Type V protein secretion: Simplicity gone awry?

Current Issues in Molecular Biology

Volumn 6, Issue 2, 2004, Pages 111-124

  Desvaux, Mickaël ^a   Parham, Nicholas J ^a   Henderson, Ian R ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BACTERIAL PROTEIN; CARRIER PROTEIN; SIGNAL PEPTIDE;

AMINO ACID SEQUENCE; BACTERIAL CELL; BACTERIAL MEMBRANE; CHANNEL GATING; GENE TRANSLOCATION; GRAM NEGATIVE BACTERIUM; NONHUMAN; OUTER MEMBRANE; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; CARRIER PROTEINS; CELL MEMBRANE; CELL WALL; GRAM-NEGATIVE BACTERIA; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; OXALIS TUBEROSA;

EID: 1942467796     PISSN: 14673037     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (127)

1. Andersen, C. (2003). Channel-tunnels, outer membrane components of type I secretion systems and multidrug efflux pumps of Gram-negative bacteria. Rev. Physiol. Biochem. Pharmacol. 147, 122-165.
2. Batey, R.T., Rambo, R.P., Lucast, L., Rha, B. and Doudna, J.A. (2000). Crystal structure of the ribonucleoprotein core of the signal recognition particle. Science. 287, 1232-1239.
3. Beha, D., Deitermann, S., Muller, M. and Koch, H.G. 2003. Export of β-lactamase is independent of the signal recognition particle. J. Biol. Chem. 278, 22161-22167.
4. Benjelloun-Touimi, Z., Sansonetti, P.J. and Parsot, C. (1995). SepA, the major extracellular protein of Shigella flexneri, autonomous secretion and involvement in tissue invasion. Mol. Microbiol. 17, 123-135.
5. Benz, I. and Schmidt, M.A. (1992). AIDA-I, the adhesin involved in diffuse adherence of the diarrhoeagenic Escherichia coli strain 2787 (O126:H27), is synthesized via a precursor molecule. Mol. Microbiol. 6, 1539-1546.
6. Berks, B.C., Sargent, F. and Palmer, T. (2000). The Tat protein export pathway. Mol. Microbiol. 35, 260-274.
7. Blocker, A., Komoriya, K. and Aizawa, S. (2003). Type III secretion systems and bacterial flagella, insights into their function from structural similarities. Proc. Natl. Acad. Sci. U S A. 100, 3027-3030.
8. Brandon, L.D., Goehring, N., Janakiraman, A., Yan, A.W., Wu, T., Beckwith, J. and Goldberg, M.B. (2003). IcsA, a polarly localized autotransporter with an atypical signal peptide, uses the Sec apparatus for secretion, although the Sec apparatus is circumferentially distributed. Mol Microbiol. 50, 45-60.
9. Brandon, L.D. and Goldberg, M.B. (2001). Periplasmic transit and disulfide bond formation of the autotransported Shigella protein IcsA. J. Bacteriol. 183, 951-958.
10. Brunder, W., Schmidt, H. and Karch, H. (1997). EspP, a novel extracellular serine protease of enterohaemorrhagic Escherichia coli O157:H7 cleaves human coagulation factor V. Mol. Microbiol. 24, 767-778.
11. Bulieris, P.V., Behrens, S., Holst, O. and Kleinschmidt, J.H. (2003). Folding and insertion of the outer membrane protein OmpA is assisted by the chaperone Skp and by lipopolysaccharide. J. Biol. Chem. 278, 9092-9099.
12. Buttner, D. and Bonas, U. (2002). Port of entry, the type III secretion translocon. Trends Microbiol. 10, 186-192.
13. Charles, M., Perez, M., Kobil, J.H. and Goldberg, M.B. (2001). Polar targeting of Shigella virulence factor IcsA in Enterobacteriacae and Vibrio. Proc. Natl. Acad. Sci. U S A. 98, 9871-9876.
14. Chen, R. and Henning, U. (1996). A periplasmic protein (Skp) of Escherichia coli selectively binds a class of outer membrane proteins. Mol. Microbiol. 19, 1287-1294.
15. Christie, P.J. (2001). Type IV secretion, intercellular transfer of macromolecules by systems ancestrally related to conjugation machines. Mol. Microbiol. 40, 294-305.
16. Christie, P.J. and Vogel, J.P. (2000). Bacterial type IV secretion, conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol. 8, 354-360.
17. Cleverley, R.M. and Gierasch, L.M. (2002). Mapping the signal sequence-binding site on SRP reveals a significant role for the NG domain. J. Biol. Chem. 277, 46763-46768.
18. Coutte, L., Antoine, R., Drobecq, H., Locht, C. and Jacob-Dubuisson, F. (2001). Subtilisin-like autotransporter serves as maturation protease in a bacterial secretion pathway. EMBO J. 20, 5040-5048.
19. Coutte, L., Willery, E., Antoine, R., Drobecq, H., Locht, C. and Jacob-Dubuisson, F. (2003). Surface anchoring of bacterial subtilisin important for maturation function. Mol. Microbiol. 49, 529-539.
20. Cristobal, S., Scotti, P., Luirink, J., von Heijne, G. and de Gier, J.W. (1999). The signal recognition particle-targeting pathway does not necessarily deliver proteins to the sec-translocase in Escherichia coli. J. Biol. Chem. 274, 20068-20070.
21. Danchin, A. (2003). Genomes and evolution. Curr. Issues Mol. Biol. 5, 37-42.
22. de Cock, H., Brandenburg, K., Wiese, A., Holst, O. and Seydel, U. (1999). Non-lamellar structure and negative charges of lipopolysaccharides required for efficient folding of outer membrane protein PhoE of Escherichia coli. J. Biol. Chem. 274, 5114-5119.
23. de Cock, H., Struyve, M., Kleerebezem, M., van der Krift, T. and Tommassen, J. (1997). Role of the carboxy-terminal phenylalanine in the biogenesis of outer membrane protein PhoE of Escherichia coli K-12. J. Mol. Biol. 269, 473-478.
24. de Gier, J.W. and Luirink, J. (2001). Biogenesis of inner membrane proteins in Escherichia coli. Mol. Microbiol. 40, 314-322.
25. Delcour, A.H. (2002). Structure and function of pore-forming beta-barrels from bacteria. J Mol Microbiol. Biotechnol. 4, 1-10.
26. Desvaux, M., Parham, N.J. and Henderson, I.R. (2003). Le système de sécrétion de type V chez les bacté ries Gram-négatives. Biofutur. 237, 34-37.
27. Domenighini, M., Relman, D., Capiau, C., Falkow, S., Prugnola, A., Scarlato, V. and Rappuoli, R. (1990). Genetic characterization of Bordetella pertussis filamentous haemagglutinin, a protein processed from an unusually large precursor. Mol. Microbiol. 4, 787-800.
28. Driessen, A.J., Fekkes, P. and van der Wolk, J.P. (1998). The Sec system. Curr. Opin. Microbiol. 1, 216-222.
29. Economou, A. (2002). Bacterial secretome, the assembly manual and operating instructions. Mol. Membr. Biol. 19, 159-169.
30. Fekkes, P. and Driessen, A.J. (1999). Protein targeting to the bacterial cytoplasmic membrane. Microbiol. Mol. Biol. Rev. 63, 161-173.
31. Ferguson, A.D., Welte, W., Hofmann, E., Lindner, B., Holst, O., Coulton, J.W. and Diederichs, K. (2000). A conserved structural motif for lipopolysaccharide recognition by procaryotic and eucaryotic proteins. Structure Fold Des. 8, 585-592.
32. Fernandez, R.C. and Weiss, A.A. (1994). Cloning and sequencing of a Bordetella pertussis serum resistance locus. Infect. Immun. 62, 4727-4738.
33. Freudl, R., Schwarz, H., Stierhof, Y.D., Gamon, K., Hindennach, I. and Henning, U. (1986). An outer membrane protein (OmpA) of Escherichia coli K-12 undergoes a conformational change during export. J. Biol. Chem. 261, 11355-11361.
34. Froderberg, L., Houben, E., Samuelson, J.C., Chen, M., Park, S.K., Phillips, G.J., Dalbey, R., Luirink, J. and De Gier, J.W. (2003). Versatility of inner membrane protein biogenesis in Escherichia coli. Mol. Microbiol. 47, 1015-1027.
35. Genevrois, S., Steeghs, L., Roholl, P., Letesson, J.J. and van der Ley, P. (2003). The Omp85 protein of Neisseria meningitidis is required for lipid export to the outer membrane. EMBO J. 22, 1780-1789.
36. Goldberg, M.B., Barzu, O., Parsot, C. and Sansonetti, P.J. (1993). Unipolar localization and ATPase activity of IcsA, a Shigella flexneri protein involved in intracellular movement. J. Bacteriol. 175, 2189-2196.
37. Grass, S. and St Geme, J.W., 3rd. (2000). Maturation and secretion of the non-typable Haemophilus influenzae HMW1 adhesin, roles of the N-terminal and C-terminal domains. Mol. Microbiol. 36, 55-67.
38. Guedin, S., Willery, E., Locht, C. and Jacob-Dubuisson, F. (1998). Evidence that a globular conformation is not compatible with FhaC-mediated secretion of the Bordetella pertussis filamentous haemagglutinin. Mol. Microbiol. 29, 763-774.
39. Guedin, S., Willery, E., Tommassen, J., Fort, E., Drobecq, H., Locht, C. and Jacob-Dubuisson, F. (2000). Novel topological features of FhaC, the outer membrane transporter involved in the secretion of the Bordetella pertussis filamentous hemagglutinin. J. Biol. Chem. 275, 30202-30210.
40. Henderson, I.R., Cappello, R. and Nataro, J.P. (2000a). Autotransporter proteins, evolution and redefining protein secretion. Trends Microbiol. 8, 529-532.
41. Henderson, I.R., Cappello, R. and Nataro, J.P. (2000b). Autotransporter proteins, evolution and redefining protein secretion, response. Trends Microbiol. 8, 534-535.
42. Henderson, I.R. and Nataro, J.P. (2001). Virulence functions of autotransporter proteins. Infect. Immun. 69, 1231-1243.
43. Henderson, I.R., Nataro, J.P., Kaper, J.B., Meyer, T.F., Farrand, S.K., Burns, D.L., Finlay, B.B. and St Geme, J.W., 3rd. (2000c). Renaming protein secretion in the Gram-negative bacteria. Trends Microbiol. 8, 352.
44. Henderson, I.R., Navarro-Garcia, F. and Nataro, J.P. (1998). The great escape, structure and function of the autotransporter proteins. Trends Microbiol. 6, 370-378.
45. Hendrixson, D.R., de la Morena, M.L., Stathopoulos, C. and St Geme, J.W., 3rd. (1997). Structural determinants of processing and secretion of the Haemophilus influenzae Hap protein. Mol. Microbiol. 26, 505-518.
46. Hoiczyk, E., Roggenkamp, A., Reichenbecher, M., Lupas, A. and Heesemann, J. (2000). Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins. EMBO J. 19, 5989-5999.
47. Ignatova, Z., Hornle, C., Nurk, A. and Kasche, V. (2002). Unusual signal peptide directs penicillin amidase from Escherichia coli to the Tat translocation machinery. Biochem. Biophys. Res. Commun. 291, 146-149.
48. Ize, B., Gerard, F. and Wu, L.F. (2002). In vivo assessment of the Tat signal peptide specificity in Escherichia coli. Arch. Microbiol. 178, 548-553.
49. Jacob-Dubuisson, F., Antoine, R. and Locht, C. (2000). Autotransporter proteins, evolution and redefining protein secretion, response. Trends Microbiol. 8, 533-534.
50. Jacob-Dubuisson, F., Buisine, C., Willery, E., Renauld-Mongenie, G. and Locht, C. (1997). Lack of functional complementation between Bordetella pertussis filamentous hemagglutinin and Proteus mirabilis HpmA hemolysin secretion machineries. J. Bacteriol. 179, 775-783.
51. Jacob-Dubuisson, F., El-Hamel, C., Saint, N., Guedin, S., Willery, E., Molle, G. and Locht, C. (1999). Channel formation by FhaC, the outer membrane protein involved in the secretion of the Bordetella pertussis filamentous hemagglutinin. J. Biol. Chem. 274, 37731-37735.
52. Jacob-Dubuisson, F., Locht, C. and Antoine, R. (2001). Two-partner secretion in Gram-negative bacteria, a thrifty, specific pathway for large virulence proteins. Mol. Microbiol. 40, 306-313.
53. Jansen, C., Heutink, M., Tommassen, J. and de Cock, H. (2000). The assembly pathway of outer membrane protein PhoE of Escherichia coli. Eur. J. Biochem. 267, 3792-3800.
54. Jose, J., Jahnig, F. and Meyer, T.F. (1995). Common structural features of IgA1 protease-like outer membrane protein autotransporters. Mol. Microbiol. 18, 378-380.
55. Jose, J., Kramer, J., Klauser, T., Pohlner, J. and Meyer, T.F. (1996). 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. 178, 107-110.
56. Kim, J., Rusch, S., Luirink, J. and Kendall, D.A. (2001). Is Ffh required for export of secretory proteins? FEBS Lett. 505, 245-248.
57. Klauser, T., Kramer, J., Otzelberger, K., Pohlner, J. and Meyer, T.F. (1993a). Characterization of the Neisseria Iga β-core. The essential unit for outer membrane targeting and extracellular protein secretion. J. Mol. Biol. 234, 579-593.
58. Klauser, T., Pohlner, J. and Meyer, T.F. (1990). Extracellular transport of cholera toxin B subunit using Neisseria IgA protease β-domain, conformation-dependent outer membrane translocation. EMBO J. 9, 1991-1999.
59. Klauser, T., Pohlner, J. and Meyer, T.F. (1992). Selective extracellular release of cholera toxin B subunit by Escherichia coli, dissection of Neisseria Iga β-mediated outer membrane transport. EMBO J. 11, 2327-2335.
60. Klauser, T., Pohlner, J. and Meyer, T.F. (1993b). The secretion pathway of IgA protease-type proteins in Gram-negative bacteria. Bioessays. 15, 799-805.
61. Koch, H.G., Hengelage, T., Neumann-Haefelin, C., MacFarlane, J., Hoffschulte, H.K., Schimz, K.L., Mechler, B. and Muller, M. (1999). 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, 2163-2173.
62. Koch, H.G., Moser, M. and Muller, M. (2003). Signal recognition particle-dependent protein targeting, universal to all kingdoms of life. Rev. Physiol. Biochem. Pharmacol. 146, 55-94.
63. Koronakis, V., Sharff, A., Koronakis, E., Luisi, B. and Hughes, C. (2000). Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature. 405, 914-919.
64. Lazar, S.W. and Kolter, R. (1996). SurA assists the folding of Escherichia coli outer membrane proteins. J Bacteriol. 178, 1770-1773.
65. Li, L.J., Dougan, G., Novotny, P. and Charles, I.G. (1991). P.70 pertactin, an outer-membrane protein from Bordetella parapertussis, cloning, nucleotide sequence and surface expression in Escherichia coli. Mol. Microbiol. 5, 409-417.
66. Loveless, B.J. and Saier, M.H., Jr. (1997). A novel family of channel-forming, autotransporting, bacterial virulence factors. Mol. Membr. Biol. 14, 113-123.
67. Ma, B., Tsai, C.J. and Nussinov, R. (2000). Binding and folding, in search of intramolecular chaperone-like building block fragments. Protein Eng. 13, 617-627.
68. Mallik, I., Smith, M.A. and Flower, A.M. (2002). Recognition of secretory proteins in Escherichia coli requires signals in addition to the signal sequence and slow folding. BMC Microbiol. 2, 32.
69. Manting, E.H. and Driessen, A.J. (2000). Escherichia coli translocase, the unravelling of a molecular machine. Mol. Microbiol. 37, 226-238.
70. Martoglio, B. and Dobberstein, B. (1998). Signal sequences, more than just greasy peptides. Trends Cell Biol. 8, 410-415.
71. Masignani, V., Comanducci, M., Giuliani, M.M., Bambini, S., Adu-Bobie, J., Arico, B., Brunelli, B., Pieri, A., Santini, L., Savino, S., Serruto, D., Litt, D., Kroll, S., Welsch, J.A., Granoff, D.M., Rappuoli, R. and Pizza, M. (2003). Vaccination against Neisseria meningitidis using three variants of the lipoprotein GNA1870. J. Exp. Med. 197, 789-799.
72. Maurer, J., Jose, J. and Meyer, T.F. (1999). Characterization of the essential transport function of the AIDA-I autotransporter and evidence supporting structural predictions. J. Bacteriol. 181, 7014-7020.
73. Miyazaki, H., Yanagida, N., Horinouchi, S. and Beppu, T. (1989). Characterization of the precursor of Serratia marcescens serine protease and COOH-terminal processing of the precursor during its excretion through the outer membrane of Escherichia coli. J. Bacteriol. 171, 6566-6572.
74. Mori, H. and Ito, K. (2001). The Sec protein-translocation pathway. Trends Microbiol. 9, 494-500.
75. Morona, R. and Van Den Bosch, L. (2003). Multicopy icsA is able to suppress the virulence defect caused by the wzz(SF) mutation in Shigella flexneri. FEMS Microbiol. Lett. 221, 213-219.
76. Muller, M., Koch, H.G., Beck, K. and Schafer, U. (2001). Protein traffic in bacteria, multiple routes from the ribosome to and across the membrane. Prog Nucleic Acid Res Mol Biol. 66, 107-157.
77. Murzin, A.G., Lesk, A.M. and Chothia, C. (1994a). Principles determining the structure of β-sheet barrels in proteins. I. A theoretical analysis. J. Mol. Biol. 236, 1369-1381.
78. Murzin, A.G., Lesk, A.M. and Chothia, C. (1994b). Principles determining the structure of β -sheet barrels in proteins. II. The observed structures. J. Mol. Biol. 236, 1382-1400.
79. Nielsen, H., Brunak, S. and von Heijne, G. (1999). Machine learning approaches for the prediction of signal peptides and other protein sorting signals. Protein Eng. 12, 3-9.
80. Nikaido, H. (1992). Porins and specific channels of bacterial outer membranes. Mol. Microbiol. 6, 435-442.
81. Nikaido, H. (1994). Porins and specific diffusion channels in bacterial outer membranes. J. Biol. Chem. 269, 3905-3908.
82. Nummelin, H., Merckel, M.C., el Tahir, Y., Ollikka, P., Skurnik, M. and Goldman, A. (2003). Structural studies of Yersinia adhesin YadA. Adv Exp Med Biol. 529, 85-88.
83. Odenbreit, S., Till, M., Hofreuter, D., Faller, G. and Haas, R. (1999). Genetic and functional characterization of the alpAB gene locus essential for the adhesion of Helicobacter pylori to human gastric tissue. Mol. Microbiol. 31, 1537-1548.
84. Ohnishi, Y., Nishiyama, M., Horinouchi, S. and Beppu, T. (1994). Involvement of the COOH-terminal pro-sequence of Serratia marcescens serine protease in the folding of the mature enzyme. J. Biol. Chem. 269, 32800-32806.
85. Oliver, D.C., Huang, G. and Fernandez, R.C. (2003a). Identification of secretion determinants of the Bordetella pertussis BrkA autotransporter. J. Bacteriol. 185, 489-495.
86. Oliver, D.C., Huang, G., Nodel, E., Pleasance, S. and Fernandez, R.C. (2003b). A conserved region within the Bordetella pertussis autotransporter BrkA is necessary for folding of its passenger domain. Mol. Microbiol. 47, 1367-1383.
87. Owen, P., Meehan, M., de Loughry-Doherty, H. and Henderson, I.R. (1996). Phase-variable outer membrane proteins in Escherichia coli. FEMS Immunol. Med. Microbiol. 16, 63-76.
88. Peterson, J.H., Woolhead, C.A. and Bernstein, H.D. (2003). Basic amino acids in a distinct subset of signal peptides promote interaction with the signal recognition particle. J. Biol. Chem. 29,(Papers In Press, published online ahead of print August 29, 2003).
89. Pohlner, J., Halter, R., Beyreuther, K. and Meyer, T.F. (1987). Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature. 325, 458-462.
90. Pugsley, A.P. (1993). The complete general secretory pathway in Gram-negative bacteria. Microbiol. Rev. 57, 50-108.
91. Purdy, G.E., Hong, M. and Payne, S.M. (2002). Shigella flexneri DegP facilitates IcsA surface expression and is required for efficient intercellular spread. Infect. Immun. 70, 6355-6364.
92. Qi, H.Y., Hyndman, J.B. and Bernstein, H.D. (2002). DnaK promotes the selective export of outer membrane protein precursors in SecA-deficient Escherichia coli. J. Biol. Chem. 277, 51077-51083.
93. Randall, L.L. and Hardy, S.J. (2002). SecB, one small chaperone in the complex milieu of the cell. Cell Mol. Life Sci. 59, 1617-1623.
94. Randall, L.L., Topping, T.B., Suciu, D. and Hardy, S.J. (1998). Calorimetric analyses of the interaction between SecB and its ligands. Protein Sci. 7, 1195-1200.
95. Renauld-Mongenie, G., Cornette, J., Mielcarek, N., Menozzi, F.D. and Locht, C. (1996). Distinct roles of the N-terminal and C-terminal precursor domains in the biogenesis of the Bordetella pertussis filamentous hemagglutinin. J. Bacteriol. 178, 1053-1060.
96. Roggenkamp, A., Ackermann, N., Jacobi, C.A., Truelzsch, K., Hoffmann, H. and Heesemann, J. (2003). Molecular analysis of transport and oligomerization of the Yersinia enterocolitica adhesin YadA. J. Bacteriol. 185, 3735-3744.
97. Salmond, G.P. and Reeves, P.J. (1993). Membrane traffic wardens and protein secretion in Gram-negative bacteria. Trends Biochem. Sci. 18, 7-12.
98. Samuelson, J.C., Chen, M., Jiang, F., Moller, I., Wiedmann, M., Kuhn, A., Phillips, G.J. and Dalbey, R.E.(2000). YidC mediates membrane protein insertion in bacteria. Nature. 406, 637-641.
99. Sandkvist, M. (2001). Biology of type II secretion. Mol. Microbiol. 40, 271-283.
100. Sapriel, G., Wandersman, C. and Delepelaire, P. (2003). The SecB chaperone is bifunctional in Serratia marcescens, SecB is involved in the Sec pathway and required for HasA secretion by the ABC transporter. J. Bacteriol. 185, 80-88.
101. Schonherr, R., Tsolis, R., Focareta, T. and Braun, V. (1993). Amino acid replacements in the Serratia marcescens haemolysin ShlA define sites involved in activation and secretion. Mol. Microbiol. 9, 1229-1237.
102. Schulz, G.E. (2003). Transmembrane beta-barrel proteins. Adv. Protein Chem. 63, 47-70.
103. Serruto, D., Adu-Bobie, J., Scarselli, M., Veggi, D., Pizza, M., Rappuoli, R. and Arico, B. (2003). Neisseria meningitidis App, a new adhesin with autocatalytic serine protease activity. Mol. Microbiol. 48, 323-334.
104. Sexton, J.A. and Vogel, J.P. (2002). Type IVB secretion by intracellular pathogens. Traffic. 3, 178-185.
105. Shannon, J.L. and Fernandez, R.C. (1999). The C-terminal domain of the Bordetella pertussis autotransporter BrkA forms a pore in lipid bilayer membranes. J. Bacteriol. 181, 5838-5842.
106. Shere, K.D., Sallustio, S., Manessis, A., D'Aversa, T.G. and Goldberg, M.B. (1997). Disruption of IcsP, the major Shigella protease that cleaves IcsA, accelerates actin-based motility. Mol. Microbiol. 25, 451-462.
107. Sijbrandi, R., Urbanus, M.L., ten Hagen-Jongman, C.M., Bernstein, H.D., Oudega, B., Otto, B.R. and Luirink, J. (2003). Signal recognition particle (SRP)-mediated targeting and Sec-dependent translocation of an extracellular Escherichia coli protein. J. Biol. Chem. 278, 4654-4659.
108. St Geme, J.W., 3rd and Cutter, D. (2000). The Haemophilus influenzae Hia adhesin is an autotransporter protein that remains uncleaved at the C terminus and fully cell associated. J. Bacteriol. 182, 6005-6013.
109. Stathopoulos, C., Hendrixson, D.R., Thanassi, D.G., Hultgren, S.J., St Geme, J.W., 3rd and Curtiss, R., 3rd. (2000). Secretion of virulence determinants by the general secretory pathway in Gram-negative pathogens, an evolving story. Microbes. Infect. 2, 1061-1072.
110. Steinhauer, J., Agha, R., Pham, T., Varga, A.W. and Goldberg, M.B. (1999). The unipolar Shigella surface protein IcsA is targeted directly to the bacterial old pole, IcsP cleavage of IcsA occurs over the entire bacterial surface. Mol. Microbiol. 32, 367-377.
111. Struyve, M., Moons, M. and Tommassen, J. (1991). Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J. Mol. Biol. 218, 141-148.
112. Szabady, R.L. and Bernstein, H.D. (2003). Function of the unusual signal peptide of the autotransporter protein EspP. In, 103th General Meeting. Washington D.C., American Society of Microbiology.
113. Tamm, A., Tarkkanen, A.M., Korhonen, T.K., Kuusela, P., Toivanen, P. and Skurnik, M. (1993). Hydrophobic domains affect the collagen-binding specificity and surface polymerization as well as the virulence potential of the YadA protein of Yersinia enterocolitica. Mol. Microbiol. 10, 995-1011.
114. Tamm, L.K., Arora, A. and Kleinschmidt, J.H. (2001). Structure and assembly of beta-barrel membrane proteins. J. Biol. Chem. 276, 32399-32402.
115. Thanassi, D.G. (2002). Ushers and secretins, channels for the secretion of folded proteins across the bacterial outer membrane. J. Mol. Microbiol. Biotechnol. 4, 11-20.
116. Thanassi, D.G. and Hultgren, S.J. (2000). Multiple pathways allow protein secretion across the bacterial outer membrane. Curr. Opin. Cell Biol. 12, 420-430.
117. Turner, D.P., Wooldridge, K.G. and Ala'Aldeen, D.A. (2002). Autotransported serine protease A of Neisseria meningitidis, an immunogenic, surface-exposed outer membrane, and secreted protein. Infect. Immun. 70, 4447-4461.
118. Valent, Q.A. (2001). Signal recognition particle mediated protein targeting in Escherichia coli. Antonie Van Leeuwenhoek. 79, 17-31.
119. Valent, Q.A., Scotti, P.A., High, S., de Gier, J.W., von Heijne, G., Lentzen, G., Wintermeyer, W., Oudega, B. and Luirink, J. (1998). The Escherichia coli SRP and SecB targeting pathways converge at the translocon. EMBO J. 17, 2504-2512.
120. Valls, M., Atrian, S., de Lorenzo, V. and Fernandez, L.A. (2000). Engineering a mouse metallothionein on the cell surface of Ralstonia eutropha CH34 for immobilization of heavy metals in soil. Nat. Biotechnol. 18, 661-665.
121. Veiga, E., de Lorenzo, V. and Fernandez, L.A. (1999). Probing secretion and translocation of a beta-autotransporter using a reporter single-chain Fv as a cognate passenger domain. Mol. Microbiol. 33, 1232-1243.
122. Veiga, E., Sugawara, E., Nikaido, H., de Lorenzo, V. and Fernandez, L.A. (2002). Export of autotransported proteins proceeds through an oligomeric ring shaped by C-terminal domains. EMBO J. 21, 2122-2131.
123. von Heijne, G. (1998). Life and death of a signal peptide. Nature. 396, 111-113.
124. Voulhoux, R., Bos, M.P., Geurtsen, J., Mols, M. and Tommassen, J. (2003). Role of a highly conserved bacterial protein in outer membrane protein assembly. Science. 299, 262-265.
125. Watanabe, M. and Blobel, G. (1989). SecB functions as a cytosolic signal recognition factor for protein export in Escherichia coli. Cell. 58, 695-705.
126. Watanabe, M. and Blobel, G. (1995). High-affinity binding of Escherichia coli SecB to the signal sequence region of a presecretory protein. Proc. Natl. Acad. Sci. U S A. 92, 10133-10136.
127. Yen, M.R., Peabody, C.R., Partovi, S.M., Zhai, Y., Tseng, Y.H. and Saier, M.H. (2002). Protein-translocating outer membrane porins of Gram-negative bacteria. Biochim. Biophys. Acta. 1562, 6-31.