Structural tolerance of bacterial autotransporters for folded passenger protein domains

Molecular Microbiology

Volumn 52, Issue 4, 2004, Pages 1069-1080

  Veiga, Esteban ^a   De Lorenzo, Víctor ^a   Fernández, Luis Angel ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; IMMUNOGLOBULIN G;

ARTICLE; BACTERIAL MEMBRANE; BACTERIAL OUTER MEMBRANE; CONTROLLED STUDY; DISULFIDE BOND; ESCHERICHIA COLI; GENE TRANSLOCATION; MEMBRANE TRANSPORT; NEISSERIA GONORRHOEAE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; SOLUBILITY; STRUCTURE ANALYSIS;

ANTIGEN-ANTIBODY REACTIONS; BACTERIAL PHYSIOLOGY; BACTERIAL PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOPHILINS; MEMBRANE PROTEINS; MUTATION; NEISSERIA GONORRHOEAE; PEPTIDYLPROLYL ISOMERASE; PERIPLASMIC PROTEINS; PROTEIN CONFORMATION; PROTEIN DISULFIDE-ISOMERASE; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; SERINE ENDOPEPTIDASES;

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

EID: 3142680440     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2004.04014.x     Document Type: Article

References (68)

1. Alzari, P.M., Lascombe, M.B., and Poljak, R.J. (1988) Three-dimensional structure of antibodies. Annu Rev Immunol 6: 555-580.
2. Arie, J.P., Sassoon, N., and Betton, J.M. (2001) Chaperone function of FkpA, a heat shock prolyl isomerase, in the periplasm of Escherichia coli. Mol Microbiol 39: 199-210.
3. Arndt, K.M., Muller, K.M., and Plückthun, A. (1998) Factors influencing the dimer to monomer transition of an antibody single-chain Fv fragment. Biochemistry 37: 12918-12926.
4. Bardwell, J.C.A., McGovern, K., and Beckwith, J. (1991) Identification of a protein required for disulfide bond formation in vivo. Cell 67: 581-589.
5. Bothmann, H., and Plückthun, A. (2000) The periplasmic Escherichia coli peptidylprolyl cis,trans-isomerase FkpA. I. Increased functional expression of antibody fragments with and without cis-prolines. J Biol Chem 275: 17100-17105.
6. Brandon, L.D., and Goldberg, M.B. (2001) Periplasmic transit and disulfide bond formation of the autotransported Shigella protein IcsA. J Bacteriol 183: 951-958.
7. Bullock, W.O., Fernández, J.M., and Short, J.M. (1987) XL1-Blue: a high efficiency plasmid transforming recA Escherichia coli strain with beta-galactosidase selection. Biotechniques 4: 376-378.
8. Carter, P., Bedouelle, H., and Winter, G. (1985) Improved oligonucleotide site-directed mutagenesis using M13 vectors. Nucleic Acids Res 13: 4431-4443.
9. Chothia, C., Gelfand, I., and Kister, A. (1998) Structural determinants in the sequences of immunoglobulin variable domain. J Mol Biol 278: 457-479.
10. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
11. Decanniere, K., Desmyter, A., Lauwereys, M., Ghahroudi, M.A., Muyldermans, S., and Wyns, L. (1999) A single-domain antibody fragment in complex with RNase A: non-canonical loop structures and nanomolar affinity using two CDR loops. Structure Fold Des 7: 361-370.
12. Desmyter, A., Transue, T.R., Ghahroudi, M.A., Thi, M.H., Poortmans, F., Hamers, R., et al. (1996) Crystal structure of a camel single-domain VH antibody fragment in complex with lysozyme, Nat Struct Biol 3: 803-811.
13. Desmyter, A., Decanniere, K., Muyldermans, S., and Wyns, L. (2001) Antigen specificity and high affinity binding provided by one single loop of a camel single-domain antibody. J Biol Chem 276: 26285-26290.
14. Emsley, P., Charles, I.G., Fairweather, N.F., and Isaacs, N.W. (1996) Structure of Bordetella pertussis virulence factor P69 pertactin. Nature 381: 90-92.
15. Gelfand, I.M., and Kister, A.E. (1995) Analysis of the relation between the sequence and secondary and three-dimensional structures of immunoglobulin molecules. Proc Natl Acad Sci USA 92: 10884-10888.
16. Glockshuber, R., Schimidt, T., and Plückthun, A. (1992) The disulfide bonds in antibody variable domains: effects on stability, folding in vitro, and functional expression in Escherichia coli. Biochemistry 31: 1270-1279.
17. Goto, Y., and Hamaguchi, K. (1979) The role of the intrachain disulfide bond in the conformation and stability of the constant fragment of the immunoglobulin light chain. J Biochem (Tokyo) 86: 1433-1441.
18. Grodberg, J., and Dunn, J.J. (1988) OmpT encodes the Escherichia coli outer membrane protease that cleaves T7 RNA polymerase during purification. J Bacteriol 170: 1245-1253.
19. Hamers-Casterman, C., Atarhouch, T., Muyldermans, S., Robinson, G., Hamers, C., Songa, E.B., et al. (1993) Naturally occurring antibodies devoid of light chains. Nature 363: 446-448.
20. Hardy, S.J., Holmgren, J., Johansson, S., Sanchez, J., and Hirst, T.R. (1988) Coordinated assembly of multisubunit proteins: oligomerization of bacterial enterotoxins in vivo and In vitro. Proc Natl Acad Sci USA 85: 109-113.
21. Harms, N., Koningstein, G., Dontje, W., Muller, M., Oudega, B., Luirink, J., and de Cock, H. (2001) The early interaction of the outer membrane protein phoe with the periplasmic chaperone Skp occurs at the cytoplasmic membrane. J Biol Chem 276: 18804-18811.
22. Henderson, I.R., and Nataro, J.P. (2001) Virulence functions of autotransporter proteins. Infect Immun 69: 1231-1243.
23. Henderson, I.R., Navarro-Garcia, F., and Nataro, J.P. (1998) The great escape: structure and function of the autotransporter proteins. Trends Microbiol 6: 370-378.
24. Henderson, I.R., Cappello, R., and Nataro, J.P. (2000) Autotransporter proteins, evolution and redefining protein secretion. Trends Microbiol 8: 529-532.
25. Jose, J., Krämer, J., Klauser, T., Pohlner, J., and Meyer, T.F. (1996) Absence of periplasmic DsbA oxidoreductase facilitates export of cysteine-containing passenger proteins to the Escherichia coli cell surface via the Igaβ autotransporter pathway. Gene 178: 107-110.
26. Jose, J., Bernhardt, R., and Hannemann, F. (2002) Cellular surface display of dimeric Adx and whole cell P450-mediated steroid synthesis on E. coli. J Biotechnol 95: 257-268.
27. Jurado, P., Ritz, D., Beckwith, J., de Lorenzo, V., and Fernandez, L.A. (2002) Production of functional single-chain Fv antibodies in the cytoplasm of Escherichia coli. J Mol Biol 320: 1-10.
28. Kajava, A.V., Cheng, N., Cleaver, R., Kessel, M., Simon, M.N., Willery, E., et al. (2001) Beta-helix model for the filamentous haemagglutinin adhesin of Bordetella pertussis and related bacterial secretory proteins. Mol Microbiol 42: 279-292.
29. Kaufmann, M., Lindner, P., Honegger, A., Blank, K., Tschopp, M., Capitani, G., et al. (2002) Crystal structure of the anti-His tag antibody 3D5 single-chain fragment complexed to its antigen. J Mol Biol 318: 135-147.
30. Keen, N.T., and Tamaki, S. (1986) Structure of two pectate lyase genes from Erwinia chrysanthemi EC16 and their high-level expression in Escherichia coli. J Bacteriol 168: 595-606.
31. Kjaergaard, K., Hasman, H., Schembri, M.A., and Klemm, P. (2002) Antigen 43-mediated autotransporter display, a versatile bacterial cell surface presentation system. J Bacteriol 184: 4197-4204.
32. Klauser, T., Pohlner, J., and Meyer, T.F. (1990) Extracellular transport of cholera toxin B subunit using Neisseria IgA protease β-domain: conformation-dependent outer membrane translocation. EMBO J 9: 1991-1999.
33. Klauser, T., Pohlner, J., and Meyer, T.F. (1992) Selective extracellular release of cholera toxin B subunit by Escherichia coli: dissection of Neisseria Igaβ-mediated outer membrane transport. EMBO J 11: 2327-2335.
34. Klauser, T., Krämer, J., Otzelberger, K., Pohlner, J., and Meyer, T.F. (1993) Characterization of the Neisseria Igaβ-core. The essential unit for outer membrane targeting and extracellular protein secretion. J Mol Biol 234: 579-593.
35. Klemm, P., Hjerrild, L., Gjermansen, M., and Schembri, M.A. (2004) Structure-function analysis of the self-recognizing Antigen 43 autotransporter protein from Escherichia coli. Mol Microbiol 51: 283-296.
36. Klose, M., Storiko, A., Stierhof, Y.D., Hindennach, I., Mutschler, B., and Henning, U. (1993) Membrane assembly of the outer membrane protein OmpA of Escherichia coli. J Biol Chem 268: 25664-25670.
37. Koebnik, R., Locher, K.P., and Van Gelder, P. (2000) Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol 37: 239-253.
38. Lattemann, C.T., Maurer, J., Gerland, E., and Meyer, T.F. (2000) Autodisplay: functional display of active beta-lactamase on the surface of Escherichia coli by the AIDA-I autotransporter. J Bacteriol 182: 3726-3733.
39. Lee, V.T., and Schneewind, O. (2001) Protein secretion and the pathogenesis of bacterial infections, Genes Dev 15: 1725-1752.
40. de Lorenzo, V., Eltis, L., Kessler, B., and Timmis, K.N. (1993) Analysis of Pseudomonas gene products using laclq/Ptrp-lac plasmids and transposons that confer conditional phenotypes. Gene 123: 17-24.
41. Lory, S. (1998) Secretion of proteins and assembly of bacterial surface organelles: shared pathways of extracellular protein targeting. Current Opinion Microbiol 1: 27-35.
42. Loveless, B.J., and Saier, M.H. Jr (1997) A novel family of channel-forming, autotransporting, bacterial virulence factors. Mol Membr Biol 14: 113-123.
43. Martin, J.L., Bardwell, J.C.A., and Kuriyan, J. (1993) Crystal structure of the DsbA protein required for disulphide bond formation in vivo. Nature 365: 464-468.
44. Miller, J.H. (1992) A Short Course In Bacterial Genetics: A Laboratory Manual And Handbook For Escherichia Coli And Related Bacteria. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
45. Missiakas, D., Betton, J.M., and Raina, S. (1996) New components of protein folding in extracytoplasmic compartments of Escherichia coli SurA, FkpA and Skp/OmpH. Mol Microbiol 21: 871-884.
46. Muyldermans, S. (2001) Single domain camel antibodies: current status. J Biotechnol 74: 277-302.
47. Muyldermans, S., and Lauwereys, M. (1999) Unique single-domain antigen binding fragments derived from naturally occurring camel heavy-chain antibodies. J Mol Recognit 12: 131-140.
48. Ohnishi, Y., Nishiyama, M., Horinouchi, S., and Beppu, T. (1994) Involvement of the COOH-terminal pro-sequence of Serratia marcescens serine protease in the folding of the mature enzyme. J Biol Chem 269: 32800-32806.
49. Oliver, D.C., Huang, G., Nodel, E., Pleasance, S., and Fernandez, R.C. (2003) A conserved region within the Bordetella pertussis autotransporter BrkA is necessary for folding of its passenger domain. Mol Microbiol 47: 1367-1383.
50. Oomen, C.J., van Ulsen, P., Van Gelder, P., Feijen, M., Tommassen, J., and Gros, P. (2004) Structure of the translocator domain of a bacterial autotransporter. EMBO J (in press).
51. Pohlner, J., Halter, R., Beyreuther, K., and Meyer, T.F. (1987) Gene structure and extracellular secretion of Neisseria gonorrhoea IgA protease. Nature 325: 458-462.
52. Proba, K., Wörn, A., Honegger, A., and Plückthun, A. (1998) Antibody scFv fragments without disulfide bonds made by molecular evolution. J Mol Biol 275: 245-253.
53. Purdy, G.E., Hong, M., and Payne, S.M. (2002) Shigella flexneri DegP facilitates IcsA surface expression and is required for efficient intercellular spread. Infect Immun 70: 6355-6364.
54. Quintela, J.C., Pedro, M.A.D., Zöllner, P., Allmaier, G., and Portillo, F.G.-d. (1997) Peptidoglycan structure of Salmonella typhimurium growing within cultured mammalian cells. Mol Microbiol 23: 693-704.
55. Ramm, K., and Plückthun, A. (2000) The periplasmic Escherichia coli peptidylprolyl cis,trans-isomerase FkpA. II. Isomerase-independent chaperone activity in vitro. J Biol Chem 275: 17106-17113.
56. Ramm, K., Gehrig, P., and Pluckthun, A. (1999) Removal of the conserved disulfide bridges from the scFv fragment of an antibody: effects on folding kinetics and aggregation. J Mol Biol 290: 535-546.
57. Riechmann, L., and Muyldermans, S. (1999) Single domain antibodies: comparison of camel VH and camelised human VH domains. J Immunol Meth 231: 25-38.
58. Ried, G., Koebnik, R., Hindennach, I., Mutschler, B., and Henning, U. (1994) Membrane topology and assembly of the outer membrane protein OmpA of Escherichia coli K12. Mol Gen Genet 243: 127-135.
59. Sheriff, S., and Constantine, K.L. (1996) Redefining the minimal antigen-binding fragment. Nat Struct Biol 3: 733-736.
60. Spiess, C., Beil, A., Ehrmann, M., Delepelaire, P., and Wandersman, C. (1999) A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97: 339-347.
61. Tamm, L.K., Arora, A., and Kleinschmidt, J.H. (2001) Structure and asssembly of beta-barrel membrane proteins. J Biol Chem 276: 32399-32402.
62. van Ulsen, P., van Alphen, L., ten Hove, J., Fransen, F., van der Ley, P., and Tommassen, J. (2003) A Neisserial autotransporter NalP modulating the processing of other autotransporters. Mol Microbiol 50: 1017-1030.
63. Valls, M., Atrian, S., de Lorenzo, V., and Fernández, L.A. (2000) Engineering a mouse metallothionein on the cell surface of Ralstonia eutropha CH34 for immobilization of heavy metals in soil. Nat Biotechnol 18: 661-665.
64. Veiga, E., de Lorenzo, V., and Fernández, L.A. (1999) Probing secretion and translocation of a beta-autotransporter using a reporter single-chain Fv as a cognate passenger domain. Mol Microbiol 33: 1232-1243.
65. Veiga, E., Sugawara, E., Nikaido, H., de Lorenzo, V., and Fernandez, L.A. (2002) Export of autotransported proteins proceeds through an oligomeric ring shaped by C-terminal domains. EMBO J 21: 2122-2131.
66. Williams, A.F., and Barclay, A.N. (1988) The immunoglobulin superfamily - domains for cell surface recognition. Annu Rev Immunol 6: 381-405.
67. Wörn, A., and Plückthun, A. (1999) Different equilibrium stability behavior of ScFv fragments: identification, classification, and improvement by protein engineering. Biochemistry 38: 8739-8750.
68. Wörn, A., and Plückthun, A. (2001) Stability engineering of antibody single-chain Fv fragments. J Mol Biol 305: 989-1010.