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

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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).

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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

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Acknowledgments

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.

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Authors and Affiliations

  1. Department of Biology II, Center for Integrated Protein Science Munich (CIPSM), Ludwig Maximilian University Munich, Grosshadernerstrasse 2, Planegg-Martinsried, 82152, Munich, Germany

    Anja Eberhart, Yana Feodorova, Congdi Song, Heinrich Leonhardt, Boris Joffe & Irina Solovei

  2. Department of Biology I, Biocenter, Ludwig Maximilian University Munich, Grosshadernerstrasse 2, Planegg-Martinsried, 82152, Munich, Germany

    Gerhard Wanner

  3. Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, 630090, Russia

    Elena Kiseleva

  4. Laboratory for Molecular and Developmental Biology, Institute for Protein Research, Osaka University, 3-2 Yamadaoka, Suita, Osaka, 565-0871, Japan

    Takahisa Furukawa

  5. Graduate School of Frontier Biosciences, Osaka University, 1-3 Yamadaoka, Suita, Osaka, 565-0871, Japan

    Hiroshi Kimura

  6. Center for Integrated Protein Science Munich (CIPSM) at the Adolf-Butenandt-Institute, Department of Molecular Biology, Ludwig Maximilian University Munich, 80336, Munich, Germany

    Gunnar Schotta

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  1. Anja Eberhart
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  2. Yana Feodorova
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  3. Congdi Song
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Correspondence to Irina Solovei.

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Responsible Editor: Dr. Beth Sullivan.

Anja Eberhart and Yana Feodorova contributed equally to this work.

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Eberhart, A., Feodorova, Y., Song, C. et al. Epigenetics of eu- and heterochromatin in inverted and conventional nuclei from mouse retina. Chromosome Res 21, 535–554 (2013). https://doi.org/10.1007/s10577-013-9375-7

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