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The Major Outer Membrane Lipoprotein of Escherichia coli:Secretion, Modification, and Processing

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The Enzymes of Biological Membranes

Abstract

The outer membrane of gram-negative bacteria has proven to be a valuable model system in which to study the many complexities of biomembrane structure, function, and biogenesis which are common not only to prokaryotic but also eukaryotic cells. The advantages in utilizing the Escherichia coli outer membrane to examine the various aspects of membrane biology are (1) the outer membrane consists of relatively few major proteins, many of which have been purified, (2) a finely detailed genetic map for E. coli as well as the structure of the genes coding for many of these proteins have been established, and (3) all of the outer membrane proteins have been shown to be synthesized in the cytoplasmic compartment and subsequently secreted across the cytoplasmic membrane prior to assembly in the outer membrane. Therefore, by utilizing these aspects of the E. coli outer membrane, one can directly address many of the fundamental questions concerning biomembranes including the functions and structure of integral membrane proteins, molecular mechanisms of biosynthesis and assembly of membrane proteins, interactions between membrane proteins themselves and with other membrane components, regulation of membrane biogenesis, and mechanisms of protein translocation across bilayer membranes.

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References

  • Blobel, G., and Dobberstein, B., 1975, Transfer of proteins across membranes, I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma, J. Cell Biol. 67:835–851.

    Article  PubMed  CAS  Google Scholar 

  • Braun, V., and Bosch, V., 1972a, Sequence of the murein lipoprotein and the attachment site of the lipid, Eur. J. Biochem. 28:51–69.

    Article  PubMed  CAS  Google Scholar 

  • Braun, V., and Bosch, V., 1972b, Repetitive sequences in the murein-lipoprotein of the cell wall of Escherichia coli, Proc. Natl. Acad. Sci. USA 69:970–974.

    Article  PubMed  CAS  Google Scholar 

  • Braun, V., and Sieglin, U., 1970, The covalent murein-lipoprotein structure of the Escherichia coli cell wall, Eur. J. Biochem. 13:336–346.

    Article  PubMed  CAS  Google Scholar 

  • Chattopadhyay, P. K., and Wu, H. C., 1977, Biosynthesis of the covalently-linked diglyceride in murein lipoprotein of Escherichia coli, Proc. Natl. Acad. Sci. USA 74:5318–5322.

    Article  PubMed  CAS  Google Scholar 

  • Chattopadhyay, P. K., Lai, J. S., and Wu, H. C., 1979, Incorporation of phosphatidylglycerol into murein lipoprotein in intact cells of Salmonella typhimurium by phospholipid vesicle fusion, J. Bacteriol. 137:309–312.

    PubMed  CAS  Google Scholar 

  • Chou, P. Y., and Fasman, G. D., 1977, ß-Turns in proteins, J. Mol. Biol. 115:135–175.

    Article  PubMed  CAS  Google Scholar 

  • Date, T., Zwizinski, C., Ludmerer, S., and Wickner, W., 1980, Mechanisms of membrane assembly. Effects of energy poisons on the conversion of soluble M13-coliphage procoat to membrane bound coat protein, Proc. Natl. Acad. Sci. USA 77:827–831.

    Article  PubMed  CAS  Google Scholar 

  • DiRenzo, J., and Inouye, M., 1979, Lipid fluidity-dependent biosynthesis and assembly of the outer membrane proteins of E. coli., Cell 17:155–161.

    Article  Google Scholar 

  • Fung, J. C., MacAlister, T. J., Weigand, R. A., and Rothfield, L. I., 1980, Morphogenesis of the bacterial division septum:Identification of potential sites of division in lkyD mutants of Salmonella typhimurium, J. Bacteriol. 143:1019–1024.

    PubMed  CAS  Google Scholar 

  • Ghrayeb, J., and Inouye, M., 1984, Nine amino acid residues at the amino terminal of lipoprotein are sufficient for its modification, processing and localization in the outermembrane of Escherichia coli, J. Biol. Chem., 259:463–467.

    PubMed  CAS  Google Scholar 

  • Halegoua, S., and Inouye, M., 1979, Translocation and assembly of outer-membrane proteins in Escherichia coli. Selective accumulation of precursors and novel assembly intermediates caused by phenylethyl alcohol, J. Mol. Biol. 130:39–61.

    Article  PubMed  CAS  Google Scholar 

  • Hall, M. N., and Schwartz, M., 1982, Reconsidering the early steps of protein secretion, Ann. Microbiol. (Inst. Pasteur) 133A:123–127.

    Article  Google Scholar 

  • Hall, M. N., Gabay, J., and Schwartz, M., 1983, Evidence for a coupling of synthesis and export of an outer membrane protein in Escherichia coli, EMBO J. 2:15–19.

    PubMed  CAS  Google Scholar 

  • Hantke, K., and Braun, V., 1973, Covalent binding of lipid to protein. Diglyceride and amide linked fatty acid at the N-terminal end of the murein lipoprotein of the Escherichia coli outer membrane, Eur. J. Biochem. 34:284–296.

    Article  PubMed  CAS  Google Scholar 

  • Hirota, Y., Suzuki, H., Nishimura, Y., and Yasuda, S., 1977, On the process of cellular division in Escherichia coli:A mutant of E. coli lacking a murein-lipoprotein, Proc. Natl. Acad. Sci. USA 74:1417–1420.

    Article  PubMed  CAS  Google Scholar 

  • Hussain, M., Ichihara, S., and Mizushima, S., 1980, Accumulation of glyceride-containing precursor of the outer membrane lipoprotein in the cytoplasmic membrane of Escherichia coli treated with globomycin, J. Biol. Chem. 255:3707–3712.

    PubMed  CAS  Google Scholar 

  • Hussain, M., Ichihira, S., and Mizushima, S., 1982, Mechanism of signal peptide cleavage in the biosynthesis of the major lipoprotein of the Escherichia coli outer membrane, J. Biol. Chem. 257:5177–5182.

    PubMed  CAS  Google Scholar 

  • Ichihara, S., Hussain, M., and Mizushima, S., 1981, Characterization of new membrane lipoproteins and their precursors of Escherichia coli, J. Biol. Chem. 256:3125–3129.

    PubMed  CAS  Google Scholar 

  • Ichihara, S., Hussain, M., and Mizushima, S., 1982, Mechanism of export of outer membrane lipoproteins through the cytoplasmic membrane in Escherichia coli, J. Biol. Chem. 257:495–500.

    PubMed  CAS  Google Scholar 

  • Inouye, M. (ed.), 1979a, Bacterial Outer Membranes:Biogenesis and Functions, Wiley-Interscience, J. Wiley and Sons, New York.

    Google Scholar 

  • Inouye, M., 1979b, Lipoprotein of the outer membrane of Escherichia coli, in:Biomembranes, Vol. 10 (L. A. Manson, ed.), Plenum Press, New York.

    Google Scholar 

  • Inouye, M., 1979c, What is the outer membrane, in:Bacterial Outer Membranes:Biogenesis and Function, Wiley-Interscience, J. Wiley and Sons, New York.

    Google Scholar 

  • Inouye, M., 1982, Lipoproteins from the bacterial outer membranes. Their gene structures and assembly mechanism, in:Membranes and Transport, Vol. 1 ( A. N. Martonosi, ed.), Plenum Press, New York, pp. 289–297.

    Google Scholar 

  • Inouye, M., and Halegoua, S., 1980, Secretion and membrane localization of proteins in Escherichia coli, CRC Crit. Rev. Biochem. 7:339–371.

    Article  PubMed  CAS  Google Scholar 

  • Inouye, M., Shaw, J., and Shen, C., 1972, The assembly of a structural lipoprotein in the envelope of Escherichia coli, J. Biol. Chem. 247:8154–8159.

    PubMed  CAS  Google Scholar 

  • Inouye, S., Lee, N., Inouye, M., Wu, H. C., Suzuki, H., Nishimura, Y., Iketani, H., and Hirota, Y., 1977a, Amino acid replacement in a mutant lipoprotein of the Escherichia coli outer membrane, J. Bacteriol. 132:308–313.

    PubMed  CAS  Google Scholar 

  • Inouye, S., Wang, S., Sekizawa, J., Halegoua, S., and Inouye, M., 1977b, Amino acid sequence for the peptide extension on the prolipoprotein of the Escherichia coli outer membrane, Proc. Natl. Acad. Sci. USA 74:1004–1008.

    Article  PubMed  CAS  Google Scholar 

  • Inouye, S., Soberon, X., Franceschini, T., Nakamura, K., Itakura, K., and Inouye, M., 1982, Role of positive charge on the amino-terminal region of the signal peptide in protein secretion across the membrane, Proc. Natl. Acad. Sci. USA 79:3438–3441.

    Article  PubMed  CAS  Google Scholar 

  • Inouye, S., Franceschini, T., Sato, M., Itakura, K., and Inouye, M., 1983a, Prolipoprotein signal peptidase of Escherichia coli requires a cysteine residue at the cleavage site, EMBO J 2:87–91.

    PubMed  CAS  Google Scholar 

  • Inouye, S., Hsu, C-P. S., Itakura, K., and Inouye, M., 1983b, Requirement for signal peptide cleavage of Escherichia coli prolipoprotein, Science, 221:59–61.

    Article  PubMed  CAS  Google Scholar 

  • Inouye, S., Vlasuk, G. P., Hsuing, H., and Inouye, M., 1984, Effects of replacing and deleting glycine residues in the hydrophobic region of the Escherichia coli prolipoprotein signal peptide on its secretion and processing. J. Biol. Chem., in press.

    Google Scholar 

  • Inukai, M., and Inouye, M., 1983, Association of the prolipoprotein accumulated in the presence of globomycin with the Escherichia coli outer membrane, Eur. J. Biochem. 130:27–32.

    Article  PubMed  CAS  Google Scholar 

  • Inukai, M., Nakajima, M., Osawa, M., Haneishi, T., and Arai, M., 1978a, Globomycin, a new peptide antibiotic with spheroplast-forming activity. II. Isolation and physiochemical and biological characterization, J. Antibiotics 31:421–425.

    CAS  Google Scholar 

  • Inukai, M., Takeuchi, M., Shimuzu, K., and Arai, M., 1978b, Mechanism of action of globomycin, J. Antibiotics 31:1203–1205.

    CAS  Google Scholar 

  • Inukai, M., Takeuchi, M., Shimuzu, K., and Arai, M., 1979, Existence of the bound form of prolipoprotein in Escherichia coli B cells treated with globomycin, J. Bacteriol 140:1098–1101.

    PubMed  CAS  Google Scholar 

  • Inukai, M., and Inouye, M., 1983a, Association of the prolipoprotein accumulated in the presence of globomycin with the Escherichia coli outer membrane, Eur. J. Biochem. 130:27–32.

    Article  PubMed  CAS  Google Scholar 

  • Inukai, M., Masui, Y., Vlasuk, G. P., and Inouye, M., 1983b, Effects of inserting eight amino acid residues into the major lipoprotein on its assembly in the outer membrane of Escherichia coli, J. Bacteriol., 155:275–280.

    PubMed  CAS  Google Scholar 

  • Inukai, M., Nakamura, K., Ghrayeb, J., and Inouye, M., 1984, Apolipoprotein, an intermediate in the processing of the major lipoprotein of the Escherichia coli outer membrane, J. Biol. Chem., 259:757–760.

    PubMed  CAS  Google Scholar 

  • Ito, K., 1982, Purification of the precursor form of maltose-binding protein, a periplasmic protein of Escherichia coli, J. Biol. Chem. 257:9895–9897.

    PubMed  CAS  Google Scholar 

  • Lai, J. S., and Wu, H. C., 1980, Incorporation of acyl moieties of phospholipid into murein lipoprotein in intact cells of Escherichia coli by phospholipid vesicle fusion, J. Bacteriol. 144:451–453.

    PubMed  CAS  Google Scholar 

  • Lai, J. S., Philbrick, W. M., and Wu, H. C., 1980, Acyl moieties in phospholipids are the precursors for the fatty acids in the murein lipoprotein of Escherichia coli, J. Biol. Chem. 255:5384–5387.

    PubMed  CAS  Google Scholar 

  • Lai, J. S., Philbrick, W. M., Hayashi, S., Inukai, M., Arai, M., Hirota, Y., and Wu, H. C., 1981, Globomycin sensitivity of Escherichia coli and Salmonella typhimurium:Effects of mutations affecting structures of murein lipoprotein, J. Bacteriol. 145:657–660.

    PubMed  CAS  Google Scholar 

  • Lee, N., Yamagata, H., and Inouye, M., 1984, Inhibition of secretion of a mutant lipoprotein across the cytoplasmic membrane by the wild type lipoprotein of the Escherichia coli outer membrane, J. Bacteriol., in press.

    Google Scholar 

  • Lin, J. J. C., Kanawaza, H., Ozols, J., and Wu, H. C., 1978, An Escherichia coli mutant with an amino acid alteration within the signal sequence of outer membrane prolipoprotein, Proc. Natl. Acad. Sci. USA 75:4891–4895.

    Article  PubMed  CAS  Google Scholar 

  • Maeda, T., Glass, J., and Inouye, M., 1981, Accumulation of the prolipoprotein of the Escherichia coli outer membrane caused by benzyloxycarbonylalanine chloromethyl ketone, J. Biol. Chem. 256:4712–4714.

    PubMed  CAS  Google Scholar 

  • Michaelis, S., and Beckwith, J., 1982, Mechanism of incorporation of cell envelope proteins in Escherichia coli, Annu. Rev. Microbiol. 36:435–465.

    Article  PubMed  CAS  Google Scholar 

  • Nakamura, K., and Inouye, M., 1979, DNA sequence of the gene for the outer membrane lipoprotein of E. coli. An extremely AT rich promoter, Cell 18:1109–1117.

    Article  PubMed  CAS  Google Scholar 

  • Nakamura, K., and Inouye, M., 1982, Construction of versatile expression cloning vehicles using the lipoprotein gene of Escherichia coli, EMBO J. 1:771–775.

    PubMed  CAS  Google Scholar 

  • Nakamura, K., Masui, Y., and Inouye, M., 1982, Use of lac promoter-operator fragments as a transcriptional control switch for the expression of the constitutive lpp gene in Escherichia coli, J. Mol. Appl. Genet. 1:289–299.

    PubMed  CAS  Google Scholar 

  • Rick, P. D., Neumeyer, B. A., and Young, D. A., 1983, Effect of altered lipid A synthesis on the synthesis of the OmpA protein in Salmonella typhimurium, J. Biol. Chem. 258:629–635.

    PubMed  CAS  Google Scholar 

  • Rotering, H., and Braun, V., 1977, Lipid deficiency in a lipoprotein mutant of Escherichia coli, FEBS Lett. 83:41–44.

    Article  PubMed  CAS  Google Scholar 

  • Schwartz, M., Roa, M., and Debarboville, M., 1981, Mutations that effect lamB gene expression at a posttranscriptional level, Proc. Natl. Acad. Sci. USA 78:2937–2941.

    Article  PubMed  CAS  Google Scholar 

  • Smith, W., Tai, P. C., and Davis, B. D., 1978, Nascent peptide as sole attachment of polysomes to membranes in bacteria, Proc. Natl. Acad. Sci. USA 75:814–817.

    Article  PubMed  CAS  Google Scholar 

  • Tokunaga, M., Tokunaga, H., and Wu, H. C., 1982a, Post-translational modification and processing of Escherichia coli prolipoprotein in vitro, Proc. Natl. Acad. Sci. USA 79:2255–2259.

    Article  PubMed  CAS  Google Scholar 

  • Tokunaga, M., Loranger, J. M., Wolfe, P. B., and Wu, H. C., 1982b, Prolipoprotein signal peptidase in Escherichia coli is distinct from the M13 procoat protein signal peptidase, J. Biol. Chem. 257:9922–9925.

    PubMed  CAS  Google Scholar 

  • Tokunaga, M., Loranger, J. M., and Wu, H. C., 1983, Isolation and characterization of an Escherichia coli clone overproducing prolipoprotein signal peptidase, J. Biol. Chem. 258:12102–12105.

    PubMed  CAS  Google Scholar 

  • Vlasuk, G. P., and Inouye, S., 1983, Site-specific mutagenesis using synthetic oligodeoxyribonucleotides as mutagens, in:Experimental Manipulation of Gene Expression ( M. Inouye, ed.), Academic Press, New York, pp. 291–303.

    Google Scholar 

  • Vlasuk, G. P., Inouye, S., Ito, H., Itakura, K., and Inouye, M., 1983, Effects of complete removal of basic amino acid residues from the signal peptide on secretion of lipoprotein in Escherichia coli, J. Biol. Chem., 258:7141–7148.

    PubMed  CAS  Google Scholar 

  • Vlasuk, G. P., Inouye, S., and Inouye, M., 1984, Effects of replacing serine and threonine residues within the signal peptide on the secretion of the major outer membrane lipoprotein of Escherichia coli, J. Biol. Chem., in press.

    Google Scholar 

  • Walter, P., and Blobel, G., 1981, Translocation of proteins across the endoplasmic reticulum. III. Signal recognition protein (SRP) causes signal sequence-dependent and site-specific arrest of chain elongation that is released by microsomal membranes, J. Cell Biol. 91:557–561.

    Article  PubMed  CAS  Google Scholar 

  • Weigand, R. A., Vinci, K. D., and Rothfield, L. I., 1976, Morphogenesis of the bacterial division septum:A new class of septation-defective mutants, Proc. Natl. Acad. Sci. USA 73:1882–1886.

    Article  PubMed  CAS  Google Scholar 

  • Weinsink, J., and Witholt, B., 1981, Conversion of free lipoprotein to the murein-bound form, Eur. J. Biochem. 117:207–212.

    Article  Google Scholar 

  • Wickner, W., 1979, The assembly of proteins into biological membranes:The membrane trigger hypothesis, Annu. Rev. Biochem. 48:23–45.

    Article  PubMed  CAS  Google Scholar 

  • Wickner, W., 1983, M-13 coat protein as a model of membrane assembly, Trends Biochem. Sci. March, pp. 90–94.

    Google Scholar 

  • Wolfe, P. B., Silver, P., and Wickner, W., 1982, The isolation of homogeneous leader peptidase from a strain of Escherichia coli which overproduces the enzyme, J. Biol. Chem. 25:7898–7902.

    Google Scholar 

  • Wu, H. C., Hou, C., Lin, J. J. C., and Yem, D. W., 1977, Biochemical characterization of a mutant lipoprotein of Escherichia coli, Proc. Natl. Acad. Sci. USA 74:1388–1392.

    Article  PubMed  CAS  Google Scholar 

  • Wu, H. C., Lai, J. S., Hayashi, S., and Giam, C. Z., 1982, Biogenesis of membrane lipoproteins in Escherichia coli, Biophys. J. 37:307–315.

    Article  PubMed  CAS  Google Scholar 

  • Yamagata, H., Ippolito, C., Inukai, M., and Inouye, M., 1982, Temperature-sensitive processing of outer membrane lipoprotein in an Escherichia coli mutant, J. Bacteriol. 152:1163–1168.

    PubMed  CAS  Google Scholar 

  • Zimmermann, R., and Wickner, W., 1983, Energetics and intermediates of the assembly of protein OmpA into the outer membrane of Escherichia coli, J. Biol. Chem. 258:3920–3925.

    PubMed  CAS  Google Scholar 

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Vlasuk, G.P., Ghrayeb, J., Inouye, M. (1985). The Major Outer Membrane Lipoprotein of Escherichia coli:Secretion, Modification, and Processing. In: Martonosi, A.N. (eds) The Enzymes of Biological Membranes. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-2355-6_9

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  • DOI: https://doi.org/10.1007/978-1-4613-2355-6_9

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