Hostname: page-component-848d4c4894-x5gtn Total loading time: 0 Render date: 2024-05-03T16:45:46.465Z Has data issue: false hasContentIssue false
  • English
  • Français

Vanilloid receptor 1 (TRPV1/VR1) co-localizes with fatty acid amide hydrolase (FAAH) in retinal amacrine cells

Published online by Cambridge University Press:  09 August 2007

SARAH ZIMOV  and
STEPHEN YAZULLA
SARAH ZIMOV
Affiliation:
Graduate Program in Neuroscience, Stony Brook University, Stony Brook, New York Current address: Harkness Eye Institute, Columbia University, Department of Ophthalmology, 630 West 168th Street, New York, New York.
STEPHEN YAZULLA
Affiliation:
Department of Neurobiology and Behavior, Stony Brook University, Stony Brook, New York
Get access Rights & Permissions [Opens in a new window]

Abstract

Fatty acid amide hydrolase (FAAH) is the degradative enzyme for anandamide (AEA), an endogenous ligand for the vanilloid receptor (TRPV1) and cannabinoid receptor 1. As FAAH and TRPV1 are integral membrane proteins, FAAH activity could modulate the availability of AEA for TRPV1 activation. Previous studies in this laboratory reported an extensive endocannabinoid system in goldfish retina. Immunocytochemistry was used to determine the relative distributions of FAAH-immunoreactivity (IR) and TRPV1-IR in goldfish retina. Here, we show the first example in an intact neural system in which TRPV1-IR co-localizes in subpopulations of FAAH-immunoreactive neurons, in this case amacrine cells. These cells are rare and consist of three subtypes: 1. ovoid cell with granular-type dendrites restricted to sublamina a, 2. pyriform cell with smooth processes in sublamina b, and 3. fusiform cell with smooth processes that project to sublaminae a and b. The varied appearances of reaction product in the dendrites suggest different subcellular localization of TRPV1, and hence function of FAAH activity regarding TRPV1 stimulation among the cell types. Ovoid and pyriform amacrine cells, but not fusiform cells, labeled with GAD-IR and constituted subsets of GABAergic amacrine cells. TRPV1 amacrine cells, though rare, are represented in the ON, OFF and ON/OFF pathways of the retina. As TRPV1 stimulation increases intracellular calcium with numerous downstream effects, co-localization of TRPV1 and FAAH suggests an autoregulatory function for anandamide. Due to the rarity of these cells, the three vanilloid amacrine cell types may be involved in global effects rather than feature extraction, for example: sampling of ambient light or maintaining homeostasis.

Keywords

TRPV1vanilloidendocannabinoidretinagoldfishamacrine cell
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 4 , July 2007 , pp. 581 - 591
Copyright
© 2007 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ahluwalia, J., Urban, L., Bevan, S. & Nagy, I. (2003). Anandamide regulates neuropeptide release from capsaicin-sensitive primary sensory neurons by activating both the cannabinoid 1 receptor and the vanilloid receptor 1 in vitro. European Journal of Neuroscience 17, 2611–2618.CrossRefGoogle Scholar
Al-Hayani, A., Wease, K.N., Ross, R.A., Pertwee, R.G. & Davies, S.N. (2001). The endogenous cannabinoid anandamide activates vanilloid receptors in the rat hippocampal slice. Neuropharmacology 41, 1000–1005.CrossRefGoogle Scholar
Brecha, N., Sharma, S.C. & Karten, H.J. (1981). Localization of substance P like immunoreactivity in the adult and developing goldfish retina. Neuroscience 6, 2737–2746.CrossRefGoogle Scholar
Cortright, D.N. & Szallasi, A. (2004). Biochemical pharmacology of the vanilloid receptor TRPV1. European Journal of Biochemistry 271, 1814–1819.CrossRefGoogle Scholar
Craib, S.J., Ellington, H.C., Pertwee, R.G. & Ross, R.A. (2001). A possible role of lipoxygenase in the activation of vanilloid receptors by anandamide in the guinea-pig isolated bronchus. British Journal of Pharmacology 134, 30–37.CrossRefGoogle Scholar
De Petrocellis, L., Bisogno, T., Maccarrone, M., Davis, J.B., Finazzi-Agro, A. & DiMarzo, V. (2001). The activity of anandamide at vanilloid VR1 receptors requires facilitated transport across the cell membrane and is limited by intracellular metabolism. Journal of Biological Chemistry 276, 12856–12863.CrossRefGoogle Scholar
Deutsch, D.G. & Chin, S.A. (1993). Enzymatic synthesis and degradation of anandamide, a cannabinoid receptor agonist. Biochemical Pharmacology 46, 791–796.CrossRefGoogle Scholar
Devane, W.A., Hanus, L., Breuer, A., Pertwee, R.G., Stevenson, L.S., Griffin, G., Gibson, D., Mandelbaum, A., Etinger, A. & Mechoulam, R. (1992). Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258, 1946–1949.CrossRefGoogle Scholar
Diana, M.A. & Marty, A. (2004). Endocannabinoid-mediated short-term synaptic plasticity: Depolarization-induced suppression of inhibition (DSI) and depolarization-induced suppression of excitation (DSE). British Journal of Pharmacology 142, 9–19.CrossRefGoogle Scholar
Dowling, J.E. & Ehinger, B. (1975). Synaptic organization of the amine-containing interplexiform cells of the goldfish and Cebus monkey retinas. Science 188, 270–273.CrossRefGoogle Scholar
Fan, S.F. & Yazulla, S. (2003). Biphasic modulation of voltage-dependent currents of retinal cones by cannabinoid CB1 agonist, WIN 55212-2. Visual Neuroscience 20, 177–188.CrossRefGoogle Scholar
Fan, S.F. & Yazulla, S. (2004). Inhibitory interaction of cannabinoid CB1 receptor and dopamine D2 receptor agonists on voltage-gated currents of goldfish cones. Visual Neuroscience 21, 69–79.CrossRefGoogle Scholar
Fan, S.F. & Yazulla, S. (2005). 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. Visual Neuroscience 22, 55–63.CrossRefGoogle Scholar
Fan, S.F. & Yazulla, S. (2007). Retrograde endocannabinoid inhibition of goldfish retinal cones in mediated by 2-arachidonoyl glycerol. Visual Neuroscience 24, 249–259.CrossRefGoogle Scholar
Fride, E. (2002). Endocannabinoids in the central nervous system—an overview. Prostaglandins Leukotrienes and Essential Fatty Acids 66, 221–233.CrossRefGoogle Scholar
Fride, E. (2005). Endocannabinoids in the central nervous system: From neuronal networks to behavior. Current Drug Targets CNS Neurological Disorders 4, 633–642.CrossRefGoogle Scholar
Glaser, S.T., Deutsch, D.D., Studholme, K.M., Zimov, S. & Yazulla, S. (2005). Endocannabinoids in the intact retina: 3H-anandamide uptake, fatty acid amide hydrolase immunoreactivity and hydrolysis of anandamide. Visual Neuroscience 22, 693–705.CrossRefGoogle Scholar
Goparaju, S.K., Ueda, N., Yamaguchi, H. & Yamamoto, S. (1998). Anandamide amidohydrolase reacting with 2-arachidonoylglycerol, another cannabinoid receptor ligand. FEBS Letters 422, 69–73.CrossRefGoogle Scholar
Gulyas, A.I., Cravatt, B.F., Bracey, M.H., Dinh, T.P., Piomelli, D., Boscia, F. & Freund, T.F. (2004). Segregation of two endocannabinoid-hydrolyzing enzymes into pre- and postsynaptic compartments in the rat hippocampus, cerebellum and amygdala. European Journal of Neuroscience 20, 441–458.CrossRefGoogle Scholar
Huang, S.M., Bisogno, T., Trevisani, M., Al Hayani, A., DePetrocellis, L., Fezza, F., Tognetto, M., Petros, T.J., Krey, J.F., Chu, C.J., Miller, J.D., Davies, S.N., Geppetti, P., Walker, J.M. & DiMarzo, V. (2002). An endogenous capsaicin-like substance with high potency at recombinant and native vanilloid VR1 receptors. Proceedings of the National Academy of Science of the USA 99, 8400–8405.CrossRefGoogle Scholar
Hwang, S.W., Cho, H., Kwak, J., Lee, S.Y., Kang, C.J., Jung, J., Cho, S., Min, K.H., Suh, Y.G., Kim, D. & Oh, U. (2000). Direct activation of capsaicin receptors by products of lipoxygenases: Endogenous capsaicin-like substances. Proceedings of the National Academy of Science of the USA 97, 6155–6160.CrossRefGoogle Scholar
Jung, J., Hwang, S.W., Kwak, J., Lee, S.Y., Kang, C.J., Kim, W.B., Kim, D. & Oh, U. (1999). Capsaicin binds to the intracellular domain of the capsaicin-activated ion channel. Journal of Neuroscience 19, 529–538.Google Scholar
Jung, J., Lee, S.Y., Hwang, S.W., Cho, H., Shin, J., Kang, Y.S., Kim, S. & Oh, U. (2002). Agonist recognition sites in the cytosolic tails of vanilloid receptor 1. Journal of Biochemistry 46, 44448–44454.CrossRefGoogle Scholar
Karai, L., Russell, J.T., Iadarola, M.J. & Olah, Z. (2004). Vanilloid receptor 1 regulates multiple calcium compartments and contributes to Ca2+-induced Ca2+-release in sensory neurons. Journal of Biological Chemistry 279, 16377–16387.CrossRefGoogle Scholar
Kedei, N., Szabo, T., Lile, J.D., Treanor, J.J., Olah, Z., Iadarola, M.J. & Blumberg, P.M. (2001). Analysis of the native quaternary structure of vanilloid receptor 1. Journal of Biological Chemistry 276, 28613–28619.CrossRefGoogle Scholar
Kim, J. & Alger, B.E. (2004). Inhibition of cyclooxygenase-2 potentiates retrograde endocannabinoid effects in hippocampus. Nature Neuroscience 7, 697–698.CrossRefGoogle Scholar
Kozak, K.R. & Marnett, L.J. (2002). Oxidative metabolism of endocannabinoids. Prostaglandins Leukotrienes & Essential Fatty Acids 66, 211–220.CrossRefGoogle Scholar
Lasater, E.M. & Dowling, J.E. (1982). Carp horizontal cells in culture respond selectively to L-glutamate and its agonists. Proceedings of the National Academy of Science of the USA 79, 936–940.CrossRefGoogle Scholar
Li, H., Marshak, D.W., Dowling, J.E. & Lam, D.M.K. (1986). Colocalization of immunoreactive substance P and neurotensin in amacrine cells of the goldfish retina. Brain Research 366, 307–313.Google Scholar
Liu, M., Liu, M.C., Magoulas, C., Priestley, J.V. & Willmott, N.J. (2003). Versatile regulation of cytosolic Ca2+ by vanilloid receptor I in rat dorsal root ganglion neurons. Journal of Cell Biology 278, 5462–5472.CrossRefGoogle Scholar
Maccarrone, M., Salvati, S., Bari, M. & Finazzi-Agro, A. (2000). Anandamide and 2-arachidonoylglycerol inhibit fatty acid amide hydrolase by activation the lipoxygenase pathway of the arachidonate cascade. Biophysics Research Communications 278, 576–583.CrossRefGoogle Scholar
Marc, R.E., Liu, W.L.S. & Muller, J.F. (1988). Gap junctions in the inner plexiform layer of the goldfish retina. Vision Research 28, 9–24.CrossRefGoogle Scholar
Marc, R.E., Murry, R.F. & Basinger, S.F. (1995). Pattern recognition of amino acid signatures in retinal neurons. Journal of Neuroscience 15, 5106–5129.Google Scholar
Marc, R.E., Stell, W.K., Bok, D. & Lam, D.M.K. (1978). GABAergic pathways in the goldfish retina. Journal of Comparative Neurology 182, 221–246.CrossRefGoogle Scholar
Marshak, D.W., Carraway, R.E. & Ferris, C.F. (1987). Characterization of immunoreactive substance P and neurotensin in the goldfish retina. Experimental Eye Research 44, 839–848.CrossRefGoogle Scholar
Marshall, I.C.B., Owen, D.E., Cripps, T.V., Davies, J.B., McNulty, S. & Smart, D. (2003). Activation of vanilloid receptor 1 by resiniferatoxin mobilizes calcium from inositol 1,4,5-trisphosphate-sensitive stores. British Journal of Pharmacology 138, 172–176.CrossRefGoogle Scholar
Mechoulam, R., Ben-Shabat, S., Hanus, L., Ligumdky, M., Kaminski, N.E., Shatz, A.R., Gopher, A., Almog, S., Martin, B.R. & Compton, D.R. (1995). Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochemical Pharmacology 50, 83–90.CrossRefGoogle Scholar
Millns, P.J., Chimenti, M., Ali, N., Ryland, E., de Lago, E., Fernandez-Ruiz, J., Chapman, V. & Kendall, D.A. (2006). Effects of inhibition of fatty acid amide hydrolase vs. the anandamide membrane transporter on TRPV1-mediated calcium responses in adult DRG neurons: The role of CB1 receptors. European Journal of Neuroscience 24, 3489–3495.Google Scholar
Ohno-Shosaku, T., Hashimotodani, Y., Maejima, T. & Kano, M. (2005). Calcium signaling and synaptic modulation: Regulation of endocannabinoid-mediated synaptic modulation by calcium. Cell Calcium 38, 369–374.CrossRefGoogle Scholar
Olah, Z., Szabo, T., Karai, L., Hough, C., Fields, R.D., Caudle, R.M., Blumberg, P.M. & Iadarola, M.J. (2001). Ligand-induced dynamic membrane changes and cell deletion conferred by vanilloid receptor 1. Journal of Biological Chemistry 276, 11021–11030.CrossRefGoogle Scholar
Opere, C.A., Zheng, W.D., Zhao, M., Lee, J.S., Kulkarni, K.H. & Ohia, S.E. (2006). Inhibition of potassium- and ischemia-evoked [3H] D-aspartate release from isolated bovine retina by cannabinoids. Current Eye Research 31, 645–653.CrossRefGoogle Scholar
Pertwee, R.G. (2005). The therapeutic potential of drugs that target cannabinoid receptors or modulate the tissue levels or actions of endocannabinoids. AAPS Journal 7, E625–E654.CrossRefGoogle Scholar
Price, T.J., Patwardhan, A.M., Flores, C.M. & Hargreaves, K.M. (2005). A role for the anandamide membrane transporter in TRPV-1 mediated neurosecretion from trigeminal sensory neurons. Neuropharmacology 49, 25–39.CrossRefGoogle Scholar
Rámon y Cajal, S. (1933). The Structure of the Retina (compiled and translated Thorpe, S.A. & M. Glickstein) 1972, Springfield, Illinois: Charles C. Thomas, Co.
Rosenbaum, T., Awaya, M. & Gordon, S.E. (2002). Subunit modification and association in VR1 ion Channels. BioMed Central Neuroscience 3, 4.Google Scholar
Ross, R.A. (2003). Anandamide and vanilloid TRPV1 receptors. British Journal of Pharmacology 140, 790–801.CrossRefGoogle Scholar
Ross, R.A., Gibson, T.M., Brockie, H.C., Leslie, M., Pashmi, G., Craib, S.J., DiMarzo, V. & Pertwee, R.G. (2001). Structure-activity relationship for the endogenous cannabinoid, anandamide, and certain of its analogues at vanilloid receptors in transfected cells and vas deferens. British Journal of Pharmacology 132, 631–640.CrossRefGoogle Scholar
Sagar, D.R., Smith, P.A., Millns, P.J., Smart, D., Kendall, D.A. & Chapman, V. (2004). TRPV1 and CB receptor-mediated effects of the endovanilloid/endocannabinoid N-arachidonoyl-dopamine on primary afferent fibre and spinal cord neuronal responses in the rat. European Journal of Neuroscience 20, 175–184.CrossRefGoogle Scholar
Sang, N., Zhang, J., Marcheselli, V., Bazan, N.G. & Chen, C. (2005). Postsynaptically synthesized prostaglandin E2 (PGE2) modulates hippocampal synaptic transmission via a presynaptic PGE2 EP2 receptor. Journal of Neuroscience 25, 9858–9870.CrossRefGoogle Scholar
Schorderet, M., Hof, P. & Magistretti, P.J. (1984). The effects of VIP on cyclic AMP and glycogen levels in vertebrate retina. Peptides 5, 295–298.CrossRefGoogle Scholar
Slanina, K.A. & Schweitzer, P. (2005). Inhibition of cyclooxygenase-2 elicits a CB1-mediated decrease of excitatory transmission in rat CA1 hippocampus. Neuropharmacology 49, 653–659.CrossRefGoogle Scholar
Struik, M., Yazulla, S. & Kamermans, M. (2006). Cannabinoid agonist WIN 55212-2 speeds up the cone light offset response in goldfish. Visual Neuroscience 23, 285–293.CrossRefGoogle Scholar
Su, Y.Y.T., Fry, K.R., Lam, D.M.K. & Watt, C.B. (1986). Enkephalin in the goldfish retina. Cellular and Molecular Neurobiology 6, 331–348.CrossRefGoogle Scholar
Teranishi, T., Negishi, K. & Kato, S. (1985). Correlations between photoresponse and morphology of amacrine cells in the carp retina. Neuroscience Research—Supplement 2, S211–S226.CrossRefGoogle Scholar
Teranishi, T., Negishi, K. & Kato, S. (1987). Functional and morphological correlates of amacrine cells in carp retina. Neuroscience 29, 935–950.CrossRefGoogle Scholar
Tsou, K., Noguerón, I., Muthian, S., Sañudo-Peña, M.C., Hillard, C.J., Deutsch, D.G. & Walker, J.M. (1998). Fatty acid amide hydrolase is located preferentially in large neurons in the rat central nervous system as revealed by immunohistochemistry. Neuroscience Letters 254, 1–4.CrossRefGoogle Scholar
Tucker, R.C., Kagaya, M., Page, C.P. & Spina, D. (2001). The endogenous cannabinoid agonist, anandamide stimulates sensory nerves in guinea-pig airways. British Journal of Pharmacology 132, 1127–1135.CrossRefGoogle Scholar
van der Stelt, M. & Di Marzo, V. (2004). Endovanilloids. European Journal of Biochemistry 271, 1827–1834.Google Scholar
van der Stelt, M. & Di Marzo, V. (2005). Cannabinoid receptors and their role in neuroprotection. Neuromolecular Medicine 7, 37–50.CrossRefGoogle Scholar
Yamada, T., Marshak, D., Basinger, S., Walsh, J., Morley, J. & Stell, W.K. (1980). Somatostatin-like immunoreactivity in the retina. Proceedings of the National Academy of Sciences of the USA 77, 1691–1695.CrossRefGoogle Scholar
Yazulla, S., Mosinger, J. & Zucker, C. (1984). Two types of pyriform Ab amacrine cells in the goldfish retina: An EM analysis of 3H-GABA uptake and somatostatin-like immunoreactivity. Brain Research 321, 352–356.CrossRefGoogle Scholar
Yazulla, S. & Studholme, K.M. (2001). Neurochemical anatomy of the zebrafish retina as determined by immunocytochemistry. Journal of Neurocytology 30, 551–592.CrossRefGoogle Scholar
Yazulla, S., Studholme, K.M., McIntosh, H.H. & Deutsch, D.G. (1999). Immunocytochemical localization of cannabinoid CB1 receptor and fatty acid amide hydrolase in rat retina. Journal of Comparative Neurology 415, 80–90.3.0.CO;2-H>CrossRefGoogle Scholar
Yazulla, S., Studholme, K.M., McIntosh, H.H. & Fan, S.F. (2000). Cannabinoid receptors on goldfish retinal bipolar cells: Electron-microscope immunocytochemistry and whole-cell recordings. Visual Neuroscience 17, 391–401.CrossRefGoogle Scholar
Yazulla, S., Studholme, K.M. & Wu, J.-Y. (1986). Comparative distribution of 3H-GABA uptake and GAD immunoreactivity in goldfish retinal amacrine cells: A double-label analysis. Journal of Comparative Neurology 244, 149–162.CrossRefGoogle Scholar
Yazulla, S., Zucker, C.L., Mosinger, J.L. & Studholme, K.M. (1985). Pyriform Ab amacrine cells in the goldfish retina: An EM immunocytochemical/autoradiographical study. In Neurocircuitry in the Retina, A Cajal Memorial, eds. Gallego, A. & Gouras, P., pp. 161–170. Amsterdam: Elsevier Press.
Yu, M., Ives, D. & Ramesha, C.S. (1997). Synthesis of prostaglandin E2 ethanolamide from anandamide by cyclooxygenase-2. Journal of Biological Chemistry 272, 21181–21186.CrossRefGoogle Scholar
Zimov, S. & Yazulla, S. (2004). Localization of vanilloid receptor 1 (TRPV1/VR1)-like inmmunoreactivity in goldfish and zebrafish retinas: Restriction to photoreceptor synaptic ribbons. Journal of Neurocytology 33, 441–452.CrossRefGoogle Scholar
Zygmunt, P.M., Petersson, J., Andersson, D.A., Chuang, H., Sorgard, M., Di Marzo, V., Julius, D. & Hogestatt, E.D. (1999). Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400, 452–457.Google Scholar