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Architecture of cannabinoid signaling in mouse retina

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Try out PMC Labs and tell us what you think. Learn More. Cannabinoid receptors and their ligands constitute an endogenous signaling system that is found throughout the body, including the eye. Cannabinoids offer considerable therapeutic potential in modulating ocular immune and inflammatory responses and in regulating intraocular pressure. The location of cannabinoid receptors 1 CB 1 in the retina is known, but recently a constellation of proteins has been identified that produce and break down endocannabinoids eCBs and modulate CB 1 function. Localization of these proteins is critical to defining specific cannabinoid signaling circuitry in the retina. These results taken together with previous anatomic and functional studies define specific cannabinoid circuitry likely to modulate eCB signaling at the first synapse of the retina as well as in the inner plexiform layer IPL. Cannabinoid receptors and their ligands constitute an endogenous signaling system that is found throughout the body, and is particularly prominent in the nervous system Devane et al. Significant strides have been made to advance our understanding of the cannabinoid signaling system since the identification of the two known cannabinoid receptors 1 and 2 — CB 1 and CB 2 Matsuda et al. Two important identified roles for CB 1 , the major subtype found in the brain, are retrograde inhibition of neurotransmission and mediation of long-term depression of synaptic responses Kreitzer and Regehr, ; Sjostrom et al. A variety of visual effects of cannabinoids have been reported in the literature reviewed in Yazulla Taken together these studies cautiously suggest the existence of cannabinoid-mediated visual effects, particularly an enhancement of light sensitivity a common theme , most marked at higher exposures. Matsuda et al. In addition, homogenates of iris, choroid, optic nerve and lacrimal gland but not lens also hydrolyzed AEA. In , Schlicker et al. Schlicker et al. Shortly afterward, Buckley et al. Buckley et al. They detected two bands of expression appearing at different embryonic stages, but anatomical identification of these layers was not possible. In addition, Porcella et al. Porcella et al. Localization of CB 1 receptors was investigated in several vertebrate species using immunocytochemical approaches Straiker et al. Both papers reported CB 1 labeling in subsets of amacrine cells and in horizontal cells as well as dense labeling in the inner plexiform layer IPL. We also reported labeling in rod and cone photoreceptor terminals while Yazulla and colleagues Yazulla et al. This latter group also described labeling with an antibody to fatty acid amide hydrolase FAAH , an enzyme known to hydrolyze the candidate eCB anandamide Cravatt et al. In the rat, they detected FAAH immunoreactivity in large ganglion cells with processes proximal to the ganglion cell layer, in the somata of horizontal cells, in large dopaminergic amacrine cells and in the dendrites of starburst amacrine cells. Bisogno Bisogno et al. Significantly, the disposition of endogenous cannabinoids — the conditions of their production, transport, and breakdown—remains poorly understood. The next step in elucidating the retinal eCB signaling system is to understand its functional role. A key obstacle to achieving this step is that we don't know where in the retina eCBs are produced and broken down. Cannabinoids often act in a retrograde manner, so if CB 1 resides at presynaptic terminals of cone and rod photoreceptors as they do in monkey Straiker et al. In principle, the source could be horizontal, bipolar of which there are ten sub-types in the mouse Wassle et al. But in mammalian systems, to date only one study using mammalian retinal neurons has been reported Lalonde et al. This study describes cannabinoid receptor-mediated inhibition of calcium signaling in ganglion cells, in neurons cultured from rat retinae. These studies represent important contributions and a promising start on the way to a circuit-based exploration of cannabinoid signaling in the mammalian retina. The advent of mouse models with specific populations of fluorescent neurons opens the possibility of targeted electrophysiological dissection of specific retinal circuits. However, for these studies to proceed in a rational fashion a comprehensive understanding of where eCBs are produced and broken down in the retina is required. The pantheon of proteins involved in eCB signaling has been substantially expanded and refined over the past decade, and reliable antibodies against these proteins have slowly come to be available. To this end, we have conducted an extensive immunocytochemical study of cannabinoid-related proteins in retina of the mouse. Eyes were removed, and the anterior eye section cut away, forming an eyecup, from which the retina was scooped. Tissue sections were mounted onto Superfrost-plus slides, washed, treated with a detergent Triton-X, 0. Yanagawa's permission. All primary antibodies, the immunogen used in their generation, their sources, and their working dilutions are listed in Table 1. Bracey et al. Each fusion protein was purified from BL21 E. The antiserum was purified in two steps, first by exclusion on a GST column and then by binding to and elution from an affinity column made with the rNAAA fusion protein C. The fusion protein was purified from BL21 E. Images were modified only in terms of brightness and contrast. The calbindin-D28K CB antibody recognized a single band of 28 kDa on Western blots of rat brain manufacturer's datasheet , and stained a pattern of cellular morphology and distribution in the mouse retina that is identical with previous reports Haverkamp and Wassle, Specificity of the parvalbumin antibody was demonstrated by the absence of immunostaining by this antibody in the parvalbumin knockout mouse Burette et al. The specificity of the GAD65 antibody was established by the recognition of a single band of 64 kDa representing glutamic acid decarboxylase GAD by Western blotting Chang and Gottlieb, ; Jevince et al. The SV2 antibody recognizes a 78 kDa transmembrane proteoglycan that is present at synapses in the central and peripheral nervous systems by Western blotting manufacturer's datasheet. The MAP2 antibody stained a single band of kDa on Western blots of adult rat brain extract manufacturer's datasheet. PKC is a well-characterized marker for rod bipolar cells in retina of many species Haverkamp and Wassle, The recoverin antibody recognized a 25 kDa band on Western blots of mouse retina Hendrickson et al. This calcium-binding protein has been detected in both rod and cone photoreceptors and in three populations of cone bipolar cells in the mouse as well as in midget bipolar cells of the primate Haverkamp et al. The NK3-R antibody stained a population of cone bipolar cells consistent with that described in previous reports Casini et al. This is consistent with a role in postsynaptic production of eCBs followed by retrograde movement of 2-AG across the synapse to act at presynaptic CB 1 receptors. The OPL labeling is restricted to large intermittent clusters in the proximal OPL, suggestive of the postsynaptic terminal of a cone bipolar cell. The rod bipolar cell marker PKC Negishi et al. K CB 1 red costaining with PSD95, which outlines rod spherules arrows and cone pedicles angled arrows shows CB 1 present within terminals of both rod and cone photoreceptor terminals. A magenta-green version of this figure is available as Supplementary Figure 1. Cannabinoid CB 1 receptors have been detected in retinas of mouse and other species Straiker et al. Although CB 1 clearly labeled cone photoreceptor terminals in primate, it was important to establish that cone terminals in mouse similarly express CB 1. Calbindin in the OPL of the mouse labels the processes and somata of horizontal cells Rabie et al. CB 1 staining was detected in the same region as calbindin, but did not colocalize with calbindin Fig 1I. CB 1 is clearly present within both rod spherules arrowheads and cone terminals angled arrows. Thus, we can conclude that pre- and post-synaptic components of an eCB signaling system are closely juxtaposed in the OPL. A magenta-green version of this figure is available as Supplementary Figure 2. These mice have been used as model system for the study of inhibitory neurons in the brain Fukushima et al. As revealed by functional and biochemical studies, several enzymes are involved in 2-AG degradation, chief among them including MGL, blockade of which has been shown to sharply prolong depolarization-induced suppression of inhibition DSI Hashimotodani et al. This proved to be the case. F MGL red costaining with PSD95 green , a marker that outlines rod and cone terminals shows MGL within a cone terminal arrow as well as punctate staining within multiple rod spherules. A magenta-green version of this figure is available as Supplementary Figure 3. However, this was not observed Fig. A magenta-green version of this figure is available as Supplementary Figure 4. B Costaining with calbindin reveals clear overlap with calbindin-positive amacrine cells arrows. A magenta-green version of this figure is available as Supplementary Figure 5. The cannabinoid receptor interacting protein 1a CRIP1a remains an enigma. Identified in a yeast two hybrid screen Niehaus et al. However, the protein remains the focus of considerable interest and our group developed an antibody against it to investigate whether and to what extent the protein colocalized with CB 1. If the protein does not colocalize with CB 1 , this would argue against functional interaction. The present study represents the first effort to examine this putative colocalization. To determine where CRIP1a is expressed in mouse retina, we developed an antibody against this protein. C DAPI staining identifies cell nuclei arrowheads. The non-transfected cells are not labeled with the hCRIP1a antibody. A magenta-green version of this figure is available as Supplementary Figure 6. Costaining with the marker calbindin which labels horizontal cells including their dendritic invaginations into rod photoreceptor terminals shows the relative location of the CRIP1a staining is proximal to the mass of rod photoreceptor terminals Fig 5G, H, arrows. We therefore proceeded to test CRIP1a against PSD95, which generally labels postsynaptic densities in the brain, but instead reliably outlines rod spherules and cone pedicles in retina Koulen et al. A magenta-green version of this figure is available as Supplementary Figure 7. A magenta-green version of this figure is available as Supplementary Figure 8. Its localization has been described in the retina of the rat and goldfish Yazulla et al. In contrast to its distribution in the rat, FAAH does not appear to colocalize with horizontal cell bodies or processes as labeled by calbindin Fig 9F, G. Finally, FAAH colocalizes with CB 1 not only in rod terminals as noted above, but also in amacrine and ganglion cells. Fig 9H. F FAAH green is not expressed in calbindin red -positive horizontal cell body. G FAAH green also does not costain with calbindin red -positive horizontal axonal terminals arrows. A magenta-green version of this figure is available as Supplementary Figure 9. To determine where NAAA is expressed in mouse retina, we developed an antibody against this protein. A DAPI staining identifies cell nuclei arrowheads. The non-transfected cells are not labeled with the rNAAA antibody. A magenta-green version of this figure is available as Supplementary Figure These findings are important because although the presence of cannabinoid CB 1 receptors as well as several candidate eCBs in the vertebrate retina is now well-established Bisogno et al. Nor has a systematic study of enzymes involved in eCB metabolism been done in murine retina. Thus, although CB 1 is believed to be present in rod and cone photoreceptor terminals and in rod bipolar cells in the IPL, the remaining components of these circuits remain unknown. A series of functional studies have demonstrated that cannabinoids affect retinal physiology, however these studies were performed in salamander and goldfish, or in cultured neurons Fan and Yazulla, ; ; ; Lalonde et al. The current study fills important gaps in our current understanding of cannabinoid retinal circuitry in an important, genetically pliable model — the mouse. Recent efforts to systematically categorize mouse bipolar cells suggest that the mouse retina is home to one population of rod bipolar cells and nine cone bipolar cells Ghosh et al. They are known to terminate in the most proximal portion of the IPL and exhibit a kainate response Hartveit, As OFF bipolar cells, they are expected to activate when a cone-stimulating light signal is turned off. Because glutamate release is decreased with light, and increased in darkness, OFF bipolar cells have a sign-conserving configuration in terms of glutamate release and post-synaptic activation. As such, the standard model of cannabinoid retrograde feedback inhibition would predict an inhibition of presynaptic glutamate release via activation of presynaptic CB 1 receptors. This could occur via inhibition of Ca channels as it does in salamander cone photoreceptors Straiker and Sullivan, The reverse may also be true. The mechanisms for production of AEA are less clear. MGL is therefore well-positioned to break down 2-AG after retrograde release onto both rod and cone terminals. MGL positive processes were widely distributed, suggesting roles in numerous circuits, but we were able to rule out expression in GAD65 containing inhibitory neurons, indicating that MGL is limited to excitatory neurons in the IPL. At least some of ABHD6 staining is post-synaptic, consistent with dendrites of ganglion or displaced amacrine cells. The postsynaptic staining is less consistent with a role in breaking down eCBs after retrograde transmission. However, there is evidence for post-synaptic actions of CB 1 Bacci et al. In the absence of information regarding likely AEA synthesis, it is impossible to identify cannabinoid circuits for AEA. Yazulla and colleagues detected FAAH immunoreactivity in large ganglion cells with processes proximal to the ganglion cell layer, in the somata of horizontal cells, a population of cone bipolar cells, large dopaminergic amacrine cells and in the dendrites of starburst amacrine cells in rat retina Yazulla et al. The mouse labeling is consistent with rat in terms of the presence of a FAAH positive cone bipolar cell population, at least one amacrine cell population and substantial neuronal labeling in the ganglion cell layer. The most notable difference between mouse and rat staining is the absence of staining in horizontal cells of the mouse, possibly a function of species difference. Our use of mouse FAAH knockout controls add confidence both to our results and to those previously obtained for the rat. The study of acyl amides in ocular pathology remains in its infancy, but there is evidence that these lipids are involved in ocular pathology. Decreased levels of PEA and 2-AG have been observed in ocular tissues of glaucoma patients, while increased levels of acyl amides including modest increases in PEA levels have been seen including modest increases in PEA levels have been seen in retinae and assorted portions of anterior eyes of patients with diabetic retinopathy Chen et al. However it remains uncertain whether such an interaction actually occurs naturally in cells, particularly in neurons. We detected a close juxtaposition of CRIP1a and CB 1 in cone terminals, leaving open the possibility that they associate in these cells. OFF cone bipolar cells hyperpolarize with light activation of cones. One plausible mechanism of 2-AG production in OFF 1 cone bipolar cells would be a darkness-induced release of glutamate followed by calcium-permeable kainate receptor activation in bipolar cells. Retrograde 2-AG may then act on photoreceptor calcium currents. For instance, in the salamander, cone calcium currents are inhibited by the cannabinoid receptor agonist WIN Straiker and Sullivan, This would represent a feedback inhibition of the OFF cone bipolar cells. Depending on the timing and degree of spread of 2-AG, neighboring rod cells might be modulated by the 2-AG produced by cone bipolar cells. In salamander, rod calcium current responses are potentiated by cannabinoids. However, how cannabinoids influence calcium dynamics in murine rod photoreceptor terminals remains to be determined. In conclusion, the CB 1 cannabinoid signaling system is composed of CB 1 receptors and an assortment of proteins that produce and break down eCBs as well as proteins that may interact with CB 1. We have made use of antibodies against many of the proteins suspected or known to fill these roles. This gives us an intriguing view of the synaptic architecture of cannabinoid signaling in the murine retina. Our results point to separate retrograde signaling circuitry at Type 1 OFF bipolar cell-cone photoreceptor synapses and at bipolar cell-rod photoreceptor synapses. National Center for Biotechnology Information , U. J Comp Neurol. Author manuscript; available in PMC Sep Hutchens , 1 Josh Radicke , 1 Benjamin F. Find articles by Sherry Shu-Jung Hu. Find articles by Andy Arnold. Jacqueline M. Find articles by Jacqueline M. Find articles by Josh Radicke. Benjamin F. Find articles by Benjamin F. Find articles by Jim Wager-Miller. Find articles by Ken Mackie. Find articles by Alex Straiker. Author information Copyright and License information Disclaimer. Copyright notice. The publisher's final edited version of this article is available at J Comp Neurol. See other articles in PMC that cite the published article. Supp Fig s Abstract Cannabinoid receptors and their ligands constitute an endogenous signaling system that is found throughout the body, including the eye. Reports of visual effects of cannabinoids A variety of visual effects of cannabinoids have been reported in the literature reviewed in Yazulla Endocannabinoids in retina Bisogno Bisogno et al. Toward an understanding of the role of endocannabinoids in retinal function The next step in elucidating the retinal eCB signaling system is to understand its functional role. Antibody Characterization All primary antibodies, the immunogen used in their generation, their sources, and their working dilutions are listed in Table 1. Table 1 Antibodies used in this study. Antibody Immunogen Manufacturer, catalog number, species, mono- vs. Open in a separate window. Figure 1. Figure 2. MGL is present in rod spherules and cone pedicles in the OPL and is expressed prominently in two laminae of the IPL As revealed by functional and biochemical studies, several enzymes are involved in 2-AG degradation, chief among them including MGL, blockade of which has been shown to sharply prolong depolarization-induced suppression of inhibition DSI Hashimotodani et al. Figure 3. Figure 4. Figure 5. Cannabinoid receptor interacting protein 1a CRIP1a expression is limited to a population of calbindin-positive amacrine cells and to presynaptic terminals of cone photoreceptors juxtaposed to Type 1 OFF cone bipolar cells The cannabinoid receptor interacting protein 1a CRIP1a remains an enigma. Figure 6. Figure 7. Figure 8. Figure 9. Figure Functional implications OFF cone bipolar cells hyperpolarize with light activation of cones. Supplementary Material Supp Fig s01 Click here to view. Supp Fig s10 Click here to view. Supp Fig s02 Click here to view. Supp Fig s03 Click here to view. Supp Fig s04 Click here to view. Supp Fig s05 Click here to view. Supp Fig s06 Click here to view. Supp Fig s07 Click here to view. Supp Fig s08 Click here to view. Supp Fig s09 Click here to view. Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids. J Biol Chem. Differential expression of neuronal calcium sensor-1 in the developing chick retina. Biosynthesis and inactivation of N-arachidonoylethanolamine anandamide and N-docosahexaenoylethanolamine in bovine retina. Arch Biochem Biophys. Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J Cell Biol. A comprehensive profile of brain enzymes that hydrolyze the endocannabinoid 2-arachidonoylglycerol. Endocannabinoid signaling in rat somatosensory cortex: laminar differences and involvement of specific interneuron types. J Neurosci. Structural adaptations in a membrane enzyme that terminates endocannabinoid signaling. Cell Mol Neurobiol. Developmental expression of neurokinin-1 and neurokinin-3 receptors in the rat retina. Characterization of the proteins purified with monoclonal antibodies to glutamic acid decarboxylase. Finding of endocannabinoids in human eye tissues: implications for glaucoma. Biochem Biophys Res Commun. Endocannabinoid-mediated synaptic plasticity in the CNS. Annu Rev Neurosci. Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Brain monoglyceride lipase participating in endocannabinoid inactivation. Biphasic modulation of voltage-dependent currents of retinal cones by cannabinoid CB1 receptor agonist WIN Vis Neurosci. Inhibitory interaction of cannabinoid CB1 receptor and dopamine D2 receptor agonists on voltage-gated currents of goldfish cones. Reciprocal inhibition of voltage-gated potassium currents I K V by activation of cannabinoid CB1 and dopamine D1 receptors in ON bipolar cells of goldfish retina. Facilitatory actions of serotonin type 3 receptors on GABAergic inhibitory synaptic transmission in the spinal superficial dorsal horn. J Neurophysiol. Retinal organization in the retinal degeneration 10 rd10 mutant mouse: a morphological and ERG study. Types of bipolar cells in the mouse retina. Endocannabinoids in the intact retina: 3 H-anandamide uptake, fatty acid amide hydrolase immunoreactivity and hydrolysis of anandamide. Segregation of two endocannabinoid-hydrolyzing enzymes into pre- and postsynaptic compartments in the rat hippocampus, cerebellum and amygdala. Eur J Neurosci. N-acylphosphatidylethanolamine-hydrolyzing phospholipase D is an important determinant of uterine anandamide levels during implantation. Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Functional organization of cone bipolar cells in the rat retina. Presynaptic monoacylglycerol lipase activity determines basal endocannabinoid tone and terminates retrograde endocannabinoid signaling in the hippocampus. Immunocytochemical description of five bipolar cell types of the mouse retina. Immunocytochemical analysis of the mouse retina. Expression of synaptic and phototransduction markers during photoreceptor development in the marmoset monkey Callithrix jacchus. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. Cannabinoid physiology and pharmacology: 30 years of progress. Distribution of EphB receptors and ephrin-B1 in the developing vertebrate spinal cord. Nigral inhibition of GABAergic neurons in mouse superior colliculus. Endocannabinoid-mediated control of synaptic transmission. Physiol Rev. Molecular composition of the endocannabinoid system at glutamatergic synapses. Inhibition of cyclooxygenase-2 potentiates retrograde endocannabinoid effects in hippocampus. Nat Neurosci. Immunocytochemical localization of the postsynaptic density protein PSD in the mammalian retina. Oxygenation of the endocannabinoid, 2-arachidonylglycerol, to glyceryl prostaglandins by cyclooxygenase Inhibition of interneuron firing extends the spread of endocannabinoid signaling in the cerebellum. Cerebellar depolarization-induced suppression of inhibition is mediated by endogenous cannabinoids. Cannabinoid receptor-mediated inhibition of calcium signaling in rat retinal ganglion cells. Mol Vis. Inactivation of N-acyl phosphatidylethanolamine phospholipase D reveals multiple mechanisms for the biosynthesis of endocannabinoids. TRPV1 channels control synaptic plasticity in the developing superior colliculus. J Physiol. Changes in endocannabinoid and palmitoylethanolamide levels in eye tissues of patients with diabetic retinopathy and age-related macular degeneration. Prostaglandins Leukot Essent Fatty Acids. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Metabolism of anandamide, an endogenous cannabinoid receptor ligand, in porcine ocular tissues. Exp Eye Res. Identification of the sites of 2-arachidonoylglycerol synthesis and action imply retrograde endocannabinoid signaling at both GABAergic and glutamatergic synapses in the ventral tegmental area. Acta Ophthalmol. Structure and function of fatty acid amide hydrolase. Annu Rev Biochem. Recoverin immunoreactivity in mammalian cone bipolar cells. Molecular characterization of a peripheral receptor for cannabinoids. Dopamine cells and rod bipolar cells contain protein kinase C-like immunoreactivity in some vertebrate retinas. Neurosci Lett. CB1 cannabinoid receptor activity is modulated by the cannabinoid receptor interacting protein CRIP 1a. Mol Pharmacol. Immunocytochemical localization of microtubule-associated proteins 1A and 2 in the rat retina. Brain Res. Molecular characterization of a phospholipase D generating anandamide and its congeners. Comparative characterization of a wild type and transmembrane domain-deleted fatty acid amide hydrolase: identification of the transmembrane domain as a site for oligomerization. Bipolar cells of the mouse retina: a gene gun, morphological study. Cannabinoid receptor CB1 mRNA is highly expressed in the rat ciliary body: implications for the antiglaucoma properties of marihuana. Brain Res Mol Brain Res. Immunocytochemical detection of 28 MW calcium-binding protein in horizontal cells of the rat retina. Cell Tissue Res. An endogenous cannabinoid as an endothelium-derived vasorelaxant. Involvement of a cannabinoid in endothelium-derived hyperpolarizing factor-mediated coronary vasorelaxation. Eur J Pharmacol. Anandamide and endothelium-derived hyperpolarizing factor act via a common vasorelaxant mechanism in rat mesentery. Endocannabinoids: a new class of vasoactive substances. Trends Pharmacol Sci. Immunocytochemical labelling of horizontal cells in mammalian retina using antibodies against calcium-binding proteins. Cannabinoid receptor-mediated inhibition of dopamine release in the retina. Naunyn Schmiedebergs Arch Pharmacol. Target cells of vitamin D in the vertebrate retina. Acta Anat Basel ; 3 — The cannabinoid agonist Win55, inhibits calcium channels by receptor-mediated and direct pathways in cultured rat hippocampal neurons. Retinal on-bipolar cells contain a nitric oxide-sensitive guanylate cyclase. Selective N-acylethanolamine-hydrolyzing acid amidase inhibition reveals a key role for endogenous palmitoylethanolamide in inflammation. A second endogenous cannabinoid that modulates long-term potentiation. Monoacyl glycerol lipase MGL limits the duration of endocannabinoid-mediated depolarization-induced suppression of excitation DSE in autaptic hippocampal neurons. Cannabinoid signaling in inhibitory autaptic hippocampal neurons. 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Cone contacts, mosaics, and territories of bipolar cells in the mouse retina. Journal of Neuroscience. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Endocannabinoids in the retina: from marijuana to neuroprotection. Prog Retin Eye Res. Immunocytochemical localization of cannabinoid CB1 receptor and fatty acid amide hydrolase in rat retina. Cannabinoid receptors on goldfish retinal bipolar cells: electron-microscope immunocytochemistry and whole-cell recordings. Support Center Support Center. External link. Please review our privacy policy. Mackie lab Straiker et al. Mackie lab characterized in this study , rabbit polyclonal. Mackie lab Berghuis et al. Mackie lab Bodor et al. Cravatt lab Bracey et al. Sigma-Aldrich, St. Louis, MO, C, mouse monoclonal. Louis, MO, P, mouse monoclonal. Affinity-purified glutamic acid decarboxylase GAD65 from rat brain. Synaptic vesicles purified from the Ommata electric organ. Microtubule-associated protein 2 MAP2 purified from rat brain. Synthetic peptide of the C-terminus of rat NK-3 aa — conjugated to bovine thyroglobulin. Abcam, Cambridge, MA, ab7, rabbit polyclonal.

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