Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1964 Sep 1;22(3):521–532. doi: 10.1083/jcb.22.3.521

RIBONUCLEIC ACID SYNTHESIS DURING MITOSIS AND MEIOSIS IN THE MOUSE TESTIS

Valerio Monesi 1
PMCID: PMC2106469  PMID: 14206420

Abstract

The pattern of ribonucleic acid synthesis during germ cell development, from the stem cell to the mature spermatid, was studied in the mouse testis, by using uridine-H3 or cytidine-H3 labeling and autoradiography. Incorporation of tritiated precursors into the RNA occurs in spermatogonia, resting primary spermatocytes (RPS), throughout the second half of pachytene stage up to early diplotene, and in the Sertoli cells. Cells in leptotene, zygotene, and in the first half of pachytene stage do not synthesize RNA. No RNA synthesis was detected in meiotic stages later than diplotene, with the exception of a very low rate of incorporation in a fraction of secondary spermatocytes and very early spermatids. At long intervals after administration of the tracer, as labeled cells develop to more mature stages, late stages of spermatogenesis also become labeled. The last structures to become labeled are the residual bodies of Regaud. Thus, the RNA synthesized during the active meiotic stages is partially retained within the cell during further development. The rate of RNA synthesis declines gradually with the maturation from type A to intermediate to type B spermatogonia and to resting primary spermatocytes. "Dormant" type A spermatogonia synthesize little or no RNA. The incorporation of RNA precursors occurs exclusively within the nucleus: at later postinjection intervals the cytoplasm also becomes labeled. In spermatogonia all mitotic stages, except metaphase and anaphase, were shown to incorporate uridine-H3. RNA synthesis is then a continuous process throughout the cell division cycle in spermatogonia (generation time about 30 hours), and stops only for a very short interval (1 hour) during metaphase and anaphase.

Full Text

The Full Text of this article is available as a PDF (1.0 MB).

Selected References

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

  1. CLELAND K. W. The spermatogenic cycle of the guinea pig. Aust J Sci Res B. 1951 Aug;4(3):344–369. doi: 10.1071/bi9510344. [DOI] [PubMed] [Google Scholar]
  2. CLERMONT Y., LEBLOND C. P. Renewal of spermatogonia in the rat. Am J Anat. 1953 Nov;93(3):475–501. doi: 10.1002/aja.1000930308. [DOI] [PubMed] [Google Scholar]
  3. DAOUST R., CLERMONT Y. Distribution of nucleic acids in germ cells during the cycle of the seminiferous epithelium in the rat. Am J Anat. 1955 Mar;96(2):255–283. doi: 10.1002/aja.1000960204. [DOI] [PubMed] [Google Scholar]
  4. FAWCETT D. W., ITO S. Observations on the cytoplasmic membranes of testicular cells, examined by phase contrast and electron microscopy. J Biophys Biochem Cytol. 1958 Mar 25;4(2):135–142. doi: 10.1083/jcb.4.2.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. FAWCETT D. W., ITO S., SLAUTTERBACK D. The occurrence of intercellular bridges in groups of cells exhibiting synchronous differentiation. J Biophys Biochem Cytol. 1959 May 25;5(3):453–460. doi: 10.1083/jcb.5.3.453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. FEINENDEGEN L. E., BOND V. P. Observations on nuclear RNA during mitosis in human cancer cells in culture (HeLa-S3), studied with tritiated cytidine. Exp Cell Res. 1963 Apr;30:393–404. doi: 10.1016/0014-4827(63)90311-2. [DOI] [PubMed] [Google Scholar]
  7. GOLDSTEIN L., MICOU J. Nuclear-cytoplasmic relationships in human cells in tissue culture. III. Auto-radiographic study of interrelation of nuclear and cytoplasmic ribonucleic acid. J Biophys Biochem Cytol. 1959 Aug;6(1):1–6. doi: 10.1083/jcb.6.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. GOLDSTEIN L., MICOU J. On the primary site of nuclear RNA synthesis. J Biophys Biochem Cytol. 1959 Oct;6:301–304. doi: 10.1083/jcb.6.2.301. [DOI] [PMC free article] [PubMed] [Google Scholar] [Retracted]
  9. HOWARD A., PELC S. R. A difference between spermatogonia and somatic tissues of mice in the incorporation of [8-14C]-adenine into deoxyribonucleic acid. Exp Cell Res. 1956 Aug;11(1):128–134. doi: 10.1016/0014-4827(56)90197-5. [DOI] [PubMed] [Google Scholar]
  10. LACOUR L. F. Ribose nucleic acid and the metaphase chromosome. Exp Cell Res. 1963 Jan;29:112–118. doi: 10.1016/0014-4827(63)90364-1. [DOI] [PubMed] [Google Scholar]
  11. LACY D. Light and electron microscopy and its use in the study of factors influencing spermatogenesis in the rat. J R Microsc Soc. 1960 Oct;79:209–225. doi: 10.1111/j.1365-2818.1959.tb04469.x. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. 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]
  14. 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]
  15. OAKBERG E. F. A description of spermiogenesis in the mouse and its use in analysis of the cycle of the seminiferous epithelium and germ cell renewal. Am J Anat. 1956 Nov;99(3):391–413. doi: 10.1002/aja.1000990303. [DOI] [PubMed] [Google Scholar]
  16. OAKBERG E. F. Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium. Am J Anat. 1956 Nov;99(3):507–516. doi: 10.1002/aja.1000990307. [DOI] [PubMed] [Google Scholar]
  17. PASTEELS J. Recherches sur le cycle germinal chez l'Ascaris; étude cytochimique des acides nucléiques dans l'oögénèse, la spermatogénès et le développement chez Parascaris equorum Goerze. Arch Biol (Liege) 1948;59(4):405–446. [PubMed] [Google Scholar]
  18. PELC S. R. On the connection between the synthesis of RNA and DNA in the testis of the mouse. Exp Cell Res. 1957 Apr;12(2):320–324. doi: 10.1016/0014-4827(57)90145-3. [DOI] [PubMed] [Google Scholar]
  19. PERRY R. P. On the nucleolar and nuclear dependence of cytoplasmic RNA synthesis in HeLa cells. Exp Cell Res. 1960 Jun;20:216–220. doi: 10.1016/0014-4827(60)90240-8. [DOI] [PubMed] [Google Scholar]
  20. PRESCOTT D. M., BENDER M. A. Synthesis of RNA and protein during mitosis in mammalian tissue culture cells. Exp Cell Res. 1962 Mar;26:260–268. doi: 10.1016/0014-4827(62)90176-3. [DOI] [PubMed] [Google Scholar]
  21. ROOSEN-RUNGE E. C. Kinetics of spermatogenesis in mammals. Ann N Y Acad Sci. 1952 Nov 20;55(4):574–584. doi: 10.1111/j.1749-6632.1952.tb26577.x. [DOI] [PubMed] [Google Scholar]
  22. ROOSEN-RUNGE E. C. The process of spermatogenesis in mammals. Biol Rev Camb Philos Soc. 1962 Aug;37:343–377. doi: 10.1111/j.1469-185x.1962.tb01616.x. [DOI] [PubMed] [Google Scholar]
  23. RUTHMANN A. Basophilic lamellar systems in the crayfish spermatocyte. J Biophys Biochem Cytol. 1958 May 25;4(3):267–274. doi: 10.1083/jcb.4.3.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. TAYLOR J. H. Nucleic acid synthesis in relation to the cell division cycle. Ann N Y Acad Sci. 1960 Oct 7;90:409–421. doi: 10.1111/j.1749-6632.1960.tb23259.x. [DOI] [PubMed] [Google Scholar]
  25. TERASIMA T., TOLMACH L. J. Growth and nucleic acid synthesis in synchronously dividing populations of HeLa cells. Exp Cell Res. 1963 Apr;30:344–362. doi: 10.1016/0014-4827(63)90306-9. [DOI] [PubMed] [Google Scholar]
  26. WOODS P. S., TAYLOR J. H. Studies of ribonucleic acid metabolism with tritium-labeled cytidine. Lab Invest. 1959 Jan-Feb;8(1):309–318. [PubMed] [Google Scholar]
  27. ZALOKAR M. Sites of protein and ribonucleic acid synthesis in the cell. Exp Cell Res. 1960 Apr;19:559–576. doi: 10.1016/0014-4827(60)90064-1. [DOI] [PubMed] [Google Scholar]

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

RESOURCES