Type V secretion: Mechanism(S) of autotransport through the bacterial outer membrane

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 367, Issue 1592, 2012, Pages 1088-1101

  Leo, Jack C ^a   Grin, Iwan ^a   Linke, Dirk ^a  

^a MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

Adhesin; Autotransport; Bacterial cell surface; Bam complex; Outer membrane; Protein secretion

Indexed keywords

ADHESION; BACTERIUM; MEMBRANE; MOLECULAR ANALYSIS; PEPTIDE; PROTEIN; SECRETION; TRANSLOCATION; VIRULENCE;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 84858226936     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2011.0208     Document Type: Review

References (122)

1. Natale, P., Bruser, T. & Driessen, A. J. 2008 Sec- and Tat-mediated protein secretion across the bacterial cytoplasmic membrane-distinct translocases and mechanisms. Biochim. Biophys. Acta 1778, 1735-1756. (doi:10.1016/j.bbamem.2007.07.015)
2. Berks, B. C., Palmer, T. & Sargent, F. 2005 Protein targeting by the bacterial twin-arginine translocation (Tat) pathway. Curr. Opin. Microbiol. 8, 174-181. (doi:10.1016/j.mib.2005.02.010)
3. Lee, P. A., Tullman-Ercek, D. & Georgiou, G. 2006 The bacterial twin-arginine translocation pathway. Annu. Rev. Microbiol. 60, 373-395. (doi:10.1146/annurev.micro.60.080805.142212)
4. Facey, S. J. & Kuhn, A. 2010 Biogenesis of bacterial inner-membrane proteins. Cell. Mol. Life Sci. 67, 2343-2362. (doi:10.1007/s00018-010-0303-0)
5. Mori, H. & Ito, K. 2001 The Sec protein-translocation pathway. Trends Microbiol. 9, 494-500. (doi:10.1016/S0966-842X(01)02174-6)
6. Prilusky, J. & Bibi, E. 2009 Studying membrane proteins through the eyes of the genetic code revealed a strong uracil bias in their coding mRNAs. Proc. Natl Acad. Sci. USA 106, 6662-6666. (doi:10.1073/pnas.0902029106)
7. Rego, A. T., Chandran, V. & Waksman, G. 2010 Two-step and one-step secretion mechanisms in Gram-negative bacteria: contrasting the type IV secretion system and the chaperone-usher pathway of pilus biogenesis. Biochem. J. 425, 475-488. (doi:10. 1042/BJ20091518)
8. Delepelaire, P. 2004 Type I secretion in Gram-negative bacteria. Biochim. Biophys. Acta 1694, 149-161. (doi:10.1016/j.bbamcr.2004.05.001)
9. Coburn, B., Sekirov, I. & Finlay, B. B. 2007 Type III secretion systems and disease. Clin. Microbiol. Rev. 20, 535-549. (doi:10.1128/CMR.00013-07)
10. Wallden, K., Rivera-Calzada, A. & Waksman, G. 2010 Type IV secretion systems: versatility and diversity in function. Cell. Microbiol. 12, 1203-1212. (doi:10.1111/j.1462-5822.2010.01499.x)
11. Johnson, T. L., Abendroth, J., Hol, W.G. & Sandkvist, M. 2006 Type II secretion: from structure to function. FEMS Microbiol. Lett. 255, 175-186. (doi:10.1111/j.1574-6968.2006.00102.x)
12. Bonemann, G., Pietrosiuk, A. & Mogk, A. 2010 Tubules and donuts: a type VI secretion story. Mol.Microbiol. 76, 815-821. (doi:10.1111/j.1365-2958.2010.07171.x)
13. Simeone, R., Bottai, D. & Brosch, R. 2009 ESX/type VII secretion systems and their role in host-pathogen interaction. Curr. Opin. Microbiol. 12, 4-10. (doi:10.1016/j.mib.2008.11.003)
14. Desvaux, M., Hebraud, M., Talon, R. & Henderson, I. R. 2009 Secretion and subcellular localizations of bacterial proteins: a semantic awareness issue. Trends Microbiol. 17, 139-145. (doi:10.1016/j.tim.2009.01.004)
15. Barnhart, M. M. & Chapman, M. R. 2006 Curli biogenesis and function. Annu. Rev. Microbiol. 60, 131-147. (doi:10.1146/annurev.micro.60.080805.142106)
16. Thanassi, D. G., Stathopoulos, C., Karkal, A. & Li, H. 2005 Protein secretion in the absence of ATP: the autotransporter, two-partner secretion and chaperone/ usher pathways of Gram-negative bacteria (review). Mol. Membr. Biol. 22, 63-72. (doi:10.1080/09687860500063290)
17. Jose, J., Jahnig, F. & Meyer, T. F. 1995 Common structural features of IgA1 protease-like outer membrane protein autotransporters. Mol. Microbiol. 18, 378-380. (doi:10.1111/j.1365-2958.1995.mmi_18020378.x)
18. Klauser, T., Pohlner, J. & Meyer, T. F. 1993 The secretion pathway of IgA protease-type proteins in Gram-negative bacteria. Bioessays 15, 799-805. (doi:10.1002/bies.950151205)
19. Jose, J. & Meyer, T. F. 2007 The autodisplay story, from discovery to biotechnical and biomedical applications. Microbiol. Mol. Biol. Rev. 71, 600-619. (doi:10.1128/MMBR.00011-07)
20. Maurer, J., Jose, J. & Meyer, T. F. 1997 Autodisplay: one-component system for efficient surface display and release of soluble recombinant proteins from Escherichia coli. J. Bacteriol. 179, 794-804.
21. Henderson, I. R., Nataro, J. P., Kaper, J. B., Meyer, T. F., Farrand, S. K., Burns, D. L., Finlay, B. B. & St Geme III, J. W. 2000 Renaming protein secretion in the Gram-negative bacteria. Trends. Microbiol. 8, 352. (doi:10.1016/S0966-842X(00)01814-X)
22. Henderson, I. R., Navarro-Garcia, F., Desvaux, M., Fernandez, R. C. & Ala'Aldeen, D. 2004 Type V protein secretion pathway: the autotransporter story. Microbiol. Mol. Biol. Rev. 68, 692-744. (doi:10.1128/MMBR.68.4.692-744.2004)
23. Mulks, M. H. & Plaut, A. G. 1978 IgA protease production as a characteristic distinguishing pathogenic from harmless Neisseriaceae. N. Engl. J. Med. 299, 973-976. (doi:10.1056/NEJM197811022991802)
24. Benz, I. & Schmidt, M. A. 1989 Cloning and expression of an adhesin (AIDA-I) involved in diffuse adherence of enteropathogenic Escherichia coli. Infect. Immun. 57, 1506-1511.
25. Leininger, E., Roberts, M., Kenimer, J.G., Charles, I.G., Fairweather, N., Novotny, P. & Brennan, M. J. 1991 Pertactin, an Arg-Gly-Asp-containing Bordetella pertussis surface protein that promotes adherence of mammalian cells. Proc. Natl Acad. Sci. USA 88, 345-349. (doi:10.1073/pnas.88.2.345)
26. Provence, D. L. & Curtiss III, R. 1994 Isolation and characterization of a gene involved in hemagglutination by an avian pathogenic Escherichia coli strain. Infect. Immun. 62, 1369-1380.
27. Yen, Y. T., Kostakioti, M., Henderson, I. R. & Stathopoulos, C. 2008 Common themes and variations in serine protease autotransporters. Trends Microbiol. 16, 370-379. (doi:10.1016/j.tim.2008.05.003)
28. Kostakioti, M. & Stathopoulos, C. 2006 Role of the alpha-helical linker of the C-terminal translocator in the biogenesis of the serine protease subfamily of autotransporters. Infect. Immun. 74, 4961-4969. (doi:10.1128/IAI.00103-06)
29. Sijbrandi, R., Urbanus, M. L., ten Hagen-Jongman, C. M., Bernstein, H. D., Oudega, B., Otto, B. R. & 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. (doi:10.1074/jbc.M211630200)
30. Jong, W. S., ten Hagen-Jongman, C.M., Ruijter, E., Orru, R. V., Genevaux, P. & Luirink, J. 2010 YidC is involved in the biogenesis of the secreted autotransporter hemoglobin protease. J. Biol. Chem. 285, 39682-39690.
31. Szabady, R. L., Peterson, J. H., Skillman, K. M. & Bernstein, H. D. 2005 An unusual signal peptide facilitates late steps in the biogenesis of a bacterial autotransporter. Proc. Natl Acad. Sci. USA 102, 221-226. (doi:10.1073/pnas.0406055102)
32. Ieva, R. & Bernstein, H. D. 2009 Interaction of an autotransporter passenger domain with BamA during its translocation across the bacterial outer membrane. Proc. Natl Acad. Sci. USA 106, 19120-19125.(doi:10.1073/pnas.0907912106)
33. Ruiz-Perez, F., Henderson, I. R., Leyton, D. L., Rossiter, A. E., Zhang, Y. & Nataro, J. P. 2009 Roles of periplasmic chaperone proteins in the biogenesis of serine protease autotransporters of Enterobacteriaceae.J. Bacteriol. 191, 6571-6583. (doi:10.1128/JB.00754-09)
34. Ruiz-Perez, F., Henderson, I. R. & Nataro, J. P. 2010 Interaction of FkpA, a peptidyl-prolyl cis/trans isomerase with EspP autotransporter protein. Gut. Microbes 1, 339-344. (doi:10.4161/gmic.1.5.13436)
35. Sauri, A., Soprova, Z., Wickstrom, D., de Gier, J. W., Van der Schors, R. C., Smit, A. B., Jong, W. S. & Luirink, J. 2009 The Bam (Omp85) complex is involved in secretion of the autotransporter haemoglobin protease. Microbiology 155, 3982-3991. (doi:10.1099/mic.0.034991-0)
36. Grosskinsky, U., Schutz, M., Fritz, M., Schmid, Y., Lamparter, M.C., Szczesny, P., Lupas, A.N., Autenrieth, I. B. & Linke, D. 2007 A conserved glycine residue of trimeric autotransporter domains plays a key role in Yersinia adhesin A autotransport. J. Bacteriol. 189, 9011-9019. (doi:10.1128/JB.00985-07)
37. Junker, M., Schuster, C. C., McDonnell, A. V., Sorg, K. A., Finn, M. C., Berger, B. & Clark, P. L. 2006 Pertactin beta-helix folding mechanism suggests common themes for the secretion and folding of autotransporter proteins. Proc. Natl Acad. Sci. USA 103, 4918-4923. (doi:10.1073/pnas.0507923103)
38. Pollock, M. R. & Richmond, M. H. 1962 Low cyst(e)ine content of bacterial extracellular proteins: its possible physiological significance. Nature 194, 446-449. (doi:10.1038/194446a0)
39. Jose, J., Kramer, J., Klauser, T., Pohlner, J. & 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. (doi:10.1016/0378-1119(96)00343-5)
40. Knowles, T. J., Scott-Tucker, A., Overduin, M. & Henderson, I. R. 2009 Membrane protein architects: the role of the BAM complex in outer membrane protein assembly. Nat. Rev. Microbiol. 7, 206-214. (doi:10.1038/nrmicro2069)
41. Arnold, T., Poynor, M., Nussberger, S., Lupas, A. N. & Linke, D. 2007 Gene duplication of the eight-stranded beta-barrel OmpX produces a functional pore: a scenario for the evolution of transmembrane beta-barrels. J. Mol. Biol. 366, 1174-1184. (doi:10.1016/j.jmb.2006.12.029)
42. Remmert, M., Biegert, A., Linke, D., Lupas, A. N. & Soding, J. 2010 Evolution of outer membrane betabarrels from an ancestral beta beta hairpin. Mol. Biol. Evol. 27, 1348-1358. (doi:10.1093/molbev/msq017)
43. Kleinschmidt, J. H. 2006 Folding kinetics of the outer membrane proteins OmpA and FomA into phospholipid bilayers. Chem. Phys. Lipids 141, 30-47. (doi:10.1016/j.chemphyslip.2006.02.004)
44. Robert, V., Volokhina, E. B., Senf, F., Bos, M. P., Van Gelder, P. & Tommassen, J. 2006 Assembly factor Omp85 recognizes its outer membrane protein substrates by a species-specific C-terminal motif. PLoS Biol. 4, e377. (doi:10.1371/journal.pbio.0040377)
45. Neuwald, A. F., Liu, J. S. & Lawrence, C. E. 1995 Gibbs motif sampling: detection of bacterial outer membrane protein repeats. Protein Sci. 4, 1618-1632. (doi:10.1002/pro.5560040820)
46. Struyve, M., Moons, M. & Tommassen, J. 1991 Carboxyterminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J. Mol. Biol. 218, 141-148. (doi:10.1016/0022-2836(91)90880-F)
47. Jain, S. & Goldberg, M. B. 2007 Requirement for YaeT in the outer membrane assembly of autotransporter proteins. J. Bacteriol. 189, 5393-5398. (doi:10.1128/JB.00228-07)
48. Ieva, R., Tian, P., Peterson, J. H. & Bernstein, H. D. 2011 Sequential and spatially restricted interactions of assembly factors with an autotransporter beta domain. Proc. Natl Acad. Sci. USA 108, E383-E391. (doi:10.1073/pnas.1103827108)
49. Sauri, A., Oreshkova, N., Soprova, Z., Jong, W. S., Sani, M., Peters, P. J., Luirink, J. & van Ulsen, P. 2011 Autotransporter beta-domains have a specific function in protein secretion beyond outer-membranetargeting. J. Mol. Biol. 412, 553-567. (doi:10.1016/j.jmb.2011.07.035)
50. Pohlner, J., Halter, R., Beyreuther, K. & Meyer, T. F. 1987 Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 325, 458-462. (doi:10.1038/325458a0)
51. Oomen, C. J., van Ulsen, P., van Gelder, P., Feijen, M., Tommassen, J. & Gros, P. 2004 Structure of the translocator domain of a bacterial autotransporter. EMBO J. 23, 1257-1266. (doi:10.1038/sj.emboj.7600148)
52. van den Berg, B. 2011 Crystal structure of a full-length autotransporter. J. Mol. Biol. 396, 627-633. (doi:10.1016/j.jmb.2009.12.061)
53. Barnard, T. J., Dautin, N., Lukacik, P., Bernstein, H.D. & Buchanan, S. K. 2007 Autotransporter structure reveals intra-barrel cleavage followed by conformational changes. Nat. Struct. Mol. Biol. 14, 1214-1220. (doi:10.1038/nsmb1322)
54. Soprova, Z., Sauri, A., van Ulsen, P., Tame, J. R., den Blaauwen, T., Jong, W. S. & Luirink, J. 2010 A conserved aromatic residue in the autochaperone domain of the autotransporter Hbp is critical for initiation of outer membrane translocation. J. Biol. Chem. 285, 38224-38233.
55. Peterson, J. H., Tian, P., Ieva, R., Dautin, N. & Bernstein, H. D. 2010 Secretion of a bacterial virulence factor is driven by the folding of a C-terminal segment. Proc. Natl Acad. Sci. USA 107, 17739-17744.
56. Oliver, D. C., Huang, G. & Fernandez, R. C. 2003 Identification of secretion determinants of the Bordetella pertussis BrkA autotransporter. J. Bacteriol. 185, 489-495. (doi:10.1128/JB.185.2.489-495.2003)
57. Junker, M., Besingi, R. N. & Clark, P. L. 2009 Vectorial transport and folding of an autotransporter virulence protein during outer membrane secretion. Mol. Microbiol.71, 1323-1332. (doi:10.1111/j.1365-2958.2009.06607.x)
58. Willems, R. J., Geuijen, C., van der Heide, H. G., Renauld, G., Bertin, P., van den Akker, W. M., Locht, C. & Mooi, F. R. 1994 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, 337-347. (doi:10.1111/j.1365-2958.1994.tb00314.x)
59. Braun, V., Ondraczek, R. & Hobbie, S. 1993 Activation and secretion of Serratia hemolysin. Zentralbl. Bakteriol. 278, 306-315. (doi:10.1016/S0934-8840(11)80847-9)
60. St Geme III, J. W. & Yeo, H. J. 2009 A prototype twopartner secretion pathway: the Haemophilus influenzae HMW1 and HMW2 adhesin systems. Trends Microbiol. 17, 355-360. (doi:10.1016/j.tim.2009.06.002)
61. Grin, I. & Linke, D. 2011 GCView: the genomic context viewer for protein homology searches. Nucleic Acids Res. 39, W353-W356. (doi:10.1093/nar/gkr364)
62. Coutte, L., Antoine, R., Drobecq, H., Locht, C. & Jacob-Dubuisson, F. 2001 Subtilisin-like autotransporter serves as maturation protease in a bacterial secretion pathway. EMBO J. 20, 5040-5048. (doi:10.1093/emboj/20.18.5040)
63. Jacob-Dubuisson, F., Buisine, C., Willery, E., Renauld-Mongenie, G. & Locht, C. 1997 Lack of functional complementation between Bordetella pertussis filamentous hemagglutinin and Proteus mirabilis HpmA hemolysin secretion machineries. J. Bacteriol. 179, 775-783.
64. Julio, S. M. & Cotter, P. A. 2005 Characterization of the filamentous hemagglutinin-like protein FhaS in Bordetella bronchiseptica. Infect. Immun. 73, 4960-4971. (doi:10.1128/IAI.73.8.4960-4971.2005)
65. Kajava, A. V., Cheng, N., Cleaver, R., Kessel, M., Simon, M. N., Willery, E., Jacob-Dubuisson, F., Locht, C. & Steven, A. C. 2001 Beta-helix model for the filamentous haemagglutinin adhesin of Bordetella pertussis and related bacterial secretory proteins. Mol.Microbiol. 42, 279-292. (doi:10.1046/j.1365-2958.2001.02598.x)
66. Lambert-Buisine, C., Willery, E., Locht, C. & Jacob-Dubuisson, F. 1998 N-terminal characterization of the Bordetella pertussis filamentous haemagglutinin. Mol. Microbiol. 28, 1283-1293. (doi:10.1046/j.1365-2958.1998.00892.x)
67. Jacob-Dubuisson, F., Locht, C. & Antoine, R. 2001 Two-partner secretion in Gram-negative bacteria: a thrifty, specific pathway for large virulence proteins. Mol. Microbiol. 40, 306-313. (doi:10.1046/j.1365-2958.2001.02278.x)
68. Delattre, A. S., Saint, N., Clantin, B., Willery, E., Lippens, G., Locht, C., Villeret, V. & Jacob-Dubuisson, F. 2011 Substrate recognition by the POTRA domains of TpsB transporter FhaC. Mol. Microbiol. 81, 99-112. (doi:10.1111/j.1365-2958.2011.07680.x)
69. Hodak, H., Clantin, B., Willery, E., Villeret, V., Locht, C. & Jacob-Dubuisson, F. 2006 Secretion signal of the filamentous haemagglutinin, a model two-partner secretion substrate. Mol. Microbiol. 61, 368-382. (doi:10.1111/j.1365-2958.2006.05242.x)
70. Clantin, B., Hodak, H., Willery, E., Locht, C., Jacob-Dubuisson, F. & Villeret, V. 2004 The crystal structure of filamentous hemagglutinin secretion domain and its implications for the two-partner secretion pathway. Proc. Natl Acad. Sci. USA 101, 6194-6199. (doi:10.1073/pnas.0400291101)
71. Yeo, H. J., Yokoyama, T., Walkiewicz, K., Kim, Y., Grass, S. & Geme III, J. W. 2007 The structure of the Haemophilus influenzae HMW1 pro-piece reveals a structural domain essential for bacterial two-partner secretion. J. Biol. Chem. 282, 31076-31084.
72. Yang, F. L. & Braun, V. 2000 ShlB mutants of Serratia marcescens allow uncoupling of activation and secretion of the ShlA hemolysin. Int. J. Med. Microbiol. 290, 529-538. (doi:10.1016/S1438-4221(00)80018-1)
73. Choi, P. S. & Bernstein, H. D. 2010 Sequential translocation of an Escherichia coli two-partner secretion pathway exoprotein across the inner and outer membranes. Mol. Microbiol. 75, 440-451. (doi:10.1111/j.1365-2958.2009.06993.x)
74. Baud, C., Hodak, H., Willery, E., Drobecq, H., Locht, C., Jamin, M. & Jacob-Dubuisson, F. 2009 Role of DegP for two-partner secretion in Bordetella. Mol. Microbiol. 74, 315-329. (doi:10.1111/j.1365-2958.2009.06860.x)
75. Guedin, S., Willery, E., Locht, C. & 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. (doi:10.1046/j.1365-2958.1998.00970.x)
76. Mazar, J. & Cotter, P. A. 2006 Topology and maturation of filamentous haemagglutinin suggest a new model for two-partner secretion. Mol. Microbiol. 62, 641-654. (doi:10.1111/j.1365-2958.2006.05392.x)
77. Mazar, J. & Cotter, P. A. 2007 New insight into the molecular mechanisms of two-partner secretion. Trends Microbiol. 15, 508-515. (doi:10.1016/j.tim.2007.10.005)
78. Clantin, B., Delattre, A. S., Rucktooa, P., Saint, N., Meli, A. C., Locht, C., Jacob-Dubuisson, F. & Villeret, V. 2007 Structure of the membrane protein FhaC: a member of the Omp85-TpsB transporter superfamily. Science 317, 957-961. (doi:10.1126/science.1143860)
79. Buscher, A. Z., Grass, S., Heuser, J., Roth, R. & St Geme III, J. W. 2006 Surface anchoring of a bacterial adhesin secreted by the two-partner secretion pathway. Mol. Microbiol. 61, 470-483. (doi:10.1111/j.1365-2958.2006.05236.x)
80. Grass, S. & St Geme III, J. W. 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. (doi:10.1046/j.1365-2958.2000.01812.x)
81. Linke, D., Riess, T., Autenrieth, I. B., Lupas, A. & Kempf, V. A. 2006 Trimeric autotransporter adhesins: variable structure, common function. Trends Microbiol. 14, 264-270. (doi:10.1016/j.tim.2006.04.005)
82. Szczesny, P. & Lupas, A. 2008 Domain annotation of trimeric autotransporter adhesions-daTAA. Bioinformatics 24, 1251-1256. (doi:10.1093/bioinfor matics/btn118)
83. Szczesny, P. et al. 2008 Structure of the head of the Bartonella adhesin BadA. PLoS Pathog. 4, e1000119. (doi:10.1371/journal.ppat.1000119)
84. Hoiczyk, E., Roggenkamp, A., Reichenbecher, M., Lupas, A. & Heesemann, J. 2000 Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins. Embo. J. 19, 5989-5999. (doi:10.1093/emboj/19.22.5989)
85. Leo, J. C., Elovaara, H., Bihan, D., Pugh, N., Kilpinen, S. K., Raynal, N., Skurnik, M., Farndale, R. W. & Goldman, A. 2010 First analysis of a bacterial collagen- binding protein with collagen Toolkits: promiscuous binding of YadA to collagens may explain how YadA interferes with host processes. Infect. Immun. 78, 3226-3236. (doi:10.1128/IAI.01057-09)
86. Nummelin, H., Merckel, M. C., Leo, J. C., Lankinen, H., Skurnik, M. & Goldman, A. 2004 The Yersinia adhesin YadA collagen-binding domain structure is a novel left-handed parallel beta-roll. Embo. J. 23, 701-711. (doi:10.1038/sj.emboj.7600100)
87. Wollmann, P., Zeth, K., Lupas, A. N. & Linke, D. 2006 Purification of the YadA membrane anchor for secondary structure analysis and crystallization. Int. J. Biol. Macromol. 39, 3-9. (doi:10.1016/j.ijbiomac.2005.11.009)
88. Riess, T. et al. 2004 Bartonella adhesin a mediates a proangiogenic host cell response. J. Exp. Med. 200, 1267-1278. (doi:10.1084/jem.20040500)
89. St Geme III, J. W. &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. (doi:10.1128/JB.182.21.6005-6013.2000)
90. Cotter, S. E., Yeo, H. J., Juehne, T. & St Geme III, J. W. 2005 Architecture and adhesive activity of the Haemophilus influenzae Hsf adhesin. J. Bacteriol. 187, 4656-4664. (doi:10.1128/JB.187.13.4656-4664.2005)
91. Conners, R. et al. 2008 The Moraxella adhesin UspA1 binds to its human CEACAM1 receptor by a deformable trimeric coiled-coil. Embo. J. 27, 1779-1789. (doi:10.1038/emboj.2008.101)
92. Hernandez Alvarez, B., Hartmann, M. D., Albrecht, R., Lupas, A. N., Zeth, K. & Linke, D. 2008 A new expression system for protein crystallization using trimeric coiled-coil adaptors. Protein Eng. Des. Sel. 21, 11-18. (doi:10.1093/protein/gzm071)
93. Hartmann, M. D. et al. 2009 A coiled-coil motif that sequesters ions to the hydrophobic core. Proc. Natl Acad. Sci. USA 106, 16950-16955. (doi:10.1073/pnas.0907256106)
94. Leo, J. C., Lyskowski, A., Hattula, K., Hartmann, M. D., Schwarz, H., Butcher, S. J., Linke, D., Lupas, A. N. & Goldman, A. 2011 The structure of E. coli IgG-binding protein D suggests a general model for bending and binding in trimeric autotransporter adhesins. Structure 19, 1021-1030. (doi:10.1016/j.str.2011.03.021)
95. Lehr, U., Schutz, M., Oberhettinger, P., Ruiz-Perez, F., Donald, J. W., Palmer, T., Linke, D., Henderson, I. R. & Autenrieth, I. B. 2010 C-terminal amino acid residues of the trimeric autotransporter adhesin YadA of Yersinia enterocolitica are decisive for its recognition and assembly by BamA. Mol. Microbiol. 78, 932-946. (doi:10.1111/j.1365-2958.2010.07377.x)
96. Meng, G., Surana, N. K., St Geme III, J.W. & Waksman, G. 2006 Structure of the outer membrane translocator domain of the Haemophilus influenzae Hia trimeric autotransporter. Embo. J. 25, 2297-2304. (doi:10.1038/sj.emboj.7601132)
97. Mikula, K. M., Leo, J. C., Lyskowski, A., Kedracka-Krok, S., Pirog, A. & Goldman, A. In press. The translocation domain in trimeric autotransporter adhesins is necessary and sufficient for trimerization and autotransportation. J. Bacteriol. 194, 827-838. (doi:10.1128/JB.05322-11)
98. Roggenkamp, A., Ackermann, N., Jacobi, C. A., Truelzsch, K., Hoffmann, H. & Heesemann, J. 2003 Molecular analysis of transport and oligomerization of the Yersinia enterocolitica adhesin YadA. J. Bacteriol. 185, 3735-3744. (doi:10.1128/JB.185.13.3735-3744.2003)
99. Alvarez, B. H., Gruber, M., Ursinus, A., Dunin-Horkawicz, S., Lupas, A. N. & Zeth, K. 2011 A transition from strong right-handed to canonical lefthanded supercoiling in a conserved coiled-coil segment of trimeric autotransporter adhesins. J. Struct. Biol. 170, 236-245. (doi:10.1016/j.jsb.2010.02.009)
100. Salacha, R., Kovacic, F., Brochier-Armanet, C., Wilhelm, S., Tommassen, J., Filloux, A., Voulhoux, R. & Bleves, S. 2010 The Pseudomonas aeruginosa patatin-like protein PlpD is the archetype of a novel Type V secretion system. Environ. Microbiol. 12, 1498-1512.
101. Arnold, T., Zeth, K. & Linke, D. 2010 Omp85 from the thermophilic cyanobacterium Thermosynechococcus elongatus differs from proteobacterial Omp85 in structure and domain composition. J. Biol. Chem. 285, 18003-18015.
102. Henderson, I. R., Cappello, R. & Nataro, J. P. 2000 Autotransporter proteins, evolution and redefining protein secretion: response. Trends Microbiol. 8, 534-535. (doi:10.1016/S0966-842X(00)01884-9)
103. Jacob-Dubuisson, F., Antoine, R. & Locht, C. 2000 Autotransporter proteins, evolution and redefining protein secretion: response. Trends Microbiol. 8, 533-534. (doi:10.1016/S0966-842X(00)01885-0)
104. Liu, H., Magoun, L., Luperchio, S., Schauer, D. B. & Leong, J. M. 1999 The Tir-binding region of enterohaemorrhagic Escherichia coli intimin is sufficient to trigger actin condensation after bacterial-induced host cell signalling. Mol. Microbiol. 34, 67-81. (doi:10.1046/j.1365-2958.1999.01574.x)
105. Frankel, G., Phillips, A. D., Trabulsi, L. R., Knutton, S., Dougan, G. & Matthews, S. 2001 Intimin and the host cell-is it bound to end in Tir(s)? Trends Microbiol. 9, 214-218. (doi:10.1016/S0966-842X(01) 02016-9)
106. Batchelor, M., Prasannan, S., Daniell, S., Reece, S., Connerton, I., Bloomberg, G., Dougan, G., Frankel, G. & Matthews, S. 2000 Structural basis for recognition of the translocated intimin receptor (Tir) by intimin from enteropathogenic Escherichia coli. EMBO J. 19, 2452-2464. (doi:10.1093/emboj/19.11.2452)
107. Isberg, R. R., Hamburger, Z. & Dersch, P. 2000 Signaling and invasin-promoted uptake via integrin receptors. Microbes Infect. 2, 793-801. (doi:10.1016/S1286-4579(00)90364-2)
108. Wentzel, A., Christmann, A., Adams, T. & Kolmar, H. 2001 Display of passenger proteins on the surface of Escherichia coli K-12 by the enterohemorrhagic E. coliintimin EaeA. J. Bacteriol. 183, 7273-7284. (doi:10.1128/JB.183.24.7273-7284.2001)
109. Touze, T., Hayward, R. D., Eswaran, J., Leong, J. M. & Koronakis, V. 2004 Self-association of EPEC intimin mediated by the beta-barrel-containing anchor domain: a role in clustering of the Tir receptor. Mol. Microbiol. 51, 73-87. (doi:10.1046/j.1365-2958.2003.03830.x)
110. Saier Jr, M. H., Yen, M. R., Noto, K., Tamang, D. G. & Elkan, C. 2009 The Transporter Classification Database: recent advances. Nucleic Acids Res. 37, D274-D278. (doi:10.1093/nar/gkn862)
111. Newman, C. L. & Stathopoulos, C. 2004 Autotransporter and two-partner secretion: delivery of large-size virulence factors by Gram-negative bacterial pathogens. Crit. Rev. Microbiol. 30, 275-286. (doi:10.1080/10408410490499872)
112. Tsai, J. C., Yen, M. R., Castillo, R., Leyton, D. L., Henderson, I. R. & Saier Jr, M. H. 2011 The bacterial intimins and invasins: a large and novel family of secreted proteins. PLoS ONE 5, e14403. (doi:10.1371/journal.pone.0014403)
113. Oberhettinger, P., Schütz, M., Heinz, N., Leo, J. C., Berger, J., Autenrieth, I. B. & Linke, D. Submitted. Intimin and invasin export their C-terminus to the bacterial cell surface using an inverse mechanism compared to classical autotransport. PLoS Pathogens.
114. Adams, T. M., Wentzel, A. & Kolmar, H. 2005 Intimin-mediated export of passenger proteins requires maintenance of a translocation-competent conformation. J. Bacteriol. 187, 522-533. (doi:10.1128/JB.187.2.522-533.2005)
115. Bodelon, G., Marin, E. & Fernandez, L. A. 2009 Role of periplasmic chaperones and BamA (YaeT/Omp85) in folding and secretion of intimin from enteropathogenic Escherichia coli strains. J. Bacteriol. 191, 5169-5179. (doi:10.1128/JB.00458-09)
116. Remmert, M., Linke, D., Lupas, A.N. & Soding, J. 2009 HHomp-prediction and classification of outer membrane proteins. Nucleic Acids Res. 37, W446-W451. (doi:10.1093/nar/gkp325)
117. Hagan, C. L., Silhavy, T. J. & Kahne, D. 2011b-Barrel membrane protein assembly by the Bam Complex. Annu. Rev. Biochem. 80, 189-210. (doi:10.1146/annurev-biochem-061408-144611)
118. Walther, D. M., Rapaport, D. & Tommassen, J. 2009 Biogenesis of beta-barrel membrane proteins in bacteria and eukaryotes: evolutionary conservation and divergence. Cell Mol. Life Sci. 66, 2789-2804. (doi:10.1007/s00018-009-0029-z)
119. Ieva, R., Skillman, K. M. & Bernstein, H. D. 2008 Incorporation of a polypeptide segment into the beta-domain pore during the assembly of a bacterial autotransporter. Mol. Microbiol. 67, 188-201. (doi:10.1111/j.1365-2958.2007.06048.x)
120. Krojer, T., Sawa, J., Schafer, E., Saibil, H. R., Ehrmann, M. & Clausen, T. 2008 Structural basis for the regulated protease and chaperone function of DegP. Nature 453, 885-890. (doi:10.1038/nature07004)
121. Phan, G. et al. 2011 Crystal structure of the FimD usher bound to its cognate FimC-FimH substrate. Nature 474, 49-53. (doi:10.1038/nature10109)
122. Khalid, S. & Sansom, M. S. 2006 Molecular dynamics simulations of a bacterial autotransporter: NalP from Neisseria meningitidis. Mol. Membr. Biol. 23, 499-508 (doi:10.1080/09687860600849531)