Protein secretion through autotransporter and two-partner pathways

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1694, Issue 1-3 SPEC.ISS., 2004, Pages 235-257

  Jacob Dubuisson, Françoise ^a   Fernandez, Rachel ^b   Coutte, Loic ^a  

^a INSTITUT PASTEUR DE LILLE   (France)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Autotransporter; Protein secretion; Two partner secretion

Indexed keywords

AUTOTRANSPORTER PROTEIN; LIPOPROTEIN; OUTER MEMBRANE PROTEIN; PROTEIN SUBUNIT; PROTEINASE; SECRETORY PROTEIN; SIGNAL RECOGNITION PARTICLE; TWO PARTNER SECRETION PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; BACTERIUM; BIOTECHNOLOGICAL PROCEDURES; CARBOXY TERMINAL SEQUENCE; CELL SURFACE; CYTOPLASM; CYTOSOL; ENZYME ACTIVITY; GRAM NEGATIVE BACTERIUM; HYDROPHOBICITY; KINETICS; MATURATION; MEMBRANE; MEMBRANE PERMEABILITY; NONHUMAN; OLIGOMERIZATION; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN CROSS LINKING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN TARGETING; PROTEIN TRANSPORT; REVIEW; RNA TRANSLATION;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; GRAM-NEGATIVE BACTERIA; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT;

NEGIBACTERIA;

EID: 8844235655     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2004.03.008     Document Type: Review

References (167)

1. Henderson I.R., Nataro J.P. Virulence functions of autotransporter proteins. Infect. Immun. 69:2001;1231-1243
2. Henderson I.R., Navarro-Garcia F., Nataro J.P. The great escape: structure and function of the autotransporter proteins. Trends Microbiol. 6:1998;370-378
3. Jacob-Dubuisson F., Locht C., Antoine R. Two-partner secretion in Gram-negative bacteria: a thrifty, specific pathway for large virulence proteins. Mol. Microbiol. 40:2001;306-313
4. Yen M.-R., Peabody C.R., Partovi S.M., Zhai Y., Tseng Y.-H., Saier M.H. Protein-translocating outer membrane porins of Gram-negative bacteria. Biochem. Biophys. Acta. 1562:2002;6-31
5. Henderson I.R., Nataro J.P., Kaper J.B., Meyer T.F., Farrand S.K., Burns D.L., Finlay B.B., St. Geme J.W. Renaming protein secretion in the Gram-negative bacteria. Trends Microbiol. 8:2000;352
6. Henderson I.R., Cappello R., Nataro J.P. Autotransporter proteins, evolution and redefining protein secretion. Trends Microbiol. 8:2000;529-532
7. Jacob-Dubuisson F., Rudy A., Locht C. Autotransporter proteins, evolution and redefining protein secretion: response. Trends Microbiol. 8:2000;534-535
8. Pugsley A.P. The complete general secretory pathway in Gram-negative bacteria. Microbiol. Rev. 57:1993;50-108
9. Filloux A., Michel G., Bally M. GSP-dependent protein secretion in gram-negative bacteria: the Xcp system of Pseudomonas aeruginosa. FEMS Microbiol. Rev. 22:1998;177-198
10. Sandkvist M. Biology of type II secretion. Mol. Microbiol. 40:2001;271-283
11. Hueck C.J. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:1998;379-433
12. Pohlner J., Halter R., Beyreuther K., Meyer T.F. Gene structure and extracellular secretion of Neisseria gonorrheae IgA protease. Nature. 325:1987;458-462
13. Klauser T., Pohlner J., Meyer T.F. The secretion pathway of IgA protease-type proteins in Gram-negative bacteria. BioEssays. 15:1993;799-805
14. Lin L., Ayala P., Larson J., Mulks M., Fukuda M., Carlsson S.R., Enns C., So M. The Neisseria type 2 IgA1 protease cleaves LAMP1 and promotes survival of bacteria within epithelial cells. Mol. Microbiol. 24:1997;1083-1094
15. Pohlner J., Langenberg U., Wölk U., Beck S.C., Meyer T.F. Uptake and nuclear transport of Neisseria IgA1 protease-associated α-proteins in human cells. Mol. Microbiol. 17:1995;1073-1083
16. St. Geme J.W., de la Morena M., Falkow S. A Haemophilus influenzae IgA protease-like protein promotes intimate interaction with human epithelial cells. Mol. Microbiol. 14:1994;217-233
17. Fink D.L., Buscher A.Z., Green B., Fernsten P., St. Geme J.W. III The Haemophilus influenzae Hap autotransporter mediates microcolony formation and adherence to epithelial cells and extracellular matrix via binding regions in the C-terminal end of the passenger domain. Cell. Microbiol. 5:2003;175-186
18. Serruto D., Adu-Bobie J., Scarselli M., Veggi D., Pizza M., Rappuoli R., Arico B. Neisseria meningitidis App, a new adhesin with autocatalytic serine protease activity. Mol. Microbiol. 48:2003;323-334
19. Hendrixson D.R., St. Geme J.W. III The Haemophilus influenzae Hap serine protease promotes adherence and microcolony formation, potentiated by a soluble host protein. Mol. Cell. 2:1998;841-850
20. Fink D.L., St. Geme J.W. III Chromosomal expression of the Haemophilus influenzae Hap autotransporter allows fine-tuned regulation of adhesive potential via inhibition of intermolecular autoproteolysis. J. Bacteriol. 185:2003;1608-1615
21. Benjelloun Touimi Z., Sansonetti P.J., Parsot C. SepA, the major extracellular protein of Shigella flexneri: autonomous secretion and involvement in tissue invasion. Mol. Microbiol. 17:1995;123-135
22. Stathopoulos C., Provence D.L., Curtiss R. Characterization of the avian pathogenic Escherichia coli hemagglutinin Tsh, a member of the immunoglobulin A protease-type family of autotransporters. Infect. Immun. 67:1999;772-781
23. Brunder W., Schmidt H., Karch H. EspP, a novel extracellular serine protease of enterohaemorrhagic Escherichia coli O157:H7 cleaves human coagulation factor V. Mol. Microbiol. 24:1997;767-778
24. Stein M., Kenny B., Stein M.A., Finlay B.B. Characterization of EspC, a 110-kilodalton protein secreted by enteropathogenic Escherichia coli which is homologous to members of the immunoglobulin A protease-like family of secreted proteins. J. Bacteriol. 178:1996;6546-6554
25. Djafari S., Ebel F., Deibel C., Kramer S., Hudel M., Chakraborty T. Characterization of an exported protease from Shiga toxin-producing Escherichia coli. Mol. Microbiol. 25:1997;771-784
26. Eslava C., Navarro-Garcia F., Czeczulin J.R., Henderson I.R., Cravioto A., Nataro J.P. Pet, an autotransporter enterotoxin from enteroaggregative Escherichia coli. Infect. Immun. 66:1998;3155-3163
27. Guyer D.M., Henderson I.R., Nataro J.P., Mobley H.L. Identification of Sat, an autotransporter toxin produced by uropathogenic Escherichia coli. Mol. Microbiol. 38:2000;53-66
28. Henderson I.R., Hicks S., Navarro-Garcia F., Elias W.P., Philips A.D., Nataro J.P. Involvement of the enteroaggregative Escherichia coli plasmid-encoded toxin in causing human intestinal damage. Infect. Immun. 67:1999;5338-5344
29. Dutta P.R., Cappello R., Navarro-Garcia F., Nataro J.P. Functional comparison of serine protease autotransporters of Enterobacteriaceae. Infect. Immun. 70:2002;7105-7113
30. Yanagida N., Uozumi T., Beppu T. Specific excretion of Serratia marcescens protease through the outer membrane of Escherichia coli. J. Bacteriol. 166:1986;937-944
31. Coutte L., Antoine R., Drobecq H., Locht C., Jacob-Dubuisson F. Subtilisin-like autotransporter serves as maturation protease in a bacterial secretion pathway. EMBO J. 20:2001;5040-5048
32. 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. 197:2003;735-742
33. Benz I., Schmidt M.A. 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. 6:1992;1539-1546
34. Laarmann S., Cutter D., Juehne T., Barenkamp S.J., St. Geme J.W. The Haemophilus influenzae Hia autotransporter harbours two adhesive pockets that reside in the passenger domain and recognize the same host cell receptor. Mol. Microbiol. 46:2002;731-743
35. Leininger E., Roberts M., Kenimer J.G., Charles I.G., Fairweather N., Novotny P., Brennan M.J. Pertactin, an Arg-Gly-Asp-containing Bordetella pertussis surface protein that promotes adherence of mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 88:1991;345-349
36. Surana N.K., Cutter D., Barenkamp S.J., St. Geme J.W. III The Haemophilus influenzae Hia autotransporter contains an unusually short, trimeric translocator domain. J. Biol. Chem. 279:2004;14679-14685
37. Kjaergaard K., Schembri M.A., Ramos C., Molin S., Klemm P. Antigen 43 facilitates formation of multispecies biofilms. Environ. Microbiol. 2:2000;695-702
38. Davis J., Smith A.L., Hughes W.R., Golomb M. Evolution of an autotransporter: domain shuffling and lateral transfer from pathogenic Haemophilus to Neisseria. J. Bacteriol. 183:2001;4626-4635
39. Henderson I.R., Lam A.C. Polymorphic proteins of Chlamydia spp.-autotransporters beyond the Proteobacteria. Trends Microbiol. 9:2001;573-578
40. Vandahl B.B., Pedersen A.S., Gevaert K., Holm A., Vandekerckhove J., Christiansen G., Birkelund S. The expression, processing and localization of polymorphic membrane proteins in Chlamydia pneumoniae strain CWL029. BMC Microbiol. 2:2002;36
41. O'Toole P.W., Austin J.W., Trust T.J. Identification and molecular characterization of a major ring-forming surface protein from the gastric pathogen Helicobacter mustelae. Mol. Microbiol. 11:1994;349-361
42. Wilhelm S., Tommassen J., Jaeger K.E. A novel lipolytic enzyme located in the outer membrane of Pseudomonas aeruginosa. J. Bacteriol. 181:1999;6977-6986
43. Schmitt W., Haas R. Genetic analysis of the Helicobacter pylori vacuolating cytotoxin: structural similarities with the IgA protease type of exported protein. Mol. Microbiol. 12:1994;307-319
44. Fernandez R.C., Weiss A.A. Cloning and sequencing of a Bordetella pertussis serum resistance locus. Infect. Immun. 62:1994;4727-4738
45. Steinhauer J., Agha R., Pham T., Varga A.W., Goldberg M.B. 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. 32:1999;367-377
46. Fukuda I., Suzuki T., Munakata H., Hayashi N., Katayama E., Yoshikawa M., Sasakawa C. Cleavage of Shigella surface protein VirG occurs at a specific site, but the secretion is not essential for intracellular spreading. J. Bacteriol. 177:1995;1719-1726
47. Jose J., Jaehnig F., Meyer T.F. Common structural features of IgA1 protease-like outer membrane protein autotransporters. Mol. Microbiol. 18:1995;378-380
48. Benjelloun-Touimi Z., Tahar M.S., Montecucco C., Sansonetti P.J., Parsot C. SepA, the 110 kDa protein secreted by Shigella flexneri: two-domain structure and proteolytic activity. Microbiology. 144:1998;1815-1822
49. Emsley P., Charles I.G., Fairweather N.F., Isaacs N.W. Structure of Bordetella pertussis virulence factor P.69 pertactin. Nature. 381:1996;90-92
50. Oliver D.C., Huang G., Nodel E., Pleasance S., Fernandez R.C. A conserved region within the Bordetella pertussis autotransporter BrkA is necessary for folding of its passenger domain. Mol. Microbiol. 47:2003;1367-1383
51. Kajava A.V., Cheng N., Cleaver R., Kessel M., Simon M.N., Willery E., Jacob-Dubuisson F., Locht C., Steven A.C. Beta-helix model for the filamentous haemagglutinin adhesin of Bordetella pertussis and related bacterial secretory proteins. Mol. Microbiol. 42:2001;279-292
52. Bradley P., Cowen L., Menke M., King J., Berger B. Betawrap: successful prediction of parallel b-helices from primary sequence reveals an association with many microbial pathogens. Proc. Natl. Acad. Sci. U. S. A. 98:2001;14819-14824
53. Nummelin H., Merckel M.C., Leo J.C., Lankinen H., Skurnik M., Goldman A. The Yersinia adhesin YadA collagen-binding domain structure is a novel left-handed parallel beta-roll. EMBO J. 23:2004;701-711
54. Tame J.R.H., van Dooren S.J.M., Oudega B., Otto B.R. Characterization and crystallization of a novel haemoglobinase from pathogenic Escherichia coli. Acta Crystallogr., D Biol. Crystallogr. 58:2002;843-845
55. Roggenkamp A., Ackermann N., Jacobi C.A., Truelzsch K., Hoffmann H., Heesemann J. Molecular analysis of transport and oligomerization of the Yersinia enterocolitica adhesin YadA. J. Bacteriol. 185:2003;3735-3744
56. 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
57. Oliver D.C., Huang G., Fernandez R.C. Identification of secretion determinants of the Bordetella pertussis BrkA autotransporter. J. Bacteriol. 185:2003;489-495
58. Klauser T., Kramer J., Otzelberger K., Pohlner J., Meyer T.F. Characterization of the Neisseria Iga beta-core. The essential unit for outer membrane targeting and extracellular protein secretion. J. Mol. Biol. 234:1993;579-593
59. Suzuki T., Lett M.-C., Sasakawa C. Extracellular transport of VirG protein in Shigella. J. Biol. Chem. 270:1995;30874-30880
60. Oomen C., van Ulsen P., van Gelder P., Feijen M., Tommassen J., Gros P. Structure of the translocator domain of a bacterial autotransporter. EMBO J. 23:2004;1257-1266
61. Suhr M., Benz I., Schmidt M.A. Processing of the AIDA-I precursor: removal of AIDAc and evidence for the outer membrane anchoring as a beta-barrel structure. Mol. Microbiol. 22:1996;31-42
62. Konieczny M.P.J., Benz I., Hollinderbaumer B., Beinke C., Niederweis M., Schmidt M.A. Modular organization of the AIDA autotransporter translocator: the N-terminal beta1-domain is surface-exposed and stabilizes the transmembrane beta2-domain. Antonie Van Leeuwenhoek. 80:2001;19-34
63. Hoiczyk E., Roggenkamp A., Reichenbecher M., Lupas A., Heesemann J. Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins. EMBO J. 19:2000;5989-5999
64. Touze T., Hayward R.D., Eswaran J., Leong J.M., Koronakis V. Self-association of EPEC intimin mediated by the beta-barrel-containing anchor domain: a role in clustering of the Tir receptor. Mol. Microbiol. 51:2004;73-87
65. Hertle R. Serratia type pore forming toxins. Curr. Protein Pept. Sci. 1:2000;75-89
66. Uphoff T.S., Welch R.A. Nucleotide sequencing of the Proteus mirabilis calcium-independent hemolysin genes (hpmA and hpmB) reveals sequence similarity with the Serratia marcescens hemolysin genes (shlA and shlB). J. Bacteriol. 172:1990;1206-1216
67. Hirono I., Tange N., Aoki T. Iron-regulated haemolysin from Edwardsiella tarda. Mol. Microbiol. 24:1997;851-856
68. Strauss E.J., Ghori N., Falkow S. An Edwardsiella tarda strain containing a mutation in a gene with homology to shlB and hpmB is defective for entry into epithelial cells in culture. Infect. Immun. 65:1997;3924-3932
69. Hertle R. Serratia marcescens hemolysin (ShlA) binds artificial membranes and forms pores in a receptor-independent manner. J. Membr. Biol. 189:2002;1-14
70. Hertle R., Hilger M., Weingardt-Kocher S., Walev I. Cytotoxic action of Serratia marcescens hemolysin on human epithelial cells. Infect. Immun. 67:1999;817-825
71. Sieben S., Hertle R., Gumpert J., Braun V. The Serratia marcescens hemolysin is secreted but not activated by stable protoplast-type L-forms of Proteus mirabilis. Arch. Microbiol. 170:1998;236-242
72. Locht C., Bertin P., Menozzi F.D., Renauld G. The filamentous haemagglutinin, a multifaceted adhesin produced by virulent Bordetella spp. Mol. Microbiol. 9:1993;653-660
73. Menozzi F.D., Boucher P.E., Riveau G., Gantiez C., Locht C. Surface-associated filamentous hemagglutinin induces autoagglutination of Bordetella pertussis. Infect. Immun. 62:1994;4261-4269
74. St. Geme J.W.I. The HMW1 adhesin of nontypeable Haemophilus influenzae recognizes sialylated glycoprotein receptors on cultured human epithelial cells. Infect. Immun. 62:1994;3881-3889
75. Kelle K., Pages J.M., Bolla J.M. A putative adhesin gene cloned from Campylobacter jejuni. Res. Microbiol. 149:1998;723-733
76. Rojas C.M., Hyun Ham J., Deng W.L., Doyle J.J., Collmer A. HecA, a member of a class of adhesins produced by diverse pathogenic bacteria, contributes to the attachment, aggregation, epidermal cell killing, and virulence phenotypes of Erwinia chrysanthemi EC16 on Nicotiana clevelandii seedlings. Proc. Natl. Acad. Sci. U. S. A. 99:2002;13142-13147
77. Ward C.K., Latimer J.L., Nika J., Vakevainen M., Mock J.R., Deng K., Blick R.J., Hansen E.J. Mutations in the lspA1 and lspA2 genes of Haemophilus ducreyi affect the virulence of this pathogen in an animal model system. Infect. Immun. 71:2003;2478-2486
78. Cope L.D., Thomas S.E., Latimer J.L., Slaughter C.A., Müller-Eberhard U., Hansen E.J. The 100-kDa haem:hemopexin-binding protein of Haemophilus influenzae: structure and localization. Mol. Microbiol. 13:1994;863-873
79. Cope L.D., Thomas S.E., Hrkal Z., Hansen E.J. Binding of heme-hemopexin complexes by soluble HxuA protein allows utilization of this complexed heme by Haemophilus influenzae. Infect. Immun. 66:1998;4511-4516
80. Locht C., Antoine R., Jacob-Dubuisson F. Bordetella pertussis, molecular pathogenesis under multiple aspects. Curr. Opin. Microbiol. 4:2001;82-89
81. Nouwens A.S., Beatson S.A., Whitchurch C.B., Walsh B.J., Schweizer H.P., Mattick J.S., Cordwell S.J. Proteome analysis of extracellular proteins regulated by the las and rhl quorum sensing systems in Pseudomonas aeruginosa PAO1. Microbiology. 149:2003;1311-1322
82. Salanoubat M., Genin S., Artiguenave F., Gouzy J., Mangenot S., Arlat M., Billault A., Brottier P., Camus J.C., Cattolico L., Chandler M., Choisne N., Claudel-Renard C., Cunnac S., Demange N., Gaspin C., Lavie M., Moisan A., Robert C., Saurin W., Schiex T., Siguier P., Thebault P., Whalen M., Wincker P., Levy M., Weissenbach J., Boucher C.A. Genome sequence of the plant pathogen Ralstonia solanacearum. Nature. 415:2002;497-502
83. Makhov A.M., Hannah J.H., Brennan M.J., Trus B.L., Kocsis E., Conway J.F., Wingfield P.T., Simon M.N., Steven A.C. Filamentous hemagglutinin of Bordetella pertussis. A bacterial adhesin formed as a 50-nm monomeric rigid rod based on a 19-residue repeat motif rich in beta strands and turns. J. Mol. Biol. 241:1994;110-124
84. Klemm P., Hjerrild L., Gjermansen M., Schembri M.A. Structure-function analysis of the self-recognizing Antigen 43 autotransporter protein from Escherichia coli. Mol. Microbiol. 51:2004;283-296
85. Domenighini M., Relman D., Capiau C., Falkow S., Prugnola A., Scarlato V., Rappuoli R. Genetic characterization of Bordetella pertussis filamentous hemagglutinin: a protein processed from an unusually large precursor. Mol. Microbiol. 4:1990;787-800
86. Ward C.K., Lumbley S.R., Latimer J.L., Cope L.D., Hansen E.J. Haemophilus ducreyi secretes a filamentous hemagglutinin-like protein. J. Bacteriol. 180:1998;6013-6022
87. Barenkamp S.J., Leininger E. Cloning, expression and DNA sequence analysis of genes encoding nontypeable Haemophilus influenzae high-molecular-weight surface-exposed proteins related to filamentous hemagglutinin of Bordetella pertussis. Infect. Immun. 60:1992;1302-1313
88. Renauld-Mongénie G., Cornette J., Mielcarek N., Menozzi F.D., Locht C. Distinct roles of the N-terminal and the C-terminal precursor domains in the biogenesis of the Bordetella pertussis filamentous hemagglutinin. J. Bacteriol. 178:1996;1053-1060
89. Schonherr R., Tsolis R., Focareta T., Braun V. Amino acid replacements in the Serratia marcescens haemolysin ShIA define sites involved in activation and secretion. Mol. Microbiol. 9:1993;1229-1237
90. Uphoff T.S., Welch R.A. Crosa C.I.C.a.J.H. Molecular Mechanisms of Bacterial Virulence. 1994;283-292 Kluwer Academics Publishing, Dordrecht
91. Grass S., St. Geme J.W. III Maturation and secretion of the non-typable Haemophilus influenzae HMW1 adhesin: roles of the N-terminal and C-terminal domains. Mol. Microbiol. 36:2000;55-67
92. Clantin B., Hodak H., Willery E., Locht C., Jacob-Dubuisson F., Villeret V. The crystal structure of filamentous haemagglutinin secretion domain and its implications for the two-partner secretion pathway. Proc. Natl. Acad. Sci. U. S. A. 101:2004;6194-6199
93. Jacob-Dubuisson F., Buisine C., Willery E., Renauld-Mongenie G., Locht C. Lack of functional complementation between Bordetella pertussis filamentous hemagglutinin and Proteus mirabilis HpmA hemolysin secretion machineries. J. Bacteriol. 179:1997;775-783
94. St. Geme J.W. III, Grass S. Secretion of the Haemophilus influenzae HMW1 and HMW2 adhesins involves a periplasmic intermediate and requires the HMWB and HMWC proteins. Mol. Microbiol. 27:1998;617-630
95. Bolter B., Soll J., Schulz A., Hinnah S., Wagner R. Origin of a chloroplast protein importer. Proc. Natl. Acad. Sci. U. S. A. 95:1998;15831-15836
96. Reumann S., Keegstra K. The endosymbiotic origin of the protein import machinery of chloroplastic envelope membranes. Trends Plant Sci. 4:1999;302-307
97. 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. U. S. A. 96:1999;784-789
98. Voulhoux R., Bos M.P., Geursten J., Mols M., Tommassen J. Role of a highly conserved bacterial protein in outer membrane assembly. Science. 299:2003;262-265
99. Genevrois S., Steeghs L., Roholl P., Letesson J.-J., van der Ley P. The Omp85 protein of Neisseria meningitidis is required for lipid export to the outer membrane. EMBO J. 22:2003;1780-1789
100. Guédin S., Willery E., Tommassen J., Fort E., Drobecq H., Locht C., Jacob-Dubuisson F. Novel topological features for FhaC, the outer membrane transporter involved in the secretion of Bordetella pertussis filamentous hemagglutinin. J. Biol. Chem. 274:2000;37731-37735
101. 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
102. Yang F.L., Braun V. ShlB mutants of Serratia marcescens allow uncoupling of activation and secretion of the ShlA hemolysin. Int. J. Med. Microbiol. 290:2000;529-538
103. Jacob-Dubuisson F., El-Hamel C., Saint N., Guedin 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;37731-37735
104. Ondraczek R., Hobbie S., Braun V. In vitro activation of the Serratia marcescens hemolysin through modification and complementation. J. Bacteriol. 174:1992;5086-5094
105. Hertle R., Brutsche S., Groeger W., Hobbie S., Koch W., Könninger U., Braun V. Specific phosphatidylethanolamine dependence of Serratia marcescens cytotoxin activity. Mol. Microbiol. 26:1997;853-865
106. Hertle R., Süssmuth R., Braun V., Jung G. Two-step fast liquid chromatographic purification of the Serratia marcescens hemolysin and peptide mapping with mass spectrometry. J. Chromatogr., B, Biomed. Sci. Appl. 737:2000;13-23
107. Walker G., Hertle R., Braun V. Activation of Serratia marcescens hemolysin through a conformational change. Infect. Immun. 72:2004;611-614
108. Braun V., Hobbie S., Ondraczek R. Serratia marcescens forms a new type of cytolysin. FEMS Microbiol. Lett. 100:1992;299-306
109. Sijbrandi R., Urbanus M.L., ten Hagen-Jongman C.M., Bernstein H.D., Oudega B., Otto B.R., Luirink J. Signal Recognition Particle (SRP)-mediated Targeting and Sec-dependent Translocation of an Extracellular Escherichia coli Protein. J. Biol. Chem. 278:2003;4654-4659
110. Brandon L.D., Goehring N., Janakiraman A., Yan A.W., Wu T., Beckwith J., Goldberg M.B. IcsA, a polarly localised autotransporter with an atypical signal peptide, uses the Sec apparatus for secretion, although the Sec apparatus is circumferentially distributed. Mol. Microbiol. 50:2003;45-60
111. Lambert-Buisine C., Willery E., Locht C., Jacob-Dubuisson F. N-terminal characterization of the Bordetella pertussis filamentous haemagglutinin. Mol. Microbiol. 28:1998;1283-1293
112. Müller M., Koch H.-G., Beck K., Schäfer U. Protein traffic in bacteria: multiple routes from the ribosome to and across the membrane. Prog. Nucleic Acid Res. Mol. Biol. 66:2001;107-157
113. Peterson J.H., Woolhead C.A., Bernstein H.D. Basic amino acids in a distinct subset of signal peptides promote interaction with the signal recognition particle. J. Biol. Chem. 278:2003;46155-46162
114. Odenbreit S., Till M., Hofreuter D., Faller G., Haas R. Genetic and functional characterization of the alpAB gene locus essential for the adhesion of Helicobacter pylori to human gastric tissue. Mol. Microbiol. 31:1999;1537-1548
115. Turner D.P., Wooldridge K.G., Ala'Aldeen D.A. Autotransported serine protease A of Neisseria meningitidis: an immunogenic, surface-exposed outer membrane, and secreted protein. Infect. Immun. 70:2002;4447-4461
116. Coutte L., Willery E., Antoine R., Drobecq H., Locht C., Jacob-Dubuisson F. Surface anchoring of bacterial subtilisin important for maturation function. Mol. Microbiol. 49:2003;529-539
117. Sankaran K., Wu H.C. Lipid modification of bacterial prolipoprotein. Transfer of diacylglyceryl moiety from phosphatidylglycerol. J. Biol. Chem. 269:1994;19701-19706
118. van Ulsen P., van Alphen L., ten Hove J., Fransen F., van der Ley P., Tommassen J. A Neisserial autotransporter NalP modulating the processing of other autotransporters. Mol. Microbiol. 50:2003;1017-1030
119. Schiebel E., Schwarz H., Braun V. Subcellular localization and unique secretion of the hemolysin of Serratia marcescens. J. Biol. Chem. 264:1989;16311-16320
120. 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
121. Brandon L.D., Goldberg M.B. Periplasmic transit and disulfide bond formation of the autotransported Shigella protein IcsA. J. Bacteriol. 183:2001;951-958
122. Klauser T., Pohlner J., Meyer T.F. Extracellular transport of cholera toxin B subunit using Neisseria IgA protease beta-domain: conformation-dependent outer membrane translocation. EMBO J. 9:1990;1991-1999
123. Klauser T., Pohlner J., Meyer T.F. Selective extracellular release of cholera toxin B subunit by Escherichia coli: dissection of Neisseria Iga beta-mediated outer membrane transport. EMBO J. 11:1992;2327-2335
124. Jose J., Kramer J., Klauser T., Pohlner J., Meyer T.F. 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. 178:1996;107-110
125. Veiga E., de Lorenzo V., Fernandez L.A. Probing secretion and translocation of a beta-autotransporter using a reporter single-chain Fv as a cognate passenger domain. Mol. Microbiol. 33:1999;1232-1243
126. Kjaergaard K., Hasman H., Schembri M.A., Klemm P. Antigen 43-mediated autotransporter display, a versatile bacterial cell surface presentation system. J. Bacteriol. 184:2002;4197-4204
127. Lattemann C.T., Maurer J., Gerland E., Meyer T.F. Autodisplay: functional display of active beta-lactamase on the surface of Escherichia coli by the AIDA-I autotransporter. J. Bacteriol. 182:2000;3726-3733
128. Maurer J., Jose J., Meyer T.F. Autodisplay: one-component system for efficient surface display and release of soluble recombinant proteins from Escherichia coli. J. Bacteriol. 179:1997;794-804
129. Coppens I., Alonso S., Antoine R., Jacob-Dubuisson F., Renauld-Mongenie G., Jacobs E., Locht C. Production of Neisseria meningitidis transferrin-binding protein B by recombinant Bordetella pertussis. Infect. Immun. 69:2001;5440-5446
130. Purdy G.E., Hong M., Payne S.M. Shigella flexneri DegP facilitates IcsA surface expression and is required for efficient intercellular spread. Infect. Immun. 70:2002;6355-6364
131. Shikata S., Shimada K., Ohnishi Y., Horinouchi S., Beppu T. Characterization of secretory intermediates of Serratia marcescens serine protease produced during its extracellular secretion from Escherichia coli cells. J. Biochem. (Tokyo). 114:1993;723-731
132. Shannon J.L., Fernandez R.C. The C-terminal domain of the Bordetella pertussis autotransporter BrkA forms a pore in lipid bilyer membranes. J. Bacteriol. 181:1999;5838-5842
133. Lee H.W., Byun S.M. The pore size of the autotransporter domain is critical for the active translocation of the passenger domain. Biochem. Biophys. Res. Commun. 307:2003;820-825
134. Veiga E., Sugawara E., Nikaido H., De Lorenzo V., Fernandez L.A. Export of autotransported proteins proceeds through an oligomeric ring shaped by C-terminal domains. EMBO J. 21:2002;2122-2131
135. Bosch D., Scholten M., Verhagen C., Tommassen J. The role of the carboxy-terminal membrane-spanning fragment in the biogenesis of Escherichia coli K12 outer membrane protein PhoE. Mol. Gen. Genet. 216:1989;144-148
136. Willems R.J.L., Geuijen C., van der Heide H.G.J., Renauld G., Bertin P., van den Akker W.M.R., Locht C., Mooi F.R. Mutational analysis of the Bordetella pertussis fim/fha gene cluster: identification of a gene with sequence similarities to haemolysin accessory genes involved in export of FHA. Mol. Microbiol. 11:1994;337-347
137. Hendrixson D.R., de la Morena M.L., Stathopoulos C., St. Geme J.W. III Structural determinants of processing and secretion of the Haemophilus influenzae Hap protein. Mol. Microbiol. 26:1997;505-518
138. St. Geme J.W. III, Cutter D. The Haemophilus influenzae Hia adhesin is an autotransporter protein that remains uncleaved at the C terminus and fully cell associated. J. Bacteriol. 82:2000;6005-6013
139. 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. 269:1994;32800-32806
140. Kawai E., Idei A., Kumura H., Shimazaki K., Akatsuka H., Omori K. The ABC-exporter genes involved in the lipase secretion are clustered with the genes for lipase, alkaline protease, and serine protease homologues in Pseudomonas fluorescens no. 33. Biochim. Biophys. Acta. 1446:1999;377-382
141. Charles I., Fairweather N., Pickard D., Besley J., Anderson R., Dougan G., Roberts M. Expression of the Bordetella pertussis P.69 pertactin adhesin in Escherichia coli: fate of the carboxy-terminal domain. Microbiology. 140:1994;3301-3308
142. Passerini di Rossi B.N., Friedman L.E., Gonzales Flecha F.L., Castello P.R., Franco M.A., Rossi J.P.F.C. Identification of Bordetella pertussis virulence-associated outer membrane proteins. FEMS Microbiol. Lett. 172:1999;9-13
143. Miyazaki H., Yanagida N., Horinouchi S., Beppu T. 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. 171:1989;6566-6572
144. Fink D.L., Cope L.D., Hansen E.J., Geme J.W. III The Haemophilus influenzae Hap autotransporter is a chymotrypsin clan serine protease and undergoes autoproteolysis via an intermolecular mechanism. J. Biol. Chem. 276:2001;39492-39500
145. Henderson I.R., Owen P. The major phase-variable outer membrane protein of Escherichia coli structurally resembles the immunoglobulin A1 protease class of exported protein and is regulated by a novel mechanism involving Dam and OxyR. J. Bacteriol. 181:1999;2132-2141
146. Navarro-Garcia F., Canizalez-Roman A., Luna J., Sears C., Nataro J.P. Plasmid-encoded toxin of enteroaggregative Escherichia coli is internalized by epithelial cells. Infect. Immun. 69:2001;1053-1060
147. Nakata N., Tobe T., Fukuda I., Suzuki T., Komatsu K., Yoshikawa M., Sasakawa C. The absence of a surface protease, OmpT, determines the intercellular spreading ability of Shigella: the relationship between the ompT and kcpA loci. Mol. Microbiol. 9:1993;459-468
148. Egile C., d'Hauteville H., Parsot C., Sansonetti P.J. SopA, the outer membrane protease responsible for polar localization of IcsA in Shigella flexneri. Mol. Microbiol. 23:1997;1063-1073
149. Shere K.D., Sallustio S., Manessis A., D'Aversa T.G., Goldberg M.B. Disruption of IcsP, the major Shigella protease that cleaves IcsA, accelerates actin-based motility. Mol. Microbiol. 25:1997;451-462
150. Finn T.M., Amsbaugh D.F. Vag8, a Bordetella pertussis bvg-regulated protein. Infect. Immun. 66:1998;3985-3989
151. Henderson I.R., Czeczulin J., Eslava C., Noriega F., Nataro J.P. Characterization of Pic, a secreted protease of Shigella flexneri and enteroaggregative Escherichia coli. Infect. Immun. 67:1999;5587-5596
152. Gould-Kostka J.L., Burns D.L., Brennan M.J., Manclark C.R. Purification and analysis of the antigenicity of a 69,000 Da protein from Bordetella pertussis. FEMS Microbiol. Lett. 55:1990;285-289
153. Grass S., Buscher A.Z., Swords W.E., Apicella M.A., Barenkamp S.J., Ozchlewski N., St. Geme J.W. III The Haemophilus influenzae HMW1 adhesin is glycosylated in a process that requires HMW1C and phosphoglucomutase, an enzyme involved in lipooligosaccharide biosynthesis. Mol. Microbiol. 48:2003;737-751
154. Benz I., Schmidt M.A. Glycosylation with heptose residues mediated by the aah gene product is essential for adherence of the AIDA-I adhesin. Mol. Microbiol. 40:2001;1403-1413
155. Lindenthal C., Elsinghorst E.A. Identification of a glycoprotein produced by enterotoxigenic Escherichia coli. Infect. Immun. 67:1999;4084-4091
156. Moormann C., Benz I., Schmidt M.A. Functional substitution of the TibC protein of enterotoxigenic Escherichia coli strains for the autotransporter adhesin heptosyltransferase of the AIDA system. Infect. Immun. 70:2002;2264-2270
157. Renauld-Mongénie G., Mielcarek N., Cornette J., Schacht A.-M., Capron A., Riveau G., Locht C. Induction of mucosal immune responses against a heterologous antigen fused to filamentous hemagglutinin after intranasal immunization with recombinant Bordetella pertussis. Proc. Natl. Acad. Sci. U. S. A. 93:1996;7944-7949
158. Reveneau N., Alonso S., Jacob-Dubuisson F., Mercenier A., Locht C. Tetanus toxin fragment C-specific priming by intra-nasal infection with recombinant Bordetella pertussis. Vaccine. 2915:2001;1-8
159. Christiansen G., Pedersen A.S., Hjerno K., Vandahl B., Birkelund S. Potential relevance of Chlamydia pneumoniae surface proteins to an effective vaccine. J. Infect. Dis. 181(Suppl. 3):2000;S528-S537
160. Longbottom D., Russell M., Dunbar S.M., Jones G.E., Herring A.J. Molecular cloning and characterization of the genes coding for the highly immunogenic cluster of 90-kilodalton envelope proteins from the Chlamydia psittaci subtype that causes abortion in sheep. Infect. Immun. 66:1998;1317-1324
161. Ait-Tahar K., Wooldridge K.G., Turner D.P., Atta M., Todd I., Ala'Aldeen D.A. Auto-transporter A protein of Neisseria meningitidis: a potent CD4+ T-cell and B-cell stimulating antigen detected by expression cloning. Mol. Microbiol. 37:2000;1094-1105
162. Crocquet-Valdes P.A., Weiss K., Walker D.H. Sequence analysis of the 190-kDa antigen-encoding gene of Rickettsia conorii (Malish 7 strain). Gene. 140:1994;115-119
163. Li Z., Diaz-Montero C.M., Valbuena G., Yu X.J., Olano J.P., Feng H.M., Walker D.H. Identification of CD8 T-lymphocyte epitopes in OmpB of Rickettsia conorii. Infect. Immun. 71:2003;3920-3926
164. Pizza M., Scarlato V., Masignani V., Giuliani M.M., Arico B., Comanducci M., Jennings G.T., Baldi L., Bartolini E., Capecchi B., Galeotti C.L., Luzzi E., Manetti R., Marchetti E., Mora M., Nuti S., Ratti G., Santini L., Savino S., Scarselli M., Storni E., Zuo P., Broeker M., Hundt E., Knapp B., Blair E., Mason T., Tettelin H., Hood D.W., Jeffries A.C., Saunders N.J., Granoff D.M., Venter J.C., Moxon E.R., Grandi G., Rappuoli R. Identification of vaccine candidates against serogroup B meningococcus by whole-genome sequencing. Science. 287:2000;1816-1820
165. Konieczny M.P., Suhr M., Noll A., Autenrieth I.B., Alexander Schmidt M. Cell surface presentation of recombinant (poly-) peptides including functional T-cell epitopes by the AIDA autotransporter system. FEMS Immunol. Med. Microbiol. 27:2000;321-332
166. Kramer U., Rizos K., Apfel H., Autenrieth I.B., Lattemann C.T. Autodisplay: development of an efficacious system for surface display of antigenic determinants in Salmonella vaccine strains. Infect. Immun. 71:2003;1944-1952
167. Valls M., Atrian S., de Lorenzo V., Fernandez L.A. Engineering a mouse metallothionein on the cell surface of Ralstonia eutropha CH34 for immobilization of heavy metals in soil. Nat. Biotechnol. 18:2000;661-665