Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1972 Feb 1;52(2):322–337. doi: 10.1083/jcb.52.2.322

A KINETIC STUDY OF DNA AND BASIC PROTEIN METABOLISM DURING SPERMATOGENESIS IN THE SAND CRAB, EMERITA ANALOGA

Jack C Vaughn 1, Lillian A Thomson 1
PMCID: PMC2108633  PMID: 4109924

Abstract

Cytochemical and radioautographic techniques define and confirm a staging scheme for developing spermatids of the decapod crab, Emerita analoga. Quantitative photometric data demonstrate that developing spermatids lose a significant proportion of their nuclear proteins, as evidenced by diminishing binding of fluorodinitrobenzene. Photometric results also show that much (but not all) of the spermatid nuclear protein loss is in somatic-type histone, as evidenced by a dramatic fall in the histone/DNA ratio of these cells during a period in which nuclear DNA content remains constant. By the end of spermiogenesis, the sperm nuclear histone and protamine content is approximately zero, whereas some nonbasic protein persists. Loss of spermatid nuclear somatic-type histone is not accompanied by synthesis of gamete-type histone (e.g. protamine or arginine-rich histone), showing that the processes of displacement and synthesis of nuclear basic proteins during histone transition are not subject to obligatory coupling. Labeling studies suggest that nonbasic acrosomal proteins (presumably partly enzymes) are synthesized in the cytoplasm, after which they move into the acrosome. Stainable basic proteins accumulate in the acrosome during precisely the period of nuclear somatic histone loss, suggesting nuclear-cytoplasmic transfer.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alfert M., Geschwind I. I. A Selective Staining Method for the Basic Proteins of Cell Nuclei. Proc Natl Acad Sci U S A. 1953 Oct;39(10):991–999. doi: 10.1073/pnas.39.10.991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Amann R. P., Koefoed-Johnsen H. H., Levi H. Excretion pattern of labelled spermatozoa and the timing of spermatozoa formation and epididymal transit in rabbits injected with thymidine-3-H. J Reprod Fertil. 1965 Oct;10(2):169–183. doi: 10.1530/jrf.0.0100169. [DOI] [PubMed] [Google Scholar]
  3. BLOCH D. P., GODMAN G. C. A microphotometric study of the syntheses of desoxyribonucleic acid and nuclear histone. J Biophys Biochem Cytol. 1955 Jan;1(1):17–28. doi: 10.1083/jcb.1.1.17. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. BLOCH D. P., HEW H. Y. Schedule of spermatogenesis in the pulmonate snail Helix aspersa, with special reference to histone transition. J Biophys Biochem Cytol. 1960 Jun;7:515–532. doi: 10.1083/jcb.7.3.515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bloch D. P. A catalog of sperm histones. Genetics. 1969;61(1 Suppl):93–111. [PubMed] [Google Scholar]
  6. Bloch D. P. Histone differentiation and nuclear activity. Chromosoma. 1966;19(3):317–339. doi: 10.1007/BF00326921. [DOI] [PubMed] [Google Scholar]
  7. Brutlag D., Schlehuber C., Bonner J. Properties of formaldehyde-treated nucleohistone. Biochemistry. 1969 Aug;8(8):3214–3218. doi: 10.1021/bi00836a013. [DOI] [PubMed] [Google Scholar]
  8. CHANDLEY A. C., BATEMAN A. J. Timing of spermatogenesis in Drosophila melanogaster using tritiated thymidine. Nature. 1962 Jan 20;193:299–300. doi: 10.1038/193299b0. [DOI] [PubMed] [Google Scholar]
  9. CLERMONT Y., LEBLOND C. P., MESSIER B. [Duration of the cycle of the seminal epithelium of the rat]. Arch Anat Microsc Morphol Exp. 1959 Dec;48(Suppl):37–55. [PubMed] [Google Scholar]
  10. Chevaillier P. Mise en evidence et etude cytochimique d'une proteine basique extranucleaire dans les spermatozoides des crustaces decapodes. J Cell Biol. 1967 Mar;32(3):547–556. doi: 10.1083/jcb.32.3.547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Das N. K., Micou-Eastwood J., Alfert M. Cytochemical and biochemical properties of basic proteins of Urechis acrosomes. J Cell Biol. 1967 Nov;35(2):455–458. doi: 10.1083/jcb.35.2.455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gledhill B. L., Gledhill M. P., Rigler R., Jr, Ringertz N. R. Changes in deoxyribonucleoprotein during spermiogenesis in the bull. Exp Cell Res. 1966 Mar;41(3):652–665. doi: 10.1016/s0014-4827(66)80116-7. [DOI] [PubMed] [Google Scholar]
  13. HUANG R. C., BONNER J. Histone, a suppressor of chromosomal RNA synthesis. Proc Natl Acad Sci U S A. 1962 Jul 15;48:1216–1222. doi: 10.1073/pnas.48.7.1216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. LEBLOND C. P., CLERMONT Y. Definition of the stages of the cycle of the seminiferous epithelium in the rat. Ann N Y Acad Sci. 1952 Nov 20;55(4):548–573. doi: 10.1111/j.1749-6632.1952.tb26576.x. [DOI] [PubMed] [Google Scholar]
  15. LEBLOND C. P., CLERMONT Y. Spermiogenesis of rat, mouse, hamster and guinea pig as revealed by the periodic acid-fuchsin sulfurous acid technique. Am J Anat. 1952 Mar;90(2):167–215. doi: 10.1002/aja.1000900202. [DOI] [PubMed] [Google Scholar]
  16. Langreth S. G. Spermiogenesis in Cancer crabs. J Cell Biol. 1969 Dec;43(3):575–603. doi: 10.1083/jcb.43.3.575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. MONESI V. AUTORADIOGRAPHIC EVIDENCE OF A NUCLEAR HISTONE SYNTHESIS DURING MOUSE SPERMIOGENESIS IN THE ABSENCE OF DETECTABLE QUANTITIES OF NUCLEAR RIBONUCLEIC ACID. Exp Cell Res. 1964 Dec;36:683–688. doi: 10.1016/0014-4827(64)90326-x. [DOI] [PubMed] [Google Scholar]
  18. MONESI V. Autoradiographic study of DNA synthesis and the cell cycle in spermatogonia and spermatocytes of mouse testis using tritiated thymidine. J Cell Biol. 1962 Jul;14:1–18. doi: 10.1083/jcb.14.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. MONESI V. RIBONUCLEIC ACID SYNTHESIS DURING MITOSIS AND MEIOSIS IN THE MOUSE TESTIS. J Cell Biol. 1964 Sep;22:521–532. doi: 10.1083/jcb.22.3.521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. MOSES M. J. Spermiogenesis in the crayfish (Procambarus clarkii) II. Description of stages. J Biophys Biochem Cytol. 1961 Jul;10:301–333. doi: 10.1083/jcb.10.3.301. [DOI] [PMC free article] [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. NEBEL B. R., AMAROSE A. P., HACKET E. M. Calendar of gametogenic development in the prepuberal male mouse. Science. 1961 Sep 22;134(3482):832–833. doi: 10.1126/science.134.3482.832. [DOI] [PubMed] [Google Scholar]
  23. Olins D. E., Olins A. L., Von Hippel P. H. On the structure and stability of DNA-protamine and DNA-polypeptide complexes. J Mol Biol. 1968 Apr 14;33(1):265–281. doi: 10.1016/0022-2836(68)90293-3. [DOI] [PubMed] [Google Scholar]
  24. Pogo B. G., Allfrey V. G., Mirsky A. E. RNA synthesis and histone acetylation during the course of gene activation in lymphocytes. Proc Natl Acad Sci U S A. 1966 Apr;55(4):805–812. doi: 10.1073/pnas.55.4.805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Raaf J., Bonner J. Properties of Escherichia coli deoxyribonucleoprotein as compared with the deoxyribonucleoprotein of higher organisms. Arch Biochem Biophys. 1968 May;125(2):567–579. doi: 10.1016/0003-9861(68)90615-2. [DOI] [PubMed] [Google Scholar]
  26. SWIERSTRA E. E., FOOTE R. H. DURATION OF SPERMATOGENESIS AND SPERMATOZOAN TRANSPORT IN THE RABBIT BASED ON CYTOLOGICAL CHANGES, DNA SYNTHESIS AND LABELING WITH TRITIATED THYMIDINE. Am J Anat. 1965 Mar;116:401–412. doi: 10.1002/aja.1001160206. [DOI] [PubMed] [Google Scholar]
  27. SWIFT H. H. The desoxyribose nucleic acid content of animal nuclei. Physiol Zool. 1950 Jul;23(3):169–198. doi: 10.1086/physzool.23.3.30152074. [DOI] [PubMed] [Google Scholar]
  28. Skalka A., Fowler A. V., Hurwitz J. The effect of histones on the enzymatic synthesis of ribonucleic acid. J Biol Chem. 1966 Feb 10;241(3):588–596. [PubMed] [Google Scholar]
  29. Vaughn J. C., Chaitoff J., Deleon R., Garland C., Thomson L. Changing nuclear histone patterns during development. II. Isolation and partial characterization of "decapodine" from sperm cells of the crab Emerita analoga. Exp Cell Res. 1969 Mar;54(3):362–366. doi: 10.1016/0014-4827(69)90215-8. [DOI] [PubMed] [Google Scholar]
  30. Vaughn J. C. Changind nuclear histone patterns during development. I. Fertilization and early cleavage in the crab, Emerita analoga. J Histochem Cytochem. 1968 Jul;16(7):473–479. doi: 10.1177/16.7.473. [DOI] [PubMed] [Google Scholar]
  31. Vaughn J. C., Locy R. D. Changing nuclear histone patterns during development. 3. The deoxyribonucleic acid content of spermatogenic cells in the crab Emerita analoga. J Histochem Cytochem. 1969 Sep;17(9):591–600. doi: 10.1177/17.9.591. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES