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. 1977 Jul 1;74(1):86–97. doi: 10.1083/jcb.74.1.86

Temporal expression of membrane antigens during mouse spermatogenesis

CF Millete, AR Bellve
PMCID: PMC2109864  PMID: 68961

Abstract

The temporal expression of cell surface antigens during mammalian spermatogenesis has been investigated using isolated populations of mouse germ cells. Spermatogenic cells at advanced stages of differentiation, including pachytene primary spermatocytes, round spermatids, and residual bodies of Regaud and mature spermatozoa, contain common antigenic membrane components which are not detected before the pachytene stage of the first meiotic prophase. These surface constituents are not detected on isolated populations of primitive type A spermatogonia, type A spermatogonia, type B spermatogonia, preleptotene primary spermatocytes, or leptotene and zygotene primary spermatocytes. These results have been demonstrated by immunofluorescence microscopy, by complement-mediated cytotoxicity, and by quantitative measurements of immunoglobulin (Ig) receptors on the plasma membrane of all cell populations examined. The cell surface antigens detected on germ cells are not found on mouse thymocytes, erythrocytes, or peripheral blood lymphocytes as determined by immunofluorescence and by cytotoxicity assays. Furthermore, absorption of antisera with kidney and liver tissue does not reduce the reactivity of the antibody preparations with spermatogenic cells, indicating that these antigenic determinants are specific to germ cells. This represents the first direct evidence for the ordered temporal appearance of plasma membrane antigens specific to particular classes of mouse spermatogenic cells. It appears that at late meiotic prophase, coincident with the production of pachytene primary spermatocytes, a variety of new components are inserted into the surface membranes of developing germ cells. The further identification and biochemical characterization of these constituents should facilitate an understanding of mammalian spermatogenesis at the molecular level.

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Selected References

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  1. Artzt K., Bennett D., Jacob F. Primitive teratocarcinoma cells express a differentiation antigen specified by a gene at the T-locus in the mouse. Proc Natl Acad Sci U S A. 1974 Mar;71(3):811–814. doi: 10.1073/pnas.71.3.811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bellvé A. R., Cavicchia J. C., Millette C. F., O'Brien D. A., Bhatnagar Y. M., Dym M. Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J Cell Biol. 1977 Jul;74(1):68–85. doi: 10.1083/jcb.74.1.68. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Blumberg P. M., Robbins P. W. Effect of proteases on activation of resting chick embryo fibroblasts and on cell surface proteins. Cell. 1975 Oct;6(2):137–147. doi: 10.1016/0092-8674(75)90004-5. [DOI] [PubMed] [Google Scholar]
  4. Dym M., Fawcett D. W. Further observations on the numbers of spermatogonia, spermatocytes, and spermatids connected by intercellular bridges in the mammalian testis. Biol Reprod. 1971 Apr;4(2):195–215. doi: 10.1093/biolreprod/4.2.195. [DOI] [PubMed] [Google Scholar]
  5. Dym M., Fawcett D. W. The blood-testis barrier in the rat and the physiological compartmentation of the seminiferous epithelium. Biol Reprod. 1970 Dec;3(3):308–326. doi: 10.1093/biolreprod/3.3.308. [DOI] [PubMed] [Google Scholar]
  6. Dym M. The fine structure of the monkey (Macaca) Sertoli cell and its role in maintaining the blood-testis barrier. Anat Rec. 1973 Apr;175(4):639–656. doi: 10.1002/ar.1091750402. [DOI] [PubMed] [Google Scholar]
  7. Fawcett D. W., Anderson W. A., Phillips D. M. Morphogenetic factors influencing the shape of the sperm head. Dev Biol. 1971 Oct;26(2):220–251. doi: 10.1016/0012-1606(71)90124-2. [DOI] [PubMed] [Google Scholar]
  8. Fawcett D. W., Leak L. V., Heidger P. M., Jr Electron microscopic observations on the structural components of the blood-testis barrier. J Reprod Fertil Suppl. 1970;10:105–122. [PubMed] [Google Scholar]
  9. Fellous M., Erickson R. P., Gachelin G., Jacob F. The time of appearance of Ia antigens during spermatogenesis in the mouse. Transplantation. 1976 Nov;22(5):440–444. doi: 10.1097/00007890-197611000-00005. [DOI] [PubMed] [Google Scholar]
  10. Gachelin G., Fellous M., Guenet J. L., Jacob F. Developmental expression of an early embryonic antigen common to mouse spermatozoa and cleavage embryos, and to human spermatozoa: its expression during spermatogenesis. Dev Biol. 1976 Jun;50(2):310–320. doi: 10.1016/0012-1606(76)90154-8. [DOI] [PubMed] [Google Scholar]
  11. Gilula N. B., Fawcett D. W., Aoki A. The Sertoli cell occluding junctions and gap junctions in mature and developing mammalian testis. Dev Biol. 1976 May;50(1):142–168. doi: 10.1016/0012-1606(76)90074-9. [DOI] [PubMed] [Google Scholar]
  12. Hagopian A., Jackson J. J., Carlo D. J., Limjuco G. A., Eylar E. H. Experimental allergic aspermatogenic orchitis. III. Isolation of spermatozoal glycoproteins and their role in allergic aspermatogenic orchitis. J Immunol. 1975 Dec;115(6):1731–1743. [PubMed] [Google Scholar]
  13. Hart D. A. Studies on nonidet P40 lysis of murine lymphoid cells. I. Use of cholera toxin and cell surface Ig to determine degree of dissociation of the plasma membrane. J Immunol. 1975 Sep;115(3):871–875. [PubMed] [Google Scholar]
  14. Henkart P. A., Fisher R. I. Characterization of the lymphocyte surface receptors for Con A and PHA. J Immunol. 1975 Feb;114(2 Pt 1):710–714. [PubMed] [Google Scholar]
  15. Herscowitz H. B., McKillip T. W. A simple method for liquid scintillation counting of 125-iodine and 51-chromium used in antigen binding and cytotoxicity studies. J Immunol Methods. 1974 Mar;4(2):253–262. doi: 10.1016/0022-1759(74)90068-4. [DOI] [PubMed] [Google Scholar]
  16. Jackson J. J., Hagopian A., Carlo D. J., Limjuco G. A., Eylar E. H. Experimental allergic aspermatogenic orchitis. 1. Isolation of a spermatozoal protein (AP1) which induces allergic aspermatogenic orchitis. J Biol Chem. 1975 Aug 10;250(15):6141–6150. [PubMed] [Google Scholar]
  17. Jackson J. J., Hagopian A., Carlo D. J., Limjuco G. A., Eylar E. H. Experimental allergic aspermatogenic orchitis. II. Some chemical properties of the AP1 protein of the sperm acrosome. Biochim Biophys Acta. 1976 Mar 18;427(1):251–261. doi: 10.1016/0005-2795(76)90301-9. [DOI] [PubMed] [Google Scholar]
  18. Kierszenbaum A. L., Tres L. L. Transcription sites in spread meiotic prophase chromosomes from mouse spermatocytes. J Cell Biol. 1974 Dec;63(3):923–935. doi: 10.1083/jcb.63.3.923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. LEVY H. B., SOBER H. A. A simple chromatographic method for preparation of gamma globulin. Proc Soc Exp Biol Med. 1960 Jan;103:250–252. doi: 10.3181/00379727-103-25476. [DOI] [PubMed] [Google Scholar]
  20. Marchalonis J. J. Lymphocyte surface immunoglobulins. Science. 1975 Oct 3;190(4209):20–29. doi: 10.1126/science.1101378. [DOI] [PubMed] [Google Scholar]
  21. Monesi V. Synthetic activities during spermatogenesis in the mouse RNA and protein. Exp Cell Res. 1965 Aug;39(1):197–224. doi: 10.1016/0014-4827(65)90023-6. [DOI] [PubMed] [Google Scholar]
  22. Nagano T., Suzuki F. Freeze-fracture observations on the intercellular junctions of Sertoli cells and of Leydig cells in the human testis. Cell Tissue Res. 1976 Feb 6;166(1):37–48. doi: 10.1007/BF00215123. [DOI] [PubMed] [Google Scholar]
  23. Schachner M., Wortham K. A., Carter L. D., Chaffee J. K. NS-4 (nervous system antigen-4), a cell surface antigen of developing and adult mouse brain and sperm. Dev Biol. 1975 Jun;44(2):313–325. doi: 10.1016/0012-1606(75)90402-9. [DOI] [PubMed] [Google Scholar]
  24. Tres L. L. Nucleolar RNA synthesis of meiotic prophase spermatocytes in the human testis. Chromosoma. 1975 Nov 24;53(2):141–151. doi: 10.1007/BF00333042. [DOI] [PubMed] [Google Scholar]
  25. Tung K. S., Unanue E. R., Dixon F. J. Pathogenesis of experimental allergic orchitis. I. Transfer with immune lymph node cells. J Immunol. 1971 Jun;106(6):1453–1462. [PubMed] [Google Scholar]
  26. Tung K. S., Unanue E. R., Dixon F. J. Pathogenesis of experimental allergic orchitis. II. The role of antibody. J Immunol. 1971 Jun;106(6):1463–1472. [PubMed] [Google Scholar]
  27. Zetter B. R., Chen L. B., Buchanan J. M. Effects of protease treatment on growth, morphology, adhesion, and cell surface proteins of secondary chick embryo fibroblasts. Cell. 1976 Mar;7(3):407–412. doi: 10.1016/0092-8674(76)90170-7. [DOI] [PubMed] [Google Scholar]

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