Immunogenetics

, Volume 27, Issue 6, pp 414–425 | Cite as

Molecular characterization and genetic mapping of class I and class II MHC genes of the domestic cat

  • Naoya Yuhki
  • Stephen J. O'Brien
Original Articles

Abstract

The major histocompatibility complex (MHC) of the domestic cat has been poorly characterized to date, primarily because of numerous difficulties in the preparation of allotypic sera. We present here a comparative analysis of class I and class II genes in domestic cat populations using molecular probes of the MHC from man and mouse. The cat possesses a minimum of 20 class I loci and 5 class II genes per haploid genome. Class I genes of the domestic cat expressed limited restriction fragment length polymorphism. The average percent difference of the size of DNA fragments between individual cats was 9.0 %, a value five times lower than the value for mice, but comparable to the human DNA polymorphism level. Class I and class II genes were both genetically mapped to feline chromosome B2 using a panel of rodent x cat somatic cell hybrids. Since feline chromosome B2 is syntenically homologous to human chromosome 6 and mouse chromosome 17, these results affirm the linkage conservation of the MHC-containing linkage group in the three mammalian orders.

Keywords

Major Histocompatibility Complex Linkage Group Restriction Fragment Length Polymorphism Cell Hybrid Mouse Chromosome 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Albert, E. D., Baur, M. P., and Mayr, W. R. (eds.): Histocompatibility Testing 1984, Springer-Verlag, Berlin, 1984Google Scholar
  2. Berman, E. J., Nash, W. G., Seuanez, H. N., and O'Brien, S. J.: Chromosomal mapping of enzyme loci in the domestic cat. GSR to C2, ADA and ITPA to A3, and LDHA-ACP2 to D1. Cytogenet. Cell Genet. 41: 114–120, 1986Google Scholar
  3. Britten, R. J., Graham, D. E., and Neufeld, B. R.: Analysis of repeating DNA sequences by reassociation. Methods Enzymol. 29: 363–418, 1974Google Scholar
  4. Chardon, P., Kirszenbaum, M., Cullen, P. R., Geffrotin, C., Auffray, C., Strominger, J. L., Cohen, D., and Vaiman, M.: Analysis of the sheep MHC using HLA class I, II, and C4 cDNA probes. Immunogenetics 22: 349–358, 1985aGoogle Scholar
  5. Chardon, P., Vaiman, M., Kirszenbaum, M., Geffrotin, C., Renard, C., and Cohen, D.: Restriction fragment length polymorphism of the major histocompatibility complex of the pig. Immunogenetics 21: 161–171, 1985bGoogle Scholar
  6. Cohen, D., Paul, P., Font, M. P., Cohen, O., Sayagh, B., Marcadet, A., Busson, M., Mahouy, G., Cann, H. M., and Dausset, J.: Analysis of HLA class I genes with restriction endonuclease fragments: implications for polymorphism of the human major histocompatibility complex. Proc. Natl. Acad. Sci. U.S.A. 80: 6289–6292, 1983Google Scholar
  7. Cotter, S. M., Hardy, W. D., Jr., and Essex, M.: Association of feline leukemia virus with lymphosarcoma and other disorders in the cat. J. Am. Vet. Med. Assoc. 166: 449–454, 1975Google Scholar
  8. Darden, A. G. and Streilein, J. W.: Syrian hamsters express two monomorphic class I major histocompatibility complex molecules. Immunogenetics 20: 603–622, 1984Google Scholar
  9. Dausset, J.: The major histocompatibility complex in man. Science 213: 1469–1474, 1981Google Scholar
  10. Davis, M. M., Cohen, D. I., Nielsen, E. A., Steinmetz, M., Paul, W. E., and Hood, L.: Cell-type-specific cDNA probes and the murine I region: the localization and orientation of Ad. Proc. Natl. Acad. Sci. U.S.A. 81: 2194–2198, 1984Google Scholar
  11. Driesel, A. J., Römer, K., Schunter, F., Laryea, M. D., Schneider, E. M., Wernet, P., Henke, J., Basler, M., and Kömpf, J.: DNA polymorphism of the major histocompatibility class I genes and their association with serologically defined haplotypes. Immunogenetics 21: 529–538, 1985Google Scholar
  12. Flavell, R. A., Allen, H., Burkly, L. C., Sherman, D. H., Waneck, G. L., and Widera, G.: Molecular biology of the H-2 histocompatibility complex. Science 233: 437–443, 1986Google Scholar
  13. Garver, J. J., Estop, A. M., Meera-Khan, P., Balner, H., and Pearson, P. L.: Evidence of similar organization of the chromosomes carrying the major histocompatibility complex in man and other primates. Cytogenet. Cell Genet. 27: 238–245, 1980Google Scholar
  14. Hardy, D. A., Bell, J. I., Long, E. O., Lindsten, T., and McDevitt, H. O.: Mapping of the class II region of the human major histocompatibility complex by pulsed-field gel electrophoresis. Nature 323: 453–455, 1986Google Scholar
  15. Hardy, W. D., Jr., Hess, P. W., MacEwen, E. G., McClelland, A. J., Zuckerman, E. E., Essex, M., Cotter, S. M., and Jarrett, O.: Biology of feline leukemia virus in the natural environment. Cancer Res. 36: 582–588, 1976Google Scholar
  16. Klein, J.: Biology of the Mouse Histocompatibility-2 Complex: Principles of Immunogenetics Applied to a Single System, Springer-Verlag, New York, 1975Google Scholar
  17. Klein, J., Figueroa, F., and Nagy, Z. A.: Genetics of the major histocompatibility complex: the final act. Annu. Rev. Immunol. 1: 119–142, 1983Google Scholar
  18. Lalley, P. A. and McKusick, V.: Report of the committee on comparative mapping. Cytogenet. Cell Genet. 40: 536–566, 1985Google Scholar
  19. Ma, N. S., Simeone, T., McLean, J., and Parham, P.: Chromosome localization and gene synteny of the major histocompatibility complex in the owl monkey, Aotus. Immunogenetics 15: 1–16, 1982Google Scholar
  20. McCarty, J. M. and Grant, C. K.: Cellular immune response in the blood of cats is restricted to autochthonous feline sarcoma virus-transformed cells. Int. J. Cancer 31: 627–631, 1983Google Scholar
  21. McGuire, K. L., Duncan, W. R., and Tucker, P. W.: Syrian hamster DNA shows limited polymorphism at class I-like loci. Immunogenetics 22: 257–268, 1985Google Scholar
  22. Neefjes, J. J., Hensen, E. J., de Kroon, T. I. P., and Ploegh, H. L.: A biochemical characterization of feline MHC products: unusually high expression of class II antigens on peripheral blood lymphocytes. Immunogenetics 23: 341–347, 1986Google Scholar
  23. Nižetić, D., Figueroa, F., Nevo, E., and Klein, J.: Major histocompatibility complex of the mole-rat. II. Restriction fragment polymorphism. Immunogenetics 22: 55–67, 1985Google Scholar
  24. O'Brien, S. J.: The extent and character of biochemical genetic variation in the domestic cat (Fells catus). J. Hered. 71: 2–8, 1980Google Scholar
  25. O'Brien, S. J. (ed.): Genetic Maps, Vol. 4, Cold Spring Harbor Press, Cold Spring Harbor, New York, 1987Google Scholar
  26. O'Brien, S. J. and Nash, W. G.: Genetic mapping in mammals: chromosome map of domestic cat. Science 216: 257–265, 1982Google Scholar
  27. O'Brien, S. J., Simonson, J. M., and Eichelberger, M. A.: Genetic analysis of hybrid cells using isozyme markers as monitors of chromosome segregation. In J. W. Shay (ed.): Techniques in Somatic Cell Genetics, pp. 513–524, Plenum Press, New York, 1982Google Scholar
  28. Orr, H. T.: Use of Southern blotting to analyze the size and restriction fragment polymorphism of HLA class I DNA in the human population. Transplant. Proc. 15: 1900–1906, 1983Google Scholar
  29. Palmer, M., Wettstein, P. J., and Frelinger, J. A.: Evidence for extensive polymorphism of class I genes in the rat major histocompatibility complex (RT1). Proc. Natl. Acad. Sci. U.S.A. 80: 7616–7620, 1983Google Scholar
  30. Pedersen, N. C., Ho, E. W., Brown, M. L., and Yamamoto, J. K.: Isolation of a T-lymphotropic virus from domestic cats with an immunodeficiency-like syndrome. Science 235: 790–793, 1987Google Scholar
  31. Ploegh, H. L., Orr, H. T., and Strominger, J. L.: Major histocompatibility antigens: the human (HLA-A, -B, -C) and murine (H-2K, H-2D) class I molecules. Cell 24: 287–299, 1981Google Scholar
  32. Pollack, M. S., Mastrota, F., Chin-Louie, J., Monney, S., and Hayes, A.: Preliminary studies of the feline histocompatibility system. Immunogenetics 16: 339–347, 1982Google Scholar
  33. Sekaly, R. P., Tonnelle, C., Strubin, M., Mach, B., and Long, E. O.: Cell surface expression of class II histocompatibility antigens occurs in the absence of the invariant chain. J. Exp. Med. 164: 1490–1504, 1986Google Scholar
  34. Sood, A. K., Pereira, D., and Weissman, S. M.: Isolation and partial nucleotide sequence of a cDNA clone for human histocompatibility antigen HLA-B by use of an oligodeoxynucleotide primer. Proc. Natl. Acad. Sci. U.S.A. 78: 616–620, 1981Google Scholar
  35. Southern, E. M.: Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol. Biol. 98: 503–517, 1975Google Scholar
  36. Srivastava, B., Duceman, B. W., Biro, P. A., Sood, A. K., and Weissman, S. M.: Molecular organization of the class I genes of major human histocompatibility complex. Immunol. Rev. 84: 93–121, 1985Google Scholar
  37. Steinmetz, M.: Genes of the immune system. In P. W. Rigby (ed.): Genetic Engineering, in press, Academic Press, New York, 1987Google Scholar
  38. Steinmetz, M. and Hood, L.: Genes of the major histocompatibility complex in mouse and man. Science 222: 727–733, 1983Google Scholar
  39. Steinmetz, M., Minard, K., Horath, S., McNicholas, J., Srelinger, J., Wake, C., Long, E., Mach, B., and Hood, L.: A molecular map of the immune response region from the major histocompatibility complex of the mouse. Nature 300: 35–42, 1982Google Scholar
  40. Stiff, M. I. and Olsen, R. G.: Feline one-way mixed lymphocyte reaction. Vet. Immunol. Immunopathol. 7: 1–9, 1984Google Scholar
  41. Streilein, J. W. and Duncan, W. R.: On the anomalous nature of the major histocompatibility complex in Syrian hamsters, Hm-1. Transplant. Proc. 15: 1540–1545, 1983Google Scholar
  42. Tarr, M. J., Olsen, R. G., Hoover, E. A., Kociba, G. J., and Schaller, J. P.: The effects of methylnitrosourea on the immune system and hematopoietic system of adult specific pathogen free cats. Chem. Biol. Interact. 28: 181–199, 1979Google Scholar
  43. Tonnelle, C., DeMars, R., and Long, E. O.: DO: a new chain gene in HLA-D with a distinct regulation of expression. EMBO J. 4: 2839–2847, 1985Google Scholar
  44. Weiss, E. H., Mellor, A., Golden, L., Fahrner, K., Simpson, E., Hurst, J., and Flavell, R. A.: The structure of a mutant H-2 gene suggests that the generation of polymorphism in H-2 genes may occur by gene conversion-like events. Nature 301: 671–694, 1983Google Scholar
  45. Wettstein, P. J., Faas, S., and Buck, D. A.: Class I and class II restriction pattern polymorphisms associated with independently derived RT1 haplotypes in inbred rats. Immunogenetics 22: 9–22, 1985Google Scholar
  46. Wolfe, J. H., Haskins, M. E., and Zmijewski, C. M.: Mixed lymphocyte reactivity in cats. Transplantation 37: 509–513, 1984Google Scholar
  47. Zinkernagel, R. M. and Doherty, P. C.: MHC-restricted cytotoxic T cells: studies on the biological role of polymorphic major transplantation antigens determining T-cell restriction-specificity, function and responsiveness. Adv. Immunol. 27: 51–177, 1979Google Scholar

Copyright information

© Springer-Verlag 1988

Authors and Affiliations

  • Naoya Yuhki
    • 1
  • Stephen J. O'Brien
    • 1
  1. 1.Laboratory of Viral CarcinogenesisNational Cancer InstituteFrederickUSA

Personalised recommendations