Atomic structure of single-stranded DNA bacteriophage ΦX174 and its functional implications

Abstract

The mechanism of DNA ejection, viral assembly and evolution are related to the structure of bacteriophage ΦX174. The F protein forms a T = 1 capsid whose major folding motif is the eight–stranded antiparallelβ barrel found in many other icosahedral viruses. Groups of 5 G proteins form 12 dominating spikes that enclose a hydrophilic channel containing some diffuse electron density. Each G protein is a tight β barrel with its strands running radially outwards and with a topology similar to that of the F protein. The 12 'pilot' H proteins per virion may be partially located in the putative ion channel. The small, basic J protein is associated with the DNA and is situated in an interior cleft of the F protein. Tentatively, there are three regions of partially ordered DNA structure, accounting for about 12% of the total genome.

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References

  1. 1

    Hayashi, M., Aoyama, A., Richardson, D. L. Jr & Hayashi, M. N. in The Bactehophages (The Viruses) Vol. 2 (ed. Calendar, R.) 1–71 (Plenum, New York, 1988).

    Google Scholar 

  2. 2

    Burgess, A. B. Proc. natn. Acad. Sci. U.S.A. 64, 613–617 (1969).

    ADS  CAS  Article  Google Scholar 

  3. 3

    Edgell, M. H., Hutchison, C. A. III & Sinsheimer, R. L. J. molec. Biol. 42, 547–557 (1969).

    CAS  Article  Google Scholar 

  4. 4

    Siden, E. J. & Hayashi, M. J. molec. Biol. 89, 1–16 (1974).

    CAS  Article  Google Scholar 

  5. 5

    Hall, C. E., Maclean, E. C. & Tessman, I. J. molec. Biol 1, 192–194 (1959).

    Article  Google Scholar 

  6. 6

    Thomas, W. J. & Horne, R. W. Virology 15, 1–7 (1961).

    Article  Google Scholar 

  7. 7

    Stouthamer, A. H., Daems, W. T. & Eigner, J. Virology 20, 246–250 (1963).

    CAS  Article  Google Scholar 

  8. 8

    Brown, D. T., Mackenzie, J. M. & Bayer, M. E. J. Virol. 7, 836–846 (1971).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. 9

    Incardona, N. L. & Selvidge, L. J. Virol. 11, 775–782 (1973).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. 10

    Jazwinski, S. M., Lindberg, A. A. & Kornberg, A. Virology 66, 268–282 (1975).

    CAS  Article  Google Scholar 

  11. 11

    Feige, U. & Stirm, S. Biochem. biophys. Res. Commun. 71, 566–573 (1976).

    CAS  Article  Google Scholar 

  12. 12

    Sinsheimer, R. L. Prog. Nucleic Acid Res. molec. Biol. 8, 115–169 (1968).

    CAS  Article  Google Scholar 

  13. 13

    Newbold, J. E. & Sinsheimer, R. L. J. Virol. 5, 427–431 (1970).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. 14

    Weisbeek, P. J., Van de Pol, J. H. & Van Arkel, G. A. Virology 52, 408–416 (1973).

    CAS  Article  Google Scholar 

  15. 15

    Dowell, C. E., Jansz, H. S. & Zandberg, J. Virology 114, 252–255 (1981).

    CAS  Article  Google Scholar 

  16. 16

    Newbold, J. E. & Sinsheimer, R. L. J. molec. Biol. 49, 49–66 (1970).

    CAS  Article  Google Scholar 

  17. 17

    Incardona, N. L. & Müller, U. R. J. molec. Biol. 181, 479–486 (1985).

    CAS  Article  Google Scholar 

  18. 18

    Doniger, J. & Tessman, I. Virology 39, 389–394 (1969).

    CAS  Article  Google Scholar 

  19. 19

    Incardona, N. L. J. Virol. 14, 469–478 (1974).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. 20

    Yazaki, K. J. virol. Meth. 2, 159–167 (1981).

    CAS  Article  Google Scholar 

  21. 21

    Mano, Y., Kawabe, T., Komano, T. & Yazaki, K. Agric. Biol. Chem. 46, 2041–2049 (1982).

    CAS  Google Scholar 

  22. 22

    Fujisawa, H. & Hayashi, M. J. Virol. 23, 439–442 (1977).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. 23

    Aoyama, A., Hamatake, R. K. & Hayashi, M. Proc. natn. Acad. Sci. U.S.A. 78, 7285–7289 (1981).

    ADS  CAS  Article  Google Scholar 

  24. 24

    Mukai, R., Hamatake, R. K. & Hayashi, M. Proc. natn. Acad. Sci. U.S.A. 76, 4877–4881 (1979).

    ADS  CAS  Article  Google Scholar 

  25. 25

    Liljas, L. Prog. Biophys. molec. Biol. 48, 1–36 (1986).

    CAS  Article  Google Scholar 

  26. 26

    Sanger, F. et al. Nature 265, 687–695 (1977).

    ADS  CAS  Article  Google Scholar 

  27. 27

    Shaw, D. C. et al. Nature 272, 510–515 (1978).

    ADS  CAS  Article  Google Scholar 

  28. 28

    Godson, G. N. in The Single-Stranded DNA Phages (eds Denhardt, D. T., Dressler, D. & Ray, D. S.) 103–112 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 1978).

    Google Scholar 

  29. 29

    Godson, G. N., Fiddes, J. C., Barrell, B. G. & Sanger, F. in The Single-Stranded DNA Phages (eds Denhardt, D. T., Dressier, D. & Ray, D. S.) 51–86 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 1978)

    Google Scholar 

  30. 30

    Lau, P. C. K. & Spencer, J. H. Gene 40, 273–284 (1985).

    CAS  Article  Google Scholar 

  31. 31

    Huber, R. & Bennett, W. S. Jr Biopolymers 22, 261–279 (1983).

    CAS  Article  Google Scholar 

  32. 32

    Sinsheimer, R. L. J. molec. Biol. 1, 37–42 (1959).

    CAS  Article  Google Scholar 

  33. 33

    Willingmann, P. et al. J. molec. Biol. 212, 345–350 (1990).

    CAS  Article  Google Scholar 

  34. 34

    Eigner, J., Stouthamer, A. H., van der Sluys, I. & Cohen, J. A. J. molec. Biol 6, 61–84 (1963).

    CAS  Article  Google Scholar 

  35. 35

    Weisbeek, P. J., Van de Pol, J. H. & Van Arkel, G. A. Virology 48, 456–462 (1972).

    CAS  Article  Google Scholar 

  36. 36

    Sanger, F. et al. J. molec. Biol. 125, 225–246 (1978).

    CAS  Article  Google Scholar 

  37. 37

    Jones, T. A. J. appl. Crystallogr. 11, 268–272 (1978).

    CAS  Article  Google Scholar 

  38. 38

    Caspar, D. L. D. & Klug, A. Cold Spring Harb. Symp. quant. Biol. 27, 1–24 (1962).

    CAS  Article  Google Scholar 

  39. 39

    Rossmann, M. G. & Johnson, J. E. A. Rev. Biochem. 58, 533–573 (1989).

    CAS  Article  Google Scholar 

  40. 40

    Rossmann, M. G. et al. Nature 317, 145–153 (1985).

    ADS  CAS  Article  Google Scholar 

  41. 41

    Tsao, J. et al. Science 251, 1456–1464 (1991).

    ADS  CAS  Article  Google Scholar 

  42. 42

    Harrison, S. C., Olson, A. J., Schutt, C. E., Winkler, F. K. & Bricogne, G. Nature 276, 368–373 (1978).

    ADS  CAS  Article  Google Scholar 

  43. 43

    Abad-Zapatero, C. et al. Nature 286, 33–39 (1980).

    ADS  CAS  Article  Google Scholar 

  44. 44

    Liljas, L. et al. J. molec. Biol. 159, 93–108 (1982).

    CAS  Article  Google Scholar 

  45. 45

    Cohen, S. S. & McCormick, F. P. Adv. Virus Res. 24, 331–387 (1979).

    CAS  Article  Google Scholar 

  46. 46

    Benevides, J. M., Stow, P. L., Ilag, L. L., Incardona, N. L. & Thomas, G. J. Jr Biochemistry 30, 4855–4863 (1991).

    CAS  Article  Google Scholar 

  47. 47

    Jazwinski, S. M., Marco, R. & Kornberg, A. Virology 66, 294–305 (1975).

    CAS  Article  Google Scholar 

  48. 48

    Chen, Z. et al. Science 245, 154–159 (1989).

    ADS  CAS  Article  Google Scholar 

  49. 49

    Saenger, W. in Principles of Nucleic Acid Structure (ed. Cantor, C. R.) 51–104 (Springer, New York, 1984).

    Google Scholar 

  50. 50

    Chapman, M. S., Minor, J., Rossmann, M. G., Diana, G. D. & Andries, K. J. molec. Biol. 217, 455–463 (1991).

    CAS  Article  Google Scholar 

  51. 51

    Argos, P. et al. Biochemistry 18, 5698–5703 (1979).

    CAS  Article  Google Scholar 

  52. 52

    Rossmann, M. G., Moras, D. & Olsen, K. W. Nature 250, 194–199 (1974).

    ADS  CAS  Article  Google Scholar 

  53. 53

    Matthews, B. W. & Rossmann, M. G. Meth. Enzym. 115, 397–420 (1985).

    CAS  Article  Google Scholar 

  54. 54

    Bloomer, A. C., Champness, J. N., Bricogne, G., Staden, R. & Klug, A. Nature 276, 362–368 (1978).

    ADS  CAS  Article  Google Scholar 

  55. 55

    Namba, K. & Stubbs, G. Science 231, 1401–1406 (1986).

    ADS  CAS  Article  Google Scholar 

  56. 56

    Valegård, K., Liljas, L., Fridborg, K. & Unge, T. Nature 345, 36–41 (1990).

    ADS  Article  Google Scholar 

  57. 57

    Choi, H. K. et al. Nature 354, 37–43 (1991).

    ADS  CAS  Article  Google Scholar 

  58. 58

    Ladenstein, R. et al. J. molec. Biol. 203, 1045–1070 (1988).

    CAS  Article  Google Scholar 

  59. 59

    Smith, T. J. et al. Science 233, 1286–1293 (1986).

    ADS  CAS  Article  Google Scholar 

  60. 60

    Rossmann, M. G. Proc. natn. Acad. Sci. U.S.A. 85, 4625–4627 (1988).

    ADS  CAS  Article  Google Scholar 

  61. 61

    Rossmann, M. G. & Blow, D. M. Acta crystallogr. 15, 24–31 (1962).

    CAS  Article  Google Scholar 

  62. 62

    Tong, L. & Rossmann, M. G. Acta crystallogr. A46, 783–792 (1990).

    CAS  Article  Google Scholar 

  63. 63

    Stauffacher, C. V. et al. in Crystallography in Molecular Biology (eds Moras, D., Drenth, J., Strandberg, B., Suck, D. & Wilson, K.) 293–308 (Plenum, New York, 1987).

    Google Scholar 

  64. 64

    Rossmann, M. G. Acta crystallogr. A46, 73–82 (1990).

    CAS  Article  Google Scholar 

  65. 65

    Rossmann, M. G. et al. J. appl. Crystallogr. (in the press).

  66. 66

    Smith, T. J. J. appl. Crystallogr. 23, 141–142 (1990).

    Article  Google Scholar 

  67. 67

    Gibson, T. J. & Argos, P. J. molec. Biol. 212, 7–9 (1990).

    ADS  CAS  Article  Google Scholar 

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McKenna, R., Xia, D., Willingmann, P. et al. Atomic structure of single-stranded DNA bacteriophage ΦX174 and its functional implications. Nature 355, 137–143 (1992). https://doi.org/10.1038/355137a0

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