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H-2-Mediated resistance to an ecotropic type C retrovirus: Localization of controlling genes and ontogenic studies of resistance

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Abstract

H-2 recombinant mice of the C57BL/10 series were used to study resistance to infection by an ecotropic (B-tropic) type C retrovirus. The gene(s) responsible for resistance was mapped to theI- E/I-C subregions. Ontogenic studies indicated that thisI-region mediated resistance is not present in the neonate but develops with age, and is firmly established within 2 weeks after birth. This temporary neonatal susceptibility in mice of resistant genotype is not the result of active suppression of the immune response.

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References

  • Adams, J. M., Jepperson, P. G. N., Sanger, F., and Barrell, B. G.: Nucleotide sequence from the coat protein cistron of R17 bacteriophage RNA.Nature 223: 1009–1014, 1969

    PubMed  Google Scholar 

  • Altman, P. L. and Katz, D. D.:Inbred and Genetically Defined Strains of Laboratory Animals. Part I: Mouse and Rat, p. 124. Fed. of Am. Soc. for Exp. Biol, Bethesda, 1979

    Google Scholar 

  • Benacerraf, B. and Dorf, M. E.: Genetic control of immune response and immune suppression byI region genes.Cold Spring Harbor Symp. Quant. Biol. 41: 465–475, 1976

    Google Scholar 

  • Benacerraf, B. and Germain, R. N.: The immune response genes of the major histocompatibility complex.Immunol. Rev. 38: 70–119, 1978

    PubMed  Google Scholar 

  • Billeter, M. A., Parsons, J. T., and Coffin, J. M.: The nucleotide sequence complexity of avian tumor virus RNA.Proc. Natl. Acad. Sci. U.S.A. 71: 3560–3564, 1974

    PubMed  Google Scholar 

  • Cunningham, A. J. and Szenberg, A.: Further improvements in the plaque assay technique for detecting single antibody-forming cells.Immunology 14: 599–600, 1968

    PubMed  Google Scholar 

  • David, C. S., Stimpfling, J. H., and Shreffler, D. C.: Identification of specificityH-2.7 as an erythrocyte antigen: control by an independent locus,H-2G, between theS andD regions.Immunogenetics 2: 131–139, 1975

    Google Scholar 

  • Debré, P., Gisselbrecht, S., Pozo, F., and Levy, J. P.: Genetic control of sensitivity to Moloney leukemia virus in mice II. Mapping of three resistant genes within theH-2 complex.J. Immunol. 123: 1806–1812, 1979

    PubMed  Google Scholar 

  • Green, M. L., Dorf, M. E., Pierres, M., and Benacerraf, B.: Reduction of syngeneic tumor growth by an antiI-J alloantiserum specific for suppressor T cells.Proc. Natl. Acad. Sci. U.S.A. 74: 5118–5121, 1977

    PubMed  Google Scholar 

  • Green, W. R., Nowinski, R. C., and Henney, C. S.: The generation and specificity of cytotoxic T cells raised against syngeneic tumor cells bearing AKR/Gross, murine leukemia virus antigens.J. Exp. Med. 150: 51–66, 1979

    PubMed  Google Scholar 

  • Hämmerling, G. J., Hämmerling, U., and Flaherty, L.: Qat-4 and Qat-5 new murine T-cell antigens governed by the Tla region and identified by monoclonal antibodies.J. Exp. Med. 150: 108–116, 1979

    PubMed  Google Scholar 

  • Huang, C.-M. and Klein, J.: Murine antigen H-2.7: Its genetics, tissue expression, and strain distribution.Immunogenetics 9: 233–243, 1979

    Google Scholar 

  • Jolicoeur, P. and Baltimore, D.: Effect ofFv-1 gene product on proviral DNA formation and integration in cells infected with murine leukemia viruses.Proc. Natl. Acad. Sci. U.S.A. 73: 2236–2240, 1976

    PubMed  Google Scholar 

  • Jones, P. P., Murphy, D. B., and McDevitt, H. O.: Two-gene control of the expression of a murineIa antigen.J. Exp. Med. 148: 925–939, 1978

    PubMed  Google Scholar 

  • Kipps, T. J., Benacerraf, B., and Dorf, M. E.: Regulation of antibody heterogeneity by suppressor T cells: diminishing suppressor T cell activity increased the number of dinitrophenyl clones in mice immunized with dinitrophenyl-poly (Glu, Lys, Phe) or dinitrophenyl-poly (Glu, Lys, Ala).Proc. Natl. Acad. Sci. U.S.A. 75: 2914–2917, 1978

    PubMed  Google Scholar 

  • Klein, J., Hauptfeld, V., and Hauptfeld, M.: Evidence for a fifth (G) region in theH-2 complex of the mouse.Immunogenetics 2: 141–150, 1975

    Google Scholar 

  • Klein, J., Flaherty, L., VandeBerg, J. L., and Shreffler, D. C.H-2 haplotypes, genes, regions and antigens: First listing.Immunogenetics 6: 489–512, 1978

    Google Scholar 

  • Lander, M. R., Moll, B., and Rowe, W. P.: A procedure for culture of cells from mouse tail biopsies: Brief communication.J. Natl. Cancer Inst. 60: 477–478, 1978

    PubMed  Google Scholar 

  • Lee, J. C., Ihle, J. N., and Heubner, R.: The humoral immune response of NIH Swiss and SWR/J mice to vaccination with formalinized AKR or Gross murine leukemia virus.Proc. Natl. Acad. Sci. U.S.A. 74: 343–347, 1977

    PubMed  Google Scholar 

  • Lilly, F. and Pincus, T.: Genetic control of murine viral leukemogenesis.Adv. Cancer Res. 17: 231–277, 1973

    Google Scholar 

  • Lonai, P. and Haran-Ghera, N.: Resistance genes to murine leukemia in theI immune response gene region of theH-2 complex.J. Exp. Med. 146: 1164–1168, 1977

    Google Scholar 

  • Lu, C. Y., Calami, E. G., and Unanue, E. R.: A defect in the antigen presenting function of macrophages from neonatal mice.Nature 282: 327–329, 1979

    PubMed  Google Scholar 

  • Melief, C. J. M., Datta, S. K., Louie, S., Johnson, S., and Schwartz, R. S.: Splenocyte plaque assay for the detection of murine leukemia virus.Proc. Soc. Exp. Biol. Med. 149: 1015–1018, 1975a

    PubMed  Google Scholar 

  • Melief, C. J. M., Louie, S., and Schwartz, R. S.: Ecotropic leukemia viruses in congenic C57BL mice; natural dissemination by milk-borne infection.J. Natl. Cancer Inst. 55: 691–698, 1975b

    PubMed  Google Scholar 

  • Meruelo, D., Lieberman, M., Ginzton, N., Deak, B., and McDevitt, H. O.: Genetic control of radiation leukemia virus-induced tumorigenesis I. Role of the major murine histocompatibility complex,H-2.J. Exp. Med. 146: 1079–1087, 1977

    Google Scholar 

  • Meruelo, D., Nimelstein, S. H., Jones, P. P., Lieberman, M., and McDevitt, H. O.: Increased synthesis and expression ofH-2 antigens on thymocytes as a result of radiation leukemia virus infection: A possible mechanism forH-2 linked control of virus-induced neoplasia.J. Exp. Med. 147: 478–487, 1978

    Google Scholar 

  • Meruelo, D.: A role for elevatedH-2 antigen expression in resistance to neoplasia caused by radiation-induced leukemia virus. Enhancement of effective tumor surveillance by killer lymphocytes.J. Exp. Med. 149: 898–909, 1979

    Google Scholar 

  • Mosier, D. E.: Ontogeny of mouse lymphocyte function I. Paradoxical elevation of reactivity of allogeneic cells and phytohemagglutinin in BALB/c fetal thymocytes.J. Immunol. 112: 305–310, 1974

    PubMed  Google Scholar 

  • Mosier, D. E. and Johnson, B. M.: Ontogeny of mouse lymphocyte function. II. Development of the ability to produce antibody is modulated by T lymphocytes.J. Exp. Med. 141: 216–226, 1975

    PubMed  Google Scholar 

  • Mosier, D. E., Zaldivar, N. M., Goldings, E., Mond, J., Scher, I., and Paul, W. E.: Formation of antibody in the newborn mouse: study of T-cell-independent antibody response.J. Infect. Dis. 136: 14–19, 1977a

    Google Scholar 

  • Mosier, D. E., Mathieson, B. J., and Campbell, P. S.: Ly phenotype and mechanism of action of mouse neonatal suppressor T cells.J. Exp. Med. 146: 59–73, 1977b

    PubMed  Google Scholar 

  • Murphy, D. B.: The I-J subregion of the murineH-2 gene complex.Springer Seminars in Immunopathology 1: 111–131, 1978

    Google Scholar 

  • Nowinski, R. C. and Doyle, T.: Antibody to murine leukemia virus: genetic control linked to theH-2 locus in PL mice.J. Immunol. 117: 350–351, 1976

    PubMed  Google Scholar 

  • Okumura, K., Herzenberg, L. A., Murphy, D. B., McDevitt, H. O., and Herzenberg, L. A.: Selective expression ofH-2 (I region) loci controlling determination in helper and suppressor T lymphocytes.J. Exp. Med. 144: 685–698, 1976

    PubMed  Google Scholar 

  • Pierres, M., Germain, R. N., Dorf, M. E., and Benacerraf, B.:In vivo effects ofanti-la alloantisera. I. Elimination of specific suppression byin vivo administration of antisera specific forI-J controlled determinants.J. Exp. Med. 147: 656–666, 1978

    PubMed  Google Scholar 

  • Rodriguez, G., Andersson, G., Wigzell, H., and Peck, A. B.: Non T-cell nature of the naturally occuring spleen-associated suppressor cells present in the newborn mouse.Eur. J. Immunol. 9: 737–746, 1979

    PubMed  Google Scholar 

  • Schwartz, R. S. and Datta, S. K.: Genetically determined resistance mechanisms in leukemia.Blood Cells 3: 591–604, 1977

    Google Scholar 

  • Sherwin, W. K., and Rowlands, Jr., D. T.: Determinants of the hierarchy of humoral immune responsiveness during ontogeny.J. Immunol. 115: 1549–1554, 1975

    PubMed  Google Scholar 

  • Shreffler, D. C.: The S region of the mouse major histocompatibility complexH-2. Genetic variation and functional role in the complement system.Transplant. Rev. 32: 140–167, 1976

    PubMed  Google Scholar 

  • Tsichlis, P. N., Bear, S. E., Tucker, H. St., G., and Schwartz, R. S.: Genetic resistance to ecotropic type-C RNA viruses.Immune Mechanisms and Disease, pp. 101–130, Academic Press, Inc., New York, 1979

    Google Scholar 

  • Tucker, H. St., G., Weens, J., Tsichlis, P. N., Schwartz, R. S., Khiroya, R., and Donnelly, J.: Influence ofH-2 complex on susceptibility to infection by murine leukemia virus.J. Immunol. 118: 1239–1243, 1977

    Google Scholar 

  • Urba, W. J. and Hildmann, W. H.:H-2 linked recessiveIr gene regulation of high antibody responsiveness to TNP hapten conjugated to autogenous albumin.Immunogenetics 6: 433–445, 1978

    Google Scholar 

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Bear, S.E., Tsichlis, P.N. & Schwanz, R.S. H-2-Mediated resistance to an ecotropic type C retrovirus: Localization of controlling genes and ontogenic studies of resistance. Immunogenetics 11, 451–465 (1980). https://doi.org/10.1007/BF01567814

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  • DOI: https://doi.org/10.1007/BF01567814

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