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. 1985 Oct;56(1):240–244. doi: 10.1128/jvi.56.1.240-244.1985

Biologically active proviral clone of myeloblastosis-associated virus type 1: implications for the genesis of avian myeloblastosis virus.

B Perbal, J S Lipsick, J Svoboda, R F Silva, M A Baluda
PMCID: PMC252511  PMID: 2993653

Abstract

A biologically active myeloblastosis-associated virus (MAV) provirus was cloned from a bacteriophage recombinant library constructed from leukemic chicken myeloblast DNA. The restriction endonuclease map of this clone was consistent with that of a type 1 MAV (MAV-1). Interference assays of virus recovered from cultured chicken embryo fibroblasts after DNA transfection established that the provirus was infectious and confirmed that it belonged to avian retrovirus subgroup A (type 1). Antipeptide antibodies raised against the env-encoded carboxyl terminus of p48myb, the transforming protein of avian myeloblastosis virus, specifically immunoprecipitated the gp37env from quail cells transfected with MAV-1 proviral DNA but not from cells infected with MAV-2. This suggests that MAV-1 rather than MAV-2 is the progenitor helper virus from which avian myeloblastosis virus arose by the transduction of cellular proto-oncogene sequences.

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Selected References

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  1. BURMESTER B. R., WALTER W. G., GROSS M. A., FONTES A. K. The oncogenic spectrum of two pure strains of avian leukosis. J Natl Cancer Inst. 1959 Aug;23:277–291. [PubMed] [Google Scholar]
  2. Benton W. D., Davis R. W. Screening lambdagt recombinant clones by hybridization to single plaques in situ. Science. 1977 Apr 8;196(4286):180–182. doi: 10.1126/science.322279. [DOI] [PubMed] [Google Scholar]
  3. Bergmann D. G., Souza L. M., Baluda M. A. Characterization of avian myeloblastosis-associated virus DNA intermediates. J Virol. 1980 May;34(2):366–372. doi: 10.1128/jvi.34.2.366-372.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bergmann D. G., Souza L. M., Baluda M. A. Vertebrate DNAs contain nucleotide sequences related to the transforming gene of avian myeloblastosis virus. J Virol. 1981 Nov;40(2):450–455. doi: 10.1128/jvi.40.2.450-455.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bizub D., Katz R. A., Skalka A. M. Nucleotide sequence of noncoding regions in Rous-associated virus-2: comparisons delineate conserved regions important in replication and oncogenesis. J Virol. 1984 Feb;49(2):557–565. doi: 10.1128/jvi.49.2.557-565.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Blattner F. R., Williams B. G., Blechl A. E., Denniston-Thompson K., Faber H. E., Furlong L., Grunwald D. J., Kiefer D. O., Moore D. D., Schumm J. W. Charon phages: safer derivatives of bacteriophage lambda for DNA cloning. Science. 1977 Apr 8;196(4286):161–169. doi: 10.1126/science.847462. [DOI] [PubMed] [Google Scholar]
  7. Bolivar F., Rodriguez R. L., Greene P. J., Betlach M. C., Heyneker H. L., Boyer H. W., Crosa J. H., Falkow S. Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene. 1977;2(2):95–113. [PubMed] [Google Scholar]
  8. Boyer H. W., Roulland-Dussoix D. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J Mol Biol. 1969 May 14;41(3):459–472. doi: 10.1016/0022-2836(69)90288-5. [DOI] [PubMed] [Google Scholar]
  9. Boyle W. J., Lipsick J. S., Reddy E. P., Baluda M. A. Identification of the leukemogenic protein of avian myeloblastosis virus and of its normal cellular homologue. Proc Natl Acad Sci U S A. 1983 May;80(10):2834–2838. doi: 10.1073/pnas.80.10.2834. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Crittenden L. B., Eagen D. A., Gulvas F. A. Assays for endogenous and exogenous lymphoid leukosis viruses and chick helper factor with RSV(--) cell lines. Infect Immun. 1979 May;24(2):379–386. doi: 10.1128/iai.24.2.379-386.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. DeLorbe W. J., Luciw P. A., Goodman H. M., Varmus H. E., Bishop J. M. Molecular cloning and characterization of avian sarcoma virus circular DNA molecules. J Virol. 1980 Oct;36(1):50–61. doi: 10.1128/jvi.36.1.50-61.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Geryk J., Mazo A., Svoboda J., Hlozánek I. Replication of transformation-defective mutants of the Prague strain of Rous sarcoma virus and isolation of a td mutant from duck-adapted PR-RSV-C. Folia Biol (Praha) 1980;26(1):34–41. [PubMed] [Google Scholar]
  13. Gilmartin G. M., Parsons J. T. Identification of transcriptional elements within the long terminal repeat of Rous sarcoma virus. Mol Cell Biol. 1983 Oct;3(10):1834–1845. doi: 10.1128/mcb.3.10.1834. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gorman C. M., Merlino G. T., Willingham M. C., Pastan I., Howard B. H. The Rous sarcoma virus long terminal repeat is a strong promoter when introduced into a variety of eukaryotic cells by DNA-mediated transfection. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6777–6781. doi: 10.1073/pnas.79.22.6777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Graham F. L., van der Eb A. J. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology. 1973 Apr;52(2):456–467. doi: 10.1016/0042-6822(73)90341-3. [DOI] [PubMed] [Google Scholar]
  16. Highfield P. E., Rafield L. F., Gilmer T. M., Parsons J. T. Molecular cloning of avian sarcoma virus closed circular DNA: structural and biological characterization of three recombinant clones. J Virol. 1980 Oct;36(1):271–279. doi: 10.1128/jvi.36.1.271-279.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ishizaki R., Langlois A. J., Bolognesi D. P. Isolation of two subgroup-specific leukemogenic viruses from standard avian myeloblastosis virus. J Virol. 1975 Apr;15(4):906–912. doi: 10.1128/jvi.15.4.906-912.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Katz R. A., Omer C. A., Weis J. H., Mitsialis S. A., Faras A. J., Guntaka R. V. Restriction endonuclease and nucleotide sequence analyses of molecularly cloned unintegrated avian tumor virus DNA: structure of large terminal repeats in circle junctions. J Virol. 1982 Apr;42(1):346–351. doi: 10.1128/jvi.42.1.346-351.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kawai S., Nishizawa M. New procedure for DNA transfection with polycation and dimethyl sulfoxide. Mol Cell Biol. 1984 Jun;4(6):1172–1174. doi: 10.1128/mcb.4.6.1172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Klempnauer K. H., Gonda T. J., Bishop J. M. Nucleotide sequence of the retroviral leukemia gene v-myb and its cellular progenitor c-myb: the architecture of a transduced oncogene. Cell. 1982 Dec;31(2 Pt 1):453–463. doi: 10.1016/0092-8674(82)90138-6. [DOI] [PubMed] [Google Scholar]
  21. Luciw P. A., Bishop J. M., Varmus H. E., Capecchi M. R. Location and function of retroviral and SV40 sequences that enhance biochemical transformation after microinjection of DNA. Cell. 1983 Jul;33(3):705–716. doi: 10.1016/0092-8674(83)90013-2. [DOI] [PubMed] [Google Scholar]
  22. Mitsialis S. A., Manley J. L., Guntaka R. V. Localization of active promoters for eucaryotic RNA polymerase II in the long terminal repeat of avian sarcoma virus DNA. Mol Cell Biol. 1983 May;3(5):811–818. doi: 10.1128/mcb.3.5.811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Moscovici C. Leukemic transformation with avian myeloblastosis virus: present status. Curr Top Microbiol Immunol. 1975;71:79–101. doi: 10.1007/978-3-642-66193-8_2. [DOI] [PubMed] [Google Scholar]
  24. Moscovici C., Moscovici M. G., Jimenez H., Lai M. M., Hayman M. J., Vogt P. K. Continuous tissue culture cell lines derived from chemically induced tumors of Japanese quail. Cell. 1977 May;11(1):95–103. doi: 10.1016/0092-8674(77)90320-8. [DOI] [PubMed] [Google Scholar]
  25. Moscovici C., Vogt P. K. Effects of genetic cellular resistance on cell transformation and virus replication in chicken hematopoietic cell cultures infected with avian myeloblastosis virus (BAI-A). Virology. 1968 Aug;35(4):487–497. doi: 10.1016/0042-6822(68)90278-x. [DOI] [PubMed] [Google Scholar]
  26. Moscovici C., Zanetti M. Studies on single foci of hematopoietic cells transformed by avian myeloblastosis virus. Virology. 1970 Sep;42(1):61–67. doi: 10.1016/0042-6822(70)90238-2. [DOI] [PubMed] [Google Scholar]
  27. Murphy H. M. A new replication-defective variant of the Bryan high-titer strain Rous sarcoma virus. Virology. 1977 Apr;77(2):705–721. doi: 10.1016/0042-6822(77)90493-7. [DOI] [PubMed] [Google Scholar]
  28. O'Rear J. J., Temin H. M. Mapping of alterations in noninfectious proviruses of spleen necrosis virus. J Virol. 1981 Jul;39(1):138–149. doi: 10.1128/jvi.39.1.138-149.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Perbal B., Baluda M. A. Avian myeloblastosis virus transforming gene is related to unique chicken DNA regions separated by at least one intervening sequence. J Virol. 1982 Jan;41(1):250–257. doi: 10.1128/jvi.41.1.250-257.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Perbal B., Baluda M. A. Organization of chicken DNA sequences homologous to the transforming gene of avian myeloblastosis virus. I. Restriction enzyme analysis of total DNA from normal and leukemic cells. J Virol. 1982 Nov;44(2):586–594. doi: 10.1128/jvi.44.2.586-594.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Perbal B., Cline J. M., Hillyard R. L., Baluda M. A. Organization of chicken DNA sequences homologous to the transforming gene of avian myeloblastosis virus. II. Isolation and characterization of lambda proto-amv DNA recombinant clones from a library of leukemic chicken DNA. J Virol. 1983 Mar;45(3):925–940. doi: 10.1128/jvi.45.3.925-940.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  33. Rushlow K. E., Lautenberger J. A., Papas T. S., Baluda M. A., Perbal B., Chirikjian J. G., Reddy E. P. Nucleotide sequence of the transforming gene of avian myeloblastosis virus. Science. 1982 Jun 25;216(4553):1421–1423. doi: 10.1126/science.6283631. [DOI] [PubMed] [Google Scholar]
  34. Rushlow K. E., Lautenberger J. A., Reddy E. P., Souza L. M., Baluda M. A., Chirikjian J. G., Papas T. S. Nucleotide sequence analysis of the long terminal repeat of avian myeloblastosis virus and adjacent host sequences. J Virol. 1982 Jun;42(3):840–846. doi: 10.1128/jvi.42.3.840-846.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Schwartz D. E., Tizard R., Gilbert W. Nucleotide sequence of Rous sarcoma virus. Cell. 1983 Mar;32(3):853–869. doi: 10.1016/0092-8674(83)90071-5. [DOI] [PubMed] [Google Scholar]
  36. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  37. Souza L. M., Briskin M. J., Hillyard R. L., Baluda M. A. Identification of the avian myeloblastosis virus genome. II. Restriction endonuclease analysis of DNA from lambda proviral recombinants and leukemic myeoblast clones. J Virol. 1980 Nov;36(2):325–336. doi: 10.1128/jvi.36.2.325-336.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Souza L. M., Komaromy M. C., Baluda M. A. Identification of a proviral genome associated with avian myeloblastic leukemia. Proc Natl Acad Sci U S A. 1980 May;77(5):3004–3008. doi: 10.1073/pnas.77.5.3004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Souza L. M., Strommer J. N., Hillyard R. L., Komaromy M. C., Baluda M. A. Cellular sequences are present in the presumptive avian myeloblastosis virus genome. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5177–5181. doi: 10.1073/pnas.77.9.5177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wahl G. M., Stern M., Stark G. R. Efficient transfer of large DNA fragments from agarose gels to diazobenzyloxymethyl-paper and rapid hybridization by using dextran sulfate. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3683–3687. doi: 10.1073/pnas.76.8.3683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Yamamoto T., de Crombrugghe B., Pastan I. Identification of a functional promoter in the long terminal repeat of Rous sarcoma virus. Cell. 1980 Dec;22(3):787–797. doi: 10.1016/0092-8674(80)90555-3. [DOI] [PubMed] [Google Scholar]

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