Advertisement

Iridoviridae pp 77-106 | Cite as

Macromolecular Synthesis in Cells Infected by Frog Virus 3

  • D. B. Willis
  • R. Goorha
  • V. G. Chinchar
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 116)

Abstract

The best studied member of the Iridoviridae is frog virus 3 (FV3), isolated by Granoff et al. (1966) from a renal adenocarcinoma of the leopard frog, Rana pipiens. Similar isolates were made from normal frog kidney and liver (FV1, FY 2, FV5–FY24), but FV3 was chosen for further investigation because of its presence in the tumor. As it turned out, this unusual cytoplasmic DNA virus bore no causal or even helper relationship to the tumor, which was the result of infection with the Lucké herpesvirus (Naegele et al. 1974), but it did have a number of interesting characteristics that made it a worthy object of study in its own right. FV3 is probably similar or identical to other amphibian virus isolates obtained from bullfrogs, newts, and toads (Wolf et al. 1968; Clark et al. 1969).

Keywords

Leopard Frog Macromolecular Synthesis Frog Virus Late Message Host Protein Synthesis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aubertin AM (1975) Arginine requirement for frog virus 3 development. Virology 63:573–576 Aubertin AM, Longchampt MO (1974) Thymidine kinase induction in FV3–infected mouse cells. Virology 58: 111–118CrossRefGoogle Scholar
  2. Aubertin AM, Guir J, Kirn A (1970) The inhibition of vaccinia virus DNA synthesis in KB cells infected with FV3. J Gen Virol 8: 105–111PubMedCrossRefGoogle Scholar
  3. Aubertin AM, Palese P, Tan KB, Vilagines R, McAuslan BR (1971) Proteins of a polyhedral cytoplas-mic deoxyvirus. III. Structure of FV3 and location of virus-associated adenosine triphosphate phosphohydrolase. J Virol 8: 643–648PubMedGoogle Scholar
  4. Aubertin AM, Hirth C, Travo C, Nonnenmacha H, Kirn A (1973) Preparation and properties of an inhibitory extract from frog virus 3 particles. J Virol 11: 694–701PubMedGoogle Scholar
  5. Aubertin AM, Travo C, Kirn A (1976) Proteins solubilized from frog virus 3 particles: effect on transcription. J Virol 18: 34–41PubMedGoogle Scholar
  6. Aubertin AM, Anton M, Bingen A, Elharrar M, Kirn A (1977) Solubilized viral proteins produce fatal hepatitis in mice. Nature 265: 456–457PubMedCrossRefGoogle Scholar
  7. Aubertin AM, Tondre L, Martin JP, Kirn A (1980) Structural polypeptides of frog virus 3, phosphory- lated proteins. FEBS Lett 112: 233–237PubMedCrossRefGoogle Scholar
  8. Aubertin AM, Tondre L, Descamps P (1981) Capping of frog virus 3 antigen on the plasma membrane of infected cells. Ann Virol Inst Pasteur 132E: 195–205CrossRefGoogle Scholar
  9. Aubertin AM, Tondre L, Lopez C, Obert G, Kirn A (1983) Sodium dodecyl sulfate-mediated transfer of electrophorectically separated DNA-binding proteins. Anal Biochem 131: 127–134PubMedCrossRefGoogle Scholar
  10. Barzilai R, Lachmi BE (1973) The effect of frog virus 3 on the biological activity of various RNA viruses. J Gen Virol 21: 201–204PubMedCrossRefGoogle Scholar
  11. Barzilai R, Finkelkraut E, Lazarus LH, Goldblum N (1974) Inhibition of simian virus 40 DNA synthesis by frog virus 3. J Gen Virol 23: 335–338PubMedCrossRefGoogle Scholar
  12. Becker A, Murialdo H (1978) Head morphogenesis of complex double-stranded DNA bacteriophages. Microbiol 42: 529–576Google Scholar
  13. Berk AJ, Sharp PA (1977) Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of SI endonuclease digested hybrids. Cell 12: 721–732PubMedCrossRefGoogle Scholar
  14. Braunwald J, Guir J, Obert G (1972) Inhibition de la synthese des proteins cellulaires dans les cellules KB infectees avec le virus 3 de la grenouille (FV3). Ann Inst Pasteur 123: 251–264Google Scholar
  15. Campadelli-Fuime G, Costanzo F, Foa-Tanasi L, LaPlaca M (1975) Modification of cellular RNA polymerase II after infection with frog virus 3. J Gen Virol 27: 341–394Google Scholar
  16. Chinchar VG, Granoff A (1984) Isolation and characterization of a frog virus 3 variant resistant to phosphonoacetate: Genetic evidence for a virus-specific DNA polymerase. Virology 138:357–361Google Scholar
  17. Chinchar VG, Coorha R, Granoff (1984 a) Early proteins are required for the formation of frog virus 3 assembly sites. Virology 135:148–156Google Scholar
  18. Chinchar VG, Metzger D, Granoff A, Goorha R (1984b) Localization of frog virus 3 proteins using monoclonal antibodies. Virology 137: 211–216PubMedCrossRefGoogle Scholar
  19. Clark HF, Gray G, Fabian F, Ziegel RF, Karzon DT (1969) Comparative studies of amphibian cytoplasmic virus strains isolated from the leopard frog, bullfrog, and newt, In: Mizell A (ed) Biology of amphibian tumors. Recent results in cancer research. Springer, Berlin Heidelberg New YorkGoogle Scholar
  20. Cordier O, Aubertin AM, Lopez C, Tondre L (1981) Inhibition de la Tranduction par le FV3: Action des proteines virales de structure solubilisees sur la synthesis proteique in vivo et in vitro. Ann Virol Inst Pasteur 132E: 25–39Google Scholar
  21. Cuillel M, Tripier F, Braunwald J, Jacrot B (1979) A low resolution structure of frog virus 3. Virology 99: 277–285PubMedCrossRefGoogle Scholar
  22. Darai G, Anders K, Koch H, Delius H, Gelderblam H, Samaleios C, Flugel RM (1983) Analysis of the genome of fish lymphocystic disease virus isolated directly from epidermal tumors of pleuronectes. Virology 126: 466–479PubMedCrossRefGoogle Scholar
  23. Delius H, Darai G, Flugel RF (1984) DNA analysis of the insect iridescent virus type 6: evidence for circular permutation and terminal redundancy. J Virol 49: 609–614PubMedGoogle Scholar
  24. Doerfler W (1983) DNA methylation and gene activity. Ann Rev Biochem 52: 93–124PubMedCrossRefGoogle Scholar
  25. Drillien R, Spehner D, Kirn A (1977) Cell killing by FV3: Evidence for cell killing by single viral particles or single viral subunits. Biochem Biophys Res Commun 79: 105–111Google Scholar
  26. Drillien R, Spehner D, Kirn A (1980) Inactivation of the toxicity of frog virus 3 proteins by UV irradiation. FEMS Lett 7:87–90 EisenGoogle Scholar
  27. H, Pereira, Da Silva LH, Jacob F (1968) The regulation and mechanism of DNA synthesis in bacteriophage lambda. Cold Spring Harbor Symp Quant Biol 33: 755–764Google Scholar
  28. Elharrar M, Kirn A (1977) Effect of frog virus 3 infection on protein synthesis activity of mouse liver ribosomes. FEMS Lett 1: 13–16CrossRefGoogle Scholar
  29. Elharrar M, Hirth C, Blanc J, Kirn A (1973) Pathogenic de l’hepatite toxique de la souris provoquee par le FV 3 (frog virus 3): Inhibition de la synthese des macromolecules du foie. Biochem Biophys Acta 319: 91–102Google Scholar
  30. Elliott RM, Kelly DC (1980) Frog virus 3 replication: Induction and intracellular distribution of polypeptides in infected cells. J Virol 33: 28–51Google Scholar
  31. Elliott RM, Bravo R, Kelly DC ( 1980 a) Frog virus 3 replication: Analysis of structural and nonstructural polypeptides in infected BHK cells by acidic and basic two-dimensional gel electrophoresis. J Virol 33: 18–27Google Scholar
  32. Elliott RM, Bateson A, Kelly DC (1980b) Phosphonacetic acid inhibition of frog virus 3 replication. J Virol 33: 539–542PubMedGoogle Scholar
  33. Fenner F, Woodroofe GM (1960) The reactivation of poxviruses II. The range of reactivating viruses. Virology 11: 185–201Google Scholar
  34. Gendrault JL, Steffan OM, Binger A, Kirn A (1981) Penetration and uncoating of frog virus 3Google Scholar
  35. FV3) in cultured rat Kupffer cells. Virology 112:375–384Google Scholar
  36. Gilbert W, Dressier D (1968) DNA replication: The rolling circle model. Cold Spring Harbor Symp Quant Biol 33: 473–484Google Scholar
  37. Goorha R (1981 a) Frog virus 3 requires RNA polymerase II for its replication. J Virol 37:496–499Google Scholar
  38. Goorha R (1981b) DNA-binding proteins in frog virus 3-infected cells. J Gen Virol 56: 131–140PubMedCrossRefGoogle Scholar
  39. Goorha R (1982) Frog virus 3 DNA replication occurs in two stages. J Virol 43: 519–528PubMedGoogle Scholar
  40. Goorha R, Granoff A (1974) Macromolecular synthesis in cells infected by frog virus 3. I. Virus-specific protein synthesis and its regulation. Virology 60: 237–250Google Scholar
  41. Goorha R, Granoff A (1979) Icosahedral cytoplasmic deoxyriboviruses. In: Fraenkel-Conrat H, Wagner RR (eds) Comprehensive virology, vol 14. Plenum, New York, pp 347–399Google Scholar
  42. Goorha R, Murti KG (1982) The genome of frog virus 3, an animal DNA virus, is circularly permuted and terminally redundant. Proc Natl Acad Sci USA 79: 248–252PubMedCrossRefGoogle Scholar
  43. Goorha R, Dixit P (1984) A temperature-sensitive (ts) mutant of frog virus 3 (FV3) is defective in second-stage DNA replication. Virology 136: 186–195PubMedCrossRefGoogle Scholar
  44. Goorha R, Murti G, Granoff A, Tirey R (1978) Macromolecular synthesis in cells infected by frog virus 3. VIII. The nucleus is a site of frog virus 3 DNA and RNA synthesis. Virology 84: 32–50PubMedCrossRefGoogle Scholar
  45. Goorha R, Willis DB, Granoff A (1979) Macromolecular synthesis in cells infected by frog virus 3. XII. Viral regulating proteins in transcriptional and post–transcriptional controls. J Virol 32: 442–448Google Scholar
  46. Goorha R, Willis DB, Granoff A, Naegele RF (1981) Characterization of a temperature-sensitive mutant of frog virus 3 defective in DNA replication. Virology 112: 40–48PubMedCrossRefGoogle Scholar
  47. Goorha R, Granoff A, Willis D, Murti KG (1984) The role of DNA methylation in virus replication: Inhibition of frog virus 3 replication by 5-azacytidine. Virology 138: 94–102PubMedCrossRefGoogle Scholar
  48. Granoff A (1969) Viruses of amphibia. Curr Top Microbiol Immunol 50: 107–137PubMedGoogle Scholar
  49. Granoff A, Came PE, Breeze DC (1966) Viruses and renal carcinoma of Rana pipiens. I. The isolation and properties of virus from normal and tumor tissue. Virology 29: 133–148Google Scholar
  50. Gravell M, Granoff A (1970) Viruses and renal adenocarcinoma of Rana pipiens. IX. The influence of temperature and host cell on replication of frog polyhedral cytoplasmic deoxyribovirus ( PCDV ). Virology 41: 596–602Google Scholar
  51. Gravell M, Naegele RF (1970) Nongenetic reactivation of frog polyhedral cytoplasmic deoxyribovirus ( PCDV ). Virology 40: 170–174Google Scholar
  52. Gravell M, Cromeans T (1971) Mechanisms involved in the nongenetic reactivation of frog polyhedral cytoplasmic deoxyribovirus: Evidence for RNA polymerase in the virion. Virology 46: 39–49Google Scholar
  53. Guir M, Braunwald J, Kirn A (1970) Inhibition de la synthese du DNA et des RNA cellulaires dans les cellules KB infectee avec le virus 3 de la grenouille (FV3). CR Hebd Acad Sci Paris 270: 2605–2608Google Scholar
  54. Houts GE, Gravell M, Darlington RW (1970) Base composition and molecular weight of DNA from a frog polyhedral cytoplasmic deoxyribovirus. Proc Soc Exp Biol Med 135: 232–236PubMedGoogle Scholar
  55. Houts GE, Gravell M, Darlington (1974) Electron microscopic observation of early events of frog virus 3 replication. Virology 58: 587–594Google Scholar
  56. Kang HS, McAuslan BR (1972) Virus-associated nucleases: Location and properties of deoxyribo-nucleases and ribonucleases in purified frog virus 3. J Virol 10: 202–210PubMedGoogle Scholar
  57. Kelly DC (1973) Icosahedral cytoplasmic deoxyriboviruses. J Gen Virol 20: 17–41PubMedCrossRefGoogle Scholar
  58. Kelly DC, Avery RJ (1974) Frog virus 3 deoxyribonucleic acid. J Gen Virol 24: 339–348PubMedCrossRefGoogle Scholar
  59. Kirn A, Steffan AM, Gut JP (1974) L’hepatite degenerative aigue de la souris, provoquee par le FV3. Nouve Presse Med 3: 145–149Google Scholar
  60. Kucera L (1970) Effects of temperature on frog polyhedral cytoplasmic deoxyribovirus multiplication: Thermosensitivity of initiation, replication, encapsidation of viral DNA. Virology 42: 576–581PubMedCrossRefGoogle Scholar
  61. Kucera LS, Granoff A (1969) Induction and regulation of DNA nucleotidyl-transferase activity in fish cells infected with frog virus 3. Virology 37: 455–463PubMedCrossRefGoogle Scholar
  62. Lee MH, Willis DB (1983) Restriction endonuclease mapping of the frog virus 3 genome. Virology 126: 317–327PubMedCrossRefGoogle Scholar
  63. Luder A, Mosig G (1982) Alternate mechanism for initiation of DNA replication forks in bacterio-phage T4-priming by RNA polymerase and by recombination. Proc Natl Acad Sci USA 79: 1101–1105PubMedCrossRefGoogle Scholar
  64. Maes R, Granoff A (1967a) Viruses and renal carcinoma of Rana pipiens. III. The relationship between input multiplicity of infection and inclusion body formation in frog virus 3-infected cells. Virology 33: 137–144PubMedCrossRefGoogle Scholar
  65. Maes R, Granoff A (1967 b) Viruses and renal carcinoma of Rana pipiens. IV. Nucleic acid synthesis in frog virus 3-infected BHK 21/13 cells. Virology 33:491–502Google Scholar
  66. Martin JP, Aubertin AM, Lecerf F, Kirn A (1981) Intracellular distribution and phosphorylation of virus-induced polypeptides in frog virus 3-infected cells. Virology 110: 349–365PubMedCrossRefGoogle Scholar
  67. Martin JP, Aubertin AM, Kirn A (1982) Expression of frog virus 3 early genes after ultraviolet irradiation. Virology 122: 402–410PubMedCrossRefGoogle Scholar
  68. Martin JP, Aubertin AM, Londre L, Kirn A (1984) Fate of frog virus 3 DNA replicated in the nucleus of arginine-deprived CHO cells. J Gen Virol 65: 721–732PubMedCrossRefGoogle Scholar
  69. McAuslan BR, Smith W (1968) DNA synthesis in frog virus 3-infected mammalian cells. J Virol 2: 1006–1015PubMedGoogle Scholar
  70. McAuslan BR, Kucera L (1969) DNA polymerase activity in FV 3-infected BHK cells. Virology 35: 328–330CrossRefGoogle Scholar
  71. McAuslan BR, Armentrout RW (1974) The biochemistry of icosahedral cytoplasmic eoxyviruses. Curr Top Microbiol Immunol 68: 77–105PubMedGoogle Scholar
  72. Miller RC (1975) Replication and molecular recombination of T4 phage. Ann Rev Microbiol 29: 355–376CrossRefGoogle Scholar
  73. Murti KG, Goorha R, Granoff A (1982) Structure of frog virus 3: Genome size and arrangement of nucleotide sequences as determined by electron microscopy. Virology 116: 275–283Google Scholar
  74. Naegele RF, Granoff A, Darlington RW (1974) The presence of the Lucke herpesvirus genome in induced tadpole tumors and its oncogenicity: Koch-Henle postulates fulfilled. Proc Nat Acad Sci US 71: 830–834Google Scholar
  75. Nishioka Y, Silverstein S (1977) Degradation of cellular mRNA during infection by herpes simplex virus. Proc Natl Acad Sci USA 74: 2370–2374PubMedCrossRefGoogle Scholar
  76. Purifoy D, Naegele RF, Granoff A (1973) Viruses and renal carcinoma of Rana pipiens. XIV. Temperature-sensitive mutants of frog virus 3 with defective encapsidation. Virology 54: 525–535PubMedCrossRefGoogle Scholar
  77. Rabussay D, Geidusch EP (1977) Regulation of gene action in the development of lytic bacteriophages. In: Fraenkel-Conrat H, Wagner RR (eds) Comprehensive virology. Plenum, New York, pp 1–196Google Scholar
  78. Raghow R, Granoff A (1979) Macromolecular synthesis in cells infected by frog virus 3. X. Inhibition of cellular protein synthesis by heat-inactivated virus. Virology 98: 319–327Google Scholar
  79. Raghow R, Granoff A (1980) Macromolecular synthesis in cells infected by frog virus 3. XIV. Characterization of the methylated nucleotide sequences in viral messenger RNAs. Virology 107: 283–294Google Scholar
  80. Raghow R, Granoff A (1983) Cell-free translation of frog virus 3 messenger RNAs: Initiation factors from infected cells discriminate between early and late viral mRNAs. J Biol Chem 258: 511–578Google Scholar
  81. Raghow R, Willis DB, Granoff A (1980) Macromolecular synthesis in cells infected by frog virus 3. XIII. Cell-free translation of immediate early viral mRNAs. Virology 100: 495–497Google Scholar
  82. Razin A, Riggs W (1980) DNA methylation and gene function. Science 210: 604–610PubMedCrossRefGoogle Scholar
  83. Robach Y, Michels B, Cerf R, Braunwald J, Darcy-Tripier F (1983) Ultrasonic absorption evidence for structural fluctuations in frog virus 3 and its subparticles. Proc Natl Acad Sci USA 80: 3981–3985PubMedCrossRefGoogle Scholar
  84. Schibler U, Kelley DE, Perry RP (1977) Comparison of methylated sequences in messenger RNA and heterogeneous nuclear RNA from mouse L cells. J Mol Biol 115: 695–714PubMedCrossRefGoogle Scholar
  85. Silberstein H, August JT (1973) Phosphorylation of animal virus proteins by a virion protein kinase. J Virol 12: 511–522PubMedGoogle Scholar
  86. Silberstein H, August JT (1976 a) Purification and properties of a virion protein kinase. J Biol Chem 251:3176–3184Google Scholar
  87. Silberstein H, August JT (1976 b) Characterization of a virion protein kinase as a virus-specified enzyme. J Biol Chem 251:3185–3190Google Scholar
  88. Skalka AM (1977) DNA replication-bacteriophage lambda. Curr Top Microbiol Immunol 78: 201–237PubMedCrossRefGoogle Scholar
  89. Smith WR, McAuslan BR (1969) Biophysical properties of frog virus 3 and its DNA: Fate of radioactive virus in early stages of infection. J Virol 4: 332–347Google Scholar
  90. Streisinger G, Emrich J, Stahl MM (1967) Chromosome structure in phage T4. III. Terminal redundancy and length determination. Proc Natl Acad Sci USA 57: 292–295Google Scholar
  91. Tannenbaum J, Goorha R, Granoff A (1978) Inhibition of vesicular stomatitis virus replication by frog virus 3. Selective action on secondary transcription. Virology 89: 560–569Google Scholar
  92. Tannenbaum J, Goorha RG, Granoff A (1979) The inhibition of vesicular stomatitis virus protein synthesis by frog virus 3. Virol 95: 227–231CrossRefGoogle Scholar
  93. Tripier-Darcy F, Braunwald J, Kirn A (1982) Localization of some frog virus 3 structural proteins. Virology 116: 635–640PubMedCrossRefGoogle Scholar
  94. Tweedell K, Granoff A (1968) Viruses and renal carcinoma of Rana pipiens V. Effect of frog virus 3 on developing frog embryos and larvae. J Nat Cancer Inst 40: 407–410PubMedGoogle Scholar
  95. Vilagines R, McAuslan BR (1971) Proteins of polyhedral cytoplasmic deoxyribovirus. II. Nucleotide phosphohydrolase activity associated with frog virus 3. J Virol 7: 619–624PubMedGoogle Scholar
  96. Watson JD (1971) Origin of concatemeric T7 DNA. Nature 239: 197–201Google Scholar
  97. Webster RG, Goorha R, Granoff A (1974) Replication of influenza virus in chick embryo fibroblasts after inhibition of host cell macromolecular synthesis by frog virus 3. Virology 58: 600–604PubMedCrossRefGoogle Scholar
  98. Willis D, Granoff A (1974) Lipid composition of frog virus 3. Virology 61: 256–269PubMedCrossRefGoogle Scholar
  99. Willis D, Granoff A ( 1976 a) Macromolecular synthesis in cells infected by frog virus 3. IV. Regulation of virus-specific RNA synthesis. Virology 70: 397–410Google Scholar
  100. Willis D, Granoff A (1976b) Macromolecular synthesis in cells infected by frog virus 3. V. The absence of polyadenylic acid in the majority of virus-specific RNA species. Virology 73: 543–547Google Scholar
  101. Willis D, Granoff A (1978) Macromolecular synthesis in cells infected by frog virus 3. IX. Two temporal classes of early viral RNA. Virology 86: 443–453Google Scholar
  102. Willis D, Granoff A (1980) Frog virus 3 DNA is heavily methylated at CpG sequences. Virology 107: 250–257PubMedCrossRefGoogle Scholar
  103. Willis DB, Goorha R, Miles M, Granoff A (1977) Macromolecular synthesis in cells infected by frog virus 3. VII. Transcriptional and post-transcriptional regulation of virus gene expression. J Virol 24: 326–342Google Scholar
  104. Willis DB, Goorha R, Granoff A (1979 a) Macromolecular synthesis in cells infected by frog virus 3 XI. A ts mutant of frog virus 3 that is defective in late transcription. Virology 98:328–335Google Scholar
  105. Willis DB, Goorha R, Granoff A (1979b) Nongenetic reactivation of frog virus 3 DNA. Virology 98: 476–479PubMedCrossRefGoogle Scholar
  106. Willis DB, Goorha R, Granoff A (1984a) DNA methyltransferase induced by frog virus 3. J Virol 49: 86–91PubMedGoogle Scholar
  107. Willis DB, Foglesong D, Granoff A (1984b) Nucleotide sequence of an immediate-early frog virus 3 gene. J Virol 53: 905–912Google Scholar
  108. Wolf K, Bullock GL, Dunbar CE, Quimby MC (1968) Tadpole edema virus: a viscerotrophic pathogen for anuran amphibians. J Infect Dis 118: 253–262PubMedCrossRefGoogle Scholar
  109. Zylber-Katz E, Weisman P (1975) Effects on host cell polyribosomes following infection with frog virus 3 at a non-permissive temperature. Arch Virol 47: 181–185PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1985

Authors and Affiliations

  • D. B. Willis
    • 1
  • R. Goorha
    • 1
  • V. G. Chinchar
    • 1
  1. 1.Department of Virology and Molecular BiologySt. Jude Children’s Research HospitalMemphisUSA

Personalised recommendations