Dynamic formation of ER-PM junctions presents a lipid phosphatase to regulate phosphoinositides

Eamonn J Dickson, Jill B. Jensen, Oscar Vivas, Martin Kruse, Alexis E. Traynor-Kaplan, Bertil Hille

Research output: Contribution to journalArticle

43 Citations (Scopus)

Abstract

Endoplasmic reticulum-plasma membrane (ER-PM) contact sites play an integral role in cellular processes such as excitation- contraction coupling and store-operated calcium entry (SOCE). Another ER-PM assembly is one tethered by the extended synaptotagmins (E-Syt). We have discovered that at steady state, E-Syt2 positions the ER and Sac1, an integral ER membrane lipid phosphatase, in discrete ER-PM junctions. Here, Sac1 participates in phosphoinositide homeostasis by limiting PM phosphatidylinositol 4-phosphate (PI(4)P), the precursor of PI(4,5)P2. Activation of G protein-coupled receptors that deplete PM PI(4,5)P2 disrupts E-Syt2-mediated ER-PM junctions, reducing Sess to the PM and permitting PM PI(4)P and PI(4,5)P2 to recover. Conversely, depletion of ER luminal calcium and subsequent activation of SOCE increases the amount of Sac1 in contact with the PM, depleting PM PI(4)P. Thus, the dynamic presence of Sac1 at ER-PM contact sites allows it to act as a cellular sensor and controller of PM phosphoinositides, thereby influencing many PM processes.

Original languageEnglish (US)
Pages (from-to)33-48
Number of pages16
JournalJournal of Cell Biology
Volume213
Issue number1
DOIs
StatePublished - Apr 1 2016
Externally publishedYes

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Phosphatidylinositols
Phosphoric Monoester Hydrolases
Endoplasmic Reticulum
Cell Membrane
Lipids
Calcium
Synaptotagmins
Excitation Contraction Coupling
Membrane Lipids
G-Protein-Coupled Receptors
Homeostasis
phosphatidylinositol 4-phosphate

ASJC Scopus subject areas

  • Cell Biology

Cite this

Dynamic formation of ER-PM junctions presents a lipid phosphatase to regulate phosphoinositides. / Dickson, Eamonn J; Jensen, Jill B.; Vivas, Oscar; Kruse, Martin; Traynor-Kaplan, Alexis E.; Hille, Bertil.

In: Journal of Cell Biology, Vol. 213, No. 1, 01.04.2016, p. 33-48.

Research output: Contribution to journalArticle

Dickson, Eamonn J ; Jensen, Jill B. ; Vivas, Oscar ; Kruse, Martin ; Traynor-Kaplan, Alexis E. ; Hille, Bertil. / Dynamic formation of ER-PM junctions presents a lipid phosphatase to regulate phosphoinositides. In: Journal of Cell Biology. 2016 ; Vol. 213, No. 1. pp. 33-48.
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