In vivo membrane assembly of the E.coli polytopic protein, melibiose permease, occurs via a Sec-independent process which requires the protonmotive force

EMBO Journal

Volumn 15, Issue 19, 1996, Pages 5202-5208

  Bassilana, Martine ^a   Gwizdek, Carole ^a  

^a Laboratoire Jean Maetz   (France)

Author keywords

E.coli; Membrane insertion; Polytopic membrane protein; Protonmotive force; Sec proteins

Indexed keywords

MELIBIOSE; MEMBRANE PROTEIN; PERMEASE;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; KINETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN TRANSPORT; PROTON MOTIVE FORCE;

ESCHERICHIA COLI;

EID: 0029790978     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00905.x     Document Type: Article

References (50)

1. Ahrem, B., Hoffschulte, H.K. and Muller, M. (1989) In vitro membrane assembly of a polytopic, transmembrane protein results in an enzymatically active conformation. J. Cell Biol., 108, 1637-1646.
2. Akiyama, Y. and Ito, K. (1989) Export of Escherichia coli alkaline phosphatase attached to an integral membrane protein SecY. J. Biol. Chem., 264, 437-442.
3. + on the translocation of charged residues explain the 'positive inside' rule. EMBO J, 13, 2267-2272.
4. Arkowitz, R.A. and Bassilana, M. (1994), Protein translocation in Escherichia coli. Biochim. Biophys. Acta, 1197, 311-343.
5. Bakker, E.P. and Mangerich, W.E. (1983) The effects of weak acids on potassium uptake by Escherichia coli K12. Biochim. Biophys. Acta, 730, 379-386.
6. Bakker, E.P. and Randall, L.L. (1984) The requirement for energy during export of β-lactamase in Escherichia coli is fulfilled by the total protonmotive force. EMBO J., 3, 895-900.
7. + melibiose symport in E.coli membrane vesicles. Biochem. Biophys. Res. Commun., 129, 626-631.
8. Botfield, M.C. and Wilson, T.H. (1988) Mutations that simultaneously alter both sugar and cation specificity in the melibiose carrier of E.coli. J. Biol. Chem., 263, 12909-12915.
9. Botfield, M.C. and Wilson, T.H. (1989) Peptide-specific antibody for the melibiose carrier of Escherichia coli localizes the carboxyl terminus to the cytoplasmic face of the membrane. J. Biol. Chem., 264, 11649-11652.
10. Botfield, M.C., Naguchi, K., Tsuchiya, T. and Wilson, T.H. (1992) Membrane topology of the melibiose carrier of Escherichia coli. J. Biol. Chem., 267, 1818-1822.
11. Brandolin, G., Doussiere, J., Gulik, A., Gulik-Krzywicki, T., Lauquin, G.J.M. and Vignais, P.V. (1980) Kinetic, binding and ultrastructural properties of the beef heart adenine nucleotide carrier protein after incorporation into phospholipid vesicles. Biochim. Biophys. Acta, 592, 592-614.
12. Cao, G., Cheng, S., Whitley, P., von Heijne, G., Kuhn, A. and Dalbey, R.E. (1994) Synergistic insertion of two hydrophobic regions drives Sec-independent membrane protein assembly. J. Biol. Chem., 269, 26898-26903.
13. Cao, G., Kuhn, A. and Dalbey, R.E. (1995) The translocation of negatively charged residues across the membrane is driven by the electrochemical potential: evidence for an electrophoresis-like membrane transfer mechanism. EMBO J., 14, 866-875.
14. Damiano, E., Bassilana, M. and Leblanc, G. (1986) Sugar binding properties of the melibiose permease in Escherichia coli membrane vesicles. J. Biol. Chem., 261, 6893-6899.
15. Date, T., Goodman J.M. and Wickner, W. (1980) Procoat, the precursor of M13 coat protein requires an electrochemical potential for membrane insertion. Proc. Natl Acad. Sci. USA, 77, 4669-4673.
16. Engelman, D.M. and Steitz, T.A. (1981) The spontaneous insertion of proteins into and across membranes: the helical hairpin hypothesis. Cell, 23, 411-422.
17. BAD promoter. J. Bacteriol., 177, 4121-4130.
18. Ito, K. and Akiyama, Y. (1991) In vivo analysis of integration of membrane proteins in Escherichia coli. Mol. Microbiol., 5, 2243-2253.
19. Klionsky, D.J., Brusilow, W.A. and Simoni, R.D. (1984) In vivo evidence for the role of the epsilon subunit as an inhibitor of the protontranslocating ATPase of Escherichia coli. J. Bacteriol, 160, 1055-1066.
20. Kuhn, A., Kreil, G. and Wickner, W. (1986a) Both hydrophobic domains of M13 procoat are required to initiate membrane insertion. EMBO J., 5, 3681-3685.
21. Kuhn, A., Wickner, W. and Kreil, G. (1986b) The cytoplasmic carboxy terminus of M13 procoat is required for the membrane insertion of its central domain. Nature, 322, 335-339.
22. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
23. +-coupled melibiose symport in E.coli. In Palmieri, F. and Quagliariello, E. (eds), Molecular Basis of Biomembrane Transport. Elsevier Science Publishers, pp. 53-62.
24. Lowry, O.H., Rosenbrough, N.J., Farr, A.L. and Randall, R.J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem., 193, 265-275.
25. MacFarlane, J. and Muller, M. (1995) The functional integration of a polytopic membrane protein of Escherichia coli is dependent on the bacteral signal-recognition particle. Eur. J. Biochem., 233, 766-771.
26. McGovern, K. and Beckwith, J. (1991) Membrane insertion of the Escherichia coli MalF protein in cells with impaired secretion machinery. J. Biol. Chem., 266, 20870-20876.
27. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
28. Murphy, C.K. and Beckwith, J. (1994) Residues essential for the function of SecE, a membrane component of the Escherichia coli secretion apparatus, are located in a conserved cytoplasmic region. Proc. Natl Acad. Sci. USA, 91, 2557-2561.
29. Oliver, D.B. and Beckwith, J. (1981) E.coli mutant pleiotropically defective in the export of secreted proteins. Cell, 25, 765-772.
30. Oliver, D.B., Cabelli, R.J., Dolan, K.M. and Jarosik, G.P. (1990) Azide-resistant mutants of Escherichia coli alter the SecA protein, an azide-sensitive component of the protein export machinery. Proc. Natl Acad. Sci. USA, 87, 8227-8231.
31. Padan, E., Zilberstein, D. and Schuldiner, S. (1981) pH homeostasis in bacteria. Biochim. Biophys. Acta, 650, 151-166.
32. Padan, E., Arbel, T., Rimon, A., BarShira, A. and Cohen, A. (1983) Biosynthesis of the lactose permease in Escherichia coli minicells and effect of carrier amplification on cell physiology. J Biol. Chem., 258, 5666-5673.
33. Phillips, G.J. and Silhavy, T.J. (1992) The E.coli ffh gene is necessary for viability and efficient protein export. Nature, 359, 744-746.
34. + sugar symport is catalyzed by a single polypeptide. Biochemistry, 34, 4412-4420.
35. Pourcher, T., Bibi, E., Kaback, H.R. and Leblanc, G. (1996) Membrane topology of the melibiose permease of Escherichia coli studied by melB-phoA fusions analysis. Biochemistry, 35, 4161-4168.
36. Pugsley, A.P. (1993) The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev., 57, 50-108.
37. Reizer, J., Reizer, A. and Saier, M.H. (1994) A functional superfamily of sodium/solute symporters. Biochim. Biophys. Acta, 1197, 133-166.
38. Saier, M.H., Werner, P.K. and Muller, M. (1989) Insertion of proteins into bacterial membranes: mechanism, characteristics and comparisons with the eucaryotic process. Microbiol Rev., 53, 333-366.
39. Shiba, K., Ito, K., Yura, T. and Cerretti, D.P. (1984) A defined mutation in the protein export gene within the spc ribosomal protein operon of Escherichia coli: isolation and characterization of a new temperature-sensitive secY mutant. EMBO J., 3, 631-635.
40. Stephan, M.M. and Jacobson, G.R. (1986) Membrane disposition of the Escherichia coli mannitol permease: identification of membrane-bound and cytoplasmic domains. Biochemistry, 25, 8230-8234.
41. Swidersky, U.E., Rienhofer-Schweer, A., Werner, P.K., Ernst, F., Benson, S.A., Hoffschulte, H.K. and Muller, M. (1992) Biochemical analysis of the biogenesis and function of the Escherichia coli export factor SecY. Eur. J. Biochem., 207, 803-811.
42. Taura, T., Baba, T., Akiyama, Y. and Ito, K. (1993) Determinants of the quantity of the stable SecY complex in the Escherichia coli cell. J. Bacteriol., 175, 7771-7775.
43. von Heijne, G. (1989) Control of topology and mode of assembly of a polytopic membrane protein by positively charged residues. Nature, 341, 456-458.
44. von Heijne, G. (1994) Sec-independent protein insertion into the inner E.coli membrane, a phenomenon in search of an explanation. FEBS Lett., 346, 69-72.
45. Werner, P.K., Saier, M.H. and Muller, M. (1992) Membrane insertion of the mannitol permease of Escherichia coli occurs in conditions of impaired SecA function. J. Biol. Chem., 267, 24523-24532.
46. Wolfe, P.B. and Wickner, W. (1984) Bacterial leader peptidase, a membrane protein without a leader peptide, uses the same export pathway as pre-secretory proteins. Cell, 36, 1067-1072.
47. Wolfe, P.B., Wickner, W. and Goodman, J.M. (1983) Sequence of the leader peptidase gene of Escherichia coli and the orientation of leader peptidase in the bacterial envelope. J. Biol. Chem., 258, 12073-12080.
48. Wolfe, P.B., Rice, M. and Wickner, W. (1985), Effects of two sec genes on protein assembly into the plasma membrane of Escherichia coli. J. Biol Chem., 260, 1836-1841.
49. Yamato, I. (1992) Membrane assembly of lactose permease of Escherichia coli. J. Biochem., 111, 444-450.
50. Yazyu, H., Shiota-Niiya, T., Shimamoto, T., Kanazawa, H., Futai, M. and Tsuchiya, T. (1984) Nucleotide sequence of the melB gene and characteristics of deduced amino-acid sequence of the melibiose carrier in E.coli. J. Biol. Chem., 259, 4320-4326.