Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1987 Oct;61(10):3266–3275. doi: 10.1128/jvi.61.10.3266-3275.1987

Important role of the long terminal repeat of the helper Moloney murine leukemia virus in Abelson virus-induced lymphoma.

P Savard, L DesGroseillers, E Rassart, Y Poirier, P Jolicoeur
PMCID: PMC255907  PMID: 3041046

Abstract

The helper virus has been shown to play a critical role in the development of lymphoma induced by the defective Abelson murine leukemia virus (A-MuLV). Indeed, A-MuLV pseudotyped with some viruses, such as the Moloney MuLV, has been shown to be highly lymphogenic, whereas A-MuLV pseudotyped with other viruses, such as the BALB/c endogenous N-tropic MuLV, has been shown to be devoid of lymphogenic potential (N. Rosenberg and D. Baltimore, J. Exp. Med. 147:1126-1141, 1978; C. D. Scher, J. Exp. Med. 147: 1044-1053, 1978). To map the viral DNA sequences encoding the determinant of the lymphogenic potential of Moloney MuLV when complexed with A-MuLV, we constructed chimeric helper viral DNA genomes in vitro between parental cloned infectious viral DNA genomes from Moloney MuLV and from BALB/c endogenous N-tropic MuLV. Chimeric helper MuLVs, recovered after transfection of NIH 3T3 cells were used to rescue A-MuLV, and the pseudotypes were inoculated into newborn NIH Swiss, CD-1, and SWR/J mice to test their lymphogenic potential. We found that a 0.44-kilobase-pair PstI-KpnI long terminal repeat-containing fragment from the Moloney MuLV was sufficient to confer some, but not complete, lymphogenic potential to a chimeric virus (p7M2) in NIH Swiss and SWR/J mice, but not in CD-1 mice. The addition of the 3'-end env sequences (comprising the carboxy terminus of gp70 and all p15E) to the U3 long terminal repeat sequences restored the full lymphogenic potential of the Moloney MuLV. Our data indicate that the 3'-end sequences of the helper Moloney MuLV are somehow involved in the development of lymphoma induced by A-MuLV. The same sequences have previously been found to harbor the determinant of leukemogenicity and of disease specificity of Moloney MuLV when inoculated alone.

Full text

PDF
3266

Images in this article

3270Image
on p.3270
3271Image
on p.3271
3272Image
on p.3272

Selected References

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

  1. Abelson H. T., Rabstein L. S. Lymphosarcoma: virus-induced thymic-independent disease in mice. Cancer Res. 1970 Aug;30(8):2213–2222. [PubMed] [Google Scholar]
  2. Alt F. W., Rosenberg N., Casanova R. J., Thomas E., Baltimore D. Immunoglobulin heavy-chain expression and class switching in a murine leukaemia cell line. Nature. 1982 Mar 25;296(5855):325–331. doi: 10.1038/296325a0. [DOI] [PubMed] [Google Scholar]
  3. Boss M., Greaves M., Teich N. Abelson virus-transformed haematopoietic cell lines with pre-B-cell characteristics. Nature. 1979 Apr 5;278(5704):551–553. doi: 10.1038/278551a0. [DOI] [PubMed] [Google Scholar]
  4. Broka C., Hozumi T., Arentzen R., Itakura K. Simplications in the synthesis of short oligonucleotide blocks. Nucleic Acids Res. 1980 Nov 25;8(22):5461–5471. doi: 10.1093/nar/8.22.5461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Caccia N., Kronenberg M., Saxe D., Haars R., Bruns G. A., Goverman J., Malissen M., Willard H., Yoshikai Y., Simon M. The T cell receptor beta chain genes are located on chromosome 6 in mice and chromosome 7 in humans. Cell. 1984 Jul;37(3):1091–1099. doi: 10.1016/0092-8674(84)90443-4. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Cianciolo G. J., Copeland T. D., Oroszlan S., Snyderman R. Inhibition of lymphocyte proliferation by a synthetic peptide homologous to retroviral envelope proteins. Science. 1985 Oct 25;230(4724):453–455. doi: 10.1126/science.2996136. [DOI] [PubMed] [Google Scholar]
  8. Cook W. D. Rapid thymomas induced by Abelson murine leukemia virus. Proc Natl Acad Sci U S A. 1982 May;79(9):2917–2921. doi: 10.1073/pnas.79.9.2917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cory S., Adams J. M., Kemp D. J. Somatic rearrangements forming active immunoglobulin mu genes in B and T lymphoid cell lines. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4943–4947. doi: 10.1073/pnas.77.8.4943. [DOI] [PMC free article] [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., Barrette M., Jolicoeur P. Physical mapping of the paralysis-inducing determinant of a wild mouse ecotropic neurotropic retrovirus. J Virol. 1984 Nov;52(2):356–363. doi: 10.1128/jvi.52.2.356-363.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. DesGroseillers L., Jolicoeur P. Physical mapping of the Fv-1 tropism host range determinant of BALB/c murine leukemia viruses. J Virol. 1983 Dec;48(3):685–696. doi: 10.1128/jvi.48.3.685-696.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. DesGroseillers L., Jolicoeur P. The tandem direct repeats within the long terminal repeat of murine leukemia viruses are the primary determinant of their leukemogenic potential. J Virol. 1984 Dec;52(3):945–952. doi: 10.1128/jvi.52.3.945-952.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Goff S. P., Witte O. N., Gilboa E., Rosenberg N., Baltimore D. Genome structure of Abelson murine leukemia virus variants: proviruses in fibroblasts and lymphoid cells. J Virol. 1981 May;38(2):460–468. doi: 10.1128/jvi.38.2.460-468.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Grunstein M., Hogness D. S. Colony hybridization: a method for the isolation of cloned DNAs that contain a specific gene. Proc Natl Acad Sci U S A. 1975 Oct;72(10):3961–3965. doi: 10.1073/pnas.72.10.3961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hedrick S. M., Germain R. N., Bevan M. J., Dorf M., Engel I., Fink P., Gascoigne N., Heber-Katz E., Kapp J., Kaufmann Y. Rearrangement and transcription of a T-cell receptor beta-chain gene in different T-cell subsets. Proc Natl Acad Sci U S A. 1985 Jan;82(2):531–535. doi: 10.1073/pnas.82.2.531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Herr W., Schwartz D., Gilbert W. Isolation and mapping of cDNA hybridization probes specific for ecotropic and nonecotropic murine leukemia proviruses. Virology. 1983 Feb;125(1):139–154. doi: 10.1016/0042-6822(83)90070-3. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Jolicoeur P., Rosenberg N., Cotellessa A., Baltimore D. Leukemogenicity of clonal isolates of murine leukemia viruses. J Natl Cancer Inst. 1978 Jun;60(6):1473–1476. doi: 10.1093/jnci/60.6.1473. [DOI] [PubMed] [Google Scholar]
  26. Kronenberg M., Goverman J., Haars R., Malissen M., Kraig E., Phillips L., Delovitch T., Suciu-Foca N., Hood L. Rearrangement and transcription of the beta-chain genes of the T-cell antigen receptor in different types of murine lymphocytes. Nature. 1985 Feb 21;313(6004):647–653. doi: 10.1038/313647a0. [DOI] [PubMed] [Google Scholar]
  27. Kurosawa Y., von Boehmer H., Haas W., Sakano H., Trauneker A., Tonegawa S. Identification of D segments of immunoglobulin heavy-chain genes and their rearrangement in T lymphocytes. Nature. 1981 Apr 16;290(5807):565–570. doi: 10.1038/290565a0. [DOI] [PubMed] [Google Scholar]
  28. Laimins L. A., Gruss P., Pozzatti R., Khoury G. Characterization of enhancer elements in the long terminal repeat of Moloney murine sarcoma virus. J Virol. 1984 Jan;49(1):183–189. doi: 10.1128/jvi.49.1.183-189.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lemay G., Jolicoeur P. Rearrangement of a DNA sequence homologous to a cell-virus junction fragment in several Moloney murine leukemia virus-induced rat thymomas. Proc Natl Acad Sci U S A. 1984 Jan;81(1):38–42. doi: 10.1073/pnas.81.1.38. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Levinson B., Khoury G., Vande Woude G., Gruss P. Activation of SV40 genome by 72-base pair tandem repeats of Moloney sarcoma virus. Nature. 1982 Feb 18;295(5850):568–572. doi: 10.1038/295568a0. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. 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]
  34. 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]
  35. Prywes R., Foulkes J. G., Rosenberg N., Baltimore D. Sequences of the A-MuLV protein needed for fibroblast and lymphoid cell transformation. Cell. 1983 Sep;34(2):569–579. doi: 10.1016/0092-8674(83)90389-6. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Risser R. The pathogenesis of Abelson virus lymphomas of the mouse. Biochim Biophys Acta. 1982 Jun 28;651(4):213–244. doi: 10.1016/0304-419x(82)90013-0. [DOI] [PubMed] [Google Scholar]
  38. Rosenberg N., Baltimore D., Scher C. D. In vitro transformation of lymphoid cells by Abelson murine leukemia virus. Proc Natl Acad Sci U S A. 1975 May;72(5):1932–1936. doi: 10.1073/pnas.72.5.1932. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Rosenberg N., Baltimore D. The effect of helper virus on Abelson virus-induced transformation of lymphoid cells. J Exp Med. 1978 Apr 1;147(4):1126–1141. doi: 10.1084/jem.147.4.1126. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sakano H., Maki R., Kurosawa Y., Roeder W., Tonegawa S. Two types of somatic recombination are necessary for the generation of complete immunoglobulin heavy-chain genes. Nature. 1980 Aug 14;286(5774):676–683. doi: 10.1038/286676a0. [DOI] [PubMed] [Google Scholar]
  41. Scher C. D. Effect of pseudotype on Abelson virus and Kirsten sarcoma virus-induced leukemia. J Exp Med. 1978 Apr 1;147(4):1044–1053. doi: 10.1084/jem.147.4.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Scher C. D., Siegler R. Direct transformation of 3T3 cells by Abelson murine leukaemia virus. Nature. 1975 Feb 27;253(5494):729–731. doi: 10.1038/253729a0. [DOI] [PubMed] [Google Scholar]
  43. Scott M. L., Davis M. M., Feinberg M. B. Transformation of T-lymphoid cells by Abelson murine leukemia virus. J Virol. 1986 Aug;59(2):434–443. doi: 10.1128/jvi.59.2.434-443.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Selten G., Cuypers H. T., Zijlstra M., Melief C., Berns A. Involvement of c-myc in MuLV-induced T cell lymphomas in mice: frequency and mechanisms of activation. EMBO J. 1984 Dec 20;3(13):3215–3222. doi: 10.1002/j.1460-2075.1984.tb02281.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. 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]
  46. 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]
  47. Siden E. J., Baltimore D., Clark D., Rosenberg N. E. Immunoglobulin synthesis by lymphoid cells transformed in vitro by Abelson murine leukemia virus. Cell. 1979 Feb;16(2):389–396. doi: 10.1016/0092-8674(79)90014-x. [DOI] [PubMed] [Google Scholar]
  48. 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]
  49. Tsichlis P. N., Strauss P. G., Hu L. F. A common region for proviral DNA integration in MoMuLV-induced rat thymic lymphomas. 1983 Mar 31-Apr 6Nature. 302(5907):445–449. doi: 10.1038/302445a0. [DOI] [PubMed] [Google Scholar]
  50. Villeneuve L., Rassart E., Jolicoeur P., Graham M., Adams J. M. Proviral integration site Mis-1 in rat thymomas corresponds to the pvt-1 translocation breakpoint in murine plasmacytomas. Mol Cell Biol. 1986 May;6(5):1834–1837. doi: 10.1128/mcb.6.5.1834. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Waneck G. L., Rosenberg N. Abelson leukemia virus induces lymphoid and erythroid colonies in infected fetal cell cultures. Cell. 1981 Oct;26(1 Pt 1):79–89. doi: 10.1016/0092-8674(81)90035-0. [DOI] [PubMed] [Google Scholar]
  52. Zoller M. J., Smith M. Oligonucleotide-directed mutagenesis of DNA fragments cloned into M13 vectors. Methods Enzymol. 1983;100:468–500. doi: 10.1016/0076-6879(83)00074-9. [DOI] [PubMed] [Google Scholar]

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

RESOURCES