DOI: 10.1101/gad.8.23.2904. Regulation of pyrBI operon expression in Escherichia coli by UTP-sensitive reiterative RNA synthesis during transcriptional initiation.

Regulation of pyrBI operon expression in Escherichia coli by UTP-sensitive reiterative RNA synthesis during transcriptional initiation.

10.1101/gad.8.23.2904

Crossref journal-article

Cold Spring Harbor Laboratory

Genes & Development (246)

Abstract

Pyrimidine-mediated regulation of pyrBI operon expression in Escherichia coli K-12 occurs through UTP-sensitive transcriptional attenuation and through a second mechanism that functions at the level of transcriptional initiation. In this study we demonstrate that this second control mechanism is based on UTP-sensitive reiterative RNA synthesis within a run of three T-A base pairs in the pyrBI initially transcribed region. Our results show that high UTP levels induce the synthesis in vitro of nascent transcripts with the sequence AAUUUUn (where n = 1 to > 30), which are not extended downstream to include pyrBI sequences. Synthesis of these transcripts, which are initiated at the predominant in vivo transcriptional start site, inhibits the production of full-length pyrBI transcripts. A TTT to GTA mutation in the pyrBI initially transcribed region eliminates reiterative transcription and stimulates productive transcription in vitro. When introduced into the E. coli chromosome, this mutation causes a sevenfold increase in pyrBI expression in cells grown under conditions of pyrimidine excess and nearly abolishes pyrimidine-mediated regulation of pyrBI expression when coupled with a mutation that eliminates attenuation control. Additional experiments indicate that the context of the three T-A base pairs within the pyrBI initially transcribed region is important for reiterative transcription. A possible mechanism for reiterative transcription and the likely involvement of this process in the regulation of other genes are discussed.

Bibliography

Liu, C., Heath, L. S., & Turnbough, C. L. (1994). Regulation of pyrBI operon expression in Escherichia coli by UTP-sensitive reiterative RNA synthesis during transcriptional initiation. Genes & Development, 8(23), 2904â2912.

Authors 3

C Liu (first)
L S Heath (additional)
C L Turnbough (additional)

References 23 Referenced 57

10.1128/jb.133.1.149-157.1978 / J. Bacteriol. / Transport of antibiotics and metabolite analogs by systems under cyclic AMP control: Positive selection of Salmonella typhimurium cya and crp mutants. (1978)
10.1111/j.1365-2958.1991.tb02113.x
10.1016/S0022-2836(64)80120-0 / J. Mol. Biol. / Mechanism of RNA polymerase action: Characterization of the DNA-dependent synthesis of polyadenylic acid. (1964)
Chan, C.L. and R. Landick. 1994. New perspectives on RNA chain elongation and termination by E. coli RNA polymerase. In Transcription: Mechanisms and regulation (ed. R. Conaway and J. Conaway), pp. 297â320. Raven Press, New York.
10.1016/S0021-9258(17)30629-4 / J. Biol. Chem. / Characterization of transcriptional initiation from promoters P1 and P2 of the pyrBI operon of Escherichia coli K12. (1990)
10.1016/S0021-9258(17)32433-X / J. Biol. Chem. / Nucleotide-specific transcriptional pausing in the pyrBI leader region of Escherichia coli K-12. (1994)
Dorit, R.L. and O. Ohara. 1991. Direct DNA sequencing of PCR products. In Current protocols in molecular biology (ed. F.M. Ausubel, R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl), pp. 15.2.3. John Wiley & Sons, New York.
10.1101/gad.5.5.707
10.1101/gad.4.10.1801
10.1006/jmbi.1994.1119
10.1016/0076-6879(87)54085-X / Methods Enzymol. / Rapid and efficient site-specific mutagenesis without phenotypic selection. (1987)
Landick, R. and C.L. Turnbough Jr. 1992. Transcriptional attenuation. In Transcriptional regulation (ed. S.L. McKnight and K.R. Yamamoto), pp. 407â446. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
10.1128/jb.171.6.3337-3342.1989 / J. Bacteriol. / Multiple control mechanisms for pyrimidine-mediated regulation of pyrBI operon expression in Escherichia coli K-12. (1989)
10.1128/jb.176.10.2938-2945.1994 / J. Bacteriol. / Effects of transcriptional start site sequence and position on nucleotide-sensitive selection of alternative start sites at the pyrC promoter in Escherichia coli. (1994)
10.1128/jb.175.8.2363-2369.1993 / J. Bacteriol. / Genetic evidence that promoter P2 is the physiologically significant promoter for the pyrBI operon of Escherichia coli K-12. (1993)
10.1093/nar/8.10.2295
Neuhard, J. and P. Nygaard. 1987. Purines and pyrimidines. In Escherichia coli and Salmonella typhimurium: Cellular and molecular biology (ed. F.C. Neidhardt, J.L. Ingraham, K.B. Low, B. Magasanik, M. Schaechter, and H.E. Umbarger), pp. 445â473. American Society for Microbiology, Washington, D.C.
10.1128/jb.163.3.991-999.1985 / J. Bacteriol. / Role of translation and attenuation in the control of pyrBI operon expression in Escherichia coli K-12. (1985)
10.1073/pnas.85.19.7149
10.1128/jb.153.2.998-1007.1983 / J. Bacteriol. / Regulation of Escherichia coli aspartate transcarbamylase synthesis by guanosine tetraphosphate and pyrimidine ribonucleoside triphosphates. (1983)
10.1073/pnas.80.2.368
10.1006/jmbi.1993.1310
10.1128/jb.158.3.1018-1024.1984 / J. Bacteriol. / Repression is relieved before attenuation in the trp operon of Escherichia coli as tryptophan starvation becomes increasingly severe. (1984)

Dates

Type	When
Created	18 years, 2 months ago (June 5, 2007, 5:15 p.m.)
Deposited	3 years, 9 months ago (Nov. 14, 2021, 9:27 p.m.)
Indexed	1 year ago (Aug. 6, 2024, 10:57 p.m.)
Issued	30 years, 9 months ago (Dec. 1, 1994)
Published	30 years, 9 months ago (Dec. 1, 1994)
Published Online	30 years, 9 months ago (Dec. 1, 1994)
Published Print	30 years, 9 months ago (Dec. 1, 1994)

Funders 0

None

BibTeX

@article{Liu_1994, title={Regulation of pyrBI operon expression in Escherichia coli by UTP-sensitive reiterative RNA synthesis during transcriptional initiation.}, volume={8}, ISSN={1549-5477}, url={http://dx.doi.org/10.1101/gad.8.23.2904}, DOI={10.1101/gad.8.23.2904}, number={23}, journal={Genes & Development}, publisher={Cold Spring Harbor Laboratory}, author={Liu, C and Heath, L S and Turnbough, C L}, year={1994}, month=dec, pages={2904–2912} }

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