dam. The and operons ( ) are possible members of class 1, although it is not known if any of these operons are regulated by Lrp or Dam. Finally, my colleagues and I ( ) recently identified a gene located at 77 min on the chromosome; the gene contains a nonmethylated GATC site dependent on the presence of Lrp, possibly a member of class 4.

Citation: Low D. 1994. Methylation-Dependent and Lrp-Dependent Fimbrial Gene Regulation in Escherichia coli, p 423-436. In Miller V, Kaper J, Portnoy D, Isberg R (ed), Molecular Genetics of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818340.ch28
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