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. 1994 Apr;68(4):2059–2064. doi: 10.1128/jvi.68.4.2059-2064.1994

Recovery from Friend disease in mice with reduced major histocompatibility complex class I expression.

K J Hasenkrug 1, G J Sprangrude 1, J Nishio 1, D M Brooks 1, B Chesebro 1
PMCID: PMC236679  PMID: 8138991

Abstract

Mice homozygous for the b allele of the MHC gene, H-2D, have a high incidence of recovery from Friend virus infections, while mice heterozygous for the b allele at H-2D have a very low incidence of recovery. Previous experiments indicated that the low recovery rates associated with heterozygosity at H-2D might be related to a gene dosage effect requiring the expression of two H-2Db alleles for high recovery. We investigated the effects of reduced H-2Db expression on recovery from Friend disease by using H-2b homozygous mice carrying a single beta 2-microglobulin gene disruption. These mice had reductions in cell surface H-2Db expression comparable to those of H-2Da/b heterozygotes. Numerous cell types with various levels of H-2Db expression were examined, and in each case, the expression levels in the beta 2-microglobulin mutants closely reflected those observed in the H-2Da/b heterozygotes. We found, however, that reduced expression did not affect recovery from Friend disease, indicating that heterozygous levels of H-2Db expression are sufficient for the high-recovery phenotype previously associated only with H-2Db homozygotes.

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Selected References

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

  1. Anderson G., Jenkinson E. J., Moore N. C., Owen J. J. MHC class II-positive epithelium and mesenchyme cells are both required for T-cell development in the thymus. Nature. 1993 Mar 4;362(6415):70–73. doi: 10.1038/362070a0. [DOI] [PubMed] [Google Scholar]
  2. Berg L. J., Frank G. D., Davis M. M. The effects of MHC gene dosage and allelic variation on T cell receptor selection. Cell. 1990 Mar 23;60(6):1043–1053. doi: 10.1016/0092-8674(90)90352-f. [DOI] [PubMed] [Google Scholar]
  3. Bix M., Raulet D. Functionally conformed free class I heavy chains exist on the surface of beta 2 microglobulin negative cells. J Exp Med. 1992 Sep 1;176(3):829–834. doi: 10.1084/jem.176.3.829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Britt W. J., Chesebro B. H-2D (Rfv-1) gene influence on recovery from Friend virus leukemia is mediated by nonleukemic cells of the spleen and bone marrow. J Exp Med. 1980 Dec 1;152(6):1795–1804. doi: 10.1084/jem.152.6.1795. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Britt W. J., Chesebro B. H-2D control of recovery from Friend virus leukemia: H-2D region influences the kinetics of the T lymphocyte response to Friend virus. J Exp Med. 1983 Jun 1;157(6):1736–1745. doi: 10.1084/jem.157.6.1736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chesebro B., Bloom M., Wehrly K., Nishio J. Persistence of infectious Friend virus in spleens of mice after spontaneous recovery from virus-induced erythroleukemia. J Virol. 1979 Dec;32(3):832–837. doi: 10.1128/jvi.32.3.832-837.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chesebro B., Miyazawa M., Britt W. J. Host genetic control of spontaneous and induced immunity to Friend murine retrovirus infection. Annu Rev Immunol. 1990;8:477–499. doi: 10.1146/annurev.iy.08.040190.002401. [DOI] [PubMed] [Google Scholar]
  8. Chesebro B., Wehrly K. Rfv-1 and Rfv-2, two H-2-associated genes that influence recovery from Friend leukemia virus-induced splenomegaly. J Immunol. 1978 Apr;120(4):1081–1085. [PubMed] [Google Scholar]
  9. Chesebro B., Wehrly K., Stimpfling J. Host genetic control of recovery from Friend leukemia virus-induced splenomegaly: mapping of a gene within the major histocompatability complex. J Exp Med. 1974 Dec 1;140(6):1457–1467. doi: 10.1084/jem.140.6.1457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chesebro B., Wehrly K. Studies on the role of the host immune response in recovery from Friend virus leukemia. II. Cell-mediated immunity. J Exp Med. 1976 Jan 1;143(1):85–99. doi: 10.1084/jem.143.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Christinck E. R., Luscher M. A., Barber B. H., Williams D. B. Peptide binding to class I MHC on living cells and quantitation of complexes required for CTL lysis. Nature. 1991 Jul 4;352(6330):67–70. doi: 10.1038/352067a0. [DOI] [PubMed] [Google Scholar]
  12. Coffman R. L., Weissman I. L. B220: a B cell-specific member of th T200 glycoprotein family. Nature. 1981 Feb 19;289(5799):681–683. doi: 10.1038/289681a0. [DOI] [PubMed] [Google Scholar]
  13. Doig D., Chesebro B. Anti-Friend virus antibody is associated with recovery from viremia and loss of viral leukemia cell-surface antigens in leukemic mice. Identification of Rfv-3 as a gene locus influencing antibody production. J Exp Med. 1979 Jul 1;150(1):10–19. doi: 10.1084/jem.150.1.10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fairchild P. J., Austyn J. M. Thymic dendritic cells: phenotype and function. Int Rev Immunol. 1990;6(2-3):187–196. doi: 10.3109/08830189009056629. [DOI] [PubMed] [Google Scholar]
  15. Hasenkrug K. J., Cory J. M., Stimpfling J. H. Monoclonal antibodies defining mouse tissue antigens encoded by the H-2 region. Immunogenetics. 1987;25(2):136–139. doi: 10.1007/BF00364282. [DOI] [PubMed] [Google Scholar]
  16. Hestdal K., Ruscetti F. W., Ihle J. N., Jacobsen S. E., Dubois C. M., Kopp W. C., Longo D. L., Keller J. R. Characterization and regulation of RB6-8C5 antigen expression on murine bone marrow cells. J Immunol. 1991 Jul 1;147(1):22–28. [PubMed] [Google Scholar]
  17. Hoatlin M. E., Kozak S. L., Lilly F., Chakraborti A., Kozak C. A., Kabat D. Activation of erythropoietin receptors by Friend viral gp55 and by erythropoietin and down-modulation by the murine Fv-2r resistance gene. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9985–9989. doi: 10.1073/pnas.87.24.9985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hochman J. H., Shimizu Y., DeMars R., Edidin M. Specific associations of fluorescent beta-2-microglobulin with cell surfaces. The affinity of different H-2 and HLA antigens for beta-2-microglobulin. J Immunol. 1988 Apr 1;140(7):2322–2329. [PubMed] [Google Scholar]
  19. Hugo P., Kappler J. W., Godfrey D. I., Marrack P. C. A cell line that can induce thymocyte positive selection. Nature. 1992 Dec 17;360(6405):679–682. doi: 10.1038/360679a0. [DOI] [PubMed] [Google Scholar]
  20. Kisielow P., Teh H. S., Blüthmann H., von Boehmer H. Positive selection of antigen-specific T cells in thymus by restricting MHC molecules. Nature. 1988 Oct 20;335(6192):730–733. doi: 10.1038/335730a0. [DOI] [PubMed] [Google Scholar]
  21. Koller B. H., Marrack P., Kappler J. W., Smithies O. Normal development of mice deficient in beta 2M, MHC class I proteins, and CD8+ T cells. Science. 1990 Jun 8;248(4960):1227–1230. doi: 10.1126/science.2112266. [DOI] [PubMed] [Google Scholar]
  22. Lavigueur A., Bernstein A. p53 transgenic mice: accelerated erythroleukemia induction by Friend virus. Oncogene. 1991 Dec;6(12):2197–2201. [PubMed] [Google Scholar]
  23. Lawlor D. A., Zemmour J., Ennis P. D., Parham P. Evolution of class-I MHC genes and proteins: from natural selection to thymic selection. Annu Rev Immunol. 1990;8:23–63. doi: 10.1146/annurev.iy.08.040190.000323. [DOI] [PubMed] [Google Scholar]
  24. Ledbetter J. A., Herzenberg L. A. Xenogeneic monoclonal antibodies to mouse lymphoid differentiation antigens. Immunol Rev. 1979;47:63–90. doi: 10.1111/j.1600-065x.1979.tb00289.x. [DOI] [PubMed] [Google Scholar]
  25. Li J. P., D'Andrea A. D., Lodish H. F., Baltimore D. Activation of cell growth by binding of Friend spleen focus-forming virus gp55 glycoprotein to the erythropoietin receptor. Nature. 1990 Feb 22;343(6260):762–764. doi: 10.1038/343762a0. [DOI] [PubMed] [Google Scholar]
  26. Miyazawa M., Nishio J., Wehrly K., Jay G., Melvold R. W., Chesebro B. Detailed mapping of the Rfv-1 gene that influences spontaneous recovery from Friend retrovirus-induced leukaemia. Eur J Immunogenet. 1992 Jun;19(3):159–164. doi: 10.1111/j.1744-313x.1992.tb00054.x. [DOI] [PubMed] [Google Scholar]
  27. Moreau-Gachelin F., Tavitian A., Tambourin P. Spi-1 is a putative oncogene in virally induced murine erythroleukaemias. Nature. 1988 Jan 21;331(6153):277–280. doi: 10.1038/331277a0. [DOI] [PubMed] [Google Scholar]
  28. Morrison R. P., Earl P. L., Nishio J., Lodmell D. L., Moss B., Chesebro B. Different H-2 subregions influence immunization against retrovirus and immunosuppression. Nature. 1987 Oct 22;329(6141):729–732. doi: 10.1038/329729a0. [DOI] [PubMed] [Google Scholar]
  29. Paul R., Schuetze S., Kozak S. L., Kozak C. A., Kabat D. The Sfpi-1 proviral integration site of Friend erythroleukemia encodes the ets-related transcription factor Pu.1. J Virol. 1991 Jan;65(1):464–467. doi: 10.1128/jvi.65.1.464-467.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ploegh H. L., Cannon L. E., Strominger J. L. Cell-free translation of the mRNAs for the heavy and light chains of HLA-A and HLA-B antigens. Proc Natl Acad Sci U S A. 1979 May;76(5):2273–2277. doi: 10.1073/pnas.76.5.2273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Polsky D., Lilly F. Suppression of H-2b-associated resistance to Friend erythroleukemia virus by a class I gene from the H-2d major histocompatibility complex haplotype. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9243–9247. doi: 10.1073/pnas.88.20.9243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Potter T. A., Boyer C., Verhulst A. M., Golstein P., Rajan T. V. Expression of H-2Db on the cell surface in the absence of detectable beta 2 microglobulin. J Exp Med. 1984 Jul 1;160(1):317–322. doi: 10.1084/jem.160.1.317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Robertson M. N., Spangrude G. J., Hasenkrug K., Perry L., Nishio J., Wehrly K., Chesebro B. Role and specificity of T-cell subsets in spontaneous recovery from Friend virus-induced leukemia in mice. J Virol. 1992 Jun;66(6):3271–3277. doi: 10.1128/jvi.66.6.3271-3277.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Springer T., Galfré G., Secher D. S., Milstein C. Mac-1: a macrophage differentiation antigen identified by monoclonal antibody. Eur J Immunol. 1979 Apr;9(4):301–306. doi: 10.1002/eji.1830090410. [DOI] [PubMed] [Google Scholar]
  35. Troxler D. H., Ruscetti S. K., Scolnick E. M. The molecular biology of Friend virus. Biochim Biophys Acta. 1980 Sep 22;605(3):305–324. doi: 10.1016/0304-419x(80)90014-1. [DOI] [PubMed] [Google Scholar]
  36. Vremec D., Zorbas M., Scollay R., Saunders D. J., Ardavin C. F., Wu L., Shortman K. The surface phenotype of dendritic cells purified from mouse thymus and spleen: investigation of the CD8 expression by a subpopulation of dendritic cells. J Exp Med. 1992 Jul 1;176(1):47–58. doi: 10.1084/jem.176.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Vukmanović S., Grandea A. G., 3rd, Faas S. J., Knowles B. B., Bevan M. J. Positive selection of T-lymphocytes induced by intrathymic injection of a thymic epithelial cell line. Nature. 1992 Oct 22;359(6397):729–732. doi: 10.1038/359729a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Watts S., Vogel J. M., Harriman W. D., Itoh T., Stauss H. J., Goodenow R. S. DNA sequence analysis of the C3H H-2Kk and H-2Dk loci. Evolutionary relationships to H-2 genes from four other mouse strains. J Immunol. 1987 Dec 1;139(11):3878–3885. [PubMed] [Google Scholar]
  39. Zijlstra M., Bix M., Simister N. E., Loring J. M., Raulet D. H., Jaenisch R. Beta 2-microglobulin deficient mice lack CD4-8+ cytolytic T cells. Nature. 1990 Apr 19;344(6268):742–746. doi: 10.1038/344742a0. [DOI] [PubMed] [Google Scholar]

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