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. 1977 Aug 1;146(2):520–534. doi: 10.1084/jem.146.2.520

Antigenic modulation of Friend virus erythroleukemic cells in vitro by serum from mice with dormant erythroleukemia

PMCID: PMC2180763  PMID: 327016

Abstract

Friend leukemia virus (FLV) erythroleukemic cells cultured in medium containing FLV-immune serum from dormant FLV-infected mice undergo modulation of FLV cell surface antigens. Modulation was determined by an increased resistance to FLV antibody-mediated complement-dependent lysis and was associated temporally with the capping of FLV-immune complexes at the cell surface. Modulated cells regained their susceptibility to FLV antibody-mediated complement-dependent lysis when transferred to medium containing normal mouse serum. After 48 h of culture in FLV-immune serum, 26% of the FLV erythroleukemic cells were devoid of FLV cell surface antigens as demonstrated by immunofluoresence. Antigenic modulation occurred to a greater extent in cells maintained in logarithmic growth than in cells in GO or resting phase. FLV-antigenic modulation is discussed as a possible mechanism by which antibody induces and maintains FLV-transformed cells in a dormant state.

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Selected References

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  1. Aoki T., Johnson P. A. Suppression of Gross leukemia cell-surface antigens: a kind of antigenic modulation. J Natl Cancer Inst. 1972 Jul;49(1):183–192. [PubMed] [Google Scholar]
  2. Boyse E. A., Stockert E., Old L. J. Modification of the antigenic structure of the cell membrane by thymus-leukemia (TL) antibody. Proc Natl Acad Sci U S A. 1967 Sep;58(3):954–957. doi: 10.1073/pnas.58.3.954. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Calafat J., Hilgers J., Van Bitterswijk W. J., Verbeet M., Hageman P. C. Antibody-induced modulation and shedding of mammary tumor virus antigens on the surfaces of GR ascites leukemia cells as compared with normal antigens. J Natl Cancer Inst. 1976 May;56(5):1019–1029. doi: 10.1093/jnci/56.5.1019. [DOI] [PubMed] [Google Scholar]
  4. Carlson G. A., Terres G. Antibody-induced killing in vivo of L1210/MTX-R cells quantitated in passively immunized mice with 131I-iododeoxyuridine-labeled cells and whole-body measurement of retained radioactivity. J Immunol. 1976 Sep;117(3):822–829. [PubMed] [Google Scholar]
  5. Davies D. A. Mouse histocompatibility isoantigens derived from normal and from tumour cells. Immunology. 1966 Aug;11(2):115–125. [PMC free article] [PubMed] [Google Scholar]
  6. Edelman G. M. Surface modulation in cell recognition and cell growth. Science. 1976 Apr 16;192(4236):218–226. doi: 10.1126/science.769162. [DOI] [PubMed] [Google Scholar]
  7. Esmon N. L., Little J. R. Different mechanisms for the modulation of TL antigens on murine lymphoid cells. J Immunol. 1976 Sep;117(3):919–926. [PubMed] [Google Scholar]
  8. Friend C., Patuleia M. C., De Harven E. Erythrocytic maturation in vitro of murine (Friend) virus-induced leukemic cells. Natl Cancer Inst Monogr. 1966 Sep;22:505–522. [PubMed] [Google Scholar]
  9. Huebner R. J., Gilden R. V., Lane W. T., Toni R., Trimmer R. W., Hill P. R. Suppression of murine type-C RNA virogenes by type-specific oncornavirus vaccines: prospects for prevention of cancer. Proc Natl Acad Sci U S A. 1976 Feb;73(2):620–624. doi: 10.1073/pnas.73.2.620. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Huebner R. J., Gilden R. V., Toni R., Hill R. W., Trimmer R. W., Fish D. C., Sass B. Prevention of spontaneous leukemia in AKR mice by type-specific immunosuppression of endogenous ecotropic virogenes. Proc Natl Acad Sci U S A. 1976 Dec;73(12):4633–4635. doi: 10.1073/pnas.73.12.4633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hütteroth T. H., Cleve H., Litwin S. D. Modulation of membrane associated immunoglobulins of cultured human lymphoid cells by specific antibody. J Immunol. 1973 May;110(5):1325–1333. [PubMed] [Google Scholar]
  12. Ioachim H. L., Dorsett B., Sabbath M., Keller S. Loss and recovery of phenotypic expression of Gross leukaemia virus. Nat New Biol. 1972 Jun 14;237(76):215–218. doi: 10.1038/newbio237215b0. [DOI] [PubMed] [Google Scholar]
  13. Joseph B. S., Oldstone M. B. Immunologic injury in measles virus infection. II. Suppression of immune injury through antigenic modulation. J Exp Med. 1975 Oct 1;142(4):864–876. doi: 10.1084/jem.142.4.864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lamm M. E., Boyse E. A., Old L. J., Lisowska-Bernstein B., Stockert E. Modulation of TL (thymus-leukemia) antigens by Fab-fragments of TL antibody. J Immunol. 1968 Jul;101(1):99–103. [PubMed] [Google Scholar]
  15. Levy M. H., Wheelock E. F. Impaired macrophage function in Friend virus leukemia: restoration by statolon. J Immunol. 1975 Mar;114(3):962–965. [PubMed] [Google Scholar]
  16. Linscott W. D. Effect of cell surface antigen density on immunological enhancement. Nature. 1970 Nov 28;228(5274):824–827. doi: 10.1038/228824a0. [DOI] [PubMed] [Google Scholar]
  17. Marx P. A., Wheelock E. F. Influence of immune stimulators on viral leukemogenesis. Ann N Y Acad Sci. 1976;276:502–512. doi: 10.1111/j.1749-6632.1976.tb41676.x. [DOI] [PubMed] [Google Scholar]
  18. Möller G. DEMONSTRATION OF MOUSE ISOANTIGENS AT THE CELLULAR LEVEL BY THE FLUORESCENT ANTIBODY TECHNIQUE. J Exp Med. 1961 Sep 30;114(4):415–434. doi: 10.1084/jem.114.4.415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nilsson U. R., Müller-Eberhard H. J. Deficiency of the fifth component of complement in mice with an inherited complement defect. J Exp Med. 1967 Jan 1;125(1):1–16. doi: 10.1084/jem.125.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Old L. J., Stockert E., Boyse E. A., Kim J. H. Antigenic modulation. Loss of TL antigen from cells exposed to TL antibody. Study of the phenomenon in vitro. J Exp Med. 1968 Mar 1;127(3):523–539. doi: 10.1084/jem.127.3.523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ortaldo J. R., Ting C. C., Herberman R. B. Modulation of fetal antigen(s) in mouse leukemia cells. Cancer Res. 1974 Jun;34(6):1366–1371. [PubMed] [Google Scholar]
  22. Schlesinger M., Chaouat M. Modulation of the H-2 antigenicity on the surface of murine peritoneal cells. Tissue Antigens. 1972;2(6):427–435. doi: 10.1111/j.1399-0039.1972.tb00063.x. [DOI] [PubMed] [Google Scholar]
  23. Sherton C. C., Evans L. H., Polonoff E., Kabat D. Relationship of Friend murine leukemia virus production to growth and hemoglobin synthesis in cultured erythroleukemia cells. J Virol. 1976 Jul;19(1):118–125. doi: 10.1128/jvi.19.1.118-125.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Stackpole C. W., Jacobson J. B., Lardis M. P. Antigenic modulation in vitro. I. Fate of thymus-leukemia (TL) antigen-antibody complexes following modulation of TL antigenicity from the surfaces of mouse leukemia cells and thymocytes. J Exp Med. 1974 Oct 1;140(4):939–953. doi: 10.1084/jem.140.4.939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Stevens J. G., Cook M. L. Maintenance of latent herpetic infection: an apparent role for anti-viral IgG. J Immunol. 1974 Dec;113(6):1685–1693. [PubMed] [Google Scholar]
  26. Takahashi T., Old L. J., McIntire K. R., Boyse E. A. Immunoglobulin and other surface antigens of cells of the immune system. J Exp Med. 1971 Oct 1;134(4):815–832. doi: 10.1084/jem.134.4.815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Toy S. T., Weislow O. S., Wheelock E. F. Suppression of established Friend virus leukemia by statolon. VII. Relative roles of interferon and the immune response in development of FV-dormant infections. Proc Soc Exp Biol Med. 1973 Jul;143(3):726–732. doi: 10.3181/00379727-143-37401. [DOI] [PubMed] [Google Scholar]
  28. Toy S. T., Whellock E. F. In vitro depression of cellular immunity by Friend virus leukemic spleen cells. Cell Immunol. 1975 May;17(1):57–73. doi: 10.1016/s0008-8749(75)80006-2. [DOI] [PubMed] [Google Scholar]
  29. Unanue E. R., Karnovsky M. J., Engers H. D. Ligand-induced movement of lymphocyte membrane macromolecules. 3. Relationship between the formation and fate of anti-Ig-surface Ig complexes and cell metabolism. J Exp Med. 1973 Mar 1;137(3):675–689. doi: 10.1084/jem.137.3.675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Unanue E. R., Perkins W. D., Karnovsky M. J. Endocytosis by lymphocytes of complexes of anti-Ig with membrane-bound Ig. J Immunol. 1972 Feb;108(2):569–572. [PubMed] [Google Scholar]
  31. Unanue E. R., Perkins W. D., Karnovsky M. J. Ligand-induced movement of lymphocyte membrane macromolecules. I. Analysis by immunofluorescence and ultrastructural radioautography. J Exp Med. 1972 Oct 1;136(4):885–906. doi: 10.1084/jem.136.4.885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. WIGZELL H. QUANTITATIVE TITRATIONS OF MOUSE H-2 ANTIBODIES USING CR-51-LABELLED TARGET CELLS. Transplantation. 1965 May;3:423–431. doi: 10.1097/00007890-196505000-00011. [DOI] [PubMed] [Google Scholar]
  33. Weislow O. S., Friedman H., Wheelock E. F. Suppression of established Friend virus leukemia by statolon. V. Reversal of virus-induced immunodepression to sheep erythrocytes. Proc Soc Exp Biol Med. 1973 Feb;142(2):401–405. doi: 10.3181/00379727-142-37032. [DOI] [PubMed] [Google Scholar]
  34. Weislow O. S., Wheelock E. F. Suppression of extablished Friend virus leukemia by statolon: potentiation of statolon's leukemosuppressive activity by chlorite-oxidized oxyamylose. Infect Immun. 1975 Jan;11(1):129–136. doi: 10.1128/iai.11.1.129-136.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wheelock E. F., Caroline N. L., Moore R. D. Suppression of established Friend virus leukemia by statolon. 3. Development of FV-leukemogenic and FV-immunogenic activities in bloods, spleens, and lymph nodes. J Natl Cancer Inst. 1971 Apr;46(4):797–802. [PubMed] [Google Scholar]
  36. Wheelock E. F., Caroline N. L., Moore R. D. Suppression of established Friend virus leukemia by statolon. I. Demonstration of a latent infection in clinically normal mice. J Virol. 1969 Jul;4(1):1–6. doi: 10.1128/jvi.4.1.1-6.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wheelock E. F., Toy S. T., Caroline N. L., Sibal L. R., Fink M. A., Beverley P. C., Allison A. C. Suppression of established Friend virus leukemia by statolon. IV. Role of humoral antibody in the development of a dormant infection. J Natl Cancer Inst. 1972 Mar;48(3):665–673. [PubMed] [Google Scholar]
  38. Yu A., Cohen E. P. Studies on the effect of specific antisera on the metabolism of cellular antigens. II. The synthesis and degradation of TL antigens of mouse cells in the presence of TL antiserum. J Immunol. 1974 Apr;112(4):1296–1307. [PubMed] [Google Scholar]
  39. de Petris S., Raff M. C. Normal distribution, patching and capping of lymphocyte surface immunoglobulin studied by electron microscopy. Nat New Biol. 1973 Feb 28;241(113):257–259. doi: 10.1038/newbio241257a0. [DOI] [PubMed] [Google Scholar]

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