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Evolution of Viral DNA-Dependent DNA Polymerases

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Abstract

DNA viruses as their host cells require a DNA-dependent DNA polymerase (Pol) to faithfully replicate their genomic information. Large eukaryotic DNA viruses as well as bacterial viruses encode a specific Pol equipped with a proofreading 3′-5′-exonuclease, and other replication proteins. All known viral Pol belong to family A and family B Pol. Common to all viral Pol is the conservation of the 3′-5′-exonuclease domain manifested by the three sequence motifs Exo I, Exo II, and Exo III. The polymerase domain of family A and B Pol is clearly distinguishable. Family A Pol share 9 distinct consensus sequences, only two of them are convincingly homologous to sequence motif B of family B Pol. The putative sequence motifs A, B, and C of the polymerase domain are located near the C-terminus in family A Pol and more central in family B Pol. Thus, family A Pol show a significant greater spacing between the Exo III motif and the Pol motif A that is especially extended in the case of the mitochondrial Pol γ. From each host and virus family whenever possible the consensus sequences of two distantly related polymerase species were aligned for assessment of phylogenetic trees, using both maximum parsimony and distance methods, and evaluated by bootstrap analysis. Three alternative methods yielded trees with identical major groupings. A subdivision of viral family B Pol was achieved resulting in a branch with Pol carrying out a protein-primed mechanism of DNA replication, including adenoviruses, bacteriophages and linear plasmids of plant and fungal origin. Archaebacterial Pol and cellular Pol ∈ were consistently found at the base of this branch. Another major branch comprised alpha- and delta-like viral Pol from mammalian herpesviruses, fish lymphocystis disease virus, insect ascovirus, and chlorella virus. Due to a lower branch integrity Pol of T-even bacteriophages, poxviruses, African swine fever virus, fish herpesvirus, and baculoviruses were not clearly resolved and placed in alternate groupings. A composite and rooted tree of family A and B Pol shows that viral Pol with a protein-priming requirement represent the oldest viral Pol species suggesting that the protein-primed mechanism is one of the earliest modes of viral DNA replication.

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References

  1. Ito J. and Braithwaite D.K., Nucleic Acids Res 19, 4045-4057, 1991.

    Google Scholar 

  2. Braithwaite D.K. and Ito J., Nucleic Acids Res 21, 787-802, 1993.

    Google Scholar 

  3. Jung G., Leavitt M.C., Hsieh J.-C., and Ito J., Proc Natl Acad Sci USA 84, 8287-8291, 1987.

    Google Scholar 

  4. Bernad A., Zaballos A., Salas M., and Blanco L., EMBO J 6, 4219-4225, 1987.

    Google Scholar 

  5. Delaru M., Poch O., Tordo N., Moras D., and Argos P., Protein Eng 3, 461-467, 1990.

    Google Scholar 

  6. Zhu W. and Ito J., Nucleic Acids Res 22, 5177-5183, 1994.

    Google Scholar 

  7. Boulet A., Simon M., Faye G., Bauer G.A., and Burgers P.M.J., EMBO J 8, 1849-1854, 1989.

    Google Scholar 

  8. Knopf K.W. and Strick R., in Becker Y. and Darai G. (eds), Frontiers of Virology, Vol 3. Springer Verlag, Berlin, 1994, pp. 87-135.

    Google Scholar 

  9. Cullmann G., Hindges R., Berchtold M.W., and Hübscher U., Gene 134, 191-200, 1993.

    Google Scholar 

  10. Wang T.S.-F., Annu Rev Biochem 60, 513-552, 1991.

    Google Scholar 

  11. Joyce C.M. and Steitz T. A., Annu Rev Biochem 63, 777-822, 1994.

    Google Scholar 

  12. Bernad A., Blanco L., Lázaro J.M., Martin G., and Salas M., Cell, 59, 219-228, 1989.

    Google Scholar 

  13. Blanco L., Bernad A., and Salas M., Gene 112, 139-144, 1992.

    Google Scholar 

  14. Kühn F.J.P. and Knopf C.W., J Biol Chem 271, 29245-29254, 1996.

    Google Scholar 

  15. Simon M., Giot L., and Faye G., EMBO J 10, 2165-2170, 1991.

    Google Scholar 

  16. Freemont P.S., Ollis D.L., Steitz T.A., and Joyce C.M., Proteins 1, 66-73, 1986.

    Google Scholar 

  17. Ruscitti T., Polayes D.A., Karu A.E., and Linn S., J Biol Chem 267, 16806-16811, 1992.

    Google Scholar 

  18. Soengas M.S., Esteban J.A., Lázaro J.M., Bernard A., Blasco M.A., Salas M., and Blanco L., EMBO J 11, 4227-4237, 1992.

    Google Scholar 

  19. Reha-Krantz L.J. and Nonay R.L., J Biol Chem 260, 27100- 27108, 1993.

    Google Scholar 

  20. Stocki S.A., Nonay R.L., and Reha-Krantz L.J., J Mol Biol 254, 15-28, 1995.

    Google Scholar 

  21. Gibbs J.S., Weisshart K., Digard P., De Bruyn-Kops A., Knipe D.M., and Coen D.M., Mol Cell Biol 11, 4786-4795, 1991.

    Google Scholar 

  22. Wang Y., Woodward S., and Hall J.D., J. Virol. 66, 1814-1816, 1992.

    Google Scholar 

  23. McGeoch D.J. and Cook S., J Mol Biol 238, 9-22, 1994.

    Google Scholar 

  24. McGeoch D.J., Cook S., Dolan A., Jamieson F.E., and Telford E.A.R., J Mol Biol 247, 443-458, 1995.

    Google Scholar 

  25. Doolittle R.F., Anderson K.L., and Feng D., In The Hierarchy of Life (Fernholm B., Bremer K., and Jornvall H., eds.), Elsevier Science Publisher, Amsterdam, 73-85, 1989.

    Google Scholar 

  26. Felsenstein, J., PHYLIP (Phylogeny Inference Package) Version 3.572c, University of Washington, 1995.

  27. Higgins D.G., Bleasby A.J., and Fuchs R., Comput Appl Biosci 8, 189-191, 1992.

    Google Scholar 

  28. Thompson J.D., Higgins D.G., and Gibson T.J., Nucleic Acids Res 22, 4673-4680, 1994.

    Google Scholar 

  29. Saitou N. and Nei M., Mol Biol Evol 4, 406-425, 1987.

    Google Scholar 

  30. Schwartz R.M. and Dayhoff M.O., In Atlas of Protein Sequence and Structure (Dayhoff M.O., ed.) National Biomedical Research Foundation, Washington D.C. Vol. 5,Supplement 3, 353-358, 1978.

    Google Scholar 

  31. Felsenstein J., Annu Rev Genet 22, 521-565, 1988.

    Google Scholar 

  32. Delius H. and Hofmann, B., Curr Top Microbiol Immunol 186, 13-31, 1994.

    Google Scholar 

  33. Argos P., Tucker A.D., and Philipson L., Virology 149, 208- 216, 1986.

    Google Scholar 

  34. Wong S.W., Wahl A.F., Yuan P.-M., Arai N., Pearson B.E., Arai K., Korn D., Hunkapiller M.W., and Wang T.S.-F., EMBO J 7, 37-47, 1988.

    Google Scholar 

  35. Hwang C.B., Ruffner K.L., and Coen D.M., J Virol 66, 1774- 1776, 1992.

    Google Scholar 

  36. Freemont P.S., Friedman J.M., Beese L.S., Sanderson M.R., and Steitz T.A., Proc Natl Acad Sci USA 85, 8924-8928, 1988.

    Google Scholar 

  37. Derbyshire V., Freemont P.S., Sanderson M.R., Beese L.S., Friedman J.M., Joyce, C.M., and Steitz T.A., Science 240, 199- 201, 1988

    Google Scholar 

  38. Derbyshire V., Grindley N.D.F., and Joyce C.M., EMBO J 10, 17-24, 1991.

    Google Scholar 

  39. Blanco L., Bernad A., Blasco M.A., and Salas M., Gene (Amst), 100, 27-38, 1991.

    Google Scholar 

  40. Gibbs J.S., Chiou H., Bastow K., Cheng Y.C., and Coen D.M., Proc Natl Acad Sci USA 85, 6672-6676, 1988.

    Google Scholar 

  41. Copeland W.C. and Wang T.S.-F., J Biol Chem 268, 11028- 11040, 1993.

    Google Scholar 

  42. Copeland W.C. and Wang T.S.-F., J Biol Chem 268, 11041- 11049, 1993.

    Google Scholar 

  43. Eom S.H., Wang J., and Steitz, T.A., Nature 382, 278-281, 1996.

    Google Scholar 

  44. Hall J.D., Orth K.L., and Claus-Walker D., J Virol 70, 4816- 4818, 1996.

    Google Scholar 

  45. Polesky A.H., Dahlberg M.E., Benkovic S.J., Grindley N.D.F., and Joyce C.M., J Biol Chem 267, 8417-8428, 1992.

    Google Scholar 

  46. Blasco, M.A., Bernad A., Blanco L., and Salas M., J Biol Chem 266, 7904-7909, 1991.

    Google Scholar 

  47. Dorsky D.I. and Crumpacke C.S., J Virol 64, 1394-1397, 1990.

    Google Scholar 

  48. Marcy A.I., Hwang C.B.C., Ruffner K.L., and Coen D.M., J Virol 64, 5883-5890, 1990.

    Google Scholar 

  49. Dong Q., Copeland, W.C., and Wang T.S.-F., J Biol Chem 268, 24163-24174, 1993.

    Google Scholar 

  50. Blasco M.A., Lazaro J.M., Bernad A., Blanco L., and Salas M., J Biol Chem 267, 19427-19434, 1992.

    Google Scholar 

  51. Blasco M.A., Lazaro J.M., Blanco L., and Salas M., J Biol Chem 268, 16763-16770, 1993.

    Google Scholar 

  52. Lawyer F.C., Stoffel S., Saik R.K., Myambo K., Drummond R., and Gelfand D.H., J Biol Chem 264, 6427-6437, 1989.

    Google Scholar 

  53. Pellock B.J., Lu A., Meagher R.B., Weise M.J., and Miller L.K., Virology 216, 146-157, 1996.

    Google Scholar 

  54. Davison A.J., Virology 186, 9-14, 1992.

    Google Scholar 

  55. Bernard J. and Mercier A., Arch Virol 132, 437-442, 1993.

    Google Scholar 

  56. Woese C.R. and Fox G.E., Proc Natl Acad Sci USA 74, 5088- 5090, 1977.

    Google Scholar 

  57. Woese C.R., Microbiol Rev 51, 221-271, 1987.

    Google Scholar 

  58. Tidona, C.A. and Darai, G., Virology 230, 207-216, 1997.

    Google Scholar 

Download references

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  1. Forschungsschwerpunkt Genomforschung und Bioinformatik, Deutsches Krebsforschungszentrum, Heidelberg, FRG; E-Mail

    Charles W. Knopf

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Knopf, C.W. Evolution of Viral DNA-Dependent DNA Polymerases. Virus Genes 16, 47–58 (1998). https://doi.org/10.1023/A:1007997609122

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