Skip to main content
SpringerLink
Log in

Phosphorylation of the histone H3.3 variant in mitosis and meiosis of the urochordate Oikopleura dioica

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

Mammalian histone variant H3.3 differs from replication-dependent histone H3.1 by five amino acids, including replacement of alanine 31 by serine. H3.3 is expressed throughout the cell cycle, primarily deposited at transcriptionally active loci independent of S-phase. Data from mammalian cells suggest that phosphorylation of serine 31 (H3.3S31P) plays a role in mitosis. Here we show that H3.3S31P also occurs during mitosis of the urochordate Oikopleura dioica, suggesting this histone modification and its function in mitosis is already present at the invertebrate–vertebrate transition. The spatial pattern differed from that of H3 phosphorylation at serine 28 (H3S28P). H3S28P was enriched near telomeric regions, but H3.3S31P differed both temporally and spatially from the mammalian pattern, being more widely distributed throughout prophase, prometaphase and metaphase chromosomes. We also identified an important role for H3.3S31P during oogenic meiosis in the semelparous O. dioica. H3.3S31P initiated together with H3S28P in all meiotic nuclei in late diplotene, after H3S10P. However, H3.3S31P was retained only on the subset of meiotic nuclei that seeded maturing oocytes and proceeded through meiosis to arrest in metaphase I. Thus, this epigenetic mark is part of a regulatory circuitry that enables O. dioica to numerically adjust oocyte production over two orders of magnitude.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ahmad K, Henikoff S (2002) The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 9: 1191-200.

    Article  CAS  PubMed  Google Scholar 

  • Ajiro K, Yasuda H, Tsuji H (1996) Vanadate triggers the transition from chromosome condensation to decondensation in a mitotic mutant (tsTM13) inactivation of p34cdc2/H1 kinase and dephosphorylation of mitosis-specific histone H3. Eur J Biochem 241: 923-30.

    Article  CAS  PubMed  Google Scholar 

  • Bosch A, Suau P (1995) Changes in core histone variant composition in differentiating neurons: the roles of differential turnover and synthesis rates. Eur J Cell Biol 68: 220-25.

    CAS  PubMed  Google Scholar 

  • Chadee DN, Hendzel MJ, Tylipski CP, Allis CD, Bazett-Jones DP, Wright JA, Davie JR (1999) Increased Ser-10 phosphorylation of histone H3 in mitogen-stimulated and oncogene-transformed mouse fibroblasts. J Biol Chem 274: 24914-4920.

    Article  CAS  PubMed  Google Scholar 

  • Chioda M, Eskeland R, Thompson EM (2002) Histone gene complement, variant expression, and mRNA processing in a urochordate Oikopleura dioica that undergoes extensive polyploidization. Mol Biol Evol 19: 2247-260.

    CAS  PubMed  Google Scholar 

  • Chioda M, Spada F, Eskeland R, Thompson EM (2004) Histone mRNAs do not accumulate during S phase of either mitotic or endoreduplicative cycles in the chordate Oikopleura dioica. Mol Cell Biol 24: 5391-403.

    Article  CAS  PubMed  Google Scholar 

  • Chow CM, Georgiou A, Szutorisz H et al. (2005) Variant histone H3.3 marks promoters of transcriptionally active genes during mammalian cell division. EMBO Rep 6: 354-60.

    Article  CAS  PubMed  Google Scholar 

  • Crosio C, Cermakian N, Allis CD, Sassone-Corsi P (2000) Light induces chromatin modification in cells of the mammalian circadian clock. Nat Neurosci 3: 1241-247.

    Article  CAS  PubMed  Google Scholar 

  • de la Barre AE, Gerson V, Gout S, Creaven M, Allis CD, Dimitrov S (2000) Core histone N-termini play an essential role in mitotic chromosome condensation. EMBO J 19: 379-91.

    Article  PubMed  Google Scholar 

  • Delsuc F, Brinkmann H, Chourrout D, Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439: 965-68.

    Article  CAS  PubMed  Google Scholar 

  • Dunn KL, Davie JR (2005) Stimulation of the Ras-MAPK pathway leads to independent phosphorylation of histone H3 on serine 10 and 28. Oncogene 24: 3492-502.

    Article  CAS  PubMed  Google Scholar 

  • Fischle W, Wang Y, Allis CD (2003) Binary switches and modification cassettes in histone biology and beyond. Nature 425: 475-79.

    Article  CAS  PubMed  Google Scholar 

  • Fischle W, Tseng BS, Dormann HL et al. (2005) Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature 438: 1116-122.

    Article  CAS  PubMed  Google Scholar 

  • Ganot P, Thompson EM (2002) Patterning through differential endoreduplication in epithelial organogenesis of the chordate, Oikopleura dioica. Dev Biol 252: 59-1.

    Article  CAS  PubMed  Google Scholar 

  • Ganot P, Bouquet JM, Thompson EM (2006a) Comparative organisation of follicle, accessory cells and spawning anlagen in dynamic semelparous clutch manipulators, the urochordate Oikopleuridae. Biol Cell 98: 389-01.

    Article  CAS  PubMed  Google Scholar 

  • Ganot P, Kallesøe T, Thompson EM (2006b) The cytoskeleton organizes germ nuclei with divergent fates and asynchronous cycles in a common cytoplasm during oogenesis in the chordate Oikopleura. Dev Biol, doi:10.1016/j.ydbio.2006.10.022.

  • Garcia BA, Barber CM, Hake SB et al. (2005) Modifications of human histone H3 variants during mitosis. Biochemistry 44: 13202-3213.

    Article  CAS  PubMed  Google Scholar 

  • Gernand D, Demidov D, Houben A (2003) The temporal and spatial pattern of histone H3 phosphorylation at serine 28 and serine 10 is similar in plants but differs between mono- and polycentric chromosomes. Cytogenet Genome Res 101: 172-76.

    Article  CAS  PubMed  Google Scholar 

  • Govin J, Caron C, Rousseaux S, Khochbin S (2005) Testis-specific histone H3 expression in somatic cells. Trends Biochem Sci 30: 357-59.

    Article  CAS  PubMed  Google Scholar 

  • Hake SB, Allis CD (2006) Histone H3 variants and their potential role in indexing mammalian genomes: The ‘H3 barcode hypothesis’ Proc Natl Acad Sci USA 103: 6428-435.

    Article  CAS  PubMed  Google Scholar 

  • Hake SB, Garcia BA, Kauer M et al. (2005) Serine 31 phosphorylation of histone variant H3.3 is specific to regions bordering centromeres in metaphase chromosomes. Proc Natl Acad Sci USA 102: 6344-349.

    Article  CAS  PubMed  Google Scholar 

  • Hake SB, Garcia BA, Duncan EM et al. (2006) Expression patterns and post-translational modifications associated with mammalian histone H3 variants. J Biol Chem 281: 559-68.

    Article  CAS  PubMed  Google Scholar 

  • Hans F, Dimitrov S (2001) Histone H3 phosphorylation and cell division. Oncogene 20: 3021-027.

    Article  CAS  PubMed  Google Scholar 

  • Hendzel MJ, Wei Y, Mancini MA et al. (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106: 348-60.

    Article  CAS  PubMed  Google Scholar 

  • Hsu JY, Sun ZW, Li X et al. (2000) Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/PP1 phosphatase in budding yeast and nematodes. Cell 102: 279-91.

    Article  CAS  PubMed  Google Scholar 

  • Ivanovska I, Khandan T, Ito T, Orr-Weaver TL (2005) A histone code in meiosis: the histone kinase, NHK-1, is required for proper chromosomal architecture in Drosophila oocytes. Genes Dev 19: 2571-582.

    Article  CAS  PubMed  Google Scholar 

  • Johnson L, Mollah S, Garcia BA et al. (2004) Mass spectrometry analysis of Arabidopsis histone H3 reveals distinct combinations of post-translational modifications. Nucleic Acids Res 32: 6511-518.

    Article  CAS  PubMed  Google Scholar 

  • Kaszas E, Cande WZ (2000) Phosphorylation of histone H3 is correlated with changes in the maintenance of sister chromatid cohesion during meiosis in maize, rather than the condensation of the chromatin. J Cell Sci 113: 3217-226.

    CAS  PubMed  Google Scholar 

  • Kimmins S, Sassone-Corsi P (2005) Chromatin remodelling and epigenetic features of germ cells. Nature 434: 583-89.

    Article  CAS  PubMed  Google Scholar 

  • Loppin B, Bonnefoy E, Anselme C, Laurencon A, Karr TL, Couble P (2005) The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature 437: 1386-390.

    Article  CAS  PubMed  Google Scholar 

  • Manzanero S, Arana P, Puertas MJ, Houben A (2000) The chromosomal distribution of phosphorylated histone H3 differs between plants and animals at meiosis. Chromosoma 109: 308-17.

    Article  CAS  PubMed  Google Scholar 

  • Margueron R, Trojer P, Reinberg D (2005) The key to development: interpreting the histone code? Curr Opin Genet Dev 15: 163-76.

    Article  CAS  PubMed  Google Scholar 

  • McKittrick E, Gafken PR, Ahmad K, Henikoff S (2004) Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc Natl Acad Sci USA 101: 1525-530.

    Article  CAS  PubMed  Google Scholar 

  • Mito Y, Henikoff JG, Henikoff S (2005) Genome-scale profiling of histone H3.3 replacement patterns. Nat Genet 37: 1090-097.

    Article  CAS  PubMed  Google Scholar 

  • Nowak SJ, Corces VG (2000) Phosphorylation of histone H3 correlates with transcriptionally active loci. Genes Dev 14: 3003-013.

    Article  CAS  PubMed  Google Scholar 

  • Prigent C, Dimitrov S (2003) Phosphorylation of serine 10 in histone H3, what for? J Cell Sci 116: 3677-685.

    Article  CAS  PubMed  Google Scholar 

  • Rice JC, Nishioka K, Sarma K, Steward R, Reinberg D, Allis CD (2002) Mitotic-specific methylation of histone H4 Lys 20 follows increased PR-Set7 expression and its localization to mitotic chromosomes. Genes Dev 16: 2225-230.

    Article  CAS  PubMed  Google Scholar 

  • Sarma K, Reinberg D (2005) Histone variants meet their match. Nat Rev Mol Cell Biol 6: 139-49.

    Article  CAS  PubMed  Google Scholar 

  • Spada F, Chioda M, Thompson EM (2005b) Histone H4 post-translational modifications in chordate mitotic and endoreduplicative cell cycles. J Cell Biochem 95: 885-01.

    Article  CAS  PubMed  Google Scholar 

  • Spada F, Vincent M, Thompson EM (2005a) Plasticity of histone modifications across the invertebrate to vertebrate transition: histone H3 lysine 4 trimethylation in heterochromatin. Chromosome Res 13: 57-2.

    Article  CAS  PubMed  Google Scholar 

  • Sullivan KF, Hechenberger M, Masri K (1994) Human CENP-A contains a histone H3 related histone fold domain that is required for targeting to the centromere. J Cell Biol 127: 581-92.

    Article  CAS  PubMed  Google Scholar 

  • Tagami H, Ray-Gallet D, Almouzni G, Nakatani Y (2004) Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116: 51-1.

    Article  CAS  PubMed  Google Scholar 

  • Torres-Padilla ME, Bannister AJ, Hurd PJ, Kouzarides T, Zernicka-Goetz M (2006) Dynamic distribution of the replacement histone variant H3.3 in the mouse oocyte and preimplantation embryos. Int J Dev Biol 50: 455-61.

    Article  CAS  PubMed  Google Scholar 

  • Troedsson C, Bouquet J-M, Aksnes DL, Thompson EM (2002) Resource allocation between somatic growth and reproductive output in the pelagic chordate, Oikopleura dioica, allows opportunistic response to nutritional variation. Mar Ecol Prog Ser 243: 83-1.

    Article  Google Scholar 

  • Wei Y, Mizzen CA, Cook RG, Gorovsky MA, Allis CD (1998) Phosphorylation of histone H3 at serine 10 is correlated with chromosome condensation during mitosis and meiosis in Tetrahymena. Proc Natl Acad Sci USA 95: 7480-484.

    Article  CAS  PubMed  Google Scholar 

  • Wei Y, Yu L, Bowen J, Gorovsky MA, Allis CD (1999) Phosphorylation of histone H3 is required for proper chromosome condensation and segregation. Cell 97: 99-09.

    Article  CAS  PubMed  Google Scholar 

  • Wirbelauer C, Bell O, Schubeler D (2005) Variant histone H3.3 is deposited at sites of nucleosomal displacement throughout transcribed genes while active histone modifications show a promoter-proximal bias. Genes Dev 19: 1761-766.

    Article  CAS  PubMed  Google Scholar 

  • Witt O, Albig W, Doenecke D (1996) Testis-specific expression of a novel human H3 histone gene. Exp Cell Res 229: 301-06.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Sars Centre for Marine Molecular Biology, Bergen High Technology Centre, University of Bergen, Thormøhlensgate 55, 5008, Bergen, Norway

    Alexandra Schulmeister, Martina Schmid & Eric M. Thompson

Authors
  1. Alexandra Schulmeister
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Martina Schmid
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eric M. Thompson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eric M. Thompson.

Electronic Supplementary Material

Below is the link to the electronic supplementary material

ESM 1

Supplementary Information (RTF 4,706 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schulmeister, A., Schmid, M. & Thompson, E.M. Phosphorylation of the histone H3.3 variant in mitosis and meiosis of the urochordate Oikopleura dioica . Chromosome Res 15, 189–201 (2007). https://doi.org/10.1007/s10577-006-1112-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-006-1112-z

Key words

Search

Navigation