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Article ; Online: The SphK1/S1P Axis Regulates Synaptic Vesicle Endocytosis via TRPC5 Channels.

Jiang, Zhong-Jiao / Gong, Liang-Wei

The Journal of neuroscience : the official journal of the Society for Neuroscience

2023 Volume 43, Issue 21, Page(s) 3807–3824

Abstract: Sphingosine-1-phosphate (S1P), a bioactive sphingolipid concentrated in the brain, is essential for normal brain functions, such as learning and memory and feeding behaviors. Sphingosine kinase 1 (SphK1), the primary kinase responsible for S1P production ...

Abstract	Sphingosine-1-phosphate (S1P), a bioactive sphingolipid concentrated in the brain, is essential for normal brain functions, such as learning and memory and feeding behaviors. Sphingosine kinase 1 (SphK1), the primary kinase responsible for S1P production in the brain, is abundant within presynaptic terminals, indicating a potential role of the SphK1/S1P axis in presynaptic physiology. Altered S1P levels have been highlighted in many neurologic diseases with endocytic malfunctions. However, it remains unknown whether the SphK1/S1P axis may regulate synaptic vesicle endocytosis in neurons. The present study evaluates potential functions of the SphK1/S1P axis in synaptic vesicle endocytosis by determining effects of a dominant negative catalytically inactive SphK1. Our data for the first time identify a critical role of the SphK1/S1P axis in endocytosis in both neuroendocrine chromaffin cells and neurons from mice of both sexes. Furthermore, our Ca
MeSH term(s)	Male ; Female ; Mice ; Animals ; Synaptic Vesicles/metabolism ; Phosphotransferases (Alcohol Group Acceptor)/metabolism ; Sphingosine/metabolism ; Endocytosis ; Lysophospholipids/metabolism ; TRPC Cation Channels
Chemical Substances	sphingosine kinase (EC 2.7.1.-) ; sphingosine 1-phosphate (26993-30-6) ; Phosphotransferases (Alcohol Group Acceptor) (EC 2.7.1.-) ; Sphingosine (NGZ37HRE42) ; Lysophospholipids ; TRPC Cation Channels ; Trpc5 protein, mouse
Language	English
Publishing date	2023-04-25
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	604637-x
ISSN	1529-2401 ; 0270-6474
ISSN (online)	1529-2401
ISSN	0270-6474
DOI	10.1523/JNEUROSCI.1494-22.2023
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Article ; Online: Phosphatidylserine is critical for vesicle fission during clathrin-mediated endocytosis.

Varga, Kelly / Jiang, Zhong-Jiao / Gong, Liang-Wei

Journal of neurochemistry

2019 Volume 152, Issue 1, Page(s) 48–60

Abstract: Phosphatidylserine (PS), a negatively charged phospholipid present predominantly at the inner leaflet of the plasma membrane, has been widely implicated in many cellular processes including membrane trafficking. Along this line, PS has been demonstrated ... ...

Abstract	Phosphatidylserine (PS), a negatively charged phospholipid present predominantly at the inner leaflet of the plasma membrane, has been widely implicated in many cellular processes including membrane trafficking. Along this line, PS has been demonstrated to be important for endocytosis, however, the involved mechanisms remain uncertain. By monitoring clathrin-mediated endocytosis (CME) of single vesicles in mouse chromaffin cells using cell-attached capacitance measurements that offer millisecond time resolution, we demonstrate in the present study that the fission-pore duration is reduced by PS addition, indicating a stimulatory role of PS in regulating the dynamics of vesicle fission during CME. Furthermore, our results show that the PS-mediated effect on the fission-pore duration is Ca
MeSH term(s)	Animals ; Cells, Cultured ; Chromaffin Cells/physiology ; Clathrin/physiology ; Clathrin-Coated Vesicles/physiology ; Endocytosis/physiology ; Exocytosis/physiology ; Female ; Gene Knockout Techniques ; Male ; Mice ; Mice, Inbred C57BL ; Phosphatidylserines/physiology ; Synaptotagmin I/genetics ; Synaptotagmin I/physiology
Chemical Substances	Clathrin ; Phosphatidylserines ; Synaptotagmin I ; Syt1 protein, mouse
Language	English
Publishing date	2019-10-27
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	80158-6
ISSN	1471-4159 ; 0022-3042 ; 1474-1644
ISSN (online)	1471-4159
ISSN	0022-3042 ; 1474-1644
DOI	10.1111/jnc.14886
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Article ; Online: Endogenous Protein-Protein Interaction Network of the NPC Cholesterol Transporter 1 in the Cerebral Cortex.

Javanshad, Roshan / Nguyen, Thu T A / Azaria, Ruth D / Li, Wenping / Edmison, Daisy / Gong, Liang-Wei / Gowrishankar, Swetha / Lieberman, Andrew P / Schultz, Mark L / Cologna, Stephanie M

Journal of proteome research

2024

Abstract: NPC intracellular cholesterol transporter 1 (NPC1) is a multipass, transmembrane glycoprotein mostly recognized for its key role in facilitating cholesterol efflux. Mutations in ... ...

Abstract	NPC intracellular cholesterol transporter 1 (NPC1) is a multipass, transmembrane glycoprotein mostly recognized for its key role in facilitating cholesterol efflux. Mutations in the
Language	English
Publishing date	2024-04-30
Publishing country	United States
Document type	Journal Article
ZDB-ID	2078618-9
ISSN	1535-3907 ; 1535-3893
ISSN (online)	1535-3907
ISSN	1535-3893
DOI	10.1021/acs.jproteome.3c00788
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Article ; Online: Investigating Phosphorylation Patterns of the Ion Channel TRPM7 Using Multiple Extraction and Enrichment Techniques Reveals New Phosphosites.

Nguyen, Thu T A / Li, Wenping / Park, Thomas J / Gong, Liang-Wei / Cologna, Stephanie M

Journal of the American Society for Mass Spectrometry

2019 Volume 30, Issue 8, Page(s) 1359–1367

Abstract: The study of membrane proteins, and in particular ion channels, is crucial to understanding cellular function. Mass spectrometry-based approaches including bottom-up strategies to study membrane proteins have been successful yet still can remain ... ...

Abstract	The study of membrane proteins, and in particular ion channels, is crucial to understanding cellular function. Mass spectrometry-based approaches including bottom-up strategies to study membrane proteins have been successful yet still can remain challenging. In this study, we sought to evaluate the phosphorylation patterns of the ion channel TRPM7 which is involved in a range of critical physiological functions. To overcome extraction obstacles associated with analyzing membrane proteins, we incorporated the use of 5% SDS solubilization coupled with SCAD and S-Trap digestion methods to eliminate detergent interference in downstream LC-MS/MS analysis. We found that the SCAD method was more efficient, yielding 84% of the overall identified proteins; however, the variability was greater than the S-Trap method. Using both methods together with TiO
MeSH term(s)	Amino Acid Sequence ; Chromatography, Liquid ; HEK293 Cells ; Humans ; Phosphopeptides/analysis ; Phosphorylation ; Protein Serine-Threonine Kinases/chemistry ; TRPM Cation Channels/chemistry ; Tandem Mass Spectrometry
Chemical Substances	Phosphopeptides ; TRPM Cation Channels ; Protein Serine-Threonine Kinases (EC 2.7.11.1) ; TRPM7 protein, human (EC 2.7.11.1)
Language	English
Publishing date	2019-05-28
Publishing country	United States
Document type	Journal Article
ZDB-ID	1073671-2
ISSN	1879-1123 ; 1044-0305
ISSN (online)	1879-1123
ISSN	1044-0305
DOI	10.1007/s13361-019-02223-5
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Article ; Online: Methods for cell-attached capacitance measurements in mouse adrenal chromaffin cell.

Varga, Kelly T / Jiang, Zhongjiao / Gong, Liang-Wei

Journal of visualized experiments : JoVE

2014 , Issue 92, Page(s) e52024

Abstract: Neuronal transmission is an integral part of cellular communication within the brain. Depolarization of the presynaptic membrane leads to vesicle fusion known as exocytosis that mediates synaptic transmission. Subsequent retrieval of synaptic vesicles is ...

Abstract	Neuronal transmission is an integral part of cellular communication within the brain. Depolarization of the presynaptic membrane leads to vesicle fusion known as exocytosis that mediates synaptic transmission. Subsequent retrieval of synaptic vesicles is necessary to generate new neurotransmitter-filled vesicles in a process identified as endocytosis. During exocytosis, fusing vesicle membranes will result in an increase in surface area and subsequent endocytosis results in a decrease in the surface area. Here, our lab demonstrates a basic introduction to cell-attached capacitance recordings of single endocytic events in the mouse adrenal chromaffin cell. This type of electrical recording is useful for high-resolution recordings of exocytosis and endocytosis at the single vesicle level. While this technique can detect both vesicle exocytosis and endocytosis, the focus of our lab is vesicle endocytosis. Moreover, this technique allows us to analyze the kinetics of single endocytic events. Here the methods for mouse adrenal gland tissue dissection, chromaffin cell culture, basic cell-attached techniques, and subsequent examples of individual traces measuring singular endocytic event are described.
MeSH term(s)	Adrenal Glands/cytology ; Adrenal Glands/physiology ; Adrenal Glands/surgery ; Animals ; Cell Culture Techniques/methods ; Chromaffin Cells/cytology ; Chromaffin Cells/physiology ; Dissection ; Electric Capacitance ; Mice ; Patch-Clamp Techniques/methods
Language	English
Publishing date	2014-10-22
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Video-Audio Media
ISSN	1940-087X
ISSN (online)	1940-087X
DOI	10.3791/52024
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Article: Methods for cell-attached capacitance measurements in mouse adrenal chromaffin cell

Varga, Kelly T / Jiang, Zhongjiao / Gong, Liang-Wei

Journal of visualized experiments. 2014 Oct. 22, , no. 92

2014

Abstract	Neuronal transmission is an integral part of cellular communication within the brain. Depolarization of the presynaptic membrane leads to vesicle fusion known as exocytosis that mediates synaptic transmission. Subsequent retrieval of synaptic vesicles is necessary to generate new neurotransmitter-filled vesicles in a process identified as endocytosis. During exocytosis, fusing vesicle membranes will result in an increase in surface area and subsequent endocytosis results in a decrease in the surface area. Here, our lab demonstrates a basic introduction to cell-attached capacitance recordings of single endocytic events in the mouse adrenal chromaffin cell. This type of electrical recording is useful for high-resolution recordings of exocytosis and endocytosis at the single vesicle level. While this technique can detect both vesicle exocytosis and endocytosis, the focus of our lab is vesicle endocytosis. Moreover, this technique allows us to analyze the kinetics of single endocytic events. Here the methods for mouse adrenal gland tissue dissection, chromaffin cell culture, basic cell-attached techniques, and subsequent examples of individual traces measuring singular endocytic event are described.
Keywords	adrenal glands ; brain ; capacitance ; cell culture ; endocytosis ; exocytosis ; mice ; neurons ; surface area ; synaptic transmission ; synaptic vesicles
Language	English
Dates of publication	2014-1022
Size	p. e52024.
Publishing place	Journal of Visualized Experiments
Document type	Article
ZDB-ID	2259946-0
ISSN	1940-087X
ISSN	1940-087X
DOI	10.3791/52024
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Article ; Online: TRPM7 is critical for short-term synaptic depression by regulating synaptic vesicle endocytosis.

Jiang, Zhong-Jiao / Li, Wenping / Yao, Li-Hua / Saed, Badeia / Rao, Yan / Grewe, Brian S / McGinley, Andrea / Varga, Kelly / Alford, Simon / Hu, Ying S / Gong, Liang-Wei

eLife

2021 Volume 10

Abstract: Transient receptor potential melastatin 7 (TRPM7) contributes to a variety of physiological and pathological processes in many tissues and cells. With a widespread distribution in the nervous system, TRPM7 is involved in animal behaviors and neuronal ... ...

Abstract	Transient receptor potential melastatin 7 (TRPM7) contributes to a variety of physiological and pathological processes in many tissues and cells. With a widespread distribution in the nervous system, TRPM7 is involved in animal behaviors and neuronal death induced by ischemia. However, the physiological role of TRPM7 in central nervous system (CNS) neuron remains unclear. Here, we identify endocytic defects in neuroendocrine cells and neurons from TRPM7 knockout (KO) mice, indicating a role of TRPM7 in synaptic vesicle endocytosis. Our experiments further pinpoint the importance of TRPM7 as an ion channel in synaptic vesicle endocytosis. Ca
MeSH term(s)	Animals ; Calcium/metabolism ; Calcium Signaling ; Chromaffin Cells/metabolism ; Endocytosis ; Excitatory Postsynaptic Potentials ; Female ; HEK293 Cells ; Humans ; Inhibitory Postsynaptic Potentials ; Kinetics ; Male ; Mice, Knockout ; Neural Inhibition ; Neuronal Plasticity ; Neurons/metabolism ; Synaptic Transmission ; Synaptic Vesicles/genetics ; Synaptic Vesicles/metabolism ; TRPM Cation Channels/genetics ; TRPM Cation Channels/metabolism ; Mice
Chemical Substances	TRPM Cation Channels ; Trpm7 protein, mouse (EC 2.7.1.-) ; Calcium (SY7Q814VUP)
Language	English
Publishing date	2021-09-27
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.66709
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Article ; Online: Extracellular and intracellular sphingosine-1-phosphate distinctly regulates exocytosis in chromaffin cells.

Jiang, Zhong-Jiao / Delaney, Taylor L / Zanin, Mark P / Haberberger, Rainer V / Pitson, Stuart M / Huang, Jian / Alford, Simon / Cologna, Stephanie M / Keating, Damien J / Gong, Liang-Wei

Journal of neurochemistry

2019 Volume 149, Issue 6, Page(s) 729–746

Abstract: Sphingosine-1-phosphate (S1P) is an essential bioactive sphingosine lipid involved in many neurological disorders. Sphingosine kinase 1 (SphK1), a key enzyme for S1P production, is concentrated in presynaptic terminals. However, the role of S1P/SphK1 ... ...

Abstract	Sphingosine-1-phosphate (S1P) is an essential bioactive sphingosine lipid involved in many neurological disorders. Sphingosine kinase 1 (SphK1), a key enzyme for S1P production, is concentrated in presynaptic terminals. However, the role of S1P/SphK1 signaling in exocytosis remains elusive. By detecting catecholamine release from single vesicles in chromaffin cells, we show that a dominant negative SphK1 (SphK1
MeSH term(s)	Animals ; Chromaffin Cells/metabolism ; Exocytosis/physiology ; Female ; Lysophospholipids/metabolism ; Male ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Sphingosine/analogs & derivatives ; Sphingosine/metabolism
Chemical Substances	Lysophospholipids ; sphingosine 1-phosphate (26993-30-6) ; Sphingosine (NGZ37HRE42)
Language	English
Publishing date	2019-05-08
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	80158-6
ISSN	1471-4159 ; 0022-3042 ; 1474-1644
ISSN (online)	1471-4159
ISSN	0022-3042 ; 1474-1644
DOI	10.1111/jnc.14703
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Article ; Online: Regulation of postsynaptic AMPA responses by synaptojanin 1.

Gong, Liang-Wei / De Camilli, Pietro

Proceedings of the National Academy of Sciences of the United States of America

2008 Volume 105, Issue 45, Page(s) 17561–17566

Abstract: Endocytosis of postsynaptic AMPA receptors is a mechanism through which efficiency of neurotransmission is regulated. We have genetically tested the hypothesis that synaptojanin 1, a phosphoinositide phosphatase implicated in the endocytosis of synaptic ... ...

Abstract	Endocytosis of postsynaptic AMPA receptors is a mechanism through which efficiency of neurotransmission is regulated. We have genetically tested the hypothesis that synaptojanin 1, a phosphoinositide phosphatase implicated in the endocytosis of synaptic vesicles presynaptically, may also function in the endocytosis of AMPA receptors postsynaptically. Electrophysiological recordings of cultured hippocampal neurons showed that miniature excitatory postsynaptic current amplitudes were larger in synaptojanin 1 knockout (KO) neurons because of an increase of surface-exposed AMPA receptors. This change did not represent an adaptive response to decreased presynaptic release in KO cultures and was rescued by the expression of wild type, but not catalytically inactive synaptojanin 1, in the postsynaptic neuron. NMDA-induced internalization of pHluorin-tagged AMPA receptors (GluR2) was impaired in KO neurons. These results reveal a function of synaptojanin 1 in constitutive and triggered internalization of AMPA receptors and thus indicate a role for phosphatidylinositol(4,5)-bisphosphate metabolism in the regulation of postsynaptic AMPA responses.
MeSH term(s)	Analysis of Variance ; Animals ; Electrophysiology ; Endocytosis/physiology ; Green Fluorescent Proteins ; Hippocampus/metabolism ; Mice ; Mice, Knockout ; Nerve Tissue Proteins/genetics ; Nerve Tissue Proteins/metabolism ; Phosphatidylinositol 4,5-Diphosphate/metabolism ; Phosphoric Monoester Hydrolases/genetics ; Phosphoric Monoester Hydrolases/metabolism ; Receptors, AMPA/metabolism ; Synaptic Transmission/physiology
Chemical Substances	Nerve Tissue Proteins ; PHluorin ; Phosphatidylinositol 4,5-Diphosphate ; Receptors, AMPA ; Green Fluorescent Proteins (147336-22-9) ; synaptojanin (EC 3.1.3.-) ; Phosphoric Monoester Hydrolases (EC 3.1.3.2)
Language	English
Publishing date	2008-11-11
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.0809221105
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Article: Regulation of postsynaptic AMPA responses by synaptojanin 1

Gong, Liang-Wei / De Camilli, Pietro

Proceedings of the National Academy of Sciences of the United States of America. 2008 Nov. 11, v. 105, no. 45

2008

Abstract	Endocytosis of postsynaptic AMPA receptors is a mechanism through which efficiency of neurotransmission is regulated. We have genetically tested the hypothesis that synaptojanin 1, a phosphoinositide phosphatase implicated in the endocytosis of synaptic vesicles presynaptically, may also function in the endocytosis of AMPA receptors postsynaptically. Electrophysiological recordings of cultured hippocampal neurons showed that miniature excitatory postsynaptic current amplitudes were larger in synaptojanin 1 knockout (KO) neurons because of an increase of surface-exposed AMPA receptors. This change did not represent an adaptive response to decreased presynaptic release in KO cultures and was rescued by the expression of wild type, but not catalytically inactive synaptojanin 1, in the postsynaptic neuron. NMDA-induced internalization of pHluorin-tagged AMPA receptors (GluR2) was impaired in KO neurons. These results reveal a function of synaptojanin 1 in constitutive and triggered internalization of AMPA receptors and thus indicate a role for phosphatidylinositol(4,5)-bisphosphate metabolism in the regulation of postsynaptic AMPA responses.
Keywords	electrophysiology ; endocytosis ; metabolism ; neurons ; receptors ; synaptic vesicles
Language	English
Dates of publication	2008-1111
Size	p. 17561-17566.
Publishing place	National Academy of Sciences
Document type	Article
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.0809221105
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