Differential Polypeptide Synthesis of the Proton-translocating ATPase of Escherichia Coli

Overview

Journal J Bacteriol

Publisher American Society for Microbiology

Specialty Microbiology

Date 1982 Sep 1

PMID 6213603

Citations 27

Authors

W S Brusilow

D J Klionsky

R D Simoni

Affiliations

Soon will be listed here.

Abstract

We investigated the regulation of the synthesis of the eight polypeptides of the Escherichia coli proton-translocating ATPase. A plasmid carrying the eight genes of the unc operon was used to direct in vivo and in vitro protein synthesis of the eight polypeptides. Analysis of these data indicates that the ATPase polypeptides are synthesized in unequal amounts both in vitro and in vivo. We identified several regions within the unc operon at which expression of a gene is either increased or decreased from that of the preceding gene. Since genetic information indicates a single polycistronic mRNA for all eight genes of this operon, the observed differential synthesis of the polypeptides is most likely the result of translational regulation. The effect of varying the temperature suggests that the secondary structure in the mRNA may affect the rate of translation initiation in the region between uncE and uncF.

Citing Articles

Insights into the adaptive response of Arabidopsis thaliana to prolonged thermal stress by ribosomal profiling and RNA-Seq.

Lukoszek R, Feist P, Ignatova Z BMC Plant Biol. 2016; 16(1):221.

PMID: 27724872 PMC: 5057212. DOI: 10.1186/s12870-016-0915-0.

The Phytohormone Ethylene Enhances Cellulose Production, Regulates CRP/FNRKx Transcription and Causes Differential Gene Expression within the Bacterial Cellulose Synthesis Operon of Komagataeibacter (Gluconacetobacter) xylinus ATCC 53582.

Augimeri R, Strap J Front Microbiol. 2016; 6:1459.

PMID: 26733991 PMC: 4686702. DOI: 10.3389/fmicb.2015.01459.

Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources.

Li G, Burkhardt D, Gross C, Weissman J Cell. 2014; 157(3):624-35.

PMID: 24766808 PMC: 4006352. DOI: 10.1016/j.cell.2014.02.033.

Structure, organization and expression of cyanobacterial ATP synthase genes.

Curtis S Photosynth Res. 2014; 18(1-2):223-44.

PMID: 24425167 DOI: 10.1007/BF00042986.

Assembly of the stator in Escherichia coli ATP synthase. Complexation of alpha subunit with other F1 subunits is prerequisite for delta subunit binding to the N-terminal region of alpha.

Senior A, Muharemagic A, Wilke-Mounts S Biochemistry. 2006; 45(51):15893-902.

PMID: 17176112 PMC: 2548287. DOI: 10.1021/bi0619730.

References

Borer P, Dengler B, Tinoco Jr I, Uhlenbeck O . Stability of ribonucleic acid double-stranded helices. J Mol Biol. 1974; 86(4):843-53. DOI: 10.1016/0022-2836(74)90357-x. View

Friedl P, Friedl C, Schairer H . The ATP synthetase of Escherichia coli K12: purification of the enzyme and reconstitution of energy-transducing activities. Eur J Biochem. 1979; 100(1):175-80. DOI: 10.1111/j.1432-1033.1979.tb02046.x. View

Simoni R, Shandell A . Energy transduction in Escherichia coli. Genetic alteration of a membrane polypeptide of the (Ca2+,Mg2+)-ATPase. J Biol Chem. 1975; 250(24):9421-7. View

Nielsen J, Hansen F, Hoppe J, Friedl P, von Meyenburg K . The nucleotide sequence of the atp genes coding for the F0 subunits a, b, c and the F1 subunit delta of the membrane bound ATP synthase of Escherichia coli. Mol Gen Genet. 1981; 184(1):33-9. DOI: 10.1007/BF00271191. View

Downie J, Gibson F, Cox G . Membrane adenosine triphosphatases of prokaryotic cells. Annu Rev Biochem. 1979; 48:103-31. DOI: 10.1146/annurev.bi.48.070179.000535. View

Kanazawa H, Mabuchi K, Kayano T, Noumi T, Sekiya T, Futai M . Nucleotide sequence of the genes for F0 components of the proton-translocating ATPase from Escherichia coli: prediction of the primary structure of F0 subunits. Biochem Biophys Res Commun. 1981; 103(2):613-20. DOI: 10.1016/0006-291x(81)90495-2. View

Gay N, Walker J . The atp operon: nucleotide sequence of the promoter and the genes for the membrane proteins, and the delta subunit of Escherichia coli ATP-synthase. Nucleic Acids Res. 1981; 9(16):3919-26. PMC: 327405. DOI: 10.1093/nar/9.16.3919. View

Gold L, Pribnow D, Schneider T, Shinedling S, Singer B, Stormo G . Translational initiation in prokaryotes. Annu Rev Microbiol. 1981; 35:365-403. DOI: 10.1146/annurev.mi.35.100181.002053. View

ZALKIN H, Yanofsky C, Squires C . Regulated in vitro synthesis of Escherichia coli tryptophan operon messenger ribonucleic acid and enzymes. J Biol Chem. 1974; 249(2):465-75. View

10.

Friedl P, Schairer H . The isolated F0 of Escherichia coli aTP-synthase is reconstitutively active in H+-conduction and ATP-dependent energy-transduction. FEBS Lett. 1981; 128(2):261-4. DOI: 10.1016/0014-5793(81)80094-4. View

11.

Hansen F, Nielsen J, Riise E, von Meyenburg K . The genes for the eight subunits of the membrane bound ATP synthase of Escherichia coli. Mol Gen Genet. 1981; 183(3):463-72. DOI: 10.1007/BF00268766. View

12.

Dougan G, Sherratt D . The transposon Tn1 as a probe for studying ColE1 structure and function. Mol Gen Genet. 1977; 151(2):151-60. DOI: 10.1007/BF00338689. View

13.

Steitz J, Jakes K . How ribosomes select initiator regions in mRNA: base pair formation between the 3' terminus of 16S rRNA and the mRNA during initiation of protein synthesis in Escherichia coli. Proc Natl Acad Sci U S A. 1975; 72(12):4734-8. PMC: 388805. DOI: 10.1073/pnas.72.12.4734. View

14.

Kanazawa H, Miki T, Tamura F, Yura T, Futai M . Specialized transducing phage lambda carrying the genes for coupling factor of oxidative phosphorylation of Escherichia coli: increased synthesis of coupling factor on induction of prophage lambda asn. Proc Natl Acad Sci U S A. 1979; 76(3):1126-30. PMC: 383202. DOI: 10.1073/pnas.76.3.1126. View

15.

DeFranco A, Koshland Jr D . Molecular cloning of chemotaxis genes and overproduction of gene products in the bacterial sensing system. J Bacteriol. 1981; 147(2):390-400. PMC: 216057. DOI: 10.1128/jb.147.2.390-400.1981. View

16.

Dunn J, Studier F . Mutations of bacteriophage T7 that affect initiation of synthesis of the gene 0.3 protein. Proc Natl Acad Sci U S A. 1978; 75(6):2741-5. PMC: 392639. DOI: 10.1073/pnas.75.6.2741. View

17.

Gunsalus R, Brusilow W, Simoni R . Gene order and gene-polypeptide relationships of the proton-translocating ATPase operon (unc) of Escherichia coli. Proc Natl Acad Sci U S A. 1982; 79(2):320-4. PMC: 345718. DOI: 10.1073/pnas.79.2.320. View

18.

Foster D, Fillingame R . Energy-transducing H+-ATPase of Escherichia coli. Purification, reconstitution, and subunit composition. J Biol Chem. 1979; 254(17):8230-6. View

19.

Tinoco Jr I, Borer P, Dengler B, Levin M, Uhlenbeck O, Crothers D . Improved estimation of secondary structure in ribonucleic acids. Nat New Biol. 1973; 246(150):40-1. DOI: 10.1038/newbio246040a0. View

20.

Roozen K, Fenwick Jr R, Curtiss 3rd R . Synthesis of ribonucleic acid and protein in plasmid-containing minicells of Escherichia coli K-12. J Bacteriol. 1971; 107(1):21-33. PMC: 246882. DOI: 10.1128/jb.107.1.21-33.1971. View