CoChat
Sign Up
Cited by 39

The DOI matches its Crossref record; 3 of the 3 references it cites were found in a registry or an index.

KDM4B-mediated reduction of H3K9me3 and H3K36me3 levels improves somatic cell reprogramming into pluripotency

Wei, Jingwei, Antony, Jisha, Meng, Fanli, MacLean, Paul, Rhind, Rebekah, Laible, Götz, Oback, Björn·2017·Scientific Reports
DOI 10.1038/s41598-017-06569-2PMC PMC5548918
Open this paper in CoChat — free account

Abstract

Correct reprogramming of epigenetic marks is essential for somatic cells to regain pluripotency. Repressive histone (H) lysine (K) methylation marks are known to be stable and difficult to reprogram. In this study, we generated transgenic mice and mouse embryonic fibroblasts (MEFs) for the inducible expression of KDM4B, a demethylase that removes H3 K9 and H3K36 trimethylation (me3) marks (H3K9/36me3). Upon inducing Kdm4b, H3K9/36me3 levels significantly decreased compared to non-induced controls. Concurrently, H3K9me1 levels significantly increased, while H3K9me2 and H3K27me3 remained unchanged. The global transcriptional impact of Kdm4b-mediated reduction in H3K9/36me3 levels was examined by comparative microarray analysis and mRNA-sequencing of three independent transgenic MEF lines. We identified several commonly up-regulated targets, including the heterochromatin-associated zinc finger protein 37 and full-length endogenous retrovirus repeat elements. Following optimized zona-free somatic nuclear transfer, reduced H3K9/36me3 levels were restored within hours. Nevertheless, hypo-methylated Kdm4b MEF donors reprogrammed six-fold better into cloned blastocysts than non-induced donors. They also reprogrammed nine-fold better into induced pluripotent stem cells that gave rise to teratomas and chimeras. In summary, we firmly established H3K9/36me3 as a major roadblock to somatic cell reprogramming and identified transcriptional targets of derestricted chromatin that could contribute towards improving this process in mouse.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41598-017-06569-2

Cites

3 of 3 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 63

  1. Morgan, H. D., Santos, F., Green, K., Dean, W. & Reik, W. Epigenetic reprogramming in mammals. Hum Mol Genet 14(Spec No. 1), R47–58 (2005). · DOI
  2. Puschendorf, M. et al. PRC1 and Suv39h specify parental asymmetry at constitutive heterochromatin in early mouse embryos. Nature genetics 40, 411–420 (2008). · DOI
  3. Santos, F., Peters, A. H., Otte, A. P., Reik, W. & Dean, W. Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Dev Biol 280, 225–236 (2005). · DOI
  4. Torres-Padilla, M. E., Parfitt, D. E., Kouzarides, T. & Zernicka-Goetz, M. Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 445, 214–218 (2007). · DOI
  5. Martello, G. & Smith, A. The nature of embryonic stem cells. Annu Rev Cell Dev Biol 30, 647–675, doi:10.1146/annurev-cellbio-100913-013116 (2014). · DOI
  6. Yamanaka, S. & Blau, H. M. Nuclear reprogramming to a pluripotent state by three approaches. Nature 465, 704–712, doi:10.1038/nature09229 (2010). · DOI
  7. Okita, K., Ichisaka, T. & Yamanaka, S. Generation of germline-competent induced pluripotent stem cells. Nature 448, 313–317 (2007). · DOI
  8. Kang, Y. K. et al. Limited demethylation leaves mosaic-type methylation states in cloned bovine pre-implantation embryos. The EMBO journal 21, 1092–1100 (2002). · DOI
  9. Santos, F. et al. Epigenetic marking correlates with developmental potential in cloned bovine preimplantation embryos. Curr Biol 13, 1116–1121 (2003). · DOI
  10. Fukuda, A. et al. Identification of inappropriately reprogrammed genes by large-scale transcriptome analysis of individual cloned mouse blastocysts. PLoS ONE 5, e11274, doi:10.1371/journal.pone.0011274 (2010). · DOI
  11. Ogura, A., Inoue, K. & Wakayama, T. Recent advancements in cloning by somatic cell nuclear transfer. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 368, 20110329, doi:10.1098/rstb.2011.0329 (2013). · DOI
  12. Huangfu, D. et al. Induction of pluripotent stem cells by defined factors is greatly improved by small-molecule compounds. Nat Biotechnol 26, 795–797 (2008). · DOI
  13. Zhao, J. et al. Significant improvement in cloning efficiency of an inbred miniature pig by histone deacetylase inhibitor treatment after somatic cell nuclear transfer. Biol Reprod 81, 525–530, doi:10.1095/biolreprod.109.077016 (2009). · DOI
  14. Pasque, V., Jullien, J., Miyamoto, K., Halley-Stott, R. P. & Gurdon, J. B. Epigenetic factors influencing resistance to nuclear reprogramming. Trends Genet 27, 516–525, doi:10.1016/j.tig.2011.08.002 (2011). · DOI
  15. Meshorer, E. et al. Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev Cell 10, 105–116 (2006). · DOI
  16. de Wit, E. et al. The pluripotent genome in three dimensions is shaped around pluripotency factors. Nature 501, 227–231, doi:10.1038/nature12420 (2013). · DOI
  17. Boskovic, A. et al. Higher chromatin mobility supports totipotency and precedes pluripotency in vivo. Genes Dev 28, 1042–1047, doi:10.1101/gad.238881.114 (2014). · DOI
  18. Fussner, E. et al. Constitutive heterochromatin reorganization during somatic cell reprogramming. The EMBO journal 30, 1778–1789, doi:10.1038/emboj.2011.96 (2011). · DOI
  19. Ahmed, K. et al. Global chromatin architecture reflects pluripotency and lineage commitment in the early mouse embryo. PLoS ONE 5, e10531, doi:10.1371/journal.pone.0010531 (2010). · DOI
  20. Soufi, A., Donahue, G. & Zaret, K. S. Facilitators and impediments of the pluripotency reprogramming factors’ initial engagement with the genome. Cell 151, 994–1004, doi:10.1016/j.cell.2012.09.045 (2012). · DOI · Paper page
  21. Wang, T. et al. The histone demethylases Jhdm1a/1b enhance somatic cell reprogramming in a vitamin-C-dependent manner. Cell Stem Cell 9, 575–587, doi:10.1016/j.stem.2011.10.005 (2011). · DOI · Paper page
  22. Liang, G., He, J. & Zhang, Y. Kdm2b promotes induced pluripotent stem cell generation by facilitating gene activation early in reprogramming. Nat Cell Biol 14, 457–466, doi:10.1038/ncb2483 (2012). · DOI
  23. Schotta, G. et al. A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev 18, 1251–1262, doi:10.1101/gad.300704300704 (2004). · DOI · Paper page
  24. Antony, J., Oback, F., Chamley, L. W., Oback, B. & Laible, G. Transient JMJD2B-Mediated Reduction of H3K9me3 Levels Improves Reprogramming of Embryonic Stem Cells into Cloned Embryos. Molecular and cellular biology 33, 974–983, doi:10.1128/MCB.01014-12 (2013). · DOI
  25. Matoba, S. et al. Embryonic development following somatic cell nuclear transfer impeded by persisting histone methylation. Cell 159, 884–895, doi:10.1016/j.cell.2014.09.055 (2014). · DOI
  26. Gaspar-Maia, A., Alajem, A., Meshorer, E. & Ramalho-Santos, M. Open chromatin in pluripotency and reprogramming. Nature reviews. Molecular cell biology 12, 36–47, doi:10.1038/nrm3036 (2011). · DOI
  27. Ma, D. K., Chiang, C. H., Ponnusamy, K., Ming, G. L. & Song, H. G9a and Jhdm2a regulate embryonic stem cell fusion-induced reprogramming of adult neural stem cells. Stem Cells 26, 2131–2141, doi:10.1634/stemcells.2008-0388 (2008). · DOI
  28. Chen, J. et al. H3K9 methylation is a barrier during somatic cell reprogramming into iPSCs. Nature genetics 45, 34–42, doi:10.1038/ng.2491 (2013). · DOI · Paper page
  29. Epsztejn-Litman, S. et al. De novo DNA methylation promoted by G9a prevents reprogramming of embryonically silenced genes. Nat Struct Mol Biol 15, 1176–1183, doi:10.1038/nsmb.1476 (2008). · DOI
  30. Nichols, J., Chambers, I. & Smith, A. Derivation of germline competent embryonic stem cells with a combination of interleukin-6 and soluble interleukin-6 receptor. Experimental cell research 215, 237–239, doi:10.1006/excr.1994.1338 (1994). · DOI
  31. Neil, G. A. & Zimmermann, U. Electrofusion. Methods Enzymol 220, 174–196 (1993). · DOI
  32. Hanna, J. et al. Human embryonic stem cells with biological and epigenetic characteristics similar to those of mouse ESCs. Proc Natl Acad Sci USA 107, 9222–9227, doi:10.1073/pnas.1004584107 (2010). · DOI
  33. Silva, J. et al. Promotion of reprogramming to ground state pluripotency by signal inhibition. PLoS biology 6, e253 (2008). · DOI
  34. Wen, B., Wu, H., Shinkai, Y., Irizarry, R. A. & Feinberg, A. P. Large histone H3 lysine 9 dimethylated chromatin blocks distinguish differentiated from embryonic stem cells. Nature genetics 41, 246–250, doi:10.1038/ng.297 (2009). · DOI
  35. Efroni, S. et al. Global transcription in pluripotent embryonic stem cells. Cell Stem Cell 2, 437–447, doi:10.1016/j.stem.2008.03.021 (2008). · DOI
  36. Fodor, B. D. et al. Jmjd2b antagonizes H3K9 trimethylation at pericentric heterochromatin in mammalian cells. Genes Dev 20, 1557–1562 (2006). · DOI
  37. Zhang, T., Cooper, S. & Brockdorff, N. The interplay of histone modifications - writers that read. EMBO reports 16, 1467–1481, doi:10.15252/embr.201540945 (2015). · DOI
  38. Ohhata, T. et al. Histone H3 Lysine 36 Trimethylation Is Established over the Xist Promoter by Antisense Tsix Transcription and Contributes to Repressing Xist Expression. Molecular and cellular biology 35, 3909–3920, doi:10.1128/MCB.00561-15 (2015). · DOI
  39. Inoue, K. et al. Impeding Xist expression from the active X chromosome improves mouse somatic cell nuclear transfer. Science 330, 496–499, doi:10.1126/science.1194174 (2010). · DOI
  40. Lachner, M., O’Carroll, D., Rea, S., Mechtler, K. & Jenuwein, T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410, 116–120, doi:10.1038/35065132 (2001). · DOI · Paper page
  41. Bannister, A. J. et al. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410, 120–124, doi:10.1038/35065138 (2001). · DOI · Paper page
  42. Canzio, D. et al. A conformational switch in HP1 releases auto-inhibition to drive heterochromatin assembly. Nature 496, 377–381, doi:10.1038/nature12032 (2013). · DOI
  43. Poleshko, A. & Katz, R. A. Specifying peripheral heterochromatin during nuclear lamina reassembly. Nucleus 5, 32–39, doi:10.4161/nucl.28167 (2014). · DOI
  44. Payen, E. et al. The centromeric/nucleolar chromatin protein ZFP-37 may function to specify neuronal nuclear domains. J Biol Chem 273, 9099–9109 (1998). · DOI
  45. Lee, P. Y., Wang, J.-X., Parisini, E., Dascher, C. C. & Nigrovic, P. A. Ly6 family proteins in neutrophil biology. Journal of Leukocyte Biology 94, 585–594, doi:10.1189/jlb.0113014 (2013). · DOI
  46. Inoue, K. et al. Inefficient reprogramming of the hematopoietic stem cell genome following nuclear transfer. J Cell Sci 119, 1985–1991 (2006). · DOI
  47. Vassena, R. et al. Tough beginnings: alterations in the transcriptome of cloned embryos during the first two cell cycles. Dev Biol 304, 75–89 (2007). · DOI
  48. Probst, A. V. et al. A strand-specific burst in transcription of pericentric satellites is required for chromocenter formation and early mouse development. Dev Cell 19, 625–638, doi:10.1016/j.devcel.2010.09.002 (2010). · DOI
  49. Kigami, D., Minami, N., Takayama, H. & Imai, H. MuERV-L is one of the earliest transcribed genes in mouse one-cell embryos. Biol Reprod 68, 651–654 (2003). · DOI
  50. Pfeiffer, M. J. et al. Differences in embryo quality are associated with differences in oocyte composition: a proteomic study in inbred mice. Proteomics 15, 675–687, doi:10.1002/pmic.201400334 (2015). · DOI
  51. Liu, H., Kim, J.-M. & Aoki, F. Regulation of histone H3 lysine 9 methylation in oocytes and early pre-implantation embryos. Development 131, 2269–2280 (2004). · DOI
  52. Gao, T. et al. Nuclear reprogramming: the strategy used in normal development is also used in somatic cell nuclear transfer and parthenogenesis. Cell Res 17, 135–150, doi:http://www.nature.com/cr/journal/v17/n2/suppinfo/cr20072s1.html (2007). · DOI
  53. Wu, G. et al. Establishment of totipotency does not depend on Oct4A. Nat Cell Biol 15, 1089–1097, doi:10.1038/ncb2816 (2013). · DOI
  54. Onder, T. T. et al. Chromatin-modifying enzymes as modulators of reprogramming. Nature 483, 598–602, doi:10.1038/nature10953 (2012). · DOI
  55. Kallingappa, P. K. et al. Quiescence Loosens Epigenetic Constraints in Bovine Somatic Cells and Improves Their Reprogramming into Totipotency. Biol Reprod. doi:10.1095/biolreprod.115.137109 (2016). · DOI
  56. Tichopad, A., Dilger, M., Schwarz, G. & Pfaffl, M. W. Standardized determination of real-time PCR efficiency from a single reaction set-up. Nucleic Acids Res 31, e122 (2003). · DOI
  57. Smith, C. et al. Simultaneous gene quantitation of multiple genes in individual bovine nuclear transfer blastocysts. Reproduction 133, 231–242 (2007). · DOI
  58. Irizarry, R. A. et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249–264, doi:10.1093/biostatistics/4.2.249 (2003). · DOI · Paper page
  59. Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140, doi:10.1093/bioinformatics/btp616 (2010). · DOI · Paper page
  60. Benjamini, Y. & Hochberg, Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society. Series B (Methodological) 57, 289–300, doi:10.2307/2346101 (1995). · DOI
  61. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079, doi:10.1093/bioinformatics/btp352 (2009). · DOI · Paper page
  62. Liao, Y., Smyth, G. K. & Shi, W. Feature Counts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930, doi:10.1093/bioinformatics/btt656 (2014). · DOI · Paper page
  63. Ying, Q. L. et al. The ground state of embryonic stem cell self-renewal. Nature 453, 519–523 (2008). · DOI · Paper page

Cited by

Sorted by citations

Metadata

Authors
Wei, J., Antony, J., Meng, F., MacLean, P., Rhind, R., Laible, G., & Oback, B.
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2017-08-08
Volume
7
Issue
1
ISSN
2045-2322
DOI
10.1038/s41598-017-06569-2
PMC
PMC5548918
Cited by
39
References
3
Language
en
Licence

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review