Summary
The replication of the avian osteopetrosis virus MAV-2-O was compared in chick embryo fibroblasts from two strains of chicken. These were G-B1 which is relatively resistant to MAV-2-O and CB which is susceptible. The production of MAV-2-O was delayed in G-B1 cells (compared with CB cells). The same result was observed after infection with Rous sarcoma viruses of subgroups B, C, and D. In addition, the transforming viruses induced foci on G-B1 fibroblasts 24 to 48 hours later than on CB fibroblasts. In G-B1 cells there was also a delayed kinetics of intracellular viral RNA production. Integrated and linear unintegrated MAV-2-O DNA species were also present in lower amounts in G-B1 than in CB fibroblasts at 3 days postinfection.In vivo studies confirmed thein vitro situation. There was a marked difference in the amount of virus present in the osteoid bone matrix and the osteocytic lacunae of osteopetrotic bones from susceptible and G-B1 chickens. In contrast to the bone lesions from susceptible animals, budding virus particles were not detectable in lesions from G-B1 chickens. There was no difference in the amount of virus in osteopetrotic and non-osteopetrotic bone of susceptible chickens suggesting that virus replication alone is not sufficient for induction of osteopetrosis and that an additional specific virus-cell interaction is required. The relative resistance of strain G-B1 may therefore, be a consequence of a reduced frequency of this interaction. Its basis may be the lower amount of integrated, as well as unintegrated, viral DNA.
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References
Biggs PM, Milne BS, Graf T, Bauer H (1973) Oncogenicity of non-transforming mutants of avian sarcoma viruses. J Gen Virol 18: 399–403
Böni-Schnetzler M, Böni J, Ferdinand F-J, Franklin RM (1985) Developmental and molecular aspects of nephroblastomas induced by avian myeloblastosis-associated virus 2-O. J Virol 55: 213–222
Böni J, Böni-Schnetzler M, Vainio E, Franklin RM (1986) Chicken strain G-B1 exhibits a relative resistance to avian osteopetrosis. Arch Virol 91: 21–36
Chirgwin JM, Przybyla AE, Macdonald RJ, Rutter WJ (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18: 5294–5299
Frank RM, Franklin RM (1982) Electron microscopy of avian osteopetrosis induced by retrovirus MAV-2-O. Calcif Tissue Int 34: 382–390
Fung Y-KT, Fadly AM, Crittenden LB, Kung H-J (1981) On the mechanism of retrovirus-induced avian lymphoid leukosis: deletion and integration of the proviruses. Proc Natl Acad Sci U.S.A. 78: 3418–3422
Huleihel M, Aboud M (1983) Inhibition of retrovirus DNA supercoiling in interferon-treated cells. J Virol 48: 120–126
Humphries EH, Danhof ML, Hlozanek I (1984) Characterization of endogenous viral loci in five lines of White Leghorn chickens. Virology 135: 125–138
Jeffreys AJ, Flavell RA (1977) A physical map of the DNA regions flanking the rabbit β-globin gene. Cell 12: 429–439
McMaster GK, Carmichael GC (1977) Analysis of single- and double-stranded nucleic acids on polyacrylamide and agarose gels by using glyoxal and acridine orange. Proc Natl Acad Sci U.S.A. 74: 4835–4838
Morgan JJ, Smith RE (1983) Rapid induction of osteopetrosis by subgroup E recombinant viruses. Virology 129: 493–500
Moscovici C, Chi D, Gazzolo L, Moscovici MG (1976) A study of plaque formation with avian RNA tumor viruses. Virology 73: 181–189
Neel BG, Hayward WS, Robinson HL, Fang J, Astrin SM (1981) Avian leukosis virus-induced tumors have common proviral integration sites and synthesize discrete new RNAs: oncogenesis by promotor insertion. Cell 23: 323–334
Neiman P, Beemon K, Luce JA (1981) Independent recombination between avian leukosis virus terminal sequences and host DNA in virus-induced proliferative disease. Proc Natl Acad Sci U.S.A. 78: 1896–1900
Nusse R, Varmus HE (1982) Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell 31: 99–109
Payne GS, Courtneidge SA, Crittenden LB, Fadly AM, Bishop JM, Varmus HE (1981) Analysis of avian leukosis virus DNA and RNA in bursal tumors: viral gene expression is not required for maintenance of the tumor state. Cell 23: 311–322
Perbal B, Cline JM, Hillyard RL, Baluda MA (1983) Organization of chicken DNA sequences homologous to the transforming gene of avian myeloblastosis virus. II. Isolation and characterization ofproto-amv DNA recombinant clones from a library of leukemic chicken DNA. J Virol 45: 925–940
Robinson HL, Miles BD (1985) Avian leukosis virus-induced osteopetrosis is associated with the persistent synthesis of viral DNA. Virology 141: 130–143
Schmidt EV, Keene JD, Linial M, Smith RE (1982) Association of 3′ terminal RNA sequences with avian leukosis viruses causing a high incidence of osteopetrosis. Virology 116: 163–180
Smith RE, Moscovici C (1969) The oncogenic effects of nontransforming viruses from avian myeloblastosis virus. Cancer Res 29: 1356–1366
Smith RE, Davids LJ, Neiman PE (1976) Comparison of an avian osteopetrosis virus with an avian lymphomatosis virus by RNA-DNA hybridization. J Virol 17: 160–167
Smith RE (1982) Avian osteopetrosis. In:Graf T, Jaenisch R (eds) Current topics in microbiology and immunology, vol 101. Springer, Berlin-Heidelberg-New York, pp 75–94
Smith RE, Morgan JH (1982) Identification of plaque isolates of an avian retrovirus causing rapid and slow onset osteopetrosis. Virology 119: 488–499
Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98: 503–517
Vogt PK (1969) Focus assay of Rous sarcoma virus. In:Habel K, Salzman NP (eds) Fundamental techniques in virology. Academic Press, New York-London, pp 198–211
Weller SK, Joy AE, Temin HM (1980) Correlation between cell killing and massive second-round superinfection by members of some subgroups of avian leukosis virus. J Virol 33: 494–506
Weller SK, Temin HM (1981) Cell killing by avian leukosis viruses. J Virol 39: 713–721
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Böni, J., Böni-Schnetzler, M., Frank, R.M. et al. MAV-2-O replicates at a reduced rate in cells from the osteopetrosis resistant G-B1 chicken. Archives of Virology 91, 37–52 (1986). https://doi.org/10.1007/BF01316726
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DOI: https://doi.org/10.1007/BF01316726