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. 1997 Jun;71(6):4485–4494. doi: 10.1128/jvi.71.6.4485-4494.1997

cis-Acting inhibitory elements within the pol-env region of human T-cell leukemia virus type 1 possibly involved in viral persistence.

A Saiga 1, S Orita 1, N Minoura-Tada 1, M Maeda 1, Y Aono 1, M Asakawa 1, K Nakahara 1, R Kubota 1, M Osame 1, H Igarashi 1
PMCID: PMC191668  PMID: 9151840

Abstract

Human T-cell leukemia virus type 1 (HTLV-1) remains latent throughout the life of the carrier, with cells containing the provirus and viral gene expression efficiently down-regulated. On a molecular level, exactly how viruses are down-regulated in vivo remains unresolved. We described here the possibility that down-regulation results from the presence of inhibitory elements within the gag-env region of the provirus in fresh peripheral blood mononuclear cells from carriers. In vitro experiments then revealed that potent cis-acting inhibitory elements (CIEs) are indeed contained in two discrete fragments from the pol region and weaker ones in the env region. The effect of CIEs is relieved by the HTLV-1 posttranscriptional regulator Rex through binding to the Rex-responsive element (RxRE), suggesting that Rex might interfere with pre-mRNA degradation and/or activate the export of mRNA molecules harboring both of the inhibitory elements and RxRE on the same RNA molecule. Thus, we propose the hypothesis that such functions of CIEs may be involved in HTLV-1 persistence.

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Selected References

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

  1. Aono Y., Imai J., Tominaga K., Orita S., Sato A., Igarashi H. Rapid, sensitive, specific, and quantitative detection of human T-cell leukemia virus type 1 sequence in peripheral blood mononuclear cells by an improved polymerase chain reaction method with nested primers. Virus Genes. 1992 Apr;6(2):159–171. doi: 10.1007/BF01703065. [DOI] [PubMed] [Google Scholar]
  2. Bhat N. K., Adachi Y., Samuel K. P., Derse D. HTLV-1 gene expression by defective proviruses in an infected T-cell line. Virology. 1993 Sep;196(1):15–24. doi: 10.1006/viro.1993.1450. [DOI] [PubMed] [Google Scholar]
  3. Bosselut R., Duvall J. F., Gégonne A., Bailly M., Hémar A., Brady J., Ghysdael J. The product of the c-ets-1 proto-oncogene and the related Ets2 protein act as transcriptional activators of the long terminal repeat of human T cell leukemia virus HTLV-1. EMBO J. 1990 Oct;9(10):3137–3144. doi: 10.1002/j.1460-2075.1990.tb07511.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bosselut R., Lim F., Romond P. C., Frampton J., Brady J., Ghysdael J. Myb protein binds to multiple sites in the human T cell lymphotropic virus type 1 long terminal repeat and transactivates LTR-mediated expression. Virology. 1992 Feb;186(2):764–769. doi: 10.1016/0042-6822(92)90044-p. [DOI] [PubMed] [Google Scholar]
  5. Brighty D. W., Rosenberg M. A cis-acting repressive sequence that overlaps the Rev-responsive element of human immunodeficiency virus type 1 regulates nuclear retention of env mRNAs independently of known splice signals. Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8314–8318. doi: 10.1073/pnas.91.18.8314. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Caput D., Beutler B., Hartog K., Thayer R., Brown-Shimer S., Cerami A. Identification of a common nucleotide sequence in the 3'-untranslated region of mRNA molecules specifying inflammatory mediators. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1670–1674. doi: 10.1073/pnas.83.6.1670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chang D. D., Sharp P. A. Messenger RNA transport and HIV rev regulation. Science. 1990 Aug 10;249(4969):614–615. doi: 10.1126/science.2143313. [DOI] [PubMed] [Google Scholar]
  8. Chen C. Y., You Y., Shyu A. B. Two cellular proteins bind specifically to a purine-rich sequence necessary for the destabilization function of a c-fos protein-coding region determinant of mRNA instability. Mol Cell Biol. 1992 Dec;12(12):5748–5757. doi: 10.1128/mcb.12.12.5748. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  10. Cochrane A. W., Jones K. S., Beidas S., Dillon P. J., Skalka A. M., Rosen C. A. Identification and characterization of intragenic sequences which repress human immunodeficiency virus structural gene expression. J Virol. 1991 Oct;65(10):5305–5313. doi: 10.1128/jvi.65.10.5305-5313.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dasgupta P., Saikumar P., Reddy C. D., Reddy E. P. Myb protein binds to human immunodeficiency virus 1 long terminal repeat (LTR) sequences and transactivates LTR-mediated transcription. Proc Natl Acad Sci U S A. 1990 Oct;87(20):8090–8094. doi: 10.1073/pnas.87.20.8090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dube D. K., Sherman M. P., Saksena N. K., Bryz-Gornia V., Mendelson J., Love J., Arnold C. B., Spicer T., Dube S., Glaser J. B. Genetic heterogeneity in human T-cell leukemia/lymphoma virus type II. J Virol. 1993 Mar;67(3):1175–1184. doi: 10.1128/jvi.67.3.1175-1184.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Franchini G., Wong-Staal F., Gallo R. C. Human T-cell leukemia virus (HTLV-I) transcripts in fresh and cultured cells of patients with adult T-cell leukemia. Proc Natl Acad Sci U S A. 1984 Oct;81(19):6207–6211. doi: 10.1073/pnas.81.19.6207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fujisawa J., Seiki M., Kiyokawa T., Yoshida M. Functional activation of the long terminal repeat of human T-cell leukemia virus type I by a trans-acting factor. Proc Natl Acad Sci U S A. 1985 Apr;82(8):2277–2281. doi: 10.1073/pnas.82.8.2277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gessain A., Barin F., Vernant J. C., Gout O., Maurs L., Calender A., de Thé G. Antibodies to human T-lymphotropic virus type-I in patients with tropical spastic paraparesis. Lancet. 1985 Aug 24;2(8452):407–410. doi: 10.1016/s0140-6736(85)92734-5. [DOI] [PubMed] [Google Scholar]
  16. Gessain A., Louie A., Gout O., Gallo R. C., Franchini G. Human T-cell leukemia-lymphoma virus type I (HTLV-I) expression in fresh peripheral blood mononuclear cells from patients with tropical spastic paraparesis/HTLV-I-associated myelopathy. J Virol. 1991 Mar;65(3):1628–1633. doi: 10.1128/jvi.65.3.1628-1633.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gitlin S. D., Dittmer J., Shin R. C., Brady J. N. Transcriptional activation of the human T-lymphotropic virus type I long terminal repeat by functional interaction of Tax1 and Ets1. J Virol. 1993 Dec;67(12):7307–7316. doi: 10.1128/jvi.67.12.7307-7316.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Goh W. C., Sodroski J., Rosen C., Essex M., Haseltine W. A. Subcellular localization of the product of the long open reading frame of human T-cell leukemia virus type I. Science. 1985 Mar 8;227(4691):1227–1228. doi: 10.1126/science.2983419. [DOI] [PubMed] [Google Scholar]
  19. Gröne M., Koch C., Grassmann R. The HTLV-1 Rex protein induces nuclear accumulation of unspliced viral RNA by avoiding intron excision and degradation. Virology. 1996 Apr 15;218(2):316–325. doi: 10.1006/viro.1996.0200. [DOI] [PubMed] [Google Scholar]
  20. Hidaka M., Inoue J., Yoshida M., Seiki M. Post-transcriptional regulator (rex) of HTLV-1 initiates expression of viral structural proteins but suppresses expression of regulatory proteins. EMBO J. 1988 Feb;7(2):519–523. doi: 10.1002/j.1460-2075.1988.tb02840.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hinuma Y., Nagata K., Hanaoka M., Nakai M., Matsumoto T., Kinoshita K. I., Shirakawa S., Miyoshi I. Adult T-cell leukemia: antigen in an ATL cell line and detection of antibodies to the antigen in human sera. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6476–6480. doi: 10.1073/pnas.78.10.6476. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Inoue J., Seiki M., Taniguchi T., Tsuru S., Yoshida M. Induction of interleukin 2 receptor gene expression by p40x encoded by human T-cell leukemia virus type 1. EMBO J. 1986 Nov;5(11):2883–2888. doi: 10.1002/j.1460-2075.1986.tb04583.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Jacobson S., Shida H., McFarlin D. E., Fauci A. S., Koenig S. Circulating CD8+ cytotoxic T lymphocytes specific for HTLV-I pX in patients with HTLV-I associated neurological disease. Nature. 1990 Nov 15;348(6298):245–248. doi: 10.1038/348245a0. [DOI] [PubMed] [Google Scholar]
  24. Kalyanaraman V. S., Sarngadharan M. G., Robert-Guroff M., Miyoshi I., Golde D., Gallo R. C. A new subtype of human T-cell leukemia virus (HTLV-II) associated with a T-cell variant of hairy cell leukemia. Science. 1982 Nov 5;218(4572):571–573. doi: 10.1126/science.6981847. [DOI] [PubMed] [Google Scholar]
  25. Kannagi M., Harada S., Maruyama I., Inoko H., Igarashi H., Kuwashima G., Sato S., Morita M., Kidokoro M., Sugimoto M. Predominant recognition of human T cell leukemia virus type I (HTLV-I) pX gene products by human CD8+ cytotoxic T cells directed against HTLV-I-infected cells. Int Immunol. 1991 Aug;3(8):761–767. doi: 10.1093/intimm/3.8.761. [DOI] [PubMed] [Google Scholar]
  26. Kashanchi F., Duvall J. F., Dittmer J., Mireskandari A., Reid R. L., Gitlin S. D., Brady J. N. Involvement of transcription factor YB-1 in human T-cell lymphotropic virus type I basal gene expression. J Virol. 1994 Jan;68(1):561–565. doi: 10.1128/jvi.68.1.561-565.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kashanchi F., Duvall J. F., Lindholm P. F., Radonovich M. F., Brady J. N. Sequences downstream of the RNA initiation site regulate human T-cell lymphotropic virus type I basal gene expression. J Virol. 1993 May;67(5):2894–2902. doi: 10.1128/jvi.67.5.2894-2902.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Katz R. A., Skalka A. M. Control of retroviral RNA splicing through maintenance of suboptimal processing signals. Mol Cell Biol. 1990 Feb;10(2):696–704. doi: 10.1128/mcb.10.2.696. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kinoshita K., Amagasaki T., Ikeda S., Suzuyama J., Toriya K., Nishino K., Tagawa M., Ichimaru M., Kamihira S., Yamada Y. Preleukemic state of adult T cell leukemia: abnormal T lymphocytosis induced by human adult T cell leukemia-lymphoma virus. Blood. 1985 Jul;66(1):120–127. [PubMed] [Google Scholar]
  30. Kinoshita T., Shimoyama M., Tobinai K., Ito M., Ito S., Ikeda S., Tajima K., Shimotohno K., Sugimura T. Detection of mRNA for the tax1/rex1 gene of human T-cell leukemia virus type I in fresh peripheral blood mononuclear cells of adult T-cell leukemia patients and viral carriers by using the polymerase chain reaction. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5620–5624. doi: 10.1073/pnas.86.14.5620. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Kiyokawa T., Seiki M., Iwashita S., Imagawa K., Shimizu F., Yoshida M. p27x-III and p21x-III, proteins encoded by the pX sequence of human T-cell leukemia virus type I. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8359–8363. doi: 10.1073/pnas.82.24.8359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Kubota R., Fujiyoshi T., Izumo S., Yashiki S., Maruyama I., Osame M., Sonoda S. Fluctuation of HTLV-I proviral DNA in peripheral blood mononuclear cells of HTLV-I-associated myelopathy. J Neuroimmunol. 1993 Feb;42(2):147–154. doi: 10.1016/0165-5728(93)90004-i. [DOI] [PubMed] [Google Scholar]
  33. Lagnado C. A., Brown C. Y., Goodall G. J. AUUUA is not sufficient to promote poly(A) shortening and degradation of an mRNA: the functional sequence within AU-rich elements may be UUAUUUA(U/A)(U/A). Mol Cell Biol. 1994 Dec;14(12):7984–7995. doi: 10.1128/mcb.14.12.7984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Lee T. H., Coligan J. E., Sodroski J. G., Haseltine W. A., Salahuddin S. Z., Wong-Staal F., Gallo R. C., Essex M. Antigens encoded by the 3'-terminal region of human T-cell leukemia virus: evidence for a functional gene. Science. 1984 Oct 5;226(4670):57–61. doi: 10.1126/science.6089350. [DOI] [PubMed] [Google Scholar]
  35. Maldarelli F., Martin M. A., Strebel K. Identification of posttranscriptionally active inhibitory sequences in human immunodeficiency virus type 1 RNA: novel level of gene regulation. J Virol. 1991 Nov;65(11):5732–5743. doi: 10.1128/jvi.65.11.5732-5743.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Malim M. H., Cullen B. R. Rev and the fate of pre-mRNA in the nucleus: implications for the regulation of RNA processing in eukaryotes. Mol Cell Biol. 1993 Oct;13(10):6180–6189. doi: 10.1128/mcb.13.10.6180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. Maruyama M., Shibuya H., Harada H., Hatakeyama M., Seiki M., Fujita T., Inoue J., Yoshida M., Taniguchi T. Evidence for aberrant activation of the interleukin-2 autocrine loop by HTLV-1-encoded p40x and T3/Ti complex triggering. Cell. 1987 Jan 30;48(2):343–350. doi: 10.1016/0092-8674(87)90437-5. [DOI] [PubMed] [Google Scholar]
  39. Miyatake S., Seiki M., Yoshida M., Arai K. T-cell activation signals and human T-cell leukemia virus type I-encoded p40x protein activate the mouse granulocyte-macrophage colony-stimulating factor gene through a common DNA element. Mol Cell Biol. 1988 Dec;8(12):5581–5587. doi: 10.1128/mcb.8.12.5581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Nagashima K., Yoshida M., Seiki M. A single species of pX mRNA of human T-cell leukemia virus type I encodes trans-activator p40x and two other phosphoproteins. J Virol. 1986 Nov;60(2):394–399. doi: 10.1128/jvi.60.2.394-399.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Nyborg J. K., Matthews M. A., Yucel J., Walls L., Golde W. T., Dynan W. S., Wachsman W. Interaction of host cell proteins with the human T-cell leukemia virus type I transcriptional control region. II. A comprehensive map of protein-binding sites facilitates construction of a simple chimeric promoter responsive to the viral tax2 gene product. J Biol Chem. 1990 May 15;265(14):8237–8242. [PubMed] [Google Scholar]
  42. Okumura K., Sakaguchi G., Takagi S., Naito K., Mimori T., Igarashi H. Sp1 family proteins recognize the U5 repressive element of the long terminal repeat of human T cell leukemia virus type I through binding to the CACCC core motif. J Biol Chem. 1996 May 31;271(22):12944–12950. doi: 10.1074/jbc.271.22.12944. [DOI] [PubMed] [Google Scholar]
  43. Orita S., Kobayashi H., Aono Y., Saiga A., Maeda M., Igarashi H. p21X mRNA is expressed as a singly spliced pX transcript from defective provirus genomes having a partial deletion of the pol-env region in human T-cell leukemia virus type 1-infected cells. Nucleic Acids Res. 1993 Aug 11;21(16):3799–3807. doi: 10.1093/nar/21.16.3799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Orita S., Kobayashi H., Saiga A., Kubota R., Osame M., Igarashi H. A spontaneous point mutation in the human T-cell leukemia virus type 1 pX gene leads to expression of a novel doubly spliced pX-mRNA that encodes a 25-kD, amino-terminal deleted rex protein. DNA Cell Biol. 1994 Apr;13(4):353–364. doi: 10.1089/dna.1994.13.353. [DOI] [PubMed] [Google Scholar]
  45. Orita S., Saiga A., Takagi S., Tanaka T., Okumura K., Aono Y., Hinuma Y., Igarashi H. A novel alternatively spliced viral mRNA transcribed in cells infected with human T cell leukemia virus type 1 is mainly responsible for expressing p21X protein. FEBS Lett. 1991 Dec 16;295(1-3):127–134. doi: 10.1016/0014-5793(91)81402-t. [DOI] [PubMed] [Google Scholar]
  46. Orita S., Sato S., Aono Y., Minoura N., Yamashita T., Hinuma Y., Igarashi H. Identification of novel singly spliced pX mRNA transcripts common to all human T-cell leukemia virus type 1-related retroviruses. Virus Genes. 1993 Jun;7(2):197–204. doi: 10.1007/BF01702399. [DOI] [PubMed] [Google Scholar]
  47. Orita S., Takagi S., Saiga A., Minoura N., Araki K., Kinoshita K., Kondo T., Hinuma Y., Igarashi H. Human T cell leukaemia virus type 1 p21X mRNA: constitutive expression in peripheral blood mononuclear cells of patients with adult T cell leukaemia. J Gen Virol. 1992 Sep;73(Pt 9):2283–2289. doi: 10.1099/0022-1317-73-9-2283. [DOI] [PubMed] [Google Scholar]
  48. Osame M., Igata A., Usuku K., Rosales R. L., Matsumoto M. Mother-to-child transmission in HTLV-I associated myelopathy. Lancet. 1987 Jan 10;1(8524):106–106. doi: 10.1016/s0140-6736(87)91946-5. [DOI] [PubMed] [Google Scholar]
  49. Osame M., Usuku K., Izumo S., Ijichi N., Amitani H., Igata A., Matsumoto M., Tara M. HTLV-I associated myelopathy, a new clinical entity. Lancet. 1986 May 3;1(8488):1031–1032. doi: 10.1016/s0140-6736(86)91298-5. [DOI] [PubMed] [Google Scholar]
  50. Parker C. E., Daenke S., Nightingale S., Bangham C. R. Activated, HTLV-1-specific cytotoxic T-lymphocytes are found in healthy seropositives as well as in patients with tropical spastic paraparesis. Virology. 1992 Jun;188(2):628–636. doi: 10.1016/0042-6822(92)90517-s. [DOI] [PubMed] [Google Scholar]
  51. Parker C. E., Nightingale S., Taylor G. P., Weber J., Bangham C. R. Circulating anti-Tax cytotoxic T lymphocytes from human T-cell leukemia virus type I-infected people, with and without tropical spastic paraparesis, recognize multiple epitopes simultaneously. J Virol. 1994 May;68(5):2860–2868. doi: 10.1128/jvi.68.5.2860-2868.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Poiesz B. J., Ruscetti F. W., Reitz M. S., Kalyanaraman V. S., Gallo R. C. Isolation of a new type C retrovirus (HTLV) in primary uncultured cells of a patient with Sézary T-cell leukaemia. Nature. 1981 Nov 19;294(5838):268–271. doi: 10.1038/294268a0. [DOI] [PubMed] [Google Scholar]
  53. Rosen C. A., Terwilliger E., Dayton A., Sodroski J. G., Haseltine W. A. Intragenic cis-acting art gene-responsive sequences of the human immunodeficiency virus. Proc Natl Acad Sci U S A. 1988 Apr;85(7):2071–2075. doi: 10.1073/pnas.85.7.2071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Saiga A., Tanaka T., Orita S., Sato A., Sato S., Hachisu T., Abe K., Kimura Y., Kondo Y., Fujiwara T. Human T-cell leukemia virus type 1 protease protein expressed in Escherichia coli possesses aspartic proteinase activity. Arch Virol. 1993;128(3-4):195–210. doi: 10.1007/BF01309434. [DOI] [PubMed] [Google Scholar]
  55. Schwartz S., Felber B. K., Pavlakis G. N. Distinct RNA sequences in the gag region of human immunodeficiency virus type 1 decrease RNA stability and inhibit expression in the absence of Rev protein. J Virol. 1992 Jan;66(1):150–159. doi: 10.1128/jvi.66.1.150-159.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Seiki M., Hattori S., Hirayama Y., Yoshida M. Human adult T-cell leukemia virus: complete nucleotide sequence of the provirus genome integrated in leukemia cell DNA. Proc Natl Acad Sci U S A. 1983 Jun;80(12):3618–3622. doi: 10.1073/pnas.80.12.3618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Seiki M., Hikikoshi A., Yoshida M. The U5 sequence is a cis-acting repressive element for genomic RNA expression of human T cell leukemia virus type I. Virology. 1990 May;176(1):81–86. doi: 10.1016/0042-6822(90)90232-g. [DOI] [PubMed] [Google Scholar]
  58. Seiki M., Inoue J., Hidaka M., Yoshida M. Two cis-acting elements responsible for posttranscriptional trans-regulation of gene expression of human T-cell leukemia virus type I. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7124–7128. doi: 10.1073/pnas.85.19.7124. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Shaw G., Kamen R. A conserved AU sequence from the 3' untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell. 1986 Aug 29;46(5):659–667. doi: 10.1016/0092-8674(86)90341-7. [DOI] [PubMed] [Google Scholar]
  60. Shyu A. B., Greenberg M. E., Belasco J. G. The c-fos transcript is targeted for rapid decay by two distinct mRNA degradation pathways. Genes Dev. 1989 Jan;3(1):60–72. doi: 10.1101/gad.3.1.60. [DOI] [PubMed] [Google Scholar]
  61. Slamon D. J., Shimotohno K., Cline M. J., Golde D. W., Chen I. S. Identification of the putative transforming protein of the human T-cell leukemia viruses HTLV-I and HTLV-II. Science. 1984 Oct 5;226(4670):61–65. doi: 10.1126/science.6089351. [DOI] [PubMed] [Google Scholar]
  62. Sodroski J. G., Rosen C. A., Haseltine W. A. Trans-acting transcriptional activation of the long terminal repeat of human T lymphotropic viruses in infected cells. Science. 1984 Jul 27;225(4660):381–385. doi: 10.1126/science.6330891. [DOI] [PubMed] [Google Scholar]
  63. 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]
  64. Tanaka Y., Fukudome K., Hayashi M., Takagi S., Yoshie O. Induction of ICAM-1 and LFA-3 by Tax1 of human T-cell leukemia virus type 1 and mechanism of down-regulation of ICAM-1 or LFA-1 in adult-T-cell-leukemia cell lines. Int J Cancer. 1995 Feb 8;60(4):554–561. doi: 10.1002/ijc.2910600421. [DOI] [PubMed] [Google Scholar]
  65. Toyoshima H., Itoh M., Inoue J., Seiki M., Takaku F., Yoshida M. Secondary structure of the human T-cell leukemia virus type 1 rex-responsive element is essential for rex regulation of RNA processing and transport of unspliced RNAs. J Virol. 1990 Jun;64(6):2825–2832. doi: 10.1128/jvi.64.6.2825-2832.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Tsujimoto H., Komuro A., Iijima K., Miyamoto J., Ishikawa K., Hayami M. Isolation of simian retroviruses closely related to human T-cell leukemia virus by establishment of lymphoid cell lines from various non-human primates. Int J Cancer. 1985 Mar 15;35(3):377–384. doi: 10.1002/ijc.2910350314. [DOI] [PubMed] [Google Scholar]
  67. Wano Y., Feinberg M., Hosking J. B., Bogerd H., Greene W. C. Stable expression of the tax gene of type I human T-cell leukemia virus in human T cells activates specific cellular genes involved in growth. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9733–9737. doi: 10.1073/pnas.85.24.9733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Wilson T., Treisman R. Removal of poly(A) and consequent degradation of c-fos mRNA facilitated by 3' AU-rich sequences. Nature. 1988 Nov 24;336(6197):396–399. doi: 10.1038/336396a0. [DOI] [PubMed] [Google Scholar]
  69. Yoshida M., Miyoshi I., Hinuma Y. Isolation and characterization of retrovirus from cell lines of human adult T-cell leukemia and its implication in the disease. Proc Natl Acad Sci U S A. 1982 Mar;79(6):2031–2035. doi: 10.1073/pnas.79.6.2031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Yoshida M., Osame M., Usuku K., Matsumoto M., Igata A. Viruses detected in HTLV-I-associated myelopathy and adult T-cell leukaemia are identical on DNA blotting. Lancet. 1987 May 9;1(8541):1085–1086. doi: 10.1016/s0140-6736(87)90506-x. [DOI] [PubMed] [Google Scholar]
  71. Yoshida M., Seiki M., Yamaguchi K., Takatsuki K. Monoclonal integration of human T-cell leukemia provirus in all primary tumors of adult T-cell leukemia suggests causative role of human T-cell leukemia virus in the disease. Proc Natl Acad Sci U S A. 1984 Apr;81(8):2534–2537. doi: 10.1073/pnas.81.8.2534. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Zandomeni R. O., Carrera-Zandomeni M., Esteban E., Donawick W., Ferrer J. F. Induction and inhibition of bovine leukaemia virus expression in naturally infected cells. J Gen Virol. 1992 Aug;73(Pt 8):1915–1924. doi: 10.1099/0022-1317-73-8-1915. [DOI] [PubMed] [Google Scholar]

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