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. 1995 Mar;177(5):1247–1253. doi: 10.1128/jb.177.5.1247-1253.1995

bor gene of phage lambda, involved in serum resistance, encodes a widely conserved outer membrane lipoprotein.

J J Barondess 1, J Beckwith 1
PMCID: PMC176730  PMID: 7868598

Abstract

bor is one of two recently identified genes of phage lambda which are expressed during lysogeny and whose products display homology to bacterial virulence proteins. bor is closely related to the iss locus of plasmid CoIV,I-K94, which promotes bacterial resistance to serum complement killing in vitro and virulence in animals. bor has a similar in vitro effect. We show here that the bor gene product is a lipoprotein located in the Escherichia coli outer membrane. We also find that antigenically related proteins are expressed by lysogens of a number of other lambdoid coliphage, in cells carrying the cloned iss gene, and in several clinical isolates of E. coli. These results demonstrate that bor sequences are widespread and present a starting point for mechanistic analysis of bor-mediated serum resistance.

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Selected References

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  1. Anilionis A., Riley M. Conservation and variation of nucleotide sequences within related bacterial genomes: Escherichia coli strains. J Bacteriol. 1980 Jul;143(1):355–365. doi: 10.1128/jb.143.1.355-365.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barondess J. J., Beckwith J. A bacterial virulence determinant encoded by lysogenic coliphage lambda. Nature. 1990 Aug 30;346(6287):871–874. doi: 10.1038/346871a0. [DOI] [PubMed] [Google Scholar]
  3. Binns M. M., Davies D. L., Hardy K. G. Cloned fragments of the plasmid ColV,I-K94 specifying virulence and serum resistance. Nature. 1979 Jun 28;279(5716):778–781. doi: 10.1038/279778a0. [DOI] [PubMed] [Google Scholar]
  4. Binns M. M., Mayden J., Levine R. P. Further characterization of complement resistance conferred on Escherichia coli by the plasmid genes traT of R100 and iss of ColV,I-K94. Infect Immun. 1982 Feb;35(2):654–659. doi: 10.1128/iai.35.2.654-659.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bliska J. B., Falkow S. Bacterial resistance to complement killing mediated by the Ail protein of Yersinia enterocolitica. Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3561–3565. doi: 10.1073/pnas.89.8.3561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Boyd A., Holland I. B. Regulation of the synthesis of surface protein in the cell cycle of E. coli B/r. Cell. 1979 Oct;18(2):287–296. doi: 10.1016/0092-8674(79)90048-5. [DOI] [PubMed] [Google Scholar]
  7. Brubaker R. R. Mechanisms of bacterial virulence. Annu Rev Microbiol. 1985;39:21–50. doi: 10.1146/annurev.mi.39.100185.000321. [DOI] [PubMed] [Google Scholar]
  8. Carbonetti N., Simnad V., Elkins C., Sparling P. F. Construction of isogenic gonococci with variable porin structure: effects on susceptibility to human serum and antibiotics. Mol Microbiol. 1990 Jun;4(6):1009–1018. doi: 10.1111/j.1365-2958.1990.tb00673.x. [DOI] [PubMed] [Google Scholar]
  9. Choi D. S., Yamada H., Mizuno T., Mizushima S. Trimeric structure and localization of the major lipoprotein in the cell surface of Escherichia coli. J Biol Chem. 1986 Jul 5;261(19):8953–8957. [PubMed] [Google Scholar]
  10. Chuba P. J., Leon M. A., Banerjee A., Palchaudhuri S. Cloning and DNA sequence of plasmid determinant iss, coding for increased serum survival and surface exclusion, which has homology with lambda DNA. Mol Gen Genet. 1989 Apr;216(2-3):287–292. doi: 10.1007/BF00334367. [DOI] [PubMed] [Google Scholar]
  11. Davies D. L., Falkiner F. R., Hardy K. G. Colicin V production by clinical isolates of Escherichia coli. Infect Immun. 1981 Feb;31(2):574–579. doi: 10.1128/iai.31.2.574-579.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fernandez-Beros M. E., Kissel V., Lior H., Cabello F. C. Virulence-related genes in ColV plasmids of Escherichia coli isolated from human blood and intestines. J Clin Microbiol. 1990 Apr;28(4):742–746. doi: 10.1128/jcm.28.4.742-746.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Filip C., Fletcher G., Wulff J. L., Earhart C. F. Solubilization of the cytoplasmic membrane of Escherichia coli by the ionic detergent sodium-lauryl sarcosinate. J Bacteriol. 1973 Sep;115(3):717–722. doi: 10.1128/jb.115.3.717-722.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hayashi S., Wu H. C. Lipoproteins in bacteria. J Bioenerg Biomembr. 1990 Jun;22(3):451–471. doi: 10.1007/BF00763177. [DOI] [PubMed] [Google Scholar]
  15. Heffernan E. J., Harwood J., Fierer J., Guiney D. The Salmonella typhimurium virulence plasmid complement resistance gene rck is homologous to a family of virulence-related outer membrane protein genes, including pagC and ail. J Bacteriol. 1992 Jan;174(1):84–91. doi: 10.1128/jb.174.1.84-91.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Heffernan E. J., Reed S., Hackett J., Fierer J., Roudier C., Guiney D. Mechanism of resistance to complement-mediated killing of bacteria encoded by the Salmonella typhimurium virulence plasmid gene rck. J Clin Invest. 1992 Sep;90(3):953–964. doi: 10.1172/JCI115972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Highton P. J., Chang Y., Myers R. J. Evidence for the exchange of segments between genomes during the evolution of lambdoid bacteriophages. Mol Microbiol. 1990 Aug;4(8):1329–1340. doi: 10.1111/j.1365-2958.1990.tb00712.x. [DOI] [PubMed] [Google Scholar]
  18. Hong K., Kinoshita T., Takeda J., Kozono H., Pramoonjago P., Kim Y. U., Inoue K. Inhibition of the alternative C3 convertase and classical C5 convertase of complement by group A streptococcal M protein. Infect Immun. 1990 Aug;58(8):2535–2541. doi: 10.1128/iai.58.8.2535-2541.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Horák V., Lanc A. Colicins of Escherichia coli strains causing urinary tract infections, sensitivity of these strains towards colicins, and their O-serotypes. Folia Microbiol (Praha) 1973;18(4):332–340. doi: 10.1007/BF02868052. [DOI] [PubMed] [Google Scholar]
  20. Isaacs S. N., Kotwal G. J., Moss B. Vaccinia virus complement-control protein prevents antibody-dependent complement-enhanced neutralization of infectivity and contributes to virulence. Proc Natl Acad Sci U S A. 1992 Jan 15;89(2):628–632. doi: 10.1073/pnas.89.2.628. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Joiner K. A. Complement evasion by bacteria and parasites. Annu Rev Microbiol. 1988;42:201–230. doi: 10.1146/annurev.mi.42.100188.001221. [DOI] [PubMed] [Google Scholar]
  22. Kaiser K., Murray N. E. Physical characterisation of the "Rac prophage" in E. coli K12. Mol Gen Genet. 1979 Sep;175(2):159–174. doi: 10.1007/BF00425532. [DOI] [PubMed] [Google Scholar]
  23. Lazzaroni J. C., Portalier R. The excC gene of Escherichia coli K-12 required for cell envelope integrity encodes the peptidoglycan-associated lipoprotein (PAL). Mol Microbiol. 1992 Mar;6(6):735–742. doi: 10.1111/j.1365-2958.1992.tb01523.x. [DOI] [PubMed] [Google Scholar]
  24. Lutkenhaus J. F., Wolf-Watz H., Donachie W. D. Organization of genes in the ftsA-envA region of the Escherichia coli genetic map and identification of a new fts locus (ftsZ). J Bacteriol. 1980 May;142(2):615–620. doi: 10.1128/jb.142.2.615-620.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Miller V. L., Bliska J. B., Falkow S. Nucleotide sequence of the Yersinia enterocolitica ail gene and characterization of the Ail protein product. J Bacteriol. 1990 Feb;172(2):1062–1069. doi: 10.1128/jb.172.2.1062-1069.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Miller V. L., Farmer J. J., 3rd, Hill W. E., Falkow S. The ail locus is found uniquely in Yersinia enterocolitica serotypes commonly associated with disease. Infect Immun. 1989 Jan;57(1):121–131. doi: 10.1128/iai.57.1.121-131.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Minshew B. H., Jorgensen J., Swanstrum M., Grootes-Reuvecamp G. A., Falkow S. Some characteristics of Escherichia coli strains isolated from extraintestinal infections of humans. J Infect Dis. 1978 May;137(5):648–654. doi: 10.1093/infdis/137.5.648. [DOI] [PubMed] [Google Scholar]
  28. Moll A., Manning P. A., Timmis K. N. Plasmid-determined resistance to serum bactericidal activity: a major outer membrane protein, the traT gene product, is responsible for plasmid-specified serum resistance in Escherichia coli. Infect Immun. 1980 May;28(2):359–367. doi: 10.1128/iai.28.2.359-367.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Nnalue N. A., Newton S., Stocker B. A. Lysogenization of Salmonella choleraesuis by phage 14 increases average length of O-antigen chains, serum resistance and intraperitoneal mouse virulence. Microb Pathog. 1990 Jun;8(6):393–402. doi: 10.1016/0882-4010(90)90026-m. [DOI] [PubMed] [Google Scholar]
  30. Ogata R. T., Levine R. P. Characterization of complement resistance in Escherichia coli conferred by the antibiotic resistance plasmid R100. J Immunol. 1980 Oct;125(4):1494–1498. [PubMed] [Google Scholar]
  31. Ogata R. T., Winters C., Levine R. P. Nucleotide sequence analysis of the complement resistance gene from plasmid R100. J Bacteriol. 1982 Aug;151(2):819–827. doi: 10.1128/jb.151.2.819-827.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Ogierman M. A., Manning P. A. TCP pilus biosynthesis in Vibrio cholerae O1: gene sequence of tcpC encoding an outer membrane lipoprotein. FEMS Microbiol Lett. 1992 Oct 1;76(1-2):179–184. doi: 10.1016/0378-1097(92)90383-y. [DOI] [PubMed] [Google Scholar]
  33. Parsot C., Taxman E., Mekalanos J. J. ToxR regulates the production of lipoproteins and the expression of serum resistance in Vibrio cholerae. Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1641–1645. doi: 10.1073/pnas.88.5.1641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Perumal N. B., Minkley E. G., Jr The product of the F sex factor traT surface exclusion gene is a lipoprotein. J Biol Chem. 1984 May 10;259(9):5357–5360. [PubMed] [Google Scholar]
  35. Pierson D. E., Falkow S. The ail gene of Yersinia enterocolitica has a role in the ability of the organism to survive serum killing. Infect Immun. 1993 May;61(5):1846–1852. doi: 10.1128/iai.61.5.1846-1852.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Pulkkinen W. S., Miller S. I. A Salmonella typhimurium virulence protein is similar to a Yersinia enterocolitica invasion protein and a bacteriophage lambda outer membrane protein. J Bacteriol. 1991 Jan;173(1):86–93. doi: 10.1128/jb.173.1.86-93.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Redfield R. J., Campbell A. M. Structure of cryptic lambda prophages. J Mol Biol. 1987 Dec 5;198(3):393–404. doi: 10.1016/0022-2836(87)90289-0. [DOI] [PubMed] [Google Scholar]
  38. Rhen M., Sukupolvi S. The role of the traT gene of the Salmonella typhimurium virulence plasmid for serum resistance and growth within liver macrophages. Microb Pathog. 1988 Oct;5(4):275–285. doi: 10.1016/0882-4010(88)90100-3. [DOI] [PubMed] [Google Scholar]
  39. Riley M., Anilionis A. Conservation and variation of nucleotide sequences within related bacterial genomes: enterobacteria. J Bacteriol. 1980 Jul;143(1):366–376. doi: 10.1128/jb.143.1.366-376.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sanger F., Coulson A. R., Hong G. F., Hill D. F., Petersen G. B. Nucleotide sequence of bacteriophage lambda DNA. J Mol Biol. 1982 Dec 25;162(4):729–773. doi: 10.1016/0022-2836(82)90546-0. [DOI] [PubMed] [Google Scholar]
  41. Smith H. W., Huggins M. B. Further observations on the association of the colicine V plasmid of Escherichia coli with pathogenicity and with survival in the alimentary tract. J Gen Microbiol. 1976 Feb;92(2):335–350. doi: 10.1099/00221287-92-2-335. [DOI] [PubMed] [Google Scholar]
  42. Stoorvogel J., van Bussel M. J., Tommassen J., van de Klundert J. A. Molecular characterization of an Enterobacter cloacae outer membrane protein (OmpX). J Bacteriol. 1991 Jan;173(1):156–160. doi: 10.1128/jb.173.1.156-160.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Stoorvogel J., van Bussel M. J., van de Klundert J. A. Biological characterization of an Enterobacter cloacae outer membrane protein (OmpX). J Bacteriol. 1991 Jan;173(1):161–167. doi: 10.1128/jb.173.1.161-167.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Strathern A., Herskowitz I. Defective prophage in Escherichia coli K12 strains. Virology. 1975 Sep;67(1):136–143. doi: 10.1016/0042-6822(75)90411-0. [DOI] [PubMed] [Google Scholar]
  45. Strauch K. L., Beckwith J. An Escherichia coli mutation preventing degradation of abnormal periplasmic proteins. Proc Natl Acad Sci U S A. 1988 Mar;85(5):1576–1580. doi: 10.1073/pnas.85.5.1576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Sukupolvi S., Riikonen P., Taira S., Saarilahti H., Rhen M. Plasmid-mediated serum resistance in Salmonella enterica. Microb Pathog. 1992 Mar;12(3):219–225. doi: 10.1016/0882-4010(92)90056-t. [DOI] [PubMed] [Google Scholar]
  47. Taylor P. W. Bactericidal and bacteriolytic activity of serum against gram-negative bacteria. Microbiol Rev. 1983 Mar;47(1):46–83. doi: 10.1128/mr.47.1.46-83.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Timmis K. N., Boulnois G. J., Bitter-Suermann D., Cabello F. C. Surface components of Escherichia coli that mediate resistance to the bactericidal activities of serum and phagocytes. Curr Top Microbiol Immunol. 1985;118:197–218. doi: 10.1007/978-3-642-70586-1_11. [DOI] [PubMed] [Google Scholar]
  49. Weiser J. N., Gotschlich E. C. Outer membrane protein A (OmpA) contributes to serum resistance and pathogenicity of Escherichia coli K-1. Infect Immun. 1991 Jul;59(7):2252–2258. doi: 10.1128/iai.59.7.2252-2258.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Wright S. D., Levine R. P. How complement kills E. coli. I. Location of the lethal lesion. J Immunol. 1981 Sep;127(3):1146–1151. [PubMed] [Google Scholar]
  51. Wright S. D., Levine R. P. How complement kills E. coli. II. The apparent two-hit nature of the lethal event. J Immunol. 1981 Sep;127(3):1152–1156. [PubMed] [Google Scholar]
  52. von Heijne G. The signal peptide. J Membr Biol. 1990 May;115(3):195–201. doi: 10.1007/BF01868635. [DOI] [PubMed] [Google Scholar]

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