Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1996 Aug;70(8):5706–5710. doi: 10.1128/jvi.70.8.5706-5710.1996

Increased interleukin-10 mRNA expression in tumor-bearing or persistently lymphocytotic animals infected with bovine leukemia virus.

D Pyeon 1, K L O'Reilly 1, G A Splitter 1
PMCID: PMC190539  PMID: 8764093

Abstract

Interleukin-10 (IL-10), produced by Th2 helper T cells, B cells, and macrophages, can inhibit cytokine production by Th1 cells and enhance B-cell proliferation and differentiation. Here, we show that peripheral blood mononuclear cells (PBMCs) from bovine leukemia virus-infected animals with late-stage disease express considerably more IL-10 mRNA than animals that are not infected or that are in the early stages of disease. In contrast, the quantities of type 1 cytokines, IL-2 and gamma interferon, decrease with disease progression. In addition, we observed that IL-10 is expressed principally by monocytes/macrophages, not B lymphocytes, in persistently lymphocytotic animals. This observation supports a role for monocytes/macrophages in progression of bovine leukemia virus infection and, of importance, indicates that proliferating B cells are not the source of IL-10 expression. These findings suggest that IL-10 produced by monocytes/macrophages may influence the progression of bovine leukosis in animals that develop persistent lymphocytosis of B cells or B-cell lymphosarcoma.

Full Text

The Full Text of this article is available as a PDF (380.6 KB).

Selected References

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

  1. Alderson M. R., Armitage R. J., Maraskovsky E., Tough T. W., Roux E., Schooley K., Ramsdell F., Lynch D. H. Fas transduces activation signals in normal human T lymphocytes. J Exp Med. 1993 Dec 1;178(6):2231–2235. doi: 10.1084/jem.178.6.2231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ameglio F., Capobianchi M. R., Castilletti C., Cordiali Fei P., Fais S., Trento E., Dianzani F. Recombinant gp120 induces IL-10 in resting peripheral blood mononuclear cells; correlation with the induction of other cytokines. Clin Exp Immunol. 1994 Mar;95(3):455–458. doi: 10.1111/j.1365-2249.1994.tb07018.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Benjamin D., Knobloch T. J., Dayton M. A. Human B-cell interleukin-10: B-cell lines derived from patients with acquired immunodeficiency syndrome and Burkitt's lymphoma constitutively secrete large quantities of interleukin-10. Blood. 1992 Sep 1;80(5):1289–1298. [PubMed] [Google Scholar]
  4. Bonney R. J., Naruns P., Davies P., Humes J. L. Antigen-antibody complexes stimulate the synthesis and release of prostaglandins by mouse peritoneal macrophages. Prostaglandins. 1979 Oct;18(4):605–616. doi: 10.1016/0090-6980(79)90027-3. [DOI] [PubMed] [Google Scholar]
  5. Burdin N., Van Kooten C., Galibert L., Abrams J. S., Wijdenes J., Banchereau J., Rousset F. Endogenous IL-6 and IL-10 contribute to the differentiation of CD40-activated human B lymphocytes. J Immunol. 1995 Mar 15;154(6):2533–2544. [PubMed] [Google Scholar]
  6. Cavaillon J. M. Cytokines and macrophages. Biomed Pharmacother. 1994;48(10):445–453. doi: 10.1016/0753-3322(94)90005-1. [DOI] [PubMed] [Google Scholar]
  7. Clerici M., Sarin A., Coffman R. L., Wynn T. A., Blatt S. P., Hendrix C. W., Wolf S. F., Shearer G. M., Henkart P. A. Type 1/type 2 cytokine modulation of T-cell programmed cell death as a model for human immunodeficiency virus pathogenesis. Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):11811–11815. doi: 10.1073/pnas.91.25.11811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Clerici M., Shearer G. M. A TH1-->TH2 switch is a critical step in the etiology of HIV infection. Immunol Today. 1993 Mar;14(3):107–111. doi: 10.1016/0167-5699(93)90208-3. [DOI] [PubMed] [Google Scholar]
  9. Clerici M., Shearer G. M. The Th1-Th2 hypothesis of HIV infection: new insights. Immunol Today. 1994 Dec;15(12):575–581. doi: 10.1016/0167-5699(94)90220-8. [DOI] [PubMed] [Google Scholar]
  10. Clerici M., Wynn T. A., Berzofsky J. A., Blatt S. P., Hendrix C. W., Sher A., Coffman R. L., Shearer G. M. Role of interleukin-10 in T helper cell dysfunction in asymptomatic individuals infected with the human immunodeficiency virus. J Clin Invest. 1994 Feb;93(2):768–775. doi: 10.1172/JCI117031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Covert J., Splitter G. Detection of cytokine transcriptional profiles from bovine peripheral blood mononuclear cells and CD4+ lymphocytes by reverse transcriptase polymerase chain reaction. Vet Immunol Immunopathol. 1995 Nov;49(1-2):39–50. doi: 10.1016/0165-2427(95)05451-b. [DOI] [PubMed] [Google Scholar]
  12. Emilie D., Touitou R., Raphael M., Peuchmaur M., Devergnee O., Rea D., Coumbraras J., Crevon M. C., Edelman L., Joab I. In vivo production of interleukin-10 by malignant cells in AIDS lymphomas. Eur J Immunol. 1992 Nov;22(11):2937–2942. doi: 10.1002/eji.1830221127. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Fiorentino D. F., Bond M. W., Mosmann T. R. Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J Exp Med. 1989 Dec 1;170(6):2081–2095. doi: 10.1084/jem.170.6.2081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Haraguchi S., Good R. A., Cianciolo G. J., James-Yarish M., Day N. K. Transcriptional down-regulation of tumor necrosis factor-alpha gene expression by a synthetic peptide homologous to retroviral envelope protein. J Immunol. 1993 Sep 1;151(5):2733–2741. [PubMed] [Google Scholar]
  16. Haraguchi S., Good R. A., Day N. K. Immunosuppressive retroviral peptides: cAMP and cytokine patterns. Immunol Today. 1995 Dec;16(12):595–603. doi: 10.1016/0167-5699(95)80083-2. [DOI] [PubMed] [Google Scholar]
  17. Haraguchi S., Good R. A., James-Yarish M., Cianciolo G. J., Day N. K. Differential modulation of Th1- and Th2-related cytokine mRNA expression by a synthetic peptide homologous to a conserved domain within retroviral envelope protein. Proc Natl Acad Sci U S A. 1995 Apr 11;92(8):3611–3615. doi: 10.1073/pnas.92.8.3611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Heeney J. L., Valli V. E. Transformed phenotype of enzootic bovine lymphoma reflects differentiation-linked leukemogenesis. Lab Invest. 1990 Mar;62(3):339–346. [PubMed] [Google Scholar]
  19. Holland G., Zlotnik A. Interleukin-10 and cancer. Cancer Invest. 1993;11(6):751–758. doi: 10.3109/07357909309046950. [DOI] [PubMed] [Google Scholar]
  20. Itoh K., Hirohata S. The role of IL-10 in human B cell activation, proliferation, and differentiation. J Immunol. 1995 May 1;154(9):4341–4350. [PubMed] [Google Scholar]
  21. Kabelitz D., Wesselborg S. Life and death of a superantigen-reactive human CD4+ T cell clone: staphylococcal enterotoxins induce death by apoptosis but simultaneously trigger a proliferative response in the presence of HLA-DR+ antigen-presenting cells. Int Immunol. 1992 Dec;4(12):1381–1388. doi: 10.1093/intimm/4.12.1381. [DOI] [PubMed] [Google Scholar]
  22. Kettmann R., Portetelle D., Mammerickx M., Cleuter Y., Dekegel D., Galoux M., Ghysdael J., Burny A., Chantrenne H. Bovine leukemia virus: an exogenous RNA oncogenic virus. Proc Natl Acad Sci U S A. 1976 Apr;73(4):1014–1018. doi: 10.1073/pnas.73.4.1014. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Korsmeyer S. J. Chromosomal translocations in lymphoid malignancies reveal novel proto-oncogenes. Annu Rev Immunol. 1992;10:785–807. doi: 10.1146/annurev.iy.10.040192.004033. [DOI] [PubMed] [Google Scholar]
  24. Koyama H., Nakanishi H., Kajikawa O., Yoshikawa H., Tsubaki S., Yoshikawa T., Saito H. T and B lymphocytes in persistent lymphocytic and leukemic cattle. Nihon Juigaku Zasshi. 1983 Aug;45(4):471–475. doi: 10.1292/jvms1939.45.471. [DOI] [PubMed] [Google Scholar]
  25. Li C. Y., Lam K. W., Yam L. T. Esterases in human leukocytes. J Histochem Cytochem. 1973 Jan;21(1):1–12. doi: 10.1177/21.1.1. [DOI] [PubMed] [Google Scholar]
  26. Lynch D. H., Ramsdell F., Alderson M. R. Fas and FasL in the homeostatic regulation of immune responses. Immunol Today. 1995 Dec;16(12):569–574. doi: 10.1016/0167-5699(95)80079-4. [DOI] [PubMed] [Google Scholar]
  27. Masood R., Lunardi-Iskandar Y., Moudgil T., Zhang Y., Law R. E., Huang C. L., Puri R. K., Levine A. M., Gill P. S. IL-10 inhibits HIV-1 replication and is induced by tat. Biochem Biophys Res Commun. 1994 Jul 15;202(1):374–383. doi: 10.1006/bbrc.1994.1938. [DOI] [PubMed] [Google Scholar]
  28. Ramsdell F., Seaman M. S., Miller R. E., Picha K. S., Kennedy M. K., Lynch D. H. Differential ability of Th1 and Th2 T cells to express Fas ligand and to undergo activation-induced cell death. Int Immunol. 1994 Oct;6(10):1545–1553. doi: 10.1093/intimm/6.10.1545. [DOI] [PubMed] [Google Scholar]
  29. Schwartz I., Bensaid A., Polack B., Perrin B., Berthelemy M., Levy D. In vivo leukocyte tropism of bovine leukemia virus in sheep and cattle. J Virol. 1994 Jul;68(7):4589–4596. doi: 10.1128/jvi.68.7.4589-4596.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tomar R. H. Breaking the asymptomatic phase of HIV-1 infection. J Clin Lab Anal. 1994;8(2):116–119. doi: 10.1002/jcla.1860080210. [DOI] [PubMed] [Google Scholar]
  31. de Waal Malefyt R., Haanen J., Spits H., Roncarolo M. G., te Velde A., Figdor C., Johnson K., Kastelein R., Yssel H., de Vries J. E. Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression. J Exp Med. 1991 Oct 1;174(4):915–924. doi: 10.1084/jem.174.4.915. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES