CC2D1B Coordinates ESCRT-III Activity during the Mitotic Reformation of the Nuclear Envelope

Leandro N. Ventimiglia; Miguel Angel Cuesta-Geijo; Nicolas Martinelli; Anna Caballe; Pauline Macheboeuf; Nolwenn Miguet; Ian M. Parnham; Yolanda Olmos; Jeremy G. Carlton; Winfried Weissenhorn; Juan Martin-Serrano

doi:10.1016/j.devcel.2018.11.012

CC2D1B Coordinates ESCRT-III Activity during the Mitotic Reformation of the Nuclear Envelope

Leandro N. Ventimiglia, Miguel Angel Cuesta-Geijo, Nicolas Martinelli, Anna Caballe, Pauline Macheboeuf, Nolwenn Miguet, Ian M. Parnham, Yolanda Olmos, Jeremy G. Carlton, Winfried Weissenhorn, Juan Martin-Serrano

CNRS Centre National de la Recerche Scientifique

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

40 Citations (Scopus)

Abstract

© 2018 The Author(s) The coordinated reformation of the nuclear envelope (NE) after mitosis re-establishes the structural integrity and the functionality of the nuclear compartment. The endosomal sorting complex required for transport (ESCRT) machinery, a membrane remodeling pathway that is highly conserved in eukaryotes, has been recently involved in NE resealing by mediating the annular fusion of the nuclear membrane (NM). We show here that CC2D1B, a regulator of ESCRT polymerization, is required to re-establish the nuclear compartmentalization by coordinating endoplasmic reticulum (ER) membrane deposition around chromatin disks with ESCRT-III recruitment to the reforming NE. Accordingly, CC2D1B determines the spatiotemporal distribution of the CHMP7-ESCRT-III axis during NE reformation. Crucially, in CC2D1B-depleted cells, ESCRT activity is uncoupled from Spastin-mediated severing of spindle microtubules, resulting in persisting microtubules that compromise nuclear morphology. Therefore, we reveal CC2D1B as an essential regulatory factor that licenses the formation of ESCRT-III polymers to ensure the orderly reformation of the NE. A faithful reformation of the nuclear envelope after mitosis is critical to ensure the proper compartmentalization of the genetic material. Ventimiglia et al. identified CC2D1B as a key regulator of this process to ensure properly timed ESCRT-III machinery recruitment and licensing of ESCRT-III filaments for nuclear envelope resealing.

Original language	English
Pages (from-to)	547-563.e6
Journal	Developmental Cell
Volume	47
Issue number	5
Early online date	3 Dec 2018
DOIs	https://doi.org/10.1016/j.devcel.2018.11.012
Publication status	E-pub ahead of print - 3 Dec 2018

Keywords

ESCRT
microtubules
nuclear envelope
Spastin

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10.1016/j.devcel.2018.11.012

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title = "CC2D1B Coordinates ESCRT-III Activity during the Mitotic Reformation of the Nuclear Envelope",

abstract = "{\textcopyright} 2018 The Author(s) The coordinated reformation of the nuclear envelope (NE) after mitosis re-establishes the structural integrity and the functionality of the nuclear compartment. The endosomal sorting complex required for transport (ESCRT) machinery, a membrane remodeling pathway that is highly conserved in eukaryotes, has been recently involved in NE resealing by mediating the annular fusion of the nuclear membrane (NM). We show here that CC2D1B, a regulator of ESCRT polymerization, is required to re-establish the nuclear compartmentalization by coordinating endoplasmic reticulum (ER) membrane deposition around chromatin disks with ESCRT-III recruitment to the reforming NE. Accordingly, CC2D1B determines the spatiotemporal distribution of the CHMP7-ESCRT-III axis during NE reformation. Crucially, in CC2D1B-depleted cells, ESCRT activity is uncoupled from Spastin-mediated severing of spindle microtubules, resulting in persisting microtubules that compromise nuclear morphology. Therefore, we reveal CC2D1B as an essential regulatory factor that licenses the formation of ESCRT-III polymers to ensure the orderly reformation of the NE. A faithful reformation of the nuclear envelope after mitosis is critical to ensure the proper compartmentalization of the genetic material. Ventimiglia et al. identified CC2D1B as a key regulator of this process to ensure properly timed ESCRT-III machinery recruitment and licensing of ESCRT-III filaments for nuclear envelope resealing.",

keywords = "ESCRT, microtubules, nuclear envelope, Spastin",

author = "Ventimiglia, {Leandro N.} and Cuesta-Geijo, {Miguel Angel} and Nicolas Martinelli and Anna Caballe and Pauline Macheboeuf and Nolwenn Miguet and Parnham, {Ian M.} and Yolanda Olmos and Carlton, {Jeremy G.} and Winfried Weissenhorn and Juan Martin-Serrano",

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T1 - CC2D1B Coordinates ESCRT-III Activity during the Mitotic Reformation of the Nuclear Envelope

AU - Ventimiglia, Leandro N.

AU - Cuesta-Geijo, Miguel Angel

AU - Martinelli, Nicolas

AU - Caballe, Anna

AU - Macheboeuf, Pauline

AU - Miguet, Nolwenn

AU - Parnham, Ian M.

AU - Olmos, Yolanda

AU - Carlton, Jeremy G.

AU - Weissenhorn, Winfried

AU - Martin-Serrano, Juan

PY - 2018/12/3

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AB - © 2018 The Author(s) The coordinated reformation of the nuclear envelope (NE) after mitosis re-establishes the structural integrity and the functionality of the nuclear compartment. The endosomal sorting complex required for transport (ESCRT) machinery, a membrane remodeling pathway that is highly conserved in eukaryotes, has been recently involved in NE resealing by mediating the annular fusion of the nuclear membrane (NM). We show here that CC2D1B, a regulator of ESCRT polymerization, is required to re-establish the nuclear compartmentalization by coordinating endoplasmic reticulum (ER) membrane deposition around chromatin disks with ESCRT-III recruitment to the reforming NE. Accordingly, CC2D1B determines the spatiotemporal distribution of the CHMP7-ESCRT-III axis during NE reformation. Crucially, in CC2D1B-depleted cells, ESCRT activity is uncoupled from Spastin-mediated severing of spindle microtubules, resulting in persisting microtubules that compromise nuclear morphology. Therefore, we reveal CC2D1B as an essential regulatory factor that licenses the formation of ESCRT-III polymers to ensure the orderly reformation of the NE. A faithful reformation of the nuclear envelope after mitosis is critical to ensure the proper compartmentalization of the genetic material. Ventimiglia et al. identified CC2D1B as a key regulator of this process to ensure properly timed ESCRT-III machinery recruitment and licensing of ESCRT-III filaments for nuclear envelope resealing.

KW - ESCRT

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KW - Spastin

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JO - Developmental Cell

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ER -

CC2D1B Coordinates ESCRT-III Activity during the Mitotic Reformation of the Nuclear Envelope

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Keywords

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