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. 1981 Jun;78(6):3706–3710. doi: 10.1073/pnas.78.6.3706

Alterations in chromatin structure during early sea urchin embryogenesis.

A Savić, P Richman, P Williamson, D Poccia
PMCID: PMC319640  PMID: 6943576

Abstract

Sea urchin sperm before fertilization possess the longest nucleosome repeat length yet determined for any chromatin. By the time the fertilized egg gives rise to a blastula or gastrula embryo, the chromatin has a considerably shorter repeat length and, in addition, a sequence of different histone variants of H1, H2A, and H2B has appeared. We have investigated the relationship between these variations in histone composition and concomitant alterations in chromatin structure during the earliest stages of embryogenesis in two species of sea urchin. In contrast to the long repeat distance in sperm, chromatin loaded with cleavage stage histones has a much smaller repeat. Later stages containing predominantly alpha histones display an intermediate spacing. More detailed analysis of the events in the first cell cycle was carried out with polyspermically fertilized eggs. During the first 30 min after fertilization, in which sperm-specific H1 is completely replaced by cleavage-stage H1, the male pronuclear repeat remains unchanged. The decrease toward the repeat length of cleavage stages begins at about the time of DNA synthesis. Higher degrees of polyspermy extend the length of the cell cycle, including the duration of S phase and the length of time to reach the first chromosome condensation. At these higher degrees of polyspermy, the decrease in repeat length is also slowed. We conclude that the adjustment of the arrangement of nucleosomes in embryonic chromatin from that found in sperm can occur within the first cell cycle and that its timing is cell-cycle dependent. The adjustment is separable from a corresponding change in H1 composition.

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Selected References

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  1. Albanese I., Di Liegro I., Cognetti G. Unusual properties of sea urchin unfertilized egg chromatin. Cell Biol Int Rep. 1980 Feb;4(2):201–210. doi: 10.1016/0309-1651(80)90075-2. [DOI] [PubMed] [Google Scholar]
  2. Arceci R. J., Gross P. R. Histone variants and chromatin structure during sea urchin development. Dev Biol. 1980 Nov;80(1):186–209. doi: 10.1016/0012-1606(80)90508-4. [DOI] [PubMed] [Google Scholar]
  3. Carroll A. G., Ozaki H. Changes in the histones of the sea urchin Stronglylocentrotus purpuratus at fertilization. Exp Cell Res. 1979 Mar 15;119(2):307–315. doi: 10.1016/0014-4827(79)90358-6. [DOI] [PubMed] [Google Scholar]
  4. Cohen L. H., Newrock K. M., Zweidler A. Stage-specific switches in histone synthesis during embryogenesis of the sea urchin. Science. 1975 Dec 5;190(4218):994–997. doi: 10.1126/science.1237932. [DOI] [PubMed] [Google Scholar]
  5. Compton J. L., Bellard M., Chambon P. Biochemical evidence of variability in the DNA repeat length in the chromatin of higher eukaryotes. Proc Natl Acad Sci U S A. 1976 Dec;73(12):4382–4386. doi: 10.1073/pnas.73.12.4382. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Easton D., Chalkley R. High-resolution electrophoretic analysis of the histones from embryos and sperm of Arbacia punctulata. Exp Cell Res. 1972 Jun;72(2):502–508. doi: 10.1016/0014-4827(72)90020-1. [DOI] [PubMed] [Google Scholar]
  7. Felsenfeld G. Chromatin. Nature. 1978 Jan 12;271(5641):115–122. doi: 10.1038/271115a0. [DOI] [PubMed] [Google Scholar]
  8. Hill R. J., Poccia D. L., Doty P. Towards a total macromolecular analysis of sea urchin embryo chromatin. J Mol Biol. 1971 Oct 28;61(2):445–462. doi: 10.1016/0022-2836(71)90392-5. [DOI] [PubMed] [Google Scholar]
  9. Keichline L. D., Wassarman P. M. Developmental study of the structure of sea urchin embryo and sperm chromatin using micrococcal nuclease. Biochim Biophys Acta. 1977 Mar 2;475(1):139–151. doi: 10.1016/0005-2787(77)90348-3. [DOI] [PubMed] [Google Scholar]
  10. Keichline L. D., Wassarman P. M. Structure of chromatin in sea urchin embryos, sperm, and adult somatic cells. Biochemistry. 1979 Jan 9;18(1):214–219. doi: 10.1021/bi00568a033. [DOI] [PubMed] [Google Scholar]
  11. Kornberg R. D. Structure of chromatin. Annu Rev Biochem. 1977;46:931–954. doi: 10.1146/annurev.bi.46.070177.004435. [DOI] [PubMed] [Google Scholar]
  12. Laskey R. A., Mills A. D., Morris N. R. Assembly of SV40 chromatin in a cell-free system from Xenopus eggs. Cell. 1977 Feb;10(2):237–243. doi: 10.1016/0092-8674(77)90217-3. [DOI] [PubMed] [Google Scholar]
  13. Lilley D. M., Pardon J. F. Structure and function of chromatin. Annu Rev Genet. 1979;13:197–233. doi: 10.1146/annurev.ge.13.120179.001213. [DOI] [PubMed] [Google Scholar]
  14. Maller J., Poccia D., Nishioka D., Kidd P., Gerhart J., Hartman H. Spindle formation and cleavage in Xenopus eggs injected with centriole-containing fractions from sperm. Exp Cell Res. 1976 May;99(2):285–294. doi: 10.1016/0014-4827(76)90585-1. [DOI] [PubMed] [Google Scholar]
  15. Miki B. L., Neelin J. M. DNA repeat lengths of erythrocyte chromatins differing in content of histones H1 and H5. Nucleic Acids Res. 1980 Feb 11;8(3):529–542. doi: 10.1093/nar/8.3.529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Nelson T., Hsieh T. S., Brutlag D. Extracts of Drosophila embryos mediate chromatin assembly in vitro. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5510–5514. doi: 10.1073/pnas.76.11.5510. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Newrock K. M., Alfageme C. R., Nardi R. V., Cohen L. H. Histone changes during chromatin remodeling in embryogenesis. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 1):421–431. doi: 10.1101/sqb.1978.042.01.045. [DOI] [PubMed] [Google Scholar]
  18. Noll M. Differences and similarities in chromatin structure of Neurospora crassa and higher eucaryotes. Cell. 1976 Jul;8(3):349–355. doi: 10.1016/0092-8674(76)90146-x. [DOI] [PubMed] [Google Scholar]
  19. Noll M., Kornberg R. D. Action of micrococcal nuclease on chromatin and the location of histone H1. J Mol Biol. 1977 Jan 25;109(3):393–404. doi: 10.1016/s0022-2836(77)80019-3. [DOI] [PubMed] [Google Scholar]
  20. Poccia D. L., Hinegardner R. T. Developmental changes in chromatin proteins of the sea urchin from blastula to mature larva. Dev Biol. 1975 Jul;45(1):81–89. doi: 10.1016/0012-1606(75)90243-2. [DOI] [PubMed] [Google Scholar]
  21. Poccia D. L., LeVine D., Wang J. C. Activity of a DNA topoisomerase (nicking-closing enzyme) during sea urchin development and the cell cycle. Dev Biol. 1978 Jun;64(2):273–283. doi: 10.1016/0012-1606(78)90078-7. [DOI] [PubMed] [Google Scholar]
  22. Poccia D., Salik J., Krystal G. Transitions in histone variants of the male pronucleus following fertilization and evidence for a maternal store of cleavage-stage histones in the sera urchin egg. Dev Biol. 1981 Mar;82(2):287–296. doi: 10.1016/0012-1606(81)90452-8. [DOI] [PubMed] [Google Scholar]
  23. Prunell A., Kornberg R. D., Lutter L., Klug A., Levitt M., Crick F. H. Periodicity of deoxyribonuclease I digestion of chromatin. Science. 1979 May 25;204(4395):855–858. doi: 10.1126/science.441739. [DOI] [PubMed] [Google Scholar]
  24. Ruderman J. V., Gross P. R. Histones and histone synthesis in sea urchin development. Dev Biol. 1974 Feb;36(2):286–298. doi: 10.1016/0012-1606(74)90052-9. [DOI] [PubMed] [Google Scholar]
  25. Schlegel R. A., Haye K. R., Litwack A. H., Phelps B. M. Nucleosome repeat lengths in the definitive erythroid series of the adult chicken. Biochim Biophys Acta. 1980 Feb 29;606(2):316–330. doi: 10.1016/0005-2787(80)90041-6. [DOI] [PubMed] [Google Scholar]
  26. Spadafora C., Bellard M., Compton J. L., Chambon P. The DNA repeat lengths in chromatins from sea urchin sperm and gastrule cells are markedly different. FEBS Lett. 1976 Oct 15;69(1):281–285. doi: 10.1016/0014-5793(76)80704-1. [DOI] [PubMed] [Google Scholar]
  27. Varshavsky A. J., Bakayev V. V., Georgiev G. P. Heterogeneity of chromatin subunits in vitro and location of histone H1. Nucleic Acids Res. 1976 Feb;3(2):477–492. doi: 10.1093/nar/3.2.477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Weintraub H. The nucleosome repeat length increases during erythropoiesis in the chick. Nucleic Acids Res. 1978 Apr;5(4):1179–1188. doi: 10.1093/nar/5.4.1179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Whitlock J. P., Jr, Simpson R. T. Removal of histone H1 exposes a fifty base pair DNA segment between nucleosomes. Biochemistry. 1976 Jul 27;15(15):3307–3314. doi: 10.1021/bi00660a022. [DOI] [PubMed] [Google Scholar]

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