Processivity errors of gene expression in Escherichia coli.

Jørgensen F; Kurland CG

doi:10.1016/s0022-2836(05)80164-0

Abstract

Not all ribosomes that initiate translation of an mRNA sequence will successfully complete it and produce a full-length protein product. By comparing the amounts of lacZ monomer and lacZ dimer protein expressed from a plasmid in a strictly controlled assay, we calculate a dimer to monomer ratio of 0.76. We interpret this to mean that ribosomes have a 76% chance of completing the synthesis of a beta-galactosidase polypeptide. The remaining 24% of the initiated chains end in processivity accidents. For the wild-type, premature RNA polymerase termination is found to account for roughly one-third of the processivity accidents. For the hyperaccurate SmP mutant, we observe a processivity of 0.28, but the presence of streptomycin improves this to 0.50. Thus, the hyperaccuracy with respect to missense substitutions for this mutant is accompanied by a reduced processivity. Addition of streptomycin increase the first error class and reduces the second one. This finding is relevant to the optimization of ribosome function and the growth performance of ribosome mutants.

Full text links

Read article at publisher's site: https://doi.org/10.1016/s0022-2836(05)80164-0

References

Articles referenced by this article (40)

Control of transcription termination.
Adhya S, Gottesman M
Annu Rev Biochem, 967-996 1978
MED: 354508
Suboptimal growth with hyper-accurate ribosomes.
Andersson DI, van Verseveld HW, Stouthamer AH, Kurland CG
Arch Microbiol, (1):96-101 1986
MED: 3963992
Title not supplied
Atkins
1972
Kinetic impairment of restrictive streptomycin-resistant ribosomes.
Bohman K, Ruusala T, Jelenc PC, Kurland CG
Mol Gen Genet, (2):90-99 1984
MED: 6394968
Evidence that the 5' end of lac mRNA starts to decay as soon as it is synthesized.
Cannistraro VJ, Kennell D
J Bacteriol, (2):820-822 1985
MED: 3918023
Specific endonucleolytic cleavage sites for decay of Escherichia coli mRNA.
Cannistraro VJ, Subbarao MN, Kennell D
J Mol Biol, (2):257-274 1986
MED: 2435917
Title not supplied
Carr
Biochem. Soc. Trans. 1985
Chain elongation rate of messenger and polypeptides in slowly growing Escherichia coli.
Coffman RL, Norris TE, Koch AL
J Mol Biol, (1):1-19 1971
MED: 4937191
Genetic studies of the lac repressor. III. Additional correlation of mutational sites with specific amino acid residues.
Coulondre C, Miller JH
J Mol Biol, (3):525-567 1977
MED: 609095
Translational frameshifting: where will it stop?
Craigen WJ, Caskey CT
Cell, (1):1-2 1987
MED: 3297347

Show 10 more references (10 of 40)

Citations & impact

Impact metrics

89

Citations

Jump to Citations

Citations of article over time

Alternative metrics

Altmetric item for https://www.altmetric.com/details/43333925

Altmetric
Discover the attention surrounding your research
https://www.altmetric.com/details/43333925

Article citations

A data-driven estimation of the ribosome drop-off rate in S. cerevisiae reveals a correlation with the genes length.
Awad S, Valleriani A, Chiarugi D
NAR Genom Bioinform, 6(2):lqae036, 18 Apr 2024
Cited by: 0 articles | PMID: 38638702 | PMCID: PMC11025885
This article is in the Europe PMC Open access subset. Refer to the copyright information in the article for licensing details.
Free full text in Europe PMC
Phenotypic mutations contribute to protein diversity and shape protein evolution.
Romero Romero ML, Landerer C, Poehls J, Toth-Petroczy A
Protein Sci, 31(9):e4397, 01 Sep 2022
Cited by: 6 articles | PMID: 36040266 | PMCID: PMC9375231
Review
This article is in the Europe PMC Open access subset. Refer to the copyright information in the article for licensing details.
Free full text in Europe PMC
Genome Expansion by tRNA +1 Frameshifting at Quadruplet Codons.
Gamper H, Masuda I, Hou YM
J Mol Biol, 434(8):167440, 04 Jan 2022
Cited by: 7 articles | PMID: 34995554 | PMCID: PMC9643101
Review Free full text in Europe PMC
Structural basis for +1 ribosomal frameshifting during EF-G-catalyzed translocation.
Demo G, Gamper HB, Loveland AB, Masuda I, Carbone CE, Svidritskiy E, Hou YM, Korostelev AA
Nat Commun, 12(1):4644, 30 Jul 2021
Cited by: 12 articles | PMID: 34330903 | PMCID: PMC8324841
This article is in the Europe PMC Open access subset. Refer to the copyright information in the article for licensing details.
Free full text in Europe PMC
Natural Product Inhibition and Enzyme Kinetics Related to Phylogenetic Characterization for Bacterial Peptidyl-tRNA Hydrolase 1.
Strange DS, Gaffin SS, Holloway WB, Kinsella MD, Wisotsky JN, McFeeters H, McFeeters RL
Molecules, 26(8):2281, 15 Apr 2021
Cited by: 1 article | PMID: 33920799 | PMCID: PMC8071115
This article is in the Europe PMC Open access subset. Refer to the copyright information in the article for licensing details.
Free full text in Europe PMC

Go to all (89) article citations

Search life-sciences literature (45,104,206 articles, preprints and more)

Processivity errors of gene expression in Escherichia coli.

Affiliations

Authors

Abstract

Full text links

References

Control of transcription termination.

Suboptimal growth with hyper-accurate ribosomes.

Title not supplied

Kinetic impairment of restrictive streptomycin-resistant ribosomes.

Evidence that the 5' end of lac mRNA starts to decay as soon as it is synthesized.

Specific endonucleolytic cleavage sites for decay of Escherichia coli mRNA.

Title not supplied

Chain elongation rate of messenger and polypeptides in slowly growing Escherichia coli.

Genetic studies of the lac repressor. III. Additional correlation of mutational sites with specific amino acid residues.

Translational frameshifting: where will it stop?

Citations & impact

Impact metrics

Citations of article over time

Alternative metrics

Article citations

A data-driven estimation of the ribosome drop-off rate in S. cerevisiae reveals a correlation with the genes length.

Phenotypic mutations contribute to protein diversity and shape protein evolution.

Genome Expansion by tRNA +1 Frameshifting at Quadruplet Codons.

Structural basis for +1 ribosomal frameshifting during EF-G-catalyzed translocation.

Natural Product Inhibition and Enzyme Kinetics Related to Phylogenetic Characterization for Bacterial Peptidyl-tRNA Hydrolase 1.

Similar Articles

Ribosome mutants with altered accuracy translate with reduced processivity.

The low expression level of pokeweed antiviral protein (PAP) gene in Escherichia coli by the inducible lac promoter is due to inefficient transcription and translation and not to the toxicity of the PAP.

Coupling of rRNA transcription and ribosomal assembly in vivo. Formation of active ribosomal subunits in Escherichia coli requires transcription of rRNA genes by host RNA polymerase which cannot be replaced by bacteriophage T7 RNA polymerase.

Some base substitutions in the leader of an Escherichia coli ribosomal RNA operon affect the structure and function of ribosomes. Evidence for a transient scaffold function of the rRNA leader.

Partnerships & funding

Similar Articles

Ribosome mutants with altered accuracy translate with reduced processivity.
J Mol Biol, 248(3):551-561, 01 May 1995

The low expression level of pokeweed antiviral protein (PAP) gene in Escherichia coli by the inducible lac promoter is due to inefficient transcription and translation and not to the toxicity of the PAP.
Arch Biochem Biophys, 351(1):82-88, 01 Mar 1998

Coupling of rRNA transcription and ribosomal assembly in vivo. Formation of active ribosomal subunits in Escherichia coli requires transcription of rRNA genes by host RNA polymerase which cannot be replaced by bacteriophage T7 RNA polymerase.
J Mol Biol, 231(3):581-593, 01 Jun 1993

Some base substitutions in the leader of an Escherichia coli ribosomal RNA operon affect the structure and function of ribosomes. Evidence for a transient scaffold function of the rRNA leader.
J Mol Biol, 233(2):203-218, 01 Sep 1993

Search life-sciences literature (45,104,206 articles, preprints and more)

Processivity errors of gene expression in Escherichia coli.

Author information

Affiliations

Authors

Abstract

Full text links

References

Title not supplied

Title not supplied

Citations & impact

Impact metrics

Citations of article over time

Alternative metrics

Article citations

Similar Articles

Partnerships & funding