Abstract
The transcriptional activity during meiotic prophase in the mouse testis is studied with light microscopy and high-resolution autoradiographic techniques using [3H]uridine as a labeled precursor. In the present study, two types of RNA synthesis are detected during meiotic prophase: an extranucleolar RNA synthesis of perichromosomal localization and a nucleolar RNA synthetic activity. In some of the autosomes and close to the basal knobs, the activity of the nucleolar organizers is evidenced by the incorporation of [3H]uridine into nucleolar masses from zygotene on and at earlier labeling times. The evolution of nucleoli and the formation of a nucleolus attached to the sex pair are described during the different meiotic stages. Perichromosomal labeling, from leptotene on, reaches a maximum during middle pachytene and falls progressively to a low level at longer incorporation times. Sertoli's cell, the most active RNA synthetic cell in the seminiferous epithelium, rises to a maximum of labeling and drops at earlier times compared with the meiotic prophase cells. The condensed sex chromosomes show some scattered silver grains especially at middle pachytene. The axial chromosome cores and synaptonemal complexes are devoid of silver grains during the meiotic prophase. The observations suggest that a control mechanism operates during meiotic prophase to regulate transcriptional activity in the sex chromosomes and to provide differential RNA synthesis in autosomal bivalents at various stages of prophase and within certain segments of the chromosomes.
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- CARO L. G., VAN TUBERGEN R. P., KOLB J. A. High-resolution autoradiography. I. Methods. J Cell Biol. 1962 Nov;15:173–188. doi: 10.1083/jcb.15.2.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DAS N. K., SIEGEL E. P., ALFERT M. SYNTHETIC ACTIVITIES DURING SPERMATOGENESIS IN THE LOCUST. J Cell Biol. 1965 May;25:387–395. doi: 10.1083/jcb.25.2.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Darnell J. E., Jr Ribonucleic acids from animal cells. Bacteriol Rev. 1968 Sep;32(3):262–290. doi: 10.1128/br.32.3.262-290.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Darnell J. E., Philipson L., Wall R., Adesnik M. Polyadenylic acid sequences: role in conversion of nuclear RNA into messenger RNA. Science. 1971 Oct 29;174(4008):507–510. doi: 10.1126/science.174.4008.507. [DOI] [PubMed] [Google Scholar]
- Das N. K., Alfert M. Nucleolar RNA synthesis during mitotic and meiotic prophase. Natl Cancer Inst Monogr. 1966 Dec;23:337–351. [PubMed] [Google Scholar]
- Fakan S., Bernhard W. Localisation of rapidly and slowly labelled nuclear RNA as visualized by high resolution autoradiography. Exp Cell Res. 1971 Jul;67(1):129–141. doi: 10.1016/0014-4827(71)90628-8. [DOI] [PubMed] [Google Scholar]
- GALL J. G., CALLAN H. G. H3 uridine incorporation in lampbrush chromosomes. Proc Natl Acad Sci U S A. 1962 Apr 15;48:562–570. doi: 10.1073/pnas.48.4.562. [DOI] [PMC free article] [PubMed] [Google Scholar]
- GRANBOULAN N., GRANBOULAN P. CYTOCHIMIE ULTRASTRUCTURALE DU NUCL'EOLE. II. ETUDE DES SITES DE SYNTH'ESE DU RNA DANS LE NUCL'EOLE ET LE NOYAU. Exp Cell Res. 1965 Jun;38:604–619. doi: 10.1016/0014-4827(65)90384-8. [DOI] [PubMed] [Google Scholar]
- HENDERSON S. A. DIFFERENTIAL RIBONUCLEIC ACID SYNTHESIS OF X AND AUTOSOMES DURING MEIOSIS. Nature. 1963 Dec 21;200:1235–1235. doi: 10.1038/2001235a0. [DOI] [PubMed] [Google Scholar]
- Hsu T. C., Cooper J. E., Mace M. L., Jr, Brinkley B. R. Arrangement of centromeres in mouse cells. Chromosoma. 1971;34(1):73–87. doi: 10.1007/BF00285517. [DOI] [PubMed] [Google Scholar]
- LITTAU V. C., ALLFREY V. G., FRENSTER J. H., MIRSKY A. E. ACTIVE AND INACTIVE REGIONS OF NUCLEAR CHROMATIN AS REVEALED BY ELECTRON MICROSCOPE AUTORADIOGRAPHY. Proc Natl Acad Sci U S A. 1964 Jul;52:93–100. doi: 10.1073/pnas.52.1.93. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Monesi V. Differential rate of ribonucleic acid synthesis in the autosomes and sex chromosomes during male meiosis in the mouse. Chromosoma. 1965;17(1):11–21. doi: 10.1007/BF00285153. [DOI] [PubMed] [Google Scholar]
- 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]
- Moore G. P. DNA-dependent RNA synthesis in fixed cells during spermatogenesis in mouse. Exp Cell Res. 1971 Oct;68(2):462–465. doi: 10.1016/0014-4827(71)90176-5. [DOI] [PubMed] [Google Scholar]
- Muramatsu M., Utakoji T., Sugano H. Rapidly-labeled nuclear RNA in Chinese hamster testis. Exp Cell Res. 1968 Oct;53(1):278–283. doi: 10.1016/0014-4827(68)90375-3. [DOI] [PubMed] [Google Scholar]
- Noel J. S., Dewey W. C., Abel J. H., Jr, Thompson R. P. Ultrastructure of the nucleolus during the Chinese hamster cell cycle. J Cell Biol. 1971 Jun;49(3):830–847. doi: 10.1083/jcb.49.3.830. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- OAKBERG E. F. Duration of spermatogenesis in the mouse. Nature. 1957 Nov 23;180(4595):1137–1138. doi: 10.1038/1801137a0. [DOI] [PubMed] [Google Scholar]
- OHNO S., KAPLAN W. D., KINOSITA R. Heterochromatic regions and nucleolus organizers in chromosomes of the mouse, Mus musculus. Exp Cell Res. 1957 Oct;13(2):358–364. doi: 10.1016/0014-4827(57)90015-0. [DOI] [PubMed] [Google Scholar]
- 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]
- Parchman L. G., Lin K. C. Nucleolar RNA synthesis during meiosis of lily microsporocytes. Nat New Biol. 1972 Oct 25;239(95):235–237. doi: 10.1038/newbio239235a0. [DOI] [PubMed] [Google Scholar]
- Polani P. E. Centromere localization at meiosis and the position of chiasmata in the male and female mouse. Chromosoma. 1972;36(4):343–374. doi: 10.1007/BF00336793. [DOI] [PubMed] [Google Scholar]
- Rocchi Brasiello A. Autoradiographic study of ribonucleic acid synthesis during spermatogenesis of Asellus aquaticus (Crust. Isopoda). Exp Cell Res. 1968 Oct;53(1):252–260. doi: 10.1016/0014-4827(68)90371-6. [DOI] [PubMed] [Google Scholar]
- SACHS L. The possibilities of crossing-over between the sex chromosomes of the house mouse. Genetica. 1955;27(5-6):309–322. doi: 10.1007/BF01664166. [DOI] [PubMed] [Google Scholar]
- Salpeter M. M., Szabo M. Sensitivity in electron microscope autoradiography. I. The effect of radiation dose. J Histochem Cytochem. 1972 Jun;20(6):425–434. doi: 10.1177/20.6.425. [DOI] [PubMed] [Google Scholar]
- Schnedl W. End-to-end association of X and Y chromosomes in mouse meiosis. Nat New Biol. 1972 Mar 8;236(62):29–30. doi: 10.1038/newbio236029a0. [DOI] [PubMed] [Google Scholar]
- Solari A. J. The spatial relationship of the X and Y chromosomes during meiotic prophase in mouse spermatocytes. Chromosoma. 1970;29(2):217–236. doi: 10.1007/BF00326080. [DOI] [PubMed] [Google Scholar]
- Solari A. J., Tres L. The localization of nucleic acids and the argentaffin substance in the sex vesicle of mouse spermatocytes. Exp Cell Res. 1967 Aug;47(1):86–96. doi: 10.1016/0014-4827(67)90212-1. [DOI] [PubMed] [Google Scholar]
- 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]
- Tres L. L., Kierszenbaum A. L., Tandler C. J. Inorganic cations in the cell nucleus. Selective accumulation during meiotic prophase in mouse testis. J Cell Biol. 1972 May;53(2):483–493. doi: 10.1083/jcb.53.2.483. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Utakoji T. Chronology of nucleic acid synthesis in meiosis of the male Chinese hamster. Exp Cell Res. 1966 Jun;42(3):585–596. doi: 10.1016/0014-4827(66)90271-0. [DOI] [PubMed] [Google Scholar]
- WOOLLAM D. H., FORD E. H. THE FINE STRUCTURE OF THE MAMMALIAN CHROMOSOME IN MEIOTIC PROPHASE WITH SPECIAL REFERENCE TO THE SYNAPTINEMAL COMPLEX. J Anat. 1964 Apr;98:163–173. [PMC free article] [PubMed] [Google Scholar]
- Yasmineh W. G., Yunis J. J. Localization of mouse satellite DNA in constitutive heterochromatin. Exp Cell Res. 1970 Jan;59(1):69–75. doi: 10.1016/0014-4827(70)90624-5. [DOI] [PubMed] [Google Scholar]