Acute depletion of diacylglycerol from the cis-Golgi affects localized nuclear envelope morphology during mitosis

Gary Hong Chun Chung, Marie-Charlotte Domart, Christopher Peddie, Judith Mantell, Kieran Mclaverty, Angela Arabiotorre, Lorna Hodgson, Richard D Byrne, Paul Verkade, Kenton Arkill, Lucy M Collinson, Banafshé Larijani

Research output: Contribution to journalArticle

Abstract

Dysregulation of nuclear envelope (NE) assembly results in various cancers; for example, renal and some lung carcinomas ensue due to NE malformation. The NE is a dynamic membrane compartment and its completion during mitosis is a highly regulated process, but the detailed mechanism still remains incompletely understood. Previous studies have found that isolated diacylglycerol (DAG)-containing vesicles are essential for completing the fusion of the NE in non-somatic cells. We investigated the impact of DAG depletion from the cis-Golgi in mammalian cells on NE reassembly. Using advanced electron microscopy, we observed an enriched DAG population of vesicles at the vicinity of the NE gaps of telophase mammalian cells. We applied a mini singlet oxygen generator-C1-domain tag that localized DAG-enriched vesicles at the perinuclear region, which suggested the existence of NE fusogenic vesicles. We quantified the impact of Golgi-DAG depletion by measuring the in situ NE rim curvature of the reforming NE. The rim curvature in these cells was significantly reduced compared with controls, which indicated a localized defect in NE morphology. Our novel results demonstrate the significance of the role of DAG from the cis-Golgi for the regulation of NE assembly.—Chung, G. H. C., M-C. Domart, C. Peddie, J. Mantell, K. Mclaverty, A. Arabiotorre, L. Hodgson, R. D. Byrne, P. Verkade, K. Arkill, L. M. Collinson, and B. Larijani. Acute depletion of diacylglycerol from the cis-Golgi affects localized nuclear envelope morphology during mitosis.

Original languageEnglish
Pages (from-to)1402-1413
Number of pages12
JournalJournal of Lipid Research
Volume59
Issue number8
Early online date12 Jun 2018
DOIs
Publication statusPublished - 1 Aug 2018

Keywords

  • Correlative light electron microscopy
  • Membrane curvature
  • Serial block face scanning electron microscopy

ASJC Scopus subject areas

  • Biochemistry
  • Endocrinology
  • Cell Biology

Cite this

Acute depletion of diacylglycerol from the cis-Golgi affects localized nuclear envelope morphology during mitosis. / Chung, Gary Hong Chun; Domart, Marie-Charlotte; Peddie, Christopher; Mantell, Judith; Mclaverty, Kieran; Arabiotorre, Angela; Hodgson, Lorna; Byrne, Richard D; Verkade, Paul; Arkill, Kenton; Collinson, Lucy M; Larijani, Banafshé.

In: Journal of Lipid Research, Vol. 59, No. 8, 01.08.2018, p. 1402-1413.

Research output: Contribution to journalArticle

Chung, GHC, Domart, M-C, Peddie, C, Mantell, J, Mclaverty, K, Arabiotorre, A, Hodgson, L, Byrne, RD, Verkade, P, Arkill, K, Collinson, LM & Larijani, B 2018, 'Acute depletion of diacylglycerol from the cis-Golgi affects localized nuclear envelope morphology during mitosis', Journal of Lipid Research, vol. 59, no. 8, pp. 1402-1413. https://doi.org/10.1194/jlr.M083899
Chung, Gary Hong Chun ; Domart, Marie-Charlotte ; Peddie, Christopher ; Mantell, Judith ; Mclaverty, Kieran ; Arabiotorre, Angela ; Hodgson, Lorna ; Byrne, Richard D ; Verkade, Paul ; Arkill, Kenton ; Collinson, Lucy M ; Larijani, Banafshé. / Acute depletion of diacylglycerol from the cis-Golgi affects localized nuclear envelope morphology during mitosis. In: Journal of Lipid Research. 2018 ; Vol. 59, No. 8. pp. 1402-1413.
@article{fe91cc8ec4524963bdc2d91e607d102f,
title = "Acute depletion of diacylglycerol from the cis-Golgi affects localized nuclear envelope morphology during mitosis",
abstract = "Dysregulation of nuclear envelope (NE) assembly results in various cancers; for example, renal and some lung carcinomas ensue due to NE malformation. The NE is a dynamic membrane compartment and its completion during mitosis is a highly regulated process, but the detailed mechanism still remains incompletely understood. Previous studies have found that isolated diacylglycerol (DAG)-containing vesicles are essential for completing the fusion of the NE in non-somatic cells. We investigated the impact of DAG depletion from the cis-Golgi in mammalian cells on NE reassembly. Using advanced electron microscopy, we observed an enriched DAG population of vesicles at the vicinity of the NE gaps of telophase mammalian cells. We applied a mini singlet oxygen generator-C1-domain tag that localized DAG-enriched vesicles at the perinuclear region, which suggested the existence of NE fusogenic vesicles. We quantified the impact of Golgi-DAG depletion by measuring the in situ NE rim curvature of the reforming NE. The rim curvature in these cells was significantly reduced compared with controls, which indicated a localized defect in NE morphology. Our novel results demonstrate the significance of the role of DAG from the cis-Golgi for the regulation of NE assembly.—Chung, G. H. C., M-C. Domart, C. Peddie, J. Mantell, K. Mclaverty, A. Arabiotorre, L. Hodgson, R. D. Byrne, P. Verkade, K. Arkill, L. M. Collinson, and B. Larijani. Acute depletion of diacylglycerol from the cis-Golgi affects localized nuclear envelope morphology during mitosis.",
keywords = "Correlative light electron microscopy, Membrane curvature, Serial block face scanning electron microscopy",
author = "Chung, {Gary Hong Chun} and Marie-Charlotte Domart and Christopher Peddie and Judith Mantell and Kieran Mclaverty and Angela Arabiotorre and Lorna Hodgson and Byrne, {Richard D} and Paul Verkade and Kenton Arkill and Collinson, {Lucy M} and Banafsh{\'e} Larijani",
note = "Copyright {\circledC} 2018 Chung et al. Published under exclusive license by The American Society for Biochemistry and Molecular Biology, Inc.",
year = "2018",
month = "8",
day = "1",
doi = "10.1194/jlr.M083899",
language = "English",
volume = "59",
pages = "1402--1413",
journal = "Journal of Lipid Research",
issn = "0022-2275",
publisher = "American Society for Biochemistry and Molecular Biology Inc.",
number = "8",

}

TY - JOUR

T1 - Acute depletion of diacylglycerol from the cis-Golgi affects localized nuclear envelope morphology during mitosis

AU - Chung, Gary Hong Chun

AU - Domart, Marie-Charlotte

AU - Peddie, Christopher

AU - Mantell, Judith

AU - Mclaverty, Kieran

AU - Arabiotorre, Angela

AU - Hodgson, Lorna

AU - Byrne, Richard D

AU - Verkade, Paul

AU - Arkill, Kenton

AU - Collinson, Lucy M

AU - Larijani, Banafshé

N1 - Copyright © 2018 Chung et al. Published under exclusive license by The American Society for Biochemistry and Molecular Biology, Inc.

PY - 2018/8/1

Y1 - 2018/8/1

N2 - Dysregulation of nuclear envelope (NE) assembly results in various cancers; for example, renal and some lung carcinomas ensue due to NE malformation. The NE is a dynamic membrane compartment and its completion during mitosis is a highly regulated process, but the detailed mechanism still remains incompletely understood. Previous studies have found that isolated diacylglycerol (DAG)-containing vesicles are essential for completing the fusion of the NE in non-somatic cells. We investigated the impact of DAG depletion from the cis-Golgi in mammalian cells on NE reassembly. Using advanced electron microscopy, we observed an enriched DAG population of vesicles at the vicinity of the NE gaps of telophase mammalian cells. We applied a mini singlet oxygen generator-C1-domain tag that localized DAG-enriched vesicles at the perinuclear region, which suggested the existence of NE fusogenic vesicles. We quantified the impact of Golgi-DAG depletion by measuring the in situ NE rim curvature of the reforming NE. The rim curvature in these cells was significantly reduced compared with controls, which indicated a localized defect in NE morphology. Our novel results demonstrate the significance of the role of DAG from the cis-Golgi for the regulation of NE assembly.—Chung, G. H. C., M-C. Domart, C. Peddie, J. Mantell, K. Mclaverty, A. Arabiotorre, L. Hodgson, R. D. Byrne, P. Verkade, K. Arkill, L. M. Collinson, and B. Larijani. Acute depletion of diacylglycerol from the cis-Golgi affects localized nuclear envelope morphology during mitosis.

AB - Dysregulation of nuclear envelope (NE) assembly results in various cancers; for example, renal and some lung carcinomas ensue due to NE malformation. The NE is a dynamic membrane compartment and its completion during mitosis is a highly regulated process, but the detailed mechanism still remains incompletely understood. Previous studies have found that isolated diacylglycerol (DAG)-containing vesicles are essential for completing the fusion of the NE in non-somatic cells. We investigated the impact of DAG depletion from the cis-Golgi in mammalian cells on NE reassembly. Using advanced electron microscopy, we observed an enriched DAG population of vesicles at the vicinity of the NE gaps of telophase mammalian cells. We applied a mini singlet oxygen generator-C1-domain tag that localized DAG-enriched vesicles at the perinuclear region, which suggested the existence of NE fusogenic vesicles. We quantified the impact of Golgi-DAG depletion by measuring the in situ NE rim curvature of the reforming NE. The rim curvature in these cells was significantly reduced compared with controls, which indicated a localized defect in NE morphology. Our novel results demonstrate the significance of the role of DAG from the cis-Golgi for the regulation of NE assembly.—Chung, G. H. C., M-C. Domart, C. Peddie, J. Mantell, K. Mclaverty, A. Arabiotorre, L. Hodgson, R. D. Byrne, P. Verkade, K. Arkill, L. M. Collinson, and B. Larijani. Acute depletion of diacylglycerol from the cis-Golgi affects localized nuclear envelope morphology during mitosis.

KW - Correlative light electron microscopy

KW - Membrane curvature

KW - Serial block face scanning electron microscopy

UR - http://www.scopus.com/inward/record.url?scp=85052377297&partnerID=8YFLogxK

U2 - 10.1194/jlr.M083899

DO - 10.1194/jlr.M083899

M3 - Article

VL - 59

SP - 1402

EP - 1413

JO - Journal of Lipid Research

JF - Journal of Lipid Research

SN - 0022-2275

IS - 8

ER -