Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1997 Feb;71(2):1196–1206. doi: 10.1128/jvi.71.2.1196-1206.1997

Second-site proviral enhancer alterations in lymphomas induced by enhancer mutants of SL3-3 murine leukemia virus: negative effect of nuclear factor 1 binding site.

S Ethelberg 1, B Hallberg 1, J Lovmand 1, J Schmidt 1, A Luz 1, T Grundström 1, F S Pedersen 1
PMCID: PMC191173  PMID: 8995642

Abstract

SL3-3 is a highly T-lymphomagenic murine retrovirus. Previously, mutation of binding sites in the U3 repeat region for the AML1 transcription factor family (also known as core binding factor [CBF], polyomavirus enhancer binding protein 2 [PEBP2], and SL3-3 enhancer factor 1 [SEF1]) were found to strongly reduce the pathogenicity of SL3-3 (B. Hallberg, J. Schmidt, A. Luz, F. S. Pedersen, and T. Grundström, J. Virol. 65:4177-4181, 1991). We have now examined the few cases in which tumors developed harboring proviruses that besides the AML1 (core) site mutations carried second-site alterations in their U3 repeat structures. In three distinct cases we observed the same type of alteration which involved deletions of regions known to contain binding sites for nuclear factor 1 (NF1) and the addition of extra enhancer repeat elements. In transient-expression experiments in T-lymphoid cells, these new U3 regions acted as stronger enhancers than the U3 regions of the original viruses. This suggests that the altered proviruses represent more-pathogenic variants selected for in the process of tumor formation. To analyze the proviral alterations, we generated a series of different enhancer-promoter reporter constructs. These constructs showed that the additional repeat elements are not critical for enhancer strength, whereas the NF1 sites down-regulate the level of transcription in T-lymphoid cells whether or not the AML1 (core) sites are functional. We therefore also tested SL3-3 viruses with mutated NF1 sites. These viruses have unimpaired pathogenic properties and thereby distinguish SL3-3 from Moloney murine leukemia virus.

Full Text

The Full Text of this article is available as a PDF (243.8 KB).

Selected References

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

  1. Alevizopoulos A., Dusserre Y., Tsai-Pflugfelder M., von der Weid T., Wahli W., Mermod N. A proline-rich TGF-beta-responsive transcriptional activator interacts with histone H3. Genes Dev. 1995 Dec 15;9(24):3051–3066. doi: 10.1101/gad.9.24.3051. [DOI] [PubMed] [Google Scholar]
  2. Apt D., Chong T., Liu Y., Bernard H. U. Nuclear factor I and epithelial cell-specific transcription of human papillomavirus type 16. J Virol. 1993 Aug;67(8):4455–4463. doi: 10.1128/jvi.67.8.4455-4463.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Apt D., Liu Y., Bernard H. U. Cloning and functional analysis of spliced isoforms of human nuclear factor I-X: interference with transcriptional activation by NFI/CTF in a cell-type specific manner. Nucleic Acids Res. 1994 Sep 25;22(19):3825–3833. doi: 10.1093/nar/22.19.3825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bae S. C., Takahashi E., Zhang Y. W., Ogawa E., Shigesada K., Namba Y., Satake M., Ito Y. Cloning, mapping and expression of PEBP2 alpha C, a third gene encoding the mammalian Runt domain. Gene. 1995 Jul 4;159(2):245–248. doi: 10.1016/0378-1119(95)00060-j. [DOI] [PubMed] [Google Scholar]
  5. Bae S. C., Yamaguchi-Iwai Y., Ogawa E., Maruyama M., Inuzuka M., Kagoshima H., Shigesada K., Satake M., Ito Y. Isolation of PEBP2 alpha B cDNA representing the mouse homolog of human acute myeloid leukemia gene, AML1. Oncogene. 1993 Mar;8(3):809–814. [PubMed] [Google Scholar]
  6. Belli B., Patel A., Fan H. Recombinant mink cell focus-inducing virus and long terminal repeat alterations accompany the increased leukemogenicity of the Mo+PyF101 variant of Moloney murine leukemia virus after intraperitoneal inoculation. J Virol. 1995 Feb;69(2):1037–1043. doi: 10.1128/jvi.69.2.1037-1043.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ben-David Y., Bernstein A. Friend virus-induced erythroleukemia and the multistage nature of cancer. Cell. 1991 Sep 6;66(5):831–834. doi: 10.1016/0092-8674(91)90428-2. [DOI] [PubMed] [Google Scholar]
  8. Celander D., Haseltine W. A. Tissue-specific transcription preference as a determinant of cell tropism and leukaemogenic potential of murine retroviruses. Nature. 1984 Nov 8;312(5990):159–162. doi: 10.1038/312159a0. [DOI] [PubMed] [Google Scholar]
  9. Celander D., Hsu B. L., Haseltine W. A. Regulatory elements within the murine leukemia virus enhancer regions mediate glucocorticoid responsiveness. J Virol. 1988 Apr;62(4):1314–1322. doi: 10.1128/jvi.62.4.1314-1322.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chu H. M., Fischer W. H., Osborne T. F., Comb M. J. NF-I proteins from brain interact with the proenkephalin cAMP inducible enhancer. Nucleic Acids Res. 1991 May 25;19(10):2721–2728. doi: 10.1093/nar/19.10.2721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Corneliussen B., Thornell A., Hallberg B., Grundström T. Helix-loop-helix transcriptional activators bind to a sequence in glucocorticoid response elements of retrovirus enhancers. J Virol. 1991 Nov;65(11):6084–6093. doi: 10.1128/jvi.65.11.6084-6093.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Duch M., Paludan K., Jørgensen P., Pedersen F. S. Lack of correlation between basal expression levels and susceptibility to transcriptional shutdown among single-gene murine leukemia virus vector proviruses. J Virol. 1994 Sep;68(9):5596–5601. doi: 10.1128/jvi.68.9.5596-5601.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dusserre Y., Mermod N. Purified cofactors and histone H1 mediate transcription regulation by CTF/NF-I. Ann N Y Acad Sci. 1993 Jun 11;684:230–232. doi: 10.1111/j.1749-6632.1993.tb32294.x. [DOI] [PubMed] [Google Scholar]
  15. Golemis E. A., Speck N. A., Hopkins N. Alignment of U3 region sequences of mammalian type C viruses: identification of highly conserved motifs and implications for enhancer design. J Virol. 1990 Feb;64(2):534–542. doi: 10.1128/jvi.64.2.534-542.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Graves R. A., Tontonoz P., Ross S. R., Spiegelman B. M. Identification of a potent adipocyte-specific enhancer: involvement of an NF-1-like factor. Genes Dev. 1991 Mar;5(3):428–437. doi: 10.1101/gad.5.3.428. [DOI] [PubMed] [Google Scholar]
  17. Hallberg B., Grundström T. Tissue specific sequence motifs in the enhancer of the leukaemogenic mouse retrovirus SL3-3. Nucleic Acids Res. 1988 Jul 11;16(13):5927–5944. doi: 10.1093/nar/16.13.5927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hallberg B., Schmidt J., Luz A., Pedersen F. S., Grundström T. SL3-3 enhancer factor 1 transcriptional activators are required for tumor formation by SL3-3 murine leukemia virus. J Virol. 1991 Aug;65(8):4177–4181. doi: 10.1128/jvi.65.8.4177-4181.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hernandez-Munain C., Krangel M. S. c-Myb and core-binding factor/PEBP2 display functional synergy but bind independently to adjacent sites in the T-cell receptor delta enhancer. Mol Cell Biol. 1995 Jun;15(6):3090–3099. doi: 10.1128/mcb.15.6.3090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ho S. N., Hunt H. D., Horton R. M., Pullen J. K., Pease L. R. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene. 1989 Apr 15;77(1):51–59. doi: 10.1016/0378-1119(89)90358-2. [DOI] [PubMed] [Google Scholar]
  21. Jackson D. A., Rowader K. E., Stevens K., Jiang C., Milos P., Zaret K. S. Modulation of liver-specific transcription by interactions between hepatocyte nuclear factor 3 and nuclear factor 1 binding DNA in close apposition. Mol Cell Biol. 1993 Apr;13(4):2401–2410. doi: 10.1128/mcb.13.4.2401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Johnson P. F., McKnight S. L. Eukaryotic transcriptional regulatory proteins. Annu Rev Biochem. 1989;58:799–839. doi: 10.1146/annurev.bi.58.070189.004055. [DOI] [PubMed] [Google Scholar]
  23. Kruse U., Sippel A. E. The genes for transcription factor nuclear factor I give rise to corresponding splice variants between vertebrate species. J Mol Biol. 1994 May 20;238(5):860–865. doi: 10.1006/jmbi.1994.1343. [DOI] [PubMed] [Google Scholar]
  24. Leib-Mösch C., Schmidt J., Etzerodt M., Pedersen F. S., Hehlmann R., Erfle V. Oncogenic retrovirus from spontaneous murine osteomas. II. Molecular cloning and genomic characterization. Virology. 1986 Apr 15;150(1):96–105. doi: 10.1016/0042-6822(86)90269-2. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Lenz J., Crowther R., Klimenko S., Haseltine W. Molecular cloning of a highly leukemogenic, ecotropic retrovirus from an AKR mouse. J Virol. 1982 Sep;43(3):943–951. doi: 10.1128/jvi.43.3.943-951.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Levanon D., Negreanu V., Bernstein Y., Bar-Am I., Avivi L., Groner Y. AML1, AML2, and AML3, the human members of the runt domain gene-family: cDNA structure, expression, and chromosomal localization. Genomics. 1994 Sep 15;23(2):425–432. doi: 10.1006/geno.1994.1519. [DOI] [PubMed] [Google Scholar]
  28. Li Y., Golemis E., Hartley J. W., Hopkins N. Disease specificity of nondefective Friend and Moloney murine leukemia viruses is controlled by a small number of nucleotides. J Virol. 1987 Mar;61(3):693–700. doi: 10.1128/jvi.61.3.693-700.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Liu P., Tarlé S. A., Hajra A., Claxton D. F., Marlton P., Freedman M., Siciliano M. J., Collins F. S. Fusion between transcription factor CBF beta/PEBP2 beta and a myosin heavy chain in acute myeloid leukemia. Science. 1993 Aug 20;261(5124):1041–1044. doi: 10.1126/science.8351518. [DOI] [PubMed] [Google Scholar]
  30. LoSardo J. E., Boral A. L., Lenz J. Relative importance of elements within the SL3-3 virus enhancer for T-cell specificity. J Virol. 1990 Apr;64(4):1756–1763. doi: 10.1128/jvi.64.4.1756-1763.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lovmand S., Kjeldgaard N. O., Jørgensen P., Pedersen F. S. Enhancer functions in U3 of Akv virus: a role for cooperativity of a tandem repeat unit and its flanking DNA sequences. J Virol. 1990 Jul;64(7):3185–3191. doi: 10.1128/jvi.64.7.3185-3191.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Mermod N., O'Neill E. A., Kelly T. J., Tjian R. The proline-rich transcriptional activator of CTF/NF-I is distinct from the replication and DNA binding domain. Cell. 1989 Aug 25;58(4):741–753. doi: 10.1016/0092-8674(89)90108-6. [DOI] [PubMed] [Google Scholar]
  33. Mink S., Härtig E., Jennewein P., Doppler W., Cato A. C. A mammary cell-specific enhancer in mouse mammary tumor virus DNA is composed of multiple regulatory elements including binding sites for CTF/NFI and a novel transcription factor, mammary cell-activating factor. Mol Cell Biol. 1992 Nov;12(11):4906–4918. doi: 10.1128/mcb.12.11.4906. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Miyoshi H., Kozu T., Shimizu K., Enomoto K., Maseki N., Kaneko Y., Kamada N., Ohki M. The t(8;21) translocation in acute myeloid leukemia results in production of an AML1-MTG8 fusion transcript. EMBO J. 1993 Jul;12(7):2715–2721. doi: 10.1002/j.1460-2075.1993.tb05933.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Morrison H. L., Soni B., Lenz J. Long terminal repeat enhancer core sequences in proviruses adjacent to c-myc in T-cell lymphomas induced by a murine retrovirus. J Virol. 1995 Jan;69(1):446–455. doi: 10.1128/jvi.69.1.446-455.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Nebl G., Mermod N., Cato A. C. Post-transcriptional down-regulation of expression of transcription factor NF1 by Ha-ras oncogene. J Biol Chem. 1994 Mar 11;269(10):7371–7378. [PubMed] [Google Scholar]
  37. Nielsen A. L., Nørby P. L., Pedersen F. S., Jørgensen P. Various modes of basic helix-loop-helix protein-mediated regulation of murine leukemia virus transcription in lymphoid cell lines. J Virol. 1996 Sep;70(9):5893–5901. doi: 10.1128/jvi.70.9.5893-5901.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Nielsen A. L., Pallisgaard N., Pedersen F. S., Jørgensen P. Basic helix-loop-helix proteins in murine type C retrovirus transcriptional regulation. J Virol. 1994 Sep;68(9):5638–5647. doi: 10.1128/jvi.68.9.5638-5647.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Nielsen A. L., Pallisgaard N., Pedersen F. S., Jørgensen P. Murine helix-loop-helix transcriptional activator proteins binding to the E-box motif of the Akv murine leukemia virus enhancer identified by cDNA cloning. Mol Cell Biol. 1992 Aug;12(8):3449–3459. doi: 10.1128/mcb.12.8.3449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Nilsson P., Hallberg B., Thornell A., Grundström T. Mutant analysis of protein interactions with a nuclear factor I binding site in the SL3-3 virus enhancer. Nucleic Acids Res. 1989 Jun 12;17(11):4061–4075. doi: 10.1093/nar/17.11.4061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Nucifora G., Rowley J. D. AML1 and the 8;21 and 3;21 translocations in acute and chronic myeloid leukemia. Blood. 1995 Jul 1;86(1):1–14. [PubMed] [Google Scholar]
  42. Ogawa E., Maruyama M., Kagoshima H., Inuzuka M., Lu J., Satake M., Shigesada K., Ito Y. PEBP2/PEA2 represents a family of transcription factors homologous to the products of the Drosophila runt gene and the human AML1 gene. Proc Natl Acad Sci U S A. 1993 Jul 15;90(14):6859–6863. doi: 10.1073/pnas.90.14.6859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Okuda T., van Deursen J., Hiebert S. W., Grosveld G., Downing J. R. AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell. 1996 Jan 26;84(2):321–330. doi: 10.1016/s0092-8674(00)80986-1. [DOI] [PubMed] [Google Scholar]
  44. Olsen H. S., Lovmand S., Lovmand J., Jørgensen P., Kjeldgaard N. O., Pedersen F. S. Involvement of nuclear factor I-binding sites in control of Akv virus gene expression. J Virol. 1990 Sep;64(9):4152–4161. doi: 10.1128/jvi.64.9.4152-4161.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Paludan K., Dai H. Y., Duch M., Jørgensen P., Kjeldgaard N. O., Pedersen F. S. Different relative expression from two murine leukemia virus long terminal repeats in unintegrated transfected DNA and in integrated retroviral vector proviruses. J Virol. 1989 Dec;63(12):5201–5207. doi: 10.1128/jvi.63.12.5201-5207.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. 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]
  47. Pedersen F. S., Paludan K., Dai H. Y., Duch M., Jørgensen P., Kjeldgaard N. O., Hallberg B., Grundström T., Schmidt J., Luz A. The murine leukemia virus LTR in oncogenesis: effect of point mutations and chromosomal integration sites. Radiat Environ Biophys. 1991;30(3):195–197. doi: 10.1007/BF01226617. [DOI] [PubMed] [Google Scholar]
  48. Plumb M., Fulton R., Breimer L., Stewart M., Willison K., Neil J. C. Nuclear factor 1 activates the feline leukemia virus long terminal repeat but is posttranscriptionally down-regulated in leukemia cell lines. J Virol. 1991 Apr;65(4):1991–1999. doi: 10.1128/jvi.65.4.1991-1999.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Rosen C. A., Haseltine W. A., Lenz J., Ruprecht R., Cloyd M. W. Tissue selectivity of murine leukemia virus infection is determined by long terminal repeat sequences. J Virol. 1985 Sep;55(3):862–866. doi: 10.1128/jvi.55.3.862-866.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Roulet E., Armentero M. T., Krey G., Corthésy B., Dreyer C., Mermod N., Wahli W. Regulation of the DNA-binding and transcriptional activities of Xenopus laevis NFI-X by a novel C-terminal domain. Mol Cell Biol. 1995 Oct;15(10):5552–5562. doi: 10.1128/mcb.15.10.5552. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Rupp R. A., Kruse U., Multhaup G., Göbel U., Beyreuther K., Sippel A. E. Chicken NFI/TGGCA proteins are encoded by at least three independent genes: NFI-A, NFI-B and NFI-C with homologues in mammalian genomes. Nucleic Acids Res. 1990 May 11;18(9):2607–2616. doi: 10.1093/nar/18.9.2607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Speck N. A., Baltimore D. Six distinct nuclear factors interact with the 75-base-pair repeat of the Moloney murine leukemia virus enhancer. Mol Cell Biol. 1987 Mar;7(3):1101–1110. doi: 10.1128/mcb.7.3.1101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Speck N. A., Renjifo B., Golemis E., Fredrickson T. N., Hartley J. W., Hopkins N. Mutation of the core or adjacent LVb elements of the Moloney murine leukemia virus enhancer alters disease specificity. Genes Dev. 1990 Feb;4(2):233–242. doi: 10.1101/gad.4.2.233. [DOI] [PubMed] [Google Scholar]
  54. Speck N. A., Renjifo B., Hopkins N. Point mutations in the Moloney murine leukemia virus enhancer identify a lymphoid-specific viral core motif and 1,3-phorbol myristate acetate-inducible element. J Virol. 1990 Feb;64(2):543–550. doi: 10.1128/jvi.64.2.543-550.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Stoye J. P., Moroni C., Coffin J. M. Virological events leading to spontaneous AKR thymomas. J Virol. 1991 Mar;65(3):1273–1285. doi: 10.1128/jvi.65.3.1273-1285.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Sun W., Graves B. J., Speck N. A. Transactivation of the Moloney murine leukemia virus and T-cell receptor beta-chain enhancers by cbf and ets requires intact binding sites for both proteins. J Virol. 1995 Aug;69(8):4941–4949. doi: 10.1128/jvi.69.8.4941-4949.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Sørensen A. B., Duch M., Amtoft H. W., Jørgensen P., Pedersen F. S. Sequence tags of provirus integration sites in DNAs of tumors induced by the murine retrovirus SL3-3. J Virol. 1996 Jun;70(6):4063–4070. doi: 10.1128/jvi.70.6.4063-4070.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Sørensen A. B., Duch M., Jørgensen P., Pedersen F. S. Amplification and sequence analysis of DNA flanking integrated proviruses by a simple two-step polymerase chain reaction method. J Virol. 1993 Dec;67(12):7118–7124. doi: 10.1128/jvi.67.12.7118-7124.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Thornell A., Hallberg B., Grundström T. Binding of SL3-3 enhancer factor 1 transcriptional activators to viral and chromosomal enhancer sequences. J Virol. 1991 Jan;65(1):42–50. doi: 10.1128/jvi.65.1.42-50.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Thornell A., Hallberg B., Grundström T. Differential protein binding in lymphocytes to a sequence in the enhancer of the mouse retrovirus SL3-3. Mol Cell Biol. 1988 Apr;8(4):1625–1637. doi: 10.1128/mcb.8.4.1625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Tsichlis P. N., Lazo P. A. Virus-host interactions and the pathogenesis of murine and human oncogenic retroviruses. Curr Top Microbiol Immunol. 1991;171:95–171. doi: 10.1007/978-3-642-76524-7_5. [DOI] [PubMed] [Google Scholar]
  62. Wang S., Wang Q., Crute B. E., Melnikova I. N., Keller S. R., Speck N. A. Cloning and characterization of subunits of the T-cell receptor and murine leukemia virus enhancer core-binding factor. Mol Cell Biol. 1993 Jun;13(6):3324–3339. doi: 10.1128/mcb.13.6.3324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Yang B. S., Gilbert J. D., Freytag S. O. Overexpression of Myc suppresses CCAAT transcription factor/nuclear factor 1-dependent promoters in vivo. Mol Cell Biol. 1993 May;13(5):3093–3102. doi: 10.1128/mcb.13.5.3093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Zaiman A. L., Lenz J. Transcriptional activation of a retrovirus enhancer by CBF (AML1) requires a second factor: evidence for cooperativity with c-Myb. J Virol. 1996 Aug;70(8):5618–5629. doi: 10.1128/jvi.70.8.5618-5629.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Zaiman A. L., Lewis A. F., Crute B. E., Speck N. A., Lenz J. Transcriptional activity of core binding factor-alpha (AML1) and beta subunits on murine leukemia virus enhancer cores. J Virol. 1995 May;69(5):2898–2906. doi: 10.1128/jvi.69.5.2898-2906.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. van Lohuizen M., Berns A. Tumorigenesis by slow-transforming retroviruses--an update. Biochim Biophys Acta. 1990 Dec 11;1032(2-3):213–235. doi: 10.1016/0304-419x(90)90005-l. [DOI] [PubMed] [Google Scholar]

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

RESOURCES