Skip to main content
Log in

Experimental allergic orchitis in mice

I. Genetic control of susceptibility and resistance to induction of autoimmune orchitis

  • Published:
Immunogenetics Aims and scope Submit manuscript

Abstract

Inbred strains of mice were studied for their susceptibility to the induction of experimental allergic orchitis after sensitization with mouse testicular homogenate in complete Freund's adjuvant accompanied by injections of extract from Bordetella pertussis. Susceptibility to autoimmune orchitis was found to be linked to the major histocompatibility complex in BALB/c and C57BL/10 mice and mapped to genes encoded within the H-2D dregion. In five of six groups of bidirectional (susceptible × resistant) F1 hybrids, H-2D d-linked susceptibility was inherited as a dominant autosomal trait. However, in (BALB/cByJ × DBA/2J)F1 and (DBA/2J × BALB/cByJ)F1 hybrids, dominant autosomal resistance to the induction of autoimmune orchitis was observed. Backcross analysis between the resistant F1 hybrid and the susceptible BALB/cByJ parent suggests that a single independently segregating DBA/2J locus is capable of negating H-2D d-linked susceptibility, and controls resistance to the induction of autoimmune orchitis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

BP extract:

Bordetella pertussis extract

CFA:

complete Freund's adjuvant

EAO:

experimental allergic orchitis

Ir:

immune response

MHC:

major histocompatibility complex

MLH:

mouse liver homogenate

MTH:

mouse testis homogenate

PI:

pathology index

References

  • Benacerraf, B. and Katz, D. H.: The histocompatibility-linked immune response genes. Adv. Cancer Res. 21: 121, 1975

    Google Scholar 

  • Bergman, R. K., Munoz, J. J., and Portis, J. L.: Vascular permeability changes in the central nervous system of rats with hyperacute experimental allergic encephalomyelitis induced with the acid of a substance from Bordetella pertussis. Infect. Immun. 21: 627–637, 1978

    Google Scholar 

  • Bernard, C. C. A.: Experimental autoimmune encephalomyelitis in mice. Genetic control of susceptibility. J. Immunogenet. 3: 263–274, 1976

    Google Scholar 

  • Bernard, C. C. A., Mitchell, G. F., Leydon, J., and Bargerbos, A.: Experimental allergic orchitis in T-cell deficient mice. Int. Arch. Allergy Appl. Immunol. 56: 256–263, 1978

    Google Scholar 

  • Blanden, R. V. and Kees, U.: Cytotoxic T-cell responses show more restricted specificity for self than for non-self H-2D-coded antigens. J. Exp. Med. 147: 1661–1670, 1978

    Google Scholar 

  • Christadoss, P., Kong, Y. M., Elrehewy, M., Rose, N. R., and David, C. S.: Genetic control of Tlymphocyte proliferative response to thyroglobulin in mice. In N. R. Rose, P. E. Bigazzi, and N. L. Warner (eds.): Genetic Control of Autoimmune Disease, pp. 445–454, Elsevier/North-Holland Press, New York, 1978

    Google Scholar 

  • Fritz, T. E., Lombard, L. S., Tyler, S. A., and Norris, W. P.: Pathology and familial incidence of orchitis and its relation to thyroiditis in a closed beagle colony. Exp. Mol. Pathol. 24: 142–158, 1976

    Google Scholar 

  • Fuchs, S., Nevo, D., Tarrab-Hazdai, R., and Yaar, I.: Strain differences in the autoimmune response of mice to acetylcholine receptors. Nature 263: 329–330, 1976

    Google Scholar 

  • Gasser, D. L., Newlin, C. M., Palm, J., and Gonates, N. K.: Genetic control of susceptibility to experimental encephalomyelitis in rats. Science 181: 872–873, 1973

    Google Scholar 

  • Gasser, D. L., Palm, J., and Gonates, N. K.: Genetic control of susceptibility to experimental allergic encephalomyelitis and the Ag-B locus of rats. J. Immunol. 115: 431–433, 1975

    Google Scholar 

  • Hansen, T. H., Ozato, K., and Sachs, D. H.: Heterogeneity of H-2D region associated genes and gene products. Adv. Immunol. 34: 39–70, 1983

    Google Scholar 

  • Hatakeyama, S., Takizawa, T., and Kawahara, Y.: Focal atrophy of the seminiferous tubule in the human testis. Acta Pathol. Jpn. 29: 901–910, 1979

    Google Scholar 

  • Klein, J.: Biology of the Mouse Histocompatibility-2 Complex, Springer-Verlag, New York, 1975

    Google Scholar 

  • Kohno, S., Munoz, J. A., Williams, T. M., Teuscher, C., Bernard, C. C. A., and Tung, K. S. K.: Immunopathology of murine experimental allergic orchitis. J. Immunol. 130: 2675–2682, 1983

    Google Scholar 

  • Kong, Y. M., David, C. S., Giraldo, A. A., Elrehewy, M., and Rose, N. R.: Regulation of autoimmune response to mouse thyroglobulin: Influence of H-2D-end genes. J. Immunol. 123: 15–18, 1979

    Google Scholar 

  • Lando, Z. and Ben-Nun, A.: Experimental autoimmune encephalomyelitis mediated by T-cell line. II. Specific requirements and the role of pertussis vaccine for the in vitro activation of the cells and induction of disease. Clin. Immunol. Immunopathol. 30: 290–303, 1984

    Google Scholar 

  • Lando, Z., Teitelbaum, D., and Arnon, R.: Genetic control of susceptibility to experimental allergic encephalomyelitis in mice. Immunogenetics 9: 435–442, 1979

    Google Scholar 

  • Lee, J. M. and Olitsky, P. K.: Simple method for enhancing development of acute disseminated encephalomyelitis in mice. Proc. Soc. Exp. Biol. Med. 89: 263–266, 1955

    Google Scholar 

  • Levine, S. and Sowinski, R.: Experimental allergic encephalomyelitis in inbred and outbred mice. J. Immunol. 110: 139–143, 1973

    Google Scholar 

  • Levine, S. and Sowinski, R.: Experimental allergic encephalomyelitis in congenic strains of mice. Immunogenetics 1: 352–356, 1974

    Google Scholar 

  • Linthicum, D. S.: Development of acute autoimmune encephalomyelitis in mice: Factors regulating the effector phase of the disease. Immunobiology 162: 211–220, 1982

    Google Scholar 

  • Linthicum, D. S. and Frelinger, J. A.: Acute autoimmune encephalomyelitis in mice. II. Susceptibility is controlled by the combination of H-2 and histamine sensitization genes. J. Exp. Med. 156: 31–40, 1982

    Google Scholar 

  • Moorhead, J. W.: Soluble factors in tolerance and contact sensitivity to DNFB in mice. II. Genetic requirements for suppression of contact sensitivity by soluble suppressor factor. J. Immunol. 119: 1773–1777, 1977

    Google Scholar 

  • Morse, S. I. and Morse, J. H.: Isolation and properties of the leukocytosis- and lymphocytosis-promoting factor of Bordetella pertussis. J. Exp. Med. 143: 1483–1502, 1976

    Google Scholar 

  • Munoz, J. J. and Bergman, R. K.: Bordetella pertussis: Immunological and other biological activities. Immunol. Sci. 4: 1–0, 1977

    Google Scholar 

  • Ovary, Z., Vris, T. W., De Szalay, C., Vaz, N. M., and Iritani, C. A.: Independent segregation of the H-2 locus and the locus for responsiveness to histamine-sensitizing factor. Proc. Natl. Acad. Sci. U.S.A. 70: 2500–2501, 1973

    Google Scholar 

  • Raine, C. S., Barnett, L. B., Brown, A., Behar, T., and McFarlin, D. E.: Neurolpathology of experimental allergic encephalomyelitis in inbred strains of mice. Lab. Invest. 43: 150–157, 1980

    Google Scholar 

  • Rose, N. R., Bacon, L. D., Sundick, R. S., Kong, Y. M., Esquivel, P., and Bigazzi, P. E.: Genetic regulation in autoimmune thyroiditis. In N. Talad (ed.): Autoimmunity: Genetic, Immunologic, Virologic and Clinical Aspects, pp. 63–87, Academic Press, New York, 1977

    Google Scholar 

  • Rudofsky, U. H., Dilwith, R. L., and Tung, K. S. K.: Susceptibility differences of inbred mice to induction of autoimmune renal tubulointertitial lesions. Lab. Invest. 43: 463–470, 1980

    Google Scholar 

  • Salomon, F. and Hedinger, C. E.: Abnormal basement membrane structures of seminiferous tubules in infertile men. Lab. Invest. 47: 543–554, 1982

    Google Scholar 

  • Salomon, F., Saremaslani, P., Jakob, M., and Hedinger, C. E.: Immune complex orchitis in infertile men. Immunoelectron microscopy of abnormal basement membrane structures. Lab. Invest. 47: 555–567, 1982

    Google Scholar 

  • Shirai, T.: Genetic basis of amoimmune disease in New Zealand mice. In Y. Yamamura and T. Tada (eds.): Progress in Immunology V, pp. 1139–1154, Academic Press, New York, 1983

    Google Scholar 

  • Steinman, L., Smith, M. E., and Forno, L. S.: Genetic control of susceptibility to experimental allergic neuritis and the immune response to P2 protein. Neurology 31: 950–955, 1981

    Google Scholar 

  • Svejgaard, A., Platz, P., and Ryder, L. P.: HLA and disease 1982—A survey. Immunol. Rev. 70: 193–218, 1983

    Google Scholar 

  • Tomazic, V., Rose, N. R., and Shreffler, D. C.: Autoirnmune murine thyroiditis. IV. Localization of genetic control of the immune response. J. Immunol. 112: 965–969, 1974

    Google Scholar 

  • Tung, K. S. K., Unanue, E. R., and Dixon, F. J.: The immunopathology of experimental allergic orchitis. Am. J. Pathol. 60: 313–324, 1970

    Google Scholar 

  • Tung, K. S. K., Ellis, L., Teuscher, C., Meng, A., Blaustein, J. C., Kohno, S., and Howell, R.: The black mink (Mustela vison). A natural model of immunologic male infertility. J. Exp. Med. 154: 1016–1032, 1981

    Google Scholar 

  • Tung, K. S. K., Ellis, L. E., Childs, G. V., and Dufau, M.: The dark mink: A model of male infertility. Endocrinology 114: 922–929, 1984

    Google Scholar 

  • Wekerle, H.: Immunological T-cell memory in the in vitro-induced experimental autoimmune orchitis. J. Exp. Med. 147: 233–250, 1978

    Google Scholar 

  • Wekerle, H. and Begemann, M.: Experimental autoimmune orchitis: in vitro induction of an autoimmune disease. J. Immunol. 116: 159–161, 1976

    Google Scholar 

  • Wekerle, H. and Begemann, M.: In vitro induction of experimental autoimmune orchitis. Characterization of a primary T lymphocyte response against testicular self antigens. Eur. J. Immunol. 8: 294–302, 1978

    Google Scholar 

  • Wekerle, H., Born, W., Kyewski, B., and Prester, M.: Cellular basis of immunological self tolerance: Cellular Immoral regulation. Behring Inst. Mitt. 65: 71–86, 1980

    Google Scholar 

  • Williams, R. M. and Moore, M. J.: Linkage of susceptibility to experimental allergic encephalomyelitis to the major histocompatibility locus in the rat. J. Exp. Med. 138: 775–783, 1973

    Google Scholar 

  • Wooley, P. H., Luthra, H. S., Stuart, J. M., and David, C. S.: Type II collagen-induced arthritis in mice. I. Major histocompatibility complex (I region) linkage and antibody correlates. J. Exp. Med. 154: 688–700, 1981

    Google Scholar 

  • Wong, T. W., Straus, F. H., and Warner, N. E.: Testicular biopsy in the study of male infertility. I. Testicular causes of infertility. Arch. Pathol. 95: 151–159, 1973

    Google Scholar 

  • Yasuda, T., Tsumita, T., Nagai, E., Mitsuzawa, Y., and Ohtani, S.: Experimental allergic encephalomyelitis (EAE) in mice. I. Induction of EAE with mouse spinal cord homogenate and myelin basic protein. Jpn. J. Exp. Med. 45: 423–427, 1975

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Teuscher, C., Smith, S.M., Goldberg, E.H. et al. Experimental allergic orchitis in mice. Immunogenetics 22, 323–333 (1985). https://doi.org/10.1007/BF00430916

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00430916

Keywords

Navigation