Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1982 Apr;42(1):237–252. doi: 10.1128/jvi.42.1.237-252.1982

Genome of Reticuloendotheliosis Virus: Characterization by Use of Cloned Proviral DNA

Nancy R Rice 1, Ronald R Hiebsch 1, Matthew A Gonda 1, Henry R Bose Jr 2, Raymond V Gilden 1
PMCID: PMC256065  PMID: 6283142

Abstract

Reticuloendotheliosis virus is an avian type C retrovirus that is capable of transforming fibroblasts and hematopoietic cells both in vivo and in vitro. This virus is highly related to the three other members of the reticuloendotheliosis virus group, including spleen necrosis virus, but it is apparently unrelated to the avian leukosis-sarcoma virus family. Previous studies have shown that it consists of a replication-competent helper virus (designated REV-A) and a defective component (designated REV) that is responsible for transformation. In this study we used restriction endonuclease mapping and heteroduplex analysis to characterize the proviral DNAs of REV-A and REV. Both producer and nonproducer transformed chicken spleen cells were used as sources of REV proviral DNA; this genome was mapped in detail, and fragments of it were cloned in λgtWES·λB. The infected canine thymus line Cf2Th(REV-A) was used as a source of REV-A proviral DNA. The restriction maps and heteroduplexes of the REV and REV-A genomes showed that (proceeding from 5′ to 3′) (i) REV contains a large fraction of the REV-A gag gene (assuming a gene order of gag-pol-env and gene sizes similar to those of other type C viruses), for the two genomes are very similar over a distance of 2.1 kilobases beginning at their 5′ termini; (ii) most or all of REV-A pol is deleted in REV; (iii) REV contains a 1.1 kilobase segment derived from the 3′ end of REV-A pol or the 5′ end of env or both; (iv) this env region in REV is followed by a 1.9-kilobase segment which is unrelated to REV-A; and (v) the helper-unrelated segment of REV extends essentially all of the way to the beginning of the 3′ long terminal repeat. Therefore, like avian myeloblastosis virus but unlike the other avian acute leukemia viruses and most mammalian and avian sarcoma viruses, REV appears to be an env gene recombinant. We also found that the REV-specific segment is derived from avian DNA, for a cloned REV fragment was able to hybridize with the DNA from an uninfected chicken. Therefore, like the other acute transforming viruses, REV appears to be the product of recombination between a replication-competent virus and host DNA. Two other defective genomes in virus-producing chicken cells were also cloned and characterized. One was very similar to REV in its presumptive gag and env segments, but instead of a host-derived insertion it contained additional env sequences. The second was similar (but not identical) to the first in its gag and env regions and appeared to contain an additional 1-kilobase inversion of REV-A sequences.

Full text

PDF
237

Images in this article

244Image
on p.244
240Image
on p.240
243Image
on p.243
245Image
on p.245
246Image
on p.246
247Image
on p.247
248Image
on p.248
249Image
on p.249

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Andersson P., Goldfarb M. P., Weinberg R. A. A defined subgenomic fragment of in vitro synthesized Moloney sarcoma virus DNA can induce cell transformation upon transfection. Cell. 1979 Jan;16(1):63–75. doi: 10.1016/0092-8674(79)90188-0. [DOI] [PubMed] [Google Scholar]
  2. Barbacid M. Cellular transformation by subgenomic feline sarcoma virus DNA. J Virol. 1981 Jan;37(1):518–523. doi: 10.1128/jvi.37.1.518-523.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bauer G., Temin H. M. Radioimmunological comparison of the DNA polymerases of avian retroviruses. J Virol. 1980 Mar;33(3):1046–1057. doi: 10.1128/jvi.33.3.1046-1057.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. 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]
  6. Chang E. H., Ellis R. W., Scolnick E. M., Lowy D. R. Transformation by cloned Harvey murine sarcoma virus DNA: efficiency increased by long terminal repeat DNA. Science. 1980 Dec 12;210(4475):1249–1251. doi: 10.1126/science.6254153. [DOI] [PubMed] [Google Scholar]
  7. Chen J. H., Hayward W. S., Moscovici C. Size and genetic content of virus-specific RNA in myeloblasts transformed by avian myeloblastosis virus (AMV). Virology. 1981 Apr 15;110(1):128–136. doi: 10.1016/0042-6822(81)90014-3. [DOI] [PubMed] [Google Scholar]
  8. Cohen S. N., Chang A. C., Hsu L. Nonchromosomal antibiotic resistance in bacteria: genetic transformation of Escherichia coli by R-factor DNA. Proc Natl Acad Sci U S A. 1972 Aug;69(8):2110–2114. doi: 10.1073/pnas.69.8.2110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Copeland N. G., Zelenetz A. D., Copper G. M. Transformation by subgenomic fragments of Rous sarcoma virus DNA. Cell. 1980 Apr;19(4):863–870. doi: 10.1016/0092-8674(80)90077-x. [DOI] [PubMed] [Google Scholar]
  10. Duesberg P. H., Bister K., Moscovici C. Genetic structure of avian myeloblastosis virus, released from transformed myeloblasts as a defective virus particle. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5120–5124. doi: 10.1073/pnas.77.9.5120. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Goldfarb M. P., Weinberg R. A. Generation of novel, biologically active Harvey sarcoma viruses via apparent illegitimate recombination. J Virol. 1981 Apr;38(1):136–150. doi: 10.1128/jvi.38.1.136-150.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. 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]
  16. Hoelzer J. D., Franklin R. B., Bose H. R., Jr Transformation by reticuloendotheliosis virus: development of a focus assay and isolation of a nontransforming virus. Virology. 1979 Feb;93(1):20–30. doi: 10.1016/0042-6822(79)90272-1. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Hu S. S., Lai M. M., Vogt P. K. Genome of avian myelocytomatosis virus MC29: analysis by heteroduplex mapping. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1265–1268. doi: 10.1073/pnas.76.3.1265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. 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]
  21. Langridge J., Langridge P., Bergquist P. L. Extraction of nucleic acids from agarose gels. Anal Biochem. 1980 Apr;103(2):264–271. doi: 10.1016/0003-2697(80)90266-3. [DOI] [PubMed] [Google Scholar]
  22. Leder P., Tiemeier D., Enquist L. EK2 derivatives of bacteriophage lambda useful in the cloning of DNA from higher organisms: the lambdagtWES system. Science. 1977 Apr 8;196(4286):175–177. doi: 10.1126/science.322278. [DOI] [PubMed] [Google Scholar]
  23. Lewis R. B., McClure J., Rup B., Niesel D. W., Garry R. F., Hoelzer J. D., Nazerian K., Bose H. R., Jr Avian reticuloendotheliosis virus: identification of the hematopoietic target cell for transformation. Cell. 1981 Aug;25(2):421–431. doi: 10.1016/0092-8674(81)90060-x. [DOI] [PubMed] [Google Scholar]
  24. Maldonado R. L., Bose H. R., Jr Group-specific antigen shared by the members of the reticuloendotheliosis virus complex. J Virol. 1976 Mar;17(3):983–990. doi: 10.1128/jvi.17.3.983-990.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Maniatis T., Hardison R. C., Lacy E., Lauer J., O'Connell C., Quon D., Sim G. K., Efstratiadis A. The isolation of structural genes from libraries of eucaryotic DNA. Cell. 1978 Oct;15(2):687–701. doi: 10.1016/0092-8674(78)90036-3. [DOI] [PubMed] [Google Scholar]
  26. Martin G. S., Radke K., Hughes S., Quintrell N., Bishop J. M., Varmus H. E. Mutants of Rous sarcoma virus with extensive deletions of the viral genome. Virology. 1979 Jul 30;96(2):530–546. doi: 10.1016/0042-6822(79)90109-0. [DOI] [PubMed] [Google Scholar]
  27. 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]
  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. 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]
  30. Purchase H. G., Ludford C., Nazerian K., Cox H. W. A new group of oncogenic viruses: reticuloendotheliosis, chick syncytial, duck infectious anemia, and spleen necrosis viruses. J Natl Cancer Inst. 1973 Aug;51(2):489–499. [PubMed] [Google Scholar]
  31. Purchase H. G., Witter R. L. The reticuloendotheliosis viruses. Curr Top Microbiol Immunol. 1975;71:103–124. doi: 10.1007/978-3-642-66193-8_3. [DOI] [PubMed] [Google Scholar]
  32. Rettenmier C. W., Anderson S. M., Riemen M. W., Hanafusa H. gag-Related polypeptides encoded by replication-defective avian oncoviruses. J Virol. 1979 Dec;32(3):749–761. doi: 10.1128/jvi.32.3.749-761.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. 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]
  34. Sedat J. W., Kelly R. B., Sinsheimer R. L. Fractionation of nucleic acid on benzoylated-naphthoylated DEAE cellulose. J Mol Biol. 1967 Jun 28;26(3):537–540. doi: 10.1016/0022-2836(67)90321-x. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. Shoemaker C., Goff S., Gilboa E., Paskind M., Mitra S. W., Baltimore D. Structure of a cloned circular Moloney murine leukemia virus DNA molecule containing an inverted segment: implications for retrovirus integration. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3932–3936. doi: 10.1073/pnas.77.7.3932. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Simek S., Rice N. R. Analysis of the nucleic acid components in reticuloendotheliosis virus. J Virol. 1980 Jan;33(1):320–329. doi: 10.1128/jvi.33.1.320-329.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. 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]
  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. Sternberg N., Tiemeier D., Enquist L. In vitro packaging of a lambda Dam vector containing EcoRI DNA fragments of Escherichia coli and phage P1. Gene. 1977 May;1(3-4):255–280. doi: 10.1016/0378-1119(77)90049-x. [DOI] [PubMed] [Google Scholar]
  41. Tanaka T., Weisblum B. Construction of a colicin E1-R factor composite plasmid in vitro: means for amplification of deoxyribonucleic acid. J Bacteriol. 1975 Jan;121(1):354–362. doi: 10.1128/jb.121.1.354-362.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wong T. C., Lai M. M. Avian reticuloendotheliosis virus contains a new class of oncogene of turkey origin. Virology. 1981 May;111(1):289–293. doi: 10.1016/0042-6822(81)90674-7. [DOI] [PubMed] [Google Scholar]
  43. Yamamoto K. R., Alberts B. M., Benzinger R., Lawhorne L., Treiber G. Rapid bacteriophage sedimentation in the presence of polyethylene glycol and its application to large-scale virus purification. Virology. 1970 Mar;40(3):734–744. doi: 10.1016/0042-6822(70)90218-7. [DOI] [PubMed] [Google Scholar]
  44. Yang W. K., Kiggans J. O., Yang D. M., Ou C. Y., Tennant R. W., Brown A., Bassin R. H. Synthesis and circularization of N- and B-tropic retroviral DNA Fv-1 permissive and restrictive mouse cells. Proc Natl Acad Sci U S A. 1980 May;77(5):2994–2998. doi: 10.1073/pnas.77.5.2994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Young H. A., Gonda M. A., De Feo D., Ellis R. W., Nagashima K., Scolnick E. M. Heteroduplex analysis of cloned rat endogenous replication-defective (30 S) retrovirus and Harvey murine sarcoma virus. Virology. 1980 Nov;107(1):89–99. doi: 10.1016/0042-6822(80)90275-5. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES