Location of Repository

Stage-specific histone modification profiles reveal global transitions in the Xenopus embryonic epigenome.

By Tobias D. Schneider, Jose M. Arteaga-Salas, Edith Mentele, Robert David, Dario Nicetto, Axel Imhof and Ralph A. W. Rupp

Abstract

Vertebrate embryos are derived from a transitory pool of pluripotent cells. By the process of embryonic induction, these precursor cells are assigned to specific fates and differentiation programs. Histone post-translational modifications are thought to play a key role in the establishment and maintenance of stable gene expression patterns underlying these processes. While on gene level histone modifications are known to change during differentiation, very little is known about the quantitative fluctuations in bulk histone modifications during development. To investigate this issue we analysed histones isolated from four different developmental stages of Xenopus laevis by mass spectrometry. In toto, we quantified 59 modification states on core histones H3 and H4 from blastula to tadpole stages. During this developmental period, we observed in general an increase in the unmodified states, and a shift from histone modifications associated with transcriptional activity to transcriptionally repressive histone marks. We also compared these naturally occurring patterns with the histone modifications of murine ES cells, detecting large differences in the methylation patterns of histone H3 lysines 27 and 36 between pluripotent ES cells and pluripotent cells from Xenopus blastulae. By combining all detected modification transitions we could cluster their patterns according to their embryonic origin, defining specific histone modification profiles (HMPs) for each developmental stage. To our knowledge, this data set represents the first compendium of covalent histone modifications and their quantitative flux during normogenesis in a vertebrate model organism. The HMPs indicate a stepwise maturation of the embryonic epigenome, which may be causal to the progressing restriction of cellular potency during development.

Topics: Medizin, ddc:610
Publisher: Ludwig-Maximilians-Universität München
Year: 2011
DOI identifier: 10.1371/journal.pone.0022548
OAI identifier: oai:epub.ub.uni-muenchen.de:15221
Provided by: Open Access LMU

Suggested articles

Preview

Citations

  1. (2009). Stability of histone modifications across mammalian genomes: implications for ‘epigenetic’ marking.
  2. (2005). Formation of an active tissue-specific chromatin domain initiated by epigenetic marking at the embryonic stem cell stage.
  3. (2006). A bivalent chromatin structure marks key developmental genes in embryonic stem cells.
  4. (2006). Chromatin signatures of pluripotent cell lines.
  5. (2005). Nuclear reorganisation of the Hoxb complex during mouse embryonic development.
  6. (2007). Human ES cell profiling broadens the reach of bivalent domains.
  7. (2008). Chromatin dynamics during epigenetic reprogramming in the mouse germ line.
  8. (2009). Distinctive chromatin in human sperm packages genes for embryo development.
  9. (2011). Genes for embryo development are packaged in blocks of multivalent chromatin in zebrafish sperm.
  10. (2009). Epigenetic dynamics of stem cells and cell lineage commitment: digging Waddington’s canal. Nature reviews Molecular cell biology 10:
  11. (2011). Control of the embryonic stem cell state.
  12. (2007). Genetic and epigenetic regulators of pluripotency.
  13. (2007). A chromatin landmark and transcription initiation at most promoters in human cells.
  14. (2006). Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells.
  15. (2007). Global epiproteomic signatures distinguish embryonic stem cells from differentiated cells.
  16. (2008). Mass spectrometry identifies and quantifies 74 unique histone H4 isoforms in differentiating human embryonic stem cells.
  17. (2008). Dissecting direct reprogramming through integrative genomic analysis.
  18. (2010). Histone H3 lysine 27 methylation asymmetry on developmentally-regulated promoters distinguish the first two lineages in mouse preimplantation embryos.
  19. (2010). Distinct histone modifications in stem cell lines and tissue lineages from the early mouse embryo.
  20. (2009). Analysis of histones in Xenopus laevis. I. A distinct index of enriched variants and modifications exists in each cell type and is remodeled during developmental transitions.
  21. (2009). Analysis of histones in Xenopus laevis. II. mass spectrometry reveals an index of cell type-specific modifications on H3 and H4.
  22. (2009). A hierarchy of H3K4me3 and H3K27me3 acquisition in spatial gene regulation in Xenopus embryos.
  23. (2010). Chromatin signature of embryonic pluripotency is established during genome activation.
  24. (2006). Enhanced histone acetylation and transcription: a dynamic perspective.
  25. (1967). Normal table of Xenopus laevis (Daudin).
  26. (1987). Vegetal pole cells and commitment to form endoderm in Xenopus laevis.
  27. (1987). Changes in states of commitment of single animal pole blastomeres of Xenopus laevis.
  28. (2009). Spemann’s organizer and the self-regulation of embryonic fields.
  29. (2006). Patterning the early Xenopus embryo.
  30. (2009). Bicaudal C, a novel regulator of Dvl signaling abutting RNA-processing bodies, controls cilia orientation and leftward flow.
  31. (2008). MesP1 drives vertebrate cardiovascular differentiation through Dkk-1-mediated blockade of Wnt-signalling.
  32. (2007). Shilatifard A
  33. (2007). Chromatin modifications and their function.
  34. (2010). Imhof A
  35. (2006). PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state.
  36. (2005). hMOF histone acetyltransferase is required for histone H4 lysine 16 acetylation in mammalian cells.
  37. (1989). Worcel A
  38. (1995). Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4.
  39. (2002). Histone acetylation and deacetylation: identification of acetylation and methylation sites of HeLa histone H4 by mass spectrometry.
  40. (2009). CBPmediated acetylation of histone H3 lysine 27 antagonizes Drosophila Polycomb silencing.
  41. (2010). Histone H3K27ac separates active from poised enhancers and predicts developmental state.
  42. (2010). Replication stress interferes with histone recycling and predeposition marking of new histones.
  43. (2008). Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly.
  44. (2009). Histone h3 lysine 56 acetylation is linked to the core transcriptional network in human embryonic stem cells.
  45. (2009). CBP/p300-mediated acetylation of histone H3 on lysine 56.
  46. (2007). Organismal differences in post-translational modifications in histones H3 and H4.
  47. (2007). Highresolution profiling of histone methylations in the human genome.
  48. (2009). Genome-wide views of chromatin structure.
  49. (2008). Transcriptioncoupled methylation of histone H3 at lysine 36 regulates dosage compensation by enhancing recruitment of the MSL complex in Drosophila melanogaster.
  50. (2009). H3K27me3 forms BLOCs over silent genes and intergenic regions and specifies a histone banding pattern on a mouse autosomal chromosome.
  51. (2006). Histone H3 variants and their potential role in indexing mammalian genomes: the "H3 barcode hypothesis".
  52. (2010). Quantitative mass spectrometry of histones
  53. (2011). Less label, more free: approaches in label-free quantitative mass spectrometry.
  54. (1993). Dynamic methylation of alfalfa histone H3.
  55. (2009). Drosophila stem cells share a common requirement for the histone H2B ubiquitin protease scrawny.
  56. (2006). Mass spectrometric characterization of human histone H3: a bird’s eye view.
  57. (2007). Genomewide maps of chromatin state in pluripotent and lineage-committed cells.
  58. (2007). The mammalian epigenome.
  59. (2010). Epigenetic Modifications in pluripotent and differentiated cells.
  60. (2010). Characterization of an antagonistic switch between histone H3 lysine 27 methylation and acetylation in the transcriptional regulation of Polycomb group target genes.
  61. (2009). Characterization of the expression pattern of the PRC2 core subunit Suz12 during embryonic development of Xenopus laevis.
  62. (2007). H3K27 demethylases, at long last.
  63. (2008). Smith A
  64. (2004). Refinement of gene expression patterns in the early Xenopus embryo.
  65. (1991). Ubiquitous MyoD transcription at the midblastula transition precedes induction-dependent MyoD expression in presumptive mesoderm of X. laevis.
  66. (2005). Establishment of mesodermal gene expression patterns in early Xenopus embryos: the role of repression.
  67. (1969). Mass culture of amphibian cells: methods and observations concerning stability of cell type.
  68. (1973). Establishment of a cell line (XTC-2) from the South African clawed toad, Xenopus laevis.
  69. (1989). Molecular Cloning: A Laboratory Manual:
  70. (2008). A chromatin-wide transition to H4K20 monomethylation impairs genome integrity and programmed DNA rearrangements in the mouse.

To submit an update or takedown request for this paper, please submit an Update/Correction/Removal Request.