Chromosome Research

, Volume 21, Issue 5, pp 535–554 | Cite as

Epigenetics of eu- and heterochromatin in inverted and conventional nuclei from mouse retina

  • Anja Eberhart
  • Yana Feodorova
  • Congdi Song
  • Gerhard Wanner
  • Elena Kiseleva
  • Takahisa Furukawa
  • Hiroshi Kimura
  • Gunnar Schotta
  • Heinrich Leonhardt
  • Boris Joffe
  • Irina SoloveiEmail author


To improve light propagation through the retina, the rod nuclei of nocturnal mammals are uniquely changed compared to the nuclei of other cells. In particular, the main classes of chromatin are segregated in them and form regular concentric shells in order; inverted in comparison to conventional nuclei. A broad study of the epigenetic landscape of the inverted and conventional mouse retinal nuclei indicated several differences between them and several features of general interest for the organization of the mammalian nuclei. In difference to nuclei with conventional architecture, the packing density of pericentromeric satellites and LINE-rich chromatin is similar in inverted rod nuclei; euchromatin has a lower packing density in both cases. A high global chromatin condensation in rod nuclei minimizes the structural difference between active and inactive X chromosome homologues. DNA methylation is observed primarily in the chromocenter, Dnmt1 is primarily associated with the euchromatic shell. Heterochromatin proteins HP1-alpha and HP1-beta localize in heterochromatic shells, whereas HP1-gamma is associated with euchromatin. For most of the 25 studied histone modifications, we observed predominant colocalization with a certain main chromatin class. Both inversions in rod nuclei and maintenance of peripheral heterochromatin in conventional nuclei are not affected by a loss or depletion of the major silencing core histone modifications in respective knock-out mice, but for different reasons. Maintenance of peripheral heterochromatin appears to be ensured by redundancy both at the level of enzymes setting the epigenetic code (writers) and the code itself, whereas inversion in rods rely on the absence of the peripheral heterochromatin tethers (absence of code readers).


Spatial organization of the nucleus Epigenetic code Core histones Histone modifications Peripheral heterochromatin LINE-rich chromatin SINE-rich chromatin X chromosome Retina Chromocenters DNMT1 HP1 



Abundant mouse SINE repeat family


Conditional knockout




DNA (cytosine-5)-methyltransferase 1


Degenerate oligonucleotide-primed PCR

ES cells

Embryonic stem cells


Fluorescence in situ hybridization


H3K9 methyltransferase


Ganglion cell layer


Heterochromatin binding protein 1


Inner nuclear layer


Histone-lysine N-methyltransferase


Abundant mouse LINE repeat family


Lamin B receptor


Long interspersed nuclear elements






Major satellite repeat


non-phosphorylated carboxy-terminal domain of RNA polymerase II

RNA Pol-II Ser2ph

Phosphorylated serine 2 of heptapeptide repeat on carboxy-terminal domain of RNA, polymerase II

RNA Pol-II Ser5ph

Phosphorylated serine 5 of heptapeptide repeat on carboxy-terminal domain of RNA, polymerase II


Scanning electron microscopy


Short interspersed nuclear elements


Transmission electron microscopy


X active chromosome


X inactive chromosome


X inactive specific transcript



We are grateful to Sandra Hake for anti-H3K56me3 antibody. This study was supported by DFG (SO1054 to IS, JO903 to BJ, HE1853 SFB/TR5 to HL). Work in the GS lab was funded by SFB-TR5 chromatin, SFB684, and BMBF. EK was supported by the Program for Basic Research of the RAS Presidium (6.12, Molecular and Cellular biology) and by a grant from the Russian Foundation for Basic Research. TF was supported by Takeda Science Foundation and Uehara Memorial Foundation. HK was supported by Grants-in-aid from the MEXT of Japan and JST, CREST.

Supplementary material

10577_2013_9375_MOESM1_ESM.doc (2 mb)
ESM 1 (DOC 2044 kb)


  1. Abe K, Naruse C, Kato T, Nishiuchi T, Saitou M, Asano M (2011) Loss of heterochromatin protein 1 gamma reduces the number of primordial germ cells via impaired cell cycle progression in mice. Biol Reprod 85:1013–1024PubMedCrossRefGoogle Scholar
  2. Almouzni G, Probst AV (2011) Heterochromatin maintenance and establishment: lessons from the mouse pericentromere. Nucleus 2:332–338PubMedCrossRefGoogle Scholar
  3. Bancaud A, Huet S, Daigle N, Mozziconacci J, Beaudouin J, Ellenberg J (2009) Molecular crowding affects diffusion and binding of nuclear proteins in heterochromatin and reveals the fractal organization of chromatin. Embo J 28:3785–3798PubMedCrossRefGoogle Scholar
  4. Black JC, Van Rechem C, Whetstine JR (2012) Histone lysine methylation dynamics: establishment, regulation, and biological impact. Mol Cell 48:491–507PubMedCrossRefGoogle Scholar
  5. Boyle S, Gilchrist S, Bridger JM, Mahy NL, Ellis JA, Bickmore WA (2001) The spatial organization of human chromosomes within the nuclei of normal and emerin-mutant cells. Hum Mol Genet 10:211–219PubMedCrossRefGoogle Scholar
  6. Carvalho C, Pereira HM, Ferreira J, Pina C, Mendonça D, Rosa AC, Carmo-Fonseca M (2001) Chromosomal G-dark bands determine the spatial organization of centromeric heterochromatin in the nucleus. Mol Biol Cell 12:3563–3572PubMedCrossRefGoogle Scholar
  7. Chandra T, Kirschner K, Thuret JY, Pope BD, Ryba T, Newman S, Ahmed K et al (2012) Independence of repressive histone marks and chromatin compaction during senescent heterochromatic layer formation. Mol Cell 47:203–214PubMedCrossRefGoogle Scholar
  8. Chen TL, Manuelidis L (1989) SINEs and LINEs cluster in distinct DNA fragments of Giemsa band size. Chromosoma 98:309–316PubMedCrossRefGoogle Scholar
  9. Cheutin T, McNairn AJ, Jenuwein T, Gilbert DM, Singh PB, Misteli T (2003) Maintenance of stable heterochromatin domains by dynamic HP1 binding. Science 299:721–725PubMedCrossRefGoogle Scholar
  10. Cremer M, Grasser F, Lanctot C, Muller S, Neusser M, Zinner R, Solovei I, Cremer T (2008) Multicolor 3D fluorescence in situ hybridization for imaging interphase chromosomes. Methods Mol Biol 463:205–239PubMedCrossRefGoogle Scholar
  11. Croft JA, Bridger JM, Boyle S, Perry P, Teague P, Bickmore WA (1999) Differences in the localization and morphology of chromosomes in the human nucleus. J Cell Biol 145:1119–1131PubMedCrossRefGoogle Scholar
  12. Dambacher S, Hahn M, Schotta G (2010) Epigenetic regulation of development by histone lysine methylation. J Hered (Edinb) 105:24–37CrossRefGoogle Scholar
  13. Eberhart A, Kimura H, Leonhardt H, Joffe B, Solovei I (2012) Reliable detection of epigenetic histone marks and nuclear proteins in tissue cryosections. Chromosome Res 20(7):849–858PubMedCrossRefGoogle Scholar
  14. Egelhofer TA, Minoda A, Klugman S, Lee K, Kolasinska-Zwierz P, Alekseyenko AA, Cheung MS et al (2011) An assessment of histone-modification antibody quality. Nat Struct Mol Biol 18:91–93PubMedCrossRefGoogle Scholar
  15. Gibcus JH, Dekker J (2013) The hierarchy of the 3D genome. Mol Cell 49:773–782PubMedCrossRefGoogle Scholar
  16. Gonzalez-Sandoval A, Towbin BD, Gasser SM (2013) The formation and sequestration of heterochromatin during development. Febs J 280(14):3212–3219PubMedCrossRefGoogle Scholar
  17. Hahn M, Dambacher S, Dulev S, Kuznetsova AY, Eck S, Worz S, Sadic D, Schulte M, Mallm JP, Maiser A, Debs P, von Melchner H, Leonhardt H, Schermelleh L, Rohr K, Rippe K, Storchova Z, Schotta G (2013) Suv4-20h2 mediates chromatin compaction and is important for cohesin recruitment to heterochromatin. Genes Dev 27:859–872PubMedCrossRefGoogle Scholar
  18. Hayashi-Takanaka Y, Yamagata K, Wakayama T, Stasevich TJ, Kainuma T, Tsurimoto T, Tachibana M, Shinkai Y, Kurumizaka H, Nozaki N, Kimura H (2011) Tracking epigenetic histone modifications in single cells using Fab-based live endogenous modification labeling. Nucleic Acids Res 39:6475–6488PubMedCrossRefGoogle Scholar
  19. Helmlinger D, Hardy S, Abou-Sleymane G, Eberlin A, Bowman AB, Gansmuller A, Picaud S, Zoghbi HY, Trottier Y, Tora L, Devys D (2006) Glutamine-expanded ataxin-7 alters TFTC/STAGA recruitment and chromatin structure leading to photoreceptor dysfunction. PLoS Biol 4:e67PubMedCrossRefGoogle Scholar
  20. Hirano Y, Hizume K, Kimura H, Takeyasu K, Haraguchi T, Hiraoka Y (2012) Lamin B receptor recognizes specific modifications of histone H4 in heterochromatin formation. J Biol Chem 287:42654–42663PubMedCrossRefGoogle Scholar
  21. Jack AP, Bussemer S, Hahn M, Punzeler S, Snyder M, Wells M, Csankovszki G, Solovei I, Schotta G, Hake SB (2013) H3K56me3 is a novel, conserved heterochromatic mark that largely but not completely overlaps with H3K9me3 in both regulation and localization. PLoS One 8:e51765PubMedCrossRefGoogle Scholar
  22. Joffe B, Leonhardt H, Solovei I (2010) Differentiation and large scale spatial organization of the genome. Curr Opin Genet Dev 20:562–569PubMedCrossRefGoogle Scholar
  23. Kadriu B, Guidotti A, Chen Y, Grayson DR (2012) DNA methyltransferases1 (DNMT1) and 3a (DNMT3a) colocalize with GAD67-positive neurons in the GAD67-GFP mouse brain. J Comp Neurol 520:1951–1964PubMedCrossRefGoogle Scholar
  24. Katoh K, Yamazaki R, Onishi A, Sanuki R, Furukawa T (2012) G9a histone methyltransferase activity in retinal progenitors is essential for proper differentiation and survival of mouse retinal cells. J Neurosci 32:17658–17670PubMedCrossRefGoogle Scholar
  25. Kimura H, Hayashi-Takanaka Y, Goto Y, Takizawa N, Nozaki N (2008) The organization of histone H3 modifications as revealed by a panel of specific monoclonal antibodies. Cell Struct Funct 33:61–73PubMedCrossRefGoogle Scholar
  26. Kind J, Pagie L, Ortabozkoyun H, Boyle S, de Vries SS, Janssen H, Amendola M, Nolen LD, Bickmore WA, van Steensel B (2013) Single-cell dynamics of genome-nuclear lamina interactions. Cell 153:178–192PubMedCrossRefGoogle Scholar
  27. Kiseleva E, Rutherford S, Cotter LM, Allen TD, Goldberg MW (2001) Steps of nuclear pore complex disassembly and reassembly during mitosis in early Drosophila embryos. J Cell Sci 114:3607–3618PubMedGoogle Scholar
  28. Kizilyaprak C, Spehner D, Devys D, Schultz P (2010) In vivo chromatin organization of mouse rod photoreceptors correlates with histone modifications. PLoS One 5:e11039PubMedCrossRefGoogle Scholar
  29. Kizilyaprak C, Spehner D, Devys D, Schultz P (2011) The linker histone H1C contributes to the SCA7 nuclear phenotype. Nucleus 2:444–454PubMedCrossRefGoogle Scholar
  30. Korenberg JR, Rykowski MC (1988) Human genome organization: Alu, lines, and the molecular structure of metaphase chromosome bands. Cell 53:391–400PubMedCrossRefGoogle Scholar
  31. Lienert F, Mohn F, Tiwari VK, Baubec T, Roloff TC, Gaidatzis D, Stadler MB, Schubeler D (2011) Genomic prevalence of heterochromatic H3K9me2 and transcription do not discriminate pluripotent from terminally differentiated cells. PLoS Genet 7:e1002090PubMedCrossRefGoogle Scholar
  32. Maison C, Bailly D, Roche D, Montes de Oca R, Probst AV, Vassias I, Dingli F, Lombard B, Loew D, Quivy JP, Almouzni G (2011) SUMOylation promotes de novo targeting of HP1alpha to pericentric heterochromatin. Nat Genet 43:220–227PubMedCrossRefGoogle Scholar
  33. Majumder S, Ghoshal K, Datta J, Smith DS, Bai S, Jacob ST (2006) Role of DNA methyltransferases in regulation of human ribosomal RNA gene transcription. J Biol Chem 281:22062–22072PubMedCrossRefGoogle Scholar
  34. Makatsori D, Kourmouli N, Polioudaki H, Shultz LD, McLean K, Theodoropoulos PA, Singh PB, Georgatos SD (2004) The inner nuclear membrane protein lamin B receptor forms distinct microdomains and links epigenetically marked chromatin to the nuclear envelope. J Biol Chem 279:25567–25573PubMedCrossRefGoogle Scholar
  35. Mehta IS, Bridger JM, Kill IR (2010) Progeria, the nucleolus and farnesyltransferase inhibitors. Biochem Soc Trans 38:287–291PubMedCrossRefGoogle Scholar
  36. Meister P, Towbin BD, Pike BL, Ponti A, Gasser SM (2010) The spatial dynamics of tissue-specific promoters during C. elegans development. Genes Dev 24:766–782PubMedCrossRefGoogle Scholar
  37. Mellén M, Ayata P, Dewell S, Kriaucionis S, Heintz N (2012) MeCP2 binds to 5hmC enriched within active genes and accessible chromatin in the nervous system. Cell 151:1417–1430PubMedCrossRefGoogle Scholar
  38. Nasonkin IO, Lazo K, Hambright D, Brooks M, Fariss R, Swaroop A (2011) Distinct nuclear localization patterns of DNA methyltransferases in developing and mature mammalian retina. J Comp Neurol 519:1914–1930PubMedCrossRefGoogle Scholar
  39. Nasonkin IO, Merbs SL, Lazo K, Oliver VF, Brooks M, Patel K, Enke RA, Nellissery J, Jamrich M, Le YZ, Bharti K, Fariss RN, Rachel RA, Zack DJ, Rodriguez-Boulan EJ, Swaroop A (2013) Conditional knockdown of DNA methyltransferase 1 reveals a key role of retinal pigment epithelium integrity in photoreceptor outer segment morphogenesis. Development 140:1330–1341PubMedCrossRefGoogle Scholar
  40. Pauler FM, Sloane MA, Huang R, Regha K, Koerner MV, Tamir I, Sommer A, Aszodi A, Jenuwein T, Barlow DP (2009) H3K27me3 forms BLOCs over silent genes and intergenic regions and specifies a histone banding pattern on a mouse autosomal chromosome. Genome Res 19:221–233PubMedCrossRefGoogle Scholar
  41. Peters AH, O’Carroll D, Scherthan H, Mechtler K, Sauer S, Schofer C, Weipoltshammer K, Pagani M, Lachner M, Kohlmaier A, Opravil S, Doyle M, Sibilia M, Jenuwein T (2001) Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107:323–337PubMedCrossRefGoogle Scholar
  42. Pinheiro I, Margueron R, Shukeir N, Eisold M, Fritzsch C, Richter FM, Mittler G, Genoud C, Goyama S, Kurokawa M, Son J, Reinberg D, Lachner M, Jenuwein T (2012) Prdm3 and Prdm16 are H3K9me1 methyltransferases required for mammalian heterochromatin integrity. Cell 150:948–960PubMedCrossRefGoogle Scholar
  43. Pinter SF, Sadreyev RI, Yildirim E, Jeon Y, Ohsumi TK, Borowsky M, Lee JT (2012) Spreading of X chromosome inactivation via a hierarchy of defined Polycomb stations. Genome Res 22:1864–1876PubMedCrossRefGoogle Scholar
  44. Popova EY, Grigoryev SA, Fan Y, Skoultchi AI, Zhang SS, Barnstable CJ (2013) Developmentally regulated linker histone h1c promotes heterochromatin condensation and mediates structural integrity of rod photoreceptors in mouse retina. J Biol Chem 288(24):17895–17907PubMedCrossRefGoogle Scholar
  45. Popova EY, Xu X, DeWan AT, Salzberg AC, Berg A, Hoh J, Zhang SS, Barnstable CJ (2012) Stage and gene specific signatures defined by histones H3K4me2 and H3K27me3 accompany mammalian retina maturation in vivo. PLoS One 7:e46867PubMedCrossRefGoogle Scholar
  46. Probst AV, Okamoto I, Casanova M, El Marjou F, Le Baccon P, Almouzni G (2010) A strand-specific burst in transcription of pericentric satellites is required for chromocenter formation and early mouse development. Dev Cell 19:625–638PubMedCrossRefGoogle Scholar
  47. Rao RC, Tchedre KT, Malik MT, Coleman N, Fang Y, Marquez VE, Chen DF (2010) Dynamic patterns of histone lysine methylation in the developing retina. Invest Ophthalmol Vis Sci 51:6784–6792PubMedCrossRefGoogle Scholar
  48. Reese BE, Tan SS (1998) Clonal boundary analysis in the developing retina using X-inactivation transgenic mosaic mice. Semin Cell Dev Biol 9:285–292PubMedCrossRefGoogle Scholar
  49. Rhee KD, Yu J, Zhao CY, Fan G, Yang XJ (2012) Dnmt1-dependent DNA methylation is essential for photoreceptor terminal differentiation and retinal neuron survival. Cell Death Dis 3:e427PubMedCrossRefGoogle Scholar
  50. Ronneberger O, Baddeley D, Scheipl F, Verveer PJ, Burkhardt H, Cremer C, Fahrmeir L, Cremer T, Joffe B (2008) Spatial quantitative analysis of fluorescently labeled nuclear structures: problems, methods, pitfalls. Chromosome Res 16:523–562PubMedCrossRefGoogle Scholar
  51. Saint-Andre V, Batsche E, Rachez C, Muchardt C (2011) Histone H3 lysine 9 trimethylation and HP1gamma favor inclusion of alternative exons. Nat Struct Mol Biol 18:337–344PubMedCrossRefGoogle Scholar
  52. Schotta G, Lachner M, Sarma K, Ebert A, Sengupta R, Reuter G, Reinberg D, Jenuwein T (2004) A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev 18:1251–1262PubMedCrossRefGoogle Scholar
  53. Schotta G, Sengupta R, Kubicek S, Malin S, Kauer M, Callen E, Celeste A, Pagani M, Opravil S, De La Rosa-Velazquez IA, Espejo A, Bedford MT, Nussenzweig A, Busslinger M, Jenuwein T (2008) A chromatin-wide transition to H4K20 monomethylation impairs genome integrity and programmed DNA rearrangements in the mouse. Genes Dev 22:2048–2061PubMedCrossRefGoogle Scholar
  54. She SR, Cote RJ, Taylor CR (1997) Antigen retrieval immunohistochemistry: past, present, and future. J Histochem Cytochem 45:327–343CrossRefGoogle Scholar
  55. She SR, Cote RJ, Taylor CR (2001) Antigen retrieval techniques: current perspectives. J Histochem Cytochem 49:931–937CrossRefGoogle Scholar
  56. Shinkai Y, Tachibana M (2011) H3K9 methyltransferase G9a and the related molecule GLP. Genes Dev 25:781–788PubMedCrossRefGoogle Scholar
  57. Siegert S, Cabuy E, Scherf BG, Kohler H, Panda S, Le YZ, Fehling HJ, Gaidatzis D, Stadler MB, Roska B (2012) Transcriptional code and disease map for adult retinal cell types. Nat Neurosci 15(487–495):S481–S482Google Scholar
  58. Solovei I (2010) Fluorescence in situ hybridization (FISH) on tissue cryosections. Methods Mol Biol 659:71–82PubMedCrossRefGoogle Scholar
  59. Solovei I, Kreysing M, Lanctot C, Kosem S, Peichl L, Cremer T, Guck J, Joffe B (2009) Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution. Cell 137:356–368PubMedCrossRefGoogle Scholar
  60. Solovei I, Wang AS, Thanisch K, Schmidt CS, Krebs S, Zwerger M, Cohen TV, Devys D, Foisner R, Peichl L, Herrmann H, Blum H, Engelkamp D, Stewart CL, Leonhardt H, Joffe B (2013) LBR and Lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell 152:584–598PubMedCrossRefGoogle Scholar
  61. Tachibana M, Matsumura Y, Fukuda M, Kimura H, Shinkai Y (2008) G9a/GLP complexes independently mediate H3K9 and DNA methylation to silence transcription. Embo J 27:2681–2690PubMedCrossRefGoogle Scholar
  62. Tachibana M, Sugimoto K, Nozaki M, Ueda J, Ohta T, Ohki M, Fukuda M, Takeda N, Niida H, Kato H, Shinkai Y (2002) G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev 16:1779–1791PubMedCrossRefGoogle Scholar
  63. Tan M, Luo H, Lee S, Jin F, Yang JS, Montellier E, Buchou T, Cheng Z, Rousseaux S, Rajagopal N, Lu Z, Ye Z, Zhu Q, Wysocka J, Ye Y, Khochbin S, Ren B, Zhao Y (2011) Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 146:1016–1028PubMedCrossRefGoogle Scholar
  64. Terrenoire E, McRonald F, Halsall JA, Page P, Illingworth RS, Taylor AM, Davison V, O’Neill LP, Turner BM (2010) Immunostaining of modified histones defines high-level features of the human metaphase epigenome. Genome Biol 11:R110PubMedCrossRefGoogle Scholar
  65. Towbin BD, Gonzalez-Aguilera C, Sack R, Gaidatzis D, Kalck V, Meister P, Askjaer P, Gasser SM (2012) Step-wise methylation of histone H3K9 positions heterochromatin at the nuclear periphery. Cell 150:934–947PubMedCrossRefGoogle Scholar
  66. Towbin BD, Meister P, Pike BL, Gasser SM (2010) Repetitive transgenes in C. elegans accumulate heterochromatic marks and are sequestered at the nuclear envelope in a copy-number- and lamin-dependent manner. Cold Spring Harb Symp Quant Biol 75:555–565PubMedCrossRefGoogle Scholar
  67. Vakoc CR, Mandat SA, Olenchock BA, Blobel GA (2005) Histone H3 lysine 9 methylation and HP1gamma are associated with transcription elongation through mammalian chromatin. Mol Cell 19:381–391PubMedCrossRefGoogle Scholar
  68. Vogel MJ, Guelen L, de Wit E, Peric-Hupkes D, Lodén M, Talhout W, Feenstra M, Abbas B, Classen AK, van Steensel B (2006) Human heterochromatin proteins form large domains containing KRAB-ZNF genes. Genome Res 16:1493–1504PubMedCrossRefGoogle Scholar
  69. Walter J, Joffe B, Bolzer A, Albiez H, Benedetti PA, Muller S, Speicher MR, Cremer T, Cremer M, Solovei I (2006) Towards many colors in FISH on 3D-preserved interphase nuclei. Cytogenet Genome Res 114:367–378PubMedCrossRefGoogle Scholar
  70. Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, Cui K, Roh TY, Peng W, Zhang MQ, Zhao K (2008) Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 40:897–903PubMedCrossRefGoogle Scholar
  71. Xhemalce B, Kouzarides T (2010) A chromodomain switch mediated by histone H3 Lys 4 acetylation regulates heterochromatin assembly. Genes Dev 24:647–652PubMedCrossRefGoogle Scholar
  72. Yamamizu K, Fujihara M, Tachibana M, Katayama S, Takahashi A, Hara E, Imai H, Shinkai Y, Yamashita JK (2012) Protein kinase A determines timing of early differentiation through epigenetic regulation with G9a. Cell Stem Cell 10:759–770PubMedCrossRefGoogle Scholar
  73. Zalokar M, Erk I (1977) Phase-partition fixation and staining of Drosophila eggs. Stain Technol 52:89–95PubMedGoogle Scholar
  74. Zheng MH, Shi M, Pei Z, Gao F, Han H, Ding YQ (2009) The transcription factor RBP-J is essential for retinal cell differentiation and lamination. Mol Brain 2:38PubMedCrossRefGoogle Scholar
  75. Zhu J, Adli M, Zou JY, Verstappen G, Coyne M, Zhang X, Durham T, Miri M, Deshpande V, De Jager PL, Bennett DA, Houmard JA, Muoio DM, Onder TT, Camahort R, Cowan CA, Meissner A, Epstein CB, Shoresh N, Bernstein BE (2013) Genome-wide chromatin state transitions associated with developmental and environmental cues. Cell 152:642–654PubMedCrossRefGoogle Scholar
  76. Zullo JM, Demarco IA, Pique-Regi R, Gaffney DJ, Epstein CB, Spooner CJ, Luperchio TR, Bernstein BE, Pritchard JK, Reddy KL, Singh H (2012) DNA sequence-dependent compartmentalization and silencing of chromatin at the nuclear lamina. Cell 149:1474–1487PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Anja Eberhart
    • 1
  • Yana Feodorova
    • 1
  • Congdi Song
    • 1
  • Gerhard Wanner
    • 2
  • Elena Kiseleva
    • 3
  • Takahisa Furukawa
    • 4
  • Hiroshi Kimura
    • 5
  • Gunnar Schotta
    • 6
  • Heinrich Leonhardt
    • 1
  • Boris Joffe
    • 1
  • Irina Solovei
    • 1
    Email author
  1. 1.Department of Biology II, Center for Integrated Protein Science Munich (CIPSM)Ludwig Maximilian University MunichMunichGermany
  2. 2.Department of Biology I, BiocenterLudwig Maximilian University MunichMunichGermany
  3. 3.Institute of Cytology and GeneticsSiberian Branch of the Russian Academy of SciencesNovosibirskRussia
  4. 4.Laboratory for Molecular and Developmental Biology, Institute for Protein ResearchOsaka UniversitySuitaJapan
  5. 5.Graduate School of Frontier BiosciencesOsaka UniversitySuitaJapan
  6. 6.Center for Integrated Protein Science Munich (CIPSM) at the Adolf-Butenandt-Institute, Department of Molecular BiologyLudwig Maximilian University MunichMunichGermany

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