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. 1992 Aug;66(8):5141–5146. doi: 10.1128/jvi.66.8.5141-5146.1992

Determinants of thymotropism in Kaplan radiation leukemia virus and nucleotide sequence of its envelope region.

L Poliquin 1, D Bergeron 1, J L Fortier 1, Y Paquette 1, R Bergeron 1, E Rassart 1
PMCID: PMC241391  PMID: 1629969

Abstract

Radiation leukemia viruses (RadLVs) are a group of murine leukemia viruses which are induced by radiation and cause T-cell leukemia. Viral clones isolated from the BL/VL3 lymphoid cell line derived from a thymoma show variable tropism and leukemogenic potential. We have constructed chimeric viruses by in vitro recombination between two viruses, a RadLV that is thymotropic and an endogenous ecotropic virus that is nonthymotropic. We show here that, in contrast to thymotropism determinants identified previously, which lie in the long terminal repeat (LTR), it is the envelope region that is responsible for the thymotropism of BL/VL3 RadLV. The nonthymotropic virus which we have rendered thymotropic by transfer of the env region of RadLV in the present study has been shown previously to become thymotropic when the LTR of another thymotropic virus is inserted in its genome. Thus, the LTR and envelope gene may be involved in complementary action to lead to thymotropism.

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Selected References

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  1. 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]
  2. Cloyd M. W., Hartley J. W., Rowe W. P. Genetic study of lymphoma induction by AKR mink cell focus-inducing virus in AKR x NFS crosses. J Exp Med. 1981 Aug 1;154(2):450–457. doi: 10.1084/jem.154.2.450. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Declève A., Lieberman M., Ihle J. N., Rosenthal P. N., Lung M. L., Kaplan H. S. Physicochemical, biological and serological properties of a leukemogenic virus isolated from cultured RadLV-induced lymphomas of C57BL/Ka mice. Virology. 1978 Oct 1;90(1):23–35. doi: 10.1016/0042-6822(78)90329-x. [DOI] [PubMed] [Google Scholar]
  4. Declève A., Sato C., Lieberman M., Kaplan H. S. Selective thymic localization of murine leukemia virus-related antigens in C57BL-Ka mice after inoculation with radiation virus. Proc Natl Acad Sci U S A. 1974 Aug;71(8):3124–3128. doi: 10.1073/pnas.71.8.3124. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. DesGroseillers L., Jolicoeur P. Mapping the viral sequences conferring leukemogenicity and disease specificity in Moloney and amphotropic murine leukemia viruses. J Virol. 1984 Nov;52(2):448–456. doi: 10.1128/jvi.52.2.448-456.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. DesGroseillers L., Rassart E., Jolicoeur P. Thymotropism of murine leukemia virus is conferred by its long terminal repeat. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4203–4207. doi: 10.1073/pnas.80.14.4203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. DesGroseillers L., Villemur R., Jolicoeur P. The high leukemogenic potential of Gross passage A murine leukemia virus maps in the region of the genome corresponding to the long terminal repeat and to the 3' end of env. J Virol. 1983 Jul;47(1):24–32. doi: 10.1128/jvi.47.1.24-32.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fowlkes B. J., Pardoll D. M. Molecular and cellular events of T cell development. Adv Immunol. 1989;44:207–264. doi: 10.1016/s0065-2776(08)60643-4. [DOI] [PubMed] [Google Scholar]
  9. Herr W., Gilbert W. Somatically acquired recombinant murine leukemia proviruses in thymic leukemias of AKR/J mice. J Virol. 1983 Apr;46(1):70–82. doi: 10.1128/jvi.46.1.70-82.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Herr W. Nucleotide sequence of AKV murine leukemia virus. J Virol. 1984 Feb;49(2):471–478. doi: 10.1128/jvi.49.2.471-478.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Holland C. A., Hartley J. W., Rowe W. P., Hopkins N. At least four viral genes contribute to the leukemogenicity of murine retrovirus MCF 247 in AKR mice. J Virol. 1985 Jan;53(1):158–165. doi: 10.1128/jvi.53.1.158-165.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Holland C. A., Thomas C. Y., Chattopadhyay S. K., Koehne C., O'Donnell P. V. Influence of enhancer sequences on thymotropism and leukemogenicity of mink cell focus-forming viruses. J Virol. 1989 Mar;63(3):1284–1292. doi: 10.1128/jvi.63.3.1284-1292.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Holland C. A., Wozney J., Chatis P. A., Hopkins N., Hartley J. W. Construction of recombinants between molecular clones of murine retrovirus MCF 247 and Akv: determinant of an in vitro host range property that maps in the long terminal repeat. J Virol. 1985 Jan;53(1):152–157. doi: 10.1128/jvi.53.1.152-157.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Janowski M., Merregaert J., Boniver J., Maisin J. R. Proviral genome of radiation leukemia virus: molecular cloning of biologically active proviral DNA and nucleotide sequence of its long terminal repeat. J Virol. 1985 Jul;55(1):251–255. doi: 10.1128/jvi.55.1.251-255.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jolicoeur P., DesGroseillers L. Neurotropic Cas-BR-E murine leukemia virus harbors several determinants of leukemogenicity mapping in different regions of the genome. J Virol. 1985 Nov;56(2):639–643. doi: 10.1128/jvi.56.2.639-643.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jolicoeur P., Rassart E. Effect of Fv-1 gene product on synthesis of linear and supercoiled viral DNA in cells infected with murine leukemia virus. J Virol. 1980 Jan;33(1):183–195. doi: 10.1128/jvi.33.1.183-195.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. KAPLAN H. S. THE ROLE OF RADIATION ON EXPERIMENTAL LEUKEMOGENESIS. Natl Cancer Inst Monogr. 1964 May;14:207–220. [PubMed] [Google Scholar]
  18. Kaplan H. S. On the natural history of the murine leukemias: presidential address. Cancer Res. 1967 Aug;27(8):1325–1340. [PubMed] [Google Scholar]
  19. Lenz J., Celander D., Crowther R. L., Patarca R., Perkins D. W., Haseltine W. A. Determination of the leukaemogenicity of a murine retrovirus by sequences within the long terminal repeat. 1984 Mar 29-Apr 4Nature. 308(5958):467–470. doi: 10.1038/308467a0. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Levin J. G., Hu S. C., Rein A., Messer L. I., Gerwin B. I. Murine leukemia virus mutant with a frameshift in the reverse transcriptase coding region: implications for pol gene structure. J Virol. 1984 Aug;51(2):470–478. doi: 10.1128/jvi.51.2.470-478.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lieberman M., Declève A., Kaplan H. S. Rapid in vitro assay for thymotropic, leukemogenic murine C-type RNA viruses. Virology. 1978 Oct 15;90(2):274–278. doi: 10.1016/0042-6822(78)90311-2. [DOI] [PubMed] [Google Scholar]
  23. Lieberman M., Declève A., Ricciardi-Castagnoli P., Boniver J., Finn O. J., Kaplan H. S. Establishment, characterization and virus expression of cell lines derived from radiation- and virus-induced lymphomas of C57BL/Ka mice. Int J Cancer. 1979 Aug;24(2):168–177. doi: 10.1002/ijc.2910240208. [DOI] [PubMed] [Google Scholar]
  24. Lieberman M., Niwa O., Declève A., Kaplan H. S. Continuous propagation of radiation leukemia virus on a C57BL mouse-embryo fibroblast line, with attenuation of leukemogenic activity. Proc Natl Acad Sci U S A. 1973 Apr;70(4):1250–1253. doi: 10.1073/pnas.70.4.1250. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Merregaert J., Nuyten J. M., Janowski M. Nucleotide sequence of the envelope gene of radiation leukemia virus. Virology. 1985 Jul 30;144(2):457–467. doi: 10.1016/0042-6822(85)90286-7. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. O'Neill H. C. Binding of the BL/VL3 murine T cell lymphoma to radiation leukaemia virus is specific for viral env determinants. J Gen Virol. 1991 Jul;72(Pt 7):1725–1728. doi: 10.1099/0022-1317-72-7-1725. [DOI] [PubMed] [Google Scholar]
  28. Oliff A., McKinney M. D., Agranovsky O. Contribution of the gag and pol sequences to the leukemogenicity of Friend murine leukemia virus. J Virol. 1985 Jun;54(3):864–868. doi: 10.1128/jvi.54.3.864-868.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Oliff A., Signorelli K., Collins L. The envelope gene and long terminal repeat sequences contribute to the pathogenic phenotype of helper-independent Friend viruses. J Virol. 1984 Sep;51(3):788–794. doi: 10.1128/jvi.51.3.788-794.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Potter H., Weir L., Leder P. Enhancer-dependent expression of human kappa immunoglobulin genes introduced into mouse pre-B lymphocytes by electroporation. Proc Natl Acad Sci U S A. 1984 Nov;81(22):7161–7165. doi: 10.1073/pnas.81.22.7161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rassart E., Jolicoeur P. Restriction analysis and molecular cloning of endogenous murine leukemia virus-specific DNA sequences of the mouse genome. Virology. 1982 Nov;123(1):175–186. doi: 10.1016/0042-6822(82)90304-x. [DOI] [PubMed] [Google Scholar]
  32. Rassart E., Paquette Y., Jolicoeur P. Inability of Kaplan radiation leukemia virus to replicate on mouse fibroblasts is conferred by its long terminal repeat. J Virol. 1988 Oct;62(10):3840–3848. doi: 10.1128/jvi.62.10.3840-3848.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Rassart E., Sankar-Mistry P., Lemay G., DesGroseillers L., Jolicoeur P. New class of leukemogenic ecotropic recombinant murine leukemia virus isolated from radiation-induced thymomas of C57BL/6 mice. J Virol. 1983 Feb;45(2):565–575. doi: 10.1128/jvi.45.2.565-575.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rassart E., Shang M., Boie Y., Jolicoeur P. Studies on emerging radiation leukemia virus variants in C57BL/Ka mice. J Virol. 1986 Apr;58(1):96–106. doi: 10.1128/jvi.58.1.96-106.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Ruscetti S., Wolff L. Spleen focus-forming virus: relationship of an altered envelope gene to the development of a rapid erythroleukemia. Curr Top Microbiol Immunol. 1984;112:21–44. doi: 10.1007/978-3-642-69677-0_2. [DOI] [PubMed] [Google Scholar]
  36. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Schwartzberg P., Colicelli J., Goff S. P. Construction and analysis of deletion mutations in the pol gene of Moloney murine leukemia virus: a new viral function required for productive infection. Cell. 1984 Jul;37(3):1043–1052. doi: 10.1016/0092-8674(84)90439-2. [DOI] [PubMed] [Google Scholar]
  38. Vogt M., Haggblom C., Swift S., Haas M. Envelope gene and long terminal repeat determine the different biological properties of Rauscher, Friend, and Moloney mink cell focus-inducing viruses. J Virol. 1985 Jul;55(1):184–192. doi: 10.1128/jvi.55.1.184-192.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]

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