Isolation and partial characterization of membrane vesicles carrying markers of the membrane adhesion sites
10.1128/jb.149.2.758-767.1982
Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

At areas of adhesion between outer membrane (OM) and inner membrane (IM) in gram-negative bacteria, newly synthesized membrane constituents are inserted, and bacteriophage infection occurs. We describe here the isolation of these sites from cell membrane fractions of Salmonella anatum. Sucrose density gradients yielded membrane vesicles of the OM and IM; their mutual cross-contamination was low, as measured by 2-keto-3-deoxyoctonate and beta-NADH-oxidase activities. To mark the areas of lipopolysaccharide synthesis in the envelope (the adhesion sites), we infected S. anatum with phage epsilon 15, which causes a rapid change (conversion) in the cell's O-antigenic composition from serogroup E1 to E2; lipopolysaccharide of type E2 also serves as receptor for phage epsilon 34. We found that the fractions of intermediate density (Int. M) from briefly converted cells bound both phage epsilon 34 and E2-specific antibody. In the electron microscope, epsilon 34 was seen to have absorbed with a high degree of significance to the Int. M fraction of briefly converted cells, but not to the Int. M fraction of unconverted cells. Furthermore, the Int. M fractions of briefly converted cells coagglutinated anti-E2-coated Staphylococcus aureus, whereas the OM and IM fractions showed comparatively little agglutination. In addition, Int. M material exhibited elevated phospholipase A1 and A2 activities comparable to those of the OM fraction; the IM was essentially phospholipase free. Our data indicate that this membrane fractionation allows one to isolate from Int. M regions a variety of activities associated with adhesion sites.

Bibliography

Bayer, M. H., Costello, G. P., & Bayer, M. E. (1982). Isolation and partial characterization of membrane vesicles carrying markers of the membrane adhesion sites. Journal of Bacteriology, 149(2), 758–767.

Authors 3
  1. M H Bayer (first)
  2. G P Costello (additional)
  3. M E Bayer (additional)
References 42 Referenced 69
  1. Adams M. H. 1959. Bacteriophages. Interscience Publishers Inc. New York.
  2. Ames , G. F. 1974 . Resolution of bacterial proteins by polyacrylamide gel electrophoresis on slabs . J. Biol. Chem. 249 : 634 - 644 . (10.1016/S0021-9258(19)43074-3) / J. Biol. Chem. / Resolution of bacterial proteins by polyacrylamide gel electrophoresis on slabs by Ames G. F. (1974)
  3. Bayer , M. E. 1968 . Areas of adhesion between wall and membane of Escherichia coli . J. Gen. Microbiol. 53 : 395 - 404 . (10.1099/00221287-53-3-395) / J. Gen. Microbiol. / Areas of adhesion between wall and membane of Escherichia coli by Bayer M. E. (1968)
  4. Bayer , M. E. 1968 . Adsorption of bacteriophages to adhesions between wall and membrane of Escherichia coli . J. Virol. 2 : 346 - 356 . (10.1128/jvi.2.4.346-356.1968) / J. Virol. / Adsorption of bacteriophages to adhesions between wall and membrane of Escherichia coli by Bayer M. E. (1968)
  5. Bayer , M. E. 1974 . Ultrastructure and organization of the bacterial envelope . Ann. N. Y. Acad. Sci. 235 : 6 - 28 . (10.1111/j.1749-6632.1974.tb43254.x) / Ann. N. Y. Acad. Sci. / Ultrastructure and organization of the bacterial envelope by Bayer M. E. (1974)
  6. Bayer M. E. 1975. Role of adhesion zones in bacterial cell-surface function and biogenesis p. 393-427. In A. Tzagoloff (ed.) Membrane biogenesis. Plenum Publishing Corp. New York. (10.1007/978-1-4684-2136-1_11)
  7. Bayer M. E. 1979. The fusion sites between the outer membrane and cytoplasmic membrane of bacteria; their role in membrane assembly and virus infection p. 167-202. In M. Inouye (ed.) Bacterial outer membranes: biogenesis and functions. John Wiley & Sons Inc. New York.
  8. Bayer , M. E. , and T. W. Starkey . 1972 . The adsorption of bacteriophage 4X174 and its interaction with Escherichia coli: a kinetic and morphological study . Virology 49 : 236 - 256 . (10.1016/S0042-6822(72)80026-6) / Virology / The adsorption of bacteriophage 4X174 and its interaction with Escherichia coli: a kinetic and morphological study by Bayer M. E. (1972)
  9. Bayer , M. E. , K. Takeda , and H. Uetake . 1980 . Effects of receptor destruction by Salmonella bacteriophages r15 and c341 . Virology 105 : 328 - 337 . (10.1016/0042-6822(80)90034-3) / Virology / Effects of receptor destruction by Salmonella bacteriophages r15 and c341 by Bayer M. E. (1980)
  10. Bayer , M. E. , and H. Thurow . 1977 . Polysaccharide capsule of Escherichia coli: microscope study of its size, structure, and sites of synthesis . J. Bacteriol. 130 : 911 - 936 . (10.1128/JB.130.2.911-936.1977) / J. Bacteriol. / Polysaccharide capsule of Escherichia coli: microscope study of its size, structure, and sites of synthesis by Bayer M. E. (1977)
  11. Bell , R. M. , R. D. Mavis , M. J. Osborn , and P. R. Vagelos . 1971 . Enzymes of phospholipid metabolism: localization in the cytoplasmic and outer membrane of the cell envelope of Escherichia coli and Salmonella typhimurium . Biochim. Biophys. Acta 249 : 628 - 635 . (10.1016/0005-2736(71)90144-1) / Biochim. Biophys. Acta / Enzymes of phospholipid metabolism: localization in the cytoplasmic and outer membrane of the cell envelope of Escherichia coli and Salmonella typhimurium by Bell R. M. (1971)
  12. Ballum , F. J. 1965 . Degradation of the homopolymer complexes polydeoxyadenylate-polydeoxythymidylate, polydeoxyinosinate-polydeoxycytidylate, and polydeoxyguanylate-polydeoxycytidylate by deoxyribonuclease I . J. Biol. Chem. 240 : 2599 - 2601 . (10.1016/S0021-9258(18)97367-9) / J. Biol. Chem. / Degradation of the homopolymer complexes polydeoxyadenylate-polydeoxythymidylate, polydeoxyinosinate-polydeoxycytidylate, and polydeoxyguanylate-polydeoxycytidylate by deoxyribonuclease I by Ballum F. J. (1965)
  13. Cohen , L. K. , D. R. Lueking , and S. Kaplan . 1979 . Intermembrane phospholipid transfer mediated by cellfree extracts of Rhodopseudomonas sphaeroides . J. Biol. Chem. 254 : 721 - 728 . (10.1016/S0021-9258(17)37865-1) / J. Biol. Chem. / Intermembrane phospholipid transfer mediated by cellfree extracts of Rhodopseudomonas sphaeroides by Cohen L. K. (1979)
  14. Cronan J. E. 1979. Phospholipid synthesis and assembly p. 35-66. In M. Inouye (ed.) Bacterial outer membranes: biogenesis and functions. John Wiley & Sons Inc. New York.
  15. Crowlesmith , I. , M. Schindler , and M. J. Osborn . 1978 . Bacteriophage P22 is not a likely probe for zones of adhesion between the inner and outer membranes of Salmonella typhimurium . J. Bacteriol. 135 : 259 - 269 . (10.1128/JB.135.1.259-269.1978) / J. Bacteriol. / Bacteriophage P22 is not a likely probe for zones of adhesion between the inner and outer membranes of Salmonella typhimurium by Crowlesmith I. (1978)
  16. De Le U , L. , J. Kingma , and B. Withold . 1979 . Nature of the regions involved in the insertion of newly synthesized protein into the outer membrane of E. coli . Biochim. Biophys. Acta 553 : 224 - 234 . (10.1016/0005-2736(79)90227-X) / Biochim. Biophys. Acta / Nature of the regions involved in the insertion of newly synthesized protein into the outer membrane of E. coli by De Le U (1979)
  17. Doi , O. , and S. Nojima . 1973 . Detergent resistant phospholipase Al and A2 in Escherichia coli . J. Biochem. 74 : 667 - 674 . (10.1093/oxfordjournals.jbchem.a130291) / J. Biochem. / Detergent resistant phospholipase Al and A2 in Escherichia coli by Doi O. (1973)
  18. Folch , J. , M. Lees , and G. H. Sloane Stanley . 1957 . A simple method for the isolation and purification of total lipides from animal tissues . J. Biol. Chem. 226 : 497 - 509 . (10.1016/S0021-9258(18)64849-5) / J. Biol. Chem. / A simple method for the isolation and purification of total lipides from animal tissues by Folch J. (1957)
  19. Heller , K. B. 1979 . Lipolytic activity copurified with the outer membrane of Serratia marcescens . J. Bacteriol. 140 : 1120 - 1122 . (10.1128/JB.140.3.1120-1122.1979) / J. Bacteriol. / Lipolytic activity copurified with the outer membrane of Serratia marcescens by Heller K. B. (1979)
  20. Jones , N. C. , and M. J. Osborn . 1977 . Translocation of phospholipids between the outer and inner membranes of Salmonella typhimurium . J. Biol. Chem. 252 : 7405 - 7412 . (10.1016/S0021-9258(19)66979-6) / J. Biol. Chem. / Translocation of phospholipids between the outer and inner membranes of Salmonella typhimurium by Jones N. C. (1977)
  21. Kellenberger , E. , and A. Ryter . 1958 . Cell wall and cytoplasmic membrane of Escherichia coli . J. Biophys. Biochem. Cytol. 4 : 323 - 326 . (10.1083/jcb.4.3.323) / J. Biophys. Biochem. Cytol. / Cell wall and cytoplasmic membrane of Escherichia coli by Kellenberger E. (1958)
  22. Lowry , 0. H. , N. J. Rosebrough , A. L. Farr , and R. J. Randall . 1951 . Protein measurement with the Folin phenol reagent . J. Biol. Chem. 193 : 265 - 275 . (10.1016/S0021-9258(19)52451-6) / J. Biol. Chem. / Protein measurement with the Folin phenol reagent by Lowry 0. (1951)
  23. Lugtenberg , B. , J. MeUers , R. Peters , P. van den Hoek , and L. van Alphen . 1975 . Electrophoretic resolution of the "major outer membrane protein " of Escherichia coli K12 into four bands. FEBS Lett. 58 : 254 - 258 . (10.1016/0014-5793(75)80272-9) / FEBS Lett. / Electrophoretic resolution of the "major outer membrane protein by Lugtenberg B. (1975)
  24. Lugtenberg , E. J. J. , and R. Peters . 1976 . Distribution of lipids in cytoplasmic and outer membranes of Escherichia coli . Biochim. Biophys. Acta 441 : 38 - 47 . (10.1016/0005-2760(76)90279-4) / Biochim. Biophys. Acta / Distribution of lipids in cytoplasmic and outer membranes of Escherichia coli by Lugtenberg E. J. J. (1976)
  25. Miura , T. , and S. Mizushima . 1969 . Separation and properties of outer and cytoplasmic membranes in Escherichia coli . Biochim. Biophys. Acta 193 : 268 - 276 . (10.1016/0005-2736(69)90188-6) / Biochim. Biophys. Acta / Separation and properties of outer and cytoplasmic membranes in Escherichia coli by Miura T. (1969)
  26. Muhlradt , P. F. , J. Menzel , J. R. Golecki , and V. Speth . 1973 . Outer membrane of Salmonella. Sites of export of newly synthesized lipopolysaccharide on the bacterial surface . Eur. J. Biochem. 35 : 471 - 481 . (10.1111/j.1432-1033.1973.tb02861.x) / Eur. J. Biochem. / Outer membrane of Salmonella. Sites of export of newly synthesized lipopolysaccharide on the bacterial surface by Muhlradt P. F. (1973)
  27. Muhlradt , P. F. , J. Menzel , J. R. Golecki , and V. Speth . 1974 . Lateral mobility and surface density of lipopolysaccharide in the outer membrane of Salmonella typhimurium . Eur. J. Biochem. 43 : 533 - 539 . (10.1111/j.1432-1033.1974.tb03440.x) / Eur. J. Biochem. / Lateral mobility and surface density of lipopolysaccharide in the outer membrane of Salmonella typhimurium by Muhlradt P. F. (1974)
  28. Murray , R. G. E. , P. Steed , and H. E. Elson . 1965 . The location of the mucopeptide in sections of the cell wall of Escherichia coli and other gram-negative bacteria . Can J. Microbiol. 11 : 547 - 560 . (10.1139/m65-072) / Can J. Microbiol. / The location of the mucopeptide in sections of the cell wall of Escherichia coli and other gram-negative bacteria by Murray R. G. E. (1965)
  29. Nishijima , M. , S. Nakaido , Y. Tamori , and S. Nojima . 1977 . Detergent-resistant phospholipase A of Escherichia coli K-12 . Eur. J. Biochem. 73 : 115 - 124 . (10.1111/j.1432-1033.1977.tb11297.x) / Eur. J. Biochem. / Detergent-resistant phospholipase A of Escherichia coli K-12 by Nishijima M. (1977)
  30. Osborn M. J. 1979. Biosynthesis and assembly of the lipopolysaccharide of the outer membrane p. 15-34. In M. Inouye (ed.) Bacterial outer membranes: biogenesis and functions. John Wiley & Sons Inc. New York.
  31. Osborn , M. J. , J. E. Gander , E. Parisi , and J. Carson . 1972 . Mechanism of assembly of the outer membrane of Salmonella typhimurium . J. Biol. Chem. 247 : 3962 - 3972 . (10.1016/S0021-9258(19)45127-2) / J. Biol. Chem. / Mechanism of assembly of the outer membrane of Salmonella typhimurium by Osborn M. J. (1972)
  32. Robbins , P. W. , and T. Uchida . 1962 . Studies on the chemical basis of the phage conversion of 0-antigens in the E-group Salmonella . Biochemistry 1 : 323 - 335 . (10.1021/bi00908a020) / Biochemistry / Studies on the chemical basis of the phage conversion of 0-antigens in the E-group Salmonella by Robbins P. W. (1962)
  33. Rouser G. G. Kritchevsky and A. Yamamoto. 1976. Column chromatographic and associated procedures for separation and determination of phosphatides and glycolipids p. 713-776. In G. V. Marinetti (ed.) Lipid chromatographic analysis. Marcel Dekker Inc. New York.
  34. Scandella , C. J. , and A. Kornberg . 1971 . A membranebound phospholipase Al purified from Escherichia coli . Biochemistry 10 : 4447 - 4456 . (10.1021/bi00800a015) / Biochemistry / A membranebound phospholipase Al purified from Escherichia coli by Scandella C. J. (1971)
  35. Schnaitman , C. A. 1970 . Protein composition of the cell wall and cytoplasmic membrane of Escherichia coli . J. Bacteriol. 104 : 890 - 901 . (10.1128/jb.104.2.890-901.1970) / J. Bacteriol. / Protein composition of the cell wall and cytoplasmic membrane of Escherichia coli by Schnaitman C. A. (1970)
  36. Scott , C. C. L. , R. A. Makula , and W. R. Finnerty . 1976 . Isolation and characterization of membranes from a hydrocarbon-oxidizing Acinetobacter sp . J. Bacteriol. 127 : 469 - 480 . (10.1128/jb.127.1.469-480.1976) / J. Bacteriol. / Isolation and characterization of membranes from a hydrocarbon-oxidizing Acinetobacter sp by Scott C. C. L. (1976)
  37. Smit , J. , Y. Kamio , and H. Nikaido . 1975 . Outer membrane of Salmonella typhimurium: chemical analysis and freeze-fracture studied with lipopolysaccharide mutants . J. Bacteriol. 124 : 942 - 958 . (10.1128/JB.124.2.942-958.1975) / J. Bacteriol. / Outer membrane of Salmonella typhimurium: chemical analysis and freeze-fracture studied with lipopolysaccharide mutants by Smit J. (1975)
  38. Svenungsson , B. , and A. A. Lindberg . 1978 . Identification of Salmonella bacteria by co-agglutination, using antibodies against synthetic disaccharide-protein antigens 02, 04 and 09, adsorbed to protein A-containing Staphylococci . Acta Pathol. Microbiol. Scand. Sect. B. 86 : 283 - 290 . / Acta Pathol. Microbiol. Scand. Sect. B. / Identification of Salmonella bacteria by co-agglutination, using antibodies against synthetic disaccharide-protein antigens 02, 04 and 09, adsorbed to protein A-containing Staphylococci by Svenungsson B. (1978)
  39. Thiel , T. , and L. Astrachan . 1978 . Absence of phospholipase activity in bacteriophage T4 . J. Virol. 27 : 835 - 837 . (10.1128/JVI.27.3.835-837.1978) / J. Virol. / Absence of phospholipase activity in bacteriophage T4 by Thiel T. (1978)
  40. Tomita , T. , S. Iwashita , and S. Kanegasaki . 1976 . Role of cell surface mobility on bacteriophage infections: translocation of Salmonella phages to membrane adhesions . Biochem. Biophys. Res. Commun. 73 : 807 - 813 . (10.1016/0006-291X(76)90881-0) / Biochem. Biophys. Res. Commun. / Role of cell surface mobility on bacteriophage infections: translocation of Salmonella phages to membrane adhesions by Tomita T. (1976)
  41. Uetake , H. , S. E. Luria , and J. W. Burrows . 1958 . Conversion of somatic antigens in Salmonella by phage infection leading to Iysis or Iysogeny . Virology 5 : 68 - 91 . (10.1016/0042-6822(58)90006-0) / Virology / Conversion of somatic antigens in Salmonella by phage infection leading to Iysis or Iysogeny by Uetake H. (1958)
  42. Zwaal R. F. A. and B. Roelofsen. 1976. Applications of pure phospholipases in membrane studies p. 352-377. In A. H. Maddy (ed.) Biochemical analysis of membranes. John Wiley & Sons Inc. New York.
Dates
Type When
Created 5 years, 7 months ago (Jan. 3, 2020, 12:29 p.m.)
Deposited 4 years ago (July 29, 2021, 1:26 p.m.)
Indexed 1 year, 3 months ago (May 16, 2024, 12:22 p.m.)
Issued 43 years, 6 months ago (Feb. 1, 1982)
Published 43 years, 6 months ago (Feb. 1, 1982)
Published Print 43 years, 6 months ago (Feb. 1, 1982)
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@article{Bayer_1982, title={Isolation and partial characterization of membrane vesicles carrying markers of the membrane adhesion sites}, volume={149}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.149.2.758-767.1982}, DOI={10.1128/jb.149.2.758-767.1982}, number={2}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Bayer, M H and Costello, G P and Bayer, M E}, year={1982}, month=feb, pages={758–767} }