Filamentous phage infection: Crystal structure of g3p in complex with its coreceptor, the C-terminal domain of TolA

Structure

Volumn 7, Issue 6, 1999, Pages 711-722

  Lubkowski, Jacek ^a   Hennecke, Frank ^b,c   Plückthun, Andreas ^b   Wlodawer, Alexander ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c CYTOS BIOTECHNOLOGY AG   (Switzerland)

Author keywords

Phage display; Phage infection; Protein fusion; Protein structure; Structure refinement

Indexed keywords

BACTERIAL PROTEIN; MEMBRANE PROTEIN;

ARTICLE; BACTERIOPHAGE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

ESCHERICHIA COLI;

EID: 0000046526     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(99)80092-6     Document Type: Article

References (64)

1. Smith, G.P. (1985). Filamentous fusion phage: Novel expression vectors that display cloned antigens on the virion surface. Science 228, 1315-1317.
2. Phizicky, E.M. & Fields, S. (1995). Protein-protein interactions: Methods for detection and analysis. Microbiol. Rev. 59, 94-123.
3. Cortese, R., et al., & Felici, F. (1996). Selection of biologically active peptides by phage display of random peptide libraries. Curr. Opin. Biotechnol. 7, 616-621.
4. Felici, F., Luzzago, A. Monaci, P., Nicosia, A., Sollazzo, M., &Traboni, C. (1995). Peptide and protein display on the surface of filamentous bacteriophage. Biotechnol. Annu. Rev. 1, 149-183.
5. Spada, S., Krebber, C. & Plückthun, A. (1997). Selectively infective phages (SIP). Biol. Chem. 378, 445-456.
6. Gray, C.W., Brown, R.S. & Marvin, D.A. (1981). Adsorption complex of filamentous fd virus. J. Mol. Biol. 146, 621-627.
7. Stengele, I., Bross, P., Garces, X., Giray, J. & Rasched, I. (1990). Dissection of functional domains in phage fd adsorption protein. Discrimination between attachment and penetration sites. J. Mol. Biol. 212, 143-149.
8. Jacobson, A. (1972). Role of F pili in the penetration of bacteriophage fl. J. Virol. 10, 835-843.
9. Riechmann, L. & Holliger, P. (1997). The C-terminal domain of TolA is the coreceptor for filamentous phage infection of E. coli. Cell 90, 351-360.
10. Click, E.M. & Webster, R.E. (1997). Filamentous phage infection: Required interactions with the TolA protein. J. Bacteriol. 179, 6464-6471.
11. Levengood, S.K., Beyer, W.F., Jr. & Webster, R.E. (1991). TolA: A membrane protein involved in colicin uptake contains an extended helical region. Proc. Natl. Acad. Sci. USA 88, 5939-5943.
12. Sun, T.P. & Webster, R.E. (1986). fii, a bacterial locus required for filamentous phage infection and its relation to colicin-tolerant tolA and tolB. J. Bacteriol. 165, 107-115.
13. Sun, T.P. & Webster, R.E. (1987). Nucleotide sequence of a gene cluster involved in entry of E colicins and single-stranded DNA of infecting filamentous bacteriophages into Escherichia coli. J. Bacteriol. 169, 2667-2674.
14. Russel, M., Whirlow, H., Sun, T.P. & Webster, R.E. (1988). Low-frequency infection of F- bacteria by transducing particles of filamentous bacteriophages. J. Bacteriol. 170, 5312-5316.
15. Webster, R.E. (1991). The tol gene products and the import of macromolecules into Escherichia coli. Mol. Microbiol. 5, 1005-1011.
16. Braun, V. & Herrmann, C. (1993). Evolutionary relationship of uptake systems for biopolymers in Escherichia coli: Cross-complementation between the TonB-ExbB- ExbD and the TolA-TolQ-TolR proteins. Mol. Microbiol. 8, 261-268.
17. Braun (1995). Energy-coupled transport and signal transduction through the gram-negative outer membrane via TonB-ExbB-ExbD-dependent receptor proteins. FEMS Microbiol. Rev. 16, 295-307.
18. Moeck, G.S. & Coulton, J.W. (1998). TonB-dependent iron acquisition: Mechanisms of siderophore-mediated active transport. Mol. Microbiol. 28, 675-681.
19. Lazzaroni, J.C., Fognini-Lefebvre, N. & Portalier, R. (1989). Cloning of the excC and excD genes involved in the release of periplasmic proteins by Escherichia coli K12. Mol. Gen. Genet. 218, 460-464.
20. Lazzaroni, J.C. & Portalier, R.C. (1981). Genetic and biochemical characterization of periplasmic-leaky mutants of Escherichia coli K-12. J. Bacteriol. 145, 1351-1358.
21. Levengood-Freyermuth, S.K., Click, E.M. & Webster, R.E. (1993). Role of the carboxyl-terminal domain of TolA in protein import and integrity of the outer membrane. J. Bacterial. 175, 222-228.
22. Rampf, B., Brass, P., Vocke, T. & Rasched, I. (1991). Release of periplasmic proteins induced in E. coli by expression of an N-terminal proximal segment of the phage fd gene 3 protein. FEBS Lett. 280, 27-31.
23. Amouroux, C., Lazzaroni, J.C. & Portalier, R. (1991). Isolation and characterization of extragenic suppressor mutants of the tolA-876 periplasmic-leaky allele in Escherichia coli K-12. FEMS Microbiol. Lett. 62, 305-313.
24. Hancock, R.W. & Braun, V. (1976). Nature of the energy requirement for the irreversible adsorption of bacteriophages T1 and phi80 to Escherichia coli. J. Bacteriol. 125, 409-415.
25. Vetter, I.R., Parker, M.W., Tucker, A.D., Lakey, J.H., Pattus, F. & Tsernoglou, D. (1998). Crystal structure of a colicin N fragment suggests a model for toxicity. Structure 6, 863-874.
26. Lazdunski, C.J. (1995). Colicin import and pore formation: A system for studying protein transport across membranes? Mol. Microbiol. 16, 1059-1066.
27. Lubkowski, J., Hennecke, F., Plückthun, A. & Wlodawer, A. (1998). The structural basis of phage display elucidated by the crystal structure of the N-terminal domains of g3p. Nat. Struct. Biol. 5, 140-147.
28. Hutchinson, E.G. & Thornton, J.M. (1996). PROMOTIF - A program to identify and analyze structural motifs in proteins. Prot. Sci. 5, 212-220.
29. Holliger, P. & Riechmann, L. (1997). A conserved infection pathway for filamentous bacteriophages is suggested by the structure of the membrane penetration domain of the minor coat protein g3p from phage fd. Structure 5, 265-275.
30. Holm, L. & Sander, C. (1993). Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233, 123-138.
31. Boisvert, D.C., Wang, J., Otwinowski, Z., Horwich, A.L. & Sigler, P.B. (1996). The 2.4 Å structure of the bacterial chaperonin GroEL complexed with ATP gamma S. Nat. Struct. Biol. 3, 170-177.
32. Das, A.K., Helps, N.R., Cohen, P.T. & Barford, D. (1996). Crystal structure of the protein serine/threonine phosphatase 2C at 2.0 Å resolution. EMBO J. 15, 6798-6809.
33. Zhang, Z., et al., & Kim, S.H. (1998). Electron transfer by domain movement in cytochrome bc1. Nature 392, 677-684.
34. Altschul, S.F., et al., & Lipman, D.J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
35. Frost, L.S., Ippen-Ihler, K. & Skurray, R.A. (1994). Analysis of the sequence and gene products of the transfer region of the F sex factor. Microbiol. Rev. 58, 162-210.
36. Krebber, C., Spada, S., Desplancq, D., Krebber, A., Ge, L. & Plückthun, A. (1997). Selectively-infective phage (SIP): A mechanistic dissection of a novel in vivo selection for protein-ligand interactions. J. Mol. Biol. 268, 607-618.
37. Guihard, G., Boulanger, P., Benedetti, H., Lloubes, R., Besnard, M. & Letellier, L. (1994). Colicin A and the Tol proteins involved in its translocation are preferentially located in the contact sites between the inner and outer membranes of Escherichia coli cells. J. Biol. Chem. 269, 5874-5880.
38. Peeters, B.P.H., Peters, RM, Schoenmakers, J.G.G. & Konings, R.N.H. (1985). Nucleotide sequence and genetic organizaton of the genome of the N-specific filamentous bacteriophage lke. Comparison with the genome of the F-specific filamentous phages M13, fd and fl. J. Mol. Biol. 181, 27-39.
39. Strassen, A.P.M., Schoenmakers, E.F.P.M., Yu, M., Schoenmakers, J.G.G., & Konings, R.N.H. (1992). Nucleotide sequence of the genome of the filamentous bacteriophage l2-2: Module evolution of the filamentous phage genome. J. Mol. Evol. 34, 141-152.
40. Endemann, H., Bross, P. & Rasched, I. (1992). The adsorption protein of phage lKe. Localization by deletion mutagenesis of domains involved in infectivity. Mol. Microbiol. 6, 471-478.
41. Huston, J.S., et al., & Oppermann, H. (1991). Protein engineering of single-chain Fv analogs and fusion proteins. Methods Enzymol. 203, 46-88.
42. Schramm, E., Wende, J., Braun, V. & Kamp, R.M. (1987). Nucleotide sequence of the colicin B activity gene cba: Consensus pentapeptide among TonB-dependent colicins and receptors. J. Bacteriol. 169, 3350-3357.
43. Wiener, M., Freymann, D., Ghosh, P. & Stroud, R.M. (1997). Crystal structure of colicin la. Nature 385, 461-464.
44. Schendel, S.L., Click, E.M., Webster, R.E. &Cramer, W.A. (1997). The TolA protein interacts with colicin E1 differently than with other group A colicins. J. Bacteriol. 179, 3683-3690.
45. Garinot-Schneider, C., Penfold, C.N., Moore, G.R., Kleanthous, C. & James, R. (1997). Identification of residues in the putative TolA box which are essential for the toxicity of the endonuclease toxin colicin E9. Microbiology 143, 2931-2938.
46. Wickner, W. (1975). Asymmetric orientation of a phage coat protein in cytoplasmic membrane of Escherichia coli. Proc. Natl Acad. Sci. USA 72, 4749-4753.
47. Armstrong, J., Hewitt, J.A. & Perham, R.N. (1983). Chemical modification of the coat protein in bacteriophage fd and orientation of the virion during assembly and disassembly. EMBO J. 10, 1641-1646.
48. Ebright, R., Dong, Q. & Messing, J. (1992). Corrected nucleotide sequence of M13mp18 gene III. Gene 114, 81-83.
49. Levengood, S.K. & Webster, R.E. (1989). Nucleotide sequences of the tolA and tolB genes and localization of their products, components of a multistep translocation system in Escherichia coli. J. Bacteriol. 171, 6600-6609.
50. Hirel, P.M., Schmitter, M.J., Dessen, P., Fayat, G. & Blanquet, S. (1989). Extent of N-terminal methionine excision from Escherichia coli proteins is governed by the sidechain length of the penultimate amino acid. Proc. Natl Acad. Sci. USA 86, 8247-8251.
51. Ge, L., Knappik, A., Pack, P., Freund, C. & Plückthun, A. (1995). Expressing antibodies in Escherichia coli. In Antibody Engineering., (Borrebaeck, C.A.K., ed.), pp. 229-266, Oxford University Press, Oxford.
52. Freund, C., Ross, A., Guth, B., Pluckthun, A. & Holak, T.A. (1993). Characterization of the linker peptide of the single-chain Fv fragment of an antibody by NMR spectroscopy. FEBS Lett. 320, 97-100.
53. Studier, F.W. & Moffatt, B.A. (1986). Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189, 113-130.
54. Plückthun, A., et al., & Riesenberg, D. (1996). Producing antibodies in Escherichia coli: From PCR to fermentation. In Antibody Engineering: A Practical Approach (McCafferty, J., Hoogenboom, H.R. & Chiswell. D.J., eds), pp. 203-252, IRL Press, Oxford.
55. Navaza, J. (1994). An automated package for molecular replacement. Acta Cryst. A 50, 157-163.
56. Sheldrick, G.M. (1997). Patterson superposition and ab initio phasing. In Methods in Enzymology. (Carter, C.W., Jr. & Sweet, R.M., eds), pp. 628-641, Academic Press, New York, NY.
57. Furey, W. & Swaminathan, S. (1990). PHASES - A program package for the processing and analysis of diffraction data for macromolecules. Acta Crystallogr. 18, 73.
58. Collaborative Computational Project, Number (1994). The CCP4 suite: Programs for protein crystallography. Acta Crystallogr. D 50, 760-763.
59. de la Fortelle, E.B.G. (1997). Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. In Methods in Enzymology. (C.W. Carter, Jr. & R.M. Sweet., eds), pp. 472-494, Academic Press, NY.
60. Brünger, A.T. (1992). X-PLOR version 3.1: A System for X-ray Crystallography and NMR. Yale University Press, New Haven, CT.
61. Sheldrick, G.M. & Schneider, T.R. (1997). SHELXL: High-resolution refinement. In Methods in Enzymology. (C.W. Carter, Jr. & R.M. Sweet., eds), pp. 319-343. Academic Press, New York, NY.
62. Zdanov, A., Schalk-Hihi, C., Gustchina, A., Tsang, M., Weatherbee, J. & Wlodawer, A. (1995). Crystal structure of interleukin-10 reveals the functional dimer with an unexpected topological similarity to interferon γ. Structure 3, 591-601.
63. Carson, M. (1991). Ribbons 4.0. J. Appl. Crystallogr. 24, 958-961.
64. Kraulis, P.J. (1991). MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-950.