Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-13T21:38:07.908Z Has data issue: false hasContentIssue false

Dopaminergic amacrine cells express opioid receptors in the mouse retina

Published online by Cambridge University Press:  03 April 2012

SHANNON K. GALLAGHER
Affiliation:
Department of Biomedical Sciences, Colorado State University, Fort Collins, Colorado
JULIA N. ANGLEN
Affiliation:
Department of Biomedical Sciences, Colorado State University, Fort Collins, Colorado
JUSTIN M. MOWER
Affiliation:
Department of Biomedical Sciences, Colorado State University, Fort Collins, Colorado
JOZSEF VIGH*
Affiliation:
Department of Biomedical Sciences, Colorado State University, Fort Collins, Colorado
*
*Address correspondence and reprint requests to: Jozsef Vigh, Department of Biomedical Sciences, Colorado State University, 1617 Campus Delivery, Fort Collins, CO 80523. E-mail: jozsef.vigh@colostate.edu

Abstract

The presence of opioid receptors has been confirmed by a variety of techniques in vertebrate retinas including those of mammals; however, in most reports, the location of these receptors has been limited to retinal regions rather than specific cell types. Concurrently, our knowledge of the physiological functions of opioid signaling in the retina is based on only a handful of studies. To date, the best-documented opioid effect is the modulation of retinal dopamine release, which has been shown in a variety of vertebrate species. Nonetheless, it is not known if opioids can affect dopaminergic amacrine cells (DACs) directly, via opioid receptors expressed by DACs. This study, using immunohistochemical methods, sought to determine whether (1) μ- and δ-opioid receptors (MORs and DORs, respectively) are present in the mouse retina, and if present, (2) are they expressed by DACs. We found that MOR and DOR immunolabeling were associated with multiple cell types in the inner retina, suggesting that opioids might influence visual information processing at multiple sites within the mammalian retinal circuitry. Specifically, colabeling studies with the DAC molecular marker anti-tyrosine hydroxylase antibody showed that both MOR and DOR immunolabeling localize to DACs. These findings predict that opioids can affect DACs in the mouse retina directly, via MOR and DOR signaling, and might modulate dopamine release as reported in other mammalian and nonmammalian retinas.

Type
Brief Communication
Copyright
Copyright © Cambridge University Press 2012

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

Abdelalim, E.M. & Tooyama, I. (2010). NPR-C is expressed in the cholinergic and dopaminergic amacrine cells in the rat retina. Peptides 31, 180183.CrossRefGoogle ScholarPubMed
Akil, H., Watson, S.J., Young, E., Lewis, M.E., Khachaturian, H. & Walker, J.M. (1984). Endogenous opioids—biology and function. Annual Review of Neuroscience 7, 223255.CrossRefGoogle ScholarPubMed
Altschuler, R.A., Mosinger, J.L., Hoffman, D.W. & Parakkal, M.H. (1982). Immunocytochemical localization of enkephalin-like immunoreactivity in the retina of the guinea pig. Proceedings of the National Academy of Sciences of the United States of America 79, 23982400.CrossRefGoogle ScholarPubMed
Bolte, S. & Cordelières, F.P. (2006). A guided tour into subcellular colocalization analysis in light microscopy. Journal of Microscopy 224, 213232.CrossRefGoogle ScholarPubMed
Brecha, N.C., Johnson, J., Kui, B., Anton, B., Keith, D., Evans, C. & Sternini, C. (1995). Mu opioid receptor immunoreactivity is expressed in the retina and retina recipient nuclei. Analgesia 1, 331334.CrossRefGoogle Scholar
Brecha, N.C., Sternini, C., Anderson, K. & Krause, J.E. (1989). Expression and cellular-localization of substance P/neurokinin A and neurofinin B messenger B mRNAs in the rat retina. Visual Neuroscience 3, 527535.CrossRefGoogle Scholar
Costes, S.V., Daelemans, D., Cho, E.H., Dobbin, Z., Pavlakis, G. & Lockett, S. (2004). Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophysical Journal 86, 39934003.CrossRefGoogle ScholarPubMed
Dubocovich, M.L. & Weiner, N. (1983). Enkephalins modulate H-3 dopamine release from rabbit retina in vitro. The Journal of Pharmacology and Experimental Therapeutics 224, 634639.Google Scholar
Galindo-Romero, C., Aviles-Trigueros, M., Jimenez-Lopez, M., Valiente-Soriano, F.J., Salinas-Navarro, M., Nadal-Nicolas, F., Villegas-Perez, M.P., Vidal-Sanz, M. & Agudo-Barriuso, M. (2011). Axotomy-induced retinal ganglion cell death in adult mice: Quantitative and topographic time course analyses. Experimental Eye Research 92, 377387.CrossRefGoogle ScholarPubMed
Gallagher, S.K., Witkovsky, P., Roux, M.J., Low, M.J., Otero-Corchon, V., Hentges, S.T. & Vigh, J. (2010). beta-Endorphin expression in the mouse retina. The Journal of Comparative Neurology 518, 31303148.CrossRefGoogle ScholarPubMed
Gomes, I., Gupta, A., Filipovska, J., Szeto, H.H., Pintar, J.E. & Devi, L.A. (2004). A role for heterodimerization of mu and delta opiate receptors in enhancing morphine analgesia. Proceedings of the National Academy of Sciences of the United States of America 101, 51355139.CrossRefGoogle ScholarPubMed
Gonzalez, R.C. & Wintz, P. (1987). Digital Image Processing. Reading, MA: Addison-Wesley Publishing Company.Google Scholar
Husain, S., Potter, D.E. & Crosson, C.E. (2009). Opioid receptor-activation: Retina protected from ischemic injury. Investigative Ophthalmology & Visual Science 50, 38533859.CrossRefGoogle ScholarPubMed
Isayama, T. & Zagon, I.S. (1991). Localization of preproenkephalin A mRNA in the neonatal rat retina. Brain Research Bulletin 27, 805808.CrossRefGoogle ScholarPubMed
Jeon, C.J., Strettoi, E. & Masland, R.H. (1998). The major cell populations of the mouse retina. The Journal of Neuroscience 18, 89368946.CrossRefGoogle ScholarPubMed
Kabli, N. & Cahill, C.M. (2007). Anti-allodynic effects of peripheral delta opioid receptors in neuropathic pain. Pain 127, 8493.CrossRefGoogle ScholarPubMed
Kieffer, B.L. (1995). Recent advances in molecular recognition and signal transduction of active peptides: Receptors for opioid peptides. Cellular and Molecular Neurobiology 15, 615635.CrossRefGoogle ScholarPubMed
Kolbinger, W. & Weiler, R. (1993). Modulation of endogenous dopamine release in the turtle retina—effects of light, calcium, and neurotransmitters. Visual Neuroscience 10, 10351041.CrossRefGoogle ScholarPubMed
Kong, J.H., Fish, D.R., Rockhill, R.L. & Masland, R.H. (2005). Diversity of ganglion cells in the mouse retina: Unsupervised morphological classification and its limits. The Journal of Comparative Neurology 489, 293310.CrossRefGoogle ScholarPubMed
Kosterlitz, H.W., Lord, J.A.H., Paterson, S.J. & Waterfield, A.A. (1980). Effects of changes in the structure of enkephalins and of narcotic analgesic drugs on their interactions with mu-receptors and delta-receptors. British Journal of Pharmacology 68, 333342.CrossRefGoogle ScholarPubMed
Kwon, M.S., Seo, Y.J., Choi, S.M., Lee, J.K., Jung, J.S., Park, S.H. & Suh, H.W. (2008). The effect of formalin pretreatment on nicotine-induced antinociceptive effect: The role of mu-opioid receptor in the hippocampus. Neuroscience 154, 415423.CrossRefGoogle ScholarPubMed
Loh, H.H., Brase, D.A., Sampathkhanna, S., Mar, J.B., Way, E.L. & Li, C.H. (1976). beta-Endorphin in vitro inhibition of striatal dopamine release. Nature 264, 567568.CrossRefGoogle ScholarPubMed
Lupp, A., Richter, N., Doll, C., Nagel, F. & Schulz, S. (2011). UMB-3, a novel rabbit monoclonal antibody, for assessing mu-opioid receptor expression in mouse, rat and human formalin-fixed and paraffin-embedded tissues. Regulatory Peptides 167, 913.CrossRefGoogle ScholarPubMed
May, C.A., Nakamura, K., Fujiyama, F. & Yanagawa, Y. (2008). Quantification and characterization of GABA-ergic amacrine cells in the retina of GAD67-GFP knock-in mice. Acta Ophthalmologica 86, 395400.CrossRefGoogle ScholarPubMed
Morgan, I.G. & Boelen, M.K. (1996). A retinal dark-light switch: A review of the evidence. Visual Neuroscience 13, 399409.CrossRefGoogle ScholarPubMed
Nadal-Nicolás, F.M., Jimenez-Lopez, M., Sobrado-Calvo, P., Nieto-Lopez, L., Canovas-Martinez, I., Salinas-Navarro, M., Vidal-Sanz, M. & Agudo, M. (2009). Brn3a as a marker of retinal ganglion cells: Qualitative and quantitative time course studies in naive and optic nerve-injured retinas. Investigative Ophthalmology & Visual Science 50, 38603868.CrossRefGoogle ScholarPubMed
Pan, H.L., Wu, Z.Z., Zhou, H.Y., Chen, S.R., Zhang, H.M. & Li, D.P. (2008). Modulation of pain transmission by G-protein-coupled receptors. Pharmacology & Therapeutics 117, 141161.CrossRefGoogle ScholarPubMed
Peng, P.H., Huang, H.S., Lee, Y.J., Chen, Y.S. & Ma, M.C. (2009). Novel role for the delta-opioid receptor in hypoxic preconditioning in rat retinas. Journal of Neurochemistry 108, 741754.CrossRefGoogle ScholarPubMed
Persson, A.I., Thorlin, T. & Eriksson, P.S. (2005). Comparison of immunoblotted delta opioid receptor proteins expressed in the adult rat brain and their regulation by growth hormone. Neuroscience Research 52, 19.CrossRefGoogle ScholarPubMed
Riazi-Esfahani, M., Kiumehr, S., Asadi-Amoli, F. & Dehpour, A.R. (2009). Effects of intravitreal morphine administered at different time points after reperfusion in a rabbit model of ischemic retinopathy. Retina 29, 262268.CrossRefGoogle Scholar
Rozenfeld, R. & Devi, L.A. (2011). Exploring a role for heteromerization in GPCR signalling specificity. The Biochemical Journal 433, 1118.CrossRefGoogle ScholarPubMed
Su, Y.Y.T. & Watt, C.B. (1987). Interaction between enkephalin and dopamine in the avian retina. Brain Research 423, 6370.Google ScholarPubMed
Tamamaki, N., Yanagawa, Y., Tomioka, R., Miyazaki, J.I., Obata, K. & Kaneko, T. (2003). Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. The Journal of Comparative Neurology 467, 6079.CrossRefGoogle ScholarPubMed
Wamsley, J.K., Palacios, J.M. & Kuhar, M.J. (1981). Autoradiographic localization of opioid receptors in the mammalian retina. Neuroscience Letters 27, 1924.CrossRefGoogle ScholarPubMed
Wang, H.B., Zhao, B., Zhong, Y.Q., Li, K.C., Li, Z.Y., Wang, Q.O., Lu, Y.J., Zhang, Z.N., He, S.Q., Zheng, H.C., Wu, S.X., Hokfelt, T.G.M., Bao, L. & Zhang, X. (2010). Coexpression of delta- and mu-opioid receptors in nociceptive sensory neurons. Proceedings of the National Academy of Sciences of the United States of America 107, 1311713122.CrossRefGoogle ScholarPubMed
Witkovsky, P. (2004). Dopamine and retinal function. Documenta Ophthalmologica 108, 1740.CrossRefGoogle ScholarPubMed
Witkovsky, P., Arango-Gonzalez, B., Haycock, J.W. & Kohler, K. (2005). Rat retinal dopaminergic neurons: Differential maturation of somatodendritic and axonal compartments. The Journal of Comparative Neurology 481, 352362.CrossRefGoogle ScholarPubMed
Witkovsky, P., Gabriel, R. & Krizaj, D. (2008). Anatomical and neurochemical characterization of dopaminergic interplexiform processes in mouse and rat retinas. The Journal of Comparative Neurology 510, 158174.CrossRefGoogle ScholarPubMed
Xiang, M.Q., Zhou, L.J., Macke, J.P., Yoshioka, T., Hendry, S.H.C., Eddy, R.L., Shows, T.B. & Nathans, J. (1995). The Brn-3 family of POU-domain factors—primary structure, binding-specificity, and expression in subsets of retinal ganglion-cells and somatosensory neurons. The Journal of Neuroscience 15, 47624785.CrossRefGoogle ScholarPubMed
Zalutsky, R.A. & Miller, R.F. (1990). The physiology of substance-P in the rabbit retina. The Journal of Neuroscience 10, 394402.CrossRefGoogle ScholarPubMed