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. 1984 Apr;81(8):2411–2415. doi: 10.1073/pnas.81.8.2411

Temporal expression of late histone messenger RNA in the sea urchin Lytechinus pictus.

J A Knowles, G J Childs
PMCID: PMC345070  PMID: 6585806

Abstract

Sea urchin histones are encoded by several multigene families. The temporal expression of one of these families, the late histones, has been studied during the early development of Lytechinus pictus. Using a nuclease S1 assay, we detected about 10,000 transcripts encoding both late H3 and H4 proteins in the unfertilized egg. This suggests that the late genes were active at some point during oogenesis. The number of late gene transcripts begins to increase 6.5 hr after fertilization (64-cell stage), indicating that these genes probably become reactivated 4.5-6.5 hr after fertilization. The maximum rate of accumulation of transcripts (4600 molecules per min per embryo) occurs 9-14 hr after fertilization (from blastula stage to hatching). The number of transcripts peaks 21 hr after fertilization (onset of gastrulation) when the embryo has accumulated 1.8 X 10(6) copies of each late mRNA (a 164-fold increase). A 5.5-fold increase in the relative rate of transcription, between 7 and 15 hr after fertilization, is partly responsible for the accumulation of these gene products. The relative synthesis of early histone message, which is encoded by a different family, decreases 18-fold during this time. Synthesis of the late transcripts continues at the higher rate after accumulation has ceased (24 hr after fertilization). The number of late transcripts begins to decrease 48 hr after fertilization, reaching about 10,000 copies at 72 hr.

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Selected References

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

  1. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  2. Bédard P. A., Brandhorst B. P. Patterns of protein synthesis and metabolism during sea urchin embryogenesis. Dev Biol. 1983 Mar;96(1):74–83. doi: 10.1016/0012-1606(83)90312-3. [DOI] [PubMed] [Google Scholar]
  3. Childs G., Levy S., Kedes L. H. Rapid purification of biologically active individual histone messenger RNAs by hybridization to cloned DNA linked to cellulose. Biochemistry. 1979 Jan 9;18(1):208–213. doi: 10.1021/bi00568a032. [DOI] [PubMed] [Google Scholar]
  4. Childs G., Maxson R., Kedes L. H. Histone gene expression during sea urchin embryogenesis: isolation and characterization of early and late messenger RNAs of Strongylocentrotus purpuratus by gene-specific hybridization and template activity. Dev Biol. 1979 Nov;73(1):153–173. doi: 10.1016/0012-1606(79)90144-1. [DOI] [PubMed] [Google Scholar]
  5. Childs G., Nocente-McGrath C., Lieber T., Holt C., Knowles J. A. Sea urchin (lytechinus pictus) late-stage histone H3 and H4 genes: characterization and mapping of a clustered but nontandemly linked multigene family. Cell. 1982 Dec;31(2 Pt 1):383–393. doi: 10.1016/0092-8674(82)90132-5. [DOI] [PubMed] [Google Scholar]
  6. Cohn R. H., Kedes L. H. Nonallelic histone gene clusters of individual sea urchins (Lytechinus pictus): mapping of homologies in coding and spacer DNA. Cell. 1979 Nov;18(3):855–864. doi: 10.1016/0092-8674(79)90137-5. [DOI] [PubMed] [Google Scholar]
  7. Cohn R. H., Kedes L. H. Nonallelic histone gene clusters of individual sea urchins (Lytechinus pictus): polarity and gene organization. Cell. 1979 Nov;18(3):843–853. doi: 10.1016/0092-8674(79)90136-3. [DOI] [PubMed] [Google Scholar]
  8. Cohn R. H., Lowry J. C., Kedes L. H. Histone genes of the sea urchin (S. purpuratus) cloned in E coli: order, polarity, and strandedness of the five histone-coding and spacer regions. Cell. 1976 Sep;9(1):147–161. doi: 10.1016/0092-8674(76)90060-x. [DOI] [PubMed] [Google Scholar]
  9. Davidson E. H., Hough-Evans B. R., Britten R. J. Molecular biology of the sea urchin embryo. Science. 1982 Jul 2;217(4554):17–26. doi: 10.1126/science.6178156. [DOI] [PubMed] [Google Scholar]
  10. DeLeon D. V., Cox K. H., Angerer L. M., Angerer R. C. Most early-variant histone mRNA is contained in the pronucleus of sea urchin eggs. Dev Biol. 1983 Nov;100(1):197–206. doi: 10.1016/0012-1606(83)90211-7. [DOI] [PubMed] [Google Scholar]
  11. Galau G. A., Klein W. H., Davis M. M., Wold B. J., Britten R. J., Davidson E. H. Structural gene sets active in embryos and adult tissues of the sea urchin. Cell. 1976 Apr;7(4):487–505. doi: 10.1016/0092-8674(76)90200-2. [DOI] [PubMed] [Google Scholar]
  12. Grunstein M. Hatching in the sea urchin Lytechinus pictus is accompanied by a shift in histone H4 gene activity. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4135–4139. doi: 10.1073/pnas.75.9.4135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Grunstein M., Schedl P. Isolation and sequence analysis of sea urchin (Lytechinus pictus) histone H4 messenger RNA. J Mol Biol. 1976 Jun 25;104(2):323–349. doi: 10.1016/0022-2836(76)90275-8. [DOI] [PubMed] [Google Scholar]
  14. Grunstein M., Schedl P., Kedes L. Sequence analysis and evolution of sea urchin (Lytechinus pictus and Strongylocentrotus purpuratus) histone H4 messenger RNAs. J Mol Biol. 1976 Jun 25;104(2):351–369. doi: 10.1016/0022-2836(76)90276-x. [DOI] [PubMed] [Google Scholar]
  15. Hentschel C. C., Birnstiel M. L. The organization and expression of histone gene families. Cell. 1981 Aug;25(2):301–313. doi: 10.1016/0092-8674(81)90048-9. [DOI] [PubMed] [Google Scholar]
  16. Hieter P. A., Hendricks M. B., Hemminki K., Weinberg E. S. Histone gene switch in the sea urchin embryo. Identification of late embryonic histone messenger ribonucleic acids and the control of their synthesis. Biochemistry. 1979 Jun 26;18(13):2707–2716. doi: 10.1021/bi00580a004. [DOI] [PubMed] [Google Scholar]
  17. Hofer E., Darnell J. E., Jr The primary transcription unit of the mouse beta-major globin gene. Cell. 1981 Feb;23(2):585–593. doi: 10.1016/0092-8674(81)90154-9. [DOI] [PubMed] [Google Scholar]
  18. Kafatos F. C., Jones C. W., Efstratiadis A. Determination of nucleic acid sequence homologies and relative concentrations by a dot hybridization procedure. Nucleic Acids Res. 1979 Nov 24;7(6):1541–1552. doi: 10.1093/nar/7.6.1541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kedes L. H. Histone genes and histone messengers. Annu Rev Biochem. 1979;48:837–870. doi: 10.1146/annurev.bi.48.070179.004201. [DOI] [PubMed] [Google Scholar]
  20. Levy S., Childs G., Kedes L. Sea urchin nuclei use RNA polymerase II to transcribe discrete histone RNAs larger than messengers. Cell. 1978 Sep;15(1):151–162. doi: 10.1016/0092-8674(78)90091-0. [DOI] [PubMed] [Google Scholar]
  21. Maniatis T., Jeffrey A., van deSande H. Chain length determination of small double- and single-stranded DNA molecules by polyacrylamide gel electrophoresis. Biochemistry. 1975 Aug 26;14(17):3787–3794. doi: 10.1021/bi00688a010. [DOI] [PubMed] [Google Scholar]
  22. Mauron A., Kedes L., Hough-Evans B. R., Davidson E. H. Accumulation of individual histone mRNAs during embryogenesis of the sea urchin Strongylocentrotus purpuratus. Dev Biol. 1982 Dec;94(2):425–434. doi: 10.1016/0012-1606(82)90359-1. [DOI] [PubMed] [Google Scholar]
  23. Maxson R. E., Jr, Wilt F. H. Accumulation of the early histone messenger RNAs during the development of Strongylocentrotus purpuratus. Dev Biol. 1982 Dec;94(2):435–440. doi: 10.1016/0012-1606(82)90360-8. [DOI] [PubMed] [Google Scholar]
  24. Maxson R. E., Jr, Wilt F. H. The rate of synthesis of histone mRNA during the development of sea urchin embryos (Strongylocentrotus purpuratus). Dev Biol. 1981 Apr 30;83(2):380–386. doi: 10.1016/0012-1606(81)90485-1. [DOI] [PubMed] [Google Scholar]
  25. Maxson R., Mohun T., Gormezano G., Childs G., Kedes L. Distinct organizations and patterns of expression of early and late histone gene sets in the sea urchin. Nature. 1983 Jan 13;301(5896):120–125. doi: 10.1038/301120a0. [DOI] [PubMed] [Google Scholar]
  26. Newrock K. M., Cohen L. H., Hendricks M. B., Donnelly R. J., Weinberg E. S. Stage-specific mRNAs coding for subtypes of H2A and H2B histones in the sea urchin embryo. Cell. 1978 Jun;14(2):327–336. doi: 10.1016/0092-8674(78)90118-6. [DOI] [PubMed] [Google Scholar]
  27. Schaffner W., Gross K., Telford J., Birnstiel M. Molecular analysis of the histone gene cluster of psammechinus miliaris: II. The arrangement of the five histone-coding and spacer sequences. Cell. 1976 Aug;8(4):471–478. doi: 10.1016/0092-8674(76)90214-2. [DOI] [PubMed] [Google Scholar]
  28. Weinberg E. S., Hendricks M. B., Hemminki K., Kuwabara P. E., Farrelly L. A. Timing and rates of synthesis of early histone mRNA in the embryo of Strongylocentrotus purpuratus. Dev Biol. 1983 Jul;98(1):117–129. doi: 10.1016/0012-1606(83)90340-8. [DOI] [PubMed] [Google Scholar]
  29. Wormington W. M., Brown D. D. Onset of 5 S RNA gene regulation during Xenopus embryogenesis. Dev Biol. 1983 Sep;99(1):248–257. doi: 10.1016/0012-1606(83)90273-7. [DOI] [PubMed] [Google Scholar]

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