Histone modifications and lamin A regulate chromatin protein dynamics in early embryonic stem cell differentiation

Nature Communications

Volumn 3, Issue , 2012, Pages

  Melcer, Shai ^a   Hezroni, Hadas ^a   Rand, Eyal ^b   Nissim Rafinia, Malka ^a   Skoultchi, Arthur ^c   Stewart, Colin L ^d,e   Bustin, Michael ^b   Meshorer, Eran ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b NATIONAL CANCER INSTITUTE   (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CHROMATIN PROTEIN; HISTONE H3; LAMIN A; UNCLASSIFIED DRUG; HISTONE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CHROMATIN; CONTROLLED STUDY; DNA METHYLATION; EMBRYONIC STEM CELL; EUCHROMATIN; HISTONE ACETYLATION; HISTONE MODIFICATION; MOUSE; NONHUMAN; NUCLEOSOME; PROTEIN FUNCTION; PROTEIN STRUCTURE; ACETYLATION; ANIMAL; CYTOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; METHYLATION; PHYSIOLOGY;

ACETYLATION; ANIMALS; CELL DIFFERENTIATION; CHROMATIN; EMBRYONIC STEM CELLS; FLUORESCENT ANTIBODY TECHNIQUE; HISTONES; LAMIN TYPE A; METHYLATION; MICE;

EID: 84863334769     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms1915     Document Type: Article

References (59)

1. Aoto, T., Saitoh, N., Ichimura, T., Niwa, H, & Nakao, M. Nuclear and chromatin reorganization in the MHC-Oct3/4 locus at developmental phases of embryonic stem cell differentiation. Dev. Biol. 298, 354-367 (2006). (Pubitemid 44468059)
2. Meshorer, E, & Misteli, T. Chromatin in pluripotent embryonic stem cells and differentiation. Nat. Rev. Mol. Cell Biol. 7, 540-546 (2006). (Pubitemid 44036459)
3. Constantinescu, D., Gray, H. L., Sammak, P. J., Schatten, G. P, & Csoka, A. B. Lamin A/C expression is a marker of mouse and human embryonic stem cell differentiation. Stem Cells 24, 177-185 (2006).
4. Mattout, A., Goldberg, M., Tzur, Y., Margalit, A, & Gruenbaum, Y. Specific and conserved sequences in D. melanogaster and C. elegans lamins and histone H2A mediate the attachment of lamins to chromosomes. J. Cell Sci. 120, 77-85 (2007). (Pubitemid 46206651)
5. Taniura, H., Glass, C, & Gerace, L. A chromatin binding site in the tail domain of nuclear lamins that interacts with core histones. J. Cell Biol. 131, 33-44 (1995).
6. Efroni, S. et al. Global transcription in pluripotent embryonic stem cells. Cell Stem Cell 2, 437-447 (2008). (Pubitemid 351598083)
7. Meshorer, E. et al. Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev. Cell 10, 105-116 (2006). (Pubitemid 43025681)
8. Azuara, V. et al. Chromatin signatures of pluripotent cell lines. Nat. Cell Biol. 8, 532-538 (2006).
9. Bernstein, B. E. et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326 (2006).
10. Pan, G. et al. Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell 1, 299-312 (2007). (Pubitemid 47355329)
11. Guenther, M. G., Levine, S. S., Boyer, L. A., Jaenisch, R, & Young, R. A. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130, 77-88 (2007). (Pubitemid 47031323)
12. Rasmussen, T. P. Developmentally-poised chromatin of embryonic stem cells. Front. Biosci. 13, 1568-1577 (2008). (Pubitemid 351594726)
13. Hawkins, R. D. et al. Distinct epigenomic landscapes of pluripotent and lineage-committed human cells. Cell Stem Cell 6, 479-491 (2010).
14. 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. Nat. Genet. 41, 246-250 (2009).
15. Misteli, T., Gunjan, A., Hock, R., Bustin, M, & Brown, D. T. Dynamic binding of histone H1 to chromatin in living cells. Nature 408, 877-881 (2000). (Pubitemid 32016100)
16. Krejci, J. et al. Genome-wide reduction in H3K9 acetylation during human embryonic stem cell differentiation. J. Cell. Physiol. 219, 677-687 (2009).
17. Catez, F., Brown, D. T., Misteli, T, & Bustin, M. Competition between histone H1 and HMGN proteins for chromatin binding sites. EMBO Rep. 3, 760-766 (2002). (Pubitemid 34966015)
18. Hezroni, H. et al. H3K9 histone acetylation predicts pluripotency and reprogramming capacity of ES cells. Nucleus 2, 300-309 (2011).
19. Hezroni, H., Sailaja, B. S, & Meshorer, E. Pluripotency-related, valproic acid (VPA)-induced genome-wide histone H3 lysine 9 (H3K9) acetylation patterns in embryonic stem cells. J. Biol. Chem. 286, 35977-35988 (2011).
20. Gaspar-Maia, A., Alajem, A., Meshorer, E, & Ramalho-Santos, M. Open chromatin in pluripotency and reprogramming. Nat. Rev. Mol. Cell Biol. 12, 36-47 (2011).
21. Hsieh, J., Nakashima, K., Kuwabara, T., Mejia, E, & Gage, F. H. Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc. Natl Acad. Sci. USA 101, 16659-16664 (2004). (Pubitemid 39557769)
22. Tachibana, M. et al. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 16, 1779-1791 (2002). (Pubitemid 34803894)
23. Peters, A. H. et al. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107, 323-337 (2001). (Pubitemid 33049976)
24. Tachibana, M., Matsumura, Y., Fukuda, M., Kimura, H, & Shinkai, Y. G9a/GLP complexes independently mediate H3K9 and DNA methylation to silence transcription. EMBO J. 27, 2681-2690 (2008).
25. Feldman, N. et al. G9a-mediated irreversible epigenetic inactivation of Oct-3/4 during early embryogenesis. Nat. Cell. Biol. 8, 188-194 (2006).
26. Chen, X. et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133, 1106-1117 (2008). (Pubitemid 351787745)
27. Nishiyama, A. et al. Uncovering early response of gene regulatory networks in ESCs by systematic induction of transcription factors. Cell Stem Cell 5, 420-433 (2009).
28. Krouwels, I. M. et al. A glue for heterochromatin maintenance: stable SUV39H1 binding to heterochromatin is reinforced by the SET domain. J. Cell Biol. 170, 537-549 (2005). (Pubitemid 41186929)
29. Guttman, M. et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458, 223-227 (2009).
30. Yokochi, T. et al. G9a selectively represses a class of late-replicating genes at the nuclear periphery. Proc. Natl Acad. Sci. USA 106, 19363-19368 (2009).
31. Bhattacharya, D., Talwar, S., Mazumder, A, & Shivashankar, G. V. Spatio-temporal plasticity in chromatin organization in mouse cell differentiation and during Drosophila embryogenesis. Biophys. J. 96, 3832-3839 (2009).
32. Meshorer, E. Chromatin in embryonic stem cell neuronal differentiation. Histol. Histopathol. 22, 311-319 (2007). (Pubitemid 46117117)
33. Pajerowski, J. D., Dahl, K. N., Zhong, F. L., Sammak, P. J, & Discher, D. E. Physical plasticity of the nucleus in stem cell differentiation. Proc. Natl Acad. Sci. USA 104, 15619-15624 (2007). (Pubitemid 350035348)
34. Phair, R. D, & Misteli, T. High mobility of proteins in the mammalian cell nucleus. Nature 404, 604-609 (2000). (Pubitemid 30205058)
35. Phair, R. D. et al. Global nature of dynamic protein-chromatin interactions in vivo: three-dimensional genome scanning and dynamic interaction networks of chromatin proteins. Mol. Cell. Biol. 24, 6393-6402 (2004). (Pubitemid 38891138)
36. Sullivan, T. et al. Loss of A-type Lamin Expression Compromises Nuclear Envelope Integrity Leading to Muscular Dystrophy. J. Cell Biol. 147, 913-920 (1999).
37. Pannetier, M, & Feil, R. Epigenetic stability of embryonic stem cells and developmental potential. Trends Biotechnol. 25, 556-562 (2007). (Pubitemid 350138175)
38. Chen, R. Z., Pettersson, U., Beard, C., Jackson-Grusby, L, & Jaenisch, R. DNA hypomethylation leads to elevated mutation rates. Nature 395, 89-93 (1998). (Pubitemid 28420236)
39. Okano, M., Bell, D. W., Haber, D. A, & Li, E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247-257 (1999). (Pubitemid 29519904)
40. Tsumura, A. et al. Maintenance of self-renewal ability of mouse embryonic stem cells in the absence of DNA methyltransferases Dnmt1, Dnmt3a and Dnmt3b. Genes Cells 11, 805-814 (2006). (Pubitemid 43923351)
41. Cedar, H, & Bergman, Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet. 10, 295-304 (2009).
42. Fan, Y. et al. Histone H1 depletion in mammals alters global chromatin structure but causes specific changes in gene regulation. Cell 123, 1199-1212 (2005). (Pubitemid 41821779)
43. Woodcock, C. L., Skoultchi, A. I, & Fan, Y. Role of linker histone in chromatin structure and function: H1 stoichiometry and nucleosome repeat length. Chromosome Res. 14, 17-25 (2006).
44. Ware, C. B. et al. Histone deacetylase inhibition elicits an evolutionarily conserved self-renewal program in embryonic stem cells. Cell Stem Cell 4, 359-369 (2009).
45. Zhou, H. et al. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 4, 381-384 (2009).
46. Shi, Y. et al. Induction of pluripotent stem cells from mouse embryonic fibroblasts by Oct4 and Klf4 with small-molecule compounds. Cell Stem Cell 3, 568-574 (2008).
47. Alder, O. et al. Ring1B and Suv39h1 delineate distinct chromatin states at bivalent genes during early mouse lineage commitment. Development 137, 2483-2492 (2010).
48. Melcer, S, & Meshorer, E. The silence of the LADs: dynamic genome-lamina interactions during ESC differentiation. Cell Stem Cell 6, 495-497 (2010).
49. Melcer, S, & Meshorer, E. Chromatin plasticity in pluripotent cells. Essays Biochem. 48, 245-262 (2010).
50. Reddy, K. L., Zullo, J. M., Bertolino, E, & Singh, H. Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature 13, 243-247 (2008). (Pubitemid 351380248)
51. Efroni, S., Melcer, S., Nissim-Rafinia, M, & Meshorer, E. Stem cells do play with dice: a statistical physics view of transcription. Cell Cycle 8, 43-48 (2009).
52. Gaspar-Maia, A. et al. Chd1 regulates open chromatin and pluripotency of embryonic stem cells. Nature 460, 863-868 (2009).
53. Ho, L. et al. An embryonic stem cell chromatin remodeling complex, esBAF, is an essential component of the core pluripotency transcriptional network. Proc. Natl Acad. Sci. USA 106, 5187-5191 (2009).
54. Yan, Z. et al. BAF250B-associated SWI/SNF chromatin-remodeling complex is required to maintain undifferentiated mouse embryonic stem cells. Stem Cells 26, 1155-1165 (2008).
55. Gilbert, N. et al. DNA methylation affects nuclear organization, histone modifications, and linker histone binding but not chromatin compaction. J. Cell Biol. 177, 401-411 (2007). (Pubitemid 46718270)
56. Cheutin, T. et al. Maintenance of stable heterochromatin domains by dynamic HP1 binding. Science 299, 721-725 (2003). (Pubitemid 36159490)
57. Gerlitz, G. et al. Migration cues induce chromatin alterations. Traffic 8, 1521-1529 (2007). (Pubitemid 47578358)
58. Nissim-Rafinia, M, & Meshorer, E. Photobleaching assays (FRAP & FLIP) to measure chromatin protein dynamics in living embryonic stem cells. J. Vis. Exp. 52, pii 2696 (2011).
59. Mills, K. I, & Ramsahoye, B. H. DNA methylation protocols. Overview. Methods Mol. Biol. 200, 1-7 (2002).