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Novel roles of cAMP receptor protein (CRP) in regulation of transport and metabolism of carbon sources.

Shimada T, Fujita N, Yamamoto K, Ishihama A - PLoS ONE (2011)

Bottom Line: Using the newly developed Genomic SELEX screening system of transcription factor-binding sequences, however, we have identified a total of at least 254 CRP-binding sites.Based on the functions of novel target genes, we conclude that CRP plays a key regulatory role in the whole processes from the selective transport of carbon sources, the glycolysis-gluconeogenesis switching to the metabolisms downstream of glycolysis, including tricarboxylic acid (TCA) cycle, pyruvate dehydrogenase (PDH) pathway and aerobic respiration.One unique regulation mode is that a single and the same CRP molecule bound within intergenic regions often regulates both of divergently transcribed operons.

View Article: PubMed Central - PubMed

Affiliation: Department of Frontier Bioscience, Hosei University, Koganei, Tokyo, Japan.

ABSTRACT
CRP (cAMP receptor protein), the global regulator of genes for carbon source utilization in the absence of glucose, is the best-studied prokaryotic transcription factor. A total of 195 target promoters on the Escherichia coli genome have been proposed to be under the control of cAMP-bound CRP. Using the newly developed Genomic SELEX screening system of transcription factor-binding sequences, however, we have identified a total of at least 254 CRP-binding sites. Based on their location on the E. coli genome, we predict a total of at least 183 novel regulation target operons, altogether with the 195 hitherto known targets, reaching to the minimum of 378 promoters as the regulation targets of cAMP-CRP. All the promoters selected from the newly identified targets and examined by using the lacZ reporter assay were found to be under the control of CRP, indicating that the Genomic SELEX screening allowed to identify the CRP targets with high accuracy. Based on the functions of novel target genes, we conclude that CRP plays a key regulatory role in the whole processes from the selective transport of carbon sources, the glycolysis-gluconeogenesis switching to the metabolisms downstream of glycolysis, including tricarboxylic acid (TCA) cycle, pyruvate dehydrogenase (PDH) pathway and aerobic respiration. One unique regulation mode is that a single and the same CRP molecule bound within intergenic regions often regulates both of divergently transcribed operons.

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The hierarchy of regulation network of CRP.A total of 70 genes for transcription factors are organized under the control of CRP. Transcription factors are classified on the basis of regulation targets: regulators for carbon metabolism (green background), nitrogen metabolism (orange background), and for stress-response (purple background). Some nucleoid proteins play not only architectural roles but also regulatory roles (blue-green background). A number of genes for uncharacterized transcription factors are under the control of CRP (black background). The set of newly identified CRP targets in this study are shown by asterisk.
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pone-0020081-g006: The hierarchy of regulation network of CRP.A total of 70 genes for transcription factors are organized under the control of CRP. Transcription factors are classified on the basis of regulation targets: regulators for carbon metabolism (green background), nitrogen metabolism (orange background), and for stress-response (purple background). Some nucleoid proteins play not only architectural roles but also regulatory roles (blue-green background). A number of genes for uncharacterized transcription factors are under the control of CRP (black background). The set of newly identified CRP targets in this study are shown by asterisk.

Mentions: Promoters for the genes encoding the key metabolic enzymes and the essential cell architectures are under the control of multiple regulators, each monitoring different environmental conditions or metabolic states [38]. After Genomic SELEX screening, we discovered that a number of genes encoding transcription factors are under the control of CRP (Fig. 6). In the case of CRP, a total of 70 transcription factors are included in the whole set of 349 CRP targets, forming a big hierarchy of transcription factor network. A total of 28 CRP targets including CRP itself are the specific regulators of carbon metabolism (shown under green background in Fig. 6), while 13 are the regulators of nitrogen metabolism (orange background in Fig. 6). Some of this-group regulators such as ArgR and GlnG control a large number of genes (more than 40 by ArgR and more than 50 by GlnG). A total of 14 factors are involved in regulation of the genes for response to external stresses (purple background in Fig. 6). Stationary phase-specific sigma RpoS is also under the control of CRP.


Novel roles of cAMP receptor protein (CRP) in regulation of transport and metabolism of carbon sources.

Shimada T, Fujita N, Yamamoto K, Ishihama A - PLoS ONE (2011)

The hierarchy of regulation network of CRP.A total of 70 genes for transcription factors are organized under the control of CRP. Transcription factors are classified on the basis of regulation targets: regulators for carbon metabolism (green background), nitrogen metabolism (orange background), and for stress-response (purple background). Some nucleoid proteins play not only architectural roles but also regulatory roles (blue-green background). A number of genes for uncharacterized transcription factors are under the control of CRP (black background). The set of newly identified CRP targets in this study are shown by asterisk.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3105977&req=5

pone-0020081-g006: The hierarchy of regulation network of CRP.A total of 70 genes for transcription factors are organized under the control of CRP. Transcription factors are classified on the basis of regulation targets: regulators for carbon metabolism (green background), nitrogen metabolism (orange background), and for stress-response (purple background). Some nucleoid proteins play not only architectural roles but also regulatory roles (blue-green background). A number of genes for uncharacterized transcription factors are under the control of CRP (black background). The set of newly identified CRP targets in this study are shown by asterisk.
Mentions: Promoters for the genes encoding the key metabolic enzymes and the essential cell architectures are under the control of multiple regulators, each monitoring different environmental conditions or metabolic states [38]. After Genomic SELEX screening, we discovered that a number of genes encoding transcription factors are under the control of CRP (Fig. 6). In the case of CRP, a total of 70 transcription factors are included in the whole set of 349 CRP targets, forming a big hierarchy of transcription factor network. A total of 28 CRP targets including CRP itself are the specific regulators of carbon metabolism (shown under green background in Fig. 6), while 13 are the regulators of nitrogen metabolism (orange background in Fig. 6). Some of this-group regulators such as ArgR and GlnG control a large number of genes (more than 40 by ArgR and more than 50 by GlnG). A total of 14 factors are involved in regulation of the genes for response to external stresses (purple background in Fig. 6). Stationary phase-specific sigma RpoS is also under the control of CRP.

Bottom Line: Using the newly developed Genomic SELEX screening system of transcription factor-binding sequences, however, we have identified a total of at least 254 CRP-binding sites.Based on the functions of novel target genes, we conclude that CRP plays a key regulatory role in the whole processes from the selective transport of carbon sources, the glycolysis-gluconeogenesis switching to the metabolisms downstream of glycolysis, including tricarboxylic acid (TCA) cycle, pyruvate dehydrogenase (PDH) pathway and aerobic respiration.One unique regulation mode is that a single and the same CRP molecule bound within intergenic regions often regulates both of divergently transcribed operons.

View Article: PubMed Central - PubMed

Affiliation: Department of Frontier Bioscience, Hosei University, Koganei, Tokyo, Japan.

ABSTRACT
CRP (cAMP receptor protein), the global regulator of genes for carbon source utilization in the absence of glucose, is the best-studied prokaryotic transcription factor. A total of 195 target promoters on the Escherichia coli genome have been proposed to be under the control of cAMP-bound CRP. Using the newly developed Genomic SELEX screening system of transcription factor-binding sequences, however, we have identified a total of at least 254 CRP-binding sites. Based on their location on the E. coli genome, we predict a total of at least 183 novel regulation target operons, altogether with the 195 hitherto known targets, reaching to the minimum of 378 promoters as the regulation targets of cAMP-CRP. All the promoters selected from the newly identified targets and examined by using the lacZ reporter assay were found to be under the control of CRP, indicating that the Genomic SELEX screening allowed to identify the CRP targets with high accuracy. Based on the functions of novel target genes, we conclude that CRP plays a key regulatory role in the whole processes from the selective transport of carbon sources, the glycolysis-gluconeogenesis switching to the metabolisms downstream of glycolysis, including tricarboxylic acid (TCA) cycle, pyruvate dehydrogenase (PDH) pathway and aerobic respiration. One unique regulation mode is that a single and the same CRP molecule bound within intergenic regions often regulates both of divergently transcribed operons.

Show MeSH
Related in: MedlinePlus