Replication of øX174 DNA Reconstituted with Purified Enzymes

  • Joseph Shlomai
  • Ken-Ichi Arai
  • Robert Low
  • Joan Kobori
  • Naoko Arai
  • Seichi Yasuda
  • Ulrich Hubscher
  • Leroy Bertsch
  • Arthur Kornberg
Part of the Developments in Molecular Virology book series (DMVI, volume 2)

Summary

Conversion of øX174 DNA to its duplex replicative form (SS→RF) is initiated by assembly of a multiprotein unit, the primosome, at a unique site on the chromosome, recognized by prepriming protein n’. At or near this site, the unique origin of øX complementary strand replication is located. The primosome and the prepriming intermediate that precedes it contain one molecule each of tightly bound dnaB protein, protein n’, protein n, protein i and undetermined stoichiometric quantities of dnaC protein, primase and protein n”. The role of dnaB protein as a “replication promotor” is to “engineer” the DNA structure to generate a signal for primase action. Processive translocation of the primosome from its assembly site, at or near the unique origin of replication, is in the 5’→3’ direction of the DNA template, and is catalyzed by protein n’ utilizing the energy of ATP (dATP) hydrolysis. Priming of synthesis of complementary strands on the nascent viral strand in the multiplication of RF (RF→RF) utilizes the same primosome which is almost completely conserved. The primosome associated with parental viral DNA in the initial SS→RF stage of øX174 DNA replication may function repeatedly in the initiation of complementary strands at the subsequent stage of RF→RF multiplication. A nucleoprotein complex functioning in RF replication has been isolated, which combines the priming, helicase, and chain elongation functions in a “replisome”-like structure at the replication fork. Its possible role in coupling continuous DNA synthesis of the leading DNA strand and discontinuous synthesis on the lagging strand is discussed.

Keywords

Hydrolysis Migration Filtration Bromide Polypeptide 

Abbreviations

øX

bacteriophage øX174

SS DNA

single-stranded DNA

RF DNA

duplex replicative form of øX174 DNA

SSB

single-stranded DNA binding protein

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Sinsheimer, R.L. Prog. Nucleic Acid Res. Mol. Biol. 8, 115–169, 1968.PubMedCrossRefGoogle Scholar
  2. 2.
    Denhardt, D.T. Comp. Virol. 7, 1–104, 1977.Google Scholar
  3. 3.
    Denhardt, D.T. CRC Crit. Rev. Microbiol. 4, 161–223, 1975.PubMedCrossRefGoogle Scholar
  4. 4.
    Tessman, E.S. J. Mol. Biol. 17, 218–236, 1966.PubMedCrossRefGoogle Scholar
  5. 5.
    Denhardt, D.T., Iwaya, M., and Larison, L.L. Virology 49, 486–496, 1972.PubMedCrossRefGoogle Scholar
  6. 6.
    Fujisawa, H., and Hayashi, M. J. Virol. 19, 416–424, 1976.Google Scholar
  7. 7.
    Tessman, E.S., and Peterson, P.K. J. Virol. 20, 400–412, 1976.PubMedGoogle Scholar
  8. 8.
    McHenry, C., and Kornberg, A. J. Biol. Chem. 252, 6478–6484, 1977.PubMedGoogle Scholar
  9. 9.
    Meyer, R.R., Shlomai, J.; Kobori, J., Bates, D.L., Rowen, L., McMacken, R., Ueda, K., and Kornberg, A. Cold Spring Harbor Symp. Quant. Biol. 43, 289–293, 1978.Google Scholar
  10. 10.
    Kornberg, A. Cold Spring Harbor Symp. Quant. Biol. 43, 1–9, 1978.Google Scholar
  11. 11.
    Wickner, S. Ann. Rev. Biochem. 47, 1163–1191, 1978.PubMedCrossRefGoogle Scholar
  12. 12.
    Kornberg, A. in RNA Polymerase, eds. Losick, R., and Chamberlin, M. ( Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y. ) pp. 331–352, 1976.Google Scholar
  13. 13.
    Geider, K. and Kornberg, A. J. Biol. Chem. 249, 3999–4005, 1974.PubMedGoogle Scholar
  14. 14.
    McMacken R., and Kornberg, A. J. Biol. Chem. 253, 3313–3319, 1978.PubMedGoogle Scholar
  15. 15.
    Bouche, J.-P., Zechel, K., and Kornberg, A. J. Biol. Chem. 250, 5995–6001, 1975.PubMedGoogle Scholar
  16. 16.
    Zechel, K., Bouche, J.-P., and Kornberg, A. J. Biol. Chem. 250, 4684–4689, 1975.PubMedGoogle Scholar
  17. 17.
    Weiner, J.H., McMacken, R., and Kornberg, A. Proc. Natl. Acad. Sci. U.S.A. 73, 752–756, 1976.PubMedCrossRefGoogle Scholar
  18. 18.
    McMacken, R., Ueda, K., and Kornberg, A. Proc. Natl. Acad. Sci. U.S.A. 74, 4190–4194, 1977.PubMedCrossRefGoogle Scholar
  19. 19.
    Uhlin, B.E., Molin, S., Gustafsson, P., and Nordstrom, K. Gene 6, 91–106, 1979.PubMedCrossRefGoogle Scholar
  20. 20.
    Arai, K., Yasuda, S., and Kornberg, A. J. Biol. Chem. 256, 5247–5252, 1981.PubMedGoogle Scholar
  21. 21.
    Kobori, J., and Kornberg, A. J. Biol. Chem., in press, 1982.Google Scholar
  22. 22.
    Arai, K., McMacken, R., Yasuda, S., and Kornberg, A. J. Biol. Chem. 256, 5247–5252, 1981.PubMedGoogle Scholar
  23. 23.
    Low, R., Shlomai, J., and Kornberg, A. J. Biol. Chem. 257, 6242–6250, 1982.PubMedGoogle Scholar
  24. 24.
    Shlomai, J., and Kornberg, A. J. Biol. Chem. 255, 6789–6793, 1980.PubMedGoogle Scholar
  25. 25.
    Arai, K., and Kornberg, A. Proc. Natl. Acad. Sci. U.S.A. 76, 4308–4312, 1979.PubMedCrossRefGoogle Scholar
  26. 26.
    Arai, K., Low, R., and Kornberg, A. Proc. Natl. Acad. Sci. U.S.A. 78, 707–711, 1981.PubMedCrossRefGoogle Scholar
  27. 27.
    Arai, K., and Kornberg, A. J. Biol. Chem. 256, 5267–5272, 1980.Google Scholar
  28. 28.
    Geider, K., Beck, E., and Schaller, H. Proc. Natl. Acad. Sci. U.S.A. 76, 645–649, 1978.CrossRefGoogle Scholar
  29. 29.
    Bouche, J.-P., Rowen, L., and Kornberg, A. J. Biol. Chem. 253, 765–769, 1978.PubMedGoogle Scholar
  30. 30.
    Hourcade, D., and Dressier, D. Proc. Natl. Acad. Sci. U.S.A. 75, 1652–1656, 1978.PubMedCrossRefGoogle Scholar
  31. 31.
    Gross, J.D. Curr. Top. Microbiol. Immunol. 57, 39–74, 1972.PubMedGoogle Scholar
  32. 32.
    Zyskind, J.W., and Smith, D.W. J. Bacteriol. 129, 1476–1486, 1977.PubMedGoogle Scholar
  33. 33.
    Wechsler, J.A., and Gross, J.D. Mol. Gen. Genet. 113, 273–284, 1971.PubMedCrossRefGoogle Scholar
  34. 34.
    Schekman, R., Wickner, W., Westergaard, O., Brutlag, D., Geider, K., Bertsch, L.L., and Kornberg, A. Proc. Natl. Acad. Sci. U.S.A. 61, 2691–2695, 1972.CrossRefGoogle Scholar
  35. 35.
    Wickner, R.B., Wright, M., Wickner, S., and Hurwitz, J. Proc. Natl. Acad. Sci. U.S.A. 69, 3233–3237, 1972.CrossRefGoogle Scholar
  36. 36.
    Eisenberg, S., Scott, J., and Kornberg, A. Proc. Natl. Acad. Sci. U.S.A. 73, 3151–3155, 1976.PubMedCrossRefGoogle Scholar
  37. 37.
    Sumida-Yasumoto, C., Ikeda, J.-E., Benz, E., Marians, K.J., Vicuna, R., Surgue, S., Ziprusky S.L., and Hurwitz, J. Cold Spring Harbor Symp. Quant. Biol. 43, 311–329, 1978.Google Scholar
  38. 38.
    Arai, K., Arai, N., Shlomai, J., and Kornberg, A. Proc. Natl. Acad. Sci. U.S.A. 77, 3322–3326, 1980.PubMedCrossRefGoogle Scholar
  39. 39.
    Tomizawa, J., and Selzer, G. Annu. Rev. Biochem. 48, 999–1034, 1979.PubMedCrossRefGoogle Scholar
  40. 40.
    Staudenbauer, W.L. Mol. Gen. Genet. 162, 243–249, 1978.PubMedCrossRefGoogle Scholar
  41. 41.
    Conrad, S.E., and Campbell, J.L. Nucleic Acid Res. 6, 3289–3304, 1979.PubMedCrossRefGoogle Scholar
  42. 42.
    Wright, M., Wickner, S., and Hurwitz, J. Proc. Natl. Acad. Sci. U.S.A. 70, 3120–3124, 1973.PubMedCrossRefGoogle Scholar
  43. 43.
    Ueda, K., McMacken, R., and Kornberg, A. J. Biol. Chem. 253, 261–269, 1978.PubMedGoogle Scholar
  44. 44.
    Reha-Krantz, L.J., and Hurwitz, J. J. Biol. Chem. 253, 4043–4050, 1978.PubMedGoogle Scholar
  45. 45.
    Reha-Krantz, L.J., and Hurwitz, J. J. Biol. Chem. 753, 4051–4057, 1978.Google Scholar
  46. 46.
    Lanka, E., Edelbluth, C., Schlicht, M., and Schuster, H. J. Biol. Chem. 253, 5847–5851, 1978.PubMedGoogle Scholar
  47. 47.
    Arai, K., and Kornberg, A. J. Biol. Chem. 256, 5260–5266, 1981.PubMedGoogle Scholar
  48. 48.
    Masukata, H., and Ogawa, T. Mol. Gen. Genet. 180, 531–538, 1980.PubMedCrossRefGoogle Scholar
  49. 49.
    Arai, K., Low, R., Kobori, J., Shlomai, J., and Kornberg, A. J. Biol. Chem. 256, 5273–5280, 1981.PubMedGoogle Scholar
  50. 50.
    Sims, J., and Dressier, D. Proc. Natl. Acad. Sci. U.S.A. 3094–3098, 1972.Google Scholar
  51. 51.
    Martin, D.M., and Godson, G.N. J. Mol. Biol. 117, 321–325, 1977.PubMedCrossRefGoogle Scholar
  52. 52.
    Schekman, R., Weiner, J.H., Weiner, A., and Kornberg, A. J. Biol. Chem. 250, 5859–5865, 1975.PubMedGoogle Scholar
  53. 53.
    Shlomai, J., and Kornberg, A. J. Biol. Chem. 255, 6794–6798, 1980.PubMedGoogle Scholar
  54. 54.
    Shlomai, J., and Kornberg, A. Proc. Natl. Acad. Sci. U.S.A. 77, 799–803, 1980.PubMedCrossRefGoogle Scholar
  55. 55.
    Fiddes, J.C., Barrell, B.G., and Godson, G.N. Proc. Natl. Acad. Sci. U.S.A. 75, 1081–1085.Google Scholar
  56. 56.
    Tabak, H.F., Griffith, J., Geider, K., Schaller, H., and Kornberg, A. J. Biol. Chem. 249, 3049–3054, 1974.PubMedGoogle Scholar
  57. 57.
    Blakesley, R.W., Dogson, J.B., Nes, I.F., and Wells, R.D. J. Biol. Chem. 252, 7300–7306, 1977.PubMedGoogle Scholar
  58. 58.
    Arai, K., and Kornberg, A. Proc. Natl. Acad. Sci. U.S.A. 78, 69–73, 1981.PubMedCrossRefGoogle Scholar
  59. 59.
    Godson, G.N., Barell, B.G., Staden, R., and Fiddes, J.C. Nature 276, 236–247, 1978.PubMedCrossRefGoogle Scholar
  60. 60.
    Widkner, S. and Hurwitz, J. Proc. Natl. Acad. Sci. U.S.A. 72, 921–925, 1975.CrossRefGoogle Scholar
  61. 61.
    Eisenberg, S., Scott, J.F., and Kornberg, A. Proc. Natl. Acad. Sci. U.S.A. 73, 1594–1597, 1976.PubMedCrossRefGoogle Scholar
  62. 62.
    Sumida-Yasumoto, C., Yudelevich, A., and Hurwitz, J. Proc. Natl. Acad. Sci. U.S.A. 73, 1887–1891, 1976.PubMedCrossRefGoogle Scholar
  63. 63.
    Eisenberg, S., Scott, J.F., and Kornberg, A. Proc. Natl. Acad. Sci. U.S.A. 23, 3151–3155, 1976.CrossRefGoogle Scholar
  64. 64.
    Eisenberg, S., Griffith, J., and Kornberg, A. Proc. Natl. Acad. Sci. U.S.A. 74, 3198–3202, 1977.PubMedCrossRefGoogle Scholar
  65. 65.
    Henry, T.J., and Knippers, R. Proc. Natl. Acad. Sci. U.S.A. 71, 1549–1553, 1974.PubMedCrossRefGoogle Scholar
  66. 66.
    Ikeda, J., Yudelevich, A., and Hurwitz, J. Proc. Natl. Acad. Sci. U.S.A. 73, 2669–2673, 1976.PubMedCrossRefGoogle Scholar
  67. 67.
    Longeveld, S.A., von Mansfeld, A.D.M., Baas, P.D., Jansz, H.S., von Arkel, G.A., and Weisbeek, P.J. Nature (London) 271, 417–420, 1978.CrossRefGoogle Scholar
  68. 68.
    Eisenberg, S., Scott, J.F., and Kornberg, A. Cold Spring Harbor Sym. Quant. Biol. 43, 295–302, 1978.Google Scholar
  69. 69.
    Eisenberg, S., and Kornberg, A. J. Biol. Chem. 254, 5328–5332, 1979.PubMedGoogle Scholar
  70. 70.
    Arai, N., Arai, K., and Kornberg, A. J. Biol. Chem. 256, 5287–5293, 1981.PubMedGoogle Scholar
  71. 71.
    Arai, N., and Kornberg, A. J. Biol. Chem. 256, 5294–5298, 1981.PubMedGoogle Scholar
  72. 72.
    Scott, J.F., Eisenberg, S., Bertsch, L.L., and Kornberg, A. Proc. Natl. Acad. Sci. U.S.A. 74, 193–197, 1977.PubMedCrossRefGoogle Scholar
  73. 73.
    Kornberg, A., Scott, J.F., and Bertsch, L.L. J. Biol. Chem. 253, 3298–3304, 1978.PubMedGoogle Scholar
  74. 74.
    Shlomai, J., Polder, L., Arai, K., and Kornberg, A. J. Biol. Chem. 256, 5233–5238, 1981.PubMedGoogle Scholar
  75. 75.
    Eisenberg, S., and Denhardt, D.T. Proc. Natl. Acad. Sci. U.S.A. 71, 984–988, 1974.PubMedCrossRefGoogle Scholar
  76. 76.
    Keegstra, W., Baas, P.D., and Jansz, H.S. J. Mol. Biol. 135, 69–89, 1979.PubMedCrossRefGoogle Scholar
  77. 77.
    Mathes, M., and Denhardt, D.T. J. Mol. Biol. 136, 45–63, 1980.CrossRefGoogle Scholar
  78. 78.
    Machida, Y., Okazaki, T., and Okazaki, R. Proc. Tatl. Acad. Sci. U.S.A. 74, 2776–2779, 1977.CrossRefGoogle Scholar
  79. 79.
    Baas, P.D., Teetstra, W.R., and Jansz, H.S. J. Mol. Biol. 125, 167–185, 1978.PubMedCrossRefGoogle Scholar
  80. 80.
    Low, R.L., Arai, K., and Kornberg, A. Proc. Natl. Acad. Sci. U.S.A. 78, 1436–1440, 1981.PubMedCrossRefGoogle Scholar
  81. 81.
    Yarsus, M., and Sinsheimer, R. J. Virol. 1, 135–144, 1967.CrossRefGoogle Scholar
  82. 82.
    Arai, N., Polder, L., Arai, K., and Kornberg, A. J. Biol. Chem. 256, 5239–5246, 1981.PubMedGoogle Scholar
  83. 83.
    Kolodner, R., and Richardson, C.C. Proc. Natl. Acad. Sci. U.S.A. 74, 1525–1529, 1977.PubMedCrossRefGoogle Scholar
  84. 84.
    Scherzinger, E., Lanka, E., Morelli, G., Seiffert, D., and Yuki, A. Eur. J. Biochem. 72, 543–558, 1977.PubMedCrossRefGoogle Scholar
  85. 85.
    Liu, C.C., Burke, R.L., Hibner, U., Barry, J., and Alberts, B. Cold Spring Harbor Symp. Quant. Biol. 43, 469–487, 1978.Google Scholar
  86. 86.
    Kornberg, A. DNA Replication, W.H. Freeman and Co., San Francisco, 1980.Google Scholar

Copyright information

© Martinus Nijhoff Publishing, Boston 1983

Authors and Affiliations

  • Joseph Shlomai
    • 1
  • Ken-Ichi Arai
  • Robert Low
  • Joan Kobori
  • Naoko Arai
  • Seichi Yasuda
  • Ulrich Hubscher
  • Leroy Bertsch
  • Arthur Kornberg
  1. 1.Department of ProtozoologyThe Hebrew University-Hadassah Medical SchoolJerusalemIsrael

Personalised recommendations