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. 1994 Jul 19;91(15):7257–7261. doi: 10.1073/pnas.91.15.7257

The H1A histone variant is an in vivo repressor of oocyte-type 5S gene transcription in Xenopus laevis embryos.

H Kandolf 1
PMCID: PMC44378  PMID: 8041776

Abstract

Previous in vitro transcription studies have pointed to the importance of histone H1 for repression of oocyte-type 5S genes of Xenopus laevis. It has been previously reported that in development up to the early gastrula stage, Xenopus embryos contain a large pool of the maternal histone H1 variant H1M but are virtually devoid of histone H1A, H1B, and H1C proteins. At the early gastrula stage, there is an increase in H1A protein synthesis and H1A becomes the predominant H1 histone variant. Concomitant with the significant appearance of H1A protein in chromatin, oocyte 5S transcription is repressed. Here it is shown that there appears to be a direct link between H1A accumulation and inhibition of oocyte-type 5S RNA synthesis. Inhibition of H1A synthesis by a ribozyme targeted to H1A mRNA leads to the continued expression of oocyte 5S genes. H1A is proposed to inhibit major oocyte 5S gene transcription by sealing the nucleosome that is positioned over the major oocyte 5S coding sequences and by driving major oocyte 5S gene chromatin into a higher-order structure in which histone H1A molecules interact cooperatively.

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Selected References

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  1. Andrews M. T., Brown D. D. Transient activation of oocyte 5S RNA genes in Xenopus embryos by raising the level of the trans-acting factor TFIIIA. Cell. 1987 Nov 6;51(3):445–453. doi: 10.1016/0092-8674(87)90640-4. [DOI] [PubMed] [Google Scholar]
  2. Baldi M. I., Mattoccia E., Bufardeci E., Fabbri S., Tocchini-Valentini G. P. Participation of the intron in the reaction catalyzed by the Xenopus tRNA splicing endonuclease. Science. 1992 Mar 13;255(5050):1404–1408. doi: 10.1126/science.1542788. [DOI] [PubMed] [Google Scholar]
  3. Bouvet P., Dimitrov S., Wolffe A. P. Specific regulation of Xenopus chromosomal 5S rRNA gene transcription in vivo by histone H1. Genes Dev. 1994 May 15;8(10):1147–1159. doi: 10.1101/gad.8.10.1147. [DOI] [PubMed] [Google Scholar]
  4. Busby S. J., Reeder R. H. Fate of amplified nucleoli in Xenopus laevis embryos. Dev Biol. 1982 Jun;91(2):458–467. doi: 10.1016/0012-1606(82)90052-5. [DOI] [PubMed] [Google Scholar]
  5. Chipev C. C., Wolffe A. P. Chromosomal organization of Xenopus laevis oocyte and somatic 5S rRNA genes in vivo. Mol Cell Biol. 1992 Jan;12(1):45–55. doi: 10.1128/mcb.12.1.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cotten M., Birnstiel M. L. Ribozyme mediated destruction of RNA in vivo. EMBO J. 1989 Dec 1;8(12):3861–3866. doi: 10.1002/j.1460-2075.1989.tb08564.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dworkin-Rastl E., Kandolf H., Smith R. C. The maternal histone H1 variant, H1M (B4 protein), is the predominant H1 histone in Xenopus pregastrula embryos. Dev Biol. 1994 Feb;161(2):425–439. doi: 10.1006/dbio.1994.1042. [DOI] [PubMed] [Google Scholar]
  8. Flynn J. M., Woodland H. R. The synthesis of histone H1 during early amphibian development. Dev Biol. 1980 Mar;75(1):222–230. doi: 10.1016/0012-1606(80)90157-8. [DOI] [PubMed] [Google Scholar]
  9. Harper M. E., Price J., Korn L. J. Chromosomal mapping of Xenopus 5S genes: somatic-type versus oocyte-type. Nucleic Acids Res. 1983 Apr 25;11(8):2313–2323. doi: 10.1093/nar/11.8.2313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Haseloff J., Gerlach W. L. Simple RNA enzymes with new and highly specific endoribonuclease activities. Nature. 1988 Aug 18;334(6183):585–591. doi: 10.1038/334585a0. [DOI] [PubMed] [Google Scholar]
  11. Jerzmanowski A., Cole R. D. Flanking sequences of Xenopus 5 S RNA genes determine differential inhibition of transcription by H1 histone in vitro. Mitotic phosphorylation of H1 decreases its inhibitory power. J Biol Chem. 1990 Jun 25;265(18):10726–10732. [PubMed] [Google Scholar]
  12. Koizumi M., Iwai S., Ohtsuka E. Cleavage of specific sites of RNA by designed ribozymes. FEBS Lett. 1988 Nov 7;239(2):285–288. doi: 10.1016/0014-5793(88)80935-9. [DOI] [PubMed] [Google Scholar]
  13. Krieg P. A., Melton D. A. In vitro RNA synthesis with SP6 RNA polymerase. Methods Enzymol. 1987;155:397–415. doi: 10.1016/0076-6879(87)55027-3. [DOI] [PubMed] [Google Scholar]
  14. Lennard A. C., Thomas J. O. The arrangement of H5 molecules in extended and condensed chicken erythrocyte chromatin. EMBO J. 1985 Dec 16;4(13A):3455–3462. doi: 10.1002/j.1460-2075.1985.tb04104.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Perry M., Thomsen G. H., Roeder R. G. Genomic organization and nucleotide sequence of two distinct histone gene clusters from Xenopus laevis. Identification of novel conserved upstream sequence elements. J Mol Biol. 1985 Oct 5;185(3):479–499. doi: 10.1016/0022-2836(85)90065-8. [DOI] [PubMed] [Google Scholar]
  16. Schlissel M. S., Brown D. D. The transcriptional regulation of Xenopus 5s RNA genes in chromatin: the roles of active stable transcription complexes and histone H1. Cell. 1984 Jul;37(3):903–913. doi: 10.1016/0092-8674(84)90425-2. [DOI] [PubMed] [Google Scholar]
  17. Seidel C. W., Peck L. J. Kinetic control of 5 S RNA gene transcription. J Mol Biol. 1992 Oct 20;227(4):1009–1018. doi: 10.1016/0022-2836(92)90517-n. [DOI] [PubMed] [Google Scholar]
  18. Smith R. C., Dworkin-Rastl E., Dworkin M. B. Expression of a histone H1-like protein is restricted to early Xenopus development. Genes Dev. 1988 Oct;2(10):1284–1295. doi: 10.1101/gad.2.10.1284. [DOI] [PubMed] [Google Scholar]
  19. Stutz F., Gouilloud E., Clarkson S. G. Oocyte and somatic tyrosine tRNA genes in Xenopus laevis. Genes Dev. 1989 Aug;3(8):1190–1198. doi: 10.1101/gad.3.8.1190. [DOI] [PubMed] [Google Scholar]
  20. Swerdlow H., Guthrie C. Structure of intron-containing tRNA precursors. Analysis of solution conformation using chemical and enzymatic probes. J Biol Chem. 1984 Apr 25;259(8):5197–5207. [PubMed] [Google Scholar]
  21. Wakefield L., Gurdon J. B. Cytoplasmic regulation of 5S RNA genes in nuclear-transplant embryos. EMBO J. 1983;2(9):1613–1619. doi: 10.1002/j.1460-2075.1983.tb01632.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Wolffe A. P., Brown D. D. Developmental regulation of two 5S ribosomal RNA genes. Science. 1988 Sep 23;241(4873):1626–1632. doi: 10.1126/science.241.4873.1626. [DOI] [PubMed] [Google Scholar]
  23. Wolffe A. P., Brown D. D. Differential 5S RNA gene expression in vitro. Cell. 1987 Dec 4;51(5):733–740. doi: 10.1016/0092-8674(87)90096-1. [DOI] [PubMed] [Google Scholar]
  24. Wolffe A. P. Dominant and specific repression of Xenopus oocyte 5S RNA genes and satellite I DNA by histone H1. EMBO J. 1989 Feb;8(2):527–537. doi: 10.1002/j.1460-2075.1989.tb03407.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Wolffe A. P. Transcription fraction TFIIIC can regulate differential Xenopus 5S RNA gene transcription in vitro. EMBO J. 1988 Apr;7(4):1071–1079. doi: 10.1002/j.1460-2075.1988.tb02915.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Woolf T. M., Jennings C. G., Rebagliati M., Melton D. A. The stability, toxicity and effectiveness of unmodified and phosphorothioate antisense oligodeoxynucleotides in Xenopus oocytes and embryos. Nucleic Acids Res. 1990 Apr 11;18(7):1763–1769. doi: 10.1093/nar/18.7.1763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Woolf T. M., Melton D. A., Jennings C. G. Specificity of antisense oligonucleotides in vivo. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7305–7309. doi: 10.1073/pnas.89.16.7305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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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