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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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Related in: MedlinePlus

Regulation of the divergently transcribed promoters by CRP.Some of the divergently aligned promoters are controlled by CRP molecule(s) bound within spacers. The gene organization and the binding sites of CRP within the spacer regions are shown: (A) divergent promoters are regulated by single and the same CRP bound within spacers; (B) divergent promoters are regulated by different CRP molecules bound within spacers; and (C) multiple CRP molecules bind to spacer between divergent promoters, but the role of each CRP remains unidentified. The numbers above DNA indicate the distance between the initiation sites of divergent transcription.
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pone-0020081-g004: Regulation of the divergently transcribed promoters by CRP.Some of the divergently aligned promoters are controlled by CRP molecule(s) bound within spacers. The gene organization and the binding sites of CRP within the spacer regions are shown: (A) divergent promoters are regulated by single and the same CRP bound within spacers; (B) divergent promoters are regulated by different CRP molecules bound within spacers; and (C) multiple CRP molecules bind to spacer between divergent promoters, but the role of each CRP remains unidentified. The numbers above DNA indicate the distance between the initiation sites of divergent transcription.

Mentions: In E. coli, it is rare that a single and the same regulator controls divergently aligned promoters, which direct transcription toward opposite directions. After a systematic comparison of the CRP-binding sites within intergenic regions of divergent promoters, both being under the control of cAMP-CRP, a single CRP-binding site was detected for a total of 11 cases, araBAD-araC, gcd-hpt, maoC-paaABCDEFGHIJK, gltA-sdhCDAB, guaBA-xseA, metY-argG, glpEGR-glpD, xylAB-xylFGHR, prpR-prpBCDE, rhaT-sodA and fruBKA-setB (Fig. 4A). One unique feature of the regulation mode by cAMP-CRP is that a single and the same transcription factor bound within an intergenic spacer region controls both of the divergently aligned promoters. Using a model system, El-Robh and Busby [43] performed a detailed study of transcription activation of divergent promoters by a single CRP molecule.


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)

Regulation of the divergently transcribed promoters by CRP.Some of the divergently aligned promoters are controlled by CRP molecule(s) bound within spacers. The gene organization and the binding sites of CRP within the spacer regions are shown: (A) divergent promoters are regulated by single and the same CRP bound within spacers; (B) divergent promoters are regulated by different CRP molecules bound within spacers; and (C) multiple CRP molecules bind to spacer between divergent promoters, but the role of each CRP remains unidentified. The numbers above DNA indicate the distance between the initiation sites of divergent transcription.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0020081-g004: Regulation of the divergently transcribed promoters by CRP.Some of the divergently aligned promoters are controlled by CRP molecule(s) bound within spacers. The gene organization and the binding sites of CRP within the spacer regions are shown: (A) divergent promoters are regulated by single and the same CRP bound within spacers; (B) divergent promoters are regulated by different CRP molecules bound within spacers; and (C) multiple CRP molecules bind to spacer between divergent promoters, but the role of each CRP remains unidentified. The numbers above DNA indicate the distance between the initiation sites of divergent transcription.
Mentions: In E. coli, it is rare that a single and the same regulator controls divergently aligned promoters, which direct transcription toward opposite directions. After a systematic comparison of the CRP-binding sites within intergenic regions of divergent promoters, both being under the control of cAMP-CRP, a single CRP-binding site was detected for a total of 11 cases, araBAD-araC, gcd-hpt, maoC-paaABCDEFGHIJK, gltA-sdhCDAB, guaBA-xseA, metY-argG, glpEGR-glpD, xylAB-xylFGHR, prpR-prpBCDE, rhaT-sodA and fruBKA-setB (Fig. 4A). One unique feature of the regulation mode by cAMP-CRP is that a single and the same transcription factor bound within an intergenic spacer region controls both of the divergently aligned promoters. Using a model system, El-Robh and Busby [43] performed a detailed study of transcription activation of divergent promoters by a single CRP molecule.

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