Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Preimplantation mouse embryos express Mhc class I genes before the first cleavage division

  • 24 Accesses

  • 29 Citations

Abstract

We have used oligonucleotide primers complementary for polymorphic regions of the mouse H-2D gene in a highly sensitive polymerase chain reaction (PCR) assay to detect the transcription of maternal and paternal class I mRNAs in gametes and preimplantation embryos. Using congenic strains of mice differencing only at the major histocompatibility loci, class I (H-2D) mRNA of both the maternal and paternal haplotypes was demonstrated in embryos from the one-cell zygote to the late blastocyst stage of development but could not be detected in vas deferens or in vitro capacitated sperm or in ovulated secondary oocytes. These data clearly show that both paternally and maternally inherited Major histocompatibility complex (Mhc) class I genes are transcribed from the earliest stages of embryonic development, and suggest that developmental regulation of expression of their protein products is principally at the post-transcriptional level.

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

References

  1. Allen, H., Fraser, J., Flyer, D., Calvin, S., and Flavell, R. β2-microglobulin is not required for cell surface expression of the murine class I histocompatibility antigen H-2Db or of a truncated H-2Db. Proc Natl Acad Sci USA 83: 7447–7451, 1986

  2. Chirgwin, J. M., Przbyls, A. E., MacDonald, R. J., and Rutter, W. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18: 5294–5299, 1979

  3. Clegg, K. B. and Piko, L. Poly(A) length, cytoplasmic adenylation and synthesis of poly(A)+RNA in early mouse embryos. Dev Biol 95: 331–341, 1983

  4. Cozard, K. M. and Warner, C. M. Detection of H-2 antigens on 8-cell mouse embryos. J Exp Zool 221: 213–217, 1982

  5. Goldbard, S. B., Verbanac, K. M., and Warner, C. M. Role of the H-2 complex in preimplantation mouse embryo development. Biol Reprod 26: 591–596, 1982

  6. Goldbard, S. B. and Warner, C. M. Genes affect the timing of early mouse embryo development. Biol Reprod 27: 419–424, 1982

  7. Hogan, B., Constantini, F., and Lacey, E. Manipulating the Mouse Embryo. Cold Spring Harbor Laboratory, Cold Spring Harbor, 1986

  8. Jaffe, L., Robertson, E. J., and Bikoff, E. K. Development failure of chimeric embryos expressing high levels of H-2Dd transplantation antigens. Proc Natl Acad Sci USA 89: 5927–5931, 1992

  9. Johnson, P. M. Immunology of reproduction: Editorial overview. Curr Opin Immunol 1: 1117–1118, 1989

  10. Klein, J., Benoist, C., David, C. S., Demant, P., Fischer-Lindahl, K., Flaherty, L., Flavell, R. A., Hammerling, U., Hood, L. E., Hunt III, S. W., Jones, P. P., Kourilsky, P., McDevitt, H. O., Meruelo, D., Murphy, D. B., Nathenson, S. G., Sachs, D. H., Steinmetz, M., Tonegawa, S., Wakeland, E. K., and Weiss, E. H. Revised nomenclature of mouse H-2 genes. Immunogenetics 32: 147–149, 1990

  11. Klein, J., Juretic, A., Baxevanis, C. N., and Nagy, Z. A. The traditional and a new version of the mouse H-2 complex. Nature 291: 455–460, 1981

  12. Krco, C. J. and Goldberg, E. H. Major histocompatibility antigens on preimplantation mouse embryos. Transplant Proc 9: 1367–1370, 1977

  13. Macek, M. B., Lopez, L. C., and Shur, B. D. Aggregation of β-1, 4-Galactosyltransferase on mouse sperm induces the acrosome reaction. Dev Biol 147: 440–444, 1991

  14. Monaco, J. J., Cho, S., and Attaya, M. Transport protein genes in the murine Mhc: possible implications for antigen processing. Science 250: 1723–1726, 1990

  15. Reyes, A. A., Schoeld, M., Itakura, K., and Wallace, R. B. Isolation of a cDNA clone for the murine transplantation antigen H-2Kb. Proc Natl Acad Sci USA 79: 3270–3274, 1982

  16. Reyes-Engel, A., Le Roy, E., Diegues, J. L., and Fernandez, N. Unusual expression pattern of the Mhc class I Q5 k gene in the AKR mouse: Possible role in embryo development. J Reprod Immunol 23: 73–81, 1993

  17. Saiki, R. K., Gelfaud, D. H., Staffel, S., Scharf, S. J., Higuchi, R. G., Horn, T., Mullis, K. B., and Erlich, H. A. Primer directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239: 487–491, 1988

  18. Sambrook, J., Fritsch, E. F., and Maniatis, T. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, 1989

  19. Sawicki, J. A., Magnuson, T., and Epstein, C. J. Evidence of the paternal genome in the 2-cell mouse embryo. Nature 294: 450–451, 1981

  20. Schwemmle, S., Bevec, D., Brem, G., Urban, M. B., Baeuerle, P. A., and Weiss, E. H. Developmental and tissue-specific expression of the Q5 k gene. Immunogenetics 34: 28–38, 1991

  21. Searle, R. F., Sellens, M. H., Elson, J., Jenkinson, E. J., and Billington, D. W. Detection of alloantigens during preimplantation development and early trophoblast differentiation in the mouse by immunoperoxidase labeling. J Exp Med 143: 348–359, 1976

  22. Singer, D. S., Hare, J., Golding, H., Flahertty, L., and Rudikoff, S. Characterization of a new sub-family of class I genes in the H-2 complex of the mouse. Immunogenetics 28: 13–21, 1988

  23. Tian, Z., Xu, Y., and Warner, C. M. Removal of Qa-2 antigen alters the Ped gene phenotype of preimplantation mouse embryos. Biol Reprod 47: 271–276, 1992

  24. Warner, C. M., Brownwell, M. S., and Ewoldsen, M. A. Why aren't embryos immunologically rejected by their mothers? Biol Reprod 38: 17–29, 1988

  25. Warner, C. M., Brownwell, M. S., and Rothschild, M. F. Analysis of litter size and weight in mice differing in Ped gene phenotype and the Q region of the H-2 complex. J Reprod Immunol 19: 303–313, 1991

  26. Watts, S., Vogel, J. M., Harriman, W. D., Itoh, T., Stauss, H. J., and Goodenow, R. S. DNA sequence analysis of the C3H H-2K k and H-2D k loci: Evolutionary relationships to H-2 genes from four other mouse strains. J Immunol 139: 3878–3885, 1987

  27. Webb, C. G., Gall, E., and Edelman, G. M. Synthesis and distribution of H-2 antigens in preimplantation mouse embryos. J Exp Med 146: 923–932, 1977

  28. Williams, D. B., Barber, B. H., Flavell, R. A., and Allen, H. Role of β2-microglobulin in the r intracellular transport and surface expression of murine class I histocompatibility molecules. J Immunol 142: 2796–2806, 1989

  29. Zinkernagel, R. P. and Doherty, P. C. Mhc restricted cytotoxic T cells: studies on the biological role of polymorphic major transplantation antigens determining T-cell restriction specificity. Adv Immunol 27: 51–177, 1979

Download references

Author information

Additional information

Correspondence to: N. Fernandez.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Sprinks, M.T., Sellens, M.H., Dealtry, G.B. et al. Preimplantation mouse embryos express Mhc class I genes before the first cleavage division. Immunogenetics 38, 35–40 (1993). https://doi.org/10.1007/BF00216388

Download citation

Keywords

  • Major Histocompatibility Complex
  • Blastocyst Stage
  • Preimplantation Embryo
  • Congenic Strain
  • Polymorphic Region