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. 1991 Feb;173(3):1223–1229. doi: 10.1128/jb.173.3.1223-1229.1991

The ompH gene of Yersinia enterocolitica: cloning, sequencing, expression, and comparison with known enterobacterial ompH sequences.

L Hirvas 1, P Koski 1, M Vaara 1
PMCID: PMC207246  PMID: 1991717

Abstract

We have recently described a previously uncharacterized outer membrane protein of Salmonella typhimurium and Escherichia coli and cloned and sequenced the corresponding gene, the ompH gene, of S. typhimurium (P. Koski, M. Rhen, J. Kantele, and M. Vaara, J. Biol. Chem. 264:18973-18980, 1989). We report here the cloning, sequencing, and expression of the corresponding gene of Yersinia enterocolitica. It is significantly homologous to the ompH genes of E. coli and S. typhimurium (homology percentages, 65 and 64%, respectively), has a promoter region strongly homologous to the E. coli 17-bp class consensus promoter, and encodes a protein consisting of 165 amino acids (22 of which form the signal sequence). The plasmid-borne Y. enterocolitica ompH was found to be expressed both in the E. coli host and in minicells. The isolated outer membrane of Y. enterocolitica was shown to contain OmpH. The homology of the Y. enterocolitica OmpH protein is 66% with E. coli OmpH and 64% with S. typhimurium OmpH. All OmpH proteins have almost identical hydrophobic profiles, charge distributions, and predicted secondary structures. Because yersiniae are considered rather distant relatives of E. coli and S. typhimurium in the Enterobacteriaceae family, these results might indicate that most or all strains of the family Enterobacteriaceae have OmpH proteins remarkably homologous to those now sequenced.

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  1. Aasland R., Coleman J., Holck A. L., Smith C. L., Raetz C. R., Kleppe K. Identity of the 17-kilodalton protein, a DNA-binding protein from Escherichia coli, and the firA gene product. J Bacteriol. 1988 Dec;170(12):5916–5918. doi: 10.1128/jb.170.12.5916-5918.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ahmad S., Weisburg W. G., Jensen R. A. Evolution of aromatic amino acid biosynthesis and application to the fine-tuned phylogenetic positioning of enteric bacteria. J Bacteriol. 1990 Feb;172(2):1051–1061. doi: 10.1128/jb.172.2.1051-1061.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beck E., Bremer E. Nucleotide sequence of the gene ompA coding the outer membrane protein II of Escherichia coli K-12. Nucleic Acids Res. 1980 Jul 11;8(13):3011–3027. doi: 10.1093/nar/8.13.3011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Braun G., Cole S. T. DNA sequence analysis of the Serratia marcescens ompA gene: implications for the organisation of an enterobacterial outer membrane protein. Mol Gen Genet. 1984;195(1-2):321–328. doi: 10.1007/BF00332766. [DOI] [PubMed] [Google Scholar]
  5. Braun G., Cole S. T. Molecular characterization of the gene coding for major outer membrane protein OmpA from Enterobacter aerogenes. Eur J Biochem. 1983 Dec 15;137(3):495–500. doi: 10.1111/j.1432-1033.1983.tb07853.x. [DOI] [PubMed] [Google Scholar]
  6. Braun G., Cole S. T. The nucleotide sequence coding for major outer membrane protein OmpA of Shigella dysenteriae. Nucleic Acids Res. 1982 Apr 10;10(7):2367–2378. doi: 10.1093/nar/10.7.2367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brenner D. J. Characterization and clinical identification of Enterobacteriaceae by DNA hybridization. Prog Clin Pathol. 1978;7:71–117. [PubMed] [Google Scholar]
  8. 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]
  9. Freudl R., Cole S. T. Cloning and molecular characterization of the ompA gene from Salmonella typhimurium. Eur J Biochem. 1983 Aug 15;134(3):497–502. doi: 10.1111/j.1432-1033.1983.tb07594.x. [DOI] [PubMed] [Google Scholar]
  10. Geyer R., Galanos C., Westphal O., Golecki J. R. A lipopolysaccharide-binding cell-surface protein from Salmonella minnesota. Isolation, partial characterization and occurrence in different Enterobacteriaceae. Eur J Biochem. 1979 Jul;98(1):27–38. doi: 10.1111/j.1432-1033.1979.tb13156.x. [DOI] [PubMed] [Google Scholar]
  11. Gotschlich E. C., Seiff M., Blake M. S. The DNA sequence of the structural gene of gonococcal protein III and the flanking region containing a repetitive sequence. Homology of protein III with enterobacterial OmpA proteins. J Exp Med. 1987 Feb 1;165(2):471–482. doi: 10.1084/jem.165.2.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hansen E. J., Hasemann C., Clausell A., Capra J. D., Orth K., Moomaw C. R., Slaughter C. A., Latimer J. L., Miller E. E. Primary structure of the porin protein of Haemophilus influenzae type b determined by nucleotide sequence analysis. Infect Immun. 1989 Apr;57(4):1100–1107. doi: 10.1128/iai.57.4.1100-1107.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hattori M., Sakaki Y. Dideoxy sequencing method using denatured plasmid templates. Anal Biochem. 1986 Feb 1;152(2):232–238. doi: 10.1016/0003-2697(86)90403-3. [DOI] [PubMed] [Google Scholar]
  14. Hirvas L., Coleman J., Koski P., Vaara M. Bacterial 'histone-like protein I' (HLP-I) is an outer membrane constituent? FEBS Lett. 1990 Mar 12;262(1):123–126. doi: 10.1016/0014-5793(90)80169-j. [DOI] [PubMed] [Google Scholar]
  15. Hofstra H., Van Tol J. D., Dankert J. Cross-reactivity of major outer membrane proteins of Enterobacteriaceae, studied by crossed immunoelectrophoresis. J Bacteriol. 1980 Jul;143(1):328–337. doi: 10.1128/jb.143.1.328-337.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Holck A., Kleppe K. Cloning and sequencing of the gene for the DNA-binding 17K protein of Escherichia coli. Gene. 1988 Jul 15;67(1):117–124. doi: 10.1016/0378-1119(88)90014-5. [DOI] [PubMed] [Google Scholar]
  17. Holck A., Lossius I., Aasland R., Kleppe K. Purification and characterization of the 17 K protein, a DNA-binding protein from Escherichia coli. Biochim Biophys Acta. 1987 Jul 24;914(1):49–54. doi: 10.1016/0167-4838(87)90160-9. [DOI] [PubMed] [Google Scholar]
  18. Hori H., Osawa S. Evolution of ribosomal proteins in Enterobacteriaceae. J Bacteriol. 1978 Mar;133(3):1089–1095. doi: 10.1128/jb.133.3.1089-1095.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Huang Y. X., Ching G., Inouye M. Comparison of the lipoprotein gene among the enterobacteriaceae. DNA sequence of Morganella morganii lipoprotein gene and its expression in Escherichia coli. J Biol Chem. 1983 Jul 10;258(13):8139–8145. [PubMed] [Google Scholar]
  20. Klugman K. P., Gotschlich E. C., Blake M. S. Sequence of the structural gene (rmpM) for the class 4 outer membrane protein of Neisseria meningitidis, homology of the protein to gonococcal protein III and Escherichia coli OmpA, and construction of meningococcal strains that lack class 4 protein. Infect Immun. 1989 Jul;57(7):2066–2071. doi: 10.1128/iai.57.7.2066-2071.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Koski P., Hirvas L., Vaara M. Complete sequence of the ompH gene encoding the 16-kDa cationic outer membrane protein of Salmonella typhimurium. Gene. 1990 Mar 30;88(1):117–120. doi: 10.1016/0378-1119(90)90068-3. [DOI] [PubMed] [Google Scholar]
  22. Koski P., Rhen M., Kantele J., Vaara M. Isolation, cloning, and primary structure of a cationic 16-kDa outer membrane protein of Salmonella typhimurium. J Biol Chem. 1989 Nov 15;264(32):18973–18980. [PubMed] [Google Scholar]
  23. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  24. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  25. Liljeström P., Mättänen P. L., Palva E. T. Cloning of the regulatory locus ompB of Salmonella typhimurium LT-2. II. Identification of the envZ gene product, a protein involved in the expression of the porin proteins. Mol Gen Genet. 1982;188(2):190–194. doi: 10.1007/BF00332674. [DOI] [PubMed] [Google Scholar]
  26. Meinkoth J., Wahl G. M. Nick translation. Methods Enzymol. 1987;152:91–94. doi: 10.1016/0076-6879(87)52012-2. [DOI] [PubMed] [Google Scholar]
  27. Miller H. Practical aspects of preparing phage and plasmid DNA: growth, maintenance, and storage of bacteria and bacteriophage. Methods Enzymol. 1987;152:145–170. doi: 10.1016/0076-6879(87)52016-x. [DOI] [PubMed] [Google Scholar]
  28. O'Neill M. C. Escherichia coli promoters. I. Consensus as it relates to spacing class, specificity, repeat substructure, and three-dimensional organization. J Biol Chem. 1989 Apr 5;264(10):5522–5530. [PubMed] [Google Scholar]
  29. Palva A. M. ompA gene in the detection of Escherichia coli and other Enterobacteriaceae by nucleic acid sandwich hybridization. J Clin Microbiol. 1983 Jul;18(1):92–100. doi: 10.1128/jcm.18.1.92-100.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Panyim S., Chalkley R. High resolution acrylamide gel electrophoresis of histones. Arch Biochem Biophys. 1969 Mar;130(1):337–346. doi: 10.1016/0003-9861(69)90042-3. [DOI] [PubMed] [Google Scholar]
  31. Rose G. D. Prediction of chain turns in globular proteins on a hydrophobic basis. Nature. 1978 Apr 13;272(5654):586–590. doi: 10.1038/272586a0. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Van der Ley P., Bekkers A., Van Meersbergen J., Tommassen J. A comparative study on the phoE genes of three enterobacterial species. Implications for structure-function relationships in a pore-forming protein of the outer membrane. Eur J Biochem. 1987 Apr 15;164(2):469–475. doi: 10.1111/j.1432-1033.1987.tb11080.x. [DOI] [PubMed] [Google Scholar]
  34. Venegas A., Gómez I., Zaror I., Yudelevich A. The nucleotide sequence of the Salmonella typhi ompC porin gene. Nucleic Acids Res. 1988 Aug 11;16(15):7721–7721. doi: 10.1093/nar/16.15.7721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Woodruff W. A., Hancock R. E. Pseudomonas aeruginosa outer membrane protein F: structural role and relationship to the Escherichia coli OmpA protein. J Bacteriol. 1989 Jun;171(6):3304–3309. doi: 10.1128/jb.171.6.3304-3309.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Yamagata H., Nakamura K., Inouye M. Comparison of the lipoprotein gene among the Enterobacteriaceae. DNA sequence of Erwinia amylovora lipoprotein gene. J Biol Chem. 1981 Mar 10;256(5):2194–2198. [PubMed] [Google Scholar]
  37. Zaleska M., Lounatmaa K., Nurminen M., Wahlström E., Mäkelä P. H. A novel virulence-associated cell surface structure composed of 47-kd protein subunits in Yersinia enterocolitica. EMBO J. 1985 Apr;4(4):1013–1018. doi: 10.1002/j.1460-2075.1985.tb03732.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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