Dopaminergic modulation of ganglion-cell photoreceptors in rat

European Journal of Neuroscience

Volumn 35, Issue 3-4, 2012, Pages 507-518

  Van Hook, Matthew J ^a,b   Wong, Kwoon Y ^a,c   Berson, David M ^a  

^a BROWN UNIVERSITY   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Cyclic AMP (cAMP); D1 receptor; Intrinsically photosensitive retinal ganglion cells (ipRGCs); Melanopsin; Retina

Indexed keywords

2,3,4,5 TETRAHYDRO 7,8 DIHYDROXY 1 PHENYL 1H 3 BENZAZEPINE; DOPAMINE; DOPAMINE 1 RECEPTOR; DOPAMINE 1A RECEPTOR; FORSKOLIN; ISOBUTYLMETHYLXANTHINE; MELANOPSIN; QUINPIROLE; UNCLASSIFIED DRUG; ADENYLATE CYCLASE ACTIVATOR; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; DOPAMINE 1 RECEPTOR STIMULATING AGENT; DOPAMINE 2 RECEPTOR; DOPAMINE 2 RECEPTOR STIMULATING AGENT; DOPAMINE 4 RECEPTOR; DOPAMINE 5 RECEPTOR; PHOSPHODIESTERASE INHIBITOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; DEPOLARIZATION; DOPAMINE RELEASE; DOPAMINERGIC TRANSMISSION; DRD1A GENE; GENE; GENE EXPRESSION; LIGHT ADAPTATION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATCH CLAMP; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; RETINA; RETINA AMACRINE CELL; RETINA GANGLION CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ANIMAL EXPERIMENT; CELL ISOLATION; DRD2 GENE; DRD4 GENE; DRD5 GENE; IMMUNOHISTOCHEMISTRY; INTRINSICALLY PHOTOSENSITIVE RETINAL GANGLION CELL; LIGHT RELATED PHENOMENA; NERVE CELL MEMBRANE CONDUCTANCE; NERVE CELL MEMBRANE STEADY POTENTIAL; PHOTOCURRENT; PHOTOTRANSDUCTION; RETINA BIPOLAR GANGLION CELL; SINGLE CELL ANALYSIS; SPIKE;

1-METHYL-3-ISOBUTYLXANTHINE; 2,3,4,5-TETRAHYDRO-7,8-DIHYDROXY-1-PHENYL-1H-3-BENZAZEPINE; ACTINS; ANIMALS; CARBAZOLES; CELLS, CULTURED; CYCLIC AMP; DOPAMINE; DOPAMINE AGONISTS; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; FORSKOLIN; GENE EXPRESSION REGULATION; LIGHT; LIGHT SIGNAL TRANSDUCTION; MALE; MEMBRANE POTENTIALS; PATCH-CLAMP TECHNIQUES; PHOTIC STIMULATION; PHOTORECEPTOR CELLS; PYRROLES; QUINPIROLE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DOPAMINE; RETINA; RETINAL GANGLION CELLS; ROD OPSINS; SODIUM CHANNEL BLOCKERS; TETRODOTOXIN; VISUAL PATHWAYS;

EID: 84857045964     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07975.x     Document Type: Article

References (75)

1. h in a motor axon. J. Neurosci., 30, 8425-8434.
2. Baver, S.B., Pickard, G.E., Sollars, P.J. & Pickard, G.E. (2008) Two types of melanopsin retinal ganglion cell differentially innervate the hypothalamic suprachiasmatic nucleus and the olivary pretectal nucleus. Eur. J. Neurosci., 27, 1763-1770.
3. Belenky, M.A., Smeraski, C.A., Provencio, I., Sollars, P.J. & Pickard, G.E. (2003) Melanopsin retinal ganglion cells receive bipolar and amacrine cell synapses. J. Comp. Neurol., 460, 380-393.
4. Berson, D.M., Dunn, F.A. & Takao, M. (2002) Phototransduction by retinal ganglion cells that set the circadian clock. Science, 295, 1070-1073.
5. Berson, D.M., Castrucci, A.M. & Provencio, I. (2010) Morphology and mosaics of melanopsin-expressing retinal ganglion cell types in mice. J. Comp. Neurol., 518, 2405-2422.
6. Bjelke, B., Goldstein, M., Tinner, B., Andersson, C., Sasack, S.R., Steinbusch, H.W.M., Lew, J.Y., He, X., Watson, S., Tengroth, B. & Fuxe, K. (1996) Dopaminergic transmission in the rat retina: evidence for volume transmission. J. Chem. Neuroanat., 12, 37-50.
7. Boelen, M.K., Mowlen, M.G. & Marshak, D.W. (1998) Light-stimulated release of dopamine from the primate retina is blocked by l-2-amino-4-phosphonobutyric acid (APB). Vis. Neurosci., 15, 97-103.
8. Chen, L. & Yang, X.L. (2007) Hyperpolarization-activated cation current is involved in modulation of the excitability of rat retinal ganglion cells by dopamine. Neuroscience, 150, 299-308.
9. Chen, S.K., Badea, T.C. & Hattar, S. (2011) Photoentrainment and pupillary light reflex are mediated by distinct populations of ipRGCs. Nature, 476, 92-95.
10. Chyb, S., Hevers, W., Forte, M., Wolfgang, W.J., Selinger, Z. & Hardie, R.C. (1999) Modulation of the light response by cAMP in Drosophila photoreceptors. J. Neurosci., 19, 8799-8807.
11. Contini, M. & Raviola, E. (2003) GABAergic synapses made by a retinal dopaminergic neuron. Proc. Natl Acad. Sci. USA, 100, 1358-1363.
12. Cragg, S.J. & Rice, M.E. (2004) Dancing past the DAT at a DA synapse. Trends Neurosci., 27, 270-277.
13. qα in Drosophila photoreceptors is facilitated by the photoreceptor-specific myosin III NINAC. J. Cell Sci., 117, 4797-4806.
14. Davila, V., Yan, Z., Craciun, L.C., Logothetis, D. & Sulzer, D. (2003) Dopamine autoreceptors do not activate G-protein gated inwardly rectifying potassium channel currents in substantia nigra dopamine neurons. J. Neurosci., 23, 5693-5697.
15. Dosé, A.C. & Burnside, B. (2000) Cloning and chromosomal localization of a human class III myosin. Genomics, 67, 333-342.
16. Dosé, A.C. & Burnside, B. (2002) A class III myosin expressed in the retina is a potential candidate for Bardet-Biedl syndrome. Genomics, 79, 621-624.
17. Feigenspan, A. & Bormann, J. (1994) Facilitation of GABAergic signaling in the retina by receptors stimulating adenylate cyclase. Proc. Natl Acad. Sci. USA, 91, 10893-10897.
18. Garris, P.A., Ciolkowski, E.L., Pastore, P. & Wightman, R.M. (1994) Efflux of dopamine from the synaptic cleft in the nucleus accumbens of the rat brain. J. Neurosci., 14, 6084-6093.
19. Gooley, J.J., Lu, J., Chou, T.C., Scammell, T.E. & Saper, C.B. (2001) Melanopsin in cells of origin of the retinohypothalamic tract. Nat. Neurosci., 4, 1165.
20. Govindaiah, G. & Cox, C.L. (2005) Excitatory actions of dopamine via D1-like receptors in the rat lateral geniculate nucleus. J. Neurophysiol., 94, 3708-3718.
21. Graham, D.M., Wong, K.Y., Shapiro, P., Frederick, C., Pattabiraman, K. & Berson, D.M. (2008) Melanopsin ganglion cells use a membrane-associated rhabdomeric phototransduction cascade. J. Neurophysiol., 99, 2522-2532.
22. Gustincich, S., Feigenspan, A., Wu, G.K., Koopman, L.J. & Raviola, E. (1997) Control of dopamine release in the retina: a transgenic approach to neural networks. Neuron, 18, 723-736.
23. Hannibal, J., Hindersson, P., Knudsen, S.M., Georg, B. & Fahrengrug, J. (2002) The photopigment melanopsin is exclusively present in pituitary adenylate cyclase-activating polypeptide-containing retinal ganglion cells of the retinohypothalamic tract. J. Neurosci., 22, RC191.
24. Hartwick, A.T.E., Bramley, J.R., Yu, J., Stevens, K.T., Allen, C.N., Baldridge, W.H., Scollars, P.J. & Pickard, G.E. (2007) Light-evoked calcium responses of isolated melanopsin-expressing retinal ganglion cells. J. Neurosci., 27, 13468-13480.
25. Hattar, S., Liao, H.W., Takao, M., Berson, D.M. & Yau, K.W. (2002) Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science, 295, 1065-1070.
26. Hattar, S., Kumar, M., Park, A., Tung, J., Yau, K.W. & Berson, D.M. (2006) Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J. Comp. Neurol., 497, 326-349.
27. + current by modulating both entry into and recovery from inactivation. J. Nerophysiol., 92, 3134-3141.
28. Hayashida, Y., Rodriguez, C.V., Ogata, G., Partida, G.J., Oi, H., Stradleigh, T.W., Lee, S.C., Colado, A.F. & Ishida, A.T. (2009) Inhibition of adult rat retinal ganglion cells by D1-type dopamine receptor activation. J. Neurosci., 29, 15001-15016.
29. Horner, T.J., Osawa, S., Schaller, M.D. & Weiss, E.R. (2005) Phorphorylation of GRK1 and GRK7 by cAMP-dependent protein kinase attenuates their enzymatic activities. J. Biol. Chem., 280, 28241-28250.
30. Huang, Q., Zhou, D., Chase, K., Gusella, J.F., Aronin, N. & DiFiglia, M. (1992) Immunohistochemical localization of the D1 dopamine receptor in rat brain reveals its axonal transport, pre- and postsynaptic localization, and prevelance in the basal ganglia, limbic system, and thalamic reticular nucleus. Proc. Natl Acad. Sci. USA, 89, 11988-11992.
31. q-dependent PLC-β1 activity by PKG and PKA is mediated by phosphorylation of RGS4 and GRK2. Am. J. Physiol. Cell Physiol., 292, C200-C208.
32. Katti, C., Dalal, J.S., Dosé, A.C. & Burnside, B.A. (2009) Cloning and distribution of myosin 3B in the mouse retina: differential distribution in cone outer segments. Exp. Eye Res., 89, 224-237.
33. Knapp, A.G. & Dowling, J.E. (1987) Dopamine enhances excitatory amino acid-gated conductances in cultured retinal horizontal cells. Nature, 325, 437-439.
34. Lee, S.J. & Montell, C. (2004) Light-dependent translocation of visual arrestin regulated by the NINAC myosin III. Neuron, 43, 95-103.
35. Lee, S.P., So, C.H., Rashid, A.J., Varghese, G., Cheng, R., Lanca, A.J., O'Dowd, B.F. & George, S.R. (2004) Dopamine D1 and D2 receptor co-activation generates a novel phospholipase C-mediated calcium signal. J. Biol. Chem., 279, 35671-35678.
36. Li, H., Gaughwin, P., Li, N. & He, S. (2004) Localization of a dopamine D1-receptor to A-type horizontal cells in the rabbit retina by single cell RT-PCR. Neurosci. Lett., 355, 146-148.
37. Liu, Y. & Lasater, E.M. (1994) Calcium currents in turtle retinal ganglion cells II Dopamine modulation via a cyclic AMP-dependent mechanism. J. Neurophysiol., 71, 743-752.
38. Maguire, G. & Werblin, F. (1994) Dopamine enhances a glutamate-gated ionic current in OFF bipolar cells of the tiger salamander retina. J. Neurosci., 14, 6094-6107.
39. Meyer-Franke, A., Kaplan, M.R., Pfrieger, F.W. & Barres, B.A. (1995) Characterization of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture. Neuron, 15, 805-819.
40. Neve, K.A., Seamand, J.K. & Trantham-Davidson, H. (2004) Dopamine receptor signaling. J. Recept. Signal Transduct. Res., 24, 165-205.
41. 2-like receptor subtype in the rat retina: biochemical and histochemical evidence. J. Neurochem., 67, 2514-2520.
42. Nguyen-Legros, J., Simon, A., Caille, I. & Bloch, B. (1997) Immunocytochemical localization of dopamine D1 receptors in the retina of mammals. Vis. Neurosci., 14, 545-551.
43. Osawa, S., Jo, R. & Weiss, E.R. (2008) Phosphorylation of GRK7 by PKA in cone photoreceptor cells is regulated by light. J. Neurochem., 107, 1314-1324.
44. Østergaard, J., Hannibal, J. & Fahrenkrug, J. (2007) Synaptic contact between melanopsin-containing retinal ganglion cells and rod bipolar cells. Invest. Ophthalmol. Vis. Sci., 48, 3812-3820.
45. Peiser, C., Trevisani, M., Groneberg, D.A., Dinh, Q.T., Lencer, D., Amadesi, S., Maggiore, B., Harrison, S., Geppetti, P. & Fischer, A. (2005) Dopamine type 2 receptor expression and function in rodent sensory systems projecting to the airways. Am. J. Physiol. Lung Cell. Mol. Physiol., 289, L153-L158.
46. Perez-Leighton, C.E., Schmidt, T.M., Abramowitz, J., Birnbaumer, L. & Kofuji, P. (2011) Intrinsic phototransduction persists in melanopsin-expressing ganglion cells lacking diacylglycerol-sensitive TRPC subunits. Eur. J. Neurosci., 33, 856-867.
47. Perez-Leon, A., Warren, E.J., Allen, C.N., Robinson, D.W. & Brown, R.L. (2006) Synaptic inputs to retinal ganglion cells that set the circadian clock. Eur. J. Neurosci., 24, 1117-1123.
48. Perlman, I. & Normann, R.A. (1998) Light adaptation and sensitivity controlling mechanisms in vertebrate photoreceptors. Prog. Retin. Eye Res., 17, 523-563.
49. Porter, J.A., Minke, B. & Montell, C. (1995) Calmodulin binding to Drosophila NinaC required for termination of phototransduction. EMBO J., 14, 4450-4459.
50. Pozdeyev, N.V. & Lavrikova, E.V. (2000) Diurnal changes of tyrosine, dopamine, and dopamine metabolites content in the retina of rats maintained at different lighting conditions. J. Mol. Neurosci., 15, 1-9.
51. Provencio, I., Jiang, G., De Grip, W.J., Hayes, W.P. & Rollag, M.D. (1998) Melanopsin: an opsin in melanophores, brain, and eye. Proc. Natl Acad. Sci. USA, 95, 340-345.
52. Puopolo, M., Hochstetler, S.E., Gustincich, S., Wightman, R.M. & Raviola, E. (2001) Extrasynaptic release of dopamine in a retinal neuron: activity dependence and transmitter modulation. Neuron, 30, 211-225.
53. h in layer V entorhinal cortex. J. Neurosci., 26, 3229-3244.
54. Sakamoto, K., Liu, C., Kasamatsu, M., Pozdeyev, N.V., Iuvone, M.P. & Tosini, G. (2005) Dopamine regulates melanopsin mRNA expression in intrinsically photoreceptive retinal ganglion cells. Eur. J. Neurosci., 22, 3129-3136.
55. Schmidt, T.M. & Kofuji, P. (2009) Functional and morphological differences among intrinsically photosensitive retinal ganglion cells. J. Neurosci., 29, 476-482.
56. Sekaran, S., Lall, G.S., Ralphs, K.L., Wolstenholme, A.J., Lucas, R.J., Foster, R.G. & Hankins, M.W. (2007) 2-Aminoethoxydiphenylborane is an acute inhibitor of directly photosensitive retinal ganglion cell activity in vitro and in vivo. J. Neurosci., 27, 3981-3986.
57. Surmeier, J., Song, W.J. & Yan, Z. (1996) Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. J. Neurosci., 16, 6579-6591.
58. Tawfeek, H.A.W. & Abou-Samra, A.B. (2008) Negative regulation of parathyroid hormone (PTH)-activated phospholipase C by PTH/PTH-related peptide receptor phosphorylation and protein kinase A. Endocrinology, 149, 4016-4023.
59. Tran, V.T. & Dickman, M. (1992) Differential localization of dopamine D1 and D2 receptors in the rat retina. Invest. Ophthalmol. Vis. Sci., 33, 1620-1626.
60. h) in ganglion-cell photoreceptors. PLoS ONE, 5, e15344.
61. Vaquero, C.F., Pignatelli, A., Partida, G.J. & Ishida, A.T. (2001) A dopamine- and protein kinase A-dependent mechanism for network adaptation in retinal ganglion cells. J. Neurosci., 21, 8624-8635.
62. Veruki, M.L. & Wässle, H. (1996) Immunohistochemical localization of dopamine D1 receptors in rat retina. Eur. J. Neurosci., 8, 2286-2297.
63. Viney, T.J., Balint, K., Hillier, D., Siegert, S., Boldogkoi, Z., Enquist, L.W., Meister, M., Cepko, C.L. & Roska, B. (2007) Local retinal circuits of melanopsin-containing ganglion cells identified by transsynaptic viral tracing. Curr. Biol., 17, 981-988.
64. Vugler, A.A., Redgrave, P., Semo, M., Lawrence, J., Greenwood, J. & Coffey, P.J. (2007) Dopamine neurons form a discrete plexus with melanopsin cells in normal and degenerating retina. Exp. Neurol., 205, 26-35.
65. Warr, C.G. & Kelly, L.E. (1996) Identification and characterization of two distinct calmodulin-binding sites in the Trpl ion-channel protein of Drosophila melanogaster. Biochem. J., 314, 497-503.
66. Warren, E.J., Allen, C.N., Brown, R.L. & Robinson, D.W. (2003) Intrinsic light responses of retinal ganglion cells projecting to the circadian system. Eur. J. Neurosci., 17, 1727-1735.
67. Warren, E.J., Allen, C.N., Brown, R.L. & Robinson, D.W. (2006) The light-activated signaling pathway in SCN-projecting rat retinal ganglion cells. Eur. J. Neurosci., 23, 2477-2487.
68. Wellis, D.P. & Werblin, F.S. (1995) Dopamine modulates GABAc receptors mediating calcium entry into and transmitter release from bipolar cell terminals in tiger salamader retina. J. Neurosci., 15, 4748-4761.
69. Weng, S., Wong, K.Y. & Berson, D.M. (2009) Circadian modulation of melanopsin-driven light response in rat ganglion-cell photoreceptors. J. Biol. Rhythms, 24, 391-402.
70. Witkovsky, P. (2004) Dopamine and retinal function. Doc. Opthalmol., 108, 17-40.
71. Wong, K.Y., Dunn, F.A. & Berson, D.M. (2005) Photoreceptor adaptation in intrinsically photosensitive retinal ganglion cells. Neuron, 48, 1001-1010.
72. Wong, K.Y., Dunn, F.A., Graham, D.M. & Berson, D.M. (2007) Synaptic influences on rat ganglion-cell photoreceptors. J. Physiol., 582, 279-296.
73. Wu, J. & Hablitz, J.J. (2005) Cooperative activation of D1 and D2 dopamine receptors enhances a hyperpolarization-activared inward current in layer I interneurons. J. Neurosci., 25, 6322-6328.
74. Yue, C., Dodge, K.L., Weber, G. & Sanborn, B.M. (1998) Phosphorylation of serine 1105 by protein kinase A inhibits phospholipase Cβ3 stimulation by Gαq. J. Biol. Chem., 273, 18023-18027.
75. Zhang, D.-Q., Wong, K.Y., Sollars, P.J., Berson, D.M., Pickard, G.E. & McMahon, D.G. (2008) Intraretinal signaling by ganglion cell photoreceptors to dopaminergic amacrine neurons. Proc. Natl Acad. Sci. USA, 105, 14181-14186.