Superresolution imaging reveals structurally distinct periodic patterns of chromatin along pachytene chromosomes

Stefan Redl, Sapun H. Parekh, René F. Ketting, Udo J. Birk, Christoph Cremer, Gerrit Best, Vijay K. Tiwari, Kikuë Tachibana-Konwalski, Kirti Prakash, David Fournier, Máté Borsos

Research output: Chapter in Book/Report/Conference proceedingChapter

22 Citations (Scopus)

Abstract

During meiosis, homologous chromosomes associate to form the synaptonemal complex (SC), a structure essential for fertility. Information about the epigenetic features of chromatin within this structure at the level of superresolution microscopy is largely lacking. We combined single-molecule localization microscopy (SMLM) with quantitative analytical methods to describe the epigenetic landscape of meiotic chromosomes at the pachytene stage in mouse oocytes. DNA is found to be nonrandomly distributed along the length of the SC in condensed clusters. Periodic clusters of repressive chromatin [trimethylation of histone H3 at lysine (Lys) 27 (H3K27me3)] are found at 500-nm intervals along the SC, whereas one of the ends of the SC displays a large and dense cluster of centromeric histone mark [trimethylation of histone H3 at Lys 9 (H3K9me3)]. Chromatin associated with active transcription [trimethylation of histone H3 at Lys 4 (H3K4me3)] is arranged in a radial hair-like loop pattern emerging laterally from the SC. These loops seem to be punctuated with small clusters of H3K4me3 with an average spread larger than their periodicity. Our findings indicate that the nanoscale structure of the pachytene chromosomes is constrained by periodic patterns of chromatin marks, whose function in recombination and higher order genome organization is yet to be elucidated.
Original languageEnglish
Title of host publicationProceedings of the National Academy of Sciences
PublisherProceedings of the National Academy of Sciences
Pages14635-14640
Number of pages6
ISBN (Print)10.1073/pnas.1516928112
DOIs
Publication statusPublished - 12 Nov 2015

Publication series

NameProceedings of the National Academy of Sciences
Volume112

Fingerprint

Synaptonemal Complex
Chromatin
Chromosomes
Histones
Lysine
Epigenomics
Histone Code
Pachytene Stage
Chromosome Structures
Meiosis
Periodicity
Hair
Genetic Recombination
Oocytes
Fertility
Microscopy
Genome
DNA

Cite this

Redl, S., Parekh, S. H., Ketting, R. F., Birk, U. J., Cremer, C., Best, G., ... Borsos, M. (2015). Superresolution imaging reveals structurally distinct periodic patterns of chromatin along pachytene chromosomes. In Proceedings of the National Academy of Sciences (pp. 14635-14640). (Proceedings of the National Academy of Sciences; Vol. 112). Proceedings of the National Academy of Sciences. https://doi.org/10.1073/pnas.1516928112
Redl, Stefan ; Parekh, Sapun H. ; Ketting, René F. ; Birk, Udo J. ; Cremer, Christoph ; Best, Gerrit ; Tiwari, Vijay K. ; Tachibana-Konwalski, Kikuë ; Prakash, Kirti ; Fournier, David ; Borsos, Máté. / Superresolution imaging reveals structurally distinct periodic patterns of chromatin along pachytene chromosomes. Proceedings of the National Academy of Sciences. Proceedings of the National Academy of Sciences, 2015. pp. 14635-14640 (Proceedings of the National Academy of Sciences).
@inbook{31872ebfd66544e581ee709d6b27334a,
title = "Superresolution imaging reveals structurally distinct periodic patterns of chromatin along pachytene chromosomes",
abstract = "During meiosis, homologous chromosomes associate to form the synaptonemal complex (SC), a structure essential for fertility. Information about the epigenetic features of chromatin within this structure at the level of superresolution microscopy is largely lacking. We combined single-molecule localization microscopy (SMLM) with quantitative analytical methods to describe the epigenetic landscape of meiotic chromosomes at the pachytene stage in mouse oocytes. DNA is found to be nonrandomly distributed along the length of the SC in condensed clusters. Periodic clusters of repressive chromatin [trimethylation of histone H3 at lysine (Lys) 27 (H3K27me3)] are found at 500-nm intervals along the SC, whereas one of the ends of the SC displays a large and dense cluster of centromeric histone mark [trimethylation of histone H3 at Lys 9 (H3K9me3)]. Chromatin associated with active transcription [trimethylation of histone H3 at Lys 4 (H3K4me3)] is arranged in a radial hair-like loop pattern emerging laterally from the SC. These loops seem to be punctuated with small clusters of H3K4me3 with an average spread larger than their periodicity. Our findings indicate that the nanoscale structure of the pachytene chromosomes is constrained by periodic patterns of chromatin marks, whose function in recombination and higher order genome organization is yet to be elucidated.",
author = "Stefan Redl and Parekh, {Sapun H.} and Ketting, {Ren{\'e} F.} and Birk, {Udo J.} and Christoph Cremer and Gerrit Best and Tiwari, {Vijay K.} and Kiku{\"e} Tachibana-Konwalski and Kirti Prakash and David Fournier and M{\'a}t{\'e} Borsos",
year = "2015",
month = "11",
day = "12",
doi = "10.1073/pnas.1516928112",
language = "English",
isbn = "10.1073/pnas.1516928112",
series = "Proceedings of the National Academy of Sciences",
publisher = "Proceedings of the National Academy of Sciences",
pages = "14635--14640",
booktitle = "Proceedings of the National Academy of Sciences",

}

Redl, S, Parekh, SH, Ketting, RF, Birk, UJ, Cremer, C, Best, G, Tiwari, VK, Tachibana-Konwalski, K, Prakash, K, Fournier, D & Borsos, M 2015, Superresolution imaging reveals structurally distinct periodic patterns of chromatin along pachytene chromosomes. in Proceedings of the National Academy of Sciences. Proceedings of the National Academy of Sciences, vol. 112, Proceedings of the National Academy of Sciences, pp. 14635-14640. https://doi.org/10.1073/pnas.1516928112

Superresolution imaging reveals structurally distinct periodic patterns of chromatin along pachytene chromosomes. / Redl, Stefan; Parekh, Sapun H.; Ketting, René F.; Birk, Udo J.; Cremer, Christoph; Best, Gerrit; Tiwari, Vijay K.; Tachibana-Konwalski, Kikuë; Prakash, Kirti; Fournier, David; Borsos, Máté.

Proceedings of the National Academy of Sciences. Proceedings of the National Academy of Sciences, 2015. p. 14635-14640 (Proceedings of the National Academy of Sciences; Vol. 112).

Research output: Chapter in Book/Report/Conference proceedingChapter

TY - CHAP

T1 - Superresolution imaging reveals structurally distinct periodic patterns of chromatin along pachytene chromosomes

AU - Redl, Stefan

AU - Parekh, Sapun H.

AU - Ketting, René F.

AU - Birk, Udo J.

AU - Cremer, Christoph

AU - Best, Gerrit

AU - Tiwari, Vijay K.

AU - Tachibana-Konwalski, Kikuë

AU - Prakash, Kirti

AU - Fournier, David

AU - Borsos, Máté

PY - 2015/11/12

Y1 - 2015/11/12

N2 - During meiosis, homologous chromosomes associate to form the synaptonemal complex (SC), a structure essential for fertility. Information about the epigenetic features of chromatin within this structure at the level of superresolution microscopy is largely lacking. We combined single-molecule localization microscopy (SMLM) with quantitative analytical methods to describe the epigenetic landscape of meiotic chromosomes at the pachytene stage in mouse oocytes. DNA is found to be nonrandomly distributed along the length of the SC in condensed clusters. Periodic clusters of repressive chromatin [trimethylation of histone H3 at lysine (Lys) 27 (H3K27me3)] are found at 500-nm intervals along the SC, whereas one of the ends of the SC displays a large and dense cluster of centromeric histone mark [trimethylation of histone H3 at Lys 9 (H3K9me3)]. Chromatin associated with active transcription [trimethylation of histone H3 at Lys 4 (H3K4me3)] is arranged in a radial hair-like loop pattern emerging laterally from the SC. These loops seem to be punctuated with small clusters of H3K4me3 with an average spread larger than their periodicity. Our findings indicate that the nanoscale structure of the pachytene chromosomes is constrained by periodic patterns of chromatin marks, whose function in recombination and higher order genome organization is yet to be elucidated.

AB - During meiosis, homologous chromosomes associate to form the synaptonemal complex (SC), a structure essential for fertility. Information about the epigenetic features of chromatin within this structure at the level of superresolution microscopy is largely lacking. We combined single-molecule localization microscopy (SMLM) with quantitative analytical methods to describe the epigenetic landscape of meiotic chromosomes at the pachytene stage in mouse oocytes. DNA is found to be nonrandomly distributed along the length of the SC in condensed clusters. Periodic clusters of repressive chromatin [trimethylation of histone H3 at lysine (Lys) 27 (H3K27me3)] are found at 500-nm intervals along the SC, whereas one of the ends of the SC displays a large and dense cluster of centromeric histone mark [trimethylation of histone H3 at Lys 9 (H3K9me3)]. Chromatin associated with active transcription [trimethylation of histone H3 at Lys 4 (H3K4me3)] is arranged in a radial hair-like loop pattern emerging laterally from the SC. These loops seem to be punctuated with small clusters of H3K4me3 with an average spread larger than their periodicity. Our findings indicate that the nanoscale structure of the pachytene chromosomes is constrained by periodic patterns of chromatin marks, whose function in recombination and higher order genome organization is yet to be elucidated.

UR - http://www.mendeley.com/research/superresolution-imaging-reveals-structurally-distinct-periodic-patterns-chromatin-along-pachytene-ch

U2 - 10.1073/pnas.1516928112

DO - 10.1073/pnas.1516928112

M3 - Chapter

C2 - 26561583

SN - 10.1073/pnas.1516928112

T3 - Proceedings of the National Academy of Sciences

SP - 14635

EP - 14640

BT - Proceedings of the National Academy of Sciences

PB - Proceedings of the National Academy of Sciences

ER -

Redl S, Parekh SH, Ketting RF, Birk UJ, Cremer C, Best G et al. Superresolution imaging reveals structurally distinct periodic patterns of chromatin along pachytene chromosomes. In Proceedings of the National Academy of Sciences. Proceedings of the National Academy of Sciences. 2015. p. 14635-14640. (Proceedings of the National Academy of Sciences). https://doi.org/10.1073/pnas.1516928112