Article | Published:

The structural basis of phage display elucidated by the crystal structure of the N-terminal domains of g3p

Nature Structural Biologyvolume 5pages140147 (1998) | Download Citation

Subjects

Abstract

The structure of the two N-terminal domains of the gene 3 protein of filamentous phages (residues 1–217) has been solved by multiwavelength anomalous diffraction and refined at 1.46 A resolution. Each domain consists of either five or eight β-strands and a single α-helix. Despite missing sequence homology, their cores superimposed with a root-mean-square deviation of 2 ?. The domains are engaged in extensive interactions, resulting in a horseshoe shape with aliphatic amino acids and threonines lining the inside, delineating the likely binding site for the F-pilus. The glycine-rich linker connecting the domains is invisible in the otherwise highly ordered structure and may confer flexibility between the domains required during the infection process.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1

    Smith, G.P. Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 228, 1315–1317 (1985).

  2. 2

    Phizicky, E.M. & Fields, S. Protein–protein interactions: methods for detection and analysis. Microbiol. Rev. 59, 94–123 (1995).

  3. 3

    Cortese, R. et al Selection of biologically active peptides by phage display of random peptide libraries. Curr. Opin. Biotechnol. 7, 616–621 (1996).

  4. 4

    Dunn, I.S. Phage display of proteins. Curr. Opin. Biotechnol. 7, 547–553 (1996).

  5. 5

    Spada, S., Krebber, C. & Plückthun, A. Selectively infective phages (SIP). Biol. Chem. 378, 445–456 (1997).

  6. 6

    Gray, C.W., Brown, R.S. & Marvin, D.A. Adsorption complex of filamentous fd virus. J. Mol. Biol. 146, 621–627 (1981).

  7. 7

    Jacobson, A. Role of F pili in the penetration of bacteriophage fl. J. Virol. 10, 835–843 (1972).

  8. 8

    Sun, T.P. & Webster, R.E. fii, a bacterial locus required for filamentous phage infection and its relation to colicin-tolerant tolA and tolB. J. Bacterial. 165, 107–115 (1986).

  9. 9

    Sun, T.P. & Webster, R.E. 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 (1987).

  10. 10

    Riechmann, L. & Holliger, P. The C-terminal domain of TolA is the coreceptorfor filamentous phage infection of E. coli. Cell 90, 351–360 (1997).

  11. 11

    Nelson, F.K., Friedman, S.M. & Smith, G.P. Filamentous phage DNA cloning vectors: a noninfective mutant with a nonpolar deletion in gene III. Virology 108, 338–350 (1981).

  12. 12

    Crissman, J.W. & Smith, G.P. Gene-Ill protein of filamentous phages: evidence for a carboxyl-terminal domain with a role in morphogenesis. Virology 132, 445–455 (1984).

  13. 13

    Endemann, H., Gailus, V. & Rasched, I. Interchangeability of the adsorption proteins of bacteriophages Ff and IKe. J. Virol. 67, 3332–3337 (1993).

  14. 14

    Hutchinson, E.G. & Thornton, J.M. PROMOTIF - a program to identify and analyze structural motifs in proteins. Protein Sci. 5, 212–220 (1996).

  15. 15

    Holm, L. & Sander, C Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233, 123–138 (1993).

  16. 16

    Cabral, J.H, et al. Crystal structure of a PDZ domain. Nature 382, 649–652 (1996).

  17. 17

    Faber, H.R. et al. 1.8 ? crystal structure of the C-terminal domain of rabbit serum haemopexin. Structure 3, 551–559 (1995).

  18. 18

    Viguera, A.R., Blanco, F.J. & Serrano, L. The order of secondary structure elements does not determine the structure of a protein but does affect its folding kinetics. J. Mol. Biol. 247, 670–681 (1995).

  19. 19

    Holliger, P. & Riechmann, L. 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 (1997).

  20. 20

    Koradi, R., Billeter, M. & Wüthrich, K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14, 51–5, 29–32 (1996).

  21. 21

    Baldwin, E.T. et al. Crystal structure of interleukin-8: symbiosis of NMR and crystallography. Proc. Natl. Acad. Sci. USA 88, 502–506 (1991).

  22. 22

    Lubkowski, J. et al. The structure of MCP-1 in two crystal forms provides a rare example of variable quarternary interactions. Nature Struct. Biol. 4, 64–69 (1997).

  23. 23

    Stengele, I., Bross, P., Garces, X., Giray, J. & Rasched, I. Dissection of functional domains in phage fd adsorption protein. Discrimination between attachment and penetration sites. J. Mol. Biol. 212, 143–149 (1990).

  24. 24

    Krebber, C. et al. Selectively-infective phage (SIP): a mechanistic dissection of a novel in vivo selection for protein-ligand interactions. J. Mol. Biol. 268, 607–618 (1997).

  25. 25

    Peters, B.P.H., Peters, R.M., Schoenmakers, J.G.G. & Konings, R.N.H. Nucleotide sequence and genetic organizaton of the genome of the N-specific filamentous bacteriophage IKe. Comparison with the genome of the F-specific filamentous phages M13, fd and fl. J. Mol. Biol. 181, 27–39 (1985).

  26. 26

    Frost, L.S., Ippen-lhler, K. & Skurray, R.A. Analysis of the sequence and gene products of the transfer region of the F sex factor. Microbiol. Rev. 58, 162–210 (1994).

  27. 27

    Marvin, D.A. & Folkhard, W. Structure of F-pili: reassessment of the symmetry. J. Mol. Biol. 191, 299–300 (1986).

  28. 28

    Glucksman, M.J., Bhattacharjee, S. & Makowski, L. Three-dimensional structure of a cloning vector. X-ray diffraction studies of filamentous bacteriophage M13 at 7? resolution. J. Mol. Biol. 226, 455–470 (1992).

  29. 29

    Lin, T.C., Webster, R.E. & Konigsberg, W. Isolation and characterization of the C and D proteins coded by gene IX and gene VI in the filamentous bacteriophage fl and fd. J. Biol. Chem. 255, 10331–10337 (1980).

  30. 30

    Grant, R.A., Lin, T.C., Webster, R.E. & Konigsberg, W. Structure of filamentous bacteriophage: isolation, characterization, and localization of the minor coat proteins and orientation of the DNA. Prog. Clin. Biol. Res. 64: 413–428 (1981).

  31. 31

    Tzagoloff, H. & Pratt, D. The initial steps in infection with coliphage M13. Virology 24, 372–380 (1964).

  32. 32

    Goldsmith, M.E. & Konigsberg, W.H. Adsorption protein of the bacteriophage fd: isolation, molecular properties, and location in the virus. Biochemistry 16, 2686–2694 (1977).

  33. 33

    Beck, E. & Zink, B. Nucleotide sequence and genome organisation of filamentous bacteriophages fl and fd. Gene 16, 35–58 (1981).

  34. 34

    Freund, C., Ross, A., Guth, B., Plückthun, A. & Holak, T.A. Characterization of the linker peptide of the single-chain Fv fragment of an antibody by NMR spectroscopy. FEBS Lett. 320, 97–100 (1993).

  35. 35

    S tudier, F.W. & Moffatt, B.A. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189, 113–130 (1986).

  36. 36

    Qoronfleh, M.W. et al. Production of selenomethionine-labeled recombinant human neutrophil collagenase in Escherichia coli. J. Biotechnol. 39, 119–128 (1995).

  37. 37

    Plückthun, A., et al. Producing antibodies in Escherichia coli: from PCR to fermentation. In Antibody engineering: a practical approach (eds McCafferty, J. & Hoogenboom, H.R., Chriswell, D.J.) 203–252 (IRL Press, Oxford; 1996).

  38. 38

    Hendrickson, W.A., Horton, J.R. & LeMaster, D.M. Selenomethionyl proteins produced for analysis by multiwavelength anomalous diffraction (MAD): a vehicle for direct determination of three dimensional structure. EMBO J. 9, 1665–1672 (1990).

  39. 39

    Matthews, B.W. Solvent content of protein crystals. J. Mol. Biol. 33, 491–497 (1968).

  40. 40

    Otwinowski, Z. An oscillation data processing suite for macromolecular crystallography (Yale University, New Haven, Connecticut, USA; 1992).

  41. 41

    Jones, T.A. & Kjeldgaard, M.O — the manual (Uppsala University, Uppsala, 1994).

  42. 42

    Brünger, A. X-plor version 3.1: a system for X-ray crystallography and NMR (Yale University Press, New Haven, Connecticut, USA; 1992).

  43. 43

    Furey, W. & Swaminathan, S. PHASES - A program package for the processing and analysis of diffraction data for macromolecules. Acta Crystallogr. 18, 73 (1990).

  44. 44

    Sheldrick, G.M. Patterson superposition and ab initio phasing. Meth. Enz. 276, 628–641 (1997).

  45. 45

    Wang, B.C. Resolution of phase ambiguity in macromolecular crystallography. Meth. Enz. 115, 90- 112 (1985).

  46. 46

    CCP4:SERC Collaborative computing project no.4 (Warrington, UK; 1979).

  47. 47

    Lundblad, R.L. & Noyes, C.M. Chemical modification of tryptophan. In Chemical reagents for protein modification (eds. Lundblad, R.L. & Noyes, C.M.) 47–71 (CRC Press, Boca Raton, Florida; 1984 ).

  48. 48

    Kraulis, P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946–950 (1991).

  49. 49

    Carson, M. RIBBONS 4.0. J. Appl.Crystallogr. 24, 958–961 (1991).

  50. 50

    Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. PROCHECK: A program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283–291 (1993).

Download references

Author information

Affiliations

  1. Macromolecular Structure Laboratory, ABL-Basic Research Program, NCI-FCRDC, P.O. Box B, Frederick, Maryland, 21702, USA

    • Jacek Lubkowski
    •  & Alexander Wlodawer
  2. Biochemisches Institut, Universität Zürich, Winterthurerstr. 190, CH-8057, Zürich, Switzerland

    • Frank Hennecke
    •  & Andreas Plückthun

Authors

  1. Search for Jacek Lubkowski in:

  2. Search for Frank Hennecke in:

  3. Search for Andreas Plückthun in:

  4. Search for Alexander Wlodawer in:

Corresponding author

Correspondence to Alexander Wlodawer.

About this article

Publication history

Received

Accepted

Issue Date

DOI

https://doi.org/10.1038/nsb0298-140

Further reading