Robert Edwards, MD

Cahill Professor of Neurology and Physiology
Kavli Institute for Fundamental Neuroscience
Weill Institute of Neuroscience
UCSF School of Medicine
+1 415 502-5687

Robert Edwards is a neuroscientist known for his work on the molecular and cellular basis of neurotransmitter release.  His group identified the proteins that transport classical transmitters into neurosecretory vesicles, contributing to characterization of their role in quantal release, their mechanism and their regulation as well as their structure. Using the transporters, he has helped to establish the phenomenon of neurotransmitter corelease.  His lab recently showed that individual neurons can release two transmitters with different frequency dependence, and the two vesicle populations recycle through distinct mechanisms.  He has also used the transporters to characterize the formation of dense core vesicles that mediate regulated release of peptides. Since the original identification of a vesicular monoamine transporter by selection in MPP+, his work has focused on the pathogenesis of Parkinson’s disease and most recently the presynaptic protein a-synuclein. The work also has implications for behavior and neuropsychiatric illness. Robert Edwards was raised in New York City, attended Yale College and Johns Hopkins Medical School.  He trained in clinical neurology, studied as a postdoctoral fellow with William J. Rutter at UCSF and joined the faculty at UCLA in 1990 before returning to UCSF in 1995.  He is a member of the National Academy of Medicine and the National Academy of Sciences.

Publications: 

Adaptor protein-3 produces synaptic vesicles that release phasic dopamine.

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

Jain S, Yee AG, Maas J, Gierok S, Xu H, Stansil J, Eriksen J, Nelson AB, Silm K, Ford CP, Edwards RH

2023

Adaptor protein AP-3 produces synaptic vesicles that release at high frequency by recruiting phospholipid flippase ATP8A1.

Nature neuroscience

Xu H, Oses-Prieto JA, Khvotchev M, Jain S, Liang J, Burlingame A, Edwards RH

2023

Adaptor Protein-3 Produces Synaptic Vesicles that Release Phasic Dopamine.

bioRxiv : the preprint server for biology

Jain S, Yee AG, Maas J, Gierok S, Xu H, Stansil J, Eriksen J, Nelson A, Silm K, Ford CP, Edwards RH

2023

Synuclein phosphorylation: pathogenic or physiologic?

NPJ Parkinson's disease

Kontaxi C, Edwards RH

2023

Substrate recognition and proton coupling by a bacterial member of solute carrier family 17.

The Journal of biological chemistry

Batarni S, Nayak N, Chang A, Li F, Hareendranath S, Zhou L, Xu H, Stroud R, Eriksen J, Edwards RH

2023

High-speed imaging reveals the bimodal nature of dense core vesicle exocytosis.

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

Zhang P, Rumschitzki D, Edwards RH

2022

Diversity of function and mechanism in a family of organic anion transporters.

Current opinion in structural biology

Li F, Eriksen J, Finer-Moore J, Stroud RM, Edwards RH

2022

SNX5 targets a monoamine transporter to the TGN for assembly into dense core vesicles by AP-3.

The Journal of cell biology

Xu H, Chang F, Jain S, Heller BA, Han X, Liu Y, Edwards RH

2022

Whole Endosome Recording of Vesicular Neurotransmitter Transporter Currents.

Methods in molecular biology (Clifton, N.J.)

Chang R, Edwards RH

2022

The Membrane Interactions of Synuclein: Physiology and Pathology.

Annual review of pathology

Runwal G, Edwards RH

2021

A dual role for α-synuclein in facilitation and depression of dopamine release from substantia nigra neurons in vivo.

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

Somayaji M, Cataldi S, Choi SJ, Edwards RH, Mosharov EV, Sulzer D

2020

Ion transport and regulation in a synaptic vesicle glutamate transporter.

Science (New York, N.Y.)

Li F, Eriksen J, Finer-Moore J, Chang R, Nguyen P, Bowen A, Myasnikov A, Yu Z, Bulkley D, Cheng Y, Edwards RH, Stroud RM

2020

The mechanism and regulation of vesicular glutamate transport: Coordination with the synaptic vesicle cycle.

Biochimica et biophysica acta. Biomembranes

Eriksen J, Li F, Edwards RH

2020

Structures suggest a mechanism for energy coupling by a family of organic anion transporters.

PLoS biology

Leano JB, Batarni S, Eriksen J, Juge N, Pak JE, Kimura-Someya T, Robles-Colmenares Y, Moriyama Y, Stroud RM, Edwards RH

2019

Synaptic Vesicle Recycling Pathway Determines Neurotransmitter Content and Release Properties.

Neuron

Silm K, Yang J, Marcott PF, Asensio CS, Eriksen J, Guthrie DA, Newman AH, Ford CP, Edwards RH

2019

A mouse model of autism implicates endosome pH in the regulation of presynaptic calcium entry.

Nature communications

Ullman JC, Yang J, Sullivan M, Bendor J, Levy J, Pham E, Silm K, Seifikar H, Sohal VS, Nicoll RA, Edwards RH

2018

Loss of a-Synuclein Does Not Affect Mitochondrial Bioenergetics in Rodent Neurons.

eNeuro

Pathak D, Berthet A, Bendor JT, Yu K, Sellnow RC, Orr AL, Nguyen MK, Edwards RH, Manfredsson FP, Nakamura K

2017

a-Synuclein promotes dilation of the exocytotic fusion pore.

Nature neuroscience

Logan T, Bendor J, Toupin C, Thorn K, Edwards RH

2017

Endogenous Leucine-Rich Repeat Kinase 2 Slows Synaptic Vesicle Recycling in Striatal Neurons.

Frontiers in synaptic neuroscience

Maas JW, Yang J, Edwards RH

2017

Sensory-Derived Glutamate Regulates Presynaptic Inhibitory Terminals in Mouse Spinal Cord.

Neuron

Mende M, Fletcher EV, Belluardo JL, Pierce JP, Bommareddy PK, Weinrich JA, Kabir ZD, Schierberl KC, Pagiazitis JG, Mendelsohn AI, Francesconi A, Edwards RH, Milner TA, Rajadhyaksha AM, van Roessel PJ, Mentis GZ, Kaltschmidt JA

2016

Protons Regulate Vesicular Glutamate Transporters through an Allosteric Mechanism.

Neuron

Eriksen J, Chang R, McGregor M, Silm K, Suzuki T, Edwards RH

2016

Sex-dependent changes in metabolism and behavior, as well as reduced anxiety after eliminating ventromedial hypothalamus excitatory output.

Molecular metabolism

Cheung CC, Krause WC, Edwards RH, Yang CF, Shah NM, Hnasko TS, Ingraham HA

2015

The role of mitochondrially derived ATP in synaptic vesicle recycling.

The Journal of biological chemistry

Pathak D, Shields LY, Mendelsohn BA, Haddad D, Lin W, Gerencser AA, Kim H, Brand MD, Edwards RH, Nakamura K

2015

Mobile binding sites regulate glutamate clearance.

Nature neuroscience

Edwards RH

2015

Loss of mitochondrial fission depletes axonal mitochondria in midbrain dopamine neurons.

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

Berthet A, Margolis EB, Zhang J, Hsieh I, Zhang J, Hnasko TS, Ahmad J, Edwards RH, Sesaki H, Huang EJ, Nakamura K

2014

Efficient, complete deletion of synaptic proteins using CRISPR.

Neuron

Incontro S, Asensio CS, Edwards RH, Nicoll RA

2014

Self-assembly of VPS41 promotes sorting required for biogenesis of the regulated secretory pathway.

Developmental cell

Asensio CS, Sirkis DW, Maas JW, Egami K, To TL, Brodsky FM, Shu X, Cheng Y, Edwards RH

2013

The function of a-synuclein.

Neuron

Bendor JT, Logan TP, Edwards RH

2013

Multiple dileucine-like motifs direct VGLUT1 trafficking.

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

Foss SM, Li H, Santos MS, Edwards RH, Voglmaier SM

2013

Ventral tegmental area glutamate neurons: electrophysiological properties and projections.

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

Hnasko TS, Hjelmstad GO, Fields HL, Edwards RH

2012

Restoration of hearing in the VGLUT3 knockout mouse using virally mediated gene therapy.

Neuron

Akil O, Seal RP, Burke K, Wang C, Alemi A, During M, Edwards RH, Lustig LR

2012

AMP-activated kinase links serotonergic signaling to glutamate release for regulation of feeding behavior in C. elegans.

Cell metabolism

Cunningham KA, Hua Z, Srinivasan S, Liu J, Lee BH, Edwards RH, Ashrafi K

2012

Fabs enable single particle cryoEM studies of small proteins.

Structure (London, England : 1993)

Wu S, Avila-Sakar A, Kim J, Booth DS, Greenberg CH, Rossi A, Liao M, Li X, Alian A, Griner SL, Juge N, Yu Y, Mergel CM, Chaparro-Riggers J, Strop P, Tampé R, Edwards RH, Stroud RM, Craik CS, Cheng Y

2012

Vesicular and plasma membrane transporters for neurotransmitters.

Cold Spring Harbor perspectives in biology

Blakely RD, Edwards RH

2012

Dopamine dysregulation in a mouse model of paroxysmal nonkinesigenic dyskinesia.

The Journal of clinical investigation

Lee HY, Nakayama J, Xu Y, Fan X, Karouani M, Shen Y, Pothos EN, Hess EJ, Fu YH, Edwards RH, Ptácek LJ

2012

Neurotransmitter corelease: mechanism and physiological role.

Annual review of physiology

Hnasko TS, Edwards RH

2011

Presynaptic regulation of quantal size: K+/H+ exchange stimulates vesicular glutamate transport.

Nature neuroscience

Goh GY, Huang H, Ullman J, Borre L, Hnasko TS, Trussell LO, Edwards RH

2011

v-SNARE composition distinguishes synaptic vesicle pools.

Neuron

Hua Z, Leal-Ortiz S, Foss SM, Waites CL, Garner CC, Voglmaier SM, Edwards RH

2011

Direct membrane association drives mitochondrial fission by the Parkinson disease-associated protein alpha-synuclein.

The Journal of biological chemistry

Nakamura K, Nemani VM, Azarbal F, Skibinski G, Levy JM, Egami K, Munishkina L, Zhang J, Gardner B, Wakabayashi J, Sesaki H, Cheng Y, Finkbeiner S, Nussbaum RL, Masliah E, Edwards RH

2011

RNAi screen identifies a role for adaptor protein AP-3 in sorting to the regulated secretory pathway.

The Journal of cell biology

Asensio CS, Sirkis DW, Edwards RH

2010

Metabolic control of vesicular glutamate transport and release.

Neuron

Juge N, Gray JA, Omote H, Miyaji T, Inoue T, Hara C, Uneyama H, Edwards RH, Nicoll RA, Moriyama Y

2010

Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate.

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

Stuber GD, Hnasko TS, Britt JP, Edwards RH, Bonci A

2010

Vesicular monoamine and glutamate transporters select distinct synaptic vesicle recycling pathways.

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

Onoa B, Li H, Gagnon-Bartsch JA, Elias LA, Edwards RH

2010

Vesicular glutamate transport promotes dopamine storage and glutamate corelease in vivo.

Neuron

Hnasko TS, Chuhma N, Zhang H, Goh GY, Sulzer D, Palmiter RD, Rayport S, Edwards RH

2010

Glutamate co-release at GABA/glycinergic synapses is crucial for the refinement of an inhibitory map.

Nature neuroscience

Noh J, Seal RP, Garver JA, Edwards RH, Kandler K

2010

Increased expression of alpha-synuclein reduces neurotransmitter release by inhibiting synaptic vesicle reclustering after endocytosis.

Neuron

Nemani VM, Lu W, Berge V, Nakamura K, Onoa B, Lee MK, Chaudhry FA, Nicoll RA, Edwards RH

2010

Injury-induced mechanical hypersensitivity requires C-low threshold mechanoreceptors.

Nature

Seal RP, Wang X, Guan Y, Raja SN, Woodbury CJ, Basbaum AI, Edwards RH

2009

Fluorescent false neurotransmitters visualize dopamine release from individual presynaptic terminals.

Science (New York, N.Y.)

Gubernator NG, Zhang H, Staal RG, Mosharov EV, Pereira DB, Yue M, Balsanek V, Vadola PA, Mukherjee B, Edwards RH, Sulzer D, Sames D

2009

Interplay between cytosolic dopamine, calcium, and alpha-synuclein causes selective death of substantia nigra neurons.

Neuron

Mosharov EV, Larsen KE, Kanter E, Phillips KA, Wilson K, Schmitz Y, Krantz DE, Kobayashi K, Edwards RH, Sulzer D

2009

Synaptic and extrasynaptic factors governing glutamatergic retinal waves.

Neuron

Blankenship AG, Ford KJ, Johnson J, Seal RP, Edwards RH, Copenhagen DR, Feller MB

2009

What the neuron tells glia.

Neuron

Edwards R

2009

Optical reporters for the conformation of alpha-synuclein reveal a specific interaction with mitochondria.

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

Nakamura K, Nemani VM, Wallender EK, Kaehlcke K, Ott M, Edwards RH

2008

Sensorineural deafness and seizures in mice lacking vesicular glutamate transporter 3.

Neuron

Seal RP, Akil O, Yi E, Weber CM, Grant L, Yoo J, Clause A, Kandler K, Noebels JL, Glowatzki E, Lustig LR, Edwards RH

2008

Pharmacology of neurotransmitter transport into secretory vesicles.

Handbook of experimental pharmacology

Chaudhry FA, Boulland JL, Jenstad M, Bredahl MK, Edwards RH

2008

Vesicular neurotransmitter transporters as targets for endogenous and exogenous toxic substances.

Annual review of pharmacology and toxicology

Chaudhry FA, Edwards RH, Fonnum F

2008

Physiology versus pathology in Parkinson's disease.

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

Nakamura K, Edwards RH

2007

Vesicular glutamate transporter 1 is required for photoreceptor synaptic signaling but not for intrinsic visual functions.

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

Johnson J, Fremeau RT, Duncan JL, Rentería RC, Yang H, Hua Z, Liu X, LaVail MM, Edwards RH, Copenhagen DR

2007

Thyronamines inhibit plasma membrane and vesicular monoamine transport.

ACS chemical biology

Snead AN, Santos MS, Seal RP, Miyakawa M, Edwards RH, Scanlan TS

2007

Do different endocytic pathways make different synaptic vesicles?

Current opinion in neurobiology

Voglmaier SM, Edwards RH

2007

Alpha-synuclein overexpression in PC12 and chromaffin cells impairs catecholamine release by interfering with a late step in exocytosis.

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

Larsen KE, Schmitz Y, Troyer MD, Mosharov E, Dietrich P, Quazi AZ, Savalle M, Nemani V, Chaudhry FA, Edwards RH, Stefanis L, Sulzer D

2006

Synaptic vesicles: half full or half empty?

Neuron

Hnasko TS, Edwards RH

2006

Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recycling.

Neuron

Voglmaier SM, Kam K, Yang H, Fortin DL, Hua Z, Nicoll RA, Edwards RH

2006

PharmGKB submission update: VI. PMT submissions of genetic variations in neurotransmitter transporters (SLC6, SLC17, and SLC18) to the PharmGKB network.

Pharmacological reviews

Badagnani I, Sorani M, Edwards RH, Brown C, Castro RA, Huang CC, Stryke D, Kawamoto M, Johns SJ, Carlson EJ, Taylor T, Chan W, De La Cruz M, Ferrin TE, Burchard EG, Herskowitz I, Kroetz DL, Giacomini KM

2006

Neural activity controls the synaptic accumulation of alpha-synuclein.

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

Fortin DL, Nemani VM, Voglmaier SM, Anthony MD, Ryan TA, Edwards RH

2005

A combinatorial code for the interaction of alpha-synuclein with membranes.

The Journal of biological chemistry

Kubo S, Nemani VM, Chalkley RJ, Anthony MD, Hattori N, Mizuno Y, Edwards RH, Fortin DL

2005

Antidepressants and the monoamine masquerade.

Neuron

Sulzer D, Edwards RH

2005

Expression of the vesicular glutamate transporters during development indicates the widespread corelease of multiple neurotransmitters.

The Journal of comparative neurology

Boulland JL, Qureshi T, Seal RP, Rafiki A, Gundersen V, Bergersen LH, Fremeau RT, Edwards RH, Storm-Mathisen J, Chaudhry FA

2004

Normal biogenesis and cycling of empty synaptic vesicles in dopamine neurons of vesicular monoamine transporter 2 knockout mice.

Molecular biology of the cell

Croft BG, Fortin GD, Corera AT, Edwards RH, Beaudet A, Trudeau LE, Fon EA

2004

Vesicular glutamate transporter 3 expression identifies glutamatergic amacrine cells in the rodent retina.

The Journal of comparative neurology

Johnson J, Sherry DM, Liu X, Fremeau RT, Seal RP, Edwards RH, Copenhagen DR

2004

The effect of rare human sequence variants on the function of vesicular monoamine transporter 2.

Pharmacogenetics

Burman J, Tran CH, Glatt C, Freimer NB, Edwards RH

2004

Lipid rafts mediate the synaptic localization of alpha-synuclein.

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

Fortin DL, Troyer MD, Nakamura K, Kubo S, Anthony MD, Edwards RH

2004

Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites.

Science (New York, N.Y.)

Fremeau RT, Kam K, Qureshi T, Johnson J, Copenhagen DR, Storm-Mathisen J, Chaudhry FA, Nicoll RA, Edwards RH

2004

VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate.

Trends in neurosciences

Fremeau RT, Voglmaier S, Seal RP, Edwards RH

2004

Plasma membrane and vesicular glutamate transporter mRNAs/proteins in hypothalamic neurons that regulate body weight.

The European journal of neuroscience

Collin M, Bäckberg M, Ovesjö ML, Fisone G, Edwards RH, Fujiyama F, Meister B

2003

Organic anion transport is the primary function of the SLC17/type I phosphate transporter family.

Pflugers Archiv : European journal of physiology

Reimer RJ, Edwards RH

2003

The H+-coupled electrogenic lysosomal amino acid transporter LYAAT1 localizes to the axon and plasma membrane of hippocampal neurons.

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

Wreden CC, Johnson J, Tran C, Seal RP, Copenhagen DR, Reimer RJ, Edwards RH

2003

Vesicular neurotransmitter transporter expression in developing postnatal rodent retina: GABA and glycine precede glutamate.

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

Johnson J, Tian N, Caywood MS, Reimer RJ, Edwards RH, Copenhagen DR

2003

The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate.

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

Fremeau RT, Burman J, Qureshi T, Tran CH, Proctor J, Johnson J, Zhang H, Sulzer D, Copenhagen DR, Storm-Mathisen J, Reimer RJ, Chaudhry FA, Edwards RH

2002

The glutamine commute: take the N line and transfer to the A.

The Journal of cell biology

Chaudhry FA, Reimer RJ, Edwards RH

2002

Glutamine uptake by neurons: interaction of protons with system a transporters.

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

Chaudhry FA, Schmitz D, Reimer RJ, Larsson P, Gray AT, Nicoll R, Kavanaugh M, Edwards RH

2002