Biogenesis of the gram-negative bacterial envelope

Cell

Volumn 91, Issue 5, 1997, Pages 567-573

  Duong, Franck ^a   Eichler, Jerry ^a   Price, Albert ^a   Leonard, Marilyn Rice ^a   Wickner, William ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL MEMBRANE; BACTERIAL OUTER MEMBRANE; BIOGENESIS; GRAM NEGATIVE BACTERIUM; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; PROTEIN TRANSPORT; REVIEW;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 0030827619     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)80444-4     Document Type: Review

References (84)

1. Akita, M., Shinkai, A., Matsuyama, S.-i., and Mizushima, S. (1991). SecA, an essential component of the secretory machinery of Escherichia coli, exists as a homodimer. Biochem. Biophys. Res. Comm. 174, 211-216.
2. Akiyama, Y., Shirai, Y., and Ito, K. (1994). Involvement of FtsH in protein assembly into and through the membrane. J. Biol. Chem. 269, 5225-5229.
3. Andersson, H., and von Heijne, G. (1993). Sec-dependent and sec-independent assembly of E. coli inner membrane proteins: The topological rules depend on chain length. EMBO J. 12, 683-691.
4. Arkowitz, R.A., and Wickner, W. (1994). SecDand SecFare required for the proton electrochemical gradient stimulation of preprotein translocase. EMBO J. 13, 954-963.
5. Baichwal, V., Liu, D., and Ames, G.F.-L. (1993). The ATP-binding component of a prokaryotic traffic ATPase is exposed to the periplasmic (external) surface. Proc. Natl. Acad. Sci. USA 90, 620-624.
6. Bassilana, M., and Gwizdek, C. (1996). In vivo membrane assembly of the E. coli polytopic protein, melibiose permease, occurs via a Sec-independent process which requires the protonmotive force. EMBO J. 15, 5202-5208.
7. Batenburg, A.M., Demel, R.A., Verkleij, A.J., and deKruijff, B. (1988) Penetration of the signal sequence of Escherichia coli phoE protein into phospholipid model membranes leads to lipid-specific changes in signal peptide structure and alterations of lipid organization. Biochemistry 27, 5678-5686.
8. Bliss, J.M., and Silver, R.P. (1997). Evidence that KpsT, the ATP-binding component of an ATP-binding cassette transporter, is exposed to the periplasm and associates with polymer during translocation of the polysialic acid capsule of Escherichia coli K1. J. Bacteriol. 179, 1400-1403.
9. Braun, V., and Sieglin, U. (1970). The covalent murein-lipoprotein structure of the Escherichia coli cell wall. Eur. J. Biochem. 13, 336-346.
10. Breukink, E., Demel, R.A., de Korte-Kool, G., and de Kruijff, B. (1992). SecA insertion into phospholipids is stimulated by negatively charged lipids and inhibited by ATP: a monolayer study. Biochemistry 31, 1119-1124.
11. Briggs, M.S., Gierasch, L.M., Zlotnick, A., Lear, J.D., and de Grado, W.F. (1985). In vivo function and membrane binding properties are correlated for Escherichia coli lamB signal peptides. Science 288, 1096-1099.
12. Cabelli, R.J., Dolan, K.M., Qian, L., and Oliver, D.B. (1991) Characterization of membrane-associated and soluble states of SecA protein from wild-type and SecA51(Ts) mutant strains of Escherichia coli. J. Biol. Chem. 266, 24420-24427.
13. Chen, X., Xu, H., and Tai, P.C. (1996). A significant fraction of functional SecA is permanently embedded in the membrane. J. Biol. Chem. 271, 29698-29706.
14. Collier, D.N., Bankaitis, V., Weiss, J.B., and Bassford, P.J., Jr. (1988). The antifolding activity of SecB promotes the export of the E. coli maltose-binding protein. Cell 53, 273-283.
15. de Gier, J.-W. L., Mansournia, P., Valent, Q.A., Phillips, G.J., Luirink, J., and von Heijne, G. (1996). Assembly of a cytoplasmic membrane protein in Escherichia coli is dependent on the signal recognition particle. FEBS Lett. 399, 307-309.
16. Derman, A.I., Puziss, J.W., Bassford, P.J., Jr., and Beckwith, J. (1993). A signal sequence is not required for protein export in prlA mutants of Escherichia coli. EMBO J. 12, 879-888.
17. Dolan, K.M., and Oliver, D. (1991). Characterization of Escherichia coli SecA protein binding to a site on its own mRNA involved in autoregulation. J. Biol. Chem. 266, 23329-23333.
18. Duong, F., and Wickner, W. (1997a). Distinct catalytic roles of the SecYE, SecG, and SecDFyajC subunits of preprotein translocase holoenzyme. EMBO J. 16, 2756-2768.
19. Duong, F., and Wickner, W. (1997b). The SecDFyajC domain of preprotein translocase controls preprotein movement by regulating SecA membrane cycling. EMBO J. 16, 4871-4879.
20. Economou, A., and Wickner, W. (1994). SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell 78, 835-843.
21. Economou, A., Pogliano, J.A., Beckwith, J., Oliver, D., and Wickner, W. (1995). SecA membrane cycling at SecYEG is driven by distinct ATP binding and hydrolysis events and is regulated by SecD and SecF. Cell 83, 1171-1181.
22. Eichler, J., and Wickner, W. (1997). Both an N-terminal 65 kDa domain and a C-terminal 30 kDa domain of SecA cycle into the membrane at SecYEG during translocation. Proc. Natl. Acad. Sci. USA 94, 5574-5578.
23. Eichler, J., Brunner, J., and Wickner, W. (1997). The protease-protected 30kDa domain of SecA is largely inaccessible to the membrane lipid phase. EMBO J. 16, 2188-2196.
24. Gannon, P.M., Li, P., and Kumamoto, C.A. (1989). The mature portion of Escherichia coli maltose-binding protein (MBP) determines the dependence of MBP on SecB for export. J. Bacteriol. 171, 813-818.
25. Guthrie, B., and Wickner, W. (1990). Trigger factor depletion or overproduction causes defective cell division but does not block protein export. J. Bacteriol. 172, 5555-5562.
26. Hardie, K.R., Lory, S., and Pugsley, A.P. (1996). Insertion of an outer membrane protein in Escherichia coli requires a chaperone-like protein. EMBO J. 15, 978-988.
27. Hardy, S.J.S., and Randall, L.L. (1991). A kinetic partitioning model of selective binding of nonnative proteins by the bacterial chaperone SecB. Science 251, 439-443.
28. Hartl, F.-U., Lecker, S., Schiebel, E., Hendrick, J.P., and Wickner, W. (1990). The binding of SecB to SecA to SecY/E mediates preprotein targeting to the E. coli membrane. Cell 63, 269-279.
29. Hendrick, J.P., and Wickner, W. (1991). SecA protein needs both acidic phospholipids and SecY/E protein for functional, high-affinity binding to the E. coli plasma membrane. J. Biol. Chem. 266, 24596-24600.
30. Hirst, T.R., and Holmgren, J. (1987). Conformation of protein secreted across bacterial outer membranes: a study of enterotoxin translocation from Vibrio cholerae. J. Bacteriol. 769, 1037-1045.
31. Joly, J.C., and Wickner, W. (1993). The SecA and SecY subunits of translocase are the nearest neighbors of a translocating preprotein, shielding it from phospholipids. EMBO J. 12, 255-263.
32. Kandror, O., Sherman, M., Rhode, M., and Goldberg, A.L. (1995) Trigger factor is involved in GroEL-dependent protein degradation in Escherichia coli and promotes binding of GroEL to unfolded proteins. EMBO J. 14, 6021-6027.
33. Kato, M., Tokuda, H., and Mizushima, S. (1992). In vitro translocation of secretory proteins posessing no charges at the mature domain takes place efficiently in a protonmotive force-dependent manner. J. Biol. Chem. 267, 413-418.
34. Kawasaki, S., Mizushima, S., and Tokuda, H. (1993). Membrane vesicles containing overproduced SecYand SecE exhibit high translocation ATPase activity and countermovement of protons in a SecA- and presecretory protein-dependent manner. J. Biol. Chem. 268, 8193-8198.
35. Kennedy, E.P. (1987). Membrane-derived oligosaccharides. In Escherichia coli and Salmonella typhimurium, J. L. Ingraham, B. Low, B. Magasanik, M. Schaechter, and H. E. Umbarger, eds. (Washington, D.C.: Am. Soc. Microbiol.).
36. Kim, Y.J., Rajapandi, T., and Oliver, D.B. (1994). SecA protein is exposed to the periplasmic surface of the E. coli inner membrane in its active state. Cell 78, 845-853.
37. Klauser, T., Pohlner, J., and Meyer, T.F. (1992). Selective extracellular release of cholera toxin B subunit by Escherichia coli: dissection of Neisseria IgAb-mediated outer membrane transport. EMBO J. 11, 2327-2335.
38. Koronakis, V., and Hughes, C. (1994). Secretion of hemolysin and other protiens out of the Gram-negative bacterial cell. In Bacterial Cell Wall, J.-M. Ghuysen and R. Hackenbeck, eds. (Elsevier: Amsterdam).
39. Lang, B.F., Burger, G., O'Kelly, C.J., Cedergren, R., Golding, G.B., Lemieux, C., Sankoff, D., Turmel, M., and Gray, M.W. (1997). An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature 387, 493-497.
40. Langley, K.E., and Kennedy, E.P. (1979). Energetics of rapid transmembrane movement and of compositional asymmetry of phosphatidylethanolamine in membranes of Bacillus megaterium. Proc. Natl. Acad. Sci. USA 76, 6245-6249.
41. Li, X., Henry, R., Yuan, J., Cline, K., and Hoffman, N.E. (1995). A chloroplast homologue of the signal recognition particle subunit SRP54 is involved in the posttranslational integration of a protein into thylakoid membranes. Proc. Natl. Acad. Sci. USA 92, 3789-3793.
42. Lill, R., Cunningham, K., Brundage, L., Ito, K., Oliver, D., and Wickner, W. (1989). The SecA protein hydrolyzes ATP and is an essential component of the protein translocation ATPase of E. coli. EMBO J. 8, 961-966.
43. Lill, R., Dowhan, W., and Wickner, W. (1990). The ATPase activity of SecA is regulated by acidic phospholipids, SecY, and the leader and mature domains of precursor proteins. Cell 60, 259-269.
44. Liu, G., Topping, T.B., and Randall, L.L. (1989). Physiological role during export for the retardation of folding by the leader peptide of maltose-binding protein. Proc. Natl. Acad. Sci. USA 86, 9213-9217.
45. Luirink, J., tenHagen-Jongman, C.M., van der Weijden, C.C., Oudega, B., High, S., Dobberstein, B., and Kusters, R. (1994). An alternative protein targeting pathway in Escherichia coli: studies on the role of FtsY. EMBO J. 13, 2289-2296.
46. MacIntyre, S., Freudl, R., Eschback, M.-L., and Henning, U. (1988) An artificial hydrophobic sequence functions as either an anchor or signal sequence at only one of two positions within the Escherichia coli outer membrane protein OmpA. J. Biol. Chem. 263, 19053-19059.
47. Majdalani, N., and Ippen-Ihler, K. (1996). Membrane insertion of the F-pilin subunit is Sec independent but requires leader peptidase B and the proton motive force. J. Bacteriol. 178, 3742-3747.
48. Missiakas, D., and Raina, S. (1997). Protein folding in the bacterial periplasm. J. Bacteriol. 179, 2465-2471.
49. Miller, J.D., Bernstein, H.D., and Walter, P. (1994). Interaction of E. coli Ffh/4.5S ribonucleoprotein and FtsY mimics that of mammalian signal recognition particle and its receptor. Nature 367, 657-659.
50. Mitchell, C., and Oliver, D. (1993). Two distinct ATP-binding domains are needed to promote protein export by Escherichia coli SecA ATPase. Mol. Microbiol. 10, 483-497.
51. Nishiyama, K.-i., Suzuki, T., and Tokuda, H. (1996). Inversion of the membrane topology of SecG coupled with SecA-dependent preprotein translocation. Cell 85, 71-81.
52. Norgren, M.,Baga, M.,Tennent, J.M., and Normark, S. (1987). Nucleotide sequence, regulation and functional analysis of the papC gene required for cell surface localization of Pap pili of uropathogenic Escherichia coli. Mol. Microbiol. 1, 169-178.
53. Oliver, D.B., and Beckwith, J. (1982). Regulation of a membrane component required for protein secretion in Escherichia coli. Cell 30, 311-319.
54. Panzner, S., Dreier, L., Hartmann, E., Kostka, S., and Rapoport, T.A. (1995). Posttranslational protein transport in yeast reconstituted with a purified complex of Sec proteins and Kar2p. Cell 81, 561-570.
55. Peek, J.A., and Taylor, R.K. (1992). Characterization of periplasmic thiol:disulfide interchange protein required for the functional maturation of secreted virulence factors of Vibrio cholerae. Proc. Natl. Acad. Sci. USA 89, 6210-6214.
56. Poritz, M.A., Bernstein, H.D., Stub, K., Zopf, D., Wilhelm, H., and Walter, P. (1990). An E. coli ribonucleoprotein containing 4.5S RNA resembles mammalian signal recognition particle. Science 250, 1111-1117.
57. Price, A., Economou, A., Duong, F., and Wickner, W. (1996) Separable ATPase and membrane insertion domains of the SecA subunit of preprotein translocase. J. Biol. Chem. 271, 31580-31584.
58. Prinz, W.A., Spiess, C., Ehrmann, M., Schierle, C., and Beckwith, J. (1996). Targeting of signal sequenceless proteins for export in Escherichia coli with altered protein translocase. EMBO J. 15, 5209-5217.
59. Pugsley, A.P. (1992). Translocation of a folded polypeptide across the outer membrane in Escherichia coli. Proc. Natl. Acad. Sci. USA 89, 12058-12062.
60. Pugsley, A.P. (1993). The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57, 50-108.
61. Raetz, C.R.H. (1993). Bacterial endotoxins: extraordinary lipids that activate eukaryotic signal transduction. J. Bacteriol. 175, 5745-5753.
62. Raetz, C.R.H., and Dowhan, W. (1990). Biosynthesis and function of phospholipids in Escherichia coli. J. Biol. Chem. 265, 1235-1238.
63. Ramamurthy, V., and Oliver, D. (1997). Topology of the integral membrane form of Escherichia coli SecA protein reveals multiple periplasmically exposed regions and modulation by ATP binding. J. Biol. Chem, 272, 23239-23246.
64. Randall, L.L., and Hardy, S.J.S. (1989). Unity in function in the absence of consensus in sequence: role of leader peptides in export. Science 243, 1156-1159.
65. Randall, L.L., Topping, T.B., and Hardy, S.J.S. (1994). The basis of recognition of non-native structure by the chaperone SecB. In The Biology of Heat Shock Proteins and Molecular Chaperones (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press), pp. 285-298.
66. Rohrer, J., and Kuhn, A. (1990). The function of a leader peptide in translocating charged amino acyl residues across a membrane. Science 250, 1418-1421.
67. Rothman, J.E., and Kennedy, E.P. (1977). Rapid transmembrane movement of newly synthesized phospholipids during membrane assembly. Proc. Natl. Acad. Sci. USA 74, 1821-1825.
68. H+ and ATP function at different steps of the catalytic cycle of preprotein translocase. Cell 64, 927-939.
69. Schneider, E., Hunke, S., and Tebbe, S. (1995). The MalK protein of the ATP-binding cassette transporter for maltose of Escherichia coli is accessible to protease digestion from the periplasmic side of the membrane. J. Bacteriol. 177, 5364-5367.
70. Seluanov, A., and Bibi, E. (1997). FtsY, the prokaryotic signal recognition particle receptor homolog, is essential for biogenesis of membrane proteins. J. Biol. Chem. 272, 2053-2055.
71. Shinkai, A., Mei, L.H., Tokuda, H., and Mizushima, S. (1991). The conformation of SecA, as revealed by its protease sensitivity, is altered upon interaction with ATP, presecretory proteins, everted membrane vesicles, and phospholipids. J. Biol. Chem. 266, 5827-5833.
72. Stirling, C.J., Rothblatt, J., Hosobuchi, M., Deshaies, R., and Schekman, R. (1992). Protein translocation mutants defective in the insertion of integral membrane proteins into the endoplasmic reticulum. Mol. Biol. Cell 3, 129-142.
73. Stoller, G., Rucknagel, K.P., Nierhaus, K.H., Schmid, F.X., Fischer, G., and Rahfeld, J.-U. (1995). A ribosome-associated peptidyl-prolyl cis/trans isomerase identified as the trigger factor. EMBO J. 14, 4939-4948.
74. Summers, R.G., Harris, C.R., and Knowles, J.R. (1989). A conservative amino acid substitution, arginine for lysine, abolishes export of a hybrid protein in Escherichia coli. Implications for the mechanism of protein export. J. Biol. Chem. 264, 20082-20088.
75. Tommassen, J., van Tol, H., and Lugtenberg, B. (1983). The ultimate localization of an outer membrane protein of Escherichia coli K-12 is not determined by the signal sequence. EMBO J. 2, 1275-1279.
76. Ulbrandt, N.D., London, E., and Oliver, D.B. (1992). Deep penetration of a portion of Escherichia coli SecA protein into model membranes is promoted by anionic lipids and by partial unfolding. J. Biol. Chem. 267, 15184-15192.
77. Ulbrandt, N.D., Newitt, J.A., and Bernstein, H.D. (1997). The E. coli signal recognition particle is required for the insertion of a subset of inner membrane proteins. Cell 88, 187-196.
78. Valent, Q.A., Kendall, D.A., High, S., Kusters, R., Oudega, B., and Luirink, J. (1995). Early events in preprotein recognition in E. coli: interaction of SRP and trigger factor with nascent polypeptides. EMBO J. 14, 5494-5505.
79. van der Does, C., den Blaauwen, T., de Wit, J.G., Manting, E.H., Groot, N.A., Fekkes, P., and Driessen, A.J.M. (1996). SecA is an intrinsic subunit of the Escherichia coli preprotein translocase and exposes its carboxyl terminus to the periplasm. Mol. Microbiol. 22, 619-629.
80. von Heijne, G. (1989). Control of topology and mode of assembly of a polytopic membrane protein by positively charged residues. Nature 341, 456-458.
81. Whitley, P., Gafvelin, G., and von Heijne, G. (1995) SecA-independent translocation of the periplasmic N-terminal tail of an Escherichia coli inner membrane protein. J. Biol. Chem. 270, 29831-29835.
82. Wickner, W. (1988). Mechanisms of membrane assembly: general lessons from the study of M13 coat protein and Escherichia coli leader peptidase. Biochemistry 27, 1081-1086.
83. 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.
84. Yang, Y.-B., Yu, N., and Tai, P.C. (1997). SecE-depleted membranes of Escherichia coli are active. SecE is not obligatorily required for the in vitro translocation of certain precursor proteins. J. Biol. Chem. 272, 13660-13665.