Multiple pathways allow protein secretion across the bacterial outer membrane

Current Opinion in Cell Biology

Volumn 12, Issue 4, 2000, Pages 420-430

  Thanassi, David G ^a   Hultgren, Scott J ^b  

^a STONY BROOK UNIVERSITY   (United States)

^b Camp B ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CHAPERONE;

BACTERIAL OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN SECRETION; REVIEW;

BACTERIA (MICROORGANISMS);

EID: 0033937939     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(00)00111-3     Document Type: Review

References (81)

1. Economou A. Following the leader: bacterial protein export through the Sec pathway. Trends Microbiol. 7:1999;315-320.
2. Henderson I.R., Novarro-Garcia F., Nataro J.P. The great escape: structure and function of the autotransporter proteins. Trends Microbiol. 6:1998;370-378.
3. Thanassi D.G., Saulino E.T., Hultgren S.J. The chaperone/usher pathway: a major terminal branch of the general secretory pathway. Curr Opin Microbiol. 1:1998;223-231.
4. Binet R., Létoffé S., Ghigo J.M., Delepelaire P., Wandersman C. Protein secretion by Gram-negative bacterial ABC exporters - a review. Gene. 192:1997;7-11.
5. Nunn D. Bacterial type II protein export and pilus biogenesis: more than just homologies? Trends Cell Biol. 9:1999;402-408.
6. Stathopoulos C., Hendrixson D.R., Thanassi D.G., Hultgren S.J., St. Geme J.W., Curtiss R. Secretion of virulence determinants by the general secretory pathway in Gram-negative pathogens: an evolving story. Microbes Infect. 2000;. in press.
7. Hueck C.J. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Molec Biol Rev. 62:1998;379-433.
8. Burns D.L. Biochemistry of type IV secretion. Curr Opin Microbiol. 2:1999;25-29.
9. Pohlner J., Halter R., Beyreuther K., Meyer T.F. Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature. 325:1987;458-462.
10. Maurer J., Jose J., Meyer T.F. Characterization of the essential transport function of the AIDA-I autotransporter and evidence supporting structural predictions. J Bacteriol. 181:1999;7014-7020.
11. Suzuki T., Lett M-C., Sasakawa C. Extracellular transport of VirG protein in Shigella. J Biol Chem. 270:1995;30 874-30 880.
12. Klauser T., Pohlner J., Meyer T.F. Extracellular transport of cholera toxin B subunit using Neisseria IgA protease β-domain: conformation-dependent outer membrane translocation. EMBO J. 9:1990;1991-1999.
13. Veiga E., de Lorenzo V., Fernández A. Probing secretion and translocation of a β-autotransporter using a reporter single-chain Fv as a cognate passenger domain. Mol Microbiol. 33:1999;1232-1243. This paper analyzes secretion by the autotransporter pathway using a single-chain antibody fragment fused to the β-domain of IgA protease. The paper challenges the notion that only unfolded passenger domains can be secreted across the OM.
14. Shannon J.L., Fernandez R.C. The C-terminal domain of the Bordetella pertussis autotransporter BrkA forms a pore in lipid bilayer membranes. J Bacteriol. 181:1999;5838-5842.
15. Könninger U.W., Hobbie S., Benz R., Braun V. The haemolysin-secreting ShlB protein of the outer membrane of Serratia marcescens: determination of surface-exposed residues and formation of ion-permeable pores by ShlB mutants in artificial lipid bilayer membranes. Mol Microbiol. 32:1999;1212-1225.
16. Jacob-Dubuisson F., El-Hamel C., Saint N., Guédin S., Willery E., Molle G., Locht C. Channel formation by FhaC, the outer membrane protein involved in the secretion of the Bordetella pertussis filamentous hemagglutinin. J Biol Chem. 274:1999;37 731-37 735.
17. Guédin S., Willery E., Locht C., Jacob-Dubuisson F. Evidence that a globular conformation is not compatible with FhaC-mediated secretion of the Bordetella pertussis filamentous haemagglutinin. Mol Microbiol. 29:1998;763-774.
18. Reumann S., Davila-Aponte J., Keegstra K. The evolutionary origin of the protein-translocating channel of chloroplastic envelope membranes: identification of a cyanobacterial homolog. Proc Natl Acad Sci USA. 96:1999;784-789.
19. Roberts J.A., Marklund B-I., Ilver D., Haslam D., Kaack M.B., Baskin G., Louis M. The Galα(1-4)Gal-specific tip adhesin of Escherichia coli P-fimbriae is needed for pyelonephritis to occur in the normal urinary tract. Proc Natl Acad Sci USA. 91:1994;11 889-11 893.
20. Langermann S., Palaszynski S., Barnhart M., Auguste G., Pinkner J.S., Burlein J., Barren P. Prevention of mucosal Escherichia coli infection by FimH-adhesin-based systemic vaccination. Science. 276:1997;607-611.
21. Kuehn M.J., Heuser J., Normark S., Hultgren S.J. P pili in uropathogenic E. coli are composite fibres with distinct fibrillar adhesive tips. Nature. 356:1992;252-255.
22. Jones C.H., Danese P.N., Pinkner J.S., Silhavy T.J., Hultgren S.J. The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems. EMBO J. 16:1997;6394-6406.
23. Saulino E.T., Thanassi D.G., Pinkner J.S., Hultgren S.J. Ramifications of kinetic partitioning on usher-mediated pilus biogenesis. EMBO J. 17:1998;2177-2185.
24. Thanassi D.G., Saulino E.T., Lombardo M-J., Roth R., Heuser J., Hultgren S.J. The PapC usher forms an oligomeric channel: implications for pilus biogenesis across the outer membrane. Proc Natl Acad Sci USA. 95:1998;3146-3151.
25. Jacob-Dubuisson F., Striker R., Hultgren S.J. Chaperone-assisted self-assembly of pili independent of cellular energy. J Biol Chem. 269:1994;12 447-12 455.
26. ••].
27. ••] present the first crystal structures of chaperone-subunit complexes from the chaperone/usher pathway. The paper reveals that the periplasmic chaperone employs a novel mechanism of action, termed donor strand complementation, to complete the fold of the subunit and suggests a model for subunit-subunit interactions in the pilus.
28. Soto G.E., Dodson K.W., Ogg D., Liu C., Heuser J., Knight S., Kihlberg J. Periplasmic chaperone recognition motif of subunits mediates quaternary interactions in the pilus. EMBO J. 17:1998;6155-6167.
29. Thanabalu T., Koronakis E., Hughes C., Koronakis V. Substrate-induced assembly of a contiguous channel for protein export from E. coli: reversible bridging of an inner-membrane translocase to an outer membrane exit pore. EMBO J. 17:1998;6487-6496.
30. Koronakis V., Li J., Koronakis E., Stauffer K. Structure of TolC, the outer membrane component of the bacterial type I efflux system, derived from two-dimensional crystals. Mol Microbiol. 23:1997;617-626.
31. Johnson J.M., Church G.M. Alignment and structure prediction of divergent protein families: periplasmic and outer membrane proteins of bacterial efflux pumps. J Mol Biol. 287:1999;695-715. This paper presents an interesting sequence analysis and structure prediction strategy, applied to the MFP and OMP components of the type I secretory pathway.
32. Benz R., Maier E., Gentschev I. TolC of Escherichia coli functions as an outer membrane channel. Int J Med Microbiol Virol Parasitol Infect Dis. 278:1993;187-196.
33. Letoffe S., Delepelaire P., Wandersman C. Protein secretion in gram-negative bacteria: assembly of the three components of ABC protein-mediated exporters is ordered and promoted by substrate binding. EMBO J. 15:1996;5804-5811.
34. Russel M. Macromolecular assembly and secretion across the bacterial cell envelope: type II protein secretion systems. J Mol Biol. 279:1998;485-499.
35. Pugsley A.P., Francetic O., Possot O.M., Sauvonnet N., Hardie K.R. Recent progress and future directions in studies of the main terminal branch of the general secretory pathway in Gram-negative bacteria - a review. Gene. 192:1997;13-19.
36. Nouwen N., Ranson N., Saibil H., Wolpensinger B., Engel A., Ghazi A., Pugsley A.P. Secretin PulD: association with pilot PulS, structure, and ion-conducting channel formation. Proc Natl Acad Sci USA. 96:1999;8173-8177. This paper describes the purification of the secretin PulD as a stable complex with the PulS lipoprotein and analysis of this complex by cryo-electron microscopy. A three-dimensional reconstruction of the complex is presented, together with evidence that the complex forms channels in lipid bilayers.
37. Genin S., Boucher C.A. A superfamily of proteins involved in different secretion pathways in gram-negative bacteria: modular structure and specificity of the N-terminal domain. Mol Gen Genet. 243:1994;112-118.
38. Bitter W., Koster M., Latijnhouwers M., de Cock H., Tommassen J. Formation of oligomeric rings by XcpQ and PilQ, which are involved in protein transport across the outer membrane of Pseudomonas aeruginosa. Mol Microbiol. 27:1998;209-219.
39. Crago A.M., Koronakis V. Salmonella InvG forms a ring-like multimer that requires the InvH lipoprotein for outer membrane localization. Mol Microbiol. 30:1998;47-56.
40. Koster M., Bitter W., de Cock H., Allaoui A., Cornelis G.R., Tommassen J. The outer membrane component, YscC, of the Yop secretion machinery of Yersinia enterocolitica forms a ring-shaped multimeric complex. Mol Microbiol. 26:1997;789-797.
41. Linderoth N.A., Simon M.N., Russel M. The filamentous phage pIV multimer visualized by scanning transmission electron microscopy. Science. 278:1997;1635-1638.
42. Marciano D.K., Russel M., Simon S.M. An aqueous channel for filamentous phage export. Science. 284:1999;1516-1519. This paper presents lipid-bilayer analysis of the secretin pIV and a pIV mutant with altered permeability characteristics. The paper provides strong evidence that secretins contain large gated channels.
43. Brok R., Van Gelder P., Winterhalter M., Ziese U., Koster A.J., de Cock H., Koster M. The C-terminal domain of the Pseudomonas Secretin XcpQ forms oligomeric rings with pore activity. J Mol Biol. 294:1999;1169-1179.
44. Guilvout I., Hardie K., Sauvonnet N., Pugsley A.P. Genetic dissection of the outer membrane secretin PulD: are there distinct domains for multimerization and secretion specificity? J Bacteriol. 181:1999;7212-7220.
45. Strom M.S., Nunn D., Lory S. Multiple roles of the pilus biogenesis protein, PilD: involvement of PilD inexcretion of enzymes from Pseudomonas aeruginosa. J Bacteriol. 173:1991;1175-1180.
46. Hobbs M., Mattick J.S. Common components in the assembly of type 4 fimbriae, DNA transfer systems, filamentous phage and protein-secretion apparatus: a general system for the formation of surface-associated protein complexes. Mol Microbiol. 10:1993;233-243.
47. Pugsley A.P. Multimers of the precursor of a type IV pilin-like component of the general secretory pathway are unrelated to pili. Mol Microbiol. 20:1996;1235-1245.
48. Sandkvist M., Bagdasarian M., Howard S.P., DiRita V.J. Interaction between the autokinase EpsE and EpsL in the cytoplasmic membrane is required for extracellular secretion in Vibrio cholerae. EMBO J. 14:1995;1664-1673.
49. Py B., Loiseau L., Barras F. Assembly of the type II secretion machineryof Erwinia chrysanthemi: direct interaction and associated conformational change between OutE, the putative ATP-binding component and the membrane protein OutL. J Mol Biol. 289:1999;659-670.
50. Possot O.M., Pugsely A.P. The conserved tetracysteine motif in the general secretory pathway component PulE is required for efficient pullulanase secretion. Gene. 192:1997;45-50.
51. Sandkvist M., Hough L.P., Bagdasarian M.M., Bagdasarian M. Direct interaction of the EpsL and EpsM proteins of the general secretion apparatus in Vibrio cholerae. J Bacteriol. 181:1999;3129-3135.
52. Bleves S., Gérard-Vincent M., Lazdunski A., Filloux A. Structure-function analysis of XcpP, a component involved in general secretory pathway-dependent protein secretion in Pseudomonas aeruginosa. J Bacteriol. 181:1999;4012-4019.
53. Possot O.M., Gérard-Vincent M., Pugsley A.P. Membrane association and multimerization of secreton component PulC. J Bacteriol. 181:1999;4004-4011.
54. Galan J.E., Bliska J.B. Cross-talk between bacterial pathogens and their host cells. Annu Rev Cell Dev Biol. 12:1996;221-255.
55. Macnab R.M. Flagella and motility. Neidhardt F.C. Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. 1996;123-145 ASM Press, Washington DC.
56. Young G.M., Schmiel D.H., Miller V.L. A new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein-secretion system. Proc Natl Acad Sci USA. 96:1999;6456-6461.
57. Kubori T., Matsushima Y., Nakamura D., Uralil J., Lara-Tejero M., Sukhan A., Galán J.E. Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science. 280:1998;602-605.
58. Blocker A., Gounon P., Larquet E., Niebuhr K., Cabiaux V., Parsot C., Sansonetti P. The tripartite type III secreton of Shigella flexneri inserts IpaB and IpaC into host membranes. J Cell Biol. 147:1999;683-693. This paper presents evidence that the Shigella IpaB and IpaC proteins, homologs of Yersinia YopB and YopD, form pores by inserting into the eukaryotic cell plasma membrane. The paper also presents electron micrographs of the Shigella type III secretion apparatus, which contains a large bulb region that presumably extends into the bacterial cytoplasm.
59. Roine E., Wei W., Yuan J., Nurmiaho-Lassila E-L., Kalkkinen N., Romatschuk M., He S.Y. Hrp pilus: an hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci USA. 94:1997;3459-3464.
60. Knutton S., Rosenshine I., Pallen M.J., Nisan I., Neves B.C., Bain C., Wolff C. A novel EspA-associated surface organelle of enterobacteric Escherichia coli involved in protein translocation into epithelial cells. EMBO J. 17:1998;2166-2176.
61. Anderson D.M., Schneewind O. Yersinia enterocolitica type III secretion: an mRNA signal that couples translation and secretion of YopQ. Mol Microbiol. 31:1999;1139-1148. This paper demonstrates that translation of the YopQ protein is coupled to its secretion by the type III system and presents evidence that an mRNA signal controls YopQ targeting.
62. Cheng L.W., Schneewind O. Yersinia enterocolitica type III secretion: on the role of SycE in targeting YopE into HeLa cells. J Biol Chem. 274:1999;22 102-22 108.
63. ••], this suggests YopB and YopD and their homologs may form a channel in the target cell membrane for translocation of effector proteins.
64. Neyt C., Cornelis G.R. Insertion of a Yop translocation pore into the macrophage plasma membrane by Yersinia enterocolitica: requirement for translocators YopB and YopD, but not LcrG. Mol Microbiol. 33:1999;971-981.
65. Håkansson S., Schesser K., Persson C., Galyov E.E., Rosqvist R., Homble F., Wolf-Watz H. The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target plasma membrane and displays a contact-dependent membrane disrupting activity. EMBO J. 15:1996;5812-5823.
66. Lee V.T., Schneewind O. Type III machines of pathogenic yersiniae secrete virulence factors into the extracellular milieu. Mol Microbiol. 31:1999;1619-1629.
67. Segal G., Purcell M., Shuman H.A. Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionaella pnumophila genome. Proc Natl Acad Sci USA. 95:1998;1669-1674.
68. Weiss A.A., Johnson F.D., Burns D.L. Molecular characterization of an operon required for pertussis toxin secretion. Proc Natl Acad Sci USA. 90:1993;2970-2974.
69. Vogel J.P., Andrews H.L., Wong S.K., Isberg R.R. Conjugative transfer by the virulence system of Legionella pneumophila. Science. 279:1998;873-876.
70. Covacci A., Falkow S., Berg D.E., Rappuoli R. Did the inheritance of a pathogenicity island modify the virulence of Helicobacter pylori? Trends Microbiol. 5:1997;205-208.
71. Fernandez D., Dang T.A.T., Spudich G.M., Zhou X-R., Berger B.R., Christie P.J. The Agrobacterium tumefaciens virB7 gene product, a proposed component of the T-complex transport apparatus, is a membrane-associated lipoprotein exposed at the periplasmic surface. J Bacteriol. 178:1996;3156-3167.
72. Thorstenson Y.R., Kuldau G.A., Zambryski P.C. Subcellular localization of seven VirB proteins of Agrobacterium tumefaciens: implications for the formation of a T-DNA transport structure. J Bacteriol. 176:1993;5233-5241.
73. Spudich G.M., Fernandez D., Zhou X-R., Christie P.J. Intermolecular disulfide bonds stabilize VirB7 homodimers and VirB7/VirB9 heterodimers during biogenesis of the Agrobacterium tumefaciens T-complex transport apparatus. Proc Natl Acad Sci USA. 93:1996;7512-7517.
74. Christie P.J., Ward J.E., Gordon M.P., Nester E.W. A gene required for transfer of T-DNA to plants encodes an ATPase with autophosphorylating activity. Proc Natl Acad Sci USA. 86:1989;9677-9681.
75. Shirasu K., Koukolikova-Nica Z., Hohn B., Kado C.I. An inner-membrane-associated virulence protein essential for T-DNA transfer from Agrobacterium tumefaciens to plants exhibits ATPase activity and similarities to conjugative transfer genes. Mol Microbiol. 11:1994;581-588.
76. Dang T.A., Zhou X-R., Graf B., Christie P.J. Dimerization of the Agrobacterium tumefaciens VirB4 ATPase and the effect of ATP-binding cassette mutations on the assembly and function of the T-DNA transporter. Mol Microbiol. 31:1999;1239-1253.
77. Bohne J., Yim A., Binns A.N. The Ti plasmid increases the efficiency of Agrobacterium tumefaciens as a recipient in virB-mediated conjugal transfer of an IncQ plasmid. Proc Natl Acad Sci USA. 95:1998;7057-7062.
78. Lai E-M., Kado C.I. Processed VirB2 is the major subunit of the promiscuous pilus of Agrobacterium tumefaiens. J Bacteriol. 180:1998;2711-2717.
79. Eisenbrandt R., Kalkum M., Lai E-M., Lurz R., Kado C.I., Lanka E. Conjugative pili of IncP plasmids, and the Ti plasmid T Pilus are composed of cyclic subunits. J Biol Chem. 274:1999;22 548-22 555. This paper shows that the structural subunits of conjugative and VirB pili are cyclized by a novel intramolecular head-to-tail peptide bond.
80. Sauvonnet N., Vignon G., Pugsley A.P., Gounon P. Pilus formation and protein secretion by the same machinery in Escherichia coli. EMBO J. 19:2000;2221-2228.
81. Odenbreit S., Puls J., Sedlmaier B., Gerland E., Fischer W., Haas R. Translocation of Heliobacter pylori CagA into gastric epithelial cells by type IV section. Science. 287:2000;1497-1500.