Protein secretion in the absence of ATP: The autotransporter, two-partner secretion and chaperone/usher pathways of Gram-negative bacteria

Molecular Membrane Biology

Volumn 22, Issue 1-2, 2005, Pages 63-72

  Thanassi, David G ^a   Stathopoulos, Christos ^b   Karkal, Aarthi ^b   Li, Huilin ^c  

^a STONY BROOK UNIVERSITY   (United States)

^b University of Houston   (United States)

^c BROOKHAVEN NATIONAL LABORATORY   (United States)

Author keywords

Autotransporter; Bacterial outer membrane; Chaperone usher; Protein secretion; Two partner secretion

Indexed keywords

ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; CHAPERONE;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; BACTERIAL MEMBRANE; BACTERIAL VIRULENCE; CELL ENERGY; CELL MEMBRANE TRANSPORT; CELL SURFACE; CYTOPLASM; ENERGY METABOLISM; GRAM NEGATIVE BACTERIUM; MEMBRANE STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REVIEW;

ADENOSINE TRIPHOSPHATE; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; CELL MEMBRANE; GRAM-NEGATIVE BACTERIA; MOLECULAR CHAPERONES; PERIPLASM; PROTEIN TRANSPORT;

BACTERIA (MICROORGANISMS); HARNESS; NEGIBACTERIA;

EID: 18844384961     PISSN: 09687688     EISSN: None     Source Type: Journal    
DOI: 10.1080/09687860500063290     Document Type: Review

References (83)

1. Thanassi DG, Hultgren SJ. Multiple pathways allow protein secretion across the bacterial outer membrane. Curr Opin Cell Biol 2000;12:420-430.
2. Stathopoulos C, Hendrixson DR, Thanassi DG, Hultgren SJ, St. Geme III JW, Curtiss III R. Secretion of virulence determinants by the general secretory pathway in Gram-negative pathogens: An evolving story. Microbes Infection 2000;2:1061-1072.
3. Pugsley A. The complete general secretory pathway in Gram negative bacteria. Microbiol Rev 1993;57:50-108.
4. Jacob-Dubuisson F, Fernandez R, Coutte L. Protein secretion through autotransporter and two-partner pathways. Biochim Biophys Acta 2004;1694:235-257.
5. Henderson IR, Novarro-Garcia F, Nataro JP. The great escape: structure and function of the autotransporter proteins. Trends Microbiol 1998;6:370-378.
6. Newman CL, Stathopoulos C. Autotransporter and two-partner secretion: Delivery of large-size virulence factors by Gram-negative bacterial pathogens. Crit Rev Mirobiol 2004;30:275-286.
7. Desvaux M, Parham NJ, Henderson IR. The autotransporter secretion system. Res Microbiol 2004;155:53-60.
8. Desvaux M, Parham NJ, Henderson IR. Type V protein secretion: simplicity gone awry? Curr Issues Mol Biol 2004;6:111-124.
9. Jacob-Dubuisson F, Locht C, Antoine R. Two-partner secretion in Gram-negative bacteria: A thrifty, specific pathway for large virulence proteins. Mol Microbiol 2001;40:306-313.
10. Thanassi DG, Saulino ET, Hultgren SJ. The chaperone/ usher pathway. A major terminal branch of the general secretory pathway. Curr Opin Microbiol 1998;1:223-231.
11. Sandkvist M. Biology of type II secretion. Mol Microbiol 2001;40:271-283.
12. Andersen C, Hughes C, Koronakis V. Protein export and drug efflux through bacterial channel-tunnels. Curr Opin Cell Biol 2001;13:412-416.
13. Hueck CJ. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Molec Biol Rev 1998;62:379-433.
14. Cascales E, Christie PJ. The versatile bacterial type IV secretion systems. Nat Rev Microbiol 2003;1:137-149.
15. Pohlner J, Halter R, Beyreuther K, Meyer TF. Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 1987;325:458-462.
16. Sijbrandi R, Urbanus ML, ten Hagen-Jongman CM, Bernstein HD, Oudega B, Otto BR, Luirink J. Signal recognition particle (SRP)-mediated targeting and Sec-dependent translocation of an extracellular Escherichia coli protein. J Biol Chem 2003;278:4654-4659.
17. Brandon LD, Goldberg MB. Periplasmic transit and disulfide bond formation of the autotransported Shigella protein IcsA. J Bacteriol 2001;183:951-958.
18. Bulieris PV, Behrens S, Holst O, Kleinschmidt JH. Folding and insertion of the outer membrane protein OmpA is assisted by the chaperone Skp and by lipopolysaccharide. J Biol Chem 2003;278:9092-9099.
19. Purdy GE, Hong M, Payne SM. Shigella flexneri DegP facilitates IcsA surface expression and is required for efficient intercellular spread. Infect Immun 2002;70:6355-6364.
20. Yen MR, Peabody CR, Partovi SM, Zhai Y, Tseng YH, Saier MH. Protein-translocating outer membrane porins of Gram-negative bacteria. Biochim Biophys Acta 2002;1562:6-31.
21. Emsley P, Charles IG, Fairweather NF, Isaacs NW. Structure of Bordetella pertussis virulence factor P.69 pertactin. Nature 1996;381:90-92.
22. Nummelin H, Merckel MC, Leo JC, Lankinen H, Skurnik M, Goldman A. The Yersinia adhesin YadA collagen-binding domain structure is a novel left-handed parallel beta-roll. EMBO J 2004;23:701-711.
23. Yeo HJ, Cotter SE, Laarmann S, Juehne T, St Geme JW, Waksman G. Structural basis for host recognition by the Haemophilus influenzae Hia autotransporter. EMBO J 2004;23:1245-1256.
24. Oliver DC, Huang G, Nodel E, Pleasance S, Fernandez RC. A conserved region within the Bordetella pertussis autotransporter BrkA is necessary for folding of its passenger domain. Mol Microbiol 2003;47:1367-1383.
25. Ohnishi Y, Nishiyama M, Horinouchi S, Beppu T. Involvement of the COOH-terminal pro-sequence of Serratia marcescens serine protease in the folding of the mature enzyme. J Biol Chem 1994;269:32800-32806.
26. Stathopoulos C, Provence DL, Curtiss R, 3rd. Characterization of the avian pathogenic Escherichia coli hemagglutinin Tsh, a member of the immunoglobulin A protease-type family of autotransporters. Infect Immun 1999;67:772-781.
27. Klauser T, Kramer J, Otzelberger K, Pohlner J, Meyer TF. Characterization of the Neisseria Iga beta-core. The essential unit for outer membrane targeting and extracellular protein secretion. J Mol Biol 1993;234:579-593.
28. Oliver DC, Huang G, Fernandez RC. Identification of secretion determinants of the Bordetella pertussis BrkA autotransporter. J Bacteriol 2003;185:489-495.
29. Maurer J, Jose J, Meyer TF. Characterization of the essential transport function of the AIDA-I autotransporter and evidence supporting structural predictions. J Bacteriol 1995;181:7014-7020.
30. Oomen CJ, Van Ulsen P, Van Gelder P, Feijen M, Tommassen J, Gros P. Structure of the translocator domain of a bacterial autotransporter. EMBO J 2004;23:1257-1266.
31. Roggenkamp A, Ackermann N, Jacobi CA, Truelzsch K, Hoffmann H, Heesemann J. Molecular analysis of transport and oligomerization of the Yersinia enterocolitica adhesin YadA. J Bacteriol 2003;185:3735-3744.
32. Surana NK, Cutter D, Barenkamp SJ, St Geme JW, 3rd. The haemophilus influenzae Hia autotransporter contains an unusually short trimeric translocator domain. J Biol Chem 2004;279:14679-14685.
33. Koronakis V, Sharff A, Koronakis E, Luisi B, Hughes C. Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 2000;405:914-919.
34. Jose J, Kramer J, Klauser T, Pohlner J, Meyer TF. Absence of periplasmic DsbA oxidoreductase facilitates export of cysteine-containing passenger proteins to the Escherichia coli cell surface via the Iga beta autotransporter pathway. Gene 1996;178:107-110.
35. Velarde JJ, Nataro JP. Hydrophobic residues of the autotransporter EspP linker domain are important for outer membrane translocation of its passenger. J Biol Chem 2004;279:31495-31504.
36. Veiga E, Sugawara E, Nikaido H, de Lorenzo V, Fernandez LA. Export of autotransported proteins proceeds through an oligomeric ring shaped by C-terminal domains. EMBO J 2002;21:2122-2131.
37. Veiga E, de Lorenzo V, Fernandez LA. Structural tolerance of bacterial autotransporters for folded passenger protein domains. Mol Microbiol 2004;52:1069-1080.
38. Voulhoux R, Tommassen J. Omp85, an evolutionarily conserved bacterial protein involved in outer-membrane-protein assembly. Res Microbiol 2004;155:129-135.
39. Paschen SA, Waizenegger T, Stan T, Preuss M, Cyrklaff M, Hell K, Rapaport D, Neupert W. Evolutionary conservation of biogenesis of beta-barrel membrane proteins. Nature 2003;426:862-866.
40. Kozjak V, Wiedemann N, Milenkovic D, Lohaus C, Meyer HE, Guiard B, Meisinger C, Pfanner N. An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane. J Biol Chem 2003;278:48520-48523.
41. Hinnah SC, Hill K, Wagner R, Schlicher T, Soll J. Reconstitution of a chloroplast protein import channel. EMBO J 1997;16:7351-7360.
42. Schleiff E, Soll J, Kuchler M, Kuhlbrandt W, Harrer R. Characterization of the translocon of the outer envelope of chloroplasts. J Cell Biol 2003;160:541-551.
43. 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 1999;96:784-789.
44. Voulhoux R, Bos MP, Geurtsen J, Mols M, Tommassen J. Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 2003;299:262-265.
45. Genevrois S, Steeghs L, Roholl P, Letesson JJ, van der Ley P. The Omp85 protein of Neisseria meningitidis is required for lipid export to the outer membrane. EMBO J 2003;22:1780-1789.
46. St Geme JW, 3rd. The HMW1 adhesin of nontypeable Haemophilus influenzae recognizes sialylated glycoprotein receptors on cultured human epithelial cells. Infect Immun 1994;62:3881-3889.
47. Locht C, Bertin P, Menozzi FD, Renauld G. The filamentous haemagglutinin, a multifaceted adhesion produced by virulent Bordetella spp. Mol Microbiol 1993;9:653-660.
48. Hertle R, Hilger M, Weingardt-Kocher S, Walev I. Cytotoxic action of Serratia marcescens hemolysin on human epithelial cells. Infect Immun 1999;67:817-825.
49. Lambert-Buisine C, Willery E, Locht C, Jacob-Dubuisson F. N-terminal characterization of the Bordetella pertussis filamentous haemagglutinin. Mol Microbiol 1998;28:1283-1293.
50. Guedin 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 1998;29:763-774.
51. Surana NK, Grass S, Hardy GG, Li H, Thanassi DG, Geme JW, 3rd. Evidence for conservation of architecture and physical properties of Omp85-like proteins throughout evolution. Proc Natl Acad Sci USA 2004;101:14497-14502.
52. Clantin B, Hodak H, Willery E, Locht C, Jacob-Dubuisson F, Villeret V. The crystal structure of filamentous hemagglutinin secretion domain and its implications for the two-partner secretion pathway. Proc Natl Acad Sci USA 2004;101:6194-6199.
53. Guedin S, Willery E, Tommassen J, Fort E, Drobecq H, Locht C, Jacob-Dubuisson F. Novel topological features of FhaC, the outer membrane transporter involved in the secretion of the Bordetella pertussis filamentous hemagglutinin. J Biol Chem 2000;275:30202-30210.
54. Könninger UW, 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 1999;32:1212-1225.
55. Yang FL, Braun V. ShlB mutants of Serratia marcescens allow uncoupling of activation and secretion of the ShlA hemolysin. Int J Med Microbiol 2000;290:529-538.
56. Schiebel E, Schwarz H, Braun V. Subcellular location and unique secretion of the hemolysin of Serratia marcescens. J Biol Chem 1989;264:16311-16320.
57. Coutte L, Alonso S, Reveneau N, Willery E, Quatannens B, Locht C, Jacob-Dubuisson F. Role of adhesin release for mucosal colonization by a bacterial pathogen. J Exp Med 2003;197:735-742.
58. Abraham SN, Sun D, Dale JB, Beachey EH. Conservation of the D-mannose-adhesion protein among type 1 fimbriated members of the family Enterobactericeae. Nature 1988;336:682-684.
59. Marklund BI, Tennent JM, Garcia E, Hamers A, Baga M, Lindberg F, Gaastra W, Normark S. Horizontal gene transfer of the Escherichia coli pap and prs pili operons as a mechanism for the development of tissue-specific adhesive properties. Molecular Microbiology 1992;6:2225-2242.
60. Kuehn MJ, Heuser J, Normark S, Hultgren SJ. P pili in uropathogenic E. coli are composite fibres with distinct fibrillar adhesive tips. Nature 1992;356:252-255.
61. Du Y, Rosqvist R, Forsberg A. Role of fraction 1 antigen of Yersinia pestis in inhibition of phagocytosis. Infect Immun 2002;70:1453-1460.
62. Galyov EE, Smirnov O, Karlishev AV, Volkovoy KI, Denesyuk AI, Nazimov IV, Rubtsov KS, Abramov VM, Dalvadyanz SM, Zav'yalov VP. Nucleotide sequence of the Yersinia pestis gene encoding F1 antigen and the primary structure of the protein. Putative T and B cell epitopes. FEBS Lett 1990;277:230-232.
63. Vetsch M, Puorger C, Spirig T, Grauschopf U, Weber-Ban EU, Glockshuber R. Pilus chaperones represent a new type of protein-folding catalyst. Nature 2004;431:329-333.
64. Bann JG, Pinkner JS, Frieden C, Hultgren SJ. Catalysis of protein folding by chaperones in pathogenic bacteria. Proc Natl Acad Sci USA 2004;101:17389-17393.
65. Choudhury D, Thompson A, Stojanoff V, Langermann S, Pinkner J, Hultgren SJ, Knight SD. X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli. Science 1999;285:1061-1066.
66. Sauer FG, Fütterer K, Pinkner JS, Dodson KW, Hultgren SJ, Waksman G. Structural basis of chaperone function and pilus biogenesis. Science 1999;285:1058-1061.
67. Sauer FG, Pinkner JS, Waksman G, Hultgren SJ. Chaperone priming of pilus subunits facilitates a topological transition that drives fiber formation. Cell 2002;111:543-551.
68. Zavialov AV, Berglund J, Pudney AF, Fooks LJ, Ibrahim TM, MacIntyre S, Knight SD. Structure and biogenesis of the capsular F1 antigen from Yersinia pestis: preserved folding energy drives fiber formation. Cell 2003;113:587-596.
69. Zavialov AV, Kersley J, Korpela T, Zav'yalov VP, MacIntyre S, Knight SD. Donor strand complementation mechanism in the biogenesis of non-pilus systems. Mol Microbiol 2002;45:983-995.
70. Ng TW, Akman L, Osisami M, Thanassi DG. The usher N terminus is the initial targeting site for chaperone-subunit complexes and participates in subsequent pilus biogenesis events. J Bacteriol 2004;186:5321-5331.
71. Nishiyama M, Vetsch M, Puorger C, Jelesarov I, Glockshuber R. Identification and characterization of the chaperone-subunit complex-binding domain from the type 1 pilus assembly platform FimD. J Mol Biol 2003;330:513-525.
72. Dodson KW, Jacob-Dubuisson F, Striker RT, Hultgren SJ. Outer membrane PapC usher discriminately recognizes periplasmic chaperone-pilus subunit complexes. Proc Natl Acad Sci USA 1993;90:3670-3674.
73. Saulino ET, Thanassi DG, Pinkner JS, Hultgren SJ. Ramifications of kinetic partitioning on usher-mediated pilus biogenesis. EMBO J 1998;17:2177-2185.
74. Jacob-Dubuisson F, Striker R, Hultgren SJ. Chaperone-assisted self-assembly of pili independent of cellular energy. J Biol Chem 1994;269:12447-12455.
75. Henderson NS, Shu Kin So S, Martin C, Kulkarni R, Thanassi DG. Topology of the outer membrane usher PapC determined by site-directed fluorescence labeling. J Biol Chem 2004;279:53747-53754.
76. Ferguson AD, Hofmann E, Coulton JW, Diederichs K, Weite W. Siderophore-mediated iron transport: Crystal structure of FhuA with bound lipopolysaccharide. Science 1998;282:2215-2220.
77. Locher KP, Rees B, Koebnik R, Mitschler A, Moulinier L, Rosenbusch JP, Moras D. Transmembrane signaling across the ligand-gated FhuA receptor: Crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell 1998;95:771-778.
78. Thanassi DG, Saulino ET, Lombardo M-J, Roth R, Heuser J, Hultgren SJ. The PapC usher forms an oligomeric channel: implications for pilus biogenesis across the outer membrane. Proc Natl Acad Sci USA 1998;95:3146-3151.
79. Li H, Qian L, Chen Z, Thahbot D, Liu G, Liu T, Thanassi DG. The outer membrane usher forms a twin-pore secretion complex. J Mol Biol 2004;344:1397-1407.
80. Gong M, Makowski L. Helical structure of Pap adhesion pili from Escherichia coli. J Mol Biol 1992;228:735-742.
81. Rehling P, Model K, Brandner K, Kovermann P, Sickmann A, Meyer HE, Kuhlbrandt W, Wagner R, Truscott KN, Pfanner N. Protein insertion into the mitochondrial inner membrane by a twin-pore translocase. Science 2003;299:1747-1751.
82. Ahting U, Thieffry M, Engelhardt H, Hegerl R, Neupert W, Nussberger S. Tom40, the pore-forming component of the protein-conducting TOM channel in the outer membrane of mitochondria. J Cell Biol 2001;153:1151-1160.
83. Barnhart MM, Sauer FG, Pinkner JS, Hultgren SJ. Chaperone-subunit-usher interactions required for donor strand exchange during bacterial pilus assembly. J Bacteriol 2003;185:2723-2730.