Chromatin Proteins and Chromatin Structure in Spermatogenesis

  • Cristóbal Mezquita
Part of the NATO ASI Series book series (NSSA, volume 101)


During spermatogenesis, the population of stem cells (diploid spermatogonia) divides and differentiates into tetraploid spermatocytes. Spermatocytes undergo meiosis, in which genetic recombination occurs, producing haploid spermatids. Spermatids, through an extraordinary process of metamorphosis called spermiogenesis, develop into a highly specialized motile vector for transportation of genetic information: the spermatozoa (Figure 1).


Primary Spermatocyte Nonhistone Protein Early Spermatid Late Spermatid Spermatid Nucleus 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    MONESI, V. (1971). Chromosome activities during meiosis and spermiogenesis. J. Reprod. Fert. (suppl.) 13, 1–14.Google Scholar
  2. 2.
    KIERSZENBAUM, A.L. and TRES, L.L. (1978). RNA transcription and chromatin structure during meiotic and postmeiotic stages of spermatogenesis. Federation Proc. 37, 2512–2516.Google Scholar
  3. 3.
    MEZQUITA, C. and TENG, C.S. (1977). Changes in nuclear and chromatin composition and genomic activity during spermatogenesis in the maturing rooster testis. Biochem. J. 164, 99–111.PubMedGoogle Scholar
  4. 4.
    KIERSZENBAUM, A.L. and TRES, L.L. (1975). Structural and transcriptional features of the mouse spermatid genome. J. Cell Biol. 65, 258–270.PubMedCrossRefGoogle Scholar
  5. IATROU, K. and DIXON, G.H. (1978). Protamine messenger RNA: its life history during spermatogenesis in rainbow trout. Federation Proc. 37, 2526–2533.Google Scholar
  6. 6.
    DISTEL, R.J., KLEENE, K.C., and HECHT, N.B. (1984). Haploid expression of a mouse testis a-tubulin gene. Science 224, 68–70.PubMedCrossRefGoogle Scholar
  7. 7.
    STERN, H. and HOTTA, I. (1977). Biochemistry of meiosis. Phil. Trans. Roy. Soc. B 277, 277–293.CrossRefGoogle Scholar
  8. 8.
    LAHDETIE, J. KAUKOPURO, S., and PARVINEN, M. (1983). Genotoxic effects of ethyl methanesulfonate and X-rays at different stages of rat spermatogenesis, studied by inhibition of DNA synthesis and induction of DNA repair in vitro. Hereditas 99, 269–278.PubMedCrossRefGoogle Scholar
  9. 9.
    SEGA, G.A. (1974). Unscheduled DNA synthesis in germ cells of male mice exposed in vivo to the chemical mutagen ethyl methanesulfonate. Proc. Natl. Acad. Sci. USA 71, 4955–4959.Google Scholar
  10. 10.
    MEZQUITA, C. and TENG, C.S. (1977). Changes in chromatin structure during spermatogenesis in maturing rooster testis as demonstrated by the initiation pattern of ribonucleic acid synthesis in vitro. Biochem. J. 170, 203–210.Google Scholar
  11. 11.
    LOIR, M. and COURTENS, J.L. (1979). Nuclear reorganization in ram spermatids. J. Ultrastruct. Res. 67, 309–324.PubMedCrossRefGoogle Scholar
  12. 12.
    LOIR, M. and LANNEAU, M. (1978). Transformation of ram spermatid chromatin. Exp. Cell Res. 155, 231–243.CrossRefGoogle Scholar
  13. 13.
    VAUGHN, J.C. and THOMSON, L.A. (1972). A kinetic study of DNA and basic protein metabolism during spermatogenesis in the sand crab, Emerita analoga. J. Cell Biol. 52, 322–337.PubMedCrossRefGoogle Scholar
  14. 14.
    NAKANO, M., TOBITA, T., and ANDO, T. (1976). Studies on a protamine (galline) from fowl sperm. Int. J. Peptide Protein Res. 8, 565–578.CrossRefGoogle Scholar
  15. 15.
    MEISTRICH, M.L., BROCK, W.A., GRIMES, S.R., PLATZ, R.D., and HNILICA, L.S. (1978). Nuclear protein transitions during spermatogenesis. Federation Proc. 37, 2522–2525.Google Scholar
  16. 16.
    KAYE, J.S. and McMASTER-KAYE, R. (1982). Characterization of the ususual basic proteins of cricket spermatid nuclei on the basis of their molecular weights and amino acid compositions. Biochim. Biophys. Acta 696, 44–51.Google Scholar
  17. 17.
    CHAUVIERE, M., LAINE, B., SAUTIERE, P., and CHEVAILLIER, P. (1983). Purification and characterization of two basic spermatid-specific proteins isolated from the dog-fish Scylliorhinus caniculus. FEBS Lett. 152, 231–235.PubMedCrossRefGoogle Scholar
  18. 18.
    MARUSHIGE, K. and DIXON, G.H. (1969). Developmental changes in chromosomal composition and template activity during spermatogenesis in trout testis. Dev. Biol. 19, 397–414.PubMedCrossRefGoogle Scholar
  19. 19.
    MARUSHIGE, K. and DIXON, G.H. (1971). Transformation of trout testis chromatin. J. Biol. Chem. 246, 5799–5805.PubMedGoogle Scholar
  20. 20.
    BUCCI, L.R., BROCK, W.A., and MEISTRICH, M.L. (1982). Distribution and synthesis of histone 1 subfractions during spermatogenesis in the rat. Exp. Cell Res. 140, 111–118.PubMedCrossRefGoogle Scholar
  21. 21.
    SEYEDIN, S.M. and KISTLER, W.S. (1983). H1 histones from mammalian testes. Exp. Cell Res. 143, 451–454.PubMedCrossRefGoogle Scholar
  22. 22.
    TROSTLE-WEIGE, P.K., MEISTRICH, M.L., BROCK, W.A., NISHIOKA, K., and BREMER, J.W. (1982). Isolation and characterization of TH2A, a germ cell-specific variant of histone 2A in rat testis. J. Biol. Chem. 257, 55560–55567.Google Scholar
  23. 23.
    CHRISTENSEN, M.E. and DIXON, G.H. (1982). Hyperacetylation of histone H4 correlates with the terminal transcriptionally inactive stages of spermatogenesis in rainbow trout. Dev. Biol. 93, 404–415.PubMedCrossRefGoogle Scholar
  24. 24.
    CHRISTENSEN, M.E., RATTNER, J.B., and DIXON, G.H. (1984). Hyperacetylation of histone H4 promotes chromatin decondensation prior to histone replacement by protamines during spermatogenesis in rainbow trout. Nucleic Acids Res. 12, 4575–4592.PubMedCrossRefGoogle Scholar
  25. 25.
    GRIMES, S.R. and HENDERSON, N. (1983). Acetylation of histones during spermatogenesis in the rat. Arch. Biochem. Biophys. 221, 108–116.PubMedCrossRefGoogle Scholar
  26. 26.
    OLIVA, R. and MEZQUITA, C. (1982). Histone H4 hyper- acetylation and rapid turnover of its acetyl groups in transcriptionally inactive rooster testis spermatids. Nucleic Acids Res. 10, 8049–8059.PubMedCrossRefGoogle Scholar
  27. 27.
    McGHEE, J.D., NICKOL, J.M., FELSENFELD, G., and RAU, D.C. (1983). Histone hyperacetylation has little effect on the higher order folding on chromatin. Nucleic Acids Res. 11, 4065–4074.PubMedCrossRefGoogle Scholar
  28. 28.
    CARY, P.D., CRANE-ROBINSON, C., BRADBURY, E.M., and DIXON, G.H. (1982). Effect of acetylation on the binding of N-terminal peptides of histone H4 to DNA. Eur. J. Biochem. 127, 137–143.PubMedCrossRefGoogle Scholar
  29. 29.
    BODE, J., HENCO, K., and WINGENDER, E. (1980). Modulation of the nucleosome particles open as the histone core becomes hyperacetylated. Eur. J. Biochem. 110, 143–152.PubMedCrossRefGoogle Scholar
  30. 30.
    BODE, J., GOMEZ-LIRA, M.M., and SCHROTER, H. (1983). Nucleosomal particles open as the histone core becomes hyperacetylated. Eur. J. Biochem. 130, 437–445.PubMedCrossRefGoogle Scholar
  31. 31.
    RUIZ-CARRILLO, A. and PALAU, J. (1973). Histones from embryos of the sea urchin Arbacia lixula. Dev. Biol. 35, 115–123.PubMedCrossRefGoogle Scholar
  32. 32.
    WANGH, L., RUIZ-CARRILLO, A., and ALLFREY, V.G. (1972). Separation and analysis of histone subfractions differing in their degree of acetylation: some correlation with genetic activity in development. Arch. Biochem. Biophys. 150 44–54.PubMedCrossRefGoogle Scholar
  33. 33.
    AGELL, N., CHIVA, M., and MEZQUITA, C. (1983). Changes in nuclear content of protein conjugate histone H2A-ubiquitin during rooster spermatogenesis. FEBS Lett. 155, 209–212.PubMedCrossRefGoogle Scholar
  34. 34.
    KLEINSCHMIDT, A.M. and MARTINSON, H.G. (1981). Structure of nucleosome core particles containing uH2A (A24). Nucleic Acids Res. 9, 2423–2331.PubMedCrossRefGoogle Scholar
  35. 35.
    MATSUI, S., SEON, B.K., and SANDBERG, A.A. (1979). Disappearance of a structural chromosomal protein A24 in mitosis: implications for molecular basis of chromatin condensation. Proc. Natl. Acad. Sci. USA 76, 6386–6390.PubMedCrossRefGoogle Scholar
  36. 36.
    LEVINGER, L. and VARSHAVSKY, A. (1982). Selective arrangement of ubiquitinated and D1 protein-containing nucleosomes within the Drosophila genome. Cell 28, 375–385.PubMedCrossRefGoogle Scholar
  37. 37.
    HERSHKO, A. (1983). Ubiquitin: roles in protein modification and breakdown. Cell 34, 11–12.PubMedCrossRefGoogle Scholar
  38. 38.
    FINLEY, D., CIECHANOVER, A., and VARSHAVSKY, A. (1984). Thermolability of ubiquitin-activating enzyme from the mammalian cell cycle mutant ts85. Cell 37, 43–55.PubMedCrossRefGoogle Scholar
  39. 39.
    CHIECHANOVER, A., FINLEY, D., and VARSHAVSKY, A. (1984). Ubiquitin dependence of selective protein degradation demonstrated in the mammalian cell cycle mutant ts85. Cell 37, 57–66.CrossRefGoogle Scholar
  40. 40.
    MARUSHIGE, U. and MARUSHIGE, K. (1983). Proteolysis of somatic type histones in transforming rat spermatid chromatin. Biochim. Biophys. Acta 761, 48–57.PubMedCrossRefGoogle Scholar
  41. 41.
    KUMAROO, K.K. and IRVING, J.L. (1984). Diisopropyl fluorophophate-interacting proteinases of nuclei of rat testis cells. Biochim. Biophys. Acta 782, 320–327.PubMedGoogle Scholar
  42. 42.
    WATSON, D.C., LEVY, B., and DIXON, G.H. (1978). Free ubiquitin is a non-histone protein of trout testis chromatin. Nature 276, 196–198.PubMedCrossRefGoogle Scholar
  43. 43.
    LOIR, M., KARATY, A., LANNEAU, M., MENEZO, Y., MUH, J.P., and SAUTIERE, P. (1984). Purification and characterization of ubiquitin from mammalian testis. FEBS Lett. 169, 199–204.PubMedCrossRefGoogle Scholar
  44. 44.
    MEZQUITA, J., CHIVA, M., VIDAL, S., and MEZQUITA, C. (1982). Effect of high nobility group non- Ustone proteins HMG-20 (ubiquitin) and HMG-17 on histone deacetylase activity in vitro. Nucleic Acids Res. 10, 1781–1797.PubMedCrossRefGoogle Scholar
  45. 45.
    HAYAISHI, O. and UEDA, K. (1982). Poly-and mono(ADP- ribosyl)ation reactions: their significance in molecular biology. In “ADP-ribosylation Reactions,” ( O. Hayaishi, and K. Ueda, eds.) pp. 3–16. Academic Press, New York.Google Scholar
  46. 46.
    MEZQUITA, C. and COROMINAS, M. (1983). ADP-ribosyl transferase activity during rooster spermatogenesis. J. Cell Biol. 97, 138a.Google Scholar
  47. 47.
    SHALL, S. (1982). ADP-ribose in DNA repair. In “ADPribosylation Reactions,” ( O. Hayaishi and K. Uei, eds.) pp. 477–520. Academic Press, New York.Google Scholar
  48. 48.
    ZAHRADKA, P. and EBISUZAKI, K. (1982). A shuttle mechanism for DNA-protein interactions. The regulation of poly(ADPribose)polymerase. Eur. J. Biochem. 127, 579–585.PubMedCrossRefGoogle Scholar
  49. 49.
    STICK, R. and SCHWARZ, H. (1982). The disappearance of the nuclear lamina during spermatogenesis: an electron microscopic and immunofluorescence study. Cell 11, 235–243.Google Scholar
  50. 50.
    PRUSLIN, F.H. and ROSMAN, T.C. (1983). Proteins of demembraned protamine-depleted mouse sperm. Homology with proteins of somatic cell nuclear envelope/matrix. Exp. Cell Res. 144, 115–126.PubMedCrossRefGoogle Scholar
  51. 51.
    CHIVA, M. and MEZQUITA, C. (1983). Quantitative changes of high mobility group non-listone chromosomal proteins HMG-1 and HMG-2 during rooster spermatogenesis. FEBS Lett. 162, 324–328.PubMedCrossRefGoogle Scholar
  52. 52.
    REECK, G.R., ISACKSON, P.J., TELLER, D.C. (1982). Domain structure in high molecular weight high mobility group nonhistone chromatin proteins. Nature 300, 76–78.PubMedCrossRefGoogle Scholar
  53. 53.
    STEIN, A., WHITLOCK, J.P., and BINA, M. (1979). Acidic polypeptides can assemble both histones and chromatin in vitro at physiological ionic strength. Proc. Acad. Sci. USA 76, 5000–5004.CrossRefGoogle Scholar
  54. 54.
    BONNE-ANDREA, C., HARPER, F., SOBCZAK, J., and DE RECONDO, A.M. (1984). Rat liver HMG-1: a physiological nucleosome assembly factor. EMBO J. 3, 1193–1199.PubMedGoogle Scholar
  55. 55.
    ADAMS, R.L.P., BURDON, R.H., and FULTON, J. (1983). Methylation of satellite DNA. Biochem. Biophys. Res. Commun. 113, 695–702.PubMedCrossRefGoogle Scholar
  56. 56.
    GAMA-SOSA, M.A., WANG, R.Y.H., KUO, K.C., GEHRKA, C.X., and EHRLICH, M. (1983). The 5-methylcytosine content of highly repeated sequences in human DNA. Nucleic Acids Res. 11, 3087–3095.PubMedCrossRefGoogle Scholar
  57. 57.
    ROCAMORA, N. and MEZQUITA, C. (1984). Hypomethylation of DNA in meiotic and postmeiotic rooster testis cells. FEBS Lett. 177, 81–84.PubMedCrossRefGoogle Scholar
  58. 58.
    RARE, B., ERICKSON, R.P., and QUINTO, M. (1983). Methylation of unique sequence DNA. during spermatogenesis in mice. Nucleic Acids Res. 11, 7947–7959.CrossRefGoogle Scholar
  59. 59.
    Ponzetto-Zimmerman, C. and WOLGEMUTH, D.J. (1984). Methylation of satellite sequences in mouse spermatogenic and somatic DNA’s. Nucleic Acids Res. 12, 2807–2821.PubMedCrossRefGoogle Scholar
  60. 60.
    SANFORD, J., FORRESTER, L., and CHAPMAN, V. (1984). Methylation patterns of repetitive DNA sequences in germ cells of Mus musculus. Nucleic Acids Res. 12, 2823–2836.PubMedCrossRefGoogle Scholar
  61. 61.
    KORBA, B.E. and HAYS, J.B. (1982). A Partially deficient methylation of cytosine in DNA at CCTGG sites stimulates genetic recombination of bacteriophage lambda. Cell 28, 531–541.Google Scholar
  62. 62.
    DRESSLER, B. and SCHMID, M. (1976). Specific arrangement of chromosome in the spermiogenesis of Gallus domesticus. Chromosoma (Berl.) 58, 387–391.CrossRefGoogle Scholar
  63. 63.
    TAYLOR, J.H. (1984). DNA methylation and cellular differentiation. In “Cell Biology Monographs,” Vol. 11. Springer-Verlag,lTien.Google Scholar
  64. 64.
    JAHNER, D., STUHLMANN, H., LOHLER, J., SIMON, I., and STEWART, C.L., HARBERS, K., JAENISCH, R. (1982). De novo of retroviral genomes during methylation and expression mouse embryogenesis. Nature 298, 623–628.PubMedCrossRefGoogle Scholar
  65. 65.
    MORRIS, D.R. (1978). Polyamine function in rapidly proliferating cells. In “Advances in Polyamine Research,” Vol. 1 ( R.A. Campbell, R.D. Morris, D. Bartos, G.D. Daves, and F. Bartos, eds.) pp. 105–115. Raven Press, New York.Google Scholar
  66. 66.
    GOSULE, L.C., CHATTORAJ, D.K., and SCHELLMAN, J.A., (1978) Condensation of phage DNA Polyamine Research by polyamines. In Advances in (R.A. Campbell, R.D. Morris, Bartos, G.D. Daves, and D. F. Bartos, eds. ) Vol. 1 Raven Press, New York. pp. 201–215.Google Scholar
  67. 67.
    OLIVA, R., VIDAL, S., and MEZQUITA, C. (1982). Cellular content and biosynthesis of polyamines during rooster spermatogenesis. Biochem. J. 208, 269–273.PubMedGoogle Scholar
  68. 68.
    MEZQUITA, C., MEZQUITA, J., VIDAL-SIVILLA, S. (1980). The polyamine spermine stimulates enzymatic acetylation of histones in rooster testis chromatin in vitro. Eur. J. Cell Biol. 22, 82.Google Scholar
  69. 69.
    GROND, C.J., RUTTEN, R.G.J., and HENNIG, W. (1984). Ultra-structure of the Y chromosomal lampbrush loops in primary spermatocytes of Drosophila hydei. Chromosoma (Berl.) 89, 85–95.CrossRefGoogle Scholar
  70. 70.
    HOTTA, Y. and STERN, H. (1981). Small nuclear RNA molecules that regulate nuclease accessibility in specific chromatin regions of meiotic cells. Cell 27, 309–319.PubMedCrossRefGoogle Scholar
  71. 71.
    HOTTA, Y. and STERN, H. (1984). The organization of DNA segments undergoing repair synthesis during pachytene. Chromosoma (Berl.) 89, 127–137.CrossRefGoogle Scholar
  72. 72.
    RYOJI, M. and WORCEL, A. (1984). Chromatin assembly in Xenopus oocytes: in vivo studies. Cell 37, 21–32.PubMedCrossRefGoogle Scholar
  73. 73.
    GLIKIN, G.C., RUBERTI, I., WORCEL, A. (1984). Chromatin assembly in Xenopus oocytes: in vitro studies. Cell 37, 33–41.PubMedCrossRefGoogle Scholar
  74. 74.
    SINGLETON, C.K., KLYSIK, J., STIRDIVANT, S.N., and WELLS, R.D. (1982). Left-handed Z-DNA is induced by supercoiling in physiological ionic conditions. Nature 299, 312–316.PubMedCrossRefGoogle Scholar
  75. 75.
    WANG, A.H.J., QUIGLEY, G.J., KOLPAK, F.J., CRAWFORD, J.L., BOOM, J.H., MAREL, G., and RICH, A. (1979). Molecular structure of a left-handed double helical DNA fragment at atomic resolution. Nature 282, 680–686.PubMedCrossRefGoogle Scholar
  76. 76.
    LOUIE, A.J. and DIXON, G.H. (1972). Trout testis cells. II. Synthesis and phosphorylation of histones and protamines in different cell types. J. Biol. Chem. 247, 5498–5505.PubMedGoogle Scholar
  77. 77.
    WARRANT, R.W. and KIM, S.H. (1978). a-Helix-double helix interaction shown in the structure of a protamine-transfer RNA comples and a nucleoprotamine model. Nature271, 130–135.Google Scholar
  78. 78.
    McINTOSH, J.R. and PORTER, K.R. (1967). Microtubules in the spermatids of domestic fowl. J. Cell Biol. 35, 153–173.PubMedCrossRefGoogle Scholar
  79. 79.
    WAYDA, M.E., ROGERS, A.E., and FLINT, S.J. (1983). The structure of nucleoprotein cores released from adenovirions. Nucleic Acids Res. 11, 441–460.CrossRefGoogle Scholar
  80. 80.
    ALTMAN, S., MODEL, P., DIXON, G.H., and WOSNICK, M.A. (1981). An E. coli gene coding for a protamine-like protein. Cell 26, 299–304.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1985

Authors and Affiliations

  • Cristóbal Mezquita
    • 1
  1. 1.Department of Physiology Faculty of MedicineUniversity of BarcelonaBarcelonaSpain

Personalised recommendations