Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-28T04:33:31.202Z Has data issue: false hasContentIssue false
  • English
  • Français

Immunolocalization of metabotropic glutamate receptors 1 and 5 in the synaptic layers of the chicken retina

Published online by Cambridge University Press:  24 April 2006

MADHUMITA SEN  and
EVANNA GLEASON
MADHUMITA SEN
Affiliation:
Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana
EVANNA GLEASON
Affiliation:
Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana
Get access Rights & Permissions [Opens in a new window]

Abstract

We have examined the distribution of metabotropic glutamate receptors (mGluRs) 1 and 5 in the adult chicken retina using preembedding immuno-electronmicroscopy. Immunoreactivity for mGluRs 1 and 5 was found in both the outer plexiform layer (OPL) and the inner plexiform layer (IPL). For mGluR1, OPL labeling was observed at cone pedicles and horizontal and bipolar cell processes. In the IPL, mGluR1 labeling could be found on bipolar cell terminals, as well as postsynaptic processes, including amacrine cell processes. Neither presynaptic nor postsynaptic elements were labeled at rod synapses. For mGluR5, OPL labeling was associated with cone pedicles as well as bipolar and horizontal cell processes. As for mGluR1, rod synapses were unlabeled. In the IPL, labeling for mGluR5 was found on bipolar cell terminals and amacrine cell processes. The presynaptic expression of these receptors in the OPL was confirmed at the light level by double-labeling experiments with SV2. The distributions of mGluRs 1 and 5 indicate that they have the potential to regulate function in both synaptic layers. Furthermore, the similar expression patterns for these two receptors indicate that they might be co-expressed and thus have the potential to interact functionally.

Keywords

Amacrine cellsCone photoreceptorElectron microscopyGlutamate receptors
Type
Research Article
Information
Visual Neuroscience , Volume 23 , Issue 2 , March 2006 , pp. 221 - 231
Copyright
2006 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

Akopian, A. & Witkovsky, P. (1996). Activation of metabotropic glutamate receptors decreases a high-threshold calcium current in spiking neurons of the Xenopus retina. Visual Neuroscience 13, 549–557.CrossRefGoogle Scholar
Aramori, I. & Nakanishi, S. (1992). Signal transduction and pharmacological characteristics of a metabotropic glutamate receptor, mGluR1, in transfected CHO cells. Neuron 8, 757–765.CrossRefGoogle Scholar
Awatramani, G.B. & Slaughter, M.M. (2001). Intensity-dependent, rapid activation of presynaptic metabotropic glutamate receptors at a central synapse. Journal of Neuroscience 21, 741–749.Google Scholar
Barlow, H.B. (1953). Summation and inhibition in the frog's retina. Journal of Physiology 119, 69–88.CrossRefGoogle Scholar
Bhattacharya, B., Babwah, A.V., Godin, C., Anborgh, P.H., Dale, L.B., Poulter, M.O., & Fergusun, S.S.G. (2004). Ral and phospholipase D2-dependent pathway for constitutive Metabotropic glutamate receptor endocytosis. Journal of Neuroscience 24, 8752–8761.Google Scholar
Bozzola, J.J. & Russell, L.D. (1992). Electron Microscopy: Principles and Techniques for Biologists. Boston, Massachusetts: Jones & Bartlett Publishers.
Brandstätter, J.H., Koulen, P., Kuhn, R., Van der Putten, H., & Wässle, H. (1996). Compartmental localization of a metabotropic glutamate receptor (mGluR7): Two different active sites at a retinal synapse. Journal of Neuroscience 16, 4749–4756.Google Scholar
Buckley, K. & Kelly, R.B. (1985). Identification of a transmembrane glycoprotein specific for secretory vesicles of neural and endocrine cells. Journal of Cell Biology 100, 1284–1294.CrossRefGoogle Scholar
Cai, W. & Pourcho, R.G. (1999). Localization of metabotropic glutamate receptors mGluR1alpha and mGluR2/3 in the cat retina. Journal of Comparative Neurology 407, 427–437.3.0.CO;2-9>CrossRefGoogle Scholar
Conn, P.J. & Pin, J.P. (1997). Pharmacology and functions of metabotropic glutamate receptors. Annual Review of Pharmacology and Toxicology 37, 205–237.CrossRefGoogle Scholar
Dale, L.B., Bhattacharya, M., Seachrist, J.L., Anborgh, P.H., & Ferguson, S.S.G. (2001). Agonist-stimulated and tonic internalization of metabotropic glutamate receptor 1a in human embryonic kidney 293 cells: Agonist-stimulated endocytosis is β-arrestin1 isoform-specific. Molecular Pharmacology 60, 1243–1253.Google Scholar
Dixon, D.B. & Copenhagen, D.R. (1997). Metabotropic glutamate receptor-mediated suppression of an inward rectifier current is linked via a cGMP cascade. Journal of Neuroscience 17, 8945–8954.Google Scholar
Dowling, J.E. (1968). Synaptic organization of the frog retina: An electron microscopic analysis comparing the retinas of frogs and primates. Proceedings of the Royal Society B (London) 170, 205–228.CrossRefGoogle Scholar
Dubin, M.W. (1970). The inner plexiform layer of the vertebrate retina: A quantitative and comparative electron microscopic analysis. Journal of Comparative Neurology 140, 479–505.CrossRefGoogle Scholar
Dyka, F.M., May, C.A., & Enz, R. (2004). Metabotropic glutamate receptors are differentially regulated under elevated intraocular pressure. Journal of Neurochemistry 90, 190–202.CrossRefGoogle Scholar
Fourgeaud, L., Bessis, A.-S., Rossignol, F., Pin, J.-P., Olivo-Marin, J.-C., & Hémar, A. (2003). The metabotropic glutamate receptor mGluR5 is endocytosed by a clathrin-independent pathway. Journal of Biological Chemistry 278, 12222–12230.CrossRefGoogle Scholar
Francesconi, A. & Duvoisin, R.M. (1998). Role of the second and third intracellular loops of metabotropic glutamate receptors in mediating dual signal transduction activation. Journal of Biological Chemistry 273, 5615–5624.CrossRefGoogle Scholar
Gafka, A.C., Vogel, K.S., & Linn, C.L. (1999). Evidence of metabotropic glutamate receptor subtypes found on catfish horizontal and bipolar retinal neurons. Neuroscience 90, 1403–1414.CrossRefGoogle Scholar
Hartveit, E., Brandstätter, J.H., Enz, R., & Wässle, H. (1995). Expression of the mRNA of seven metabotropic glutamate receptors (mGlur1 to 7) in the rat retina. An in situ hybridization study on tissue sections and isolated cells. European Journal of Neuroscience 7, 1472–1483.Google Scholar
Higgs, M.H. & Lukasiewicz, P.D. (2002). Activation of group II metabotropic glutamate receptors inhibits glutamate release from salamander retinal photoreceptors. Visual Neuroscience 19, 275–281.CrossRefGoogle Scholar
Higgs, M.H., Romano, C., & Lukasiewicz, P.D. (2002). Presynaptic effects of group III metabotropic glutamate receptors on excitatory synaptic transmission in the retina. Neuroscience 115, 163–172.CrossRefGoogle Scholar
Hirasawa, H., Shiells, R., & Yamada, M. (2002). A metabotropic glutamate receptor regulates transmitter release from cone presynaptic terminals in carp retinal slices. Journal of General Physiology 119, 55–68.CrossRefGoogle Scholar
Hodos, W., Dawes, E.A., & Keating, M.J. (1982). Properties of the receptive fields of frog retinal ganglion cells as revealed by their responses to moving stimuli. Neuroscience 7, 1533–1544.CrossRefGoogle Scholar
Hoffpauir, B.K. & Gleason, E.L. (2002). Activation of mGluR5 modulates GABA(A) receptor function in retinal amacrine cells. Journal of Neurophysiology 88, 1766–1776.Google Scholar
Holden, A.L. (1977). Responses of directional ganglion cells in the pigeon retina. Journal of Physiology 270, 253–269.CrossRefGoogle Scholar
Hollmann, M. & Heinemann, S. (1994). Cloned glutamate receptors. Annual Review of Neuroscience 17, 31–108.CrossRefGoogle Scholar
Iacovelli, L., Salvatore, L., Capobianco, L., Picascia, A., Barletta, E., Storto, M., Mariggio, S., Sallese, M., Porcellini, A., Nicole, F., & De Blasi, A. (2003). Role of G protein-coupled receptor kinase 4 and β-arestin 1 in agonist-stimulated metabotripic glutamate receptor 1 internalization and activation of mitogen-activated protein kinases. Journal of Biological Chemistry 278, 12433–12442.CrossRefGoogle Scholar
Joly, C., Gomeza, J., Brabet, I., Curry, K., Bockaert, J., & Pin, J.P. (1995). Molecular, functional, and pharmacological characterization of the metabotropic glutamate receptor type 5 splice variants: Comparison with mGluR1. Journal of Neuroscience 15, 3970–3981.Google Scholar
Koulen, P., Kuhn, R., Wässle, H., & Brandstätter, J.H. (1997). Group I metabotropic glutamate receptors mGluR1alpha and mGluR5a: Localization in both synaptic layers of the rat retina. Journal of Neuroscience 17, 2200–2211.Google Scholar
Koulen, P., Kuhn, R., Wässle, H., & Brandstätter, J.H. (1999). Modulation of the intracellular calcium concentration in photoreceptor terminals by a presynaptic metabotropic glutamate receptor. Proceedings of the National Academy of Sciences of the U.S.A. 96, 9909–9914.CrossRefGoogle Scholar
Kreimborg, K.M., Lester, M.L., Medler, K.F., & Gleason, E.L. (2001). Group I metabotropic glutamate receptors are expressed in the chicken retina and by cultured retinal amacrine cells. Journal of Neurochemistry 77, 452–465.CrossRefGoogle Scholar
Linn, C.L. & Gafka, A.C. (1999). Activation of metabotropic glutamate receptors modulates the voltage-gated sustained calcium current in a teleost horizontal cell. Journal of Neurophysiology 81, 425–434.Google Scholar
Liposits, Z., Sherman, D., Phelix, C., & Paull, W.K. (1986). A combined light and electron microscopic immunocytochemical method for the simultaneous localization of multiple tissue antigens. Tyrosine hydroxylase immunoreactive innervation of corticotropin releasing factor synthesizing neurons in the paraventricular nucleus of the rat. Histochemistry 85, 95–106.Google Scholar
Maturana, H.R. & Frenk, S. (1963). Directional movement and horizontal edge detectors in the pigeon retina. Science 142, 977–979.CrossRefGoogle Scholar
Mundell, S.J., Pula, G., More, J.C.A., Jane, D.E., Roberts, P.J., & Kelly, E. (2004). Activation of cyclic AMP-dependent protein kinase inhibits the desensitization and internalization of metabotropic glutamate receptors 1a and 1b. Molecular Pharmacology 65, 1507–1516.CrossRefGoogle Scholar
Nomura, A., Shigemoto, R., Nakamura, Y., Okamoto, N., Mizuno, N., & Nakanishi, S. (1994). Developmentally regulated postsynaptic localization of a metabotropic glutamate receptor in rat rod bipolar cells. Cell 77, 361–369.CrossRefGoogle Scholar
Pearlman, A.L. & Hughes, C.P. (1976). Functional role of efferents to the avian retina. I. Analysis of retinal ganglion cell receptive fields. Journal of Comparative Neurology 166, 111–122.Google Scholar
Pin, J.P., Waeber, C., Prezeau, L., Bockaert, J., & Heinemann, S.F. (1992). Alternative splicing generates metabotropic glutamate receptors inducing different patterns of calcium release in Xenopus oocytes. Proceedings of the National Academy of Sciences of the U.S.A. 89, 10331–10335.CrossRefGoogle Scholar
Robbins, J., Reynolds, A.M., Treseder, S., & Davies, R. (2003). Enhancement of low-voltage-activated calcium currents by group II metabotropic glutamate receptors in rat retinal ganglion cells. Molecular and Cellular Neurosciences 23, 341–350.CrossRefGoogle Scholar
Shen, W. & Slaughter, M.M. (1998). Metabotropic and ionotropic glutamate receptors regulate calcium channel currents in salamander retinal ganglion cells. Journal of Physiology 510, 815–828.CrossRefGoogle Scholar
Sosa, R. & Gleason, E. (2004). Activation of mGluR5 modulates Ca2+ current in retinal amacrine cells. Visual Neuroscience 21, 807–816.CrossRefGoogle Scholar
Sosa, R., Hoffpauir, B., Rankin, M.L., Bruch, R.C., & Gleason, E.L. (2002). Metabotropic glutamate receptor 5 and calcium signaling in retinal amacrine cells. Journal of Neurochemistry 81, 973–983.CrossRefGoogle Scholar
Vardi, N., Duvoisin, R., Wu, G., & Sterling, P. (2000). Localization of mGluR6 to dendrites of ON bipolar cells in primate retina. Journal of Comparative Neurology 423, 402–412.3.0.CO;2-E>CrossRefGoogle Scholar
Vardi, N. & Morigiwa, K. (1997). ON cone bipolar cells in rat express the metabotropic receptor mGluR6. Visual Neuroscience 14, 789–794.CrossRefGoogle Scholar
Vigh, J. & Lasater, E.M. (2003). Intracellular calcium release resulting from mGluR1 receptor activation modulates GABAA currents in wide-field retinal amacrine cells: A study with caffeine. European Journal of Neuroscience 17, 2237–2248.CrossRefGoogle Scholar