The nuclear periphery of embryonic stem cells is a transcriptionally permissive and repressive compartment

Journal of Cell Science

Volumn 122, Issue 20, 2009, Pages 3729-3737

  Luo, Li ^a,b   Gassman, Katherine L ^a   Petell, Lydia M ^a   Wilson, Christian L ^a,c   Bewersdorf, Joerg ^a   Shopland, Lindsay S ^a  

^a JACKSON LABORATORY   (United States)

^b NANJING MEDICAL UNIVERSITY   (China)

^c University of Maine   (United States)

Author keywords

Chromatin; Embryonic stem cell; Epigenetics; Nucleus

Indexed keywords

HISTONE H3; LYSINE;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL TYPE; CHROMATIN; CONTROLLED STUDY; CYTOLOGY; EMBRYONIC STEM CELL; EPIGENETICS; FLUORESCENCE IN SITU HYBRIDIZATION; GENE REPRESSION; IMAGE ANALYSIS; IMMUNOFLUORESCENCE; MICROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; QUANTITATIVE ANALYSIS; WESTERN BLOTTING;

ANIMALS; CELL COMPARTMENTATION; CHROMATIN; EMBRYONIC STEM CELLS; EPIGENESIS, GENETIC; FIBROBLASTS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; NEURONS; NIH 3T3 CELLS; NUCLEAR ENVELOPE; ORGAN SPECIFICITY; TRANSCRIPTION, GENETIC;

EID: 70350349888     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.052555     Document Type: Article

References (74)

1. Akhtar, A. and Gasser, S. M. (2007). The nuclear envelope and transcriptional control. Nat. Rev. Genet. 8, 507-517.
2. Andrulis, E. D., Neiman, A. M., Zappulla, D. C. and Sternglanz, R. (1998). Perinuclear localization of chromatin facilitates transcriptional silencing. Nature 394, 592-595.
3. Azuara, V., Perry, P., Sauer, S., Spivakov, M., Jorgensen, H. F., John, R. M., Gouti, M., Casanova, M., Warnes, G., Merkenschlager, M. et al. (2006). Chromatin signatures of pluripotent cell lines. Nat. Cell Biol. 8, 532-538.
4. Bartova, E., Pachernik, J., Harnicarova, A., Kovarik, A., Kovarikova, M., Hofmanova, J., Skalnikova, M., Kozubek, M. and Kozubek, S. (2005). Nuclear levels and patterns of histone H3 modification and HP1 proteins after inhibition of histone deacetylases. J. Cell Sci. 118, 5035-5046.
5. Bernstein, B. E., Mikkelsen, T. S., Xie, X., Kamal, M., Huebert, D. J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K. et al. (2006). A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326.
6. Bewersdorf, J., Bennett, B. T. and Knight, K. L. (2006). H2AX chromatin structures and their response to DNA damage revealed by 4Pi microscopy. Proc. Natl. Acad. Sci. USA 103, 18137-18142.
7. Blobel, G. (1985). Gene gating: a hypothesis. Proc. Natl. Acad. Sci. USA 82, 8527-8529.
8. Brickner, D. G., Cajigas, I., Fondufe-Mittendorf, Y., Ahmed, S., Lee, P. C., Widom, J. and Brickner, J. H. (2007). H2A.Z-mediated localization of genes at the nuclear periphery confers epigenetic memory of previous transcriptional state. PLoS Biol. 5, e81.
9. Brickner, J. H. and Walter, P. (2004). Gene recruitment of the activated INO1 locus to the nuclear membrane. PLoS Biol. 2, e342.
10. Brown, C. R., Kennedy, C. J., Delmar, V. A., Forbes, D. J. and Silver, P. A. (2008). Global histone acetylation induces functional genomic reorganization at mammalian nuclear pore complexes. Genes Dev. 22, 627-639.
11. Butler, J. T., Hall, L. L., Smith, K. P. and Lawrence, J. B. (2009). Changing nuclear landscape and unique PML structures during early epigenetic transitions of human embryonic stem cells. J. Cell Biochem. 107, 609-621.
12. Casolari, J. M., Brown, C. R., Komili, S., West, J., Hieronymus, H. and Silver, P. A. (2004). Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization. Cell 117, 427-439.
13. Cedar, H. and Bergman, Y. (2009). Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet. 10, 295-304.
14. Chuang, C. H., Carpenter, A. E., Fuchsova, B., Johnson, T., de Lanerolle, P. and Belmont, A. S. (2006). Long-range directional movement of an interphase chromosome site. Curr. Biol. 16, 825-831.
15. Constantinescu, D., Gray, H. L., Sammak, P. J., Schatten, G. P. and Csoka, A. B. (2006). Lamin A/C expression is a marker of mouse and human embryonic stem cell differentiation. Stem Cells 24, 177-185.
16. Dechat, T., Pfleghaar, K., Sengupta, K., Shimi, T., Shumaker, D. K., Solimando, L. and Goldman, R. D. (2008). Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev. 22, 832-853.
17. Efroni, S., Duttagupta, R., Cheng, J., Dehghani, H., Hoeppner, D. J., Dash, C., Bazett- Jones, D. P., Le Grice, S., McKay, R. D., Buetow, K. H. et al. (2008). Global transcription in pluripotent embryonic stem cells. Cell Stem Cell 2, 437-447.
18. Fakan, S. (1994). Perichromatin fibrils are in situ forms of nascent transcripts. Trends Cell Biol. 4, 86-90.
19. Ferreira, J., Paolella, G., Ramos, C. and Lamond, A. I. (1997). Spatial organization of large-scale chromatin domains in the nucleus: a magnified view of single chromosome territories. J. Cell Biol. 139, 1597-1610.
20. Finlan, L. E., Sproul, D., Thomson, I., Boyle, S., Kerr, E., Perry, P., Ylstra, B., Chubb, J. R. and Bickmore, W. A. (2008). Recruitment to the nuclear periphery can alter expression of genes in human cells. PLoS Genet. 4, e1000039.
21. Francastel, C., Schubeler, D., Martin, D. I. and Groudine, M. (2000). Nuclear compartmentalization and gene activity. Nat. Rev. Mol. Cell Biol. 1, 137-143.
22. Fraser, P. and Bickmore, W. (2007). Nuclear organization of the genome and the potential for gene regulation. Nature 447, 413-417.
23. Fricker, M., Hollinshead, M., White, N. and Vaux, D. (1997). Interphase nuclei of many mammalian cell types contain deep, dynamic, tubular membrane-bound invaginations of the nuclear envelope. J. Cell Biol. 136, 531-544.
24. Gruenbaum, Y., Margalit, A., Goldman, R. D., Shumaker, D. K. and Wilson, K. L. (2005). The nuclear lamina comes of age. Nat. Rev. Mol. Cell Biol. 6, 21-31.
25. Guelen, L., Pagie, L., Brasset, E., Meuleman, W., Faza, M. B., Talhout, W., Eussen, B. H., de Klein, A., Wessels, L., de Laat, W. et al. (2008). Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453, 948-951.
26. Guenther, M. G., Levine, S. S., Boyer, L. A., Jaenisch, R. and Young, R. A. (2007). A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130, 77-88.
27. Hewitt, S. L., High, F. A., Reiner, S. L., Fisher, A. G. and Merkenschlager, M. (2004). Nuclear repositioning marks the selective exclusion of lineage-inappropriate transcription factor loci during T helper cell differentiation. Eur. J. Immunol. 34, 3604-3613.
28. Hiratani, I., Ryba, T., Itoh, M., Yokochi, T., Schwaiger, M., Chang, C. W., Lyou, Y., Townes, T. M., Schubeler, D. and Gilbert, D. M. (2008). Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol. 6, e245.
29. Hutchinson, N. and Weintraub, H. (1985). Localization of DNAse I-sensitive sequences to specific regions of interphase nuclei. Cell 43, 471-482.
30. Iborra, F. J., Pombo, A., Jackson, D. A. and Cook, P. R. (1996). Active RNA polymerases are localized within discrete transcription 'factories' in human nuclei. J. Cell Sci. 109, 1427-1436.
31. Jackson, D. A., Hassan, A. B., Errington, R. J. and Cook, P. R. (1993). Visualization of focal sites of transcription within human nuclei. EMBO J. 12, 1059-1065.
32. Johnson, C., Primorac, D., McKinstry, M., McNeil, J., Rowe, D. and Lawrence, J. B. (2000). Tracking COL1A1 RNA in osteogenesis imperfecta. splice-defective transcripts initiate transport from the gene but are retained within the SC35 domain. J. Cell Biol. 150, 417-432.
33. Kiseleva, E., Allen, T. D., Rutherford, S., Bucci, M., Wente, S. R. and Goldberg, M. W. (2004). Yeast nuclear pore complexes have a cytoplasmic ring and internal filaments. J. Struct. Biol. 145, 272-288.
34. Knowles, B. B., Aden, D. P. and Solter, D. (1978). Monoclonal antibody detecting a stage-specific embryonic antigen (SSEA-1) on preimplantation mouse embryos and teratocarcinoma cells. Curr. Top. Microbiol. Immunol. 81, 51-53.
35. Kobor, M. S. and Greenblatt, J. (2002). Regulation of transcription elongation by phosphorylation. Biochim. Biophys. Acta 1577, 261-275.
36. Kosak, S. T., Skok, J. A., Medina, K. L., Riblet, R., Le Beau, M. M., Fisher, A. G. and Singh, H. (2002). Subnuclear compartmentalization of immunoglobulin loci during lymphocyte development. Science 296, 158-162.
37. Kumaran, R. I. and Spector, D. L. (2008). A genetic locus targeted to the nuclear periphery in living cells maintains its transcriptional competence. J. Cell Biol. 180, 51-65.
38. Kupper, K., Kolbl, A., Biener, D., Dittrich, S., von Hase, J., Thormeyer, T., Fiegler, H., Carter, N. P., Speicher, M. R., Cremer, T. et al. (2007). Radial chromatin positioning is shaped by local gene density, not by gene expression. Chromosoma 116, 285-306.
39. Lanctot, C., Cheutin, T., Cremer, M., Cavalli, G. and Cremer, T. (2007). Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions. Nat. Rev. Genet. 8, 104-115.
40. Lawrence, J. B. and Clemson, C. M. (2008). Gene associations: true romance or chance meeting in a nuclear neighborhood? J. Cell Biol. 182, 1035-1038.
41. Lawrence, J. B., Singer, R. H. and McNeil, J. A. (1990). Interphase and metaphase resolution of different distances within the human dystrophin gene. Science 249, 928-932.
42. Levi, V., Ruan, Q., Plutz, M., Belmont, A. S. and Gratton, E. (2005). Chromatin dynamics in interphase cells revealed by tracking in a two-photon excitation microscope. Biophys. J. 89, 4275-4285.
43. Levsky, J. M., Shenoy, S. M., Pezo, R. C. and Singer, R. H. (2002). Single-cell gene expression profiling. Science 297, 836-840.
44. Lunyak, V. V. and Rosenfeld, M. G. (2008). Epigenetic regulation of stem cell fate. Hum. Mol. Genet. 17, R28-R36.
45. Meaburn, K. J. and Misteli, T. (2008). Locus-specific and activity-independent gene repositioning during early tumorigenesis. J. Cell Biol. 180, 39-50.
46. Meshorer, E., Yellajoshula, D., George, E., Scambler, P. J., Brown, D. T. and Misteli, T. (2006). Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev. Cell 10, 105-116.
47. Mikkelsen, T. S., Ku, M., Jaffe, D. B., Issac, B., Lieberman, E., Giannoukos, G., Alvarez, P., Brockman, W., Kim, T. K., Koche, R. P. et al. (2007). Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448, 553-560.
48. Mohn, F., Weber, M., Rebhan, M., Roloff, T. C., Richter, J., Stadler, M. B., Bibel, M. and Schubeler, D. (2008). Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol. Cell 30, 755-766.
49. Nash, R. E., Puvion, E. and Bernhard, W. (1975). Perichromatin fibrils as components of rapidly labeled extranucleolar RNA. J. Ultrastruct. Res. 53, 395-405.
50. Ovcharenko, I., Loots, G. G., Nobrega, M. A., Hardison, R. C., Miller, W. and Stubbs, L. (2005). Evolution and functional classification of vertebrate gene deserts. Genome Res. 15, 137-145.
51. Pan, G., Tian, S., Nie, J., Yang, C., Ruotti, V., Wei, H., Jonsdottir, G. A., Stewart, R. and Thomson, J. A. (2007). Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell 1, 299-312.
52. Peters, A. H., Kubicek, S., Mechtler, K., O'Sullivan, R. J., Derijck, A. A., Perez-Burgos, L., Kohlmaier, A., Opravil, S., Tachibana, M., Shinkai, Y. et al. (2003). Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol. Cell 12, 1577-1589.
53. Puschendorf, M., Terranova, R., Boutsma, E., Mao, X., Isono, K., Brykczynska, U., Kolb, C., Otte, A. P., Koseki, H., Orkin, S. H. et al. (2008). PRC1 and Suv39h specify parental asymmetry at constitutive heterochromatin in early mouse embryos. Nat. Genet. 40, 411-420.
54. Ragoczy, T., Bender, M. A., Telling, A., Byron, R. and Groudine, M. (2006). The locus control region is required for association of the murine beta-globin locus with engaged transcription factories during erythroid maturation. Genes Dev. 20, 1447-1457.
55. Reddy, K. L., Zullo, J. M., Bertolino, E. and Singh, H. (2008). Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature 452, 243-247.
56. Ronneberger, O., Baddeley, D., Scheipl, F., Verveer, P. J., Burkhardt, H., Cremer, C., Fahrmeir, L., Cremer, T. and Joffe, B. (2008). Spatial quantitative analysis of fluorescently labeled nuclear structures: problems, methods, pitfalls. Chromosome Res. 16, 523-562.
57. Sadoni, N., Langer, S., Fauth, C., Bernardi, G., Cremer, T., Turner, B. M. and Zink, D. (1999). Nuclear organization of mammalian genomes: polar chromosome territories build up functionally distinct higher order compartments. J. Cell Biol. 146, 1211-1226.
58. Shopland, L. S., Byron, M., Stein, J. L., Lian, J. B., Stein, G. S. and Lawrence, J. B. (2001). Replication-dependent histone gene expression is related to Cajal body (CB) association but does not require sustained CB contact. Mol. Biol. Cell 12, 565-576.
59. Shopland, L. S., Peterson, K., Lynch, C. R., Thornton, K., Kepper, N., Stein, S., Vincent, S., Molloy, K., Kreth, G., Cremer, C. et al. (2006). Folding and organization of a contiguous chromosome region according to the gene distribution pattern in primary genomic sequence. J. Cell Biol. 174, 27-38.
60. Shumaker, D. K., Dechat, T., Kohlmaier, A., Adam, S. A., Bozovsky, M. R., Erdos, M. R., Eriksson, M., Goldman, A. E., Khuon, S., Collins, F. S. et al. (2006). Mutant nuclear lamin A leads to progressive alterations of epigenetic control in premature aging. Proc. Natl. Acad. Sci. USA 103, 8703-8708.
61. Solovei, I., Cavallo, A., Schermelleh, L., Jaunin, F., Scasselati, C., Cmarko, D., Cremer, C., Fakan, S. and Cremer, T. (2002). Spatial preservation of nuclear chromatin architecture during three-dimensional fluorescence in situ hybridization (3D-FISH). Exp. Cell Res. 276, 10-23.
62. Spivakov, M. and Fisher, A. G. (2007). Epigenetic signatures of stem-cell identity. Nat. Rev. Genet. 8, 263-271.
63. Stock, J. K., Giadrossi, S., Casanova, M., Brookes, E., Vidal, M., Koseki, H., Brockdorff, N., Fisher, A. G. and Pombo, A. (2007). Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells. Nat. Cell Biol. 9, 1428-1435.
64. Sullivan, T., Escalante-Alcalde, D., Bhatt, H., Anver, M., Bhat, N., Nagashima, K., Stewart, C. L. and Burke, B. (1999). Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J. Cell Biol. 147, 913-920.
65. Tam, R., Shopland, L. S., Johnson, C. V., McNeil, J. A. and Lawrence, J. B. (2002). Applications of RNA FISH for visualizating gene expression and nuclear architecture. In Fish: A Practical Approach (ed. B. Beatty, S. Mai and J. Squire), pp. 93-118. Oxford: Oxford University Press.
66. Terranova, R., Yokobayashi, S., Stadler, M. B., Otte, A. P., van Lohuizen, M., Orkin, S. H. and Peters, A. H. (2008). Polycomb group proteins Ezh2 and Rnf2 direct genomic contraction and imprinted repression in early mouse embryos. Dev. Cell 15, 668-679.
67. Wansink, D. G., Schul, W., VanDerKraan, I., VanSteensel, B., VanDriel, R. and DeJong, L. (1993). Fluorescent labeling of nascent RNA reveals transcription by RNA polymerase II in domains scattered throughout the nucleus. J. Cell Biol. 122, 283-293.
68. Wiblin, A. E., Cui, W., Clark, A. J. and Bickmore, W. A. (2005). Distinctive nuclear organisation of centromeres and regions involved in pluripotency in human embryonic stem cells. J. Cell Sci. 118, 3861-3868.
69. Williams, R. R., Azuara, V., Perry, P., Sauer, S., Dvorkina, M., Jorgensen, H., Roix, J., McQueen, P., Misteli, T., Merkenschlager, M. et al. (2006). Neural induction promotes large-scale chromatin reorganisation of the Mash1 locus. J. Cell Sci. 119, 132-140.
70. Xing, Y., Johnson, C. V., Dobner, P. and Lawrence, J. B. (1993). Differential nuclear distribution of intron and exon sequences for endogenous RNAs revealed by fluorescence in situ hybridization. Science 259, 1326-1330.
71. Yuan, H., Corbi, N., Basilico, C. and Dailey, L. (1995). Developmental-specific activity of the FGF-4 enhancer requires the synergistic action of Sox2 and Oct-3. Genes Dev. 9, 2635-2645.
72. Zhao, S., Nichols, J., Smith, A. G. and Li, M. (2004). SoxB transcription factors specify neuroectodermal lineage choice in ES cells. Mol. Cell Neurosci. 27, 332-342.
73. Zhao, X. D., Han, X., Chew, J. L., Liu, J., Chiu, K. P., Choo, A., Orlov, Y. L., Sung, W. K., Shahab, A., Kuznetsov, V. A. et al. (2007). Whole-genome mapping of histone H3 Lys4 and 27 trimethylations reveals distinct genomic compartments in human embryonic stem cells. Cell Stem Cell 1, 286-298.
74. Zink, D., Amaral, M. D., Englmann, A., Lang, S., Clarke, L. A., Rudolph, C., Alt, F., Luther, K., Braz, C., Sadoni, N. et al. (2004). Transcription-dependent spatial arrangements of CFTR and adjacent genes in human cell nuclei. J. Cell Biol. 166, 815-825.