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 Solovei
Article

Abstract

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).

Keywords

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 

Abbreviations

B1

Abundant mouse SINE repeat family

CKO

Conditional knockout

DAPI

4′,6-diamidino-2-phenylindole

DNMT1

DNA (cytosine-5)-methyltransferase 1

DOP-PCR

Degenerate oligonucleotide-primed PCR

ES cells

Embryonic stem cells

FISH

Fluorescence in situ hybridization

G9a

H3K9 methyltransferase

GCL

Ganglion cell layer

HP1

Heterochromatin binding protein 1

INL

Inner nuclear layer

KMTase

Histone-lysine N-methyltransferase

L1

Abundant mouse LINE repeat family

LBR

Lamin B receptor

LINE

Long interspersed nuclear elements

5mc

5-methylcytosine

5hmc

5-hydroxymethylcytosine

MSR

Major satellite repeat

RNA Pol-II CTDx

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

SEM

Scanning electron microscopy

SINE

Short interspersed nuclear elements

TEM

Transmission electron microscopy

Xa

X active chromosome

Xi

X inactive chromosome

Xist

X inactive specific transcript

Supplementary material

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

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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
  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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