Robert Edwards, MD
Professor
Neurology
School of Medicine

Using the transporters, he 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 elucidate 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 function of presynaptic protein -synuclein, which has a central, causative role in the disorder. He also identified the first opioid receptor (delta-) and the transporters involved in glutamate recycling. The work in his lab has implications for behavior and neural degeneration, in particular Parkinson's disease.

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.

• Substrate recognition and proton coupling by a bacterial member of solute carrier family 17.
  The Journal of biological chemistry 2023 Batarni S, Nayak N, Chang A, Li F, Hareendranath S, Zhou L, Xu H, Stroud R, Eriksen J, Edwards RH
• 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 2022 Zhang P, Rumschitzki D, Edwards RH
• Diversity of function and mechanism in a family of organic anion transporters.
  Current opinion in structural biology 2022 Li F, Eriksen J, Finer-Moore J, Stroud RM, Edwards RH
• SNX5 targets a monoamine transporter to the TGN for assembly into dense core vesicles by AP-3.
  The Journal of cell biology 2022 Xu H, Chang F, Jain S, Heller BA, Han X, Liu Y, Edwards RH
• Whole Endosome Recording of Vesicular Neurotransmitter Transporter Currents.
  Methods in molecular biology (Clifton, N.J.) 2022 Chang R, Edwards RH
• Allosteric Inhibition of a Vesicular Glutamate Transporter by an Isoform-Specific Antibody.
  Biochemistry 2021 Eriksen J, Li F, Stroud RM, Edwards RH
• The Membrane Interactions of Synuclein: Physiology and Pathology.
  Annual review of pathology 2021 Runwal G, Edwards RH
• 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 2020 Somayaji M, Cataldi S, Choi SJ, Edwards RH, Mosharov EV, Sulzer D
• Ion transport and regulation in a synaptic vesicle glutamate transporter.
  Science (New York, N.Y.) 2020 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
• The mechanism and regulation of vesicular glutamate transport: Coordination with the synaptic vesicle cycle.
  Biochimica et biophysica acta. Biomembranes 2020 Eriksen J, Li F, Edwards RH
• Structures suggest a mechanism for energy coupling by a family of organic anion transporters.
  PLoS biology 2019 Leano JB, Batarni S, Eriksen J, Juge N, Pak JE, Kimura-Someya T, Robles-Colmenares Y, Moriyama Y, Stroud RM, Edwards RH
• Synaptic Vesicle Recycling Pathway Determines Neurotransmitter Content and Release Properties.
  Neuron 2019 Silm K, Yang J, Marcott PF, Asensio CS, Eriksen J, Guthrie DA, Newman AH, Ford CP, Edwards RH
• The dual role of chloride in synaptic vesicle glutamate transport.
  eLife 2018 Chang R, Eriksen J, Edwards RH
• A mouse model of autism implicates endosome pH in the regulation of presynaptic calcium entry.
  Nature communications 2018 Ullman JC, Yang J, Sullivan M, Bendor J, Levy J, Pham E, Silm K, Seifikar H, Sohal VS, Nicoll RA, Edwards RH
• Loss of α-Synuclein Does Not Affect Mitochondrial Bioenergetics in Rodent Neurons.
  eNeuro 2017 Pathak D, Berthet A, Bendor JT, Yu K, Sellnow RC, Orr AL, Nguyen MK, Edwards RH, Manfredsson FP, Nakamura K
• α-Synuclein promotes dilation of the exocytotic fusion pore.
  Nature neuroscience 2017 Logan T, Bendor J, Toupin C, Thorn K, Edwards RH
• Endogenous Leucine-Rich Repeat Kinase 2 Slows Synaptic Vesicle Recycling in Striatal Neurons.
  Frontiers in synaptic neuroscience 2017 Maas JW, Yang J, Edwards RH
• One Cycle Fuels Another: The Energetics of Neurotransmitter Release.
  Neuron 2017 Silm K, Edwards RH
• A slow excitatory postsynaptic current mediated by a novel metabotropic glutamate receptor in CA1 pyramidal neurons.
  Neuropharmacology 2016 Sheng N, Yang J, Silm K, Edwards RH, Nicoll RA
• Sensory-Derived Glutamate Regulates Presynaptic Inhibitory Terminals in Mouse Spinal Cord.
  Neuron 2016 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,…
• Protons Regulate Vesicular Glutamate Transporters through an Allosteric Mechanism.
  Neuron 2016 Eriksen J, Chang R, McGregor M, Silm K, Suzuki T, Edwards RH
• Sex-dependent changes in metabolism and behavior, as well as reduced anxiety after eliminating ventromedial hypothalamus excitatory output.
  Molecular metabolism 2015 Cheung CC, Krause WC, Edwards RH, Yang CF, Shah NM, Hnasko TS, Ingraham HA
• The role of mitochondrially derived ATP in synaptic vesicle recycling.
  The Journal of biological chemistry 2015 Pathak D, Shields LY, Mendelsohn BA, Haddad D, Lin W, Gerencser AA, Kim H, Brand MD, Edwards RH, Nakamura K
• Mobile binding sites regulate glutamate clearance.
  Nature neuroscience 2015 Edwards RH
• Loss of mitochondrial fission depletes axonal mitochondria in midbrain dopamine neurons.
  The Journal of neuroscience : the official journal of the Society for Neuroscience 2014 Berthet A, Margolis EB, Zhang J, Hsieh I, Zhang J, Hnasko TS, Ahmad J, Edwards RH, Sesaki H, Huang EJ, Nakamura K
• Efficient, complete deletion of synaptic proteins using CRISPR.
  Neuron 2014 Incontro S, Asensio CS, Edwards RH, Nicoll RA
• Self-assembly of VPS41 promotes sorting required for biogenesis of the regulated secretory pathway.
  Developmental cell 2013 Asensio CS, Sirkis DW, Maas JW, Egami K, To TL, Brodsky FM, Shu X, Cheng Y, Edwards RH
• Widespread dysregulation of peptide hormone release in mice lacking adaptor protein AP-3.
  PLoS genetics 2013 Sirkis DW, Edwards RH, Asensio CS
• The function of α-synuclein.
  Neuron 2013 Bendor JT, Logan TP, Edwards RH
• Multiple dileucine-like motifs direct VGLUT1 trafficking.
  The Journal of neuroscience : the official journal of the Society for Neuroscience 2013 Foss SM, Li H, Santos MS, Edwards RH, Voglmaier SM
• Ventral tegmental area glutamate neurons: electrophysiological properties and projections.
  The Journal of neuroscience : the official journal of the Society for Neuroscience 2012 Hnasko TS, Hjelmstad GO, Fields HL, Edwards RH
• Restoration of hearing in the VGLUT3 knockout mouse using virally mediated gene therapy.
  Neuron 2012 Akil O, Seal RP, Burke K, Wang C, Alemi A, During M, Edwards RH, Lustig LR
• AMP-activated kinase links serotonergic signaling to glutamate release for regulation of feeding behavior in C. elegans.
  Cell metabolism 2012 Cunningham KA, Hua Z, Srinivasan S, Liu J, Lee BH, Edwards RH, Ashrafi K
• Fabs enable single particle cryoEM studies of small proteins.
  Structure (London, England : 1993) 2012 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
• Vesicular and plasma membrane transporters for neurotransmitters.
  Cold Spring Harbor perspectives in biology 2012 Blakely RD, Edwards RH
• Dopamine dysregulation in a mouse model of paroxysmal nonkinesigenic dyskinesia.
  The Journal of clinical investigation 2012 Lee HY, Nakayama J, Xu Y, Fan X, Karouani M, Shen Y, Pothos EN, Hess EJ, Fu YH, Edwards RH, Ptácek LJ
• Neurotransmitter corelease: mechanism and physiological role.
  Annual review of physiology 2011 Hnasko TS, Edwards RH
• Presynaptic regulation of quantal size: K+/H+ exchange stimulates vesicular glutamate transport.
  Nature neuroscience 2011 Goh GY, Huang H, Ullman J, Borre L, Hnasko TS, Trussell LO, Edwards RH
• v-SNARE composition distinguishes synaptic vesicle pools.
  Neuron 2011 Hua Z, Leal-Ortiz S, Foss SM, Waites CL, Garner CC, Voglmaier SM, Edwards RH
• Pathway-specific genetic attenuation of glutamate release alters select features of competition-based visual circuit refinement.
  Neuron 2011 Koch SM, Dela Cruz CG, Hnasko TS, Edwards RH, Huberman AD, Ullian EM
• Direct membrane association drives mitochondrial fission by the Parkinson disease-associated protein alpha-synuclein.
  The Journal of biological chemistry 2011 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
• RNAi screen identifies a role for adaptor protein AP-3 in sorting to the regulated secretory pathway.
  The Journal of cell biology 2010 Asensio CS, Sirkis DW, Edwards RH
• Metabolic control of vesicular glutamate transport and release.
  Neuron 2010 Juge N, Gray JA, Omote H, Miyaji T, Inoue T, Hara C, Uneyama H, Edwards RH, Nicoll RA, Moriyama Y
• 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 2010 Stuber GD, Hnasko TS, Britt JP, Edwards RH, Bonci A
• Vesicular monoamine and glutamate transporters select distinct synaptic vesicle recycling pathways.
  The Journal of neuroscience : the official journal of the Society for Neuroscience 2010 Onoa B, Li H, Gagnon-Bartsch JA, Elias LA, Edwards RH
• Vesicular glutamate transport promotes dopamine storage and glutamate corelease in vivo.
  Neuron 2010 Hnasko TS, Chuhma N, Zhang H, Goh GY, Sulzer D, Palmiter RD, Rayport S, Edwards RH
• Glutamate co-release at GABA/glycinergic synapses is crucial for the refinement of an inhibitory map.
  Nature neuroscience 2010 Noh J, Seal RP, Garver JA, Edwards RH, Kandler K
• Increased expression of alpha-synuclein reduces neurotransmitter release by inhibiting synaptic vesicle reclustering after endocytosis.
  Neuron 2010 Nemani VM, Lu W, Berge V, Nakamura K, Onoa B, Lee MK, Chaudhry FA, Nicoll RA, Edwards RH
• Injury-induced mechanical hypersensitivity requires C-low threshold mechanoreceptors.
  Nature 2009 Seal RP, Wang X, Guan Y, Raja SN, Woodbury CJ, Basbaum AI, Edwards RH
• Fluorescent false neurotransmitters visualize dopamine release from individual presynaptic terminals.
  Science (New York, N.Y.) 2009 Gubernator NG, Zhang H, Staal RG, Mosharov EV, Pereira DB, Yue M, Balsanek V, Vadola PA, Mukherjee B, Edwards RH, Sulzer D, Sames D
• Interplay between cytosolic dopamine, calcium, and alpha-synuclein causes selective death of substantia nigra neurons.
  Neuron 2009 Mosharov EV, Larsen KE, Kanter E, Phillips KA, Wilson K, Schmitz Y, Krantz DE, Kobayashi K, Edwards RH, Sulzer D
• Synaptic and extrasynaptic factors governing glutamatergic retinal waves.
  Neuron 2009 Blankenship AG, Ford KJ, Johnson J, Seal RP, Edwards RH, Copenhagen DR, Feller MB
• What the neuron tells glia.
  Neuron 2009 Edwards R
• 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 2008 Nakamura K, Nemani VM, Wallender EK, Kaehlcke K, Ott M, Edwards RH
• Sensorineural deafness and seizures in mice lacking vesicular glutamate transporter 3.
  Neuron 2008 Seal RP, Akil O, Yi E, Weber CM, Grant L, Yoo J, Clause A, Kandler K, Noebels JL, Glowatzki E, Lustig LR, Edwards RH
• Pharmacology of neurotransmitter transport into secretory vesicles.
  Handbook of experimental pharmacology 2008 Chaudhry FA, Boulland JL, Jenstad M, Bredahl MK, Edwards RH
• Vesicular neurotransmitter transporters as targets for endogenous and exogenous toxic substances.
  Annual review of pharmacology and toxicology 2008 Chaudhry FA, Edwards RH, Fonnum F
• The neurotransmitter cycle and quantal size.
  Neuron 2007 Edwards RH
• Physiology versus pathology in Parkinson's disease.
  Proceedings of the National Academy of Sciences of the United States of America 2007 Nakamura K, Edwards RH
• 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 2007 Johnson J, Fremeau RT, Duncan JL, Rentería RC, Yang H, Hua Z, Liu X, LaVail MM, Edwards RH, Copenhagen DR
• Thyronamines inhibit plasma membrane and vesicular monoamine transport.
  ACS chemical biology 2007 Snead AN, Santos MS, Seal RP, Miyakawa M, Edwards RH, Scanlan TS
• Do different endocytic pathways make different synaptic vesicles?
  Current opinion in neurobiology 2007 Voglmaier SM, Edwards RH
• 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 2006 Larsen KE, Schmitz Y, Troyer MD, Mosharov E, Dietrich P, Quazi AZ, Savalle M, Nemani V, Chaudhry FA, Edwards RH, Stefanis L, Sulzer D
• Synaptic vesicles: half full or half empty?
  Neuron 2006 Hnasko TS, Edwards RH
• Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recycling.
  Neuron 2006 Voglmaier SM, Kam K, Yang H, Fortin DL, Hua Z, Nicoll RA, Edwards RH
• PharmGKB submission update: VI. PMT submissions of genetic variations in neurotransmitter transporters (SLC6, SLC17, and SLC18) to the PharmGKB network.
  Pharmacological reviews 2006 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 …
• Functional implications of neurotransmitter co-release: glutamate and GABA share the load.
  Current opinion in pharmacology 2005 Seal RP, Edwards RH
• Neural activity controls the synaptic accumulation of alpha-synuclein.
  The Journal of neuroscience : the official journal of the Society for Neuroscience 2005 Fortin DL, Nemani VM, Voglmaier SM, Anthony MD, Ryan TA, Edwards RH
• Sorting of vesicular monoamine transporter 2 to the regulated secretory pathway confers the somatodendritic exocytosis of monoamines.
  Neuron 2005 Li H, Waites CL, Staal RG, Dobryy Y, Park J, Sulzer DL, Edwards RH
• A combinatorial code for the interaction of alpha-synuclein with membranes.
  The Journal of biological chemistry 2005 Kubo S, Nemani VM, Chalkley RJ, Anthony MD, Hattori N, Mizuno Y, Edwards RH, Fortin DL
• Antidepressants and the monoamine masquerade.
  Neuron 2005 Sulzer D, Edwards RH
• Expression of the vesicular glutamate transporters during development indicates the widespread corelease of multiple neurotransmitters.
  The Journal of comparative neurology 2004 Boulland JL, Qureshi T, Seal RP, Rafiki A, Gundersen V, Bergersen LH, Fremeau RT, Edwards RH, Storm-Mathisen J, Chaudhry FA
• Normal biogenesis and cycling of empty synaptic vesicles in dopamine neurons of vesicular monoamine transporter 2 knockout mice.
  Molecular biology of the cell 2004 Croft BG, Fortin GD, Corera AT, Edwards RH, Beaudet A, Trudeau LE, Fon EA
• Vesicular glutamate transporter 3 expression identifies glutamatergic amacrine cells in the rodent retina.
  The Journal of comparative neurology 2004 Johnson J, Sherry DM, Liu X, Fremeau RT, Seal RP, Edwards RH, Copenhagen DR
• The effect of rare human sequence variants on the function of vesicular monoamine transporter 2.
  Pharmacogenetics 2004 Burman J, Tran CH, Glatt C, Freimer NB, Edwards RH
• Lipid rafts mediate the synaptic localization of alpha-synuclein.
  The Journal of neuroscience : the official journal of the Society for Neuroscience 2004 Fortin DL, Troyer MD, Nakamura K, Kubo S, Anthony MD, Edwards RH
• Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites.
  Science (New York, N.Y.) 2004 Fremeau RT, Kam K, Qureshi T, Johnson J, Copenhagen DR, Storm-Mathisen J, Chaudhry FA, Nicoll RA, Edwards RH
• VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate.
  Trends in neurosciences 2004 Fremeau RT, Voglmaier S, Seal RP, Edwards RH
• Plasma membrane and vesicular glutamate transporter mRNAs/proteins in hypothalamic neurons that regulate body weight.
  The European journal of neuroscience 2003 Collin M, Bäckberg M, Ovesjö ML, Fisone G, Edwards RH, Fujiyama F, Meister B
• Organic anion transport is the primary function of the SLC17/type I phosphate transporter family.
  Pflugers Archiv : European journal of physiology 2003 Reimer RJ, Edwards RH
• 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 2003 Wreden CC, Johnson J, Tran C, Seal RP, Copenhagen DR, Reimer RJ, Edwards RH
• 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 2003 Johnson J, Tian N, Caywood MS, Reimer RJ, Edwards RH, Copenhagen DR
• 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 2002 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
• Cell-specific expression of the glutamine transporter SN1 suggests differences in dependence on the glutamine cycle.
  The European journal of neuroscience 2002 Boulland JL, Osen KK, Levy LM, Danbolt NC, Edwards RH, Storm-Mathisen J, Chaudhry FA
• The glutamine commute: take the N line and transfer to the A.
  The Journal of cell biology 2002 Chaudhry FA, Reimer RJ, Edwards RH
• Glutamine uptake by neurons: interaction of protons with system a transporters.
  The Journal of neuroscience : the official journal of the Society for Neuroscience 2002 Chaudhry FA, Schmitz D, Reimer RJ, Larsson P, Gray AT, Nicoll R, Kavanaugh M, Edwards RH