Lipopolysaccharides and divalent cations are involved in the formation of an assembly-competent intermediate of outer-membrane protein PhoE of E.Coli

EMBO Journal

Volumn 15, Issue 20, 1996, Pages 5567-5573

  De Cock, Hans ^a   Tommassen, Jan ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Assembly; Lipopolysaccharide; Outer membrane; Porin; Protein folding

Indexed keywords

DIVALENT CATION; LIPOPOLYSACCHARIDE; MONOMER; OUTER MEMBRANE PROTEIN; TRITON X 100;

ARTICLE; CHANNEL GATING; ESCHERICHIA COLI; GRAM NEGATIVE BACTERIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FOLDING; PURIFICATION; THERMOSTABILITY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 0029903977     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00941.x     Document Type: Article

References (37)

1. Ames, G.F.-L., Spudich, E.N. and Nikaido, H. (1974) Protein composition of the outer membrane of Salmonella typhimurium: effect of lipopolysaccharide mutations. J. Bacteriol., 117, 406-416.
2. Bligh, G.G. and Dyer, W.G. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol., 37, 911-917.
3. Bocquet-Pagès, C., Lazdunski, C. and Lazdunski, A. (1981) Lipid-synthesis-dependent biosynthesis (or assembly) of major outer membrane proteins of Escherichia coli. Eur. J. Biochem., 118, 105-111.
4. Bolla, J.-M., Lazdunski, C. and Pagès, J.M. (1988) The assembly of the major outer membrane protein OmpF of Escherichia coli depends on lipid synthesis. EMBO J., 7, 3595-3599.
5. Bosch, D., Leunissen, J., Verbakel, J., de Jong, M., van Erp, H. and Tommassen, J. (1986) Periplasmic accumulation of truncated forms of outer membrane PhoE protein of Escherichia coli K-12. J. Mol. Biol., 189, 449-455.
6. Casadaban, M.J. (1976) Regulation of the regulatory gene for the arabinose pathway araC. J. Mol. Biol., 104, 541-555.
7. Cowan, S.W., Schirmer, T., Rummel, G., Steiert, M., Ghosh, R., Pauptit, R.A., Jansonius, J.N. and Rosenbusch, J.P. (1992) Crystal structures explain functional properties of two E.coli porins. Nature, 358, 727-733.
8. de Cock, H., Meeldijk, J., Overduin, P., Verkleij, A. and Tommassen, J. (1989) Membrane biogenesis in Escherichia coli: effects of a secA mutation. Biochim. Biophys. Acta, 985, 313-319.
9. de Cock, H., Hekstra, D. and Tommassen, J. (1990a) In vitro trimerization of outer membrane protein PhoE. Biochimie, 72, 177-182.
10. de Cock, H., Hendriks, R., de Vrije, T. and Tommassen, J. (1990b) Assembly of an in vitro synthesized Escherichia coli outer membrane porin into its stable trimeric configuration. J. Biol. Chem., 265, 4646-4651.
11. de Cock, H., van Blokland, S. and Tommassen, J. (1996) In vitro insertion and assembly of outer membrane protein PhoE of Escherichia coli K-12 into the outer membrane: role of Triton X-100. J. Biol. Chem., 271, 12885-12890.
12. de Vrije, T., Tommassen, J. and de Kruijff, B. (1987) Optimal posttranslational translocation of the precursor of PhoE protein across Escherichia coli membrane vesicles requires both ATP and the protonmotive force. Biochim. Biophys. Acta, 900, 63-72.
13. Freudl, R., Schwarz, H., Klose, M., Movva, N.R. and Henning, U. (1985) The nature of information required for export and sorting, present within the outer membrane protein OmpA of Escherichia coli K-12. EMBO J., 4, 3593-3598.
14. Galanos, C., Lüderitz, O. and Westphal, O. (1969) A new method for the extraction of R lipopolysaccharides. Eur. J. Biochem., 9, 245-249.
15. Klose, M., Schwarz, H., MacIntyre, S., Freudl, R., Eschbach, M.-L. and Henning, U. (1988) Internal deletions in the gene for an Escherichia coli outer membrane protein define an area possibly important for recognition of the outer membrane by this polypeptide. J. Biol. Chem., 263, 13291-13296.
16. Koplow, J. and Goldfine, H. (1974) Alterations in the outer membrane of the cell envelope of heptose-deficient mutants of Escherichia coli. J. Bacteriol., 117, 527-543.
17. Lugtenberg, B. and van Alphen, L. (1983) Molecular architecture and functioning of the outer membrane of Escherichia coli and other Gram-negative bacteria. Biochim. Biophys. Acta, 737, 51-115.
18. Lugtenberg, B., Meijers, J., Peters, R., van der Hoek, P. and van Alphen, L. (1975) Electrophoretic resolution of the 'major outer membrane protein' of Escherichia coli K-12 into four bands. FEBS Lett., 58, 254-258.
19. Nakayama, H., Mitsui, T., Nishihara, M. and Kito, M. (1980) Relation between temperature of E.coli and phase transition temperatures of its cytoplasmic and outer membrane. Biochim. Biophys. Acta, 601, 1-10.
20. Nikaido, H. and Ried, J. (1990) Biogenesis of prokaryotic pores. Experientia, 46, 174-180.
21. Nikaido, H. and Vaara, M. (1985) Molecular basis of bacterial outer membrane permeability. Microbiol. Rev., 49, 1-32.
22. Pagès, C., Lazdunski, C. and Lazdunski, A. (1982) The receptor of bacteriophage lambda: evidence for a biosynthesis dependent on lipid synthesis. Eur. J. Biochem., 122, 381-386.
23. Pelham, H.R.B. (1989) Control of protein exit from the endoplasmic reticulum. Annu. Rev. Cell Biol., 5, 1-23.
24. Ried, G., Hindennach, I. and Henning, U. (1990) Role of lipopolysaccharide in assembly of Escherichia coli outer membrane proteins OmpA. OmpC and OmpF. J. Bacteriol., 172, 6048-6053.
25. Sen, K. and Nikaido, H. (1990) In vitro trimerization of OmpF porin secreted by spheroplasts of Escherichia coli. Proc. Natl Acad. Sci. USA, 87, 743-747.
26. Sen, K. and Nikaido, H. (1991a) Trimerization of an in vitro synthesized OmpF porin of Escherichia coli outer membrane. J. Biol. Chem., 266, 11295-11300.
27. Sen, K. and Nikaido, H. (1991b) Lipopolysaccharide structure required for the in vitro trimerization of Escherichia coli OmpF porin. J. Bacteriol., 173, 926-928.
28. Struyvé, M., Moons, M. and Tommassen, J. (1991) Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J. Mol. Biol., 218, 141-148.
29. Thom, J.R. and Randall, L.L. (1988) Role of the leader peptide of maltose-binding protein in two steps of the export process. J. Bacteriol., 170, 5654-5661.
30. Tommassen, J. (1988) Biogenesis and membrane topology of outer membrane proteins in Escherichia coli. In Op den Kamp, J.A.F (ed.), Membrane Biogenesis, Vol. H16. NATO ASI Series. Springer-Verlag, Berlin, pp. 351-373.
31. Tommassen, J. and de Cock, H. (1995) Export and assembly of outer membrane proteins in E.coli. In Tartakoff, A.M. and Dalbey, R.E. (eds), Advances in Cell and Molecular Biology of Membranes and Organelles. Vol. 4. JAI Press, Greenwich, Connecticut, pp. 145-173.
32. Tommassen, J. and Lugtenberg, B. (1981) Localization of phoE, the structural gene for outer membrane protein e in Escherichia coli K-12. J. Bacteriol., 147, 118-123.
33. van Alphen, L., Verkleij, A., Leunissen-Bijvelt, J. and Lugtenberg, B. (1978) Architecture of the outer membrane of Escherichia coli III. Protein-lipopolysaccharide complexes in intramembraneous particles. J. Bacteriol., 134, 1089-1098.
34. van der Ley, P., de Graaff, P. and Tommassen, J. (1986) Shielding of Escherichia coli outer membrane proteins as receptors for bacteriophages and colicins by O-antigenic chains of lipopolysaccharide. J. Bacteriol., 168, 449-451.
35. Van Gelder, P., de Cock, H. and Tommassen, J. (1994) Detergent-induced folding of the outer-membrane protein PhoE, a pore protein induced by phosphate limitation. Eur. J. Biochem., 226, 783-787.
36. Westphal, O. and Jann, K. (1965) Bacterial lipopolysaccharides. In Whistler, R.L. (ed.), Methods in Carbohydrate Chemistry. Vol. V. Academic Press, New York, pp. 83-91.
37. Wickner, W., Driessen, A.J.M. and Hartl, F.-U. (1991) The enzymology of protein translocation across the Escherichia coli plasma membrane. Annu. Rev. Biochem., 60, 101-124.