Hostname: page-component-745bb68f8f-mzp66 Total loading time: 0 Render date: 2025-01-12T02:44:29.310Z Has data issue: false hasContentIssue false
  • English
  • Français

Scotopic vision in the monkey is modulated by the G protein-coupled receptor 55

Published online by Cambridge University Press:  18 March 2016

JOSEPH BOUSKILA ,
VANESSA HARRAR ,
PASHA JAVADI ,
CHRISTIAN CASANOVA ,
YOSHIO HIRABAYASHI Open the ORCID record for YOSHIO HIRABAYASHI [Opens in a new window] ,
ICHIRO MATSUO ,
JYUNPEI OHYAMA ,
JEAN-FRANÇOIS BOUCHARD Open the ORCID record for JEAN-FRANÇOIS BOUCHARD [Opens in a new window]  and
MAURICE PTITO
JOSEPH BOUSKILA
Affiliation:
School of Optometry, University of Montreal, Montreal, Quebec, Canada Biomedical Sciences, Faculty of Medicine, University of Montreal, Montreal, Quebec, Canada
VANESSA HARRAR
Affiliation:
School of Optometry, University of Montreal, Montreal, Quebec, Canada
PASHA JAVADI
Affiliation:
School of Optometry, University of Montreal, Montreal, Quebec, Canada
CHRISTIAN CASANOVA
Affiliation:
School of Optometry, University of Montreal, Montreal, Quebec, Canada
YOSHIO HIRABAYASHI
Affiliation:
Laboratory for Molecular Membrane Neuroscience, RIKEN Brain Science Institute, Wako, Japan
ICHIRO MATSUO
Affiliation:
Division of Molecular Science, Gunma University, Maebashi, Japan
JYUNPEI OHYAMA
Affiliation:
Division of Molecular Science, Gunma University, Maebashi, Japan
JEAN-FRANÇOIS BOUCHARD*
Affiliation:
School of Optometry, University of Montreal, Montreal, Quebec, Canada
MAURICE PTITO*
Affiliation:
School of Optometry, University of Montreal, Montreal, Quebec, Canada Neuropsychiatry Laboratory and Brainlab, Department of Neuroscience and Pharmacology, University of Copenhagen, Copenhagen, Denmark
*
*Address correspondence to: Maurice Ptito and Jean-François Bouchard, School of Optometry, room 260-7, 3744 Jean-Brillant, University of Montreal, Montreal, Quebec H3T 1P1, Canada. E-mail: [email protected], [email protected]
*Address correspondence to: Maurice Ptito and Jean-François Bouchard, School of Optometry, room 260-7, 3744 Jean-Brillant, University of Montreal, Montreal, Quebec H3T 1P1, Canada. E-mail: [email protected], [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The endogenous cannabinoid system plays important roles in the retina of mice and monkeys via their classic CB1 and CB2 receptors. We have previously reported that the G protein-coupled receptor 55 (GPR55), a putative cannabinoid receptor, is exclusively expressed in rod photoreceptors in the monkey retina, suggesting its possible role in scotopic vision. To test this hypothesis, we recorded full-field electroretinograms (ERGs) after the intravitreal injection of the GPR55 agonist lysophosphatidylglucoside (LPG) or the selective GPR55 antagonist CID16020046 (CID), under light- and dark-adapted conditions. Thirteen vervet monkeys (Chlorocebus sabaeus) were used in this study: four controls (injected with the vehicle dimethyl sulfoxide, DMSO), four injected with LPG and five with CID. We analyzed amplitudes and latencies of the a-wave (photoreceptor responses) and the b-wave (rod and cone system responses) of the ERG. Our results showed that after injection of LPG, the amplitude of the scotopic b-wave was significantly higher, whereas after the injection of CID, it was significantly decreased, compared to the vehicle (DMSO). On the other hand, the a-wave amplitude, and the a-wave and b-wave latencies, of the scotopic ERG responses were not significantly affected by the injection of either compound. Furthermore, the photopic ERG waveforms were not affected by either drug. These results support the hypothesis that GPR55 plays an instrumental role in mediating scotopic vision.

Keywords

G protein-coupled receptor 55LPGCID16020046RetinaElectroretinogramMonkey
Type
Research Article
Information
Visual Neuroscience , Volume 33 , 2016 , E006
Copyright
Copyright © Cambridge University Press 2016 

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

Adams, A.J., Brown, B., Flom, M.C., Jones, R.T. & Jampolsky, A. (1975). Alcohol and marijuana effects on static visual acuity. American Journal of Optometry and Physiological Optics 52, 729–735.CrossRefGoogle ScholarPubMed
Adams, A.J., Brown, B., Haegerstrom-Portnoy, G., Flom, M.C. & Jones, R.T. (1978). Marijuana, alcohol, and combined drug effects on the time course of glare recovery. Psychopharmacology 56, 81–86.CrossRefGoogle ScholarPubMed
Bee, W.H. (2001). Standardized electroretinography in primates: A non-invasive preclinical tool for predicting ocular side effects in humans. Current Opinion in Drug Discovery and Development 4, 81–91.Google ScholarPubMed
Bouskila, J., Burke, M.W., Zabouri, N., Casanova, C., Ptito, M. & Bouchard, J.F. (2012). Expression and localization of the cannabinoid receptor type 1 and the enzyme fatty acid amide hydrolase in the retina of vervet monkeys. Neuroscience 202, 117–130.CrossRefGoogle ScholarPubMed
Bouskila, J., Javadi, P., Casanova, C., Ptito, M. & Bouchard, J.F. (2013a). Muller cells express the cannabinoid CB2 receptor in the vervet monkey retina. Journal of Comparative Neurology 521, 2399–2415.CrossRefGoogle ScholarPubMed
Bouskila, J., Javadi, P., Casanova, C., Ptito, M. & Bouchard, J.F. (2013b). Rod photoreceptors express GPR55 in the adult vervet monkey retina. PLoS One 8, e81080.CrossRefGoogle ScholarPubMed
Bouskila, J., Javadi, P., Palmour, R.M., Bouchard, J.F. & Ptito, M. (2014). Standardized full-field electroretinography in the Green Monkey (Chlorocebus sabaeus). PLoS One 9, e111569.CrossRefGoogle ScholarPubMed
Cécyre, B., Zabouri, N., Huppé-Gourgues, F., Bouchard, J.F. & Casanova, C. (2013). Roles of cannabinoid receptors type 1 and 2 on the retinal function of adult mice. Investigative Ophthalmology and Visual Science 54, 8079–8090.CrossRefGoogle ScholarPubMed
Dawson, W.W., Jimenez-Antillon, C.F., Perez, J.M. & Zeskind, J.A. (1977). Marijuana and vision—After ten years' use in Costa Rica. Investigative Ophthalmology and Visual Science 16, 689–699.Google ScholarPubMed
Duvvuri, S., Majumdar, S. & Mitra, A.K. (2003). Drug delivery to the retina: Challenges and opportunities. Expert Opinion on Biological Therapy 3, 45–56.CrossRefGoogle Scholar
Freund, T.F., Katona, I. & Piomelli, D. (2003). Role of endogenous cannabinoids in synaptic signaling. Physiological Reviews 83, 1017–1066.CrossRefGoogle ScholarPubMed
Guy, A.T., Nagatsuka, Y., Ooashi, N., Inoue, M., Nakata, A., Greimel, P., Inoue, A., Nabetani, T., Murayama, A., Ohta, K., Ito, Y., Aoki, J., Hirabayashi, Y. & Kamiguchi, H. (2015). Neuronal development. Glycerophospholipid regulation of modality-specific sensory axon guidance in the spinal cord. Science 349, 974–977.CrossRefGoogle ScholarPubMed
Henstridge, C.M., Balenga, N.A., Ford, L.A., Ross, R.A., Waldhoer, M. & Irving, A.J. (2009). The GPR55 ligand L-alpha-lysophosphatidylinositol promotes RhoA-dependent Ca2+ signaling and NFAT activation. FASEB Journal 23, 183–193.Google ScholarPubMed
Kargl, J., Balenga, N., Parzmair, G.P., Brown, A.J., Heinemann, A. & Waldhoer, M. (2012). The cannabinoid receptor CB1 modulates the signaling properties of the lysophosphatidylinositol receptor GPR55. Journal of Biological Chemistry 287, 44234–44248.CrossRefGoogle ScholarPubMed
Kiplinger, G.F., Manno, J.E., Rodda, B.E. & Forney, R.B. (1971). Dose-response analysis of the effects of tetrahydrocannabinol in man. Clinical Pharmacology and Therapeutics 12, 650–657.CrossRefGoogle ScholarPubMed
Kreitzer, A.C. & Regehr, W.G. (2001a). Cerebellar depolarization-induced suppression of inhibition is mediated by endogenous cannabinoids. Journal of Neuroscience 21, RC174.CrossRefGoogle ScholarPubMed
Kreitzer, A.C. & Regehr, W.G. (2001b). Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29, 717–727.CrossRefGoogle ScholarPubMed
Kumar, A., Qiao, Z., Kumar, P. & Song, Z.H. (2012). Effects of palmitoylethanolamide on aqueous humor outflow. Investigative Ophthalmology and Visual Science 53, 4416–4425.CrossRefGoogle ScholarPubMed
Liu, B., Song, S., Jones, P.M. & Persaud, S.J. (2015). GPR55: From orphan to metabolic regulator? Pharmacology and Therapeutics 145, 35–42.CrossRefGoogle ScholarPubMed
López, E.M., Tagliaferro, P., Onaivi, E.S. & López-Costa, J.J. (2011). Distribution of CB2 cannabinoid receptor in adult rat retina. Synapse 65, 388–392.CrossRefGoogle ScholarPubMed
Marc, R.E., Jones, B.W., Watt, C.B. & Strettoi, E. (2003). Neural remodeling in retinal degeneration. Progress in Retinal and Eye Research 22, 607–655.CrossRefGoogle ScholarPubMed
Marmor, M.F., Fulton, A.B., Holder, G.E., Miyake, Y., Brigell, M., Bach, M. & International Society for Clinical Electrophysiology of Vision (2009). ISCEV Standard for full-field clinical electroretinography (2008 update). Documenta Ophthalmologica 118, 69–77.CrossRefGoogle Scholar
McCulloch, D.L., Marmor, M.F., Brigell, M.G., Hamilton, R., Holder, G.E., Tzekov, R. & Bach, M. (2015). ISCEV Standard for full-field clinical electroretinography (2015 update). Documenta Ophthalmologica 130, 1–12.CrossRefGoogle Scholar
Miller, R.F. & Dowling, J.E. (1970). Intracellular responses of the Muller (glial) cells of mudpuppy retina: Their relation to b-wave of the electroretinogram. Journal of Neurophysiology 33, 323–341.CrossRefGoogle ScholarPubMed
Nair, G., Kim, M., Nagaoka, T., Olson, D.E., Thule, P.M., Pardue, M.T. & Duong, T.Q. (2011). Effects of common anesthetics on eye movement and electroretinogram. Documenta Ophthalmologica 122, 163–176.CrossRefGoogle ScholarPubMed
Noyes, R. Jr., Brunk, S.F., Avery, D.A. & Canter, A.C. (1975). The analgesic properties of delta-9-tetrahydrocannabinol and codeine. Clinical Pharmacology and Therapeutics 18, 84–89.CrossRefGoogle ScholarPubMed
Ohno-Shosaku, T., Maejima, T. & Kano, M. (2001). Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29, 729–738.CrossRefGoogle ScholarPubMed
Oka, S., Nakajima, K., Yamashita, A., Kishimoto, S. & Sugiura, T. (2007). Identification of GPR55 as a lysophosphatidylinositol receptor. Biochemical and Biophysical Research Communications 362, 928–934.CrossRefGoogle ScholarPubMed
Perlman, I. (1983). Relationship between the amplitudes of the b wave and the a wave as a useful index for evaluating the electroretinogram. British Journal of Ophthalmology 67, 443–448.CrossRefGoogle Scholar
Robson, J.G. & Frishman, L.J. (1995). Response linearity and kinetics of the cat retina: The bipolar cell component of the dark-adapted electroretinogram. Visual Neuroscience 12, 837–850.CrossRefGoogle ScholarPubMed
Ryberg, E., Larsson, N., Sjogren, S., Hjorth, S., Hermansson, N.O., Leonova, J., Elebring, T., Nilsson, K., Drmota, T. & Greasley, P.J. (2007). The orphan receptor GPR55 is a novel cannabinoid receptor. British Journal of Pharmacology 152, 1092–1101.CrossRefGoogle ScholarPubMed
Sampath, A.P. & Rieke, F. (2004). Selective transmission of single photon responses by saturation at the rod-to-rod bipolar synapse. Neuron 41, 431–443.CrossRefGoogle ScholarPubMed
Steinberg, R.H., Linsenmeier, R.A. & Griff, E.R. (1985). Retinal pigment epithelial cell contributions to the electroretinogram and electrooculogram. Progress in Retinal Research 4, 33–66.CrossRefGoogle Scholar
Straiker, A., Stella, N., Piomelli, D., Mackie, K., Karten, H.J. & Maguire, G. (1999a). Cannabinoid CB1 receptors and ligands in vertebrate retina: Localization and function of an endogenous signaling system. Proceedings of the National Academy of Sciences of the United States of America 96, 14565–14570.CrossRefGoogle ScholarPubMed
Straiker, A.J., Maguire, G., Mackie, K. & Lindsey, J. (1999b). Localization of cannabinoid CB1 receptors in the human anterior eye and retina. Investigative Ophthalmology and Visual Science 40, 2442–2448.Google ScholarPubMed
Sylantyev, S., Jensen, T.P., Ross, R.A. & Rusakov, D.A. (2013). Cannabinoid- and lysophosphatidylinositol-sensitive receptor GPR55 boosts neurotransmitter release at central synapses. Proceedings of the National Academy of Sciences of the United States of America 110, 5193–5198.CrossRefGoogle ScholarPubMed
Tian, N. & Slaughter, M.M. (1995). Correlation of dynamic responses in the ON bipolar neuron and the b-wave of the electroretinogram. Vision Research 35, 1359–1364.CrossRefGoogle ScholarPubMed
Wen, R. & Oakley, B. II (1990). K(+)-evoked Muller cell depolarization generates b-wave of electroretinogram in toad retina. Proceedings of the National Academy of Sciences of the United States of America 87, 2117–2121.CrossRefGoogle ScholarPubMed
Wilson, R.I. & Nicoll, R.A. (2001). Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410, 588–592.CrossRefGoogle ScholarPubMed
Yazulla, S. (2008). Endocannabinoids in the retina: From marijuana to neuroprotection. Progress in Retinal and Eye Research 27, 501–526.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Zabouri, N., Bouchard, J.F. & Casanova, C. (2011a). Cannabinoid receptor type 1 expression during postnatal development of the rat retina. Journal of Comparative Neurology 519, 1258–1280.CrossRefGoogle ScholarPubMed
Zabouri, N., Ptito, M., Casanova, C. & Bouchard, J.F. (2011b). Fatty acid amide hydrolase expression during retinal postnatal development in rats. Neuroscience 195, 145–165.CrossRefGoogle ScholarPubMed