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. 1986 Dec;83(23):8849–8853. doi: 10.1073/pnas.83.23.8849

A GTP-binding protein of Escherichia coli has homology to yeast RAS proteins.

J Ahnn, P E March, H E Takiff, M Inouye
PMCID: PMC387030  PMID: 3097637

Abstract

The DNA sequence of a gene (era) located immediately downstream of the gene (rnc) encoding ribonuclease III of Escherichia coli was determined and found to encode a protein of 316 amino acid residues. The amino acid sequence of this protein, Era, has significant similarity to the yeast RAS proteins. Overexpression of the Era protein was achieved and GTP cross-linking experiments demonstrated that the protein was indeed capable of binding GTP, as are the yeast and mammalian ras gene products. These data indicate that ras-related sequences occur not only in eukaryotes but also in prokaryotes.

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Selected References

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  1. Broek D., Samiy N., Fasano O., Fujiyama A., Tamanoi F., Northup J., Wigler M. Differential activation of yeast adenylate cyclase by wild-type and mutant RAS proteins. Cell. 1985 Jul;41(3):763–769. doi: 10.1016/s0092-8674(85)80057-x. [DOI] [PubMed] [Google Scholar]
  2. Capon D. J., Chen E. Y., Levinson A. D., Seeburg P. H., Goeddel D. V. Complete nucleotide sequences of the T24 human bladder carcinoma oncogene and its normal homologue. Nature. 1983 Mar 3;302(5903):33–37. doi: 10.1038/302033a0. [DOI] [PubMed] [Google Scholar]
  3. Capon D. J., Seeburg P. H., McGrath J. P., Hayflick J. S., Edman U., Levinson A. D., Goeddel D. V. Activation of Ki-ras2 gene in human colon and lung carcinomas by two different point mutations. Nature. 1983 Aug 11;304(5926):507–513. doi: 10.1038/304507a0. [DOI] [PubMed] [Google Scholar]
  4. Chou P. Y., Fasman G. D. Empirical predictions of protein conformation. Annu Rev Biochem. 1978;47:251–276. doi: 10.1146/annurev.bi.47.070178.001343. [DOI] [PubMed] [Google Scholar]
  5. DeFeo-Jones D., Scolnick E. M., Koller R., Dhar R. ras-Related gene sequences identified and isolated from Saccharomyces cerevisiae. Nature. 1983 Dec 15;306(5944):707–709. doi: 10.1038/306707a0. [DOI] [PubMed] [Google Scholar]
  6. Der C. J., Krontiris T. G., Cooper G. M. Transforming genes of human bladder and lung carcinoma cell lines are homologous to the ras genes of Harvey and Kirsten sarcoma viruses. Proc Natl Acad Sci U S A. 1982 Jun;79(11):3637–3640. doi: 10.1073/pnas.79.11.3637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fukui Y., Kaziro Y. Molecular cloning and sequence analysis of a ras gene from Schizosaccharomyces pombe. EMBO J. 1985 Mar;4(3):687–691. doi: 10.1002/j.1460-2075.1985.tb03684.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gallwitz D., Donath C., Sander C. A yeast gene encoding a protein homologous to the human c-has/bas proto-oncogene product. Nature. 1983 Dec 15;306(5944):704–707. doi: 10.1038/306704a0. [DOI] [PubMed] [Google Scholar]
  9. Hall A., Marshall C. J., Spurr N. K., Weiss R. A. Identification of transforming gene in two human sarcoma cell lines as a new member of the ras gene family located on chromosome 1. Nature. 1983 Jun 2;303(5916):396–400. doi: 10.1038/303396a0. [DOI] [PubMed] [Google Scholar]
  10. Inouye S., Inouye M. Up-promoter mutations in the lpp gene of Escherichia coli. Nucleic Acids Res. 1985 May 10;13(9):3101–3110. doi: 10.1093/nar/13.9.3101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Jurnak F. Structure of the GDP domain of EF-Tu and location of the amino acids homologous to ras oncogene proteins. Science. 1985 Oct 4;230(4721):32–36. doi: 10.1126/science.3898365. [DOI] [PubMed] [Google Scholar]
  12. Land H., Parada L. F., Weinberg R. A. Cellular oncogenes and multistep carcinogenesis. Science. 1983 Nov 18;222(4625):771–778. doi: 10.1126/science.6356358. [DOI] [PubMed] [Google Scholar]
  13. March P. E., Ahnn J., Inouye M. The DNA sequence of the gene (rnc) encoding ribonuclease III of Escherichia coli. Nucleic Acids Res. 1985 Jul 11;13(13):4677–4685. doi: 10.1093/nar/13.13.4677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. March P. E., Inouye M. Characterization of the lep operon of Escherichia coli. Identification of the promoter and the gene upstream of the signal peptidase I gene. J Biol Chem. 1985 Jun 25;260(12):7206–7213. [PubMed] [Google Scholar]
  15. March P. E., Inouye M. GTP-binding membrane protein of Escherichia coli with sequence homology to initiation factor 2 and elongation factors Tu and G. Proc Natl Acad Sci U S A. 1985 Nov;82(22):7500–7504. doi: 10.1073/pnas.82.22.7500. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Maxam A. M., Gilbert W. A new method for sequencing DNA. Proc Natl Acad Sci U S A. 1977 Feb;74(2):560–564. doi: 10.1073/pnas.74.2.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. McCormick F., Clark B. F., la Cour T. F., Kjeldgaard M., Norskov-Lauritsen L., Nyborg J. A model for the tertiary structure of p21, the product of the ras oncogene. Science. 1985 Oct 4;230(4721):78–82. doi: 10.1126/science.3898366. [DOI] [PubMed] [Google Scholar]
  18. McGrath J. P., Capon D. J., Smith D. H., Chen E. Y., Seeburg P. H., Goeddel D. V., Levinson A. D. Structure and organization of the human Ki-ras proto-oncogene and a related processed pseudogene. Nature. 1983 Aug 11;304(5926):501–506. doi: 10.1038/304501a0. [DOI] [PubMed] [Google Scholar]
  19. Neuman-Silberberg F. S., Schejter E., Hoffmann F. M., Shilo B. Z. The Drosophila ras oncogenes: structure and nucleotide sequence. Cell. 1984 Jul;37(3):1027–1033. doi: 10.1016/0092-8674(84)90437-9. [DOI] [PubMed] [Google Scholar]
  20. Parada L. F., Tabin C. J., Shih C., Weinberg R. A. Human EJ bladder carcinoma oncogene is homologue of Harvey sarcoma virus ras gene. Nature. 1982 Jun 10;297(5866):474–478. doi: 10.1038/297474a0. [DOI] [PubMed] [Google Scholar]
  21. Powers S., Kataoka T., Fasano O., Goldfarb M., Strathern J., Broach J., Wigler M. Genes in S. cerevisiae encoding proteins with domains homologous to the mammalian ras proteins. Cell. 1984 Mar;36(3):607–612. doi: 10.1016/0092-8674(84)90340-4. [DOI] [PubMed] [Google Scholar]
  22. Reddy E. P., Reynolds R. K., Santos E., Barbacid M. A point mutation is responsible for the acquisition of transforming properties by the T24 human bladder carcinoma oncogene. Nature. 1982 Nov 11;300(5888):149–152. doi: 10.1038/300149a0. [DOI] [PubMed] [Google Scholar]
  23. Reymond C. D., Gomer R. H., Mehdy M. C., Firtel R. A. Developmental regulation of a Dictyostelium gene encoding a protein homologous to mammalian ras protein. Cell. 1984 Nov;39(1):141–148. doi: 10.1016/0092-8674(84)90199-5. [DOI] [PubMed] [Google Scholar]
  24. Sacerdot C., Dessen P., Hershey J. W., Plumbridge J. A., Grunberg-Manago M. Sequence of the initiation factor IF2 gene: unusual protein features and homologies with elongation factors. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7787–7791. doi: 10.1073/pnas.81.24.7787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Santos E., Tronick S. R., Aaronson S. A., Pulciani S., Barbacid M. T24 human bladder carcinoma oncogene is an activated form of the normal human homologue of BALB- and Harvey-MSV transforming genes. Nature. 1982 Jul 22;298(5872):343–347. doi: 10.1038/298343a0. [DOI] [PubMed] [Google Scholar]
  27. Seeburg P. H., Colby W. W., Capon D. J., Goeddel D. V., Levinson A. D. Biological properties of human c-Ha-ras1 genes mutated at codon 12. Nature. 1984 Nov 1;312(5989):71–75. doi: 10.1038/312071a0. [DOI] [PubMed] [Google Scholar]
  28. Shih T. Y., Papageorge A. G., Stokes P. E., Weeks M. O., Scolnick E. M. Guanine nucleotide-binding and autophosphorylating activities associated with the p21src protein of Harvey murine sarcoma virus. Nature. 1980 Oct 23;287(5784):686–691. doi: 10.1038/287686a0. [DOI] [PubMed] [Google Scholar]
  29. Shilo B. Z., Weinberg R. A. DNA sequences homologous to vertebrate oncogenes are conserved in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1981 Nov;78(11):6789–6792. doi: 10.1073/pnas.78.11.6789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shimizu K., Birnbaum D., Ruley M. A., Fasano O., Suard Y., Edlund L., Taparowsky E., Goldfarb M., Wigler M. Structure of the Ki-ras gene of the human lung carcinoma cell line Calu-1. Nature. 1983 Aug 11;304(5926):497–500. doi: 10.1038/304497a0. [DOI] [PubMed] [Google Scholar]
  31. Shimizu K., Goldfarb M., Suard Y., Perucho M., Li Y., Kamata T., Feramisco J., Stavnezer E., Fogh J., Wigler M. H. Three human transforming genes are related to the viral ras oncogenes. Proc Natl Acad Sci U S A. 1983 Apr;80(8):2112–2116. doi: 10.1073/pnas.80.8.2112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Shine J., Dalgarno L. The 3'-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1342–1346. doi: 10.1073/pnas.71.4.1342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Stein R. B., Robinson P. S., Scolnick E. M. Photoaffinity labeling with GTP of viral p21 ras protein expressed in Escherichia coli. J Virol. 1984 May;50(2):343–351. doi: 10.1128/jvi.50.2.343-351.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Studier F. W. Genetic mapping of a mutation that causes ribonucleases III deficiency in Escherichia coli. J Bacteriol. 1975 Oct;124(1):307–316. doi: 10.1128/jb.124.1.307-316.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Tabin C. J., Bradley S. M., Bargmann C. I., Weinberg R. A., Papageorge A. G., Scolnick E. M., Dhar R., Lowy D. R., Chang E. H. Mechanism of activation of a human oncogene. Nature. 1982 Nov 11;300(5888):143–149. doi: 10.1038/300143a0. [DOI] [PubMed] [Google Scholar]
  36. Taparowsky E., Shimizu K., Goldfarb M., Wigler M. Structure and activation of the human N-ras gene. Cell. 1983 Sep;34(2):581–586. doi: 10.1016/0092-8674(83)90390-2. [DOI] [PubMed] [Google Scholar]
  37. Taparowsky E., Suard Y., Fasano O., Shimizu K., Goldfarb M., Wigler M. Activation of the T24 bladder carcinoma transforming gene is linked to a single amino acid change. Nature. 1982 Dec 23;300(5894):762–765. doi: 10.1038/300762a0. [DOI] [PubMed] [Google Scholar]
  38. Tatchell K., Robinson L. C., Breitenbach M. RAS2 of Saccharomyces cerevisiae is required for gluconeogenic growth and proper response to nutrient limitation. Proc Natl Acad Sci U S A. 1985 Jun;82(11):3785–3789. doi: 10.1073/pnas.82.11.3785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Temeles G. L., Gibbs J. B., D'Alonzo J. S., Sigal I. S., Scolnick E. M. Yeast and mammalian ras proteins have conserved biochemical properties. Nature. 1985 Feb 21;313(6004):700–703. doi: 10.1038/313700a0. [DOI] [PubMed] [Google Scholar]
  40. Uno I., Mitsuzawa H., Matsumoto K., Tanaka K., Oshima T., Ishikawa T. Reconstitution of the GTP-dependent adenylate cyclase from products of the yeast CYR1 and RAS2 genes in Escherichia coli. Proc Natl Acad Sci U S A. 1985 Dec;82(23):7855–7859. doi: 10.1073/pnas.82.23.7855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Varmus H. E. The molecular genetics of cellular oncogenes. Annu Rev Genet. 1984;18:553–612. doi: 10.1146/annurev.ge.18.120184.003005. [DOI] [PubMed] [Google Scholar]
  42. Willumsen B. M., Norris K., Papageorge A. G., Hubbert N. L., Lowy D. R. Harvey murine sarcoma virus p21 ras protein: biological and biochemical significance of the cysteine nearest the carboxy terminus. EMBO J. 1984 Nov;3(11):2581–2585. doi: 10.1002/j.1460-2075.1984.tb02177.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Wolfe P. B., Wickner W., Goodman J. M. Sequence of the leader peptidase gene of Escherichia coli and the orientation of leader peptidase in the bacterial envelope. J Biol Chem. 1983 Oct 10;258(19):12073–12080. [PubMed] [Google Scholar]
  44. Yokota T., Sugisaki H., Takanami M., Kaziro Y. The nucleotide sequence of the cloned tufA gene of Escherichia coli. Gene. 1980 Dec;12(1-2):25–31. doi: 10.1016/0378-1119(80)90012-8. [DOI] [PubMed] [Google Scholar]
  45. Yuasa Y., Srivastava S. K., Dunn C. Y., Rhim J. S., Reddy E. P., Aaronson S. A. Acquisition of transforming properties by alternative point mutations within c-bas/has human proto-oncogene. Nature. 1983 Jun 30;303(5920):775–779. doi: 10.1038/303775a0. [DOI] [PubMed] [Google Scholar]
  46. Zengel J. M., Archer R. H., Lindahl L. The nucleotide sequence of the Escherichia coli fus gene, coding for elongation factor G. Nucleic Acids Res. 1984 Feb 24;12(4):2181–2192. doi: 10.1093/nar/12.4.2181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. la Cour T. F., Nyborg J., Thirup S., Clark B. F. Structural details of the binding of guanosine diphosphate to elongation factor Tu from E. coli as studied by X-ray crystallography. EMBO J. 1985 Sep;4(9):2385–2388. doi: 10.1002/j.1460-2075.1985.tb03943.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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