The biogenesis and assembly of bacterial membrane proteins

Current Opinion in Microbiology

Volumn 3, Issue 2, 2000, Pages 203-209

  Bernstein, Harris D ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CHAPERONIN; MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN; POLYPEPTIDE;

BACTERIAL MEMBRANE; BACTERIAL OUTER MEMBRANE; BIOGENESIS; ESCHERICHIA COLI; MEMBRANE TRANSPORT; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN FOLDING; REVIEW;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 0034076007     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1369-5274(00)00076-X     Document Type: Review

References (69)

1. Kumamoto C.A., Beckwith J. Evidence for specificity at an early step in protein export in Escherichia coli. J Bacteriol. 163:1985;267-274.
2. Collier D.N., Bankaitis V.A., Weiss J.B., Bassford P.J. Jr. The antifolding activity of SecB promotes the export of the E. coli maltose-binding protein. Cell. 53:1988;273-283.
3. Gannon P.M., Li P., Kumamoto C.A. The mature portion of Escherichia coli maltose-binding protein (MBP) determines the dependence of MBP on SecB for export. J Bacteriol. 171:1989;813-818.
4. Lee C., Beckwith J. Cotranslational and posttranslational protein translocation in prokaryotic systems. Ann Rev Cell Biol. 2:1986;315-336.
5. de Gier J-W.L., Mansournia P., Valent Q.A., Phillips G.J., Luirink J., von Heijne G. Assembly of a cytoplasmic membrane protein in Escherichia coli is dependent on the signal recognition particle. FEBS Letters. 399:1996;307-309.
6. Seluanov A., Bibi E. FtsY, the prokaryotic signal recognition particle receptor homologue, is essential for biogenesis of membrane proteins. J Biol Chem. 272:1997;2053-2055.
7. Ulbrandt N.D., Newitt J.A., Bernstein H.D. The E. coli signal recognition particle is required for the insertion of a subset of inner membrane proteins. Cell. 88:1997;187-196.
8. Valent Q.A., Scotti P.A., High S., deGier J-W.L., von Heijne G., Lentzen G., Wintermeyer W., Oudega B., Luirink J. The Escherichia coli SRP and SecB targeting pathways converge at the translocon. EMBO J. 17:1998;2504-2512. Short nascent inner membrane proteins (IMPs) bound to SRP were shown to be transferred to components of the translocon in the presence of FtsY and GTP by UV cross-linking analysis. This study showed that a key step in the SRP targeting reaction, namely the release of nascent chains and their insertion into the translocon, is evolutionarily conserved.
9. Koch H-G., Hengelage T., Neumann-Haefelin C., MacFarlane J., Hoffschulte H.K., Schimz K-L., Mechler B., Müller M. In vitro studies with purified components reveal signal recognition particle (SRP) and SecA/SecB as constituents of two independent protein-targeting pathways of Escherichia coli. Mol Biol Cell. 10:1999;2163-2173. The insertion of inner membrane proteins (IMPs) into membrane vesicles was shown to be dependent on purified SRP and SRP receptor in a biochemical assay. Although several previous studies had shown that disruption of the SRP pathway blocks the membrane insertion of IMPs in vivo, this paper contained the first demonstration that SRP plays a direct role in the insertion process. Evidence that SRP substrates are delivered to the SecY complex was also presented.
10. Walter P., Johnson A.E. Signal sequence recognition and protein targeting to the endoplasmic reticulum membrane. Ann Rev Cell Biol. 10:1994;87-119.
11. Görlich D., Prehn S., Hartmann E., Kalies K.U., Rapoport T.A. A mammalian homolog of SEC61p and SECYp is associated with ribosomes and nascent polypeptides during translocation. Cell. 71:1992;489-503.
12. Brown S. Mutations in the gene for EF-G reduce the requirement for 4.5S RNA in the growth of E. coli. Cell. 49:1987;825-833.
13. Valent Q.A., Kendall D.A., High S., Kusters R., Oudega B., Luirink J. Early events in preprotein recognition in E. coli: interaction of SRP and trigger factor with nascent polypeptides. EMBO J. 14:1995;5494-5505.
14. de Gier J-W.L., Scotti P.A., Sääf A., Valent Q.A., Kuhn A., Luirink J., von Heijne G. Differential use of the signal recognition particle translocase targeting pathway for inner membrane protein assembly in Escherichia coli. Proc Natl Acad Sci USA. 95:1998;14646-14651. The membrane insertion of the bacteriophage M13 procoat protein was rendered both SecY and SRP-dependent by greatly increasing the hydrophobicity of its signal sequence. This study provides important evidence that factors that increase the propensity of an inner membrane protein to aggregate in the cytoplasm also increase its dependence on SRP and the Sec machinery. The results also imply that the hydrophobicity of targeting signals provides the basis for SRP recognition in vivo.
15. Beck K., Wu L-F., Brunner J., Müller M. Discrimination between SRP- and SecA/SecB-dependent substrates involves selective recognition of nascent chains by SRP and trigger factor. EMBO J. 19:2000;134-143. Using a chemical and UV-crosslinking approach, SRP was shown to interact with the first transmembrane segment of mannitol permease. By contrast, short pro-OmpA nascent chains interacted primarily with trigger factor. After depletion of trigger factor, however, an interaction between SRP and pro-OmpA could be observed. Although the generality and physiological significance of the data need to be investigated, these experiments present a plausible explanation for the partitioning of inner membrane proteins and presecretory proteins into two different targeting pathways and suggest that under some conditions presecretory proteins might be targeted by SRP.
16. Newitt J.A., Ulbrandt N.D., Bernstein H.D. The structure of multiple polypeptide domains determines the signal recognition particle targeting requirement of Escherichia coli inner membrane proteins. J Bacteriol. 181:1999;4561-4567. The insertion of a subset of bitopic inner membrane proteins (IMPs) was observed to be SRP-independent, and the insertion of a polytopic IMP was observed to be only partially SRP-dependent. This study suggests that although the hydrophobicity of targeting signals normally routes proteins into the SRP pathway, the sequence or structure of both hydrophobic and hydrophilic domains determines the degree to which insertion occurs in the absence of SRP.
17. Scotti P.A., Valent Q.A., Manting E.H., Urbanus M.L., Driessen A.J.M., Oudega B., Luirink J. SecA is not required for signal recognition particle-mediated targeting and initial membrane insertion of a nascent inner membrane protein. J Biol Chem. 274:1999;29883-29888.
18. Meyer T.H., Ménéret J-F., Breitling R., Miller K.R., Akey C.W., Rapoport T.A. The bacterial SecY/E translocation complex forms channel-like structures similar to those of the eukaryotic Sec61p complex. J Mol Biol. 285:1999;1789-1800. A SecY/E complex was purified from B. subtilis and shown to be active in a protein translocation assay when reconstituted into proteoliposomes. Electron microscopy demonstrated that SecY/E forms quasi-pentagonal oligomeric ring structures in detergent solution and in proteoliposomes. The size and shape of the particles are similar to those formed by yeast and mammalian Sec61p complexes. In addition to providing strong evidence that the structure of the translocon is evolutionarily conserved, this study showed that the SecG subunit, which is not absolutely essential for protein translocation in E. coli, is also not required for ring formation.
19. Pohlschroder M., Prinz W.A., Hartmann E., Beckwith J. Protein translocation in the three domains of life: variations on a theme. Cell. 91:1997;563-566.
20. Emr S.D., Hanley-Way S., Silhavy T.J. Suppressor mutations that restore export of a protein with a defective signal sequence. Cell. 23:1981;79-88.
21. Jungnickel B., Rapoport T.A. A posttargeting signal sequence recognition event in the endoplasmic reticulum membrane. Cell. 82:1995;261-270.
22. Belin D., Bost S., Vassalli J.D., Strub K. A two-step recognition of signal sequences determines the translocation efficiency of proteins. EMBO J. 15:1996;468-478.
23. Flower A.M., Osborne R.S., Silhavy T.J. The allele-specific synthetic lethality of prlA-prlG double mutants predicts interactive domains of SecY and SecE. EMBO J. 14:1995;884-893.
24. ••]).
25. Plath K., Mothes W., Wilkinson B.M., Stirling C.J., Rapoport T.A. Signal sequence recognition in posttranslational transport across the yeast ER membrane. Cell. 94:1998;795-807. Using an elegant combination of UV crosslinking, site-directed mutagenesis and site-specific proteolysis, the authors obtained a detailed map of the signal-sequence-binding pocket of yeast Sec61α. In addition to suggesting a general mechanism by which signal sequences and transmembrane segments open the translocon to permit polypeptide transport, the results also suggested how prl mutations might promote the translocation of proteins containing defective signal sequences.
26. Martoglio B., Hofmann M.W., Brunner J., Dobberstein B. The protein-conducting channel in the membrane of the endoplasmic reticulum is open laterally toward the lipid bilayer. Cell. 81:1995;207-214.
27. Mothes W., Heinrich S.U., Graf R., Nilsson I., von Heijne G., Brunner J., Rapoport T.A. Molecular mechanism of membrane protein integration into the endoplasmic reticulum. Cell. 89:1997;523-533.
28. Newitt J.A., Bernstein H.D. A mutation in the Escherichia coli secY gene that produces distinct effects on inner membrane protein insertion and protein export. J Biol Chem. 273:1998;12451-12456.
29. Wickner W., Leonard M.R. Escherichia coli preprotein translocase. J Biol Chem. 271:1996;29514-29516.
30. Qi H-Y., Bernstein H.D. SecA is required for the insertion of inner membrane proteins targeted by the Escherichia coli signal recognition particle. J Biol Chem. 274:1999;8993-8997.
31. Crowley K.S., Reinhart G.D., Johnson A.E. The signal sequence moves through a ribosomal tunnel into a noncytoplasmic aqueous environment at the ER membrane early in translocation. Cell. 73:1993;1101-1115.
32. von Heijne G. Control of topology and mode of assembly of a polytopic membrane protein by positively charged residues. Nature. 341:1989;456-458.
33. Kiefer D., Hu X., Dalbey R., Kuhn A. Negatively charged amino acid residues play an active role in orienting the Sec-independent Pf3 coat protein in the Escherichia coli inner membrane. EMBO J. 16:1997;2197-2204.
34. Kiefer D., Kuhn A. Hydrophobic forces drive spontaneous membrane insertion of the bacteriophage Pf3 coat protein without topological control. EMBO J. 18:1999;6299-6306. In this paper and [33], the membrane insertion of the 44 amino acid Pf3 coat protein was shown to be dependent on the membrane potential both in vivo and in vitro. Topology appeared to be generated by an electrophoretic mechanism in which negatively charged residues that flank the transmembrane segment (TMS) are transported across the inner membrane (IM). A strong influence of negatively charged residues was observed only when the hydrophobicity of the TMS was limited. When the hydrophobicity of the TMS was increased, the topology of the protein was controlled by positively charged residues which remained anchored in the cytoplasm by electrostatic attraction to acidic lipids. These studies on a simple model protein may provide important insights into the factors that influence the orientation of all IM proteins.
35. Ehrmann M., Beckwith J. Proper insertion of a complex membrane protein in the absence of its amino-terminal export signal. J Biol Chem. 266:1991;16530-16533.
36. Bibi E., Stearns S.M., Kaback H.R. The N-terminal 22 amino acid residues in the lactose permease of Escherchia coli are not obligatory for membrane insertion or transport activity. Proc Natl Acad Sci USA. 89:1992;3180-3184.
37. Bibi E., Verner G., Chang C-Y., Kaback H.R. Organization and stability of a polytopic membrane protein: deletion analysis of the lactose permease of Escherichia coli. Proc Natl Acad Sci USA. 88:1991;7271-7275.
38. McGovern K., Ehrmann M., Beckwith J. Decoding signals for membrane protein assembly using alkaline phosphatase fusions. EMBO J. 10:1991;2773-2782.
39. Gafvelin G., von Heijne G. Topological 'frustration' in multispanning E. coli inner membrane proteins. Cell. 77:1994;401-412.
40. Spiess M. Heads or tails - what determines the orientation of proteins in the membrane. FEBS Letters. 369:1995;76-79.
41. Kimbrough T.G., Manoil C. Role of a small cytoplasmic domain in the establishment of serine chemoreceptor membrane topology. J Bacteriol. 176:1994;7718-7720.
42. Lee J.I., Hwang P.P., Hansen C., Wilson T.H. Possible salt bridges between transmembrane alpha-helices of the lactose carrier of Escherichia coli. J Biol Chem. 267:1992;20758-20764.
43. Prinz W.A., Boyd D.H., Ehrmann M., Beckwith J. The protein translocation apparatus contributes to determining the topology of an integral membrane protein in Escherichia coli. J Biol Chem. 273:1998;8419-8424. The alkaline phosphatase moiety of two different MalF-alkaline phosphatase fusion proteins was shown to be cytoplasmic in wild-type cells but periplasmic in cells containing the prlA4 mutation. These results provide strong evidence that the translocon can influence the topology of at least some inner membrane proteins.
44. Bibi E., Kaback H.R. In vivo expression of the lacY gene in two segments leads to functional lac permease. Proc Natl Acad Sci USA. 87:1990;4325-4329.
45. Kaback H.R. The lactose permease of Escherichia coli: past, present, and future. Konings W.N., Kaback H.R., Lolkema J.S. Handbook of Biological Physics: Transport Processes in Eukaryotic and Prokaryotic Organisms, vol. II. 1996;203-227 Elsevier, Amsterdam.
46. Wen J., Chen X., Bowie J.U. Exploring the allowed sequence space of a membrane protein. Nat Struct Biol. 3:1996;141-148.
47. McKenna E., Hardy D., Kaback H.R. Evidence that the final turn of the last transmembrane helix in the lactose permease is required for folding. J Biol Chem. 267:1992;6471-6474.
48. Braun P., Persson B., Kaback H.R., von Heijne G. Alanine insertion scanning mutagenesis of lactose permease transmembrane helices. J Biol Chem. 272:1997;29566-29571.
49. Bogdanov M., Sun J., Kaback H.R., Dowhan W. A phospholipid acts as a chaperone in assembly of a membrane transport protein. J Biol Chem. 271:1996;11615-11618.
50. Bogdanov M., Dowhan W. Phospholipid-assisted protein folding: phosphatidylethanolamine is required at a late step of the conformational maturation of the polytopic protein lactose permease. EMBO J. 17:1998;5255-5264. Using a coupled translation-membrane insertion assay, the proper folding of LacY was shown to be separable from its incorporation into inverted membrane vesicles. Either co- or post-translational synthesis of phosphatidylethanolamine (PE) in PE-deficient vesicles corrected a specific LacY folding defect. Analysis of LacY from PE-containing cells showed that the protein could be purified away from PE and still retain its native structure. Taken together with previous results (see [49]), these data strongly suggest that PE assists the folding of LacY via a transient non-covalent interaction.
51. Nikaido H. Outer membrane. Neidhardt F.C. Escherichia coli and Salmonella: Cellular and Molecular Biology. 1996;29-47 ASM Press, Washington, DC.
52. Eppens E.F., Nouwen N., Tommassen J. Folding of a bacterial outer membrane protein during passage through the periplasm. EMBO J. 16:1997;4295-4301.
53. Chen R., Henning U. A periplasmic protein (Skp) of Escherichia coli selectively binds a class of outer membrane proteins. Mol Microbiol. 19:1996;1287-1294.
54. Schäfer U., Beck K., Müller M. Skp, a molecular chaperone of Gram negative bacteria, is required for the formation of soluble periplasmic intermediates of outer membrane proteins. J Biol Chem. 274:1999;24567-24574. Pro-OmpA synthesized in a cell-free system was shown to interact with Skp on the periplasmic side of inverted membrane vesicles in UV cross-linking experiments. Moreover, OmpA (but not the periplasmic protein MalE) was released very slowly from the inner membrane in a skp null strain and appeared to aggregate in the periplasm of cells deficient in both Skp and DegP. These experiments provide significant evidence that Skp plays a direct role in the biogenesis of outer membrane proteins.
55. de Cock H., Schäfer U., Potgeter M., Demel R., Müller M., Tommassen J. Affinity of the periplasmic chaperone Skp of Escherichia coli for phospholipids, lipopolysaccharides and non-native outer membrane proteins. Eur J Biochem. 259:1999;96-103.
56. Missiakis D., Betton J-M., Raina S. New components of protein folding in extracytoplasmic compartments of Escherichia coli SurA, FkpA, and Skp/OmpH. Mol Microbiol. 21:1996;871-884.
57. Lazar S.W., Kolter R. SurA assists the folding of Escherichia coli outer membrane proteins. J Bacteriol. 178:1996;1770-1773.
58. Rouvière P.E., Gross C.A. SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins. Genes Dev. 10:1996;3170-3182.
59. Dartigalongue C., Raina S. A new heat-shock gene, ppiD, encodes a peptidyl-prolyl isomerase required for folding of outer membrane proteins in Escherichia coli. EMBO J. 17:1998;3968-3980. PpiD was isolated as a multi-copy suppressor of a surA null mutation and shown to restore the normal assembly of outer membrane proteins (OMPs). Purified PpiD protein was demonstrated to have peptidyl-prolyl isomerase activity. Besides identifying a potentially novel OMP-specific chaperone, this study also provided evidence that expression of ppiD is regulated by a unique mechanism.
60. Spiess C., Beil A., Ehrmann M. A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell. 97:1999;339-347. Although the activity of the oxidoreductase DsbA is normally required for the proper folding of the periplasmic protein MalS, a substantial level of native MalS was observed in cells containing a dsbA null mutation at low temperature. Native MalS was not observed, however, in cells that lack DegP, a protease that degrades misfolded MalS in the periplasm at high temperature. Both wild-type DegP and a proteolytically inactive variant were shown to promote refolding of denatured MalS in vitro. These experiments provide the first evidence that a single protein can act as both a protease and a chaperone. Given evidence that both outer membrane proteins (OMPs) and periplasmic proteins are substrates for DegP, these data raise the intriguing possibility that DegP might facilitate OMP assembly under some physiological conditions.
61. Surrey T., Jähnig F. Refolding and oriented insertion of a membrane protein into a lipid bilayer. Proc Natl Acad Sci USA. 89:1992;7457-7461.
62. Sen K., Nikaido H. In vitro trimerization of OmpF porin secreted by spheroplasts of Escherichia coli. Proc Natl Acad Sci USA. 87:1990;743-747.
63. Freund R., Schwarz H., Stierhof Y-D., Gamon K., Hindennach I., Henning U. An outer membrane protein (OmpA) of Escherichia coli K-12 undergoes a conformational change during export. J Biol Chem. 261:1986;11355-11361.
64. Koebnik R. Structural and functional roles of the surface-exposed loops of the β-barrel membrane protein OmpA from Escherichia coli. J Bacteriol. 181:1999;3688-3694.
65. Koebnik R. In vivo membrane assembly of split variants of the E. coli outer membrane protein OmpA. EMBO J. 15:1996;3529-3537.
66. Koebnik R. Membrane assembly of the Escherichia coli outer membrane protein OmpA: exploring sequence constraints on transmembrane β-strands. J Mol Biol. 285:1999;1801-1810. Amino acid sequences of OmpA β-strands 4, 6 and 8 were randomized and the assembly of a large number of mutant proteins was assessed in vivo. By analyzing the types of amino acid substitutions that were tolerated, important insights into the principles that govern the folding of a model outer membrane protein β-barrel were obtained.
67. Bosch D., Leunissen J., Verbakel J., de Jong M., van Erp H., Tommassen J. Periplasmic accumulation of truncated forms of outer-membrane PhoE protein of Escherichia coli K-12. J Mol Biol. 189:1986;449-455.
68. Charbit A., Ronco J., Michel V., Werts C., Hofnung M. Permissive sites and topology of an outer membrane protein with a reporter epitope. J Bacteriol. 173:1991;262-275.
69. Scotti P.A., Urbanus M.L., Brunner J., deGier J-W.L., von Heijne G., van der Does C., Driessen A.J.M., Oudega B., Luirink J. YidC, the Escherichia coli homologue of mitochondrial Oxa7p, is a component of the Sec translocase. EMBO J. 19:2000;542-549. UV-crosslinking experiments show that the TMS of a nascent inner membrane protein is in proximity to a novel translocon-associated protein, YidC, during the membrane insertion process.