Nuclear Architecture of Rod Photoreceptor Cells Adapts to Vision in Mammalian Evolution

We show that the nuclear architecture of rod photoreceptor cells differs fundamentally in nocturnal and diurnal mammals. The rods of diurnal retinas possess the conventional architecture found in nearly all eukaryotic cells, with most heterochromatin situated at the nuclear periphery and euchromatin...

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Published inCell Vol. 137; no. 2; pp. 356 - 368
Main Authors Solovei, Irina, Kreysing, Moritz, Lanctôt, Christian, Kösem, Süleyman, Peichl, Leo, Cremer, Thomas, Guck, Jochen, Joffe, Boris
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 17.04.2009
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Abstract We show that the nuclear architecture of rod photoreceptor cells differs fundamentally in nocturnal and diurnal mammals. The rods of diurnal retinas possess the conventional architecture found in nearly all eukaryotic cells, with most heterochromatin situated at the nuclear periphery and euchromatin residing toward the nuclear interior. The rods of nocturnal retinas have a unique inverted pattern, where heterochromatin localizes in the nuclear center, whereas euchromatin, as well as nascent transcripts and splicing machinery, line the nuclear border. The inverted pattern forms by remodeling of the conventional one during terminal differentiation of rods. The inverted rod nuclei act as collecting lenses, and computer simulations indicate that columns of such nuclei channel light efficiently toward the light-sensing rod outer segments. Comparison of the two patterns suggests that the conventional architecture prevails in eukaryotic nuclei because it results in more flexible chromosome arrangements, facilitating positional regulation of nuclear functions.
AbstractList We show that the nuclear architecture of rod photoreceptor cells differs fundamentally in nocturnal and diurnal mammals. The rods of diurnal retinas possess the conventional architecture found in nearly all eukaryotic cells, with most heterochromatin situated at the nuclear periphery and euchromatin residing toward the nuclear interior. The rods of nocturnal retinas have a unique inverted pattern, where heterochromatin localizes in the nuclear center, whereas euchromatin, as well as nascent transcripts and splicing machinery, line the nuclear border. The inverted pattern forms by remodeling of the conventional one during terminal differentiation of rods. The inverted rod nuclei act as collecting lenses, and computer simulations indicate that columns of such nuclei channel light efficiently toward the light-sensing rod outer segments. Comparison of the two patterns suggests that the conventional architecture prevails in eukaryotic nuclei because it results in more flexible chromosome arrangements, facilitating positional regulation of nuclear functions.
Author Cremer, Thomas
Solovei, Irina
Guck, Jochen
Lanctôt, Christian
Kösem, Süleyman
Peichl, Leo
Kreysing, Moritz
Joffe, Boris
Author_xml – sequence: 1
  givenname: Irina
  surname: Solovei
  fullname: Solovei, Irina
  organization: Division of Anthropology and Human Genetics, Biocenter, Ludwig-Maximilians University Munich, Grosshadernerstrasse 2, 82152 Planegg-Martinsried, Germany
– sequence: 2
  givenname: Moritz
  surname: Kreysing
  fullname: Kreysing, Moritz
  organization: Department of Physics, Cavendish Laboratory, University of Cambridge, J.J. Thomson Avenue, Cambridge CB3 0HE, UK
– sequence: 3
  givenname: Christian
  surname: Lanctôt
  fullname: Lanctôt, Christian
  organization: Division of Anthropology and Human Genetics, Biocenter, Ludwig-Maximilians University Munich, Grosshadernerstrasse 2, 82152 Planegg-Martinsried, Germany
– sequence: 4
  givenname: Süleyman
  surname: Kösem
  fullname: Kösem, Süleyman
  organization: Division of Anthropology and Human Genetics, Biocenter, Ludwig-Maximilians University Munich, Grosshadernerstrasse 2, 82152 Planegg-Martinsried, Germany
– sequence: 5
  givenname: Leo
  surname: Peichl
  fullname: Peichl, Leo
  organization: Max Planck Institute for Brain Research, Deutschordenstrasse 46, D-60528 Frankfurt am Main, Germany
– sequence: 6
  givenname: Thomas
  surname: Cremer
  fullname: Cremer, Thomas
  organization: Division of Anthropology and Human Genetics, Biocenter, Ludwig-Maximilians University Munich, Grosshadernerstrasse 2, 82152 Planegg-Martinsried, Germany
– sequence: 7
  givenname: Jochen
  surname: Guck
  fullname: Guck, Jochen
  email: jg473@cam.ac.uk
  organization: Department of Physics, Cavendish Laboratory, University of Cambridge, J.J. Thomson Avenue, Cambridge CB3 0HE, UK
– sequence: 8
  givenname: Boris
  surname: Joffe
  fullname: Joffe, Boris
  email: boris.joffe@lrz.uni-muenchen.de
  organization: Division of Anthropology and Human Genetics, Biocenter, Ludwig-Maximilians University Munich, Grosshadernerstrasse 2, 82152 Planegg-Martinsried, Germany
BackLink https://www.ncbi.nlm.nih.gov/pubmed/19379699$$D View this record in MEDLINE/PubMed
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Snippet We show that the nuclear architecture of rod photoreceptor cells differs fundamentally in nocturnal and diurnal mammals. The rods of diurnal retinas possess...
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StartPage 356
SubjectTerms Animals
Animals, Outbred Strains
Biological Evolution
Cell Differentiation
Cell Nucleus - genetics
CELLBIO
DNA
Euchromatin
EVO_ECOL
Heterochromatin
Histones - metabolism
Mammals
Mice
Mice, Inbred C57BL
Retina - cytology
Retinal Rod Photoreceptor Cells - cytology
Retinal Rod Photoreceptor Cells - physiology
Vision, Ocular - physiology
Title Nuclear Architecture of Rod Photoreceptor Cells Adapts to Vision in Mammalian Evolution
URI https://dx.doi.org/10.1016/j.cell.2009.01.052
https://www.ncbi.nlm.nih.gov/pubmed/19379699
https://search.proquest.com/docview/20528568
https://search.proquest.com/docview/67144996
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