Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1984 Dec;81(23):7441–7445. doi: 10.1073/pnas.81.23.7441

Retrovirus-induced expression of interleukin 2 receptors on cells of human B-cell lineage.

K Sugamura, M Fujii, N Kobayashi, M Sakitani, M Hatanaka, Y Hinuma
PMCID: PMC392162  PMID: 6095296

Abstract

We provide direct evidence for interleukin 2 receptor (IL2R) induction by human T-cell leukemia/lymphoma virus (HTLV) in human B-cell lines. A lymphoblastoid B-cell line (LCL-Ter) was established by Epstein-Barr virus-induced transformation of peripheral blood lymphocytes derived from a healthy HTLV carrier and cloned in vitro. HTLV gp21 and/or p19 antigens were detected in eight LCL-Ter clones, all of which also expressed the IL2R antigens Tac and Hiei (defined by monoclonal antibodies). However, five other LCL-Ter clones, which were negative for the HTLV antigens, did not express the IL2R antigens. Furthermore, when the IL2R-negative B-cell line LCL-Kan, derived form a normal donor, was cocultured with HTLV-producer cells, three HTLV-carrying clones were obtained and found to constitutively express IL2R. IL2R induced by HTLV on these B-cell lines bound recombinant interleukin 2 and were similar in apparent molecular mass (approximately equal to 60 kDa) to the IL2R of peripheral blood lymphocytes stimulated with phytohemagglutinin.

Full text

PDF
7441

Images in this article

Selected References

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

  1. Andrew M. E., Braciale V. L., Braciale T. J. Regulation of interleukin 2 receptor expression on murine cytotoxic T lymphocyte clones. J Immunol. 1984 Feb;132(2):839–844. [PubMed] [Google Scholar]
  2. Arya S. K., Wong-Staal F., Gallo R. C. T-cell growth factor gene: lack of expression in human T-cell leukemia-lymphoma virus-infected cells. Science. 1984 Mar 9;223(4640):1086–1087. doi: 10.1126/science.6320374. [DOI] [PubMed] [Google Scholar]
  3. Cantrell D. A., Smith K. A. Transient expression of interleukin 2 receptors. Consequences for T cell growth. J Exp Med. 1983 Dec 1;158(6):1895–1911. doi: 10.1084/jem.158.6.1895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Clapham P., Nagy K., Cheingsong-Popov R., Exley M., Weiss R. A. Productive infection and cell-free transmission of human T-cell leukemia virus in a nonlymphoid cell line. Science. 1983 Dec 9;222(4628):1125–1127. doi: 10.1126/science.6316502. [DOI] [PubMed] [Google Scholar]
  5. Deuel T. F., Huang J. S., Huang S. S., Stroobant P., Waterfield M. D. Expression of a platelet-derived growth factor-like protein in simian sarcoma virus transformed cells. Science. 1983 Sep 30;221(4618):1348–1350. doi: 10.1126/science.6310754. [DOI] [PubMed] [Google Scholar]
  6. Downward J., Yarden Y., Mayes E., Scrace G., Totty N., Stockwell P., Ullrich A., Schlessinger J., Waterfield M. D. Close similarity of epidermal growth factor receptor and v-erb-B oncogene protein sequences. Nature. 1984 Feb 9;307(5951):521–527. doi: 10.1038/307521a0. [DOI] [PubMed] [Google Scholar]
  7. Fukui K., Noma T., Takeuchi K., Kobayashi N., Hatanaka M., Honjo T. Origin of adult T-cell leukemia virus. Implication for its zoonosis. Mol Biol Med. 1983 Nov;1(4):447–456. [PubMed] [Google Scholar]
  8. GREENWOOD F. C., HUNTER W. M., GLOVER J. S. THE PREPARATION OF I-131-LABELLED HUMAN GROWTH HORMONE OF HIGH SPECIFIC RADIOACTIVITY. Biochem J. 1963 Oct;89:114–123. doi: 10.1042/bj0890114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gallo R. C., Wong-Staal F. Retroviruses as etiologic agents of some animal and human leukemias and lymphomas and as tools for elucidating the molecular mechanism of leukemogenesis. Blood. 1982 Sep;60(3):545–557. [PubMed] [Google Scholar]
  10. Gootenberg J. E., Ruscetti F. W., Mier J. W., Gazdar A., Gallo R. C. Human cutaneous T cell lymphoma and leukemia cell lines produce and respond to T cell growth factor. J Exp Med. 1981 Nov 1;154(5):1403–1418. doi: 10.1084/jem.154.5.1403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gotoh Y. I., Sugamura K., Hinuma Y. Healthy carriers of a human retrovirus, adult T-cell leukemia virus (ATLV): demonstration by clonal culture of ATLV-carrying T cells from peripheral blood. Proc Natl Acad Sci U S A. 1982 Aug;79(15):4780–4782. doi: 10.1073/pnas.79.15.4780. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hattori T., Uchiyama T., Toibana T., Takatsuki K., Uchino H. Surface phenotype of Japanese adult T-cell leukemia cells characterized by monoclonal antibodies. Blood. 1981 Sep;58(3):645–647. [PubMed] [Google Scholar]
  13. Hemler M. E., Brenner M. B., McLean J. M., Strominger J. L. Antigenic stimulation regulates the level of expression of interleukin 2 receptor on human T cells. Proc Natl Acad Sci U S A. 1984 Apr;81(7):2172–2175. doi: 10.1073/pnas.81.7.2172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hinuma S., Sugamura K., Tsukamoto K., Hinuma Y. Constitutive production of phagocytosis inducing factor(s) in a monocyte/macrophage lineage cell line (THP-1) by retrovirus-transformed human T cell lines. Microbiol Immunol. 1984;28(8):935–947. doi: 10.1111/j.1348-0421.1984.tb00749.x. [DOI] [PubMed] [Google Scholar]
  15. Hinuma Y., Gotoh Y., Sugamura K., Nagata K., Goto T., Nakai M., Kamada N., Matsumoto T., Kinoshita K. A retrovirus associated with human adult T-cell leukemia: in vitro activation. Gan. 1982 Apr;73(2):341–344. [PubMed] [Google Scholar]
  16. Kobayashi N., Konishi H., Sabe H., Shigesada K., Noma T., Honjo T., Hatanaka M. Genomic structure of HTLV (human T-cell leukemia virus): detection of defective genome and its amplification in MT-2 cells. EMBO J. 1984 Jun;3(6):1339–1343. doi: 10.1002/j.1460-2075.1984.tb01974.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Korsmeyer S. J., Greene W. C., Cossman J., Hsu S. M., Jensen J. P., Neckers L. M., Marshall S. L., Bakhshi A., Depper J. M., Leonard W. J. Rearrangement and expression of immunoglobulin genes and expression of Tac antigen in hairy cell leukemia. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4522–4526. doi: 10.1073/pnas.80.14.4522. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lando Z., Sarin P., Megson M., Greene W. C., Waldman T. A., Gallo R. C., Broder S. Association of human T-cell leukaemia/lymphoma virus with the Tac antigen marker for the human T-cell growth factor receptor. Nature. 1983 Oct 20;305(5936):733–736. doi: 10.1038/305733a0. [DOI] [PubMed] [Google Scholar]
  19. Markwell M. A., Fox C. F. Surface-specific iodination of membrane proteins of viruses and eucaryotic cells using 1,3,4,6-tetrachloro-3alpha,6alpha-diphenylglycoluril. Biochemistry. 1978 Oct 31;17(22):4807–4817. doi: 10.1021/bi00615a031. [DOI] [PubMed] [Google Scholar]
  20. Merlino G. T., Xu Y. H., Ishii S., Clark A. J., Semba K., Toyoshima K., Yamamoto T., Pastan I. Amplification and enhanced expression of the epidermal growth factor receptor gene in A431 human carcinoma cells. Science. 1984 Apr 27;224(4647):417–419. doi: 10.1126/science.6200934. [DOI] [PubMed] [Google Scholar]
  21. Miyoshi I., Kubonishi I., Yoshimoto S., Akagi T., Ohtsuki Y., Shiraishi Y., Nagata K., Hinuma Y. Type C virus particles in a cord T-cell line derived by co-cultivating normal human cord leukocytes and human leukaemic T cells. Nature. 1981 Dec 24;294(5843):770–771. doi: 10.1038/294770a0. [DOI] [PubMed] [Google Scholar]
  22. Nagy K., Clapham P., Cheingsong-Popov R., Weiss R. A. Human T-cell leukemia virus type I: induction of syncytia and inhibition by patients' sera. Int J Cancer. 1983 Sep 15;32(3):321–328. doi: 10.1002/ijc.2910320310. [DOI] [PubMed] [Google Scholar]
  23. Poiesz B. J., Ruscetti F. W., Gazdar A. F., Bunn P. A., Minna J. D., Gallo R. C. Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7415–7419. doi: 10.1073/pnas.77.12.7415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Robb R. J., Greene W. C. Direct demonstration of the identity of T cell growth factor binding protein and the Tac antigen. J Exp Med. 1983 Oct 1;158(4):1332–1337. doi: 10.1084/jem.158.4.1332. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Robb R. J., Munck A., Smith K. A. T cell growth factor receptors. Quantitation, specificity, and biological relevance. J Exp Med. 1981 Nov 1;154(5):1455–1474. doi: 10.1084/jem.154.5.1455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Robbins K. C., Antoniades H. N., Devare S. G., Hunkapiller M. W., Aaronson S. A. Structural and immunological similarities between simian sarcoma virus gene product(s) and human platelet-derived growth factor. Nature. 1983 Oct 13;305(5935):605–608. doi: 10.1038/305605a0. [DOI] [PubMed] [Google Scholar]
  27. Salahuddin S. Z., Markham P. D., Lindner S. G., Gootenberg J., Popovic M., Hemmi H., Sarin P. S., Gallo R. C. Lymphokine production by cultured human T cells transformed by human T-cell leukemia-lymphoma virus-I. Science. 1984 Feb 17;223(4637):703–707. doi: 10.1126/science.6320367. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Sporn M. B., Todaro G. J. Autocrine secretion and malignant transformation of cells. N Engl J Med. 1980 Oct 9;303(15):878–880. doi: 10.1056/NEJM198010093031511. [DOI] [PubMed] [Google Scholar]
  30. Sugamura K., Fujii M., Kannagi M., Sakitani M., Takeuchi M., Hinuma Y. Cell surface phenotypes and expression of viral antigens of various human cell lines carrying human T-cell leukemia virus. Int J Cancer. 1984 Aug 15;34(2):221–228. doi: 10.1002/ijc.2910340213. [DOI] [PubMed] [Google Scholar]
  31. Sugamura K., Fujii M., Ueda S., Hinuma Y. Identification of a glycoprotein, gp21, of adult T cell leukemia virus by monoclonal antibody. J Immunol. 1984 Jun;132(6):3180–3184. [PubMed] [Google Scholar]
  32. Sugamura K., Matsuyama M., Fujii M., Kannagi M., Hinuma Y. Establishment of human cell lines constitutively producing immune interferon: transformation of normal T cells by a human retrovirus. J Immunol. 1983 Oct;131(4):1611–1612. [PubMed] [Google Scholar]
  33. Sutherland R., Delia D., Schneider C., Newman R., Kemshead J., Greaves M. Ubiquitous cell-surface glycoprotein on tumor cells is proliferation-associated receptor for transferrin. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4515–4519. doi: 10.1073/pnas.78.7.4515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Suzuki R., Handa K., Itoh K., Kumagai K. Natural killer (NK) cells as a responder to interleukin 2 (IL 2). I. Proliferative response and establishment of cloned cells. J Immunol. 1983 Feb;130(2):981–987. [PubMed] [Google Scholar]
  35. Tanaka Y., Koyanagi Y., Chosa T., Yamamoto N., Hinuma Y. Monoclonal antibody reactive with both p28 and p19 of adult T-cell leukemia virus-specific polypeptides. Gan. 1983 Jun;74(3):327–330. [PubMed] [Google Scholar]
  36. Tanaka Y., Tozawa H., Koyanagi Y., Yamamoto N., Hinuma Y. A new monoclonal antibody recognizing an antigen of human lymphocytes similar or identical to Tac antigen. Microbiol Immunol. 1984;28(9):1041–1055. doi: 10.1111/j.1348-0421.1984.tb00760.x. [DOI] [PubMed] [Google Scholar]
  37. Tsudo M., Uchiyama T., Uchino H., Yodoi J. Failure of regulation of Tac antigen/TCGF receptor on adult T-cell leukemia cells by anti-Tac monoclonal antibody. Blood. 1983 May;61(5):1014–1016. [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES