Live imaging of chromatin distribution reveals novel principles of nuclear architecture and chromatin compartmentalization

Daria Amiad-Pavlov; Dana Lorber; Gaurav Bajpai; Adriana Reuveny; Francesco Roncato; Ronen Alon; Samuel Safran; Talila Volk

doi:10.1126/sciadv.abf6251

Live imaging of chromatin distribution reveals novel principles of nuclear architecture and chromatin compartmentalization

Daria Amiad-Pavlov, Dana Lorber, Gaurav Bajpai, Adriana Reuveny, Francesco Roncato, Ronen Alon, Samuel Safran, Talila Volk^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

40 Citations (Scopus)

Abstract

The three-dimensional organization of chromatin contributes to transcriptional control, but information about native chromatin distribution is limited. Imaging chromatin in live Drosophila larvae, with preserved nuclear volume, revealed that active and repressed chromatin separates from the nuclear interior and forms a peripheral layer underneath the nuclear lamina. This is in contrast to the current view that chromatin distributes throughout the nucleus. Furthermore, peripheral chromatin organization was observed in distinct Drosophila tissues, as well as in live human effector T lymphocytes and neutrophils. Lamin A/C up-regulation resulted in chromatin collapse toward the nuclear center and correlated with a significant reduction in the levels of active chromatin. Physical modeling suggests that binding of lamina-associated domains combined with chromatin self-attractive interactions recapitulate the experimental chromatin distribution profiles. Together, our findings reveal a novel mode of mesoscale organization of peripheral chromatin sensitive to lamina composition, which is evolutionary conserved.

Original language	English
Article number	eabf6251
Journal	Science Advances
Volume	7
Issue number	23
DOIs	https://doi.org/10.1126/sciadv.abf6251
Publication status	Published - 2 Jun 2021

Funding

We thank K. Hiroshi (Osaka University, Japan), K. Furukawa (Niigata University, Japan), and the Bloomington Stock Center for providing fly lines. We are grateful to D. Deviri and O. Cohen from the Department of Chemical and Biological Physics, Weizmann Institute of Science for discussions and support. The images in this paper were acquired at the Advanced Optical Imaging Unit, de Picciotto-Lesser Cell Observatory unit, at the Moross Integrated Cancer Center Life Science Core Facilities, Weizmann Institute of Science. We thank M. Shemesh and Y. Addadi for advising on image acquisition, O. Golani for advising on imaging analysis, and R. Rotkopf for statistical analysis, all from the Life Sciences Core Facility, Weizmann Institute. Special thanks to M. Abbate from Arivis V4D support team for incorporating custom Python script for 3D radial shells. We are grateful to G. Ankaoua and B. Pasmantirer from the Physics Core Facilities at Weizmann Institute for helping in the design of the live imaging device. We thank D. Antes (DAntes Scientific Illustration) for the schematic model illustration. Funding: This study was supported by grants from “The French Muscular Dystrophy Association (AFM-Téléthon)” grant no. 22339, NSF-BSF (BSF grant no. 2016738), Israel Science Foundation (ISF) grant no. 750/17 awarded to T.V., Weizmann Krenter-Katz Interdisciplinary Research at the Interfaces of Life and Exact Sciences awarded to T.V. and S.S., and Tandem Call Weizmann–PIC3i Curie 2019-2021. R.A.’s research was supported by ISF grant no. 791/17.

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title = "Live imaging of chromatin distribution reveals novel principles of nuclear architecture and chromatin compartmentalization",

abstract = "The three-dimensional organization of chromatin contributes to transcriptional control, but information about native chromatin distribution is limited. Imaging chromatin in live Drosophila larvae, with preserved nuclear volume, revealed that active and repressed chromatin separates from the nuclear interior and forms a peripheral layer underneath the nuclear lamina. This is in contrast to the current view that chromatin distributes throughout the nucleus. Furthermore, peripheral chromatin organization was observed in distinct Drosophila tissues, as well as in live human effector T lymphocytes and neutrophils. Lamin A/C up-regulation resulted in chromatin collapse toward the nuclear center and correlated with a significant reduction in the levels of active chromatin. Physical modeling suggests that binding of lamina-associated domains combined with chromatin self-attractive interactions recapitulate the experimental chromatin distribution profiles. Together, our findings reveal a novel mode of mesoscale organization of peripheral chromatin sensitive to lamina composition, which is evolutionary conserved.",

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Live imaging of chromatin distribution reveals novel principles of nuclear architecture and chromatin compartmentalization

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