Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1985 Jul;55(1):184–192. doi: 10.1128/jvi.55.1.184-192.1985

Envelope gene and long terminal repeat determine the different biological properties of Rauscher, Friend, and Moloney mink cell focus-inducing viruses.

M Vogt, C Haggblom, S Swift, M Haas
PMCID: PMC254914  PMID: 4009793

Abstract

The nucleotide sequence of the envelope (env) gene and the long terminal repeat (LTR) of an infectious clone of Rauscher mink cell focus-inducing (R-MCF) virus has been determined and compared with the published env gene and LTR sequences of Friend (F)- and Moloney (M)-MCF viruses. The sequence shows that R-MCF virus, like other MCF viruses, is a recombinant virus. Its env gene contains sequences which were acquired from an env gene in the mouse genome and which confer on the MCF virus its dualtropic host range. Unlike F-MCF and M-MCF viruses, R-MCF virus will not replicate in NIH 3T3 cells. The deduced amino acid sequence for the gp70 of R-MCF differs from that of F- and M-MCF viruses by 15 amino acids between residues 49 and 138 of gp70. These differences in amino acid sequences may be responsible for the inability of R-MCF virus to replicate in NIH 3T3 cells. The host range of two hybrid viruses constructed in vitro is consistent with this hypothesis. R-MCF virus and Friend murine leukemia virus (F-MLV) show 98% identity in their env gene 3' from the acquired env sequences. This contrasts with 82% identity between the env gene of R-MCF virus and M-MLV. The LTR of R-MCF shows 98% identity with the LTR of F-MCF as compared to 88% identity with the LTR of M-MCF. This striking similarity between the sequences of R-MCF, F-MCF, and F-MLV is surprising since the Rauscher virus and the Friend virus are thought to have originated independently. The high degree of similarity suggests that Rauscher and Friend viruses have a common origin. In contrast to M-MLV, which induces predominantly a lymphoid disease, R- and F-MCF viruses induce an erythroproliferative disease in NIH Swiss mice. A hybrid R-MCF virus with a genome derived primarily from R-MCF virus and a 3' end including the U3 region derived from M-MLV induces a lymphoid disease instead of an erythroid disease. This result indicates that it is the U3 region which determines the tissue specificity of the MCF virus-induced disease. It is suggested that the putative viral enhancers in the U3 region play two roles in the process of leukemogenesis: in the Friend and Rauscher disease, the viral enhancers act by increasing the transcription of the MCF env gene; in the thymic lymphoma, the enhancers activate mainly the expression of cellular genes.

Full text

PDF
184

Selected References

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

  1. Adachi A., Sakai K., Kitamura N., Nakanishi S., Niwa O., Matsuyama M., Ishimoto A. Characterization of the env gene and long terminal repeat of molecularly cloned Friend mink cell focus-inducing virus DNA. J Virol. 1984 Jun;50(3):813–821. doi: 10.1128/jvi.50.3.813-821.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bestwick R. K., Boswell B. A., Kabat D. Molecular cloning of biologically active Rauscher spleen focus-forming virus and the sequences of its env gene and long terminal repeat. J Virol. 1984 Sep;51(3):695–705. doi: 10.1128/jvi.51.3.695-705.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Blattner F. R., Blechl A. E., Denniston-Thompson K., Faber H. E., Richards J. E., Slightom J. L., Tucker P. W., Smithies O. Cloning human fetal gamma globin and mouse alpha-type globin DNA: preparation and screening of shotgun collections. Science. 1978 Dec 22;202(4374):1279–1284. doi: 10.1126/science.725603. [DOI] [PubMed] [Google Scholar]
  4. Bosselman R. A., van Straaten F., Van Beveren C., Verma I. M., Vogt M. Analysis of the env gene of a molecularly cloned and biologically active Moloney mink cell focus-forming proviral DNA. J Virol. 1982 Oct;44(1):19–31. doi: 10.1128/jvi.44.1.19-31.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chatis P. A., Holland C. A., Hartley J. W., Rowe W. P., Hopkins N. Role for the 3' end of the genome in determining disease specificity of Friend and Moloney murine leukemia viruses. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4408–4411. doi: 10.1073/pnas.80.14.4408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chatis P. A., Holland C. A., Silver J. E., Frederickson T. N., Hopkins N., Hartley J. W. A 3' end fragment encompassing the transcriptional enhancers of nondefective Friend virus confers erythroleukemogenicity on Moloney leukemia virus. J Virol. 1984 Oct;52(1):248–254. doi: 10.1128/jvi.52.1.248-254.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chesebro B., Wehrly K., Nishio J., Evans L. Leukemia induction by a new strain of Friend mink cell focus-inducing virus: synergistic effect of Friend ecotropic murine leukemia virus. J Virol. 1984 Jul;51(1):63–70. doi: 10.1128/jvi.51.1.63-70.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cloyd M. W. Characterization of target cells for MCF viruses in AKR mice. Cell. 1983 Jan;32(1):217–225. doi: 10.1016/0092-8674(83)90512-3. [DOI] [PubMed] [Google Scholar]
  9. Corcoran L. M., Adams J. M., Dunn A. R., Cory S. Murine T lymphomas in which the cellular myc oncogene has been activated by retroviral insertion. Cell. 1984 May;37(1):113–122. doi: 10.1016/0092-8674(84)90306-4. [DOI] [PubMed] [Google Scholar]
  10. Cuypers H. T., Selten G., Quint W., Zijlstra M., Maandag E. R., Boelens W., van Wezenbeek P., Melief C., Berns A. Murine leukemia virus-induced T-cell lymphomagenesis: integration of proviruses in a distinct chromosomal region. Cell. 1984 May;37(1):141–150. doi: 10.1016/0092-8674(84)90309-x. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  13. FRIEND C. Cell-free transmission in adult Swiss mice of a disease having the character of a leukemia. J Exp Med. 1957 Apr 1;105(4):307–318. doi: 10.1084/jem.105.4.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Habara A., Reddy E. P., Aaronson S. A. Rauscher murine leukemia virus: molecular cloning of infectious integrated proviral DNA. J Virol. 1982 Nov;44(2):731–735. doi: 10.1128/jvi.44.2.731-735.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Ishimoto A., Adachi A., Sakai K., Yorifuji T., Tsuruta S. Rapid emergence of mink cell focus-forming (MCF) virus in various mice infected with NB-tropic friend virus. Virology. 1981 Sep;113(2):644–655. doi: 10.1016/0042-6822(81)90193-8. [DOI] [PubMed] [Google Scholar]
  18. Koch W., Hunsmann G., Friedrich R. Nucleotide sequence of the envelope gene of Friend murine leukemia virus. J Virol. 1983 Jan;45(1):1–9. doi: 10.1128/jvi.45.1.1-9.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Koch W., Zimmermann W., Oliff A., Friedrich R. Molecular analysis of the envelope gene and long terminal repeat of Friend mink cell focus-inducing virus: implications for the functions of these sequences. J Virol. 1984 Mar;49(3):828–840. doi: 10.1128/jvi.49.3.828-840.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Li Y., Holland C. A., Hartley J. W., Hopkins N. Viral integration near c-myc in 10-20% of mcf 247-induced AKR lymphomas. Proc Natl Acad Sci U S A. 1984 Nov;81(21):6808–6811. doi: 10.1073/pnas.81.21.6808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Linemeyer D. L., Menke J. G., Ruscetti S. K., Evans L. H., Scolnick E. M. Envelope gene sequences which encode the gp52 protein of spleen focus-forming virus are required for the induction of erythroid cell proliferation. J Virol. 1982 Jul;43(1):223–233. doi: 10.1128/jvi.43.1.223-233.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  23. Müller R., Müller D. Co-transfection of normal NIH/3T3 DNA and retroval LTR sequences: a novel strategy for the detection of potential c-onc genes. EMBO J. 1984 May;3(5):1121–1127. doi: 10.1002/j.1460-2075.1984.tb01939.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. O'Kunewick J. P., Phillips E. L., Erhard P. Increase in number of splenic transplantable colony-forming units in the SJL-J mice after infection with Rauscher leukemia virus. J Natl Cancer Inst. 1972 Oct;49(4):1101–1106. [PubMed] [Google Scholar]
  25. Oliff A. I., Hager G. L., Chang E. H., Scolnick E. M., Chan H. W., Lowy D. R. Transfection of molecularly cloned Friend murine leukemia virus DNA yields a highly leukemogenic helper-independent type C virus. J Virol. 1980 Jan;33(1):475–486. doi: 10.1128/jvi.33.1.475-486.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Oliff A., Collins L., Mirenda C. Molecular cloning of Friend mink cell focus-inducing virus: identification of mink cell focus-inducing virus-like messages in normal and transformed cells. J Virol. 1983 Nov;48(2):542–546. doi: 10.1128/jvi.48.2.542-546.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. RAUSCHER F. J. A virus-induced disease of mice characterized by erythrocytopoiesis and lymphoid leukemia. J Natl Cancer Inst. 1962 Sep;29:515–543. [PubMed] [Google Scholar]
  29. Ruscetti S., Davis L., Feild J., Oliff A. Friend murine leukemia virus-induced leukemia is associated with the formation of mink cell focus-inducing viruses and is blocked in mice expressing endogenous mink cell focus-inducing xenotropic viral envelope genes. J Exp Med. 1981 Sep 1;154(3):907–920. doi: 10.1084/jem.154.3.907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ruta M., Bestwick R., Machida C., Kabat D. Loss of leukemogenicity caused by mutations in the membrane glycoprotein structural gene of Friend spleen focus-forming virus. Proc Natl Acad Sci U S A. 1983 Aug;80(15):4704–4708. doi: 10.1073/pnas.80.15.4704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Seifert E., Claviez M., Frank H., Hunsmann G., Schwarz H., Schäfer W. XII. Produktion grösserer Mengen von Friend-Virus durch eine permanente Zell-Suspensions-Kultur (Eveline-Suspensions-Zellen) Z Naturforsch C. 1975 Sep-Oct;30(5):698–700. [PubMed] [Google Scholar]
  32. Shinnick T. M., Lerner R. A., Sutcliffe J. G. Nucleotide sequence of Moloney murine leukaemia virus. Nature. 1981 Oct 15;293(5833):543–548. doi: 10.1038/293543a0. [DOI] [PubMed] [Google Scholar]
  33. Steffen D. Proviruses are adjacent to c-myc in some murine leukemia virus-induced lymphomas. Proc Natl Acad Sci U S A. 1984 Apr;81(7):2097–2101. doi: 10.1073/pnas.81.7.2097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Stow N. D., Wilkie N. M. An improved technique for obtaining enhanced infectivity with herpes simplex virus type 1 DNA. J Gen Virol. 1976 Dec;33(3):447–458. doi: 10.1099/0022-1317-33-3-447. [DOI] [PubMed] [Google Scholar]
  35. Troxler D. H., Scolnick E. M. Rapid leukemia induced by cloned friend strain of replicating murine type-C virus. Association with induction of xenotropic-related RNA sequences contained in spleen focus-forming virus. Virology. 1978 Mar;85(1):17–27. doi: 10.1016/0042-6822(78)90408-7. [DOI] [PubMed] [Google Scholar]
  36. Van Beveren C., van Straaten F., Galleshaw J. A., Verma I. M. Nucleotide sequence of the genome of a murine sarcoma virus. Cell. 1981 Nov;27(1 Pt 2):97–108. doi: 10.1016/0092-8674(81)90364-0. [DOI] [PubMed] [Google Scholar]
  37. Vogt M. Properties of "mink cell focus-inducing" (MCF) virus isolated from spontaneous lymphoma lines of BALB/c mice carrying Moloney leukemia virus as an endogenous virus. Virology. 1979 Feb;93(1):226–236. doi: 10.1016/0042-6822(79)90290-3. [DOI] [PubMed] [Google Scholar]
  38. Vogt M. Virus cloned from the Rauscher virus complex induces erythroblastosis and thymic lymphoma. Virology. 1982 Apr 15;118(1):225–228. doi: 10.1016/0042-6822(82)90336-1. [DOI] [PubMed] [Google Scholar]
  39. van Griensven L. J., Vogt M. Rauscher "mink cell focus-inducing" (MCF) virus causes erythroleukemia in mice: its isolation and properties. Virology. 1980 Mar;101(2):376–388. doi: 10.1016/0042-6822(80)90451-1. [DOI] [PubMed] [Google Scholar]

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

RESOURCES