Abstract
Mice were injected intraperitoneally with 15 µc of H3-thymidine. The time course of the labeling in spermatogonia and spermatocytes was studied by using autoradiography on 5 µ sections stained by the periodic acid-Schiff method and hematoxylin over a period of 57 hours after injection. Four generations of type A (called AI, AII, AIII, and AIV), one of intermediate, and one of type B spermatogonia occur in one cycle of the seminiferous epithelium. The average life span is about the same in all spermatogonia, i.e., about 27 to 30.5 hours. The average pre-DNA synthetic time, including the mitotic stages from metaphase through telophase and the portion of interphase preceding DNA synthesis, is also not very different, ranging between 7.5 and 10.5 hours. A remarkable difference exists, however, in the duration of DNA synthesis and of the post-DNA synthetic period. The average DNA synthetic time is very long and is highly variable in type B (14.5 hours), a little shorter and less variable in intermediate (12.5 hours) and AIV (13 hours) spermatogonia, and much shorter and very constant in AIII (8 hours), AII and AI (7 to 7.5 hours) spermatogonia. Conversely, the average post-DNA synthetic time, corresponding essentially to the duration of the prophase, is short and very constant in type B (4.5 hours), longer and variable in intermediate (6 hours) and AIV (8 hours) spermatogonia, and much longer and much more variable in AIII (11 hours), AII and AI (14 hours) spermatogonia. The premeiotic synthesis of DNA takes place in primary spermatocytes during the resting phase and terminates just before the visible onset of the meiotic prophase. Its average duration is 14 hours. No further synthesis of DNA takes place in later stages of spermatogenesis.
Full Text
The Full Text of this article is available as a PDF (1.2 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- 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]
- CRATHORN A. R., SHOOTER K. V. Uptake of thymidine and synthesis of deoxyribonucleic acid in mouse ascites cells. Nature. 1960 Aug 13;187:614–615. doi: 10.1038/187614a0. [DOI] [PubMed] [Google Scholar]
- CRONKITE E. P., BOND V. P., FLIEDNER T. M., RUBINI J. R. The use of tritiated thymidine in the study of DNS synthesis and cell turnover in hemopoietic tissues. Lab Invest. 1959 Jan-Feb;8(1):263–277. [PubMed] [Google Scholar]
- DREW R. M., PAINTER R. B. Action of tritiated thymidine on the clonal growth of mammalian cells. Radiat Res. 1959 Oct;11:535–544. [PubMed] [Google Scholar]
- FITZGERALD P. J., EIDINOFF M. L., KNOLL J. E., SIMMEL E. B. Tritium in radioautography. Science. 1951 Nov 9;114(2967):494–498. doi: 10.1126/science.114.2967.494. [DOI] [PubMed] [Google Scholar]
- 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]
- HOWARD A., PELC S. R. P32 autoradiographs of mouse testis; preliminary observations of the timing of spermatogenic stages. Br J Radiol. 1950 Nov;23(275):634–641. doi: 10.1259/0007-1285-23-275-634. [DOI] [PubMed] [Google Scholar]
- Hughes W. L., Bond V. P., Brecher G., Cronkite E. P., Painter R. B., Quastler H., Sherman F. G. CELLULAR PROLIFERATION IN THE MOUSE AS REVEALED BY AUTORADIOGRAPHY WITH TRITIATED THYMIDINE. Proc Natl Acad Sci U S A. 1958 May;44(5):476–483. doi: 10.1073/pnas.44.5.476. [DOI] [PMC free article] [PubMed] [Google Scholar]
- JOHNSON H. A., CRONKITE E. P. The effect of tritiated thymidine on mouse spermatogonia. Radiat Res. 1959 Dec;11:825–831. [PubMed] [Google Scholar]
- LAJTHA L. G., OLIVER R., ELLIS F. Incorporation of 32P and adenine 14C into DNA by human bone marrow cells in vitro. Br J Cancer. 1954 Jun;8(2):367–379. doi: 10.1038/bjc.1954.38. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LAJTHA L. G., OLIVER R. The application of autoradiography in the study of nucleic acid metabolism. Lab Invest. 1959 Jan-Feb;8(1):214–224. [PubMed] [Google Scholar]
- 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]
- LIMA-DE-FARIA A. Differential uptake of tritiated thymidine into hetero- and euchromatin in Melanoplus and Secale. J Biophys Biochem Cytol. 1959 Dec;6:457–466. doi: 10.1083/jcb.6.3.457. [DOI] [PMC free article] [PubMed] [Google Scholar]
- MCQUADE H. A., FRIEDKIN M. Radiation effects of thymidine-H-3 and thymidine-C-14. Exp Cell Res. 1960 Oct;21:118–125. doi: 10.1016/0014-4827(60)90352-9. [DOI] [PubMed] [Google Scholar]
- MENDELSOHN M. L., DOHAN F. C., Jr, MOORE H. A., Jr Autoradiographic analysis of cell proliferation in spontaneous breast cancer of C3H mouse. I. Typical cell cycle and timing of DNA synthesis. J Natl Cancer Inst. 1960 Sep;25:477–484. [PubMed] [Google Scholar]
- MESSIER B., LEBLOND C. P. Cell proliferation and migration as revealed by radioautography after injection of thymidine-H3 into male rats and mice. Am J Anat. 1960 May;106:247–285. doi: 10.1002/aja.1001060305. [DOI] [PubMed] [Google Scholar]
- NATARAJAN A. T. Chromosome breakage and mitotic inhibition induced by tritiated thymidine in root meristems of Vicia faba. Exp Cell Res. 1961 Jan;22:275–281. doi: 10.1016/0014-4827(61)90106-9. [DOI] [PubMed] [Google Scholar]
- PAINTER R. B., DREW R. M., GIAUQUE B. G. Further studies on deoxyribonucleic acid metabolism in mammalian cell cultures. Exp Cell Res. 1960 Oct;21:98–105. doi: 10.1016/0014-4827(60)90350-5. [DOI] [PubMed] [Google Scholar]
- PAINTER R. B., DREW R. M., HUGHES W. L. Inhibition of HeLa growth by intranuclear tritium. Science. 1958 May 23;127(3308):1244–1245. doi: 10.1126/science.127.3308.1244. [DOI] [PubMed] [Google Scholar]
- PAINTER R. B., DREW R. M. Studies on deoxyribonucleic acid metabolism in human cancer cell cultures (HeLa). I. The temporal relationships of deoxyribonucleic acid synthesis to mitosis and turnover time. Lab Invest. 1959 Jan-Feb;8(1):278–285. [PubMed] [Google Scholar]
- PAINTER R. B., FORRO F., Jr, HUGHES W. L. Distribution of tritium-labelled thymidine in Escherichia coli during cell multiplication. Nature. 1958 Feb 1;181(4605):328–329. doi: 10.1038/181328a0. [DOI] [PubMed] [Google Scholar]
- PLAUT W. The effect of tritium on the interpretation of autoradiographic studies on chromosomes. Lab Invest. 1959 Jan-Feb;8(1):286–295. [PubMed] [Google Scholar]
- QUASTLER H., SHERMAN F. G. Cell population kinetics in the intestinal epithelium of the mouse. Exp Cell Res. 1959 Jun;17(3):420–438. doi: 10.1016/0014-4827(59)90063-1. [DOI] [PubMed] [Google Scholar]
- REICHARD P., ESTBORN B. Utilization of desoxyribosides in the synthesis of polynucleotides. J Biol Chem. 1951 Feb;188(2):839–846. [PubMed] [Google Scholar]
- RUBINI J. R., CRONKITE E. P., BOND V. P., FLIEDNER T. M. The metabolism and fate of tritiated thymidine in man. J Clin Invest. 1960 Jun;39:909–918. doi: 10.1172/JCI104111. [DOI] [PMC free article] [PubMed] [Google Scholar]
- SIRLIN J. L., EDWARDS R. G. The labelling of mammalina spermatozoa with radioactive tracers. J Exp Zool. 1958 Apr;137(3):363–388. doi: 10.1002/jez.1401370302. [DOI] [PubMed] [Google Scholar]
- SIRLIN J. L., EDWARDS R. G. The labelling of mouse sperm by adenine-8-C-14. Exp Cell Res. 1955 Dec;9(3):596–599. doi: 10.1016/0014-4827(55)90093-8. [DOI] [PubMed] [Google Scholar]
- SISKEN J. E. The synthesis of nucleic acids and proteins in the nuclei of Tradescantia root tips. Exp Cell Res. 1959 Mar;16(3):602–614. doi: 10.1016/0014-4827(59)90128-4. [DOI] [PubMed] [Google Scholar]
- 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]
- TAYLOR J. H. Asynchronous duplication of chromosomes in cultured cells of Chinese hamster. J Biophys Biochem Cytol. 1960 Jun;7:455–464. doi: 10.1083/jcb.7.3.455. [DOI] [PMC free article] [PubMed] [Google Scholar]
- TAYLOR J. H. The mode of chromosome duplication in Crepis capillaris. Exp Cell Res. 1958 Oct;15(2):350–357. doi: 10.1016/0014-4827(58)90036-3. [DOI] [PubMed] [Google Scholar]
- Taylor J. H., Woods P. S., Hughes W. L. THE ORGANIZATION AND DUPLICATION OF CHROMOSOMES AS REVEALED BY AUTORADIOGRAPHIC STUDIES USING TRITIUM-LABELED THYMIDINEE. Proc Natl Acad Sci U S A. 1957 Jan 15;43(1):122–128. doi: 10.1073/pnas.43.1.122. [DOI] [PMC free article] [PubMed] [Google Scholar]