Skip to main content
The EMBO Journal logoLink to The EMBO Journal
. 1989 Jun;8(6):1855–1860. doi: 10.1002/j.1460-2075.1989.tb03581.x

DNA topoisomerase II activity in nonreplicating, transcriptionally inactive, chicken late spermatids.

J Roca 1, C Mezquita 1
PMCID: PMC401034  PMID: 2548858

Abstract

To study a possible differential involvement of type I and type II DNA topoisomerases in the functional and structural changes that chromatin undergoes during spermatogenesis, we have determined both enzymatic activities in chicken testis cell nuclei at successive stages of differentiation. Whereas DNA topoisomerase I varies in parallel with transcriptional activity, DNA topoisomerase II was present in both replicating, transcriptionally active chicken testis cells and nonreplicating, transcriptionally inactive late spermatids. The presence of DNA topoisomerase II activity in late spermatids and, in addition, the relative increment of drug-induced topo-II-mediated DNA cleavage detected in these cells, suggest that DNA topoisomerase II might modulate the topology of DNA during the marked changes that chromatin structure undergoes in the nucleohistone-nucleoprotamine transition at the end of the spermiogenesis and could be involved in the final organization of DNA within the nucleus of the male gamete.

Full text

PDF
1855

Images in this article

Selected References

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

  1. Bennett M. D., Heslop-Harrison J. S., Smith J. B., Ward J. P. DNA density in mitotic and meiotic metaphase chromosomes of plants and animals. J Cell Sci. 1983 Sep;63:173–179. doi: 10.1242/jcs.63.1.173. [DOI] [PubMed] [Google Scholar]
  2. Berrios M., Osheroff N., Fisher P. A. In situ localization of DNA topoisomerase II, a major polypeptide component of the Drosophila nuclear matrix fraction. Proc Natl Acad Sci U S A. 1985 Jun;82(12):4142–4146. doi: 10.1073/pnas.82.12.4142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brill S. J., DiNardo S., Voelkel-Meiman K., Sternglanz R. Need for DNA topoisomerase activity as a swivel for DNA replication for transcription of ribosomal RNA. 1987 Mar 26-Apr 1Nature. 326(6111):414–416. doi: 10.1038/326414a0. [DOI] [PubMed] [Google Scholar]
  4. Chow K. C., Ross W. E. Topoisomerase-specific drug sensitivity in relation to cell cycle progression. Mol Cell Biol. 1987 Sep;7(9):3119–3123. doi: 10.1128/mcb.7.9.3119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cozzarelli N. R. DNA topoisomerases. Cell. 1980 Nov;22(2 Pt 2):327–328. doi: 10.1016/0092-8674(80)90341-4. [DOI] [PubMed] [Google Scholar]
  6. Culotta V., Sollner-Webb B. Sites of topoisomerase I action on X. laevis ribosomal chromatin: transcriptionally active rDNA has an approximately 200 bp repeating structure. Cell. 1988 Feb 26;52(4):585–597. doi: 10.1016/0092-8674(88)90471-0. [DOI] [PubMed] [Google Scholar]
  7. DiNardo S., Voelkel K., Sternglanz R. DNA topoisomerase II mutant of Saccharomyces cerevisiae: topoisomerase II is required for segregation of daughter molecules at the termination of DNA replication. Proc Natl Acad Sci U S A. 1984 May;81(9):2616–2620. doi: 10.1073/pnas.81.9.2616. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Duguet M., Lavenot C., Harper F., Mirambeau G., De Recondo A. M. DNA topoisomerases from rat liver: physiological variations. Nucleic Acids Res. 1983 Feb 25;11(4):1059–1075. doi: 10.1093/nar/11.4.1059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Earnshaw W. C., Halligan B., Cooke C. A., Heck M. M., Liu L. F. Topoisomerase II is a structural component of mitotic chromosome scaffolds. J Cell Biol. 1985 May;100(5):1706–1715. doi: 10.1083/jcb.100.5.1706. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fleischmann G., Pflugfelder G., Steiner E. K., Javaherian K., Howard G. C., Wang J. C., Elgin S. C. Drosophila DNA topoisomerase I is associated with transcriptionally active regions of the genome. Proc Natl Acad Sci U S A. 1984 Nov;81(22):6958–6962. doi: 10.1073/pnas.81.22.6958. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Garner M. M., Felsenfeld G., O'Dea M. H., Gellert M. Effects of DNA supercoiling on the topological properties of nucleosomes. Proc Natl Acad Sci U S A. 1987 May;84(9):2620–2623. doi: 10.1073/pnas.84.9.2620. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gasser S. M., Laemmli U. K. The organisation of chromatin loops: characterization of a scaffold attachment site. EMBO J. 1986 Mar;5(3):511–518. doi: 10.1002/j.1460-2075.1986.tb04240.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gasser S. M., Laroche T., Falquet J., Boy de la Tour E., Laemmli U. K. Metaphase chromosome structure. Involvement of topoisomerase II. J Mol Biol. 1986 Apr 20;188(4):613–629. doi: 10.1016/s0022-2836(86)80010-9. [DOI] [PubMed] [Google Scholar]
  14. Gellert M. DNA topoisomerases. Annu Rev Biochem. 1981;50:879–910. doi: 10.1146/annurev.bi.50.070181.004311. [DOI] [PubMed] [Google Scholar]
  15. Gilmour D. S., Elgin S. C. Localization of specific topoisomerase I interactions within the transcribed region of active heat shock genes by using the inhibitor camptothecin. Mol Cell Biol. 1987 Jan;7(1):141–148. doi: 10.1128/mcb.7.1.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gilmour D. S., Pflugfelder G., Wang J. C., Lis J. T. Topoisomerase I interacts with transcribed regions in Drosophila cells. Cell. 1986 Feb 14;44(3):401–407. doi: 10.1016/0092-8674(86)90461-7. [DOI] [PubMed] [Google Scholar]
  17. Glikin G. C., Blangy D. In vitro transcription by Xenopus oocytes RNA polymerase III requires a DNA topoisomerase II activity. EMBO J. 1986 Jan;5(1):151–155. doi: 10.1002/j.1460-2075.1986.tb04189.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Green G. R., Poccia D. L. Phosphorylation of sea urchin sperm H1 and H2B histones precedes chromatin decondensation and H1 exchange during pronuclear formation. Dev Biol. 1985 Mar;108(1):235–245. doi: 10.1016/0012-1606(85)90026-0. [DOI] [PubMed] [Google Scholar]
  19. Heck M. M., Earnshaw W. C. Topoisomerase II: A specific marker for cell proliferation. J Cell Biol. 1986 Dec;103(6 Pt 2):2569–2581. doi: 10.1083/jcb.103.6.2569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Heck M. M., Hittelman W. N., Earnshaw W. C. Differential expression of DNA topoisomerases I and II during the eukaryotic cell cycle. Proc Natl Acad Sci U S A. 1988 Feb;85(4):1086–1090. doi: 10.1073/pnas.85.4.1086. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Heller R. A., Shelton E. R., Dietrich V., Elgin S. C., Brutlag D. L. Multiple forms and cellular localization of Drosophila DNA topoisomerase II. J Biol Chem. 1986 Jun 15;261(17):8063–8069. [PubMed] [Google Scholar]
  22. Igó-Kemenes T., Zachau H. G. Domains in chromatin structure. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 1):109–118. doi: 10.1101/sqb.1978.042.01.012. [DOI] [PubMed] [Google Scholar]
  23. Kierszenbaum A. L., Tres L. L. RNA transcription and chromatin structure during meiotic and postmeiotic stages of spermatogenesis. Fed Proc. 1978 Sep;37(11):2512–2516. [PubMed] [Google Scholar]
  24. Kikuchi Y., Nash H. A. Nicking-closing activity associated with bacteriophage lambda int gene product. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3760–3764. doi: 10.1073/pnas.76.8.3760. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kohen R., Szyf M., Chevion M. Quantitation of single- and double-strand DNA breaks in vitro and in vivo. Anal Biochem. 1986 May 1;154(2):485–491. doi: 10.1016/0003-2697(86)90019-9. [DOI] [PubMed] [Google Scholar]
  26. Liu L. F. DNA topoisomerases--enzymes that catalyse the breaking and rejoining of DNA. CRC Crit Rev Biochem. 1983;15(1):1–24. doi: 10.3109/10409238309102799. [DOI] [PubMed] [Google Scholar]
  27. Liu L. F., Davis J. L., Calendar R. Novel topologically knotted DNA from bacteriophage P4 capsids: studies with DNA topoisomerases. Nucleic Acids Res. 1981 Aug 25;9(16):3979–3989. doi: 10.1093/nar/9.16.3979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Liu L. F., Liu C. C., Alberts B. M. Type II DNA topoisomerases: enzymes that can unknot a topologically knotted DNA molecule via a reversible double-strand break. Cell. 1980 Mar;19(3):697–707. doi: 10.1016/s0092-8674(80)80046-8. [DOI] [PubMed] [Google Scholar]
  29. Lähdetie J., Kaukopuro S., Parvinen M. 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. 1983;99(2):269–278. doi: 10.1111/j.1601-5223.1983.tb00899.x. [DOI] [PubMed] [Google Scholar]
  30. McIntosh J. R., Porter K. R. Microtubules in the spermatids of the domestic fowl. J Cell Biol. 1967 Oct;35(1):153–173. doi: 10.1083/jcb.35.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Meistrich M. L. Separation of spermatogenic cells and nuclei from rodent testes. Methods Cell Biol. 1977;15:15–54. doi: 10.1016/s0091-679x(08)60207-1. [DOI] [PubMed] [Google Scholar]
  32. Mezquita C., Teng C. S. Studies on sex-organ development. Changes in nuclear and chromatin composition and genomic activity during spermatogenesis in the maturing rooster testis. Biochem J. 1977 Apr 15;164(1):99–111. doi: 10.1042/bj1640099. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Muller M. T., Pfund W. P., Mehta V. B., Trask D. K. Eukaryotic type I topoisomerase is enriched in the nucleolus and catalytically active on ribosomal DNA. EMBO J. 1985 May;4(5):1237–1243. doi: 10.1002/j.1460-2075.1985.tb03766.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Nelson W. G., Liu L. F., Coffey D. S. Newly replicated DNA is associated with DNA topoisomerase II in cultured rat prostatic adenocarcinoma cells. Nature. 1986 Jul 10;322(6075):187–189. doi: 10.1038/322187a0. [DOI] [PubMed] [Google Scholar]
  35. Ness P. J., Koller T., Thoma F. Topoisomerase I cleavage sites identified and mapped in the chromatin of Dictyostelium ribosomal RNA genes. J Mol Biol. 1988 Mar 5;200(1):127–139. doi: 10.1016/0022-2836(88)90338-5. [DOI] [PubMed] [Google Scholar]
  36. Oliva R., Bazett-Jones D., Mezquita C., Dixon G. H. Factors affecting nucleosome disassembly by protamines in vitro. Histone hyperacetylation and chromatin structure, time dependence, and the size of the sperm nuclear proteins. J Biol Chem. 1987 Dec 15;262(35):17016–17025. [PubMed] [Google Scholar]
  37. Oliva R., Mezquita C. Marked differences in the ability of distinct protamines to disassemble nucleosomal core particles in vitro. Biochemistry. 1986 Oct 21;25(21):6508–6511. doi: 10.1021/bi00369a025. [DOI] [PubMed] [Google Scholar]
  38. Risley M. S., Einheber S., Bumcrot D. A. Changes in DNA topology during spermatogenesis. Chromosoma. 1986;94(3):217–227. doi: 10.1007/BF00288496. [DOI] [PubMed] [Google Scholar]
  39. Ross W., Rowe T., Glisson B., Yalowich J., Liu L. Role of topoisomerase II in mediating epipodophyllotoxin-induced DNA cleavage. Cancer Res. 1984 Dec;44(12 Pt 1):5857–5860. [PubMed] [Google Scholar]
  40. Rowe T. C., Wang J. C., Liu L. F. In vivo localization of DNA topoisomerase II cleavage sites on Drosophila heat shock chromatin. Mol Cell Biol. 1986 Apr;6(4):985–992. doi: 10.1128/mcb.6.4.985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sullivan D. M., Glisson B. S., Hodges P. K., Smallwood-Kentro S., Ross W. E. Proliferation dependence of topoisomerase II mediated drug action. Biochemistry. 1986 Apr 22;25(8):2248–2256. doi: 10.1021/bi00356a060. [DOI] [PubMed] [Google Scholar]
  42. Surani M. A., Barton S. C., Norris M. L. Nuclear transplantation in the mouse: heritable differences between parental genomes after activation of the embryonic genome. Cell. 1986 Apr 11;45(1):127–136. doi: 10.1016/0092-8674(86)90544-1. [DOI] [PubMed] [Google Scholar]
  43. Taudou G., Mirambeau G., Lavenot C., der Garabedian A., Vermeersch J., Duguet M. DNA topoisomerase activities in concanavalin A-stimulated lymphocytes. FEBS Lett. 1984 Oct 29;176(2):431–435. doi: 10.1016/0014-5793(84)81212-0. [DOI] [PubMed] [Google Scholar]
  44. Uemura T., Ohkura H., Adachi Y., Morino K., Shiozaki K., Yanagida M. DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell. 1987 Sep 11;50(6):917–925. doi: 10.1016/0092-8674(87)90518-6. [DOI] [PubMed] [Google Scholar]
  45. Uemura T., Tanagida M. Mitotic spindle pulls but fails to separate chromosomes in type II DNA topoisomerase mutants: uncoordinated mitosis. EMBO J. 1986 May;5(5):1003–1010. doi: 10.1002/j.1460-2075.1986.tb04315.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Vosberg H. P. DNA topoisomerases: enzymes that control DNA conformation. Curr Top Microbiol Immunol. 1985;114:19–102. doi: 10.1007/978-3-642-70227-3_2. [DOI] [PubMed] [Google Scholar]
  47. Wang J. C. DNA topoisomerases. Annu Rev Biochem. 1985;54:665–697. doi: 10.1146/annurev.bi.54.070185.003313. [DOI] [PubMed] [Google Scholar]
  48. Zhang H., Wang J. C., Liu L. F. Involvement of DNA topoisomerase I in transcription of human ribosomal RNA genes. Proc Natl Acad Sci U S A. 1988 Feb;85(4):1060–1064. doi: 10.1073/pnas.85.4.1060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. von Wettstein D., Rasmussen S. W., Holm P. B. The synaptonemal complex in genetic segregation. Annu Rev Genet. 1984;18:331–413. doi: 10.1146/annurev.ge.18.120184.001555. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES