Skip to main content
PMC home page
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1993 Mar 1;177(3):763–774. doi: 10.1084/jem.177.3.763

Lymphotoxin is an autocrine growth factor for Epstein-Barr virus- infected B cell lines

PMCID: PMC2190931  PMID: 8382256

Abstract

Because human lymphotoxin (LT) was originally isolated from a lymphoblastoid cell line, we investigated the role of this molecule in three newly established Epstein-Barr virus (EBV)-infected human B cell lines. These lines were derived from acute lymphoblastic leukemia (Z- 6), myelodysplastic syndrome (Z-43), and acute myelogenous leukemia (Z- 55) patients who had a prior EBV infection. Each lymphoblastoid cell line had a karyotype that was different from that of the original parent leukemic cells, and all expressed B cell, but not T cell or myeloid surface markers. In all three lines, rearranged immunoglobulin heavy chain joining region (JH) bands were found, and the presence of EBV DNA was confirmed by Southern blotting. Z-6, Z-43, and Z-55 cell lines constitutively produced 192, 48, and 78 U/ml LT, respectively, as assessed by a cytotoxicity assay and antibody neutralization. Levels of tumor necrosis factor (TNF) were undetectable. Scatchard analysis revealed that all the cell lines expressed high-affinity TNF/LT receptors with receptor densities of 4197, 1258, and 1209 sites/cell on Z-6, Z-43, and Z-55, respectively. Furthermore, labeled TNF binding could be reversed by both unlabeled TNF, as well as by LT. Studies with p60 and p80 receptor-specific antibodies revealed that the three lines expressed primarily the p80 form of the TNF receptor. When studied in a clonogenic assay, exogenous LT stimulated proliferation of all three cell lines in a dose-dependent fashion at concentrations ranging from 25 to 500 U/ml. Similar results were obtained with [3H]TdR incorporation. Monoclonal anti-LT neutralizing antibodies at concentrations of 25-500 U/ml inhibited cellular multiplication in a dose-dependent manner. It is interesting that in spite of a common receptor, TNF (1,000 U/ml) had no direct effect on Z-55 cell growth, whereas it partially reversed the stimulatory effect of exogenous LT. In addition, TNF inhibited Z-6 and Z-43 cell proliferation, and its suppressive effect was reversed by exogenous LT. Both p80 and p60 forms of soluble TNF receptors suppressed the lymphoblastoid cell line proliferation and their inhibitory effect was partially reversed by LT. Our data suggest that (a) LT is an autocrine growth factor for EBV- transformed lymphoblastoid B cell lines; and (b) anti-LT antibodies, soluble TNF/LT receptors, and TNF itself can suppress the growth of lymphoblastoid cells, probably by modulating or competing with LT.(ABSTRACT TRUNCATED AT 400 WORDS)

Full Text

The Full Text of this article is available as a PDF (1.8 MB).

Selected References

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

  1. Abbondanzo S. L., Sato N., Straus S. E., Jaffe E. S. Acute infectious mononucleosis. CD30 (Ki-1) antigen expression and histologic correlations. Am J Clin Pathol. 1990 May;93(5):698–702. doi: 10.1093/ajcp/93.5.698. [DOI] [PubMed] [Google Scholar]
  2. Aggarwal B. B., Eessalu T. E., Hass P. E. Characterization of receptors for human tumour necrosis factor and their regulation by gamma-interferon. Nature. 1985 Dec 19;318(6047):665–667. doi: 10.1038/318665a0. [DOI] [PubMed] [Google Scholar]
  3. Aggarwal B. B., Eessalu T. E. Induction of receptors for tumor necrosis factor-alpha by interferons is not a major mechanism for their synergistic cytotoxic response. J Biol Chem. 1987 Jul 25;262(21):10000–10007. [PubMed] [Google Scholar]
  4. Aggarwal B. B., Henzel W. J., Moffat B., Kohr W. J., Harkins R. N. Primary structure of human lymphotoxin derived from 1788 lymphoblastoid cell line. J Biol Chem. 1985 Feb 25;260(4):2334–2344. [PubMed] [Google Scholar]
  5. Aggarwal B. B. Human lymphotoxin. Methods Enzymol. 1985;116:441–448. doi: 10.1016/s0076-6879(85)16035-0. [DOI] [PubMed] [Google Scholar]
  6. Baumann M. A., Paul C. C. Interleukin-5 is an autocrine growth factor for Epstein-Barr virus-transformed B lymphocytes. Blood. 1992 Apr 1;79(7):1763–1767. [PubMed] [Google Scholar]
  7. Bertoglio J., Wollman E., Rimsky L., Fradelizi D., Shaw A. A novel protein from cloned human B-cell line displays IL-1 bioactivity. J Immunol. 1988 Oct 15;141(8):2869–2870. [PubMed] [Google Scholar]
  8. Blazar B. A., Sutton L. M., Strome M. Self-stimulating growth factor production by B-cell lines derived from Burkitt's lymphomas and other lines transformed in vitro by Epstein-Barr virus. Cancer Res. 1983 Oct;43(10):4562–4568. [PubMed] [Google Scholar]
  9. Bringman T. S., Aggarwal B. B. Monoclonal antibodies to human tumor necrosis factors alpha and beta: application for affinity purification, immunoassays, and as structural probes. Hybridoma. 1987 Oct;6(5):489–507. doi: 10.1089/hyb.1987.6.489. [DOI] [PubMed] [Google Scholar]
  10. Brockhaus M., Schoenfeld H. J., Schlaeger E. J., Hunziker W., Lesslauer W., Loetscher H. Identification of two types of tumor necrosis factor receptors on human cell lines by monoclonal antibodies. Proc Natl Acad Sci U S A. 1990 Apr;87(8):3127–3131. doi: 10.1073/pnas.87.8.3127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Browning J., Ribolini A. Studies on the differing effects of tumor necrosis factor and lymphotoxin on the growth of several human tumor lines. J Immunol. 1989 Sep 15;143(6):1859–1867. [PubMed] [Google Scholar]
  12. Carswell E. A., Old L. J., Kassel R. L., Green S., Fiore N., Williamson B. An endotoxin-induced serum factor that causes necrosis of tumors. Proc Natl Acad Sci U S A. 1975 Sep;72(9):3666–3670. doi: 10.1073/pnas.72.9.3666. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cordingley F. T., Bianchi A., Hoffbrand A. V., Reittie J. E., Heslop H. E., Vyakarnam A., Turner M., Meager A., Brenner M. K. Tumour necrosis factor as an autocrine tumour growth factor for chronic B-cell malignancies. Lancet. 1988 Apr 30;1(8592):969–971. doi: 10.1016/s0140-6736(88)91782-5. [DOI] [PubMed] [Google Scholar]
  14. Cuturi M. C., Murphy M., Costa-Giomi M. P., Weinmann R., Perussia B., Trinchieri G. Independent regulation of tumor necrosis factor and lymphotoxin production by human peripheral blood lymphocytes. J Exp Med. 1987 Jun 1;165(6):1581–1594. doi: 10.1084/jem.165.6.1581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Diehl V., Henle G., Henle W., Kohn G. Demonstration of a herpes group virus in cultures of peripheral leukocytes from patients with infectious mononucleosis. J Virol. 1968 Jul;2(7):663–669. doi: 10.1128/jvi.2.7.663-669.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Digel W., Stefanic M., Schöniger W., Buck C., Raghavachar A., Frickhofen N., Heimpel H., Porzsolt F. Tumor necrosis factor induces proliferation of neoplastic B cells from chronic lymphocytic leukemia. Blood. 1989 Apr;73(5):1242–1246. [PubMed] [Google Scholar]
  17. Donhuijsen-Ant R., Abken H., Bornkamm G., Donhuijsen K., Grosse-Wilde H., Neumann-Haefelin D., Westerhausen M., Wiegand H. Fatal Hodgkin and non-Hodgkin lymphoma associated with persistent Epstein-Barr virus in four brothers. Ann Intern Med. 1988 Dec 15;109(12):946–952. doi: 10.7326/0003-4819-109-12-946. [DOI] [PubMed] [Google Scholar]
  18. Engelmann H., Aderka D., Rubinstein M., Rotman D., Wallach D. A tumor necrosis factor-binding protein purified to homogeneity from human urine protects cells from tumor necrosis factor toxicity. J Biol Chem. 1989 Jul 15;264(20):11974–11980. [PubMed] [Google Scholar]
  19. Engelmann H., Novick D., Wallach D. Two tumor necrosis factor-binding proteins purified from human urine. Evidence for immunological cross-reactivity with cell surface tumor necrosis factor receptors. J Biol Chem. 1990 Jan 25;265(3):1531–1536. [PubMed] [Google Scholar]
  20. Estrov Z., Cohen A., Gelfand E. W., Freedman M. H. Synergistic antiproliferative effects on HL-60 cells: deferoxamine enhances cytosine arabinoside, methotrexate, and daunorubicin cytotoxicity. Am J Pediatr Hematol Oncol. 1988 Winter;10(4):288–291. doi: 10.1097/00043426-198824000-00003. [DOI] [PubMed] [Google Scholar]
  21. Garrett I. R., Durie B. G., Nedwin G. E., Gillespie A., Bringman T., Sabatini M., Bertolini D. R., Mundy G. R. Production of lymphotoxin, a bone-resorbing cytokine, by cultured human myeloma cells. N Engl J Med. 1987 Aug 27;317(9):526–532. doi: 10.1056/NEJM198708273170902. [DOI] [PubMed] [Google Scholar]
  22. Gatanaga T., Hwang C. D., Kohr W., Cappuccini F., Lucci J. A., 3rd, Jeffes E. W., Lentz R., Tomich J., Yamamoto R. S., Granger G. A. Purification and characterization of an inhibitor (soluble tumor necrosis factor receptor) for tumor necrosis factor and lymphotoxin obtained from the serum ultrafiltrates of human cancer patients. Proc Natl Acad Sci U S A. 1990 Nov;87(22):8781–8784. doi: 10.1073/pnas.87.22.8781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Gordon J., Ley S. C., Melamed M. D., Aman P., Hughes-Jones N. C. Soluble factor requirements for the autostimulatory growth of B lymphoblasts immortalized by Epstein-Barr virus. J Exp Med. 1984 May 1;159(5):1554–1559. doi: 10.1084/jem.159.5.1554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Gordon J., Ley S. C., Melamed M. D., English L. S., Hughes-Jones N. C. Immortalized B lymphocytes produce B-cell growth factor. Nature. 1984 Jul 12;310(5973):145–147. doi: 10.1038/310145a0. [DOI] [PubMed] [Google Scholar]
  25. Gray P. W., Aggarwal B. B., Benton C. V., Bringman T. S., Henzel W. J., Jarrett J. A., Leung D. W., Moffat B., Ng P., Svedersky L. P. Cloning and expression of cDNA for human lymphotoxin, a lymphokine with tumour necrosis activity. Nature. 1984 Dec 20;312(5996):721–724. doi: 10.1038/312721a0. [DOI] [PubMed] [Google Scholar]
  26. Gregory C. D., Dive C., Henderson S., Smith C. A., Williams G. T., Gordon J., Rickinson A. B. Activation of Epstein-Barr virus latent genes protects human B cells from death by apoptosis. Nature. 1991 Feb 14;349(6310):612–614. doi: 10.1038/349612a0. [DOI] [PubMed] [Google Scholar]
  27. Hearing J. C., Nicolas J. C., Levine A. J. Identification of Epstein-Barr virus sequences that encode a nuclear antigen expressed in latently infected lymphocytes. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4373–4377. doi: 10.1073/pnas.81.14.4373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Henle G., Henle W., Diehl V. Relation of Burkitt's tumor-associated herpes-ytpe virus to infectious mononucleosis. Proc Natl Acad Sci U S A. 1968 Jan;59(1):94–101. doi: 10.1073/pnas.59.1.94. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Henle W., Diehl V., Kohn G., Zur Hausen H., Henle G. Herpes-type virus and chromosome marker in normal leukocytes after growth with irradiated Burkitt cells. Science. 1967 Sep 1;157(3792):1064–1065. doi: 10.1126/science.157.3792.1064. [DOI] [PubMed] [Google Scholar]
  30. Herbst H., Dallenbach F., Hummel M., Niedobitek G., Pileri S., Müller-Lantzsch N., Stein H. Epstein-Barr virus latent membrane protein expression in Hodgkin and Reed-Sternberg cells. Proc Natl Acad Sci U S A. 1991 Jun 1;88(11):4766–4770. doi: 10.1073/pnas.88.11.4766. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Janssen O., Kabelitz D. Tumor necrosis factor selectively inhibits activation of human B cells by Epstein-Barr virus. J Immunol. 1988 Jan 1;140(1):125–130. [PubMed] [Google Scholar]
  32. Jelinek D. F., Lipsky P. E. Enhancement of human B cell proliferation and differentiation by tumor necrosis factor-alpha and interleukin 1. J Immunol. 1987 Nov 1;139(9):2970–2976. [PubMed] [Google Scholar]
  33. Kehrl J. H., Alvarez-Mon M., Delsing G. A., Fauci A. S. Lymphotoxin is an important T cell-derived growth factor for human B cells. Science. 1987 Nov 20;238(4830):1144–1146. doi: 10.1126/science.3500512. [DOI] [PubMed] [Google Scholar]
  34. Kehrl J. H., Miller A., Fauci A. S. Effect of tumor necrosis factor alpha on mitogen-activated human B cells. J Exp Med. 1987 Sep 1;166(3):786–791. doi: 10.1084/jem.166.3.786. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kintner C., Sugden B. Identification of antigenic determinants unique to the surfaces of cells transformed by Epstein-Barr virus. Nature. 1981 Dec 3;294(5840):458–460. doi: 10.1038/294458a0. [DOI] [PubMed] [Google Scholar]
  36. Knecht H., Sahli R., Shaw P., Meyer C., Bachmann E., Odermatt B. F., Bachmann F. Detection of Epstein-Barr virus DNA by polymerase chain reaction in lymph node biopsies from patients with angioimmunoblastic lymphadenopathy. Br J Haematol. 1990 Aug;75(4):610–614. doi: 10.1111/j.1365-2141.1990.tb07807.x. [DOI] [PubMed] [Google Scholar]
  37. Knowles D. M., Inghirami G., Ubriaco A., Dalla-Favera R. Molecular genetic analysis of three AIDS-associated neoplasms of uncertain lineage demonstrates their B-cell derivation and the possible pathogenetic role of the Epstein-Barr virus. Blood. 1989 Feb 15;73(3):792–799. [PubMed] [Google Scholar]
  38. Kohno T., Brewer M. T., Baker S. L., Schwartz P. E., King M. W., Hale K. K., Squires C. H., Thompson R. C., Vannice J. L. A second tumor necrosis factor receptor gene product can shed a naturally occurring tumor necrosis factor inhibitor. Proc Natl Acad Sci U S A. 1990 Nov;87(21):8331–8335. doi: 10.1073/pnas.87.21.8331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Lantz M., Gullberg U., Nilsson E., Olsson I. Characterization in vitro of a human tumor necrosis factor-binding protein. A soluble form of a tumor necrosis factor receptor. J Clin Invest. 1990 Nov;86(5):1396–1402. doi: 10.1172/JCI114853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Loetscher H., Steinmetz M., Lesslauer W. Tumor necrosis factor: receptors and inhibitors. Cancer Cells. 1991 Jun;3(6):221–226. [PubMed] [Google Scholar]
  41. Loken M. R., Shah V. O., Dattilio K. L., Civin C. I. Flow cytometric analysis of human bone marrow. II. Normal B lymphocyte development. Blood. 1987 Nov;70(5):1316–1324. [PubMed] [Google Scholar]
  42. Nathan C. F. Secretory products of macrophages. J Clin Invest. 1987 Feb;79(2):319–326. doi: 10.1172/JCI112815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Nemerow G. R., Mold C., Schwend V. K., Tollefson V., Cooper N. R. Identification of gp350 as the viral glycoprotein mediating attachment of Epstein-Barr virus (EBV) to the EBV/C3d receptor of B cells: sequence homology of gp350 and C3 complement fragment C3d. J Virol. 1987 May;61(5):1416–1420. doi: 10.1128/jvi.61.5.1416-1420.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Niedobitek G., Hamilton-Dutoit S., Herbst H., Finn T., Vetner M., Pallesen G., Stein H. Identification of Epstein-Barr virus-infected cells in tonsils of acute infectious mononucleosis by in situ hybridization. Hum Pathol. 1989 Aug;20(8):796–799. doi: 10.1016/0046-8177(89)90075-0. [DOI] [PubMed] [Google Scholar]
  45. Old L. J. Tumor necrosis factor. Sci Am. 1988 May;258(5):59-60, 69-75. doi: 10.1038/scientificamerican0588-59. [DOI] [PubMed] [Google Scholar]
  46. Olsson I., Lantz M., Nilsson E., Peetre C., Thysell H., Grubb A., Adolf G. Isolation and characterization of a tumor necrosis factor binding protein from urine. Eur J Haematol. 1989 Mar;42(3):270–275. doi: 10.1111/j.1600-0609.1989.tb00111.x. [DOI] [PubMed] [Google Scholar]
  47. PULVERTAFT J. V. CYTOLOGY OF BURKITT'S TUMOUR (AFRICAN LYMPHOMA). Lancet. 1964 Feb 1;1(7327):238–240. doi: 10.1016/s0140-6736(64)92345-1. [DOI] [PubMed] [Google Scholar]
  48. Pallesen G., Hamilton-Dutoit S. J., Rowe M., Young L. S. Expression of Epstein-Barr virus latent gene products in tumour cells of Hodgkin's disease. Lancet. 1991 Feb 9;337(8737):320–322. doi: 10.1016/0140-6736(91)90943-j. [DOI] [PubMed] [Google Scholar]
  49. Pathak S. Chromosome banding techniques. J Reprod Med. 1976 Jul;17(1):25–28. [PubMed] [Google Scholar]
  50. Paul C. C., Keller J. R., Armpriester J. M., Baumann M. A. Epstein-Barr virus transformed B lymphocytes produce interleukin-5. Blood. 1990 Apr 1;75(7):1400–1403. [PubMed] [Google Scholar]
  51. Pennica D., Nedwin G. E., Hayflick J. S., Seeburg P. H., Derynck R., Palladino M. A., Kohr W. J., Aggarwal B. B., Goeddel D. V. Human tumour necrosis factor: precursor structure, expression and homology to lymphotoxin. Nature. 1984 Dec 20;312(5996):724–729. doi: 10.1038/312724a0. [DOI] [PubMed] [Google Scholar]
  52. Pike S. E., Markey S. P., Ijames C., Jones K. D., Tosato G. The role of lactic acid in autocrine B-cell growth stimulation. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11081–11085. doi: 10.1073/pnas.88.24.11081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. ROSENAU W., MOON H. D. Lysis of homologous cells by sensitized lymphocytes in tissue culture. J Natl Cancer Inst. 1961 Aug;27:471–483. [PubMed] [Google Scholar]
  54. Rimsky L., Wakasugi H., Ferrara P., Robin P., Capdevielle J., Tursz T., Fradelizi D., Bertoglio J. Purification to homogeneity and NH2-terminal amino acid sequence of a novel interleukin 1 species derived from a human B cell line. J Immunol. 1986 May 1;136(9):3304–3310. [PubMed] [Google Scholar]
  55. Rocchi G., Felici A., Ragona G., Heinz A. Quantitative evaluation of Epstein-Barr-virus-infected mononuclear peripheral blood leukocytes in infectious mononucleosis. N Engl J Med. 1977 Jan 20;296(3):132–134. doi: 10.1056/NEJM197701202960302. [DOI] [PubMed] [Google Scholar]
  56. Seckinger P., Isaaz S., Dayer J. M. A human inhibitor of tumor necrosis factor alpha. J Exp Med. 1988 Apr 1;167(4):1511–1516. doi: 10.1084/jem.167.4.1511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Seckinger P., Isaaz S., Dayer J. M. Purification and biologic characterization of a specific tumor necrosis factor alpha inhibitor. J Biol Chem. 1989 Jul 15;264(20):11966–11973. [PubMed] [Google Scholar]
  58. Seckinger P., Vey E., Turcatti G., Wingfield P., Dayer J. M. Tumor necrosis factor inhibitor: purification, NH2-terminal amino acid sequence and evidence for anti-inflammatory and immunomodulatory activities. Eur J Immunol. 1990 May;20(5):1167–1174. doi: 10.1002/eji.1830200533. [DOI] [PubMed] [Google Scholar]
  59. Seckinger P., Zhang J. H., Hauptmann B., Dayer J. M. Characterization of a tumor necrosis factor alpha (TNF-alpha) inhibitor: evidence of immunological cross-reactivity with the TNF receptor. Proc Natl Acad Sci U S A. 1990 Jul;87(13):5188–5192. doi: 10.1073/pnas.87.13.5188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Seregina T. M., Mekshenkov M. I., Turetskaya R. L., Nedospasov S. A. An autocrine growth factor constitutively produced by a human lymphoblastoid B-cell line is serologically related to lymphotoxin (TNF-beta). Mol Immunol. 1989 Mar;26(3):339–342. doi: 10.1016/0161-5890(89)90089-8. [DOI] [PubMed] [Google Scholar]
  61. Shapiro R. S., McClain K., Frizzera G., Gajl-Peczalska K. J., Kersey J. H., Blazar B. R., Arthur D. C., Patton D. F., Greenberg J. S., Burke B. Epstein-Barr virus associated B cell lymphoproliferative disorders following bone marrow transplantation. Blood. 1988 May;71(5):1234–1243. [PubMed] [Google Scholar]
  62. Shearer W. T., Ritz J., Finegold M. J., Guerra I. C., Rosenblatt H. M., Lewis D. E., Pollack M. S., Taber L. H., Sumaya C. V., Grumet F. C. Epstein-Barr virus-associated B-cell proliferations of diverse clonal origins after bone marrow transplantation in a 12-year-old patient with severe combined immunodeficiency. N Engl J Med. 1985 May 2;312(18):1151–1159. doi: 10.1056/NEJM198505023121804. [DOI] [PubMed] [Google Scholar]
  63. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  64. Sullivan J. L. Epstein-Barr virus and lymphoproliferative disorders. Semin Hematol. 1988 Jul;25(3):269–279. [PubMed] [Google Scholar]
  65. Swendeman S., Thorley-Lawson D. A. The activation antigen BLAST-2, when shed, is an autocrine BCGF for normal and transformed B cells. EMBO J. 1987 Jun;6(6):1637–1642. doi: 10.1002/j.1460-2075.1987.tb02412.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Tanner J., Weis J., Fearon D., Whang Y., Kieff E. Epstein-Barr virus gp350/220 binding to the B lymphocyte C3d receptor mediates adsorption, capping, and endocytosis. Cell. 1987 Jul 17;50(2):203–213. doi: 10.1016/0092-8674(87)90216-9. [DOI] [PubMed] [Google Scholar]
  67. Tartaglia L. A., Goeddel D. V. Two TNF receptors. Immunol Today. 1992 May;13(5):151–153. doi: 10.1016/0167-5699(92)90116-O. [DOI] [PubMed] [Google Scholar]
  68. Tosato G., Gerrard T. L., Goldman N. G., Pike S. E. Stimulation of EBV-activated human B cells by monocytes and monocyte products. Role of IFN-beta 2/B cell stimulatory factor 2/IL-6. J Immunol. 1988 Jun 15;140(12):4329–4336. [PubMed] [Google Scholar]
  69. Tosato G., Tanner J., Jones K. D., Revel M., Pike S. E. Identification of interleukin-6 as an autocrine growth factor for Epstein-Barr virus-immortalized B cells. J Virol. 1990 Jun;64(6):3033–3041. doi: 10.1128/jvi.64.6.3033-3041.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Uchibayashi N., Kikutani H., Barsumian E. L., Hauptmann R., Schneider F. J., Schwendenwein R., Sommergruber W., Spevak W., Maurer-Fogy I., Suemura M. Recombinant soluble Fc epsilon receptor II (Fc epsilon RII/CD23) has IgE binding activity but no B cell growth promoting activity. J Immunol. 1989 Jun 1;142(11):3901–3908. [PubMed] [Google Scholar]
  71. Wakasugi H., Rimsky L., Mahe Y., Kamel A. M., Fradelizi D., Tursz T., Bertoglio J. Epstein-Barr virus-containing B-cell line produces an interleukin 1 that it uses as a growth factor. Proc Natl Acad Sci U S A. 1987 Feb;84(3):804–808. doi: 10.1073/pnas.84.3.804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Weiss L. M., Jaffe E. S., Liu X. F., Chen Y. Y., Shibata D., Medeiros L. J. Detection and localization of Epstein-Barr viral genomes in angioimmunoblastic lymphadenopathy and angioimmunoblastic lymphadenopathy-like lymphoma. Blood. 1992 Apr 1;79(7):1789–1795. [PubMed] [Google Scholar]
  73. Yukawa K., Kikutani H., Owaki H., Yamasaki K., Yokota A., Nakamura H., Barsumian E. L., Hardy R. R., Suemura M., Kishimoto T. A B cell-specific differentiation antigen, CD23, is a receptor for IgE (Fc epsilon R) on lymphocytes. J Immunol. 1987 Apr 15;138(8):2576–2580. [PubMed] [Google Scholar]
  74. Zipf T. F., Lauzon G. J., Longenecker B. M. A monoclonal antibody detecting a 39,000 m.w. molecule that is present on B lymphocytes and chronic lymphocytic leukemia cells but is rare on acute lymphocytic leukemia blasts. J Immunol. 1983 Dec;131(6):3064–3072. [PubMed] [Google Scholar]
  75. zur Hausen H., Schulte-Holthausen H., Klein G., Henle W., Henle G., Clifford P., Santesson L. EBV DNA in biopsies of Burkitt tumours and anaplastic carcinomas of the nasopharynx. Nature. 1970 Dec 12;228(5276):1056–1058. doi: 10.1038/2281056a0. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Experimental Medicine are provided here courtesy of The Rockefeller University Press

RESOURCES