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. 1994 Sep;68(9):5845–5853. doi: 10.1128/jvi.68.9.5845-5853.1994

Involvement of the cyclic AMP-responsive element binding protein in bovine leukemia virus expression in vivo.

E Adam 1, P Kerkhofs 1, M Mammerickx 1, R Kettmann 1, A Burny 1, L Droogmans 1, L Willems 1
PMCID: PMC236989  PMID: 8057465

Abstract

The TAR element (Tax-responsive element; also called TxRE) is a major determinant of the regulation of bovine leukemia virus (BLV) expression. In order to gain insight into the mechanisms of viral expression, complexes formed between proteins and the TAR enhancer DNA were analyzed by gel retardation assays. We report here that nuclear lysates from ex vivo-isolated B lymphocytes contain proteins that specifically bind to TAR. An antibody directed toward the cyclic AMP-responsive element binding (CREB) protein supershifted a complex (C1) present only in BLV-infected B lymphocytes. The CREB protein thus appears to be a major transcription factor involved in BLV expression in vivo.

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Selected References

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

  1. Angel P., Imagawa M., Chiu R., Stein B., Imbra R. J., Rahmsdorf H. J., Jonat C., Herrlich P., Karin M. Phorbol ester-inducible genes contain a common cis element recognized by a TPA-modulated trans-acting factor. Cell. 1987 Jun 19;49(6):729–739. doi: 10.1016/0092-8674(87)90611-8. [DOI] [PubMed] [Google Scholar]
  2. Armstrong A. P., Franklin A. A., Uittenbogaard M. N., Giebler H. A., Nyborg J. K. Pleiotropic effect of the human T-cell leukemia virus Tax protein on the DNA binding activity of eukaryotic transcription factors. Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7303–7307. doi: 10.1073/pnas.90.15.7303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baliga V., Ferrer J. F. Expression of the bovine leukemia virus and its internal antigen in blood lymphocytes. Proc Soc Exp Biol Med. 1977 Nov;156(2):388–391. doi: 10.3181/00379727-156-39942. [DOI] [PubMed] [Google Scholar]
  4. Beimling P., Moelling K. Direct interaction of CREB protein with 21 bp Tax-response elements of HTLV-ILTR. Oncogene. 1992 Feb;7(2):257–262. [PubMed] [Google Scholar]
  5. Castagna M., Takai Y., Kaibuchi K., Sano K., Kikkawa U., Nishizuka Y. Direct activation of calcium-activated, phospholipid-dependent protein kinase by tumor-promoting phorbol esters. J Biol Chem. 1982 Jul 10;257(13):7847–7851. [PubMed] [Google Scholar]
  6. Cockerell G. L., Rovnak J. The correlation between the direct and indirect detection of bovine leukemia virus infection in cattle. Leuk Res. 1988;12(6):465–469. doi: 10.1016/0145-2126(88)90112-9. [DOI] [PubMed] [Google Scholar]
  7. Derse D. Bovine leukemia virus transcription is controlled by a virus-encoded trans-acting factor and by cis-acting response elements. J Virol. 1987 Aug;61(8):2462–2471. doi: 10.1128/jvi.61.8.2462-2471.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Derse D., Diniak A. J., Casey J. W., Deininger P. L. Nucleotide sequence and structure of integrated bovine leukemia virus long terminal repeats. Virology. 1985 Feb;141(1):162–166. doi: 10.1016/0042-6822(85)90193-x. [DOI] [PubMed] [Google Scholar]
  9. Deschamps J., Kettmann R., Burny A. Experiments with cloned complete tumor-derived bovine leukemia virus information prove that the virus is totally exogenous to its target animal species. J Virol. 1981 Nov;40(2):605–609. doi: 10.1128/jvi.40.2.605-609.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Esteban E. N., Thorn R. M., Ferrer J. F. Characterization of the blood lymphocyte population in cattle infected with the bovine leukemia virus. Cancer Res. 1985 Jul;45(7):3225–3230. [PubMed] [Google Scholar]
  11. Ferrer J. F., Marshak R. R., Abt D. A., Kenyon S. J. Relationship between lymphosarcoma and persistent lymphocytosis in cattle: a review. J Am Vet Med Assoc. 1979 Oct 1;175(7):705–708. [PubMed] [Google Scholar]
  12. Gonzalez G. A., Montminy M. R. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell. 1989 Nov 17;59(4):675–680. doi: 10.1016/0092-8674(89)90013-5. [DOI] [PubMed] [Google Scholar]
  13. Gupta P., Ferrer J. F. Expression of bovine leukemia virus genome is blocked by a nonimmunoglobulin protein in plasma from infected cattle. Science. 1982 Jan 22;215(4531):405–407. doi: 10.1126/science.6276975. [DOI] [PubMed] [Google Scholar]
  14. Gupta P., Kashmiri S. V., Ferrer J. F. Transcriptional control of the bovine leukemia virus genome: role and characterization of a non-immunoglobulin plasma protein from bovine leukemia virus-infected cattle. J Virol. 1984 Apr;50(1):267–270. doi: 10.1128/jvi.50.1.267-270.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hai T. W., Liu F., Allegretto E. A., Karin M., Green M. R. A family of immunologically related transcription factors that includes multiple forms of ATF and AP-1. Genes Dev. 1988 Oct;2(10):1216–1226. doi: 10.1101/gad.2.10.1216. [DOI] [PubMed] [Google Scholar]
  16. Hardy S., Shenk T. Adenoviral control regions activated by E1A and the cAMP response element bind to the same factor. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4171–4175. doi: 10.1073/pnas.85.12.4171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jensen W. A., Wicks-Beard B. J., Cockerell G. L. Inhibition of protein kinase C results in decreased expression of bovine leukemia virus. J Virol. 1992 Jul;66(7):4427–4433. doi: 10.1128/jvi.66.7.4427-4433.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kara C. J., Liou H. C., Ivashkiv L. B., Glimcher L. H. A cDNA for a human cyclic AMP response element-binding protein which is distinct from CREB and expressed preferentially in brain. Mol Cell Biol. 1990 Apr;10(4):1347–1357. doi: 10.1128/mcb.10.4.1347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Katoh I., Yoshinaka Y., Ikawa Y. Bovine leukemia virus trans-activator p38tax activates heterologous promoters with a common sequence known as a cAMP-responsive element or the binding site of a cellular transcription factor ATF. EMBO J. 1989 Feb;8(2):497–503. doi: 10.1002/j.1460-2075.1989.tb03403.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kettmann R., Cleuter Y., Mammerickx M., Meunier-Rotival M., Bernardi G., Burny A., Chantrenne H. Genomic integration of bovine leukemia provirus: comparison of persistent lymphocytosis with lymph node tumor form of enzootic. Proc Natl Acad Sci U S A. 1980 May;77(5):2577–2581. doi: 10.1073/pnas.77.5.2577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kettmann R., Deschamps J., Cleuter Y., Couez D., Burny A., Marbaix G. Leukemogenesis by bovine leukemia virus: proviral DNA integration and lack of RNA expression of viral long terminal repeat and 3' proximate cellular sequences. Proc Natl Acad Sci U S A. 1982 Apr;79(8):2465–2469. doi: 10.1073/pnas.79.8.2465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kettmann R., Marbaix G., Cleuter Y., Portetelle D., Mammerickx M., Burny A. Genomic integration of bovine leukemia provirus and lack of viral RNA expression in the target cells of cattle with different responses to BLV infection. Leuk Res. 1980;4(6):509–519. doi: 10.1016/0145-2126(80)90062-4. [DOI] [PubMed] [Google Scholar]
  23. Lagarias D. M., Radke K. Transcriptional activation of bovine leukemia virus in blood cells from experimentally infected, asymptomatic sheep with latent infections. J Virol. 1989 May;63(5):2099–2107. doi: 10.1128/jvi.63.5.2099-2107.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lee W., Mitchell P., Tjian R. Purified transcription factor AP-1 interacts with TPA-inducible enhancer elements. Cell. 1987 Jun 19;49(6):741–752. doi: 10.1016/0092-8674(87)90612-x. [DOI] [PubMed] [Google Scholar]
  25. Lin Y. S., Green M. R. Interaction of a common cellular transcription factor, ATF, with regulatory elements in both E1a- and cyclic AMP-inducible promoters. Proc Natl Acad Sci U S A. 1988 May;85(10):3396–3400. doi: 10.1073/pnas.85.10.3396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Marriott S. J., Lindholm P. F., Brown K. M., Gitlin S. D., Duvall J. F., Radonovich M. F., Brady J. N. A 36-kilodalton cellular transcription factor mediates an indirect interaction of human T-cell leukemia/lymphoma virus type I TAX1 with a responsive element in the viral long terminal repeat. Mol Cell Biol. 1990 Aug;10(8):4192–4201. doi: 10.1128/mcb.10.8.4192. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Miller L. D., Miller J. M., Olson C. Inoculation of calves with particles resembling C-type virus from cultures of bovine lymphosarcoma. J Natl Cancer Inst. 1972 Feb;48(2):423–428. [PubMed] [Google Scholar]
  28. Montminy M. R., Bilezikjian L. M. Binding of a nuclear protein to the cyclic-AMP response element of the somatostatin gene. Nature. 1987 Jul 9;328(6126):175–178. doi: 10.1038/328175a0. [DOI] [PubMed] [Google Scholar]
  29. Nakabeppu Y., Ryder K., Nathans D. DNA binding activities of three murine Jun proteins: stimulation by Fos. Cell. 1988 Dec 2;55(5):907–915. doi: 10.1016/0092-8674(88)90146-8. [DOI] [PubMed] [Google Scholar]
  30. Nakamura M., Niki M., Ohtani K., Sugamura K. Differential activation of the 21-base-pair enhancer element of human T-cell leukemia virus type I by its own trans-activator and cyclic AMP. Nucleic Acids Res. 1989 Jul 11;17(13):5207–5221. doi: 10.1093/nar/17.13.5207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Portetelle D., Mammerickx M., Burny A. Use of two monoclonal antibodies in an ELISA test for the detection of antibodies to bovine leukaemia virus envelope protein gp51. J Virol Methods. 1989 Feb;23(2):211–222. doi: 10.1016/0166-0934(89)90135-3. [DOI] [PubMed] [Google Scholar]
  32. Roesler W. J., Vandenbark G. R., Hanson R. W. Cyclic AMP and the induction of eukaryotic gene transcription. J Biol Chem. 1988 Jul 5;263(19):9063–9066. [PubMed] [Google Scholar]
  33. Sagata N., Yasunaga T., Ogawa Y., Tsuzuku-Kawamura J., Ikawa Y. Bovine leukemia virus: unique structural features of its long terminal repeats and its evolutionary relationship to human T-cell leukemia virus. Proc Natl Acad Sci U S A. 1984 Aug;81(15):4741–4745. doi: 10.1073/pnas.81.15.4741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sagata N., Yasunaga T., Tsuzuku-Kawamura J., Ohishi K., Ogawa Y., Ikawa Y. Complete nucleotide sequence of the genome of bovine leukemia virus: its evolutionary relationship to other retroviruses. Proc Natl Acad Sci U S A. 1985 Feb;82(3):677–681. doi: 10.1073/pnas.82.3.677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sassone-Corsi P., Ransone L. J., Verma I. M. Cross-talk in signal transduction: TPA-inducible factor jun/AP-1 activates cAMP-responsive enhancer elements. Oncogene. 1990 Mar;5(3):427–431. [PubMed] [Google Scholar]
  36. Seamon K. B., Daly J. W. Forskolin: its biological and chemical properties. Adv Cyclic Nucleotide Protein Phosphorylation Res. 1986;20:1–150. [PubMed] [Google Scholar]
  37. Singh H., LeBowitz J. H., Baldwin A. S., Jr, Sharp P. A. Molecular cloning of an enhancer binding protein: isolation by screening of an expression library with a recognition site DNA. Cell. 1988 Feb 12;52(3):415–423. doi: 10.1016/s0092-8674(88)80034-5. [DOI] [PubMed] [Google Scholar]
  38. Stock N. D., Ferrer J. F. Replicating C-type virus in phytohemagglutinin-treated buffy-coat cultures of bovine origin. J Natl Cancer Inst. 1972 Apr;48(4):985–996. [PubMed] [Google Scholar]
  39. Suzuki T., Fujisawa J. I., Toita M., Yoshida M. The trans-activator tax of human T-cell leukemia virus type 1 (HTLV-1) interacts with cAMP-responsive element (CRE) binding and CRE modulator proteins that bind to the 21-base-pair enhancer of HTLV-1. Proc Natl Acad Sci U S A. 1993 Jan 15;90(2):610–614. doi: 10.1073/pnas.90.2.610. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Tan T. H., Horikoshi M., Roeder R. G. Purification and characterization of multiple nuclear factors that bind to the TAX-inducible enhancer within the human T-cell leukemia virus type 1 long terminal repeat. Mol Cell Biol. 1989 Apr;9(4):1733–1745. doi: 10.1128/mcb.9.4.1733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Van den Broeke A., Cleuter Y., Chen G., Portetelle D., Mammerickx M., Zagury D., Fouchard M., Coulombel L., Kettmann R., Burny A. Even transcriptionally competent proviruses are silent in bovine leukemia virus-induced sheep tumor cells. Proc Natl Acad Sci U S A. 1988 Dec;85(23):9263–9267. doi: 10.1073/pnas.85.23.9263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wagner S., Green M. R. HTLV-I Tax protein stimulation of DNA binding of bZIP proteins by enhancing dimerization. Science. 1993 Oct 15;262(5132):395–399. doi: 10.1126/science.8211160. [DOI] [PubMed] [Google Scholar]
  43. Willems L., Gegonne A., Chen G., Burny A., Kettmann R., Ghysdael J. The bovine leukemia virus p34 is a transactivator protein. EMBO J. 1987 Nov;6(11):3385–3389. doi: 10.1002/j.1460-2075.1987.tb02661.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Willems L., Kettmann R., Chen G., Portetelle D., Burny A., Derse D. A cyclic AMP-responsive DNA-binding protein (CREB2) is a cellular transactivator of the bovine leukemia virus long terminal repeat. J Virol. 1992 Feb;66(2):766–772. doi: 10.1128/jvi.66.2.766-772.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Yamamoto K. K., Gonzalez G. A., Biggs W. H., 3rd, Montminy M. R. Phosphorylation-induced binding and transcriptional efficacy of nuclear factor CREB. Nature. 1988 Aug 11;334(6182):494–498. doi: 10.1038/334494a0. [DOI] [PubMed] [Google Scholar]
  46. Yoshimura T., Fujisawa J., Yoshida M. Multiple cDNA clones encoding nuclear proteins that bind to the tax-dependent enhancer of HTLV-1: all contain a leucine zipper structure and basic amino acid domain. EMBO J. 1990 Aug;9(8):2537–2542. doi: 10.1002/j.1460-2075.1990.tb07434.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Zhao L. J., Giam C. Z. Human T-cell lymphotropic virus type I (HTLV-I) transcriptional activator, Tax, enhances CREB binding to HTLV-I 21-base-pair repeats by protein-protein interaction. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):7070–7074. doi: 10.1073/pnas.89.15.7070. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Zhao L. J., Giam C. Z. Interaction of the human T-cell lymphotrophic virus type I (HTLV-I) transcriptional activator Tax with cellular factors that bind specifically to the 21-base-pair repeats in the HTLV-I enhancer. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11445–11449. doi: 10.1073/pnas.88.24.11445. [DOI] [PMC free article] [PubMed] [Google Scholar]

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