Diacylglycerol, phosphatidic acid, and their metabolic enzymes in synaptic vesicle recycling

Becky Tu-Sekine, Hana Goldschmidt, Daniel Max Raben

Research output: Contribution to journalArticle

Abstract

The synaptic vesicle (SV) cycle includes exocytosis of vesicles loaded with a neurotransmitter such as glutamate, coordinated recovery of SVs by endocytosis, refilling of vesicles, and subsequent release of the refilled vesicles from the presynaptic bouton. SV exocytosis is tightly linked with endocytosis, and variations in the number of vesicles, and/or defects in the refilling of SVs, will affect the amount of neurotransmitter available for release ( Sudhof, 2004). There is increasing interest in the roles synaptic vesicle lipids and lipid metabolizing enzymes play in this recycling. Initial emphasis was placed on the role of polyphosphoinositides in SV cycling as outlined in a number of reviews ( Lim and Wenk, 2009; Martin, 2012; Puchkov and Haucke, 2013; Rohrbough and Broadie, 2005). Other lipids are now recognized to also play critical roles. For example, PLD1 ( Humeau etal., 2001; Rohrbough and Broadie, 2005) and some DGKs ( Miller etal., 1999; Nurrish etal., 1999) play roles in neurotransmission which is consistent with the critical roles for phosphatidic acid (PtdOH) and diacylglycerol (DAG) in the regulation of SV exo/endocytosis ( Cremona etal., 1999; Exton, 1994; Huttner and Schmidt, 2000; Lim and Wenk, 2009; Puchkov and Haucke, 2013; Rohrbough and Broadie, 2005). PLD generates phosphatidic acid by catalyzing the hydrolysis of phosphatidylcholine (PtdCho) and in some systems this PtdOH is de-phosphorylated to generate DAG. In contrast, DGK catalyzes the phosphorylation of DAG thereby converting it into PtdOH. While both enzymes are poised to regulate the levels of DAG and PtdOH, therefore, they both lead to the generation of PtdOH and could have opposite effects on DAG levels. This is particularly important for SV cycling as PtdOH and DAG are both needed for evoked exocytosis ( Lim and Wenk, 2009; Puchkov and Haucke, 2013; Rohrbough and Broadie, 2005). Two lipids and their involved metabolic enzymes, two sphingolipids have also been implicated in exocytosis: sphingosine ( Camoletto etal., 2009; Chan etal., 2012; Chan and Sieburth, 2012; Darios etal., 2009; Kanno etal., 2010; Rohrbough etal., 2004) and sphingosine-1-phosphate ( Chan, Hu, 2012; Chan and Sieburth, 2012; Kanno etal., 2010). Finally a number of reports have focused on the somewhat less well studies roles of sphingolipids and cholesterol in SV cycling. In this report, we review the recent understanding of the roles PLDs, DGKs, and DAG lipases, as well as sphingolipids and cholesterol play in synaptic vesicle cycling.

Original languageEnglish (US)
Pages (from-to)147-152
Number of pages6
JournalAdvances in Biological Regulation
Volume57
DOIs
StatePublished - Jan 1 2015

Fingerprint

Phosphatidic Acids
Synaptic Vesicles
Diglycerides
Exocytosis
Enzymes
Sphingolipids
Endocytosis
Lipids
Neurotransmitter Agents
Cholesterol
Phosphatidylinositol Phosphates
Sphingosine
Lipoprotein Lipase
Recycling
Phosphatidylcholines
Synaptic Transmission
Glutamic Acid
Hydrolysis
Phosphorylation

Keywords

  • Cholesterol
  • Diacylglycerol
  • Diacylglycerol kinase
  • Neuroscience
  • Phosphatidic acid
  • Phospholipase D
  • Sphingosine
  • Synaptic vesicle cycle

ASJC Scopus subject areas

  • Cancer Research
  • Genetics
  • Molecular Biology
  • Molecular Medicine
  • Medicine(all)

Cite this

Diacylglycerol, phosphatidic acid, and their metabolic enzymes in synaptic vesicle recycling. / Tu-Sekine, Becky; Goldschmidt, Hana; Raben, Daniel Max.

In: Advances in Biological Regulation, Vol. 57, 01.01.2015, p. 147-152.

Research output: Contribution to journalArticle

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AB - The synaptic vesicle (SV) cycle includes exocytosis of vesicles loaded with a neurotransmitter such as glutamate, coordinated recovery of SVs by endocytosis, refilling of vesicles, and subsequent release of the refilled vesicles from the presynaptic bouton. SV exocytosis is tightly linked with endocytosis, and variations in the number of vesicles, and/or defects in the refilling of SVs, will affect the amount of neurotransmitter available for release ( Sudhof, 2004). There is increasing interest in the roles synaptic vesicle lipids and lipid metabolizing enzymes play in this recycling. Initial emphasis was placed on the role of polyphosphoinositides in SV cycling as outlined in a number of reviews ( Lim and Wenk, 2009; Martin, 2012; Puchkov and Haucke, 2013; Rohrbough and Broadie, 2005). Other lipids are now recognized to also play critical roles. For example, PLD1 ( Humeau etal., 2001; Rohrbough and Broadie, 2005) and some DGKs ( Miller etal., 1999; Nurrish etal., 1999) play roles in neurotransmission which is consistent with the critical roles for phosphatidic acid (PtdOH) and diacylglycerol (DAG) in the regulation of SV exo/endocytosis ( Cremona etal., 1999; Exton, 1994; Huttner and Schmidt, 2000; Lim and Wenk, 2009; Puchkov and Haucke, 2013; Rohrbough and Broadie, 2005). PLD generates phosphatidic acid by catalyzing the hydrolysis of phosphatidylcholine (PtdCho) and in some systems this PtdOH is de-phosphorylated to generate DAG. In contrast, DGK catalyzes the phosphorylation of DAG thereby converting it into PtdOH. While both enzymes are poised to regulate the levels of DAG and PtdOH, therefore, they both lead to the generation of PtdOH and could have opposite effects on DAG levels. This is particularly important for SV cycling as PtdOH and DAG are both needed for evoked exocytosis ( Lim and Wenk, 2009; Puchkov and Haucke, 2013; Rohrbough and Broadie, 2005). Two lipids and their involved metabolic enzymes, two sphingolipids have also been implicated in exocytosis: sphingosine ( Camoletto etal., 2009; Chan etal., 2012; Chan and Sieburth, 2012; Darios etal., 2009; Kanno etal., 2010; Rohrbough etal., 2004) and sphingosine-1-phosphate ( Chan, Hu, 2012; Chan and Sieburth, 2012; Kanno etal., 2010). Finally a number of reports have focused on the somewhat less well studies roles of sphingolipids and cholesterol in SV cycling. In this report, we review the recent understanding of the roles PLDs, DGKs, and DAG lipases, as well as sphingolipids and cholesterol play in synaptic vesicle cycling.

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KW - Diacylglycerol

KW - Diacylglycerol kinase

KW - Neuroscience

KW - Phosphatidic acid

KW - Phospholipase D

KW - Sphingosine

KW - Synaptic vesicle cycle

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