Abstract
SL3-3 is a leukemogenic, ecotropic retrovirus produced by a T-cell line derived from a spontaneous lymphoma of an AKR mouse. We have isolated a molecular clone of its DNA provirus from infected NIH 3T3 fibroblasts. Cloned proviral DNA produced infectious virus upon transfection onto NIH 3T3 cells. Virus derived by transfection induced lymphomas at high frequency in AKR/J, C3H(f)/Bi, CBA/J, and NFS/N mice. Heteroduplex and RNase T1 fingerprinting analyses showed that the genomes of SL3-3 and the non-leukemogenic virus, Akv, contain no major substitutions relative to one another and differ by only a few base changes. These results unambiguously show that SL3-3 is a highly leukemogenic virus and that major rearrangements of the genome relative to Akv are not required for virulence.
Full text
PDF








Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- 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]
- 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]
- Buchhagen D. L., Pedersen F. S., Crowther R. L., Haseltine W. A. Most sequence differences between the genomes of the Akv virus and a leukemogenic Gross A virus passaged in vitro are located near the 3' terminus. Proc Natl Acad Sci U S A. 1980 Jul;77(7):4359–4363. doi: 10.1073/pnas.77.7.4359. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Buchhagen D. L., Pincus T., Stutman O., Fleissner E. Leukemogenic activity of murine type C viruses after long-term passage in vitro. Int J Cancer. 1976 Dec 15;18(6):835–842. doi: 10.1002/ijc.2910180616. [DOI] [PubMed] [Google Scholar]
- Chan H. W., Bryan T., Moore J. L., Staal S. P., Rowe W. P., Martin M. A. Identification of ecotropic proviral sequences in inbred mouse strains with a cloned subgenomic DNA fragment. Proc Natl Acad Sci U S A. 1980 Oct;77(10):5779–5783. doi: 10.1073/pnas.77.10.5779. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chattopadhyay S. K., Cloyd M. W., Linemeyer D. L., Lander M. R., Rands E., Lowy D. R. Cellular origin and role of mink cell focus-forming viruses in murine thymic lymphomas. Nature. 1982 Jan 7;295(5844):25–31. doi: 10.1038/295025a0. [DOI] [PubMed] [Google Scholar]
- Chattopadhyay S. K., Lander M. R., Gupta S., Rands E., Lowy D. R. Origin of mink cytopathic focus-forming (MCF) viruses:comparison with ecotropic and xenotropic murine leukemia virus genomes. Virology. 1981 Sep;113(2):465–483. doi: 10.1016/0042-6822(81)90175-6. [DOI] [PubMed] [Google Scholar]
- Chattopadhyay S. K., Lander M. R., Rands E., Lowy D. R. Structure of endogenous murine leukemia virus DNA in mouse genomes. Proc Natl Acad Sci U S A. 1980 Oct;77(10):5774–5778. doi: 10.1073/pnas.77.10.5774. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cloyd M. W., Hartley J. W., Rowe W. P. Lymphomagenicity of recombinant mink cell focus-inducing murine leukemia viruses. J Exp Med. 1980 Mar 1;151(3):542–552. doi: 10.1084/jem.151.3.542. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Copeland N. G., Cooper G. M. Transfection by exogenous and endogenous murine retrovirus DNAs. Cell. 1979 Feb;16(2):347–356. doi: 10.1016/0092-8674(79)90011-4. [DOI] [PubMed] [Google Scholar]
- Elder J. H., Gautsch J. W., Jensen F. C., Lerner R. A., Hartley J. W., Rowe W. P. Biochemical evidence that MCF murine leukemia viruses are envelope (env) gene recombinants. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4676–4680. doi: 10.1073/pnas.74.10.4676. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Famulari N. G., English K. J. Env gene products of AKR dual-tropic viruses: examination of peptide maps and cell surface expression. J Virol. 1981 Dec;40(3):971–976. doi: 10.1128/jvi.40.3.971-976.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- GROSS L. Development and serial cellfree passage of a highly potent strain of mouse leukemia virus. Proc Soc Exp Biol Med. 1957 Apr;94(4):767–771. doi: 10.3181/00379727-94-23080. [DOI] [PubMed] [Google Scholar]
- Hartley J. W., Wolford N. K., Old L. J., Rowe W. P. A new class of murine leukemia virus associated with development of spontaneous lymphomas. Proc Natl Acad Sci U S A. 1977 Feb;74(2):789–792. doi: 10.1073/pnas.74.2.789. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hays E. F., Vredevoe D. L. A discrepancy in XC and oncogenicity assays for murine leukemia virus in AKR mice. Cancer Res. 1977 Mar;37(3):726–730. [PubMed] [Google Scholar]
- Hayward W. S., Neel B. G., Astrin S. M. Activation of a cellular onc gene by promoter insertion in ALV-induced lymphoid leukosis. Nature. 1981 Apr 9;290(5806):475–480. doi: 10.1038/290475a0. [DOI] [PubMed] [Google Scholar]
- Khan A. S., Repaske R., Garon C. F., Chan H. W., Rowe W. P., Martin M. A. Characterization of proviruses cloned from mink cell focus-forming virus-infected cellular DNA. J Virol. 1982 Feb;41(2):435–448. doi: 10.1128/jvi.41.2.435-448.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lee J. C., Ihle J. N. Chronic immune stimulation is required for Moloney leukaemia virus-induced lymphomas. Nature. 1981 Jan 29;289(5796):407–409. doi: 10.1038/289407a0. [DOI] [PubMed] [Google Scholar]
- Lenz J., Crowther R., Straceski A., Haseltine W. Nucleotide sequence of the Akv env gene. J Virol. 1982 May;42(2):519–529. doi: 10.1128/jvi.42.2.519-529.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Linemeyer D. L., Ruscetti S. K., Scolnick E. M., Evans L. H., Duesberg P. H. Biological activity of the spleen focus-forming virus is encoded by a molecularly cloned subgenomic fragment of spleen focus-forming virus DNA. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1401–1405. doi: 10.1073/pnas.78.3.1401. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lowy D. R., Rands E., Chattopadhyay S. K., Garon C. F., Hager G. L. Molecular cloning of infectious integrated murine leukemia virus DNA from infected mouse cells. Proc Natl Acad Sci U S A. 1980 Jan;77(1):614–618. doi: 10.1073/pnas.77.1.614. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lung M. L., Hering C., Hartley J. W., Rowe W. P., Hopkins N. Analysis of the genomes of mink cell focus-inducing murine type-C viruses: a progress report. Cold Spring Harb Symp Quant Biol. 1980;44(Pt 2):1269–1274. doi: 10.1101/sqb.1980.044.01.138. [DOI] [PubMed] [Google Scholar]
- 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]
- McGrath M. S., Weissman I. L. AKR leukemogenesis: identification and biological significance of thymic lymphoma receptors for AKR retroviruses. Cell. 1979 May;17(1):65–75. doi: 10.1016/0092-8674(79)90295-2. [DOI] [PubMed] [Google Scholar]
- Neel B. G., Hayward W. S., Robinson H. L., Fang J., Astrin S. M. Avian leukosis virus-induced tumors have common proviral integration sites and synthesize discrete new RNAs: oncogenesis by promoter insertion. Cell. 1981 Feb;23(2):323–334. doi: 10.1016/0092-8674(81)90128-8. [DOI] [PubMed] [Google Scholar]
- Nowinski R. C., Hays E. F. Oncogenicity of AKR endogenous leukemia viruses. J Virol. 1978 Jul;27(1):13–18. doi: 10.1128/jvi.27.1.13-18.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
- O'Donnell P. V., Stockert E., Obata Y., Old L. J. Leukemogenic properties of AKR dualtropic (MCF) viruses: amplification of murine leukemia virus-related antigens on thymocytes and acceleration of leukemia development in AKR mice. Virology. 1981 Jul 30;112(2):548–563. doi: 10.1016/0042-6822(81)90301-9. [DOI] [PubMed] [Google Scholar]
- Payne G. S., Courtneidge S. A., Crittenden L. B., Fadly A. M., Bishop J. M., Varmus H. E. Analysis of avian leukosis virus DNA and RNA in bursal tumours: viral gene expression is not required for maintenance of the tumor state. Cell. 1981 Feb;23(2):311–322. doi: 10.1016/0092-8674(81)90127-6. [DOI] [PubMed] [Google Scholar]
- Pedersen F. S., Crowther R. L., Hays E. F., Nowinski R. C., Haseltine W. A. Structure of retroviral RNAs produced by cell lines derived from spontaneous lymphomas of AKR mice. J Virol. 1982 Jan;41(1):18–29. doi: 10.1128/jvi.41.1.18-29.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pedersen F. S., Crowther R. L., Tenney D. Y., Reimold A. M., Haseltine W. A. Novel leukaemogenic retroviruses isolated from cell line derived from spontaneous AKR tumour. Nature. 1981 Jul 9;292(5819):167–170. doi: 10.1038/292167a0. [DOI] [PubMed] [Google Scholar]
- Pedersen F. S., Haseltine W. A. Analysis of the genome of an endogenous, ecotropic retrovirus of the AKR strain of mice: micromethod for detailed characterization of high-molecular-weight RNA. J Virol. 1980 Jan;33(1):349–365. doi: 10.1128/jvi.33.1.349-365.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Quint W., Quax W., van der Putten H., Berns A. Characterization of AKR murine leukemia virus sequences in AKR mouse substrains and structure of integrated recombinant genomes in tumor tissues. J Virol. 1981 Jul;39(1):1–10. doi: 10.1128/jvi.39.1.1-10.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Robinson H. L., Pearson M. N., DeSimone D. W., Tsichlis P. N., Coffin J. M. Subgroup-E avian-leukosis-virus-associated disease in chickens. Cold Spring Harb Symp Quant Biol. 1980;44(Pt 2):1133–1141. doi: 10.1101/sqb.1980.044.01.122. [DOI] [PubMed] [Google Scholar]
- Rommelaere J., Faller D. V., Hopkins N. Characterization and mapping of RNase T1-resistant oligonucleotides derived from the genomes of Akv and MCF murine leukemia viruses. Proc Natl Acad Sci U S A. 1978 Jan;75(1):495–499. doi: 10.1073/pnas.75.1.495. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roy-Burman P., Dougherty M., Pal B. K., Charman H. P., Klement V., Gardner M. B. Assay for type C virus in mouse sera based on particulate reverse transcriptase activity. J Virol. 1976 Sep;19(3):1107–1110. doi: 10.1128/jvi.19.3.1107-1110.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tiemeier D. C., Tilghman S. M., Polsky F. I., Seidman J. G., Leder A., Edgell M. H., Leder P. A comparison of two cloned mouse beta-globin genes and their surrounding and intervening sequences. Cell. 1978 Jun;14(2):237–245. doi: 10.1016/0092-8674(78)90110-1. [DOI] [PubMed] [Google Scholar]
- Tsichlis P. N., Coffin J. M. Recombinants between endogenous and exogenous avian tumor viruses: role of the C region and other portions of the genome in the control of replication and transformation. J Virol. 1980 Jan;33(1):238–249. doi: 10.1128/jvi.33.1.238-249.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yoshimura F. K., Breda M. Lack of AKR ecotropic provirus amplification in AKR leukemic thymuses. J Virol. 1981 Sep;39(3):808–815. doi: 10.1128/jvi.39.3.808-815.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]