Cotranslational Insertion of Selenocysteine into Formate Dehydrogenase from Escherichia Coli Directed by a UGA Codon

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1987 May 1

PMID 3033637

Citations 87

Authors

F Zinoni

A Birkmann

W Leinfelder

A Bock

Affiliations

Soon will be listed here.

Abstract

The structural gene (fdhF) for the 80-kDa selenopolypeptide of formate dehydrogenase (formate:benzyl viologen oxidoreductase, EC 1.2.--.--) from Escherichia coli contains an in-frame UGA codon at amino acid position 140 that is translated. Translation of gene fusions between N-terminal parts of fdhF with lacZ depends on the availability of selenium in the medium when the hybrid gene contains the UGA codon; it is independent of the presence of selenium when an fdhF portion upstream of the UGA position is fused to lacZ. Transcription does not require the presence of selenium in either case. By localized mutagenesis, the UGA codon was converted into serine (UCA) and cysteine (UGC and UGU) codons. Each mutation relieved the selenium dependency of fdhF mRNA translation. Selenium incorporation was completely abolished in the case of the UCA insertion and was reduced to about 10% when the UGA was replaced by a cysteine codon. Insertion of UCA yielded an inactive fdhF gene product, while insertion of UGC and UGU resulted in polypeptides with lowered activities as components in the system formerly known as formate hydrogenlyase. Altogether the results indicate that the UGA codon at position 140 directs the cotranslational insertion of selenocysteine into the fdhF polypeptide chain.

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References

Balch W, WOLFE R . New approach to the cultivation of methanogenic bacteria: 2-mercaptoethanesulfonic acid (HS-CoM)-dependent growth of Methanobacterium ruminantium in a pressureized atmosphere. Appl Environ Microbiol. 1976; 32(6):781-91. PMC: 170461. DOI: 10.1128/aem.32.6.781-791.1976. View

Lehrach H, Diamond D, Wozney J, Boedtker H . RNA molecular weight determinations by gel electrophoresis under denaturing conditions, a critical reexamination. Biochemistry. 1977; 16(21):4743-51. DOI: 10.1021/bi00640a033. View

SANGER F, Nicklen S, Coulson A . DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977; 74(12):5463-7. PMC: 431765. DOI: 10.1073/pnas.74.12.5463. View

Chang A, Cohen S . Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol. 1978; 134(3):1141-56. PMC: 222365. DOI: 10.1128/jb.134.3.1141-1156.1978. View

Crea R, Kraszewski A, Hirose T, Itakura K . Chemical synthesis of genes for human insulin. Proc Natl Acad Sci U S A. 1978; 75(12):5765-9. PMC: 393054. DOI: 10.1073/pnas.75.12.5765. View

Casadaban M, Cohen S . Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage: in vivo probe for transcriptional control sequences. Proc Natl Acad Sci U S A. 1979; 76(9):4530-3. PMC: 411611. DOI: 10.1073/pnas.76.9.4530. View

Maxam A, Gilbert W . Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980; 65(1):499-560. DOI: 10.1016/s0076-6879(80)65059-9. View

Csonka L, Clark A . Construction of an Hfr strain useful for transferring recA mutations between Escherichia coli strains. J Bacteriol. 1980; 143(1):529-30. PMC: 294283. DOI: 10.1128/jb.143.1.529-530.1980. View

Casadaban M, Chou J, Cohen S . In vitro gene fusions that join an enzymatically active beta-galactosidase segment to amino-terminal fragments of exogenous proteins: Escherichia coli plasmid vectors for the detection and cloning of translational initiation signals. J Bacteriol. 1980; 143(2):971-80. PMC: 294402. DOI: 10.1128/jb.143.2.971-980.1980. View

10.

Cox J, Edwards E, Demoss J . Resolution of distinct selenium-containing formate dehydrogenases from Escherichia coli. J Bacteriol. 1981; 145(3):1317-24. PMC: 217135. DOI: 10.1128/jb.145.3.1317-1324.1981. View

11.

Diamond A, Dudock B, HATFIELD D . Structure and properties of a bovine liver UGA suppressor serine tRNA with a tryptophan anticodon. Cell. 1981; 25(2):497-506. DOI: 10.1016/0092-8674(81)90068-4. View

12.

Aiba H, Adhya S, de Crombrugghe B . Evidence for two functional gal promoters in intact Escherichia coli cells. J Biol Chem. 1981; 256(22):11905-10. View

13.

Howe J, Hershey J . A sensitive immunoblotting method for measuring protein synthesis initiation factor levels in lysates of Escherichia coli. J Biol Chem. 1981; 256(24):12836-9. View

14.

HATFIELD D, Diamond A, Dudock B . Opal suppressor serine tRNAs from bovine liver form phosphoseryl-tRNA. Proc Natl Acad Sci U S A. 1982; 79(20):6215-9. PMC: 347090. DOI: 10.1073/pnas.79.20.6215. View

15.

Condell R, Tappel A . Amino acid sequence around the active-site selenocysteine of rat liver glutathione peroxidase. Biochim Biophys Acta. 1982; 709(2):304-9. DOI: 10.1016/0167-4838(82)90472-1. View

16.

Messing J, Vieira J . A new pair of M13 vectors for selecting either DNA strand of double-digest restriction fragments. Gene. 1982; 19(3):269-76. DOI: 10.1016/0378-1119(82)90016-6. View

17.

Zoller M, Smith M . Oligonucleotide-directed mutagenesis of DNA fragments cloned into M13 vectors. Methods Enzymol. 1983; 100:468-500. DOI: 10.1016/0076-6879(83)00074-9. View

18.

Norrander J, Kempe T, Messing J . Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene. 1983; 26(1):101-6. DOI: 10.1016/0378-1119(83)90040-9. View

19.

Gunzler W, Steffens G, Grossmann A, Kim S, Otting F, Wendel A . The amino-acid sequence of bovine glutathione peroxidase. Hoppe Seylers Z Physiol Chem. 1984; 365(2):195-212. DOI: 10.1515/bchm2.1984.365.1.195. View

20.

Kramer W, Drutsa V, Jansen H, Kramer B, PFLUGFELDER M, Fritz H . The gapped duplex DNA approach to oligonucleotide-directed mutation construction. Nucleic Acids Res. 1984; 12(24):9441-56. PMC: 320472. DOI: 10.1093/nar/12.24.9441. View