Hostname: page-component-8448b6f56d-sxzjt Total loading time: 0 Render date: 2024-04-20T02:23:46.463Z Has data issue: false hasContentIssue false
  • English
  • Français

GABAA and GABAC receptor antagonists increase retinal cyclic GMP levels through nitric oxide synthase

Published online by Cambridge University Press:  30 March 2004

DOU YU  and
WILLIAM D. ELDRED
DOU YU
Affiliation:
Department of Biology, Boston University, Boston
WILLIAM D. ELDRED
Affiliation:
Department of Biology, Boston University, Boston
Get access Rights & Permissions [Opens in a new window]

Abstract

The nitric oxide (NO)/cyclic guanosine monophosphate (cGMP) signal transduction pathway plays a role in every retinal cell type. Previous studies have shown that excitatory glutamatergic synaptic pathways can increase cGMP-like immunoreactivity (cGMP-LI) in retina through stimulation of NO production, but little is known about the role of synaptic inhibition in the modulation of cGMP-LI. Gamma-amino-n-butyric acid (GABA) plays critical roles in modulating excitatory synaptic pathways in the retina. Therefore, we used GABA receptor antagonists to explore the role of GABAergic inhibitory synaptic pathways on the modulation of the NO/cGMP signal-transduction system. Cyclic GMP immunocytochemistry was used to investigate the effects of the GABA receptor antagonists bicuculline, picrotoxin, and (1,2,5,6-tetrahyropyridin-4-yl) methylphosphinic acid (TPMPA) on levels of cGMP-LI. Cyclic GMP-LI was strongly increased in response to the GABAA receptor antagonist bicuculline, while the GABAC receptor antagonist TPMPA had little effect on cGMP-LI. The GABAA/GABAC receptor antagonist, picrotoxin, caused a moderate increase in cGMP-LI, which was mimicked by the combination of bicuculline and TPMPA. The nitric oxide synthase inhibitor, S-methyl-L-thiocitrulline (SMTC), blocked the increased cGMP-LI in response to stimulation with either bicuculline or picrotoxin. Treatments with either of the glutamate receptor antagonists (5R,10S)-(+)-5-methyl-10,11-dihydro-5H-dibenzo[a,d]cyclohepten-5,10-imine (MK-801) or 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) partially blocked the increases in cGMP-LI seen in response to bicuculline, but a combination of MK-801 and CNQX completely eliminated these increases. These results suggest that inhibitory synaptic pathways involving both types of GABA receptors work through excitatory glutamatergic receptors to regulate the NO/cGMP signal-transduction pathway in retina.

Keywords

Nitric oxideGABA receptorscGMPTurtleRetinaAmacrine cellBipolar cellImmunocytochemistry
Type
Research Article
Information
Visual Neuroscience , Volume 20 , Issue 6 , November 2003 , pp. 627 - 637
Copyright
© 2003 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

Ahmad, I., Leinders-Zufall, T., Kocsis, J.D., Shepherd, G.M., Zufall, F., & Barnstable, C.J. (1994). Retinal ganglion cells express a cGMP-gated cation conductance activatable by nitric oxide donors. Neuron 12, 155–165.Google Scholar
Blute, T.A., Mayer, B., & Eldred, W.D. (1997). Immunocytochemical and histochemical localization of nitric oxide synthase in the turtle retina. Visual Neuroscience 14, 717–729.Google Scholar
Blute, T.A., Velasco, P., & Eldred, W.D. (1998). Functional localization of soluble guanylate cyclase in turtle retina: Modulation of cGMP by nitric oxide donors. Visual Neuroscience 15, 485–498.Google Scholar
Blute, T.A., De Grenier, J., & Eldred, W.D. (1999). Stimulation with N-methyl-D-aspartate or kainic acid increases cyclic guanosine monophosphate-like immunoreactivity in turtle retina: Involvement of nitric oxide synthase. Journal of Comparative Neurology 404, 75–85.Google Scholar
Bormann, J., Hamill, O.P., & Sakmann, B. (1987). Mechanism of anion permeation through channels gated by glycine and gamma-aminobutyric acid in mouse cultured spinal neurons. Journal of Physiology 385, 243–286.Google Scholar
Cao, L. & Eldred, W.D. (2001). Subcellular localization of neuronal nitric oxide synthase in turtle retina: Electron immunocytochemistry. Visual Neuroscience 18, 949–960.Google Scholar
Cook, P.B., Lukasiewicz, P.D., & McReynolds, J.S. (2000). GABA(C) receptors control adaptive changes in a glycinergic inhibitory pathway in salamander retina. Journal of Neuroscience 20, 806–812.Google Scholar
De Vente, J. & Steinbusch, H.W.M. (1992). On the stimulation of soluble and particulate guanylate cyclase in the rat brain and the involvement of nitric oxide as studied by cGMP immunocytochemistry. Acta Histochemica 92, 13–38.Google Scholar
DeVries, S.H. & Schwartz, E.A. (1989). Modulation of an electrical synapse between solitary pairs of catfish horizontal cells by dopamine and second messengers. Journal of Physiology 414, 351–375.Google Scholar
Dong, C.J. & Werblin, F.S. (1998). Temporal contrast enhancement via GABAC feedback at bipolar terminals in the tiger salamander retina. Journal of Neurophysiology 79, 2171–2180.Google Scholar
Dong, C.J., Picaud, S.A, & Werblin, F.S. (1994). GABA transporters and GABAC-like receptors on catfish cone- but not rod-driven horizontal cells. Journal of Neuroscience 14, 2648–2658.Google Scholar
Eldred, W.D. & Karten, H.J. (1985). Ultrastructure and synaptic contacts of enkephalinergic amacrine cells in the retina of turtle (Pseudemys scripta). Journal of Comparative Neurology 232, 36–42.Google Scholar
Enz, R., Brandstätter, J.H., Wässle, H., & Bormann, J. (1996). Immunocytochemical localization of the GABAC receptor rho subunits in the mammalian retina. Journal of Neuroscience 16, 4479–4490.Google Scholar
Feigenspan, A. & Bormann, J. (1998). GABA-gated Cl− channels in the rat retina. Progress in Retinal and Eye Research 7, 99–126.Google Scholar
Feigenspan, A., Wässle, H., & Bormann, J. (1993). Pharmacology of GABA receptor Cl− channels in rat retinal bipolar cells. Nature 361, 159–162.Google Scholar
Fletcher, E.L., Koulen, P., & Wässle, H. (1998). GABAA and GABAC receptors on mammalian rod bipolar cells. Journal of Comparative Neurology 396, 351–365.Google Scholar
Greferath, U., Müller, F., Wässle, H., Shivers, B., & Seeburg, P. (1993). Localization of GABAA receptors in the rat retina. Visual Neuroscience 10, 551–561.Google Scholar
Grünert, U., Haverkamp, S., Fletcher, E.L., & Wässle, H. (2002). Synaptic distribution of ionotropic glutamate receptors in the inner plexiform layer of the primate retina. Journal of Comparative Neurology 447, 138–151.Google Scholar
Haverkamp, S., Kolb, H., & Cuenca, N. (2000). Morphological and neurochemical diversity of neuronal nitric oxide synthase-positive amacrine cells in the turtle retina. Cell and Tissue Research 302, 11–19.Google Scholar
Ientile, R., Pedale, S., Picciurro, V., Macaione, V., Fabiano, C., & Macaione, S. (1997). Nitric oxide mediates NMDA-evoked [3H] GABA release from chick retina cells. FEBS Letters 417, 345–348.Google Scholar
Kapousta-Bruneau, N.V. (2000). Opposite effects of GABA(A) and GABA(C) receptor antagonists on the b-wave of ERG recorded from the isolated rat retina. Vision Research 40, 1653–1665.Google Scholar
Koulen, P., Brandstätter, J.H., Kroger, S., Enz, R., Bormann, J., & Wässle, H. (1997). Immunocytochemical localization of the GABA(C) receptor rho subunits in the cat, goldfish, and chicken retina. Journal of Comparative Neurology 380, 520–532.Google Scholar
Kusaka, S., Dabin, I., Barnstable, C.J., & Puro, D.G. (1996). cGMP-mediated effects on the physiology of bovine and human retinal Müller (glial) cells. Journal of Physiology 497, 813–824.Google Scholar
Lukasiewicz, P.D. (1996). GABAC receptors in the vertebrate retina. Molecular Neurobiology 12, 181–194.Google Scholar
Lukasiewicz, P.D. & Werblin, F.S. (1994). A novel GABA receptor modulates synaptic transmission from bipolar to ganglion and amacrine cells in the tiger salamander retina. Journal of Neuroscience 14, 1213–1223.Google Scholar
Lukasiewicz, P.D., Maple, B.R., & Werblin, F.S. (1994). A novel GABA receptor on bipolar cell terminals in the tiger salamander retina. Journal of Neuroscience 14, 1202–1212.Google Scholar
Mills, S.L. & Massey, S.C. (1995). Differential properties of two gap junctional pathways made by AII amacrine cells. Nature 377, 676–677.Google Scholar
Miyachi, E. & Murakami, M. (1991). Synaptic inputs to turtle horizontal cells analyzed after blocking of gap junctions by intracellular injection of cyclic nucleotides. Vision Research 31, 631–635.Google Scholar
Miyachi, E., Murakami, M.M., & Nakaki, T. (1990). Arginine blocks gap junctions between retinal horizontal cells. Neuroreport 1, 107–110.Google Scholar
Nathanson, J.A., Scavone, C., Scanlon, C., & McKee, M. (1995). The cellular Na+ pump as a site of action for carbon monoxide and glutamate: A mechanism for long-term modulation of cellular activity. Neuron 14, 781–794.Google Scholar
Nawy, S. & Jahr, C.E. (1991). cGMP-gated conductance in retinal bipolar cells is suppressed by the photoreceptor transmitter. Neuron 7, 677–683.Google Scholar
Oh, S.J., Kim, I.B., Lee, M.Y., Chun, M.H., & Chung, J.W. (1998). NOS-like immunoreactive neurons express GABA-like immunoreactivity in rabbit and rat retinae. Experimental Brain Research 120, 109–113.Google Scholar
Picaud, S., Pattnaik, B., Hicks, D., Forster, V., Fontaine, V., Sahel, J., & Dreyfus, H. (1998). GABAA and GABAC receptors in adult porcine cones: Evidence from a photoreceptor-glia co-culture model. Journal of Physiology 513, 33–42.Google Scholar
Qian, H. & Dowling, J.E. (1993). Novel GABA responses from rod-driven retinal horizontal cells. Nature 361, 162–164.Google Scholar
Qian, H. & Ripps, H. (2001). The GABAC receptors of retinal neurons. Progress in Brain Research 131, 295–308.Google Scholar
Ragozzino, D., Woodward, R.M., Murata, Y., Eusebi, F., Overman, L.E., & Miledi, R. (1996). Design and in vitro pharmacology of a selective gamma-aminobutyric acid C receptor antagonist. Molecular Pharmacology 50, 1024–1030.Google Scholar
Roska, B., Nemeth, E., & Werblin, F.S. (1998). Response to change is facilitated by a three-neuron disinhibitory pathway in the tiger salamander retina. Journal of Neuroscience 18, 3451–3459.Google Scholar
Sagar, S.M. (1990). NADPH-diaphorase reactive neurons of the rabbit retina: Differential sensitivity to excitotoxins and unusual morphologic features. Journal of Comparative Neurology 300, 309–319.Google Scholar
Shen, W. & Slaughter, M.M. (2001). Multireceptor GABAergic regulation of synaptic communication in amphibian retina. Journal of Physiology 530, 55–67.Google Scholar
Shields, C.R., Tran, M.N., Wong, R.O.L., & Lukasiewicz, P.D. (2000). Distinct ionotropic GABA receptors mediate presynaptic and postsynaptic inhibition in retinal bipolar cells. Journal of Neuroscience 20, 2673–2682.Google Scholar
Shiells, R. & Falk, G. (1992). Retinal on-bipolar cells contain a nitric oxide-sensitive guanylate cyclase. Neuroreport 3, 845–848.Google Scholar
Vaney, D.I. & Young, H.M. (1988). GABA-like immunoreactivity in NADPH-diaphorase amacrine cells of the rabbit retina. Brain Research 474, 380–385.Google Scholar
Vitanova, L., Kupenova, P., Haverkamp, S., Popova, E., Mitova, L., & Wässle, H. (2001). Immunocytochemical and electrophysiological characterization of GABA receptors in the frog and turtle retina. Vision Research 41, 691–704.Google Scholar
Wässle, H., Koulen, P., Brandstätter, J.H., Fletcher, E.L., & Becker, C.-M. (1998). Glycine and GABA receptors in the mammalian retina. Vision Research 38, 1411–1430.Google Scholar
Wellis, D.P. & Werblin, F.S. (1995). Dopamine modulates GABAC receptors mediating inhibition of calcium entry into and transmitter release from bipolar cell terminals in tiger salamander retina. Journal of Neuroscience 15, 4748–4761.Google Scholar
Yang, C.Y., Lin, Z.S., & Yazulla, S. (1992). Localization of GABAA receptor subtypes in the tiger salamander retina. Visual Neuroscience 8, 57–64.Google Scholar
Yau, K.W. & Baylor, D.A. (1989). Cyclic GMP-activated conductance of retinal photoreceptor cells. Annual Review of Neuroscience 12, 289–327.Google Scholar
Zeevalk, G.D. & Nicklas, W.J. (1994). Nitric oxide in retina: Relation to excitatory amino acids and excitotoxicity. Experimental Eye Research 58, 343–350.Google Scholar
Zhang, J., Jung, C.S., & Slaughter, M.M. (1997). Serial inhibitory synapses in retina. Visual Neuroscience 14, 553–563.Google Scholar