Skip to main content
Advertisement

Main menu

  • Home
  • Articles
    • Accepted manuscripts
    • Issue in progress
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Sign up for alerts
  • About us
    • About Development
    • About the Node
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contacts
    • Subscriptions
    • Feedback
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

User menu

  • Log in
  • Log out

Search

  • Advanced search
Development
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

supporting biologistsinspiring biology

Development

  • Log in
Advanced search

RSS  Twitter  Facebook  YouTube 

  • Home
  • Articles
    • Accepted manuscripts
    • Issue in progress
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Sign up for alerts
  • About us
    • About Development
    • About the Node
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contacts
    • Subscriptions
    • Feedback
JOURNAL ARTICLES
Temporally restricted spatial localization of acetylated isoforms of histone H4 and RNA polymerase II in the 2-cell mouse embryo
D.M. Worrad, B.M. Turner, R.M. Schultz
Development 1995 121: 2949-2959;
D.M. Worrad
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
B.M. Turner
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
R.M. Schultz
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • Article
  • Info & metrics
  • PDF
Loading

Summary

Using immunofluorescent labeling and laser-scanning confocal microscopy, we show that isoforms of histone H4 acetylated on lysine 5, 8 and/or 12 (H4.Ac5-12), as well as RNA polymerase II, become enriched at the nuclear periphery around the time of zygotic gene activation, i.e., the 2-cell stage, in the preimplantation mouse embryo. In contrast, DNA and H4 acetylated on lysine 16 are uniformly distributed throughout the cytoplasm. Culture of embryos with inhibitors of histone deacetylase trichostatin A and trapoxin results in an increase in the (1) amount of acetylated histone H4 detected by immunoblotting, (2) intensity and sharpness of the peripheral staining for H4.Ac5-12, and (3) relative rate of synthesis of proteins that are markers for zygotic gene activation. The enhanced staining for H4.Ac5-12 at the nuclear periphery seems to require DNA replication, but appears independent of cytokinesis or transcription, since its development is inhibited by aphidicolin but not by either cytochalasin D or alpha-amanitin. Lastly, the restricted localization of H4.Ac 5–12 is not observed in the 4-cell embryo or at later stages of preimplantation development. These results suggest that changes in chromatin structure underlie, at least in part, zygotic gene activation in the mouse.

Reference

    1. Barnes F. L.,
    2. First N. L.
    (1991) Embryonic transcription in in vitro cultured bovine embryos. Mol. Reprod. Dev 29, 117–123
    OpenUrlCrossRefPubMedWeb of Science
    1. Bolton V. N.,
    2. Oades P. J.,
    3. Johnson M. H.
    (1984) The relationship between cleavage, DNA replication, and gene expression in the mouse 2-cell embryos. J. Embryol. Exp. Morph 79, 139–163
    OpenUrlPubMedWeb of Science
    1. Braunstein M.,
    2. Rose A. B.,
    3. Holmes S. G.,
    4. Allis C. D.,
    5. Broach J. R.
    (1993) Transcriptional silencing in yeast is associated with reduced nucleosome acetylation. Genes Dev 7, 592–604
    OpenUrlAbstract/FREE Full Text
    1. Candido E. P. M.,
    2. Reeves R.,
    3. Davie J. R.
    (1978) Sodium butyrate inhibits histone deacetylation in cultured cells. Cell 14, 105–113
    OpenUrlCrossRefPubMedWeb of Science
    1. Chatot C. L.,
    2. Ziomek C. A.,
    3. Bavister B. D.,
    4. Lewis J. L.,
    5. Torres I.
    (1989) An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro. J. Reprod. Fertil 86, 679–688
    OpenUrlAbstract/FREE Full Text
    1. Christians E.,
    2. Campion E.,
    3. Thompson E. M.,
    4. Renard J.-P.
    (1995) Expression of the HSP 70. 1 gene, a landmark of early zygotic gene activity in the mouse embryo, is restricted tot he first burst of transcription. Development 112, 113–122
    OpenUrl
    1. Ciemerych M. A.,
    2. Czolowska R.
    (1993) Differential chromatin condensation of female and male pronuclei in mouse zygotes. Mol. Reprod. Dev 34, 73–80
    OpenUrlCrossRefPubMed
    1. Conover J. C.,
    2. Temeles G. L.,
    3. Zimmermann J. W.,
    4. Burke B.,
    5. Schultz R. M.
    (1991) Stage-specific expression of a family of proteins that are major products of zygotic gene activation in the mouse embryo. Dev. Biol 144, 392–404
    OpenUrlCrossRefPubMedWeb of Science
    1. Erbach G. T.,
    2. Lawitts J. A.,
    3. Papaioannou V. E.,
    4. Biggers J. D.
    (1994) Differential growth of the mouse preimplantation embryo in chemically defined media. Biol. Reprod 50, 1027–1033
    OpenUrlAbstract
    1. Dimitrov S.,
    2. Almouzni G.,
    3. Dasso M.,
    4. Wolffe A. P.
    (1993) Chromatin transitions during early Xenopus embryogenesis: Changes in histone H4 acetylation and in linker histone type. Dev. Biol 160, 214–227
    OpenUrlCrossRefPubMedWeb of Science
    1. Felsenfeld G.
    (1992) Chromatin as an essential part of the transcriptional mechanism. Nature 355, 219–224
    OpenUrlCrossRefPubMed
    1. Hebbes T. R.,
    2. Thorne A. W.,
    3. Crane-Robinson C.
    (1988) A direct link between core histone acetylation and transcriptionally active chromatin. EMBO J 7, 1395–1402
    OpenUrlPubMedWeb of Science
    1. Hebbes T. R.,
    2. Thorne A. W.,
    3. Clayton A. L.,
    4. Crane-Robinson C.
    (1992) Histone acetylation and globin gene switching. Nuc. Acids Res 20, 1017–1022
    OpenUrlAbstract/FREE Full Text
    1. Hebbes T. R.,
    2. Clayton A. L.,
    3. Thorne A. W.,
    4. Crane-Robinson C.
    (1994) Core histone hyeracetylation co-maps with generalized DNase-I sensitivity in the chicken beta globin chromosomal domain. EMBO J 13, 1823–1830
    OpenUrlPubMedWeb of Science
    1. Jeppesen P.,
    2. Turner B. M.
    (1993) The inactive X chromosome in female mammals is distinguished by a lack of histone H4 acetylation, a cytogenetic marker for gene expression. Cell 74, 281–289
    OpenUrlCrossRefPubMedWeb of Science
    1. Johnson M. H.,
    2. Nasr-Esfahani M. H.
    (1994) Radical solutions and cultural problems: Could free oxygen radicals be responsible for the impaired development of preimplantation mammalian embryos in vitro?. BioEssays 16, 31–38
    OpenUrlCrossRefPubMedWeb of Science
    1. Kijima M.,
    2. Yoshida M.,
    3. Sugita K.,
    4. Horinouchi S.,
    5. Beppu T.
    (1993) Trapoxin, an antitumor cyclic tetrapeptide, is an irreversible inhibitor of mammalian histone deacetylase. J. Biol. Chem 268, 22429–22435
    OpenUrlAbstract/FREE Full Text
    1. Kruh J.
    (1982) Effects of sodium butyrate, a new pharmacological agent, on cells in culture. Mol. Cell. Biochem 42, 65–82
    OpenUrlCrossRefPubMedWeb of Science
    1. Laemmli U. K.
    (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685
    OpenUrlCrossRefPubMed
    1. Latham K. E.,
    2. Solter D.,
    3. Schultz R. M.
    (1992) Acquisition of a transcriptionally permissive state during the 1-cell stage of mouse embryogenesis. Dev. Biol 149, 457–462
    OpenUrlCrossRefPubMedWeb of Science
    1. Laybourn P. J.,
    2. Kadonaga J. T.
    (1991) Role of nucleosomal cores and histone H1 in regulation of transcription by RNA polymerase II. Science 254, 238–245
    OpenUrlAbstract/FREE Full Text
    1. Lee D. Y.,
    2. Hayes J. J.,
    3. Pruss D.,
    4. Wolffe A. P.
    (1993) A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell 72, 73–84
    OpenUrlCrossRefPubMedWeb of Science
    1. Lin R.,
    2. Leone J. W.,
    3. Cook R. G.,
    4. Allis C. D.
    (1989) Antibodies specific to acetylated histones document the existence of deposition-and transcription-related histone acetylation in Tetrahymena. J. Cell Biol 108, 1577–1588
    OpenUrlAbstract/FREE Full Text
    1. Lu H.,
    2. Zawel L.,
    3. Fisher L.,
    4. Egly J. M.,
    5. Reinberg D.
    (1992) Human general transcription factor IIH phosphorylates the C-terminal domain of RNA polymerase II. Nature 358, 641–645
    OpenUrlCrossRefPubMed
    1. Majumder S.,
    2. Miranda M.,
    3. DePamphilis M. L.
    (1993) Analysis of gene expression in mouse preimplantation embryos demonstrates that the primary role of enhancers is to relieve repression of promoters. EMBO J 12, 1131–1140
    OpenUrlPubMedWeb of Science
    1. Martínez-Salas E.,
    2. Linney E.,
    3. Hassall J.,
    4. DePamphilis M. L.
    (1989) The need for enhancers in gene expression first appears during mouse development with formation of the zygotic nucleus. Genes Dev 3, 1493–1506
    OpenUrlAbstract/FREE Full Text
    1. Matsumoto K.,
    2. Anzai M.,
    3. Nakagata N.,
    4. Takahashi A.,
    5. Takahashi Y.,
    6. Miyata K.
    (1994) Onset of paternal gene activation in early mouse embryos fertilized with transgenic mouse sperm. Mol. Reprod. Dev 39, 136–140
    OpenUrlCrossRefPubMedWeb of Science
    1. Nomura A.,
    2. Maruyama Y. K.,
    3. Yoneda M.
    (1991) Initiation of DNA replication cycle in fertilized eggs of the starfish, Asterina pectinifera. Dev. Biol 143, 289–296
    OpenUrlCrossRefPubMedWeb of Science
    1. Pavlok A.,
    2. Kopecny V.,
    3. Lucas-Hahn A.,
    4. Niemann H.
    (1993) Transcriptional activity and nuclear ultrastructure of 8-cell bovine embryos developed by in vitro maturation and fertilization of oocytes from different growth categories of antral follicles. Mol. Reprod. Dev 35, 233–243
    OpenUrlCrossRefPubMedWeb of Science
    1. Petzdolt U.
    (1984) Regulation of stage-specific gene expression during early mouse development: Effect of cytochalasin B and aphidicolin on stage-specific protein synthesis in mouse eggs. Cell Differ 15, 163–167
    OpenUrlCrossRefPubMed
    1. Poueymirou W. T.,
    2. Schultz R. M.
    (1987) Differential effects of activators of cAMP-dependent protein kinase and protein kinase C on cleavage of one-cell mouse embryos and protein synthesis and phosphorylation in one-and two-cell embryos. Dev. Biol 121, 489–498
    OpenUrlCrossRefPubMed
    1. Poueymirou W. T.,
    2. Schultz R. M.
    (1989) Regulation of mouse preimplantation development: Inhibition of synthesis of proteins in the two-cell embryo that require transcription by inhibitors of cAMP-dependent protein kinase. Dev. Biol 133, 588–599
    OpenUrlCrossRefPubMedWeb of Science
    1. Ram P. T.,
    2. Schultz R. M.
    (1993) Reporter gene expression in G2 of the 1-cell mouse embryo. Dev. Biol 156, 552–556
    OpenUrlCrossRefPubMedWeb of Science
    1. Schultz R. M.
    (1993) Regulation of zygotic gene activation in the mouse. BioEssays 15, 531–538
    OpenUrlCrossRefPubMedWeb of Science
    1. Serizawa H.,
    2. Conaway J. W.,
    3. Conaway R. C.
    (1994) An oligomeric form of the large subunit of transcription factor (TF) IIE activates phosphorylation of the RNA polymerase II carboxyl-terminal domain by TFIIH. J. Biol. Chem 269, 20750–20756
    OpenUrlAbstract/FREE Full Text
    1. Sobel R. E.,
    2. Cook R. G.,
    3. Perry C. A.,
    4. Annunziato A. T.,
    5. Allis C. D.
    (1995) Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc. Natl. Acad. Sci. USA 92, 1237–1241
    OpenUrlAbstract/FREE Full Text
    1. Telford N. A.,
    2. Watson A. J.,
    3. Schultz G. A.
    (1990) Transition from maternal to embryonic control in early mammalian development: A comparison of several species. Mol. Reprod. Dev 26, 90–100
    OpenUrlCrossRefPubMedWeb of Science
    1. Thorne A. W.,
    2. Kmiciek D.,
    3. Mitchelson K.,
    4. Sautiere P.,
    5. Crane-Robinson C.
    (1990) Patterns of histone acetylation. Eur. J. Biochem 193, 701–713
    OpenUrlPubMedWeb of Science
    1. Turner B. M.
    (1991) Histone acetylation and control of gene expression. J. Cell Sci 99, 13–20
    OpenUrlFREE Full Text
    1. Turner B. M.
    (1993) Decoding the nucleosome. Cell 75, 5–8
    OpenUrlCrossRefPubMedWeb of Science
    1. Turner B. M.,
    2. Fellows G.
    (1989) Specific antibodies reveal ordered and cell-cycle-related use of histone-H4 acetylation sites in mammalian cells. Eur. J. Biochem 179, 131–139
    OpenUrlPubMedWeb of Science
    1. Turner B. M.,
    2. O'Neill L. P.,
    3. Allan I. M.
    (1989) Histone H4 acetylation in human cells. Frequency of acetylation at different sites defined by immunolabeling with site-specific antibodies. FEBS Lett 253, 141–145
    OpenUrlCrossRefPubMedWeb of Science
    1. Vernet M.,
    2. Bonnerot C.,
    3. Briand P.,
    4. Nicolas J.-F.
    (1992) Changes in permissiveness for the expression of microinjected DNA during the first cleavage of mouse embryos. Mech. Dev 36, 129–139
    OpenUrlCrossRefPubMed
    1. Vernet M.,
    2. Cavard C.,
    3. Zider A.,
    4. Fergelot P.,
    5. Grimber G.,
    6. Briand P.
    (1993) In vitro manipulation of early mouse embryos induces HIV1-LTRlacZ transgene expression. Development 119, 1293–1300
    OpenUrlAbstract
    1. Wiekowski M.,
    2. Miranda M.,
    3. DePamphilis M. L.
    (1991) Regulation of gene expression in preimplantation mouse embryos: Effects of the zygotic clock and the first mitosis on promoter and enhancer activities. Dev. Biol 147, 403–414
    OpenUrlCrossRefPubMedWeb of Science
    1. Wiekowski M.,
    2. Miranda M.,
    3. DePamphilis M. L.
    (1993) Requirements for promoter activity in mouse oocytes and embryos distinguish paternal pronuclei from maternal and zygotic nuclei. Dev. Biol 159, 366–378
    OpenUrlCrossRefPubMedWeb of Science
    1. Wolffe A. P.
    (1991) Implications of DNA replication for eukaryotic gene expression. J. Cell Sci 99, 201–206
    OpenUrlAbstract/FREE Full Text
    1. Wolffe A. P.
    (1994) The transcription of chromatin templates. Curr. Opinion Gen. Dev 4, 245–254
    OpenUrlCrossRefPubMed
    1. Wolffe A. P.,
    2. Dimitrov S.
    (1993) Histone-modulated gene activity: Developmental implications. Crit. Rev. Euk. Gene Exp 3, 167–191
    OpenUrlPubMed
    1. Worrad D. M.,
    2. Ram P. T.,
    3. Schultz R. M.
    (1994) Regulation of gene expression in the mouse oocyte and early preimplantation embryo: Developmental changes in Sp1 and TATA box-binding protein, TBP. Development 120, 2347–2357
    OpenUrlAbstract
    1. Yoshida M.,
    2. Kijima M.,
    3. Akita M.,
    4. Beppu T.
    (1990) Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A. J. Biol. Chem 265, 17174–17179
    OpenUrlAbstract/FREE Full Text
Previous ArticleNext Article
Back to top
Previous ArticleNext Article

This Issue

 Download PDF

Email

Thank you for your interest in spreading the word on Development.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Temporally restricted spatial localization of acetylated isoforms of histone H4 and RNA polymerase II in the 2-cell mouse embryo
(Your Name) has sent you a message from Development
(Your Name) thought you would like to see the Development web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
JOURNAL ARTICLES
Temporally restricted spatial localization of acetylated isoforms of histone H4 and RNA polymerase II in the 2-cell mouse embryo
D.M. Worrad, B.M. Turner, R.M. Schultz
Development 1995 121: 2949-2959;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
JOURNAL ARTICLES
Temporally restricted spatial localization of acetylated isoforms of histone H4 and RNA polymerase II in the 2-cell mouse embryo
D.M. Worrad, B.M. Turner, R.M. Schultz
Development 1995 121: 2949-2959;

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Alerts

Please log in to add an alert for this article.

Sign in to email alerts with your email address

Article navigation

  • Top
  • Article
  • Info & metrics
  • PDF

Related articles

Cited by...

More in this TOC section

  • Drosophila puckered regulates Fos/Jun levels during follicle cell morphogenesis
  • A BAC transgenic analysis of the Mrf4/Myf5 locus reveals interdigitated elements that control activation and maintenance of gene expression during muscle development
  • Visualization and functional characterization of the developing murine cardiac conduction system
Show more JOURNAL ARTICLES

Similar articles

Other journals from The Company of Biologists

Journal of Cell Science

Journal of Experimental Biology

Disease Models & Mechanisms

Biology Open

Advertisement

Kathryn Virginia Anderson (1952-2020)

Developmental geneticist Kathryn Anderson passed away at home on 30 November 2020. Tamara Caspary, a former postdoc and friend, remembers Kathryn and her remarkable contribution to developmental biology.


Zooming into 2021

In a new Editorial, Editor-in-Chief James Briscoe and Executive Editor Katherine Brown reflect on the triumphs and tribulations of the last 12 months, and look towards a hopefully calmer and more predictable year.


Read & Publish participation extends worldwide

Over 60 institutions in 12 countries are now participating in our Read & Publish initiative. Here, James Briscoe explains what this means for his institution, The Francis Crick Institute. Find out more and view our full list of participating institutions.


Upcoming special issues

Imaging Development, Stem Cells and Regeneration
Submission deadline: 30 March 2021
Publication: mid-2021

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

Both special issues welcome Review articles as well as Research articles, and will be widely promoted online and at key global conferences.


Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Sign up to join our next session:

10 February
Time: 13:00 (GMT)
Chaired by: preLights

Articles

  • Accepted manuscripts
  • Issue in progress
  • Latest complete issue
  • Issue archive
  • Archive by article type
  • Special issues
  • Subject collections
  • Sign up for alerts

About us

  • About Development
  • About the Node
  • Editors and board
  • Editor biographies
  • Travelling Fellowships
  • Grants and funding
  • Journal Meetings
  • Workshops
  • The Company of Biologists

For authors

  • Submit a manuscript
  • Aims and scope
  • Presubmission enquiries
  • Article types
  • Manuscript preparation
  • Cover suggestions
  • Editorial process
  • Promoting your paper
  • Open Access
  • Biology Open transfer

Journal info

  • Journal policies
  • Rights and permissions
  • Media policies
  • Reviewer guide
  • Sign up for alerts

Contact

  • Contact Development
  • Subscriptions
  • Advertising
  • Feedback

 Twitter   YouTube   LinkedIn

© 2021   The Company of Biologists Ltd   Registered Charity 277992