Transcript Elongation and Termination Are Competitive Kinetic Processes

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1991 Mar 15

PMID 1706521

Citations 47

Authors

P H von Hippel

T D Yager

Affiliations

Soon will be listed here.

Abstract

In this paper, we develop a kinetic approach to predict the efficiency of termination at intrinsic (factor independent) terminators of Escherichia coli and related organisms. In general, our predictions agree well with experimental results. Our analysis also suggests that termination efficiency can readily be modulated by protein factors and environmental variables that shift the kinetic competition toward either elongation or termination. A quantitative framework for the consideration of such regulatory effects is developed and the strengths and limitations of the approach are discussed.

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References

Gill S, Yager T, von Hippel P . Thermodynamic analysis of the transcription cycle in E. coli. Biophys Chem. 1990; 37(1-3):239-50. DOI: 10.1016/0301-4622(90)88023-l. View

Rhodes G, CHAMBERLIN M . Ribonucleic acid chain elongation by Escherichia coli ribonucleic acid polymerase. I. Isolation of ternary complexes and the kinetics of elongation. J Biol Chem. 1974; 249(20):6675-83. View

Andrews C, Richardson J . Transcription termination factor rho mediates simultaneous release of RNA transcripts and DNA template from complexes with Escherichia coli RNA polymerase. J Biol Chem. 1985; 260(9):5826-31. View

Lynn S, Kasper L, GARDNER J . Contributions of RNA secondary structure and length of the thymidine tract to transcription termination at the thr operon attenuator. J Biol Chem. 1988; 263(1):472-9. View

Freier S, Kierzek R, Jaeger J, Sugimoto N, Caruthers M, Neilson T . Improved free-energy parameters for predictions of RNA duplex stability. Proc Natl Acad Sci U S A. 1986; 83(24):9373-7. PMC: 387140. DOI: 10.1073/pnas.83.24.9373. View

Lynn S, Bauer C, Chapman K, GARDNER J . Identification and characterization of mutants affecting transcription termination at the threonine operon attenuator. J Mol Biol. 1985; 183(4):529-41. DOI: 10.1016/0022-2836(85)90169-x. View

Breslauer K, Frank R, Blocker H, Marky L . Predicting DNA duplex stability from the base sequence. Proc Natl Acad Sci U S A. 1986; 83(11):3746-50. PMC: 323600. DOI: 10.1073/pnas.83.11.3746. View

Arndt K, CHAMBERLIN M . RNA chain elongation by Escherichia coli RNA polymerase. Factors affecting the stability of elongating ternary complexes. J Mol Biol. 1990; 213(1):79-108. DOI: 10.1016/S0022-2836(05)80123-8. View

Kolter R, Yanofsky C . Genetic analysis of the tryptophan operon regulatory region using site-directed mutagenesis. J Mol Biol. 1984; 175(3):299-312. DOI: 10.1016/0022-2836(84)90350-4. View

10.

Morgan W, Bear D, von Hippel P . Specificity of release by Escherichia coli transcription termination factor rho of nascent mRNA transcripts initiated at the lambda PR. J Biol Chem. 1984; 259(13):8664-71. View

11.

Winkler M, Mullis K, Barnett J, Stroynowski I, Yanofsky C . Transcription termination at the tryptophan operon attenuator is decreased in vitro by an oligomer complementary to a segment of the leader transcript. Proc Natl Acad Sci U S A. 1982; 79(7):2181-5. PMC: 346154. DOI: 10.1073/pnas.79.7.2181. View

12.

Carpousis A, Gralla J . Cycling of ribonucleic acid polymerase to produce oligonucleotides during initiation in vitro at the lac UV5 promoter. Biochemistry. 1980; 19(14):3245-53. DOI: 10.1021/bi00555a023. View

13.

Zurawski G, Yanofsky C . Escherichia coli tryptophan operon leader mutations, which relieve transcription termination, are cis-dominant to trp leader mutations, which increase transcription termination. J Mol Biol. 1980; 142(1):123-9. DOI: 10.1016/0022-2836(80)90210-7. View

14.

Farnham P, Platt T . Rho-independent termination: dyad symmetry in DNA causes RNA polymerase to pause during transcription in vitro. Nucleic Acids Res. 1981; 9(3):563-77. PMC: 327222. DOI: 10.1093/nar/9.3.563. View

15.

Christie G, Farnham P, Platt T . Synthetic sites for transcription termination and a functional comparison with tryptophan operon termination sites in vitro. Proc Natl Acad Sci U S A. 1981; 78(7):4180-4. PMC: 319752. DOI: 10.1073/pnas.78.7.4180. View

16.

Yanofsky C, vanCleemput M . Nucleotide sequence of trpE of Salmonella typhimurium and its homology with the corresponding sequence of Escherichia coli. J Mol Biol. 1982; 155(3):235-46. DOI: 10.1016/0022-2836(82)90003-1. View

17.

Stauffer G, Zurawski G, Yanofsky C . Single base-pair alterations in the Escherichia coli trp operon leader region that relieve transcription termination at the trp attenuator. Proc Natl Acad Sci U S A. 1978; 75(10):4833-7. PMC: 336215. DOI: 10.1073/pnas.75.10.4833. View

18.

Miozzari G, Yanofsky C . The regulatory region of the trp operon of Serratia marcescens. Nature. 1978; 276(5689):684-9. DOI: 10.1038/276684a0. View

19.

Bertrand K, Korn L, Lee F, Yanofsky C . The attenuator of the tryptophan operon of Escherichia coli. Heterogeneous 3'-OH termini in vivo and deletion mapping of functions. J Mol Biol. 1977; 117(1):227-47. DOI: 10.1016/0022-2836(77)90032-8. View

20.

Manley J, Proudfoot N, Platt T . RNA 3'-end formation. Genes Dev. 1989; 3(12B):2218-22. DOI: 10.1101/gad.3.12b.2218. View