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9 Transcriptional Regulatory Mechanisms during Development

Authors: Lee Kroos1, Sumiko Inouye2
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Affiliations: 1: Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824; 2: Department of Biochemistry, Robert Wood Johnson Medical School, Piscataway, NJ 08854
Content Type: Monograph
Publication Year: 2008
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Abstract:

This chapter focuses primarily on transcriptional regulation of developmental genes. While the identification of developmentally regulated genes continues, now on a comprehensive genome-wide scale with the use of DNA microarray expression profiling, an understanding of the -acting DNA elements and -acting proteins (RNA polymerase [RNAP] with particular sigma factors, activators, and repressors) has emerged for a handful of developmental genes. In prokaryotes, sigma factors of RNAP play a key role in the regulation of gene expression by recognizing specific promoters and initiating transcription. As in other bacteria with a large number of sigma factors, such as , most of the expansion of the σ family in is due to members of the extracytoplasmic function (ECF) subfamily. Transcriptional activation, rather than relief from repression, appears to account for induction of most developmentally regulated genes studied so far, though some genes are subject to both positive and negative control. ActB is encoded by the second gene of an operon that regulates the level of CsgA, the C-signaling protein, during development. Several transcription factors key to the developmental process have been identified. Some of these, like MrpC and FruA, emerged from transposon mutagenesis screens. Others, like σ and σ, were identified by cross-hybridization with other sigma factor genes.

Citation: Kroos L, Inouye S. 2008. 9 Transcriptional Regulatory Mechanisms during Development, p 149-168. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch9

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9 Transcriptional Regulatory Mechanisms during Myxococcus xanthus Development
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Citation: Kroos L, Inouye S. 2008. 9 Transcriptional Regulatory Mechanisms during Development, p 149-168. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch9
/content/10.1128/9781555815677.ch09.ch09fig01
Figure 1
Alignment of parts of the amino acid sequences of SigA-G. Amino acids identical in more than 50% of the sequences are indicated by a black background. Conserved subregions of sigma factors and their functions are denoted under the sequences (Helmann and Chamberlin, 1988; ).
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Figure 1

Alignment of parts of the amino acid sequences of SigA-G. Amino acids identical in more than 50% of the sequences are indicated by a black background. Conserved subregions of sigma factors and their functions are denoted under the sequences (Helmann and Chamberlin, 1988; ).

Citation: Kroos L, Inouye S. 2008. 9 Transcriptional Regulatory Mechanisms during Development, p 149-168. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch9
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Figure 2
Typical anti-σ/σ regulatory circuit. A signal leads to destruction of the integral membrane anti-σ , freeing the σ to bind RNAP core subunits αββ́, and the resulting holoenzyme transcribes an operon encoding the σ and its anti-σ, as well as target genes of the regulon.
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Image of Figure 2
Figure 2

Typical anti-σ/σ regulatory circuit. A signal leads to destruction of the integral membrane anti-σ , freeing the σ to bind RNAP core subunits αββ́, and the resulting holoenzyme transcribes an operon encoding the σ and its anti-σ, as well as target genes of the regulon.

Citation: Kroos L, Inouye S. 2008. 9 Transcriptional Regulatory Mechanisms during Development, p 149-168. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch9
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Figure 3
Three types of transcriptional activators involved in development. The left part depicts an HPK or STPK in the inner membrane, undergoing autophosphorylation in response to an extracellular signal that has traversed the outer membrane (not shown) and is present in the periplasm. Transfer of phosphate from ATP to the FHA domain of an EBP by the STPK, or from the HPK to the receiver domain of a response regulator EBP, is proposed to facilitate DNA binding and/or oligomerization of the EBP. EBPs typically bind to DNA 70 to 150 bp upstream of the transcriptional start site (Buck et al., 2000). From the more distal sites, DNA looping is required for the EBP to interact with σ-RNAP. ATP hydrolysis by the EBP allows it to convert the σ-RNAP closed promoter complex to the open complex, activating transcription. The upper right part depicts a membrane-embedded HPK sensing a signal (e.g., C-signal) and transferring phosphate to FruA, a response regulator that is not an EBP. This is speculative since an HPK that phosphorylates FruA has not yet been identified. Phosphorylated FruA is shown interacting with RNAP containing a σ family member (σ-RNAP) whose identity also has not been established. Based on the sites of binding of the FruA DNA-binding domain mapped so far, DNA looping may not be required for FruA to interact with RNAP, which presumably facilitates recruitment or a subsequent step in transcription initiation. While FruA phosphorylation likely involves at least one membrane-embedded HPK that responds to extracellular C-signal, the pathway might be more complex (e.g., one or more phosphotransfer proteins might function between the HPK and FruA) and FruA might also be phosphorylated by one or more HPKs that are not membrane embedded and respond to intracellular signals. Likewise, EBP phosphorylation pathways can involve more than two components and can respond to intracellular cues via cytoplasmic kinases. The lower right part depicts MrpC responding to an unknown cytoplasmic signal by binding to DNA and activating transcription, an example of a one-component system. For simplicity, MrpC is shown binding to the same promoter region as phosphorylated FruA, and the Ω4400 promoter region is the first example of such a promoter region ( ; Mittal and Kroos, unpublished). σ-RNAP denotes RNAP containing a sigma factor in the σ family. The identity of the sigma factor responsible for Ω4400 promoter recognition is unknown.
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10.1128/9781555815677/f0155-01.gif
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Figure 3

Three types of transcriptional activators involved in development. The left part depicts an HPK or STPK in the inner membrane, undergoing autophosphorylation in response to an extracellular signal that has traversed the outer membrane (not shown) and is present in the periplasm. Transfer of phosphate from ATP to the FHA domain of an EBP by the STPK, or from the HPK to the receiver domain of a response regulator EBP, is proposed to facilitate DNA binding and/or oligomerization of the EBP. EBPs typically bind to DNA 70 to 150 bp upstream of the transcriptional start site (Buck et al., 2000). From the more distal sites, DNA looping is required for the EBP to interact with σ-RNAP. ATP hydrolysis by the EBP allows it to convert the σ-RNAP closed promoter complex to the open complex, activating transcription. The upper right part depicts a membrane-embedded HPK sensing a signal (e.g., C-signal) and transferring phosphate to FruA, a response regulator that is not an EBP. This is speculative since an HPK that phosphorylates FruA has not yet been identified. Phosphorylated FruA is shown interacting with RNAP containing a σ family member (σ-RNAP) whose identity also has not been established. Based on the sites of binding of the FruA DNA-binding domain mapped so far, DNA looping may not be required for FruA to interact with RNAP, which presumably facilitates recruitment or a subsequent step in transcription initiation. While FruA phosphorylation likely involves at least one membrane-embedded HPK that responds to extracellular C-signal, the pathway might be more complex (e.g., one or more phosphotransfer proteins might function between the HPK and FruA) and FruA might also be phosphorylated by one or more HPKs that are not membrane embedded and respond to intracellular signals. Likewise, EBP phosphorylation pathways can involve more than two components and can respond to intracellular cues via cytoplasmic kinases. The lower right part depicts MrpC responding to an unknown cytoplasmic signal by binding to DNA and activating transcription, an example of a one-component system. For simplicity, MrpC is shown binding to the same promoter region as phosphorylated FruA, and the Ω4400 promoter region is the first example of such a promoter region ( ; Mittal and Kroos, unpublished). σ-RNAP denotes RNAP containing a sigma factor in the σ family. The identity of the sigma factor responsible for Ω4400 promoter recognition is unknown.

Citation: Kroos L, Inouye S. 2008. 9 Transcriptional Regulatory Mechanisms during Development, p 149-168. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch9
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Figure 4
Model for a signaling and gene regulatory cascade leading to FruA-dependent gene expression. See the text for explanation.
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Image of Figure 4
Figure 4

Model for a signaling and gene regulatory cascade leading to FruA-dependent gene expression. See the text for explanation.

Citation: Kroos L, Inouye S. 2008. 9 Transcriptional Regulatory Mechanisms during Development, p 149-168. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch9
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Figure 5
Conserved regulatory elements in C-signal-dependent promoter regions and in the promoter region. The promoter —10 and —35 regions are shown, except in the case of Ω4499, which has a C box centered at —33 bp relative to the transcriptional start site (right-angle arrow). The position and sequence of C boxes (boxed; matching the consensus sequence CAYYCCY, in which Y means C or T, except in the cases of the and Ω4406 promoter regions, which contain C-box-like sequences) and 5-bp elements (bold, matching the consensus sequence GAACA) are shown for each promoter region. An essential 10-bp element is shown for the Ω4403 promoter region, and sequences centered at —83.5 and —79 bp that exert a twofold or more positive effect on Ω4400 and Ω4499 expression, respectively, are also shown. See the text for references.
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Figure 5

Conserved regulatory elements in C-signal-dependent promoter regions and in the promoter region. The promoter —10 and —35 regions are shown, except in the case of Ω4499, which has a C box centered at —33 bp relative to the transcriptional start site (right-angle arrow). The position and sequence of C boxes (boxed; matching the consensus sequence CAYYCCY, in which Y means C or T, except in the cases of the and Ω4406 promoter regions, which contain C-box-like sequences) and 5-bp elements (bold, matching the consensus sequence GAACA) are shown for each promoter region. An essential 10-bp element is shown for the Ω4403 promoter region, and sequences centered at —83.5 and —79 bp that exert a twofold or more positive effect on Ω4400 and Ω4499 expression, respectively, are also shown. See the text for references.

Citation: Kroos L, Inouye S. 2008. 9 Transcriptional Regulatory Mechanisms during Development, p 149-168. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch9
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Tables

9 Transcriptional Regulatory Mechanisms during Myxococcus xanthus Development
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Citation: Kroos L, Inouye S. 2008. 9 Transcriptional Regulatory Mechanisms during Development, p 149-168. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch9
/content/10.1128/9781555815677.ch09.ch09tab01
Table 1
Putative σ-RNAP-transcribed genes
Generic image for table
Table 1

Putative σ-RNAP-transcribed genes

Citation: Kroos L, Inouye S. 2008. 9 Transcriptional Regulatory Mechanisms during Development, p 149-168. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch9
/content/10.1128/9781555815677.ch09.ch09tab02
Table 2
σ-RNAP-transcribed genes
Generic image for table
Table 2

σ-RNAP-transcribed genes

Citation: Kroos L, Inouye S. 2008. 9 Transcriptional Regulatory Mechanisms during Development, p 149-168. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch9
/content/10.1128/9781555815677.ch09.ch09tab03
Table 3
EBPs that affect motility and/or development
Generic image for table
Table 3

EBPs that affect motility and/or development

Citation: Kroos L, Inouye S. 2008. 9 Transcriptional Regulatory Mechanisms during Development, p 149-168. In Whitworth D (ed), Myxobacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815677.ch9

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