The Mechanism of Adenovirus DNA Replication and the Characterization of Replication Proteins

  • John S. Sussenbach
  • Peter C. van der Vliet
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 109)

Abstract

The replication of the genome of human adenoviruses in permissive host cells is a highly efficient process. During the infection cycle a total amount of viral DNA is synthesized comparable to the entire chromosomal DNA content of the infected cell. In order to unravel the mechanism of adenovirus DNA replication this process has been studied in a number of experimental systems.

Keywords

Electrophoresis Serine Dodecyl Pyrimidine Nucleoside 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ariga H, Klein H, Levine A J, Horwitz MS (1980) A cleavage product of the adenoviral DNA binding protein is active in DNA replication in vitro. Virology 101: 307–310PubMedCrossRefGoogle Scholar
  2. Babich A, Nevins JR (1981) The stability of early adenovirus mRNA is controlled by the viral 72-kD binding protein. Cell 26: 371–379PubMedCrossRefGoogle Scholar
  3. Berger NA, Kauff RA, Sikorsky GW (1978) ATP-independent DNA synthesis in vaccinia-infected L cells. Biochim Biophys Acta 520: 531–538PubMedGoogle Scholar
  4. Bodnar JW, Pearson GD (1980) Kinetics of adenovirus DNA replication. II Initiation of adenovirus DNA replication. Virology 105: 357–370PubMedCrossRefGoogle Scholar
  5. Bos JC, Polder LJ, Bernards R, Schrier PI, van den Elsen PJ, van der Eb AJ, van Ormondt H (1981) The 2.2 kB Elb mRNA of human Ad12 and Ad5 codes for two tumor antigens starting at different AVG triplets. Cell 27: 121–131PubMedCrossRefGoogle Scholar
  6. Byrd PJ, Chia W, Rigby PWJ, Gallimore PH (1982) Cloning of DNA fragments from the left end of the adenovirus type 12 genome: transformation by cloned early region I. J Gen Virol 60: 279–293PubMedCrossRefGoogle Scholar
  7. Carter TH, Blanton RA (1978) Possible role of the 72000 dalton DNA binding protein in regulation of adenovirus type 5 early gene expression. J Virol 25: 664–674PubMedGoogle Scholar
  8. Carter TH, Ginsberg HS (1976) Viral transcription in KB cells infected by temperature-sensitive early mutants of adenovirus type 5. J Virol 18: 156–166PubMedGoogle Scholar
  9. Challberg MD, Kelly TJ (1979a) Adenovirus DNA replication in vitro. Proc Natl Acad Sci USA 76: 655–659PubMedCrossRefGoogle Scholar
  10. Challberg MD, Kelly TJ (1979b) Adenovirus DNA replication in vitro: origin and direction of daughter strand synthesis. J Mol Biol 135: 999–1012PubMedCrossRefGoogle Scholar
  11. Challberg MD, Kelly TJ (1981) Processing of the adenovirus terminal protein. J Virol 38: 272–277PubMedGoogle Scholar
  12. Challberg MD, Desiderio SV, Kelly TJ (1980) Adenovirus DNA replication in vitro: characterization of a protein covalently linked to nascent DNA strands. Proc Natl Acad Sci USA 77: 5105–5109PubMedCrossRefGoogle Scholar
  13. Challberg MD, Ostrove JM, Kelly TJ (1982) Initiation of adenovirus DNA replication: detection of covalent complexes between nucleotide and the 80 kD terminal protein. J Virol 41: 265–270PubMedGoogle Scholar
  14. Chen S, Zubay G, Ginsberg HS (1980) The replication pattern of adenovirus DNA in vivo reproduced in vitro. Eur J Biochem 104: 587–594PubMedCrossRefGoogle Scholar
  15. Chou PY, Fasman GD (1978) Prediction of the secondary structure of proteins from their amino acid sequence. Adv Enzymol 47: 45–148PubMedGoogle Scholar
  16. Conaway RC, Lehman IR (1982) Synthesis by the DNA primase of Drosophila Melanogaster of a primer with a unique chain length. Proc Natl Acad Sci USA 79: 4584–4588Google Scholar
  17. Coombs DH, Robinson AJ, Bodnar JW, James CJ, Pearson GD (1978) Detection of DNA- protein complexes: the adenovirus DNA-terminal protein and HeLa DNA protein complexes. Cold Spring Harbor Symp Quant Biol 43: 741–753Google Scholar
  18. Daniell E (1976) Genome structure of incomplete particles of adenovirus. J Virol 19: 685–708PubMedGoogle Scholar
  19. De Jong PJ, Kwant MM, van Driel W, Jansz HS, van der Vliet (1983) The ATP requirements of adenovirus type 5 DNA replication and cellular DNA replication. Virology 124: 45–58PubMedCrossRefGoogle Scholar
  20. Desiderio SV, Kelly TJ (1981) Structure of the linkage between adenovirus DNA and the 55000 molecular weight terminal protein. J Mol Biol 145: 319–337PubMedCrossRefGoogle Scholar
  21. Friedfeld BR, Krevolin MD, Horwitz MS (1983) Effects of the adenovirus H5ts125 and H5ts107 DNA binding proteins on DNA replication in vitro. Virology 124: 380–389CrossRefGoogle Scholar
  22. Ginsberg HS, Ensinger MJ, Kauffman RS, Mayer AJ, Lundholm U (1974) Cell transformation: a study of regulation with types 5 and 12 adenovirus temperature-sensitive mutants. Cold Spring Harbor Symp Quant Biol 39: 419–426Google Scholar
  23. Hirschhorn RR, Abrams R (1978) Synthesis of herpes simplex virus DNA in soluble nuclear extracts. Biochim Biophys Res Commun 84: 1129–1135CrossRefGoogle Scholar
  24. Horwitz MS (1978) Temperature-sensitive replication of H5ts125 adenovirus DNA in vitro. Proc Natl Acad Sci USA 75: 4291–4295PubMedCrossRefGoogle Scholar
  25. Horwitz MS, Ariga M (1981) Multiple rounds of adenovirus synthesis in vitro. Proc Natl Acad Sci USA 78: 1476–1480PubMedCrossRefGoogle Scholar
  26. Kaplan LM, Kleinman RE, Horwitz MS (1977) Replication of adenovirus type 2 DNA in vitro. Proc Natl Acad Sci USA 74: 4425–4429PubMedCrossRefGoogle Scholar
  27. Kaplan LM, Ariga H, Hurwitz J, Horwitz MS (1979) Complementation of the temperature sensitive defect in H5ts125 adenovirus DNA replication in vitro. Proc Natl Acad Sci USA 76: 5534–5538PubMedCrossRefGoogle Scholar
  28. Kedinger C, Brison O, Perrin F, Wilhelm J (1978) Structural analysis of replicative intermediates from adenovirus type 2 infected HeLa cell nuclei. J Virol 26: 364–379PubMedGoogle Scholar
  29. Kelly TJ, Lechner RL (1978) The structure of replicating adenovirus DNA molecules: characterization of DNA-protein complexes from infected cells. Cold Spring Harbor Symp Quant Biol 43: 721–728Google Scholar
  30. Klein H, Maltzman W, Levine AJ (1979) Structure function relationships of the adenovirus DNA binding protein. J Biol Chem 254: 11051–11060PubMedGoogle Scholar
  31. Klessig DF, Chow LT (1980) Incomplete splicing and deficient accumulation of the fiber mRNA in monkey cells infected by human adenovirus type 2. J Mol Biol 139: 221–242PubMedCrossRefGoogle Scholar
  32. Klessig DF, Grodzicker T (1979) Mutations that allow human Ad2 and Ad5 to express late genes in monkey cells map in the viral gene encoding the 72 kD DNA binding protein. Cell 17: 957–966PubMedCrossRefGoogle Scholar
  33. Krokan H, Schaffer P, de Pamphilis ML (1979) Involvement of eucaryotie DNA polymerase α and γ in the replication of cellular and viral DNA. Biochemistry 18: 4431–4443PubMedCrossRefGoogle Scholar
  34. Kruijer W, van Schaik FMA, Sussenbach JS (1981) Structure and organization of the gene coding for the DNA binding protein of adenovirus type 5. Nucleic Acids Res 9: 4439–4457PubMedCrossRefGoogle Scholar
  35. Kruijer W, Nicolas JC, van Schaik FMA, Sussenbach JS (1983a) Structure and function of DNA binding proteins from revertants of adenovirus type 5 mutants with a temperature- sensitive DNA replication. Virology 124: 425–433CrossRefGoogle Scholar
  36. Kruijer W, van Schaik FMA, Speijer JG, Sussenbach JS (1983b) Structure and function of adenovirus DNA binding protein. Comparison of the amino acid sequences of Ad5 and Ad12 proteins derived from the nucleotide sequence of the corresponding genes. Virology 120: 140–153CrossRefGoogle Scholar
  37. Kwant MM, van der Vliet (1980) Differential effect of aphidicolin on adenovirus DNA synthesis and cellular DNA synthesis. Nucleic Acids Res 8: 3993–4007PubMedCrossRefGoogle Scholar
  38. Lechner RL, Kelly TJ (1977) The structure of replicating adenovirus 2 DNA molecules. Cell 12: 1007–1020PubMedCrossRefGoogle Scholar
  39. Lenstra J A, Hofsteenge J, Beintema JJ (1977) Invariant features of the structure of pancreatic ribonuclease. J Mol Biol 109: 185–193PubMedCrossRefGoogle Scholar
  40. Lichy JH, Horwitz MS, Hurwitz J (1981) Formation of a covalent complex between the 80000 dalton adenovirus terminal protein and 5’-dCMP in vitro. Proc Natl Acad Sci USA 78: 2678–2682PubMedCrossRefGoogle Scholar
  41. Lichy JH, Field J, Horwitz MS, Hurwitz J (1982) Separation of the adenovirus terminal protein precursor from its associated DNA polymerase: role of both proteins in the initiation of adenovirus DNA replication. Proc Natl Acad Sci USA 79: 5225–5229PubMedCrossRefGoogle Scholar
  42. Lim VI (1974) Structural principles of the globular organization of protein chains. A stereochemical theory of globular protein secondary structure. J Mol Biol 88: 857–872PubMedCrossRefGoogle Scholar
  43. Linne T, Philipson L (1980) Further characterization of the phosphate moiety of the adenovirus type 2 DNA-binding protein. Eur J Biochem 103: 259–270PubMedCrossRefGoogle Scholar
  44. Longiaru M, Ikeda J, Jarkovsky Z, Horwitz SB, Horwitz MS (1979) The effect of aphidicolin on adenovirus DNA synthesis. Nucleic Acids Res 6: 3369–3386PubMedCrossRefGoogle Scholar
  45. Nagata K, Guggenheimer RA, Enomoto T, Lichy JH, Hurwitz J (1982) Adenovirus DNA replication in vitro: identification of a host factor that stimulates synthesis of the preterminal protein-dCMP complex. Proc Natl Acad Sci USA 79: 6438–6442PubMedCrossRefGoogle Scholar
  46. Nevins JR, Jensen-Winkler J (1980) Regulation of early adenovirus transcription: a protein product from early region 2 specifically represses region 4 transcription. Proc Natl Acad Sci USA 77: 1893–1987PubMedCrossRefGoogle Scholar
  47. Nicolas JC, Ingrand D, Sarnow P, Levine AJ (1982) A mutation in the adenovirus type 5 DNA binding protein that fails to autoregulate the production of the DNA binding protein. Virology 122: 481–485PubMedCrossRefGoogle Scholar
  48. Ostrove JM, Rosenfeld P, Williams JR, Kelly TJ (1983) In vitro complementation as an assay for purification of adenovirus DNA replication proteins. Proc Natl Acad Sci USA 80: 935–939PubMedCrossRefGoogle Scholar
  49. Pincus S, Robertson W, Rekosh D (1981) Characterization of the effect of aphidicolin on adenovirus DNA replication: evidence in support of a protein primer model of initiation. Nucleic Acids Res 9: 4919–4338PubMedCrossRefGoogle Scholar
  50. Rekosh DMK, Russell WC, Bellett AJD, Robinson A J (1977) Identification of a protein linked to the ends of adenovirus DNA. Cell 11: 283–295PubMedCrossRefGoogle Scholar
  51. Rijnders AWM, van Maarschalkerweerd MW, Visser L, Reemst AMCB, Sussenbach JS, Rozijn TH (1983) Expression of integrated viral DNA sequences outside the transforming region of eight adenovirus transformed cell lines. Biochim Biophys Acta 739: 48–56PubMedGoogle Scholar
  52. Rijnders AWM, van Bergen BGM, van der Vliet PC, Sussenbach JS (to be published) Immunological characterization of the role of adenovirus terminalprotein in viral DNA replication. VirologyGoogle Scholar
  53. Rose GD (1978) Prediction of chain turns in globular proteins on a hydrophobic base. Nature 272: 586–590PubMedCrossRefGoogle Scholar
  54. Shaw CH, Rekosh DM, Russell WC (1980) Adenovirus DNA synthesis in vitro is catalyzed by DNA polymerase γ. J Gen Virol 48: 231–236PubMedCrossRefGoogle Scholar
  55. Spadari S, Sala F, Pedrali-Noy G (1982) Aphidicolin: a specific inhibitor of nuclear DNA replication in eukaryotes. Trends Biochem Sci 7: 29–31CrossRefGoogle Scholar
  56. Steenbergh PH, Maat J, van Ormondt H, Sussenbach JS (1977) The nucleotide sequence at the termini of adenovirus 5 DNA. Nucleic Acids Res 4: 4371–4390PubMedCrossRefGoogle Scholar
  57. Stillman BW (1981) Adenovirus DNA replication in vitro: a protein linked to the 5’-end of nascent DNA strands. J Virol 37: 139–147PubMedGoogle Scholar
  58. Stillman BW, Bellett AJD (1979) An adenovirus protein associated with the ends of replicating DNA molecules. Virology 93: 69–79PubMedCrossRefGoogle Scholar
  59. Stillman BW, Lewis JB, Chow LT, Mathews MB, Smart JE (1981) Identification of the gene and mRNA for the adenovirus terminal protein precursor. Cell 23: 497–508PubMedCrossRefGoogle Scholar
  60. Stillman BW, Topp WC, Engler JA (1982a) Conserved sequences at the origin of adenovirus DNA replication. J Virol 44: 530–537PubMedGoogle Scholar
  61. Stillman BW, Tamanoi F, Mathews MB (1982b) Purification of an adenovirus-coded DNA polymerase that is required for initiation of DNA replication. Cell 31: 613–623PubMedCrossRefGoogle Scholar
  62. Stow ND (1982) The infectivity of adenovirus genomes lacking DNA sequences from their left-hand termini. Nucleic Acids Res 10: 5105–5119PubMedCrossRefGoogle Scholar
  63. Sussenbach JS, Kuijk MG (1977) Studies on the mechanism of replication of adenovirus DNA. V The location of termini of replication. Virology 77: 149–157PubMedCrossRefGoogle Scholar
  64. Sussenbach JS, Kuijk MG (1978) The mechanism of replication of adenovirus DNA. VI Localization of the origins of the displacement synthesis. Virology 84: 509–517PubMedCrossRefGoogle Scholar
  65. Sussenbach JS, van der Vliet PC, Ellens DJ, Jansz HS (1972) Linear intermediates in the replication of adenovirus DNA. Nature 239: 47–49Google Scholar
  66. Tamanoi F, Stillman BW (1982) Function of adenovirus terminal protein in the initiation of DNA replication. Proc Natl Acad Sci USA 79: 2221–2225PubMedCrossRefGoogle Scholar
  67. Van Bergen BGM, van der Vliet PC (1983) Temperature-sensitive initiation and elongation of adenovirus DNA replication in vitro with nuclear extracts from H5ts36, H5ts149 and H5ts125 infected HeLa cells. J Virol 42: 642–648Google Scholar
  68. Van Bergen BGM, van der Ley PA, van Driel W, van Mansfeld ADM, van der Vliet PC (1983) Replication of origin containing adenovirus DNA fragments that do not carry the terminal protein. Nucleic Acids Res 11: 1975–1990PubMedCrossRefGoogle Scholar
  69. Van der Vliet PC, Kwant MM (1978) Role of DNA polymerase γ in adenovirus DNA replication. Nature 276: 532–534PubMedCrossRefGoogle Scholar
  70. Van der Vliet PC, Levine AJ (1973) DNA binding proteins specific for cells infected by adenoviruses. Nature 246: 1709–174Google Scholar
  71. Van der Vliet PC, Sussenbach JS (1972) The mechanism of adenovirus DNA synthesis in isolated nuclei. Eur J Biochem 30: 584–592PubMedCrossRefGoogle Scholar
  72. Van der Vliet PC, Sussenbach JS (1975) An adenovirus type 5 gene function required for initiation of viral DNA replication. Virology 67: 415–426PubMedCrossRefGoogle Scholar
  73. Van der Vliet, Levine AJ, Ensinger M, Ginsbergs HS (1975) Thermolabile DNA binding proteins from cells infected with a temperature-sensitive mutant of adenovirus defective in viral DNA synthesis. J Virol 15: 348–354Google Scholar
  74. Van der Vliet PC, Zandberg J, Jansz HS (1977) Evidence for a function of the adenovirus DNA binding protein in initiation of DNA synthesis as well as in elongation on nascent DNA chains. Virology 80: 98–110PubMedCrossRefGoogle Scholar
  75. Van Wielink PS, Naaktgeboren N, Sussenbach JS (1979) Presence of protein at the termini of intracellular adenovirus type 5 DNA. Biochim Biophys Acta 563: 89–99PubMedGoogle Scholar
  76. Wilhelm J, Brison O, Kedinger C, Chambon P (1976) Characterization of adenovirus type 2 transcriptional complexes isolated from infected HeLa cell nuclei. J Virol 15: 744–758Google Scholar
  77. Winnacker EL (1975) Adenovirus type 2 DNA replication. I Evidence for discontinuous replication. J Virol 15: 744–758PubMedGoogle Scholar
  78. Wohlgemuth DJ, Hsu M-T (1981) Visualization of nascent RNA transcripts and simultaneous transcription and replication in viral nucleoprotein complexes from adenovirus 2-infected HeLa cells. J Mol Biol 147: 247–268CrossRefGoogle Scholar
  79. Yagura T, Kozu T, Seno T (1982) Mouse DNA polymerase accompanied by a novel RNA polymerase activity: purification and partial characterization. J Biochem 91: 607–618PubMedGoogle Scholar
  80. Yamashita T, Arens M, Green M (1977) Adenovirus DNA replication. Isolation of a soluble replication system and analysis of the in vitro DNA product. J Biol Chem 252: 7940–7954PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1983

Authors and Affiliations

  • John S. Sussenbach
    • 1
  • Peter C. van der Vliet
    • 1
  1. 1.Laboratory for Physiological ChemistryState University of UtrechtUtrechtThe Netherlands

Personalised recommendations