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Lipid species affect morphology of endoplasmic reticulum: a sea urchin oocyte model of reversible manipulation

Ulloa, Gabriela; Hamati, Fadi; Dick, Alexander; Fitzgerald, Julie; Mantell, Judith; Verkade, Paul; Collinson, Lucy; Arkill, Kenton; Larijani, Banafshe; Poccia, Dominic

Authors

Gabriela Ulloa

Fadi Hamati

Alexander Dick

Julie Fitzgerald

Judith Mantell

Paul Verkade

Lucy Collinson

Banafshe Larijani

Dominic Poccia



Abstract

The endoplasmic reticulum (ER) is a large multifunctional organelle of eukaryotic cells. Malfunction of the ER in various disease states, such as atherosclerosis, Type 2 diabetes, cancer, Alzheimer’s and Parkinson’s diseases and amyotrophic lateral sclerosis, often correlates with alterations in its morphology. The ER exhibits regionally variable membrane morphology that includes, at the extremes, large relatively flat surfaces and interconnected tubular structures highly curved in cross-section. Much evidence suggests that ER morphology is controlled by shaping proteins that associate with membrane lipids. To investigate the role of these lipids in ER morphology, we developed a sea urchin oocyte model which is a relatively quiescent cell in which the ER consists mostly of tubules. We altered levels of endogenous diacylglycerol, phosphatidylethanolamine and phosphatidylcholine by microinjection of enzymes or lipid delivery by fusion with liposomes and evaluated shape changes with two- and three-dimensional confocal imaging and three-dimensional electron microscopy techniques. Decreases and increases in the levels of lipids such as diacylglycerol or phosphatidylethanolamine characterized by negative spontaneous curvature correlated with conversion to sheet structures or tubules respectively. The effects of endogenous alterations of diacylglycerol were reversible upon exogenous delivery of lipids of negative spontaneous curvature. These data suggest that shaping proteins require threshold amounts of such lipids and that localized deficiencies of the lipids could contribute to alterations of ER morphology. The oocyte modeling system should be beneficial to future studies directed at understanding the precise spatial and compositional requirements of lipid species in interactions leading to alterations of organelle shaping.

Citation

Ulloa, G., Hamati, F., Dick, A., Fitzgerald, J., Mantell, J., Verkade, P., …Poccia, D. (2019). Lipid species affect morphology of endoplasmic reticulum: a sea urchin oocyte model of reversible manipulation. Journal of Lipid Research, 60(11), 1880-1891. https://doi.org/10.1194/jlr.ra119000210

Journal Article Type Article
Acceptance Date Sep 23, 2019
Online Publication Date Sep 23, 2019
Publication Date Nov 1, 2019
Deposit Date Oct 3, 2019
Publicly Available Date Nov 22, 2019
Journal Journal of Lipid Research
Print ISSN 0022-2275
Electronic ISSN 1539-7262
Publisher American Society for Biochemistry and Molecular Biology
Peer Reviewed Peer Reviewed
Volume 60
Issue 11
Pages 1880-1891
DOI https://doi.org/10.1194/jlr.ra119000210
Keywords Cell Biology; Biochemistry; Endocrinology
Public URL https://nottingham-repository.worktribe.com/output/2742160
Publisher URL http://www.jlr.org/content/early/2019/09/23/jlr.RA119000210.abstract

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