The autodisplay story, from discovery to biotechnical and biomedical applications

Microbiology and Molecular Biology Reviews

Volumn 71, Issue 4, 2007, Pages 600-619

  Jose, Joachim ^a   Meyer, Thomas F ^b  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN INVOLVED IN DIFFUSE ADHERENCE I; APOPROTEIN; BACTERIAL VACCINE; CARRIER PROTEIN; EPITOPE; ESTERASE; IMMUNOGLOBULIN A1 PROTEASE; OXIDOREDUCTASE; PEPTIDE LIBRARY; PROTEINASE; SALMONELLOSIS VACCINE; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; BACTERIAL OUTER MEMBRANE; BIOTECHNOLOGY; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE TRANSPORT; CELL SURFACE; CHIRALITY; DISEASE MODEL; ELECTRON TRANSPORT; ENZYME ACTIVITY; ENZYME INHIBITION; ESCHERICHIA COLI; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; NEISSERIA GONORRHOEAE; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PROTEIN SECRETION; PROTEIN TRANSPORT; REVIEW; SALMONELLA; VACCINATION;

ADHESINS, ESCHERICHIA COLI; BACTERIAL OUTER MEMBRANE PROTEINS; BIOTECHNOLOGY; CARRIER PROTEINS; EPITOPES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GRAM-NEGATIVE BACTERIA; MODELS, MOLECULAR; NEISSERIA GONORRHOEAE; RECOMBINANT PROTEINS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA; NEISSERIA GONORRHOEAE; SALMONELLA;

EID: 37349047429     PISSN: 10922172     EISSN: None     Source Type: Journal    
DOI: 10.1128/MMBR.00011-07     Document Type: Review

References (150)

1. Adams, T. M., A. Wentzel, and H. Kolmar. 2005. Intimin-mediated export of passenger proteins requires maintenance of a translocation-competent conformation. J. Bacteriol. 187:522-533.
2. Barbar, E., G. Barany, and C. Woodward. 1996. Unfolded BPTI variants with a single disulfide bond have diminished non-native structure distant from the crosslink. Fold. Des. 1:65-76.
3. Becker, S., H. U. Schmoldt, T. M. Adams, S. Wilhelm, and H. Kolmar. 2004. Ultra-high-throughput screening based on cell-surface display and fluorescence-activated cell sorting for the identification of novel biocatalysts. Curr. Opin. Biotechnol. 15:323-329.
4. Becker, S., S. Theile, N. Heppeler, A. Michalczyk, A. Wentzel, S. Wilhelm, K. E. Jaeger, and H. Kolmar. 2005. A generic system for the Escherichia coli cell-surface display of lipolytic enzymes. FEBS Lett. 579:1177-1182.
5. Benhar, I. 2001. Biotechnological applications of phage and cell display. Biotechnol. Adv. 19:1-33.
6. Benz, I., S. Knochenhauer, and M. A. Schmidt. 1990. Molecular mechanisms of adherence of enteropathogenic Escherichia coli. Z. Gastroenterol. Verh. 25:67-70.
7. Benz, I., and M. A. Schmidt. 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.
8. Benz, I., and M. A. Schmidt. 1989. Cloning and expression of an adhesin (AIDA-I) involved in diffuse adherence of enteropathogenic Escherichia coli. Infect. Immun. 57:1506-1511.
9. Benz, I., and M. A. Schmidt. 1990. Diffuse adherence of enteropathogenic Escherichia coli strains. Res. Microbiol. 141:785-786.
10. Benz, I., and M. A. Schmidt. 1993. Diffuse adherence of enteropathogenic Escherichia coli strains - processing of AIDA-I. Zentbl. Bakteriol. 278:197-208.
11. Benz, I., and M. A. Schmidt. 1992. Isolation and serologic characterization of AIDA-I, the adhesin mediating the diffuse adherence phenotype of the diarrhea-associated Escherichia coli strain 2787 (O126:H27). Infect. Immun. 60:13-18.
12. Bernhardt, R. 1996. Cytochrome P450: structure, function, and generation of reactive oxygen species. Rev. Physiol. Biochem. Pharmacol. 127:137-221.
13. Bessette, P. H., J. J. Rice, and P. S. Daugherty. 2004. Rapid isolation of high-affinity protein binding peptides using bacterial display. Protein Eng. Des. Sel. 17:731-739.
14. Bornscheuer, U. T. 2002. Microbial carboxyl esterases: classification, properties and application in biocatalysis. FEMS Microbiol. Rev. 26:73-81.
15. Breinig, F., and M. J. Schmitt. 2002. Spacer-elongated cell wall fusion proteins improve cell surface expression in the yeast Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 58:637-644.
16. Casali, N., M. Konieczny, M. A. Schmidt, and L. W. Riley. 2002. Invasion activity of a Mycobacterium tuberculosis peptide presented by the Escherichia coli AIDA autotransporter. Infect. Immun. 70:6846-6852.
17. Charbit, A., J. C. Boulain, A. Ryter, and M. Hofnung. 1986. Probing the topology of a bacterial membrane protein by genetic insertion of a foreign epitope; expression at the cell surface. EMBO J. 5:3029-3037.
18. Chervaux, C., N. Sauvonnet, A. Le Clainche, B. Kenny, A. L. Hung, J. K. Broome-Smith, and I. B. Holland. 1995. Secretion of active beta-lactamase to the medium mediated by the Escherichia coli haemolysin transport pathway. Mol. Gen. Genet. 249:237-245.
19. Creighton, T. E. 1992. The disulfide folding pathway of BPTI. Science 256:111-114.
20. Daugherty, P. S., B. L. Iverson, and G. Georgiou. 2000. Flow cytometric screening of cell-based libraries. J. Immunol. Methods 243:211-227.
21. Davey, H. M., and D. B. Kell. 1996. Flow cytometry and cell sorting of heterogeneous microbial populations: the importance of single-cell analyses. Microbiol. Rev. 60:641-696.
22. Fischer, W., R. Buhrdorf, E. Gerland, and R. Haas. 2001. Outer membrane targeting of passenger proteins by the vacuolating cytotoxin autotransporter of Helicobacter pylori. Infect. Immun. 69:6769-6775.
23. Fisher, K. A., and W. Stoeckenius. 1982. Membrane models. Springer, Berlin, Germany.
24. Francisco, J. A., R. Campbell, B. L. Iverson, and G. Georgiou. 1993. Production and fluorescence-activated cell sorting of Escherichia coli expressing a functional antibody fragment on the external surface. Proc. Natl. Acad. Sci. USA 90:10444-10448.
25. Francisco, J. A., C. F. Earhart, and G. Georgiou. 1992. Transport and anchoring of beta-lactamase to the external surface of Escherichia coli. Proc. Natl. Acad. Sci. USA 89:2713-2717.
26. Freudl, R., S. Maclntyre, M. Degen, and U. Henning. 1986. Cell surface exposure of the outer membrane protein OmpA of Escherichia coli K-12. J. Mol. Biol. 188:491-494.
27. Gentschev, I., H. Mollenkopf, Z. Sokolovic, J. Hess, S. H. Kaufmann, and W. Goebel. 1996. Development of antigen-delivery systems, based on the Escherichia coli hemolysin secretion pathway. Gene 179:133-140.
28. Georgiou, G., C. Stathopoulos, P. S. Daugherty, A. R. Nayak, B. L. Iverson, and R. Curtiss III. 1997. Display of heterologous proteins on the surface of microorganisms: from the screening of combinatorial libraries to live recombinant vaccines. Nat. Biotechnol. 15:29-34.
29. Ghosh, A. S., and K. D. Young. 2005. Helical disposition of proteins and lipopolysaccharide in the outer membrane of Escherichia coli. J. Bacteriol. 187:1913-1922.
30. Giffhorn, F., S. Kopper, A. Huwig, and S. Freimund. 2000. Rare sugars and sugar-based synthons by chemo-enzymatic synthesis. Enzyme Microb. Technol. 27:734-742.
31. Grinberg, A. V., F. Hannemann, B. Schiffler, J. Muller, U. Heinemann, and R. Bernhardt. 2000. Adrenodoxin: structure, stability, and electron transfer properties. Proteins 40:590-612.
32. Grodberg, J., and J. J. Dunn. 1988. ompT encodes the Escherichia coli outer membrane protease that cleaves T7 RNA polymerase during purification. J. Bacteriol. 170:1245-1253.
33. Guina, T., E. C. Yi, H. Wang, M. Hackett, and S. I. Miller. 2000. A PhoP-regulated outer membrane protease of Salmonella enterica serovar Typhimurium promotes resistance to alpha-helical antimicrobial peptides. J. Bacteriol. 182:4077-4086.
34. Haddad, D., S. Liljeqvist, S. Kumar, M. Hansson, S. Stahl, H. Perlmann, P. Perlmann, and K. Berzins. 1995. Surface display compared to periplasmic expression of a malarial antigen in Salmonella typhimurium and its implications for immunogenicity. FEMS Immunol. Med. Microbiol. 12:175-186.
35. Halter, R., J. Pohlner, and T. F. Meyer. 1984. IgA protease of Neisseria gonorrhoeae: isolation and characterization of the gene and its extracellular product. EMBO J. 3:1595-1601.
36. Hannemann, F., A. K. Bera, B. Fischer, M. Lisurek, K. Teuchner, and R. Bernhardt. 2002. Unfolding and conformational studies on bovine adrenodoxin probed by engineered intrinsic tryptophan fluorescence. Biochemistry 41:11008-11016.
37. Henderson, I. R., R. Cappello, and J. P. Nataro. 2000. Autotransporter proteins, evolution and redefining protein secretion. Trends Microbiol. 8:529-532.
38. Henderson, I. R., F. Navarro-Garcia, M. Desvaux, R. C. Fernandez, and D. Ala'Aldeen. 2004. Type V protein secretion pathway: the autotransporter story. Microbiol. Mol. Biol. Rev. 68:692-744.
39. Hess, J., A. Dreher, I. Gentschev, W. Goebel, C. Ladel, D. Miko, and S. H. Kaufmann. 1996. Protein p60 participates in intestinal host invasion by Listeria monocytogenes. Zentbl. Bakteriol. 284:263-272.
40. Isticato, R., G. Cangiano, H. T. Tran, A. Ciabattini, D. Medaglini, M. R. Oggioni, M. De Felice, G. Pozzi, and E. Ricca. 2001. Surface display of recombinant proteins on Bacillus subtilis spores. J. Bacteriol. 183:6294-6301.
41. Jacob-Dubuisson, F., R. Fernandez, and L. Coutte. 2004. Protein secretion through autotransporter and two-partner pathways. Biochim. Biophys. Acta 1694:235-257.
42. Jain, S., P. van Ulsen, I. Benz, M. A. Schmidt, R. Fernandez, J. Tommassen, and M. B. Goldberg. 2006. Polar localization of the autotransporter family of large bacterial virulence proteins. J. Bacteriol. 188:4841-4850.
43. Janssen, R., and J. Tommassen. 1994. PhoE protein as a carrier for foreign epitopes. Int. Rev. Immunol. 11:113-121.
44. Jose, J., R. Bernhardt, and F. Hannemann. 2002. Cellular surface display of dimeric Adx and whole cell P450-mediated steroid synthesis on E. coli. J. Biotechnol. 95:257-268.
45. Jose, J., D. Betscheider, and D. Zangen. 2005. Bacterial surface display library screening by target enzyme labeling: identification of new human cathepsin G inhibitors. Anal. Biochem. 346:258-267.
46. Jose, J., and S. Handel. 2003. Monitoring the cellular surface display of recombinant proteins by cysteine labeling and flow cytometry. Chembiochem. 4:396-405.
47. Jose, J., F. Hannemann, and R. Bernhardt. 2001. Functional display of active bovine adrenodoxin on the surface of E. coli by chemical incorporation of the 2Fe-2S cluster. Chembiochem. 2:695-701.
48. Jose, J., F. Jahnig, and T. F. Meyer. 1995. Common structural features of IgA1 protease-like outer membrane protein autotransporters letter. Mol. Microbiol. 18:378-380.
49. Jose, J., J. Kramer, T. Klauser, J. Pohlner, and T. F. Meyer. 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.
50. Jose, J., and S. von Schwichow. 2004. Autodisplay of active sorbitol dehydrogenase (SDH) yields a whole cell biocatalyst for the synthesis of rare sugars. Chembiochem. 5:100-108.
51. Jose, J., and S. von Schwichow. 2004. "Cystope tagging" for labeling and detection of recombinant protein expression. Anal. Biochem. 331:267-274.
52. Jose, J., and D. Zangen. 2005. Autodisplay of the protease inhibitor aprotinin in Escherichia coli. Biochem. Biophys. Res. Commun. 333:1218-1226.
53. Jung, H. C., J. M. Lebeault, and J. G. Pan. 1998. Surface display of Zymomonas mobilis levansucrase by using the ice-nucleation protein of Pseudomonas syringae 5. Nat. Biotechnol. 16:576-580.
54. Kjaergaard, K., H. Hasman, M. A. Schembri, and P. Klemm. 2002. Antigen 43-mediated autotransporter display, a versatile bacterial cell surface presentation system. J. Bacteriol. 184:4197-4204.
55. Klauser, T., J. Kramer, K. Otzelberger, J. Pohlner, and T. F. Meyer. 1993. Characterization of the Neisseria Iga beta-core. The essential unit for outer membrane targeting and extracellular protein secretion. J. Mol. Biol. 234:579-593.
56. Klauser, T., J. Pohlner, and T. F. Meyer. 1990. Extracellular transport of cholera toxin B subunit using Neisseria IgA protease beta-domain: conformation-dependent outer membrane translocation. EMBO J. 9:1991-1999.
57. Klauser, T., J. Pohlner, and T. F. Meyer. 1993. The secretion pathway of IgA protease-type proteins in gram-negative bacteria. Bioessays 15:799-805.
58. Klauser, T., J. Pohlner, and T. F. Meyer. 1992. Selective extracellular release of cholera toxin B subunit by Escherichia coli: dissection of Neisseria Iga beta-mediated outer membrane transport. EMBO J. 11:2327-2335.
59. Klemm, P., and M. A. Schembri. 2000. Fimbriae-assisted bacterial surface display of heterologous peptides 3. Int. J. Med. Microbiol. 290:215-221.
60. Koebnik, R., K. P. Locher, and P. Van Gelder. 2000. Structure and function of bacterial outer membrane proteins: barrels in a nutshell 2. Mol. Microbiol. 37:239-253.
61. Konieczny, M. P., M. Suhr, A. Noll, I. B. Autenrieth, and M. Alexander Schmidt. 2000. Cell surface presentation of recombinant (poly-) peptides including functional T-cell epitopes by the AIDA autotransporter system. FEMS Immunol. Med. Microbiol. 27:321-332.
62. Konieczny, M. P. J., I. Benz, B. Hollinderbaumer, C. Beinke, M. Niederweis, and M. A. Schmidt. 2001. Modular organization of the AIDA autotransporter translocator: the N-terminal beta1-domain is surface-exposed and stabilizes the transmembrane beta2-domain. Antonie van Leeuwenhoek 80:19-34.
63. Kornacker, M. G., and A. P. Pugsley. 1990. The normally periplasmic enzyme beta-lactamase is specifically and efficiently translocated through the Escherichia coli outer membrane when it is fused to the cell-surface enzyme pullulanase. Mol. Microbiol. 4:1101-1109.
64. Kramer, U., K. Rizos, H. Apfel, I. B. Autenrieth, and C. T. Lattemann. 2003. Autodisplay: development of an efficacious system for surface display of antigenic determinants in Salmonella vaccine strains. Infect. Immun. 71:1944-1952.
65. Lattemann, C. T., J. Maurer, E. Gerland, and T. F. Meyer. 2000. Autodisplay: functional display of active beta-lactamase on the surface of Escherichia coli by the AIDA-I autotransporter. J. Bacteriol. 182:3726-3733.
66. Lee, H. W., and S. M. Byun. 2003. The pore size of the autotransporter domain is critical for the active translocation of the passenger domain. Biochem. Biophys. Res. Commun. 307:820-825.
67. Lee, S. Y., J. H. Choi, and Z. Xu. 2003. Microbial cell-surface display. Trends Biotechnol. 21:45-52.
68. Li, H., L. Qian, Z. Chen, D. Thibault, G. Liu, T. Liu, and D. G. Thanassi. 2004. The outer membrane usher forms a twin-pore secretion complex. J. Mol. Biol. 344:1397-1407.
69. Liljeqvist, S., P. Samuelson, M. Hansson, T. N. Nguyen, H. Binz, and S. Stahl. 1997. Surface display of the cholera toxin B subunit on Staphylococcus xylosus and Staphylococcus camosus. Appl. Environ. Microbiol. 63:2481-2488.
70. Loveless, B. J., and M. H. Saier, Jr. 1997. A novel family of channel-forming, autotransporting, bacterial virulence factors. Mol. Membr. Biol. 14:113-123.
71. Lu, Z., B. C. Tripp, and J. M. McCoy. 1998. Displaying libraries of conformationally constrained peptides on the surface of Escherichia coli as flagellin fusions. Methods Mol. Biol. 87:265-280.
72. Malmborg, A. C., E. Soderlind, L. Frost, and C. A. Borrebaeck. 1997. Selective phage infection mediated by epitope expression on F pilus. J. Mol. Biol. 273:544-551.
73. Maurer, J., J. Jose, and T. F. Meyer. 1997. Autodisplay: one-component system for efficient surface display and release of soluble recombinant proteins from Escherichia coli. J. Bacteriol. 179:794-804.
74. Maurer, J., J. Jose, and T. F. Meyer. 1999. Characterization of the essential transport function of the AIDA-I autotransporter and evidence supporting structural predictions. J. Bacteriol. 181:7014-7020.
75. McBride, J. D., H. N. Freeman, and R. J. Leatherbarrow. 1999. Selection of human elastase inhibitors from a conformationally constrained combinatorial peptide library. Eur. J. Biochem. 266:403-404 12.
76. Meng, G., N. K. Surana, J. W. St. Gerne III, and G. Waksman. 2006. Structure of the outer membrane translocator domain of the Haemophilus influenzae Hia trimeric autotransporter. EMBO J. 25:2297-2304.
77. Meyer, T. F., R. Halter, and J. Pohlner. 1987. Mechanism of extracellular secretion of an IgA protease by gram-negative host cells. Adv. Exp. Med. Biol. 216B:1271-1281.
78. Miyazaki, H., N. Yanagida, S. Horinouchi, and T. Beppu. 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.
79. Muhlradt, P. F., J. Menzel, J. R. Golecki, and V. Speth. 1974. Lateral mobility and surface density of lipopolysaccharide in the outer membrane of Salmonella typhimurium. Eur. J. Biochem. 43:533-539.
80. Muller, A., J. J. Muller, Y. A. Muller, H. Uhlmann, R. Bernhardt, and U. Heinemann. 1998. New aspects of electron transfer revealed by the crystal structure of a truncated bovine adrenodoxin, Adx(4-108). Structure 6:269-280.
81. Muller, D., I. Benz, D. Tapadar, C. Buddenborg, L. Greune, and M. A. Schmidt. 2005. Arrangement of the translocator of the autotransporter adhesin involved in diffuse adherence on the bacterial surface. Infect. Immun. 73:3851-3859.
82. Murzin, A. G., A. M. Lesk, and C. Chothia. 1994. Principles determining the structure of beta-sheet barrels in proteins. I. A theoretical analysis. J. Mol. Biol. 236:1369-1381.
83. Murzin, A. G., A. M. Lesk, and C. Chothia. 1994. Principles determining the structure of beta-sheet barrels in proteins. II. The observed structures. J. Mol. Biol. 236:1382-1400.
84. Nguyen, T. N., M. Hansson, S. Stahl, T. Bachi, A. Robert, W. Domzig, H. Binz, and M. Uhlen. 1993. Cell-surface display of heterologous epitopes on Staphylococcus xylosus as a potential delivery system for oral vaccination. Gene 128:89-94.
85. Odenbreit, S., M. Till, D. Hofreuter, G. Faller, and R. Haas. 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.
86. Oliver, D. C., G. Huang, E. Nodel, S. Pleasance, and R. C. Fernandez. 2003. A conserved region within the Bordetella pertussis autotransporter BrkA is necessary for folding of its passenger domain. Mol. Microbiol. 47:1367-1383.
87. Oomen, C. J., P. Van Ulsen, P. Van Gelder, M. Feijen, J. Tommassen, and P. Gros. 2004. Structure of the translocator domain of a bacterial autotransporter. EMBO J. 23:1257-1266.
88. Panda, T., and B. S. Gowrishankar. 2005. Production and applications of esterases. Appl. Microbiol. Biotechnol. 67:160-169.
89. Peterson, J. H., R. L. Szabady, and H. D. Bernstein. 2006. An unusual signal peptide extension inhibits the binding of bacterial presecretory proteins to the signal recognition particle, trigger factor, and the SecYEG complex. J. Biol. Chem. 281:9038-9048.
90. Philippsen, A., T. Schirmer, M. A. Stein, F. Giffhorn, and J. Stetefeld. 2005. Structure of zinc-independent sorbitol dehydrogenase from Rhodobacter sphaeroides at 2.4 A resolution. Acta Crystallogr. D 61:374-379.
91. Pikuleva, I. A., K. Tesh, M. R. Waterman, and Y. Kim. 2000. The tertiary structure of full-length bovine adrenodoxin suggests functional dimers. Arch. Biochem. Biophys. 373:44-55.
92. Pohlner, J., R. Halter, K. Beyreuther, and T. F. Meyer. 1987. Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 325:458-462.
93. Pohlner, J., T. Klauser, E. Kuttler, and R. Halter. 1992. Sequence-specific cleavage of protein fusions using a recombinant Neisseria type 2 IgA protease. Biotechnology 10:799-804.
94. Reetz, M. T. 2000. Evolution in the test tube as a means to create enantioselective enzymes for use in organic synthesis. Sci. Prog. 83:157-172.
95. Reetz, M. T., S. Wilensek, D. Zha, and K. E. Jaeger. 2001. Directed evolution of an enantioselective enzyme through combinatorial multiple-cassette mutagenesis. Angew. Chem. Int. 40:3589-3591.
96. Rizos, K., C. T. Lattemann, D. Bumann, T. F. Meyer, and T. Aebischer. 2003. Autodisplay: efficacious surface exposure of antigenic UreA fragments from Helicobacter pylori in Salmonella vaccine strains. Infect. Immun. 71:6320-6328.
97. Robert, V., E. B. Volokhina, F. Senf, M. P. Bos, P. Van Gelder, and J. Tommassen. 2006. Assembly factor Omp85 recognizes its outer membrane protein substrates by a species-specific C-terminal motif. PLoS Biol. 4:e377.
98. Rosalki, S. B. 2001. C-reactive protein. Int. J. Clin. Pract. 55:269-270.
99. Ruiz-Olvera, P., F. Ruiz-Perez, N. V. Sepulveda, A. Santiago-Machuca, R. Maldonado-Rodriguez, G. Garcia-Elorriaga, and C. Gonzalez-Bonilla. 2003. Display and release of the Plasmodium falciparum circumsporozoite protein using the autotransporter MisL of Salmonella enterica. Plasmid 50:12-27.
100. Ruiz-Perez, F., R. Leon-Kempis, A. Santiago-Machuca, G. Ortega-Pierres, E. Barry, M. Levine, and C. Gonzalez-Bonilla. 2002. Expression of the Plasmodium falciparum immunodominant epitope (NANP)(4) on the surface of Salmonella enterica using the autotransporter MisL. Infect. Immun. 70:3611-3620.
101. Rutherford, N., M. E. Charbonneau, F. Berthiaume, J. M. Betton, and M. Mourez. 2006. The periplasmic folding of a cysteineless autotransporter passenger domain interferes with its outer membrane translocation. J. Bacteriol. 188:4111-4116.
102. Samuelson, P., M. Hansson, N. Ahlborg, C. Andreoni, F. Gotz, T. Balhi, T. N. Nguyen. H. Binz, M. Uhlen, and S. Stahl. 1995. Cell surface display of recombinant proteins on Staphylococcus carnosus. J. Bacteriol. 177:1470-1476.
103. Schauder, S., K. H. Schneider, and F. Giffhorn. 1995. Polyol metabolism of Rhodobacter sphaeroides: biochemical characterization of a short-chain sorbitol dehydrogenase. Microbiology 141:1857-1863.
104. Schindler, M., M. J. Osborn, and D. E. Koppel. 1980. Lateral diffusion of lipopolysaccharide in the outer membrane of Salmonella typhimurium. Nature 285:261-263.
105. Schmidt, M., M. Baumann, E. Henke, M. Konarzycka-Bessler, and U. T. Bornscheuer. 2004. Directed evolution of lipases and esterases. Methods Enzymol. 388:199-207.
106. Schreuder, M. P., A. T. Mooren, H. Y. Toschka, C. T. Verrips, and F. M. Klis. 1996. Immobilizing proteins on the surface of yeast cells. Trends Biotechnol. 14:115-120.
107. Schultheiss, E., C. Paar, H. Schwab, and J. Jose. 2002. Functional esterase surface display by the autotransporter pathway in Escherichia coli. J. Mol. Catal. 18:89-97.
108. Shamamian, P., J. D. Schwartz, B. J. Pocock, S. Monea, D. Whiting, S. G. Marcus, and P. Mignatti. 2001. Activation of progelatinase A (MMP-2) by neutrophil elastase, cathepsin G, and proteinase-3: a role for inflammatory cells in tumor invasion and angiogenesis. J. Cell Physiol. 189:197-206.
109. Shannon, J. L., and R. C. Fernandez. 1999. The C-terminal domain of the Bordetella pertussis autotransporter BrkA forms a pore in lipid bilayer membranes. J. Bacteriol. 181:5838-5842.
110. Shikata, S., K. Shimada, H. Kataoka, S. Horinouchi, and T. Beppu. 1992. Detection of large COOH-terminal domains processed from the precursor of Serratia marcescens serine protease in the outer membrane of Escherichia coli. J. Biochem. 111:627-632.
111. Shikata, S., K. Shimada, Y. Ohnishi, S. Horinouchi, and T. Beppu. 1993. Characterization of secretory intermediates of Serratia marcescens serine protease produced during its extracellular secretion from Escherichia coli cells. J. Biochem. (Tokyo) 114:723-731.
112. Shimada, K., Y. Ohnishi, S. Horinouchi, and T. Beppu. 1994. Extracellular transport of pseudoazurin of Alcaligenes faecalis in Escherichia coli using the COOH-terminal domain of Serratia marcescens serine protease. J. Biochem. 116:327-334.
113. Shiomi, D., M. Yoshimoto, M. Homma, and I. Kawagishi. 2006. Helical distribution of the bacterial chemoreceptor via colocalization with the Sec protein translocation machinery. Mol. Microbiol. 60:894-906.
114. Skillman, K. M., T. J. Barnard, J. H. Peterson, R. Ghirlando, and H. D. Bernstein. 2005. Efficient secretion of a folded protein domain by a monomeric bacterial autotransporter. Mol. Microbiol. 58:945-958.
115. Smith, G. P. 1985. Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 228:1315-1317.
116. Smith, G. P., and V. A. Petrenko. 1997. Phage display. Chem. Rev. 97:391-410.
117. Stahl, S., A. Robert, E. Gunneriusson, H. Wernerus, F. Cano, S. Liljeqvist, M. Hansson, T. N. Nguyen, and P. Samuelson. 2000. Staphylococcal surface display and its applications. Int. J. Med. Microbiol. 290:571-577.
118. Stathopoulos, C., G. Georgiou, and C. F. Earhart. 1996. Characterization of Escherichia coli expressing an Lpp'OmpA(46-159)-PhoA fusion protein localized in the outer membrane. Appl. Microbiol. Biotechnol. 45:112-119.
119. Steidler, L., J. Viaene, W. Fiers, and E. Remaut. 1998. Functional display of a heterologous protein on the surface of Lactococcus lactis by means of the cell wall anchor of Staphylococcus aureus protein A. Appl. Environ. Microbiol. 64:342-345.
120. Stein, M. A., A. Schafer, and F. Giffhorn. 1997. Cloning, nucleotide sequence, and overexpression of smoS, a component of a novel operon encoding an ABC transporter and polyol dehydrogenases of Rhodobacter sphaeroides Si4. J. Bacteriol. 179:6335-6340.
121. Steiner, D., P. Forrer, M. T. Stumpp, and A. Pluckthun. 2006. Signal sequences directing cotranslational translocation expand the range of proteins amenable to phage display. Nat. Biotechnol. 24:823-831.
122. St. Gerne, J. W., III, and D. Cutter. 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.
123. Strauss, A., and F. Gotz. 1996. In vivo immobilization of enzymatically active polypeptides on the cell surface of Staphylococcus camosus. Mol. Microbiol. 21:491-500.
124. Suhr, M., I. Benz, and M. A. Schmidt. 1996. Processing of the AIDA-I precursor: removal of AIDAc and evidence for the outer membrane anchoring as a beta-barrel structure. Mol. Microbiol. 22:31-42.
125. Suzuki, T., M. C. Lett, and C. Sasakawa. 1995. Extracellular transport of VirG protein in Shigella. J. Biol. Chem. 270:30874-30880.
126. Szabady, R. L., J. H. Peterson, K. M. Skillman, and H. D. Bernstein. 2005. An unusual signal peptide facilitates late steps in the biogenesis of a bacterial autotransporter. Proc. Natl. Acad. Sci. USA 102:221-226.
127. Thanassi, D. G., E. T. Saulino, M. J. Lombarde, R. Roth, J. Heuser, and S. J. Hultgren. 1998. The PapC usher forms an oligomeric channel: implications for pilus biogenesis across the outer membrane. Proc. Natl. Acad. Sci. USA 95:3146-3151.
128. Tommassen, J. 2007. Biochemistry. Getting into and through the outer membrane. Science 317:903-904.
129. Ueda, M., and T. A. 2000. Genetic immobilization of proteins on the yeast cell surface. Biotechnol. Adv. 18:121-140.
130. Vails, M., S. Atrian, V. de Lorenzo, and L. A. Fernandez. 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.
131. Vails, M., V. de Lorenzo, R. Gonzalez-Duarte, and S. Atrian. 2000. Engineering outer-membrane proteins in Pseudomonas putida for enhanced heavy-metal bioadsorption. J. Inorg. Biochem. 79:219-223.
132. Van der Vaart, J. M., R. te Biesebeke, J. W. Chapman, H. Y. Toschka, F. M. Klis, and C. T. Verrips. 1997. Comparison of cell wall proteins of Saccharomyces cerevisiae as anchors for cell surface expression of heterologous proteins. Appl. Environ. Microbiol. 63:615-620.
133. van Ulsen, P., L. van Alphen, J. ten Hove, F. Fransen, P. van der Ley, and J. Tommassen. 2003. A neisserial autotransporter NalP modulating the processing of other autotransporters. Mol. Microbiol. 50:1017-1030.
134. Veiga, E., V. de Lorenzo, and L. A. Fernandez. 2003. Autotransporters as scaffolds for novel bacterial adhesins: surface properties of Escherichia coli cells displaying Jun/Fos dimerization domains. J. Bacteriol. 185:5585-5590.
135. Veiga, E., V. De Lorenzo, and L. A. Fernandez. 2003. Neutralization of enteric coronaviruses with Escherichia coli cells expressing single-chain Fv-autotransporter fusions. J. Virol. 77:13396-13398.
136. Veiga, E., V. de Lorenzo, and L. A. Fernandez. 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.
137. Veiga, E., V. de Lorenzo, and L. A. Fernandez. 2004. Structural tolerance of bacterial autotransporters for folded passenger protein domains. Mol. Microbiol. 52:1069-1080.
138. Veiga, E., E. Sugawara, H. Nikaido, V. de Lorenzo, and L. A. Fernandez. 2002. Export of autotransported proteins proceeds through an oligomeric ring shaped by C-terminal domains. EMBO J. 21:2122-2131.
139. Voulhoux, R., M. P. Bos, J. Geurtsen, M. Mois, and J. Tommassen. 2003. Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299:262-265.
140. Voulhoux, R., and J. Tommassen. 2004. Omp85, an evolutionarily conserved bacterial protein involved in outer-membrane-protein assembly. Res. Microbiol. 155:129-135.
141. Wentzel, A., A. Christmann, T. Adams, and H. Kolmar. 2001. Display of passenger proteins on the surface of Escherichia coli K-12 by the enterohemorrhagic E. coli intimin EaeA. J. Bacteriol. 183:7273-7284.
142. Wentzel, A., A. Christmann, R. Kratzner, and H. Kolmar. 1999. Sequence requirements of the GPNG beta-turn of the Ecballium elaterium trypsin inhibitor II explored by combinatorial library screening. J. Biol. Chem. 274:21037-21043.
143. Wernerus, H., and S. Stahl. 2004. Biotechnological applications for surface-engineered bacteria. Biotechnol. Appl. Biochem. 40:209-228.
144. Wilhelm, S., J. Tommassen, and K. E. Jaeger. 1999. A novel lipolytic enzyme located in the outer membrane of Pseudomonas aeruginosa. J. Bacteriol. 181:6977-6986.
145. Yanagida, N., T. Uozumi, and T. Beppu. 1986. Specific excretion of Serratia marcescens protease through the outer membrane of Escherichia coli. J. Bacteriol. 166:937-944.
146. Yang, T. H., J. G. Pan, Y. S. Seo, and J. S. Rhee. 2004. Use of Pseudomonas putida EstA as an anchoring motif for display of a periplasmic enzyme on the surface of Escherichia coli. Appl. Environ. Microbiol. 70:6968-6976.
147. Yavin, E. J., and M. Fridkin. 1998. Peptides derived from human C-reactive protein inhibit the enzymatic activities of human leukocyte elastase and cathepsin G: use of overlapping peptide sequences to identify a unique inhibitor. J. Pept. Res. 51:282-289.
148. Yavin, E. J., L. Yan, D. M. Desiderio, and M. Fridkin. 1996. Synthetic peptides derived from the sequence of human C-reactive protein inhibit the enzymatic activities of human leukocyte elastase and human leukocyte cathepsin G. Int. J. Pept. Protein Res. 48:465-176.
149. Yeung, Y. A., and K. D. Wittrup. 2002. Quantitative screening of yeast surface-displayed polypeptide libraries by magnetic bead capture. Biotechnol. Prog. 18:212-220.
150. Zhu, C., F. Ruiz-Perez, Z. Yang, Y. Mao, V. L. Hackethal, K. M. Greco, W. Choy, K. Davis, J. R. Butterton, and E. C. Boedeker. 2006. Delivery of heterologous protein antigens via hemolysin or autotransporter systems by an attenuated 1er mutant of rabbit enteropathogenic Escherichia coli. Vaccine 24:3821-3831.