Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1977 Nov;132(2):411–418. doi: 10.1128/jb.132.2.411-418.1977

Lysozyme-promoted association of protein I molecules in the outer membrane of Escherichia coli.

I Chopra, G B Howe, P R Ball
PMCID: PMC221879  PMID: 334740

Abstract

Incubation of whole envelopes prepared from sonically oscillated Escherichia coli K-12 cultures with lysozyme in vitro resulted in the appearance of a protein species with an apparent molecular weight double that of outer membrane protein I. Similar dimers were also detected in purified outer membranes and whole envelopes from lysozyme-induced spheroplasts of E. coli K-12. This was confirmed by two-dimensional electrophoresis in which the dimers were resolved in the second dimension to run as single polypeptides of protein I. Formation of dimers was correlated with peptidoglycan degradation, but the ability of protein I molecules to associate may vary between strains of E. coli, since dimers were found only in outer membranes from E. coli W7. We suggest that extensive degradation of peptidoglycan leads to nonspecific formation of protein I aggregates, but that these aggregates do not occur in vivo.

Full text

PDF
411

Images in this article

416Image
on p.416

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Achtman M., Willetts N., Clark A. J. Beginning a genetic analysis of conjugational transfer determined by the F factor in Escherichia coli by isolation and characterization of transfer-deficient mutants. J Bacteriol. 1971 May;106(2):529–538. doi: 10.1128/jb.106.2.529-538.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BLIGH E. G., DYER W. J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959 Aug;37(8):911–917. doi: 10.1139/o59-099. [DOI] [PubMed] [Google Scholar]
  3. Beacham I. R., Haas D., Yagil E. Mutants of Escherichia coli "cryptic" for certain periplasmic enzymes: evidence for an alteration of the outer membrane. J Bacteriol. 1977 Feb;129(2):1034–1044. doi: 10.1128/jb.129.2.1034-1044.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Braun V., Bosch V., Hantke K., Schaller K. Structure and biosynthesis of functionally defined areas of the Escherichia coli outer membrane. Ann N Y Acad Sci. 1974 May 10;235(0):66–82. doi: 10.1111/j.1749-6632.1974.tb43257.x. [DOI] [PubMed] [Google Scholar]
  5. Braun V. Covalent lipoprotein from the outer membrane of Escherichia coli. Biochim Biophys Acta. 1975 Oct 31;415(3):335–377. doi: 10.1016/0304-4157(75)90013-1. [DOI] [PubMed] [Google Scholar]
  6. Braun V., Rotering H., Ohms J. P., Hagenmaier H. Conformational studies on murein-lipoprotein from the outer membrane of Escherichia coli. Eur J Biochem. 1976 Nov 15;70(2):601–610. doi: 10.1111/j.1432-1033.1976.tb11051.x. [DOI] [PubMed] [Google Scholar]
  7. CITTI J. E., SANDINE W. E., ELLIKER P. R. BETA-GALACTOSIDASE OF STREPTOCOCCUS LACTIS. J Bacteriol. 1965 Apr;89:937–942. doi: 10.1128/jb.89.4.937-942.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chopra I., Lacey R. W., Connolly J. Biochemical and genetic basis of tetracycline resistance in Staphylococcus aureus. Antimicrob Agents Chemother. 1974 Oct;6(4):397–404. doi: 10.1128/aac.6.4.397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chopra I. Mechanism of plasmic-mediated resistance to cadmium in Staphylococcus aureus. Antimicrob Agents Chemother. 1975 Jan;7(1):8–14. doi: 10.1128/aac.7.1.8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Costerton J. W., Cheng K. J. The role of the bacterial cell envelope in antibiotic resistance. J Antimicrob Chemother. 1975 Dec;1(4):363–377. doi: 10.1093/jac/1.4.363. [DOI] [PubMed] [Google Scholar]
  11. Costerton J. W., Ingram J. M., Cheng K. J. Structure and function of the cell envelope of gram-negative bacteria. Bacteriol Rev. 1974 Mar;38(1):87–110. doi: 10.1128/br.38.1.87-110.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Garten W., Hindennach I., Henning U. The major proteins of the Escherichia coli outer cell-envelope membrane. Cyanogen bromide fragments of protein I, composition and order. Eur J Biochem. 1975 Dec 1;60(1):303–307. doi: 10.1111/j.1432-1033.1975.tb21004.x. [DOI] [PubMed] [Google Scholar]
  13. Henning U., Haller I. Mutants of Escherichia coli K12 lacking all 'major' proteins of the outer cell envelope membrane. FEBS Lett. 1975 Jul 15;55(1):161–164. doi: 10.1016/0014-5793(75)80983-5. [DOI] [PubMed] [Google Scholar]
  14. Hindennach I., Henning U. The major proteins of the Excherichia coli outer cell envelope membrane. Preparative isolation of all major membrane proteins. Eur J Biochem. 1975 Nov 1;59(1):207–213. doi: 10.1111/j.1432-1033.1975.tb02443.x. [DOI] [PubMed] [Google Scholar]
  15. Holden K. G., Yim N. C., Griggs L. J., Weisbach J. A. Gel electrophoresis of mucous glycoproteins. I. Effect of gel porosity. Biochemistry. 1971 Aug 3;10(16):3105–3109. doi: 10.1021/bi00792a019. [DOI] [PubMed] [Google Scholar]
  16. Inouye M. A three-dimensional molecular assembly model of a lipoprotein from the Escherichia coli outer membrane. Proc Natl Acad Sci U S A. 1974 Jun;71(6):2396–2400. doi: 10.1073/pnas.71.6.2396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Inouye M., Hirashima A., Lee N. Discussion paper: biosynthesis and assembly of a structural lipoprotein in the envelope of Escherichia coli. Ann N Y Acad Sci. 1974 May 10;235(0):83–90. doi: 10.1111/j.1749-6632.1974.tb43258.x. [DOI] [PubMed] [Google Scholar]
  18. Inoyye S., Takeishi K., Lee N., DeMartini M., Hirashima A., Inouye M. Lipoprotein from the outer membrane of Escherichia coli: purification, paracrystallization, and some properties of its free form. J Bacteriol. 1976 Jul;127(1):555–563. doi: 10.1128/jb.127.1.555-563.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. LURIA S. E., ADAMS J. N., TING R. C. Transduction of lactose-utilizing ability among strains of E. coli and S. dysenteriae and the properties of the transducing phage particles. Virology. 1960 Nov;12:348–390. doi: 10.1016/0042-6822(60)90161-6. [DOI] [PubMed] [Google Scholar]
  20. Lugtenberg B., Bronstein H., van Selm N., Peters R. Peptidoglycan-associated outer membrane proteins in gammegatine bacteria. Biochim Biophys Acta. 1977 Mar 17;465(3):571–578. doi: 10.1016/0005-2736(77)90274-7. [DOI] [PubMed] [Google Scholar]
  21. Lugtenberg B., Meijers J., Peters R., van der Hoek P., van Alphen L. Electrophoretic resolution of the "major outer membrane protein" of Escherichia coli K12 into four bands. FEBS Lett. 1975 Oct 15;58(1):254–258. doi: 10.1016/0014-5793(75)80272-9. [DOI] [PubMed] [Google Scholar]
  22. Lugtenberg B., Peters R., Bernheimer H., Berendsen W. Influence of cultural conditions and mutations on the composition of the outer membrane proteins of Escherichia coli. Mol Gen Genet. 1976 Sep 23;147(3):251–262. doi: 10.1007/BF00582876. [DOI] [PubMed] [Google Scholar]
  23. Nakae T. Identification of the outer membrane protein of E. coli that produces transmembrane channels in reconstituted vesicle membranes. Biochem Biophys Res Commun. 1976 Aug 9;71(3):877–884. doi: 10.1016/0006-291x(76)90913-x. [DOI] [PubMed] [Google Scholar]
  24. Nakae T., Nikaido H. Outer membrane as a diffusion barrier in Salmonella typhimurium. Penetration of oligo- and polysaccharides into isolated outer membrane vesicles and cells with degraded peptidoglycan layer. J Biol Chem. 1975 Sep 25;250(18):7359–7365. [PubMed] [Google Scholar]
  25. Nikaido H. Outer membrane of Salmonella typhimurium. Transmembrane diffusion of some hydrophobic substances. Biochim Biophys Acta. 1976 Apr 16;433(1):118–132. doi: 10.1016/0005-2736(76)90182-6. [DOI] [PubMed] [Google Scholar]
  26. Nikaido H., Song S. A., Shaltiel L., Nurminen M. Outer membrane of Salmonella XIV. Reduced transmembrane diffusion rates in porin-deficient mutants. Biochem Biophys Res Commun. 1976 May 23;76(2):324–330. doi: 10.1016/0006-291x(77)90728-8. [DOI] [PubMed] [Google Scholar]
  27. O'Farrell P. H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PMC free article] [PubMed] [Google Scholar]
  28. Osborn M. J., Gander J. E., Parisi E., Carson J. Mechanism of assembly of the outer membrane of Salmonella typhimurium. Isolation and characterization of cytoplasmic and outer membrane. J Biol Chem. 1972 Jun 25;247(12):3962–3972. [PubMed] [Google Scholar]
  29. Palva E. T., Randall L. L. Nearest-neighbor analysis of Escherichia coli outer membrane proteins using cleavable cross-links. J Bacteriol. 1976 Sep;127(3):1558–1560. doi: 10.1128/jb.127.3.1558-1560.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Reithmeier R. A., Bragg P. D. Cross-linking of the proteins in the outer membrane of Escherichia coli. Biochim Biophys Acta. 1977 Apr 18;466(2):245–256. doi: 10.1016/0005-2736(77)90222-x. [DOI] [PubMed] [Google Scholar]
  31. Schmitges C. J., Henning U. The major proteins of the Escherichia coli outer cell-envelope membrane. Heterogeneity of protein I. Eur J Biochem. 1976 Mar 16;63(1):47–52. doi: 10.1111/j.1432-1033.1976.tb10205.x. [DOI] [PubMed] [Google Scholar]
  32. Schweizer M., Schwarz H., Sonntag I., Henning U. Mutational change of membrane architecture. Mutants of Escherichia coli K12 missing major proteins of the outer cell envelope membrane. Biochim Biophys Acta. 1976 Oct 19;448(3):474–491. doi: 10.1016/0005-2736(76)90301-1. [DOI] [PubMed] [Google Scholar]
  33. Weber K., Osborn M. The reliability of molecular weight determinations by dodecyl sulfate-polyacrylamide gel electrophoresis. J Biol Chem. 1969 Aug 25;244(16):4406–4412. [PubMed] [Google Scholar]
  34. Yamato I., Anraku Y., Hirosawa K. Cytoplasmic membrane vesicles of Escherichia coli. A simple method for preparing the cytoplasmic and outer membranes. J Biochem. 1975 Apr;77(4):705–718. doi: 10.1093/oxfordjournals.jbchem.a130774. [DOI] [PubMed] [Google Scholar]
  35. van Alphen L., Lugtenberg B., van Boxtel R., Verhoef K. Architecture of the outer membrane of Escherichia coli K12. I. Action of phospholipases A2 and C on wild type strains and outer membrane mutants. Biochim Biophys Acta. 1977 Apr 18;466(2):257–268. doi: 10.1016/0005-2736(77)90223-1. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES