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. 1981 Dec;40(3):800–811. doi: 10.1128/jvi.40.3.800-811.1981

Characterization of reticuloendotheliosis virus strain T DNA and isolation of a novel variant of reticuloendotheliosis virus strain T by molecular cloning.

I S Chen, T W Mak, J J O'Rear, H M Temin
PMCID: PMC256691  PMID: 6275117

Abstract

Reticuloendotheliosis virus strain T (REV-T) is a highly oncogenic avian retrovirus which causes a rapid neoplastic disease of the lymphoreticular system. Upon infection, this virus gives rise to two species of unintegrated linear viral DNA, which are 8.3 and 5.5 kilobase pairs long and represent the helper virus (REV-A) and the oncogenic component (REV-T), respectively. Restriction endonuclease cleavage maps of these two DNA components indicate that REV-T DNA has a large portion of the genome deleted with respect to REV-A DNA and a substitution about 0.8 to 1.5 kilobase pairs long that is unrelated to REV-A DNA. These additional sequences comprise the putative transforming region of REV-T (rel). A chicken spleen cell line transformed by REV-T produced virus which upon infection gives rise to three species of unintegrated linear viral DNA (8.3, 5.5, and 3,3 kilobase pairs). We isolated the proviruses of the 8.3- and 3.3-kilobase pair species from this cell line by cloning in the phage vector Charon 4A. Restriction enzyme mapping showed that the two proviral clones are proviruses of REV-A and a variant of REV-T, respectively. A subclone of the variant REV-T provirus specific for the rel sequences of REV-T was used as a hybridization probe to demonstrate that the rel sequences are different from the putative transforming sequences of Schmidt-Ruppin Rous sarcoma virus strain A, avain myelocytomatosis virus, avian myeloblastosis virus, avian erythroblastosis virus, Abelson murine leukemia virus, and Friend erythroleukemia virus. In addition, the rel-specific hybridization probe was used to identify a specific set of sequences which are present in uninfected avian DNAs digested with several restriction enzymes. The corresponding cell sequences are not arranged like rel in REV-T.

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Selected References

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  1. Battula N., Temin H. M. Sites of integration of infectious DNA of avian reticuloendotheliosis viruses in different avian cellular DNAs. Cell. 1978 Feb;13(2):387–398. doi: 10.1016/0092-8674(78)90207-6. [DOI] [PubMed] [Google Scholar]
  2. Beug H., von Kirchbach A., Döderlein G., Conscience J. F., Graf T. Chicken hematopoietic cells transformed by seven strains of defective avian leukemia viruses display three distinct phenotypes of differentiation. Cell. 1979 Oct;18(2):375–390. doi: 10.1016/0092-8674(79)90057-6. [DOI] [PubMed] [Google Scholar]
  3. Bister K., Hayman M. J., Vogt P. K. Defectiveness of avian myelocytomatosis virus MC29: isolation of long-term nonproducer cultures and analysis of virus-specific polypeptide synthesis. Virology. 1977 Oct 15;82(2):431–448. doi: 10.1016/0042-6822(77)90017-4. [DOI] [PubMed] [Google Scholar]
  4. Breitman M. L., Lai M. M., Vogt P. K. The genomic RNA of avian reticuloendotheliosis virus REV. Virology. 1980 Jan 30;100(2):450–461. doi: 10.1016/0042-6822(80)90535-8. [DOI] [PubMed] [Google Scholar]
  5. Chen I. S., Temin H. M. Ribonucleotides in unintegrated linear spleen necrosis virus DNA. J Virol. 1980 Mar;33(3):1058–1073. doi: 10.1128/jvi.33.3.1058-1073.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chen J. H. Expression of endogenous avian myeloblastosis virus information in different chicken cells. J Virol. 1980 Oct;36(1):162–170. doi: 10.1128/jvi.36.1.162-170.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cooper G. M., Temin H. M. Infectious rous sarcoma virus and reticuloendotheliosis virus DNAs. J Virol. 1974 Nov;14(5):1132–1141. doi: 10.1128/jvi.14.5.1132-1141.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dale B., Ozanne B. Characterization of mouse cellular deoxyribonucleic acid homologous to Abelson murine leukemia virus-specific sequences. Mol Cell Biol. 1981 Aug;1(8):731–742. doi: 10.1128/mcb.1.8.731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Donoghue D. J., Sharp P. A., Weinberg R. A. An MSV-specific subgenomic mRNA in MSV-transformed G8-124 cells. Cell. 1979 May;17(1):53–63. doi: 10.1016/0092-8674(79)90294-0. [DOI] [PubMed] [Google Scholar]
  11. Feldman R. A., Hanafusa T., Hanafusa H. Characterization of protein kinase activity associated with the transforming gene product of Fujinami sarcoma virus. Cell. 1980 Dec;22(3):757–765. doi: 10.1016/0092-8674(80)90552-8. [DOI] [PubMed] [Google Scholar]
  12. Franchini G., Even J., Sherr C. J., Wong-Staal F. onc sequences (v-fes) of Snyder-Theilen feline sarcoma virus are derived from noncontiguous regions of a cat cellular gene (c-fes). Nature. 1981 Mar 12;290(5802):154–157. doi: 10.1038/290154a0. [DOI] [PubMed] [Google Scholar]
  13. Franklin R. B., Maldonado R. L., Bose H. R. Isolation and characterization of reticuloendotheliosis virus transformed bone marrow cells. Intervirology. 1974;3(5-6):342–352. doi: 10.1159/000149771. [DOI] [PubMed] [Google Scholar]
  14. Fritsch E., Temin H. M. Formation and structure of infectious DNA of spleen necrosis virus. J Virol. 1977 Jan;21(1):119–130. doi: 10.1128/jvi.21.1.119-130.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Goff S. P., Gilboa E., Witte O. N., Baltimore D. Structure of the Abelson murine leukemia virus genome and the homologous cellular gene: studies with cloned viral DNA. Cell. 1980 Dec;22(3):777–785. doi: 10.1016/0092-8674(80)90554-1. [DOI] [PubMed] [Google Scholar]
  16. Gonda M. A., Rice N. R., Gilden R. V. Avian reticuloendotheliosis virus: characterization of the high-molecular-weight viral RNA in transforming and helper virus populations. J Virol. 1980 Jun;34(3):743–751. doi: 10.1128/jvi.34.3.743-751.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gonda T. J., Sheiness D. K., Fanshier L., Bishop J. M., Moscovici C., Moscovici M. G. The genome and the intracellular RNAs of avian myeloblastosis virus. Cell. 1981 Jan;23(1):279–290. doi: 10.1016/0092-8674(81)90292-0. [DOI] [PubMed] [Google Scholar]
  18. Graf T., Beug H. Avian leukemia viruses: interaction with their target cells in vivo and in vitro. Biochim Biophys Acta. 1978 Nov 17;516(3):269–299. doi: 10.1016/0304-419x(78)90011-2. [DOI] [PubMed] [Google Scholar]
  19. Hayman M. J., Royer-Pokora B., Graf T. Defectiveness of avian erythroblastosis virus: synthesis of a 75K gag-related protein. Virology. 1979 Jan 15;92(1):31–45. doi: 10.1016/0042-6822(79)90212-5. [DOI] [PubMed] [Google Scholar]
  20. Hirt B. Selective extraction of polyoma DNA from infected mouse cell cultures. J Mol Biol. 1967 Jun 14;26(2):365–369. doi: 10.1016/0022-2836(67)90307-5. [DOI] [PubMed] [Google Scholar]
  21. Hoelzer J. D., Lewis R. B., Wasmuth C. R., Bose H. R., Jr Hematopoietic cell transformation by reticuloendotheliosis virus: characterization of the genetic defect. Virology. 1980 Jan 30;100(2):462–474. doi: 10.1016/0042-6822(80)90536-x. [DOI] [PubMed] [Google Scholar]
  22. Hu S. S., Lai M. M., Wong T. C., Cohen R. S., Sevoian M. Avian reticuloendotheliosis virus: characterization of genome structure by heteroduplex mapping. J Virol. 1981 Mar;37(3):899–907. doi: 10.1128/jvi.37.3.899-907.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kang C. Y., Temin H. M. Lack of sequence homology among RNAs of avian leukosis-sarcoma viruses, reticuloendotheliosis viruses, and chicken endogenous RNA-directed DNA polymerase activity. J Virol. 1973 Dec;12(6):1314–1324. doi: 10.1128/jvi.12.6.1314-1324.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kang C. Y., Temin H. M. Reticuloendotheliosis virus nucleic acid sequences in cellular DNA. J Virol. 1974 Nov;14(5):1179–1188. doi: 10.1128/jvi.14.5.1179-1188.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Keshet E., O'Rear J. J., Temin H. M. DNA of noninfectious and infectious integrated spleen necrosis virus (SNV) is colinear with unintegrated SNV DNA and not grossly abnormal. Cell. 1979 Jan;16(1):51–61. doi: 10.1016/0092-8674(79)90187-9. [DOI] [PubMed] [Google Scholar]
  26. Keshet E., Temin H. M. Sites of integration of reticuloendotheliosis virus DNA in chicken DNA. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3372–3376. doi: 10.1073/pnas.75.7.3372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nunberg J. H., Kaufman R. J., Chang A. C., Cohen S. N., Schimke R. T. Structure and genomic organization of the mouse dihydrofolate reductase gene. Cell. 1980 Feb;19(2):355–364. doi: 10.1016/0092-8674(80)90510-3. [DOI] [PubMed] [Google Scholar]
  28. O'Rear J. J., Mizutani S., Hoffman G., Fiandt M., Temin H. M. Infectious and noninfectious recombinant clones of the provirus of SNV differ in cellular DNA and are apparently the same in viral DNA. Cell. 1980 Jun;20(2):423–430. doi: 10.1016/0092-8674(80)90628-5. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Oskarsson M., McClements W. L., Blair D. G., Maizel J. V., Vande Woude G. F. Properties of a normal mouse cell DNA sequence (sarc) homologous to the src sequence of Moloney sarcoma virus. Science. 1980 Mar 14;207(4436):1222–1224. doi: 10.1126/science.6243788. [DOI] [PubMed] [Google Scholar]
  31. Reynolds F. H., Jr, Sacks T. L., Deobagkar D. N., Stephenson J. R. Cells nonproductively transformed by Abelson murine leukemia virus express a high molecular weight polyprotein containing structural and nonstructural components. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3974–3978. doi: 10.1073/pnas.75.8.3974. [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. Roussel M., Saule S., Lagrou C., Rommens C., Beug H., Graf T., Stehelin D. Three new types of viral oncogene of cellular origin specific for haematopoietic cell transformation. Nature. 1979 Oct 11;281(5731):452–455. doi: 10.1038/281452a0. [DOI] [PubMed] [Google Scholar]
  34. Sheiness D., Bishop J. M. DNA and RNA from uninfected vertebrate cells contain nucleotide sequences related to the putative transforming gene of avian myelocytomatosis virus. J Virol. 1979 Aug;31(2):514–521. doi: 10.1128/jvi.31.2.514-521.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sheiness D., Vennstrom B., Bishop J. M. Virus-specific RNAs in cells infected by avian myelocytomatosis virus and avian erythroblastosis virus: modes of oncogene expression. Cell. 1981 Jan;23(1):291–300. doi: 10.1016/0092-8674(81)90293-2. [DOI] [PubMed] [Google Scholar]
  36. Shimotohno K., Mizutani S., Temin H. M. Sequence of retrovirus provirus resembles that of bacterial transposable elements. Nature. 1980 Jun 19;285(5766):550–554. doi: 10.1038/285550a0. [DOI] [PubMed] [Google Scholar]
  37. 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]
  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. Spector D. H., Varmus H. E., Bishop J. M. Nucleotide sequences related to the transforming gene of avian sarcoma virus are present in DNA of uninfected vertebrates. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4102–4106. doi: 10.1073/pnas.75.9.4102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Stehelin D., Varmus H. E., Bishop J. M., Vogt P. K. DNA related to the transforming gene(s) of avian sarcoma viruses is present in normal avian DNA. Nature. 1976 Mar 11;260(5547):170–173. doi: 10.1038/260170a0. [DOI] [PubMed] [Google Scholar]
  41. Stephenson J. R., Khan A. S., Sliski A. H., Essex M. Feline oncornavirus-associated cell membrane antigen: evidence for an immunologically crossreactive feline sarcoma virus-coded protein. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5608–5612. doi: 10.1073/pnas.74.12.5608. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Temin H. M., Kassner V. K. Replication of reticuloendotheliosis viruses in cell culture: acute infection. J Virol. 1974 Feb;13(2):291–297. doi: 10.1128/jvi.13.2.291-297.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Theilen G. H., Zeigel R. F., Twiehaus M. J. Biological studies with RE virus (strain T) that induces reticuloendotheliosis in turkeys, chickens, and Japanese quail. J Natl Cancer Inst. 1966 Dec;37(6):731–743. [PubMed] [Google Scholar]
  44. Vennström B., Fanshier L., Moscovici C., Bishop J. M. Molecular cloning of the avian erythroblastosis virus genome and recovery of oncogenic virus by transfection of chicken cells. J Virol. 1980 Nov;36(2):575–585. doi: 10.1128/jvi.36.2.575-585.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Wahli W., Dawid I. B., Wyler T., Weber R., Ryffel G. U. Comparative analysis of the structural organization of two closely related vitellogenin genes in X. laevis. Cell. 1980 May;20(1):107–117. doi: 10.1016/0092-8674(80)90239-1. [DOI] [PubMed] [Google Scholar]
  46. Witte O. N., Rosenberg N., Paskind M., Shields A., Baltimore D. Identification of an Abelson murine leukemia virus-encoded protein present in transformed fibroblast and lymphoid cells. Proc Natl Acad Sci U S A. 1978 May;75(5):2488–2492. doi: 10.1073/pnas.75.5.2488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Wozney J., Hanahan D., Morimoto R., Boedtker H., Doty P. Fine structural analysis of the chicken pro alpha 2 collagen gene. Proc Natl Acad Sci U S A. 1981 Feb;78(2):712–716. doi: 10.1073/pnas.78.2.712. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Yoshida M., Kawai S., Toyoshima K. Unifected avian cells contain structurally unrelated progenitors of viral sarcoma genes. Nature. 1980 Oct 16;287(5783):653–654. doi: 10.1038/287653a0. [DOI] [PubMed] [Google Scholar]

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