Abstract
Chickens from Regional Poultry Research Laboratory (RPRL) inbred line 63 are resistant to virally-induced Marek's disease (MD) and lymphoid leukosis (LL) and are relatively strong regressors of virally-induced Rous sarcomas. In contrast, RPRL line 100 chickens are highly susceptible to MD and LL and are weaker regressors of Rous sarcomas than line 63. RPRL lines 100 and 63 differ for alleles at the IgG-1 (G-1) allotype locus, but have identical IgM-1 (M-1) allotype alleles. To test the possible association of the G-1 locus with variations in resistance to virally-induced tumors, homozygous and heterozygous genotypes among F3 crosses were infected. F3 chickens with different G-1 types were comparable in their resistance to MD tumors following inoculation with the JM strain of the MD virus, and for their ability to regress Rous sarcoma tumors induced by the Rous sarcoma virus (RSV) RAV-1. However, following RAV-1 virus infection a smaller proportion of G-1 a/G-1 a F3 or F4 birds developed LL tumors than G-1 a/G-1 e and G-1 e/G-1 e birds. Genes determining immunoglobulin heavy chains were therefore associated with a recessive resistance to B-cell lymphomagenesis in chickens.
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Bacon, L. D., Polley, C. R., Cole, R. K., and Rose, N. R.: Genetic influences on spontaneous autoimmune thyroiditis in (CS x OS) F2 chickens. Immunogenetics 12: 339–349, 1981a
Bacon, L. D., Witter, R. L., Crittenden, L. B., Fadly, A., and Motta, J.: B-haplotype influence on Marek's disease, Rous sarcoma and lymphoid leukosis virus-induced tumor in chickens. Poult. Sci. 60: 1132–1139, 1981b
Bacon, L. D., Fadly, A. M., and Crittenden, L. B.: Avian leukosis virus (ALV) infection in 15.B congenic chickens. Poult. Sci. 63: 558 (Abstract), 1984
Bacon, L. D., Fredericksen, T. L., Gilmour, D. G., Fadly, A. M., and Crittenden, L. B.: Tests of association of lymphocyte alloantigen genotypes with resistance to viral oncogenesis in chickens. II. Rous sarcoma and lymphoid leukosis in progeny derived from 63 x 15, and 100 x 63 crosses. Poult. Sci. 64: 39–47, 1985
Balcarova, J., Derka, J., Hála, K., and Hraba, T.: Genetic control of immune response to dinitrophenol group in inbred lines of chickens. Folia Biol. (Praha) 20: 346–349, 1974
Benedict, A. A.: Immunoglobulin allotypes: Chicken. In P. L. Altman and D. D. Katz (eds.): Inbred and Genetically Defined Strains of Laboratory Animals Part 2. Hamster, Guinea Pig, Rabbit and Chickens, pp. 661–664, Federation of American Societies for Experimental Biology, Handbook 111, Bethesda, 1979
Benedict, A. A., Pollard, L. W., Marrow, P. R., Abplanalp, H. A., Maurer, P. H., and Briles, W. E.: Genetic control of immune responses in chickens. I. Responses to a terpolymer of poly(Gly60Ala30Tyr10) associated with the major histocompatibility complex. Immunogenetics 2: 313–324, 1975
Biozzi, G., Stiffel, C., Mouton, D., and Bouthillier, Y.: Selection of lines of mice with high and low antibody responses to complex immunogens. In B. Benacerraf (ed.): Immunogenetics and Immunodeficiency, pp. 180–227, MTP Press Ltd., Lancaster, 1975
Briles, W. E. and Briles, R. W.: Identification of haplotypes of the chicken major histocompatibility complex (B). Immunogenetics 15: 449–459, 1982
Briles, W. E., Briles, R. W., Taffs, R. E., and Stone, H. A.: Resistance to a malignant lymphoma in chickens is mapped to subregion of major histocompatibility (B) complex. Science 219: 977–979, 1983
Chubb, R. C. and Churchill, A. E.: Precipitating antibodies associated with Marek's disease. Vet. Rec. 82: 4–13, 1968
Collins, W. M., Briles, W. E., Zsigray, R. M., Dunlop, W. R., Corbett, A. C., Clark, K. K., Marks, J. L., and McGrail, T. P.: The B-locus (MHC) in the chicken: Association with the fate of RSV-induced tumors. Immunogenetics 5: 333–343, 1977
Collins, W. M., Heinzelmann, E. W., Corbett, A. C., Zsigray, R. M., and Dunlop, W. R.: Rous sarcoma regression in seven highly inbred lines of White Leghorns. Poult. Sci. 59: 1172–1177, 1980
Cooper, M. D., Purchase, H. G., Beckman, D. E., and Gathings, W. E.: Studies on the nature of the abnormality of B-cell differentiation in avian lymphoid leukosis: Production of heterogeneous IgM by tumor cells. J. Immunol. 113: 1211–1222, 1974
Corcoran, L. M., Cory, S., and Adams, J. M.: Transposition of the immunoglobulin heavy chain enhancer to the myc oncogene in a murine plasmacytoma. Cell 40: 71–79, 1985
Crews, S., Barth, R., Hood, L., Prehn, J., and Calame, K.: Mouse c-myc is located on chromosome 15 and translocated to chromosome 12 in plasmacytomas. Science 218: 1319–1321, 1982
Crittenden, L. B. and Kung, H. J.: Mechanisms of induction of lymphoid leukosis and related neoplasms by avian leukosis viruses. In J. M. Goldman and O. Jarrett (eds.): Leukemia and Lymphoma Research, Vol. 1, Mechanisms of Viral Leukaemogenesis, pp. 65–88, Churchill-Livingstone, New York, 1984
Crittenden, L. B., Eagen, D. A., and Gulvas, F. A.: Assays for endogenous and exogenous lymphoid leukosis viruses and chick helper factor with RSV(−) cell lines. Infect. Immun. 24: 379–386, 1979a
Crittenden, L. B., Witter, R. L., Okazaki, W., and Neiman, P. E.: Lymphoid neoplasms in chicken flocks free of infection with exogenous avian tumor viruses. J. Natl. Cancer Inst. 63: 191–199, 1979b
Fahrlander, P. D., Sumegi, J., Yang, J. Q., Wiener, F., Marcu, K. B., and Klein, G.: Activation of the c-myc oncogene by the immunoglobulin heavy-chain gene enhancer after multiple switch regionmediated chromosome rearrangement in a murine plasmacytoma. Proc. Natl. Acad. Sci. U.S.A. 82: 3746–3750, 1985
Foppoli, J. M. and Benedict, A. A.: An allotypic marker on chicken immunoglobulin light chains. J. Immunol. 122: 1681–1685, 1979
Foppoli, J. M. and Benedict, A. A.: Localization of two chicken IgM allotypes to H chains. Mol. Immunol. 17: 439–444, 1980
Foppoli, J. M., Ch'ng, L. K., Benedict, A. A., Iványi, J., Derka, J., and Wakeland, E. K.: Genetic nomenclature for chicken immunoglobulin allotypes: An extensive survey of inbred lines and antisera. Immunogenetics 8: 385–404, 1979
Games, P. A.: An improved t table for simultaneous control g contrasts. J. Am. Stat. Assoc. 72: 531–534, 1977
Hála, K., Boyd, R., and Wick, G.: Chicken major histocompatibility complex and disease. Scand. J. Immunol. 14: 607–616, 1981
Hayward, W. S., Neel, B. H., and Astrin, S. M.: Activation of a cellular one gene by promoter insertion in ALV-induced lymphoid leukosis. Nature 290: 475–480, 1981
Iványi, J.: Polymorphism of chicken serum allotypes. J. Immunogenet. 2: 69–78, 1975
Korsmeyer, J. J. and Waldman, T. A.: Immunoglobulin genes: Rearrangement and translocation in human lymphoid malignancy. J. Clin. Immunol. 4: 1–11, 1984
Neiman, P., Wolf, C., Enrietto, P. J., and Cooper, G. M.: A retroviral myc gene induces preneoplastic transformation of lymphocytes in a bursal transplantation assay. Proc. Natl. Acad. Sci U.S.A. 82: 222–226, 1985
Neumann, U. and Witter, R. L.: Differential diagnosis of lymphoid leukosis and Marek's disease by tumor-associated criteria. I. Studies on experimentally infected chickens. Avian Dis. 23: 417–425, 1979
Payne, L. N. and Rennie, M.: The proportions of B and T lymphocytes in lymphomas, peripheral nerves and lymphoid organs in Marek's disease. Avian Pathol. 5: 147–154, 1976
Pink, J. R. L.: An allotypic marker on chicken immunoglobulin M. Eur. J. Immunol. 4: 679–681, 1974
Pink, J. R. L. and Iványi, J.: Close linkage between genes coding for allotypic markers on chicken IgG and IgM. Eur. J. Immunol. 5: 506–507, 1975
Purchase, H. G., Gilmour, D. G., Romero, C. H., and Okazaki, W.: Postinfection genetic resistance to avian lymphoid leukosis resides in B target cell. Nature 270: 61–62, 1977
Roussel, M., Saule, S., Lagrou, C., Rommens, C., Beug, H., and Graf, T.: Three new types of viral oncogene of cellular origin speck for hematopoietic cell transformation. Nature 281: 452–455, 1979
Rowley, J. D.: Identification of the constant chromosome regions involved in human hematologic malignant disease. Science 216: 749–750, 1982
Schierman, L. W. and Nordskog, A. W.: Relationship of blood type to histocompatibility in chickens. Science 134: 1008–1009, 1961
Schierman, L. W., Watanabe, D. H., and McBride, R. A.: Genetic control of Rous sarcoma regression in chickens: Linkage with the major bistocompatibility complex. Immunogenetics 5: 325–333, 1977
Sevoian, M., Chamberlain, D. M., and Counter, F. T.: Avian lymphomatosis. 1. Experimental reproduction of the neural and visceral forms. Vet. Med. 57: 500–501, 1962
Sokal, R. R. and Rohlf, F. J. (eds.): In: Biometry, pp. 601–607, W. H. Freeman and Co., San Francisco, 1969
Solomon, J. J., Burmester, B. R., and Fredrickson, T. N.: Investigations of lymphoid leukosis infection in genetically similar chicken populations. Avian Dis. 10: 477–484, 1966
Stephens, E. A., Witter, R. L., Lee, L. F., Sharma, J. M., Nazerian, K., and Longenecker, B. M.: Characteristics of JMV Marek's disease tumor: A nonproductively infected transplantable cell lacking rescuable virus. J. Natl. Cancer Inst. 57: 865–874, 1976
Stone, H. A.: Use of highly inbred chickens in research. USDA Technical Bulletin, no. 1514, 1975
Taub, R., Kirsch, I., Morton, C., Lenoir, G., Swan, D., Tronick, S., Aaronson, S., and Leder, P.: Translocation of the c-myc gene into the immunoglobulin heavy chain locus in human Burkitt's lymphoma and murine plasmacytoma cells. Proc. Natl. Acad. Sci. U.S.A. 79: 7837–7841, 1982
van Loghem, E.: The immunoglobulin genes: Genetics, biological and clinical significance. Clin. Immunol. Allergy 4: 607–622, 1984
Wakeland, E. K., Foppoli, J. M., and Benedict, A. A.: Structural and genetic studies on chicken 7S immunoglobulin allotypes. III. Proposed nomenclature for the CS-gene alleles. J. Immunol. 119: 1218–1222, 1977
Witter, R. L., Nazerian, K., Purchase, H. G., and Burgoyne, G. H.: Isolation from turkeys of a cell-associated herpesvirus antigenically related to Marek's disease virus. Am. J. Vet. Res. 31: 325–338, 1970
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Bacon, L.D., Ch'ng, L.K., Spencer, J. et al. Tests of association of immunoglobulin allotype genes and viral oncogenesis in chickens. Immunogenetics 23, 213–220 (1986). https://doi.org/10.1007/BF00373015
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DOI: https://doi.org/10.1007/BF00373015