Periplasmic export machines for outer membrane assembly

Current Opinion in Structural Biology

Volumn 18, Issue 4, 2008, Pages 466-474

  Whitfield, Chris ^a   Naismith, James H ^b  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOCONJUGATE; LIPOPOLYSACCHARIDE; LIPOPROTEIN; MOLECULAR SCAFFOLD; OUTER MEMBRANE PROTEIN; POLYSACCHARIDE;

CELL ENVELOPE; CELL PROTECTION; CELL STRUCTURE; IMMUNE RESPONSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN STRUCTURE; REVIEW; STRUCTURE ANALYSIS;

BACTERIAL OUTER MEMBRANE PROTEINS; GRAM-NEGATIVE BACTERIA; LIPOPOLYSACCHARIDES; LIPOPROTEINS; MODELS, MOLECULAR; PERIPLASM; PROTEIN CONFORMATION; PROTEIN FOLDING;

NEGIBACTERIA;

EID: 49549110489     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2008.04.001     Document Type: Review

References (68)

1. Nikaido H. Molecular basis of bacterial outer membrane permeability revisited. Micr Mol Biol Rev 67 (2003) 593-656
2. Schulz G.E. The structure of bacterial outer membrane proteins. Biochim Biophys Acta 1565 (2002) 308-317
3. Whitfield C. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Ann Rev Biochem 75 (2006) 39-68. A review describing the state of the art in capsule biosynthesis, focusing on paradigms from E. coli prototypes.
4. Ruiz N., Kahne D., and Silhavy T.J. Advances in understanding bacterial outer-membrane biogenesis. Nat Rev Microbiol 4 (2006) 57-66
5. Bos M.P., Robert V., and Tommassen J. Biogenesis of the gram-negative bacterial outer membrane. Ann Rev Biochem 61 (2007) 191-214. Detailed review of the state of the art in outer membrane assembly.
6. Gold V.A., Duong F., and Collinson I. Structure and function of the bacterial Sec translocon. Mol Membr Biol 24 (2007) 387-394
7. Mogensen J.E., and Otzen D.E. Interactions between folding factors and bacterial outer membrane proteins. Mol Microbiol 57 (2005) 326-346
8. Wu T., Malinverni J., Ruiz N., Kim S., Silhavy T.J., and Kahne D. Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121 (2005) 235-245. The existence of a multiprotein complex containing YaeT and the lipoproteins YfiO, NlpB, and YfgL is established by elegant genetic and biochemical approaches. Genetic data assigns an intriguing role for YfgL in homeostasis of outer membrane assembly, coordinating outer membrane protein and LPS assembly.
9. Xu X., Wang S., Hu Y.X., and McKay D.B. The periplasmic bacterial molecular chaperone SurA adapts its structure to bind peptides in different conformations to assert a sequence preference for aromatic residues. J Mol Biol 373 (2007) 367-381
10. Sklar J.G., Wu T., Kahne D., and Silhavy T.J. Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli. Genes Dev 21 (2007) 2473-2484. Describes a depletion strategy to assess the roles and relationships of a chaperone proteins in the assembly of outer membrane proteins. Identifies SurA as the major chaperone.
11. Korndorfer I.P., Dommel M.K., and Skerra A. Structure of the periplasmic chaperone Skp suggests functional similarity with cytosolic chaperones despite differing architecture. Nat Struct Mol Biol 11 (2004) 1015-1020
12. Walton T.A., and Sousa M.C. Crystal structure of Skp, a prefoldin-like chaperone that protects soluble and membrane proteins from aggregation. Mol Cell 15 (2004) 367-374
13. Bulieris P.V., Behrens S., Holst O., and Kleinschmidt J.H. Folding and insertion of the outer membrane protein OmpA is assisted by the chaperone Skp and by lipopolysaccharide. J Biol Chem 278 (2003) 9092-9099
14. Qu J., Mayer C., Behrens S., Holst O., and Kleinschmidt J.H. The trimeric periplasmic chaperone Skp of Escherichia coli forms 1:1 complexes with outer membrane proteins via hydrophobic and electrostatic interactions. J Mol Biol 374 (2007) 91-105
15. Sklar J.G., Wu T., Gronenberg L.S., Malinverni J.C., Kahne D., and Silhavy T.J. Lipoprotein SmpA is a component of the YaeT complex that assembles outer membrane proteins in Escherichia coli. Proc Natl Acad Sci U S A 104 (2007) 6400-6405
16. Stegmeier J.F., and Andersen C. Characterization of pores formed by YaeT (Omp85) from Escherichia coli. J Biochem 140 (2006) 275-283
17. Kim S., Malinverni J.C., Sliz P., Silhavy T.J., Harrison S.C., and Kahne D. Structure and function of an essential component of the outer membrane protein assembly machine. Science 317 (2007) 961-964. The structure of the periplasmic domain of YaeT and its POTRA-domain fold is described. This paper proposes a model for the function of YaeT and the multiprotein complex it resides in. A dimer, thought to be a crystallographic artefact provides insight into a possible β-strand augmentation principle for interaction with export substrate proteins.
18. Bos M.P., Robert V., and Tommassen J. Functioning of outer membrane protein assembly factor Omp85 requires a single POTRA domain. EMBO Rep 8 (2007) 1149-1154
19. Robert V., Volokhina E.B., Senf F., Bos M.P., Van Gelder P., and Tommassen J. Assembly factor Omp85 recognizes its outer membrane protein substrates by a species-specific C-terminal motif. PLoS Biol 4 (2006) e377. In vitro reconstitution of the interaction between YaeT and a substrate β-barrel protein. Begins to establish the principles involved in YaeT recognition of its substrates.
20. Werner J., and Misra R. YaeT (Omp85) affects the assembly of lipid-dependent and lipid-independent outer membrane proteins of Escherichia coli. Mol Microbiol 57 (2005) 1450-1459
21. Koronakis V., Sharff A., Koronakis E., Luisi B., and Hughes C. Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 405 (2000) 914-919
22. Tommassen J. Biochemistry. Getting into and through the outer membrane. Science 317 (2007) 903-904
23. Tokuda H., and Matsuyama S. Sorting of lipoproteins to the outer membrane in E. coli. Biochim Biophys Acta 1694 (2004) IN1-9
24. Miyamoto S., and Tokuda H. Diverse effects of phospholipids on lipoprotein sorting and ATP hydrolysis by the ABC transporter LolCDE complex. Biochim Biophys Acta 1768 (2007) 1848-1854
25. Narita S., and Tokuda H. An ABC transporter mediating the membrane detachment of bacterial lipoproteins depending on their sorting signals. FEBS Lett 580 (2006) 1164-1170
26. Taniguchi N., Matsuyama S., and Tokuda H. Mechanisms underlying energy-independent transfer of lipoproteins from LolA to LolB, which have similar unclosed β-barrel structures. J Biol Chem 280 (2005) 34481-34488
27. Tefsen B., Geurtsen J., Beckers F., Tommassen J., and de Cock H. Lipopolysaccharide transport to the bacterial outer membrane in spheroplasts. J Biol Chem 280 (2005) 4504-4509
28. Mühlradt P.F., Menzel J., Golecki J.R., and Speth V. Outer membrane of Salmonella. Sites of export of newly synthesized lipopolysaccharide on the bacterial surface. Eur J Biochem 35 (1973) 471-481
29. Kellenberger E. The 'Bayer bridges' confronted with results from improved electron microscopy methods. Mol Microbiol 4 (1990) 697-705
30. Bayer M.E. Zones of membrane adhesion in the cryofixed envelope of Escherichia coli. J Struct Biol 107 (1991) 268-280
31. Ghosh A.S., and Young K.D. Helical disposition of proteins and lipopolysaccharide in the outer membrane of Escherichia coli. J Bacteriol 187 (2005) 1913-1922. Identifies a helical pattern of LPS insertion sites on the surface of E. coli and discusses the issues associated with lateral diffusion of large macromolecuales in the outer membrane.
32. Braun M., and Silhavy T.J. Imp/OstA is required for cell envelope biogenesis in Escherichia coli. Mol Microbiol 45 (2002) 1289-1302
33. Bos M.P., Tefsen B., Geurtsen J., and Tommassen J. Identification of an outer membrane protein required for the transport of lipopolysaccharide to the bacterial cell surface. Proc Natl Acad Sci U S A 101 (2004) 9417-9422. By exploiting the unusual ability of N. meningitidis to survive without LPS biosynthesis, the authors provide the first direct evidence that Imp is involved in the assembly of LPS in the outer membrane. Imp is the first component of the LPS assembly pathway to be defined.
34. Wu T., McCandlish A.C., Gronenberg L.S., Chng S.S., Silhavy T.J., and Kahne D. Identification of a protein complex that assembles lipopolysaccharide in the outer membrane of Escherichia coli. Proc Natl Acad Sci U S A 103 (2006) 11754-11759. Describes the involvement of an outer membrane lipoprotein, RlpB, in the assembly of LPS and its interactions with Imp. The parallels to the YaeT/YfiO/NlpB/SmpA/YfgL complex for outer membrane protein assembly are striking.
35. Sperandeo P., Cescutti R., Villa R., Di Benedetto C., Candia D., Deho G., and Polissi A. Characterization of lptA and lptB, two essential genes implicated in lipopolysaccharide transport to the outer membrane of Escherichia coli. J Bacteriol 189 (2007) 244-253
36. Drummelsmith J., and Whitfield C. Translocation of group 1 capsular polysaccharide to the surface of Escherichia coli (O9a:K30) requires a multimeric complex in the outer membrane. EMBO J 19 (2000) 57-66
37. Nesper J., Hill C.M., Paiment A., Harauz G., Beis K., Naismith J.H., and Whitfield C. Translocation of group 1 capsular polysaccharide in Escherichia coli serotype K30. Structural and functional analysis of the outer membrane lipoprotein Wza. J Biol Chem 278 (2003) 49763-49772
38. Morona R., Van Den Bosch L., and Daniels C. Evaluation of Wzz/MPA1/MPA2 proteins based on the presence of coiled-coil regions. Microbiology 146 (2000) 1-4
39. Drummelsmith J., and Whitfield C. Gene products required for surface expression of the capsular form of the group 1 K antigen in Escherichia coli (O9a:K30). Mol Microbiol 31 (1999) 1321-1332
40. Wugeditsch T., Paiment A., Hocking J., Drummelsmith J., Forrester C., and Whitfield C. Phosphorylation of Wzc, a tyrosine autokinase, is essential for assembly of group 1 capsular polysaccharides in Escherichia coli. J Biol Chem 276 (2001) 2361-2371
41. Paulsen I.T., Beness A.M., and Saier M.H.J. Computer-based analyses of the protein constituents of transport systems catalysing export of complex carbohydrates in bacteria. Microbiology 143 (1997) 2685-2699
42. Beis K., Collins R.F., Ford R.C., Kamis A.B., Whitfield C., and Naismith J.H. Three-dimensional structure of Wza, the protein required for translocation of group 1 capsular polysaccharide across the outer membrane of Escherichia coli. J Biol Chem 279 (2004) 28227-28732
43. Dong C., Beis K., Nesper J., Brunkan-Lamontagne A.L., Clarke B.R., Whitfield C., and Naismith J.H. Wza the translocon for E. coli capsular polysaccharides defines a new class of membrane protein. Nature 444 (2006) 226-229. This paper reports the first crystal structure of an OMA protein and provides insight into possible mechanisms for the export of capsular polysaccharide. Wza is the only outer membrane protein reported to date that contains an α-helical outer membrane channel.
44. Collins R.F., and Derrick J.P. Wza: a new structural paradigm for outer membrane secretory proteins?. Trends Microbiol 15 (2007) 96-100
45. Collin S., Guilvout I., Chami M., and Pugsley A.P. YaeT-independent multimerization and outer membrane association of secretin PulD. Mol Microbiol 64 (2007) 1350-1357
46. Guilvout I., Chami M., Engel A., Pugsley A.P., and Bayan N. Bacterial outer membrane secretin PulD assembles and inserts into the inner membrane in the absence of its pilotin. EMBO J 25 (2006) 5241-5249
47. Voulhoux R., Bos M.P., Geurtsen J., Mols M., and Tommassen J. Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299 (2003) 262-265
48. Carbonnelle E., Helaine S., Prouvensier L., Nassif X., and Pelicic V. Type IV pilus biogenesis in Neisseria meningitidis: PilW is involved in a step occurring after pilus assembly, essential for fibre stability and function. Mol Microbiol 55 (2005) 54-64
49. Grangeasse C., Cozzone A.J., Deutscher J., and Mijakovic I. Tyrosine phosphorylation: an emerging regulatory device of bacterial physiology. Trends Biochem Sci 32 (2007) 86-94. One subfamily of PCP proteins involved in capsule assembly in Gram-negative and Gram-positive bacteria contains novel tyrosine autokinase activities. This review provides a detailed overview of the structures and diverse functions of these proteins.
50. Leipe D.D., Wolf Y.I., Koonin E.V., and Aravind L. Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol 317 (2002) 41-72
51. Soulat D., Jault J.M., Geourjon C., Gouet P., Cozzone A.J., and Grangeasse C. Tyrosine-kinase Wzc from Escherichia coli possesses an ATPase activity regulated by autophosphorylation. FEMS Microbiol Lett 274 (2007) 252-259
52. Paiment A., Hocking J., and Whitfield C. Impact of phosphorylation of specific residues in the tyrosine autokinase, Wzc, on its activity in assembly of group 1 capsules in Escherichia coli. J Bacteriol 184 (2002) 6437-6447
53. Obadia B., Lacour S., Doublet P., Baubichon-Cortay H., Cozzone A.J., and Grangeasse C. Influence of tyrosine-kinase Wzc activity on colanic acid production in Escherichia coli K12 cells. J Mol Biol 367 (2007) 42-53
54. Collins R.F., Beis K., Clarke B.R., Ford R.C., Hulley M., Naismith J.H., and Whitfield C. Periplasmic protein-protein contacts in the inner membrane protein Wzc form a tetrameric complex required for the assembly of Escherichia coli group 1 capsules. J Biol Chem 281 (2006) 2144-2150. The interaction of an octamer of the outer membrane protein, Wza, and a tetramer of the inner membrane protein, Wzc, cretes a molecular machine for export of group 1 capsular polysaccharides. Cry-EM structures reveal conformational changes in Wza mediated by the interactions and provide additional insight into the capsule export pathway.
55. Grangeasse C., Doublet P., and Cozzone A.J. Tyrosine phosphorylation of protein kinase Wzc from Escherichia coli K12 occurs through a two-step process. J Biol Chem 277 (2002) 7127-7135
56. Tocilj A., Munger C., Proteau A., Morona R., Purins L., Ajamian E., Wagner J., Papadopoulos M., Van Den Bosch L., Rubinstein J.L., et al. Bacterial polysaccharide co-polymerases share a common framework for control of polymer length. Nat Struct Mol Biol 15 (2008) 130-138. Proteins in the PCP family participate in polymerization of many different polysaccharide structure in Gram-negative and Gram-positive bacteria with diverse biologies. This study provides the first detailed structural view of a periplasmic domain from PCP members. The structure reveals a novel fold with an extended ∝-helical domain and opens the way to biochemical approaches to probe PCP interactions and functions.
57. Whitfield C., and Larue K. Stop and go: regulation of chain length in the biosynthesis of bacterial polysaccharides. Nat Struct Mol Biol 15 (2008) 121-123
58. Collins R.F., Beis K., Dong C., Botting C.H., McDonnell C., Ford R.C., Clarke B.R., Whitfield C., and Naismith J.H. The 3D structure of a periplasm-spanning platform required for assembly of group 1 capsular polysaccharides in Escherichia coli. Proc Natl Acad Sci U S A 104 (2007) 2390-2395
59. Matias V.R., Al-Amoudi A., Dubochet J., and Beveridge T.J. Cryo-transmission electron microscopy of frozen-hydrated sections of Escherichia coli and Pseudomonas aeruginosa. J Bacteriol 185 (2003) 6112-6118
60. Bayer M.E., and Thurow H. Polysaccharide capsule of Escherichia coli: microscope study of its size, structure, and sites of synthesis. J Bacteriol 130 (1977) 911-936
61. Andersen C., Koronakis E., Bokma E., Eswaran J., Humphreys D., Hughes C., and Koronakis V. Transition to the open state of the TolC periplasmic tunnel entrance. Proc Natl Acad Sci U S A 99 (2002) 11103-11108. The TolC protein from drug efflux systems has an extended periplasmic domain formed from 12 helices. The authors use mutations designed to disrupt interactions within the helical domain to provide supporting evidence for a model where TolC opens by an 'iris-like' realignment in the helices.
62. Murakami S., Nakashima R., Yamashita E., and Yamaguchi A. Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 419 (2002) 587-593
63. Lobedanz S., Bokma E., Symmons M.F., Koronakis E., Hughes C., and Koronakis V. A periplasmic coiled-coil interface underlying TolC recruitment and the assembly of bacterial drug efflux pumps. Proc Natl Acad Sci U S A 104 (2007) 4612-4617. This paper describes experiments designed to test predictions molecular modelling of interactions between TolC and the periplasmic adaptor protein, AcrA. The working model addresses the accommodation of these interactions during transition of TolC to the open state, a critical element in drug efflux pump action.
64. Higgins M.K., Bokma E., Koronakis E., Hughes C., and Koronakis V. Structure of the periplasmic component of a bacterial drug efflux pump. Proc Natl Acad Sci U S A 101 (2004) 9994-9999
65. Mikolosko J., Bobyk K., Zgurskaya H.I., and Ghosh P. Conformational flexibility in the multidrug efflux system protein AcrA. Structure 14 (2006) 577-587
66. Eswaran J., Hughes C., and Koronakis V. Locking TolC entrance helices to prevent protein translocation by the bacterial Type I export apparatus. J Mol Biol 327 (2003) 309-315
67. Seeger M.A., Schiefner A., Eicher T., Verrey F., Diederichs K., and Pos K.M. Structural asymmetry of AcrB trimer suggests a peristaltic pump mechanism. Science 313 (2006) 1295-1298
68. Seeger M.A., von Ballmoos C., Eicher T., Brandstatter L., Verrey F., Diederichs K., and Pos K.M. Engineered disulfide bonds support the functional rotation mechanism of multidrug efflux pump AcrB. Nat Struct Mol Biol 15 (2008) 199-205. From X-ray crystal data, AcrB is proposed to act like a 'periplasmic pump' with several conformational states contributing to the pump action. Here, the authors test this prediction by introducing cysteines at precise positions. Disufide bond formation inhibited function and this effect could be reversed by reducing agents, confirming a functional rotation mechanism.