Skip to main content
The EMBO Journal logoLink to The EMBO Journal
. 1986 Jul;5(7):1615–1623. doi: 10.1002/j.1460-2075.1986.tb04404.x

A transcriptional enhancer with specificity for erythroid cells is located in the long terminal repeat of the Friend murine leukemia virus.

Z Bösze, H J Thiesen, P Charnay
PMCID: PMC1166987  PMID: 3462001

Abstract

We investigated the ability of the U3 region of the long terminal repeats (LTR) of the Friend murine leukemia virus (Fr-MuLV) and Moloney murine leukemia virus (Mo-MuLV) to promote transcription in a variety of human cell lines. Our analysis reveals the presence of a transcriptional enhancer with specificity for erythroid cells in the U3 region of the Fr-MuLV. This constitutes the first example of an enhancer with such a property. Analysis of the Mo-MuLV enhancer suggests that it is active at least in erythroid and lymphoid cells and has thus a less restricted specificity than the Fr-MuLV enhancer. The different tissue specificities of the two enhancers correlate with the different tissue selectivities and pathogenic properties of the two viruses.

Full text

PDF
1617

Images in this article

Selected References

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

  1. Alton N. K., Vapnek D. Nucleotide sequence analysis of the chloramphenicol resistance transposon Tn9. Nature. 1979 Dec 20;282(5741):864–869. doi: 10.1038/282864a0. [DOI] [PubMed] [Google Scholar]
  2. Andersson L. C., Jokinen M., Gahmberg C. G. Induction of erythroid differentiation in the human leukaemia cell line K562. Nature. 1979 Mar 22;278(5702):364–365. doi: 10.1038/278364a0. [DOI] [PubMed] [Google Scholar]
  3. Augereau P., Wasylyk B. The MLV and SV40 enhancers have a similar pattern of transcriptional activation. Nucleic Acids Res. 1984 Dec 11;12(23):8801–8818. doi: 10.1093/nar/12.23.8801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Banerji J., Olson L., Schaffner W. A lymphocyte-specific cellular enhancer is located downstream of the joining region in immunoglobulin heavy chain genes. Cell. 1983 Jul;33(3):729–740. doi: 10.1016/0092-8674(83)90015-6. [DOI] [PubMed] [Google Scholar]
  5. Banerji J., Rusconi S., Schaffner W. Expression of a beta-globin gene is enhanced by remote SV40 DNA sequences. Cell. 1981 Dec;27(2 Pt 1):299–308. doi: 10.1016/0092-8674(81)90413-x. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Charnay P., Maniatis T. Transcriptional regulation of globin gene expression in the human erythroid cell line K562. Science. 1983 Jun 17;220(4603):1281–1283. doi: 10.1126/science.6574602. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. 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]
  10. Ciliberto G., Dente L., Cortese R. Cell-specific expression of a transfected human alpha 1-antitrypsin gene. Cell. 1985 Jun;41(2):531–540. doi: 10.1016/s0092-8674(85)80026-x. [DOI] [PubMed] [Google Scholar]
  11. Clark S. P., Kaufhold R., Chan A., Mak T. W. Comparison of the transcriptional properties of the Friend and Moloney retrovirus long terminal repeats: importance of tandem duplications and of the core enhancer sequence. Virology. 1985 Jul 30;144(2):481–494. doi: 10.1016/0042-6822(85)90288-0. [DOI] [PubMed] [Google Scholar]
  12. D'Onofrio C., Colantuoni V., Cortese R. Structure and cell-specific expression of a cloned human retinol binding protein gene: the 5'-flanking region contains hepatoma specific transcriptional signals. EMBO J. 1985 Aug;4(8):1981–1989. doi: 10.1002/j.1460-2075.1985.tb03881.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Drew S. I., Terasaki P. I., Billing R. J., Bergh O. J., Minowada J., Klein E. Group-specific human granulocyte antigens on a chronic myelogenous leukemia cell line with a Philadelphia chromosome marker. Blood. 1977 May;49(5):715–718. [PubMed] [Google Scholar]
  14. Ephrussi A., Church G. M., Tonegawa S., Gilbert W. B lineage--specific interactions of an immunoglobulin enhancer with cellular factors in vivo. Science. 1985 Jan 11;227(4683):134–140. doi: 10.1126/science.3917574. [DOI] [PubMed] [Google Scholar]
  15. Gillies S. D., Folsom V., Tonegawa S. Cell type-specific enhancer element associated with a mouse MHC gene, E beta. Nature. 1984 Aug 16;310(5978):594–597. doi: 10.1038/310594a0. [DOI] [PubMed] [Google Scholar]
  16. Gillies S. D., Morrison S. L., Oi V. T., Tonegawa S. A tissue-specific transcription enhancer element is located in the major intron of a rearranged immunoglobulin heavy chain gene. Cell. 1983 Jul;33(3):717–728. doi: 10.1016/0092-8674(83)90014-4. [DOI] [PubMed] [Google Scholar]
  17. Gorman C. M., Merlino G. T., Willingham M. C., Pastan I., Howard B. H. The Rous sarcoma virus long terminal repeat is a strong promoter when introduced into a variety of eukaryotic cells by DNA-mediated transfection. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6777–6781. doi: 10.1073/pnas.79.22.6777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Graves B. J., Eisenman R. N., McKnight S. L. Delineation of transcriptional control signals within the Moloney murine sarcoma virus long terminal repeat. Mol Cell Biol. 1985 Aug;5(8):1948–1958. doi: 10.1128/mcb.5.8.1948. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hamada H., Seidman M., Howard B. H., Gorman C. M. Enhanced gene expression by the poly(dT-dG).poly(dC-dA) sequence. Mol Cell Biol. 1984 Dec;4(12):2622–2630. doi: 10.1128/mcb.4.12.2622. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Herbomel P., Bourachot B., Yaniv M. Two distinct enhancers with different cell specificities coexist in the regulatory region of polyoma. Cell. 1984 Dec;39(3 Pt 2):653–662. doi: 10.1016/0092-8674(84)90472-0. [DOI] [PubMed] [Google Scholar]
  22. Hinuma Y., Konn M., Yamaguchi J., Wudarski D. J., Blakeslee J. R., Jr, Grace J. T., Jr Immunofluorescence and herpes-type virus particles in the P3HR-1 Burkitt lymphoma cell line. J Virol. 1967 Oct;1(5):1045–1051. doi: 10.1128/jvi.1.5.1045-1051.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Jolly D. J., Esty A. C., Subramani S., Friedmann T., Verma I. M. Elements in the long terminal repeat of murine retroviruses enhance stable transformation by thymidine kinase gene. Nucleic Acids Res. 1983 Mar 25;11(6):1855–1872. doi: 10.1093/nar/11.6.1855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Klein E., Ben-Bassat H., Neumann H., Ralph P., Zeuthen J., Polliack A., Vánky F. Properties of the K562 cell line, derived from a patient with chronic myeloid leukemia. Int J Cancer. 1976 Oct 15;18(4):421–431. doi: 10.1002/ijc.2910180405. [DOI] [PubMed] [Google Scholar]
  25. Klein G., Zeuthen J., Eriksson I., Terasaki P., Bernoco M., Rosén A., Masucci G., Povey S., Ber R. Hybridization of a myeloid leukemia-derived human cell line (K562) with a human Burkitt's lymphoma line (P3HR-1). J Natl Cancer Inst. 1980 Apr;64(4):725–738. [PubMed] [Google Scholar]
  26. Knowles B. B., Howe C. C., Aden D. P. Human hepatocellular carcinoma cell lines secrete the major plasma proteins and hepatitis B surface antigen. Science. 1980 Jul 25;209(4455):497–499. doi: 10.1126/science.6248960. [DOI] [PubMed] [Google Scholar]
  27. 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]
  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. Laimins L. A., Khoury G., Gorman C., Howard B., Gruss P. Host-specific activation of transcription by tandem repeats from simian virus 40 and Moloney murine sarcoma virus. Proc Natl Acad Sci U S A. 1982 Nov;79(21):6453–6457. doi: 10.1073/pnas.79.21.6453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Linney E., Davis B., Overhauser J., Chao E., Fan H. Non-function of a Moloney murine leukaemia virus regulatory sequence in F9 embryonal carcinoma cells. 1984 Mar 29-Apr 4Nature. 308(5958):470–472. doi: 10.1038/308470a0. [DOI] [PubMed] [Google Scholar]
  31. Lozzio C. B., Lozzio B. B. Human chronic myelogenous leukemia cell-line with positive Philadelphia chromosome. Blood. 1975 Mar;45(3):321–334. [PubMed] [Google Scholar]
  32. Lozzio C. B., Lozzio B. B., Yang W. K., Ichiki A. T., Bamberger E. G. Absence of thymus-derived lymphocyte markers in myelogenous leukemia (Ph1+) cell line K-562. Cancer Res. 1976 Dec;36(12):4657–4662. [PubMed] [Google Scholar]
  33. Martin P., Papayannopoulou T. HEL cells: a new human erythroleukemia cell line with spontaneous and induced globin expression. Science. 1982 Jun 11;216(4551):1233–1235. doi: 10.1126/science.6177045. [DOI] [PubMed] [Google Scholar]
  34. Menezes J., Leibold W., Klein G., Clements G. Establishment and characterization of an Epstein-Barr virus (EBC)-negative lymphoblastoid B cell line (BJA-B) from an exceptional, EBV-genome-negative African Burkitt's lymphoma. Biomedicine. 1975 Jul;22(4):276–284. [PubMed] [Google Scholar]
  35. Mercola M., Goverman J., Mirell C., Calame K. Immunoglobulin heavy-chain enhancer requires one or more tissue-specific factors. Science. 1985 Jan 18;227(4684):266–270. doi: 10.1126/science.3917575. [DOI] [PubMed] [Google Scholar]
  36. Mosthaf L., Pawlita M., Gruss P. A viral enhancer element specifically active in human haematopoietic cells. Nature. 1985 Jun 13;315(6020):597–600. doi: 10.1038/315597a0. [DOI] [PubMed] [Google Scholar]
  37. Neuberger M. S. Expression and regulation of immunoglobulin heavy chain gene transfected into lymphoid cells. EMBO J. 1983;2(8):1373–1378. doi: 10.1002/j.1460-2075.1983.tb01594.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Oliff A., Ruscetti S., Douglass E. C., Scolnick E. Isolation of transplantable erythroleukemia cells from mice infected with helper-independent Friend murine leukemia virus. Blood. 1981 Aug;58(2):244–254. [PubMed] [Google Scholar]
  39. 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]
  40. Papayannopoulou T., Nakamoto B., Yokochi T., Chait A., Kannagi R. Human erythroleukemia cell line (HEL) undergoes a drastic macrophage-like shift with TPA. Blood. 1983 Oct;62(4):832–845. [PubMed] [Google Scholar]
  41. Queen C., Stafford J. Fine mapping of an immunoglobulin gene activator. Mol Cell Biol. 1984 Jun;4(6):1042–1049. doi: 10.1128/mcb.4.6.1042. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Rutherford T. R., Clegg J. B., Weatherall D. J. K562 human leukaemic cells synthesise embryonic haemoglobin in response to haemin. Nature. 1979 Jul 12;280(5718):164–165. doi: 10.1038/280164a0. [DOI] [PubMed] [Google Scholar]
  43. Rutherford T., Clegg J. B., Higgs D. R., Jones R. W., Thompson J., Weatherall D. J. Embryonic erythroid differentiation in the human leukemic cell line K562. Proc Natl Acad Sci U S A. 1981 Jan;78(1):348–352. doi: 10.1073/pnas.78.1.348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Schulze F., Boehnlein E., Gruss P. Mutational analyses of the Moloney murine sarcoma virus enhancer. DNA. 1985 Jun;4(3):193–202. doi: 10.1089/dna.1985.4.193. [DOI] [PubMed] [Google Scholar]
  45. Shaul Y., Rutter W. J., Laub O. A human hepatitis B viral enhancer element. EMBO J. 1985 Feb;4(2):427–430. doi: 10.1002/j.1460-2075.1985.tb03646.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. 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]
  47. Silver J. E., Fredrickson T. N. Susceptibility to Friend helper virus leukemias in CXB recombinant inbred mice. J Exp Med. 1983 Nov 1;158(5):1693–1702. doi: 10.1084/jem.158.5.1693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Tambourin P. E., Wendling F., Jasmin C., Smadja-Joffe F. The physiopathology of Friend leukemia. Leuk Res. 1979;3(3):117–129. doi: 10.1016/0145-2126(79)90009-2. [DOI] [PubMed] [Google Scholar]
  49. Treisman R., Proudfoot N. J., Shander M., Maniatis T. A single-base change at a splice site in a beta 0-thalassemic gene causes abnormal RNA splicing. Cell. 1982 Jul;29(3):903–911. doi: 10.1016/0092-8674(82)90452-4. [DOI] [PubMed] [Google Scholar]
  50. Van Beveren C., Rands E., Chattopadhyay S. K., Lowy D. R., Verma I. M. Long terminal repeat of murine retroviral DNAs: sequence analysis, host-proviral junctions, and preintegration site. J Virol. 1982 Feb;41(2):542–556. doi: 10.1128/jvi.41.2.542-556.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Walker M. D., Edlund T., Boulet A. M., Rutter W. J. Cell-specific expression controlled by the 5'-flanking region of insulin and chymotrypsin genes. Nature. 1983 Dec 8;306(5943):557–561. doi: 10.1038/306557a0. [DOI] [PubMed] [Google Scholar]
  52. Weber F., Schaffner W. Enhancer activity correlates with the oncogenic potential of avian retroviruses. EMBO J. 1985 Apr;4(4):949–956. doi: 10.1002/j.1460-2075.1985.tb03723.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Wolff L., Kaminchik J., Hankins W. D., Ruscetti S. K. Sequence comparisons of the anemia- and polycythemia-inducing strains of Friend spleen focus-forming virus. J Virol. 1985 Feb;53(2):570–578. doi: 10.1128/jvi.53.2.570-578.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Yoshimura F. K., Davison B., Chaffin K. Murine leukemia virus long terminal repeat sequences can enhance gene activity in a cell-type-specific manner. Mol Cell Biol. 1985 Oct;5(10):2832–2835. doi: 10.1128/mcb.5.10.2832. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES