Hostname: page-component-848d4c4894-tn8tq Total loading time: 0 Render date: 2024-07-07T16:38:37.207Z Has data issue: false hasContentIssue false
  • English
  • Français

Gycine and GABA interact to regulate the nitric oxide/cGMP signaling pathway in the turtle retina

Published online by Cambridge University Press:  03 February 2006

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

Abstract

Nitric oxide (NO) is a free radical that is important in retinal signal transduction and cyclic guanosine monophosphate (cGMP) is a critical downstream messenger of NO. The NO/cGMP signaling pathway has been shown to modulate neurotransmitter release and gap junction coupling in horizontal cells and amacrine cells, and increase the gain of the light response in photoreceptors. However, many of the mechanisms controlling the production of NO and cGMP remain unclear. Previous studies have shown activation of NO/cGMP production in response to stimulation with N-methyl-d-aspartate (NMDA) or nicotine, and the differential modulation of cGMP production by GABAA and GABAC receptors (GABAARs and GABACRs). This study used cGMP immunocytochemistry and NO imaging to investigate how the inhibitory GABAergic and glycinergic systems modulate the production of NO and cGMP. Our data show that blocking glycine receptors (GLYR) with strychnine (STRY) produced moderate increases in cGMP-like immunoreactivity (cGMP-LI) in select types of amacrine and bipolar cells, and strong increases in NO-induced fluorescence (NO-IF). TPMPA, a selective GABACR antagonist, greatly reduced the increases in cGMP-LI stimulated by STRY, but did not influence the increase in NO-IF stimulated by STRY. Bicuculline (BIC), a GABAAR antagonist, however, enhanced the increases in both the cGMP-LI and NO-IF stimulated by STRY. CNQX, a selective antagonist for α-Amino-3-hydroxy-5-methyl-4-isoxazoleproprionic acid hydrobromide/kainic acid (AMPA/KA) receptors, eliminated both the increases in cGMP-LI and NO-IF stimulated by STRY, while MK801, a selective antagonist for NMDA receptors, slightly increased the cGMP-LI and slightly decreased the NO-IF stimulated by STRY. Finally, double labeling of NO-stimulated cGMP and either GLY or GABA indicated that cGMP predominantly colocalized with GLY. Taken together, these findings support the hypothesis that GLY and GABA interact in the regulation of the NO/cGMP signaling pathway, where GLY primarily inhibits NO production and GABA has a greater effect on cGMP production. Such interacting inhibitory pathways could shape the course of signal transduction of the NO/cGMP pathway under different physiological situations.

Keywords

Nitric oxidecGMPGABAGlycineTurtleRetina
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 6 , November 2005 , pp. 825 - 838
Copyright
© 2005 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

Ammermüller, J. & Kolb, H. (1995). The organization of the turtle inner retina. I. ON- and OFF-center pathways. Journal of Comparative Neurology 358, 1–34.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.CrossRefGoogle 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, 75–85.3.0.CO;2-F>CrossRefGoogle Scholar
Blute, T.A., Lee, M.R., & Eldred, W.D. (2000). Direct imaging of NMDA-stimulated nitric oxide production in the retina. Visual Neuroscience 17, 557–566.CrossRefGoogle Scholar
Blute, T.A., Strang, C., Keyser, K.T., & Eldred, W.D. (2003). Activation of the cGMP/nitric oxide signal transduction system by nicotine in the retina. Visual Neuroscience 20, 165–176.CrossRefGoogle Scholar
Crooks, J. & Kolb, H. (1992). Localization of GABA, glycine, glutamate and tyrosine hydroxylase in the human retina. Journal of Comparative Neurology 15, 287–302.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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
Eldred, W.D. (2000). Nitric oxide in the retina. Functional neuroanatomy of the nitric oxide system. In Handbook of Chemical Neuroanatomy, Vol. 17, eds. Steinbusch, H.W.M., De Vente, J. & Vincent, S.R., pp. 111–145. New York: Elsevier.
Eldred, W.D. & Cheung, K. (1989). Immunocytochemical localization of glycine in the retina of the turtle (Pseudemys scripta). Visual Neuroscience 2, 331–338.CrossRefGoogle Scholar
Enz, R., Brandstatter, 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
Greferath, U., Muller, F., Wässle, H., Shivers, B., & Seeburg, P. (1993). Localization of GABAA receptors in the rat retina. Visual Neuroscience 10, 551–561.CrossRefGoogle 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. Jouirnal of Comparative Neurology 447, 138–151.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle Scholar
Kalloniatis, M., Marc, R.E., & Murry, R.F. (1996). Amino acid signatures in the primate retina. Journal of Neuroscience 16, 6807–6829.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, 520–532.3.0.CO;2-3>CrossRefGoogle Scholar
Kurenni, D.E., Thurlow, G.A., Turner, R.W., Moroz, L.L., Sharkey, K.A., & Barnes, S. (1995). Nitric oxide synthase in tiger salamander retina. Journal of Comparative Neurology 361, 525–536.CrossRefGoogle Scholar
Lukasiewicz, P.D. (1996). GABAC receptors in the vertebrate retina. Molecular Neurobiology 12, 181–194.CrossRefGoogle 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
Marc, R.E., Murry, R.F., & Basinger, S.F. (1995). Pattern recognition of amino acid signatures in retinal neurons. Journal of Neuroscience 15, 5106–5129.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.M., & Nakaki, T. (1990). Arginine blocks gap junctions between retinal horizontal cells. NeuroReport 1, 107–110.CrossRefGoogle Scholar
Ohkuma, S., Katsura, M., Chen, D.Z., Narihara, H., & Kuriyama, K. (1996a). Nitric oxide-evoked [3H] gamma-aminobutyric acid release is mediated by two distinct release mechanisms. Brain Research Molecular Brain Research 36, 137–144.Google Scholar
Ohkuma, S., Katsura, M., Guo, J.L., Narihara, H., Hasegawa, T., & Kuriyama, K. (1996b). Role of peroxynitrite in [3H] gamma-aminobutyric acid release evoked by nitric oxide and its mechanism. European Journal of Pharmacology 301, 179–188.Google Scholar
Pourcho, R.G. & Goebel, D.J. (1985). A combined Golgi and autoradiographic study of (3H)glycine-accumulating amacrine cells in the cat retina. Journal of Comparative Neurology 233, 473–480.CrossRefGoogle Scholar
Prast, H. & Philippu, A. (2001). Nitric oxide as modulator of neuronal function. Progress in Neurobiology 64, 51–68.CrossRefGoogle Scholar
Qian, H. & Ripps, H. (2001). The GABAC receptors of retinal neurons. Progress in Brain Research 131, 295–308.CrossRefGoogle 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
Sagar, S. (1990). NADPH-diaphorase reactive neurons of the rabbit retina: Differential sensitivity to excitotoxins and unusual morphologic features. Journal of Comparative Neurology 300, 309–319.CrossRefGoogle Scholar
Savchenko, A., Barnes, S., & Kramer, R.H. (1997). Cyclic-nucleotide-gated channels mediate synaptic feedback by nitric oxide. Nature 390, 694–698.Google Scholar
Shen, W. & Slaughter, M.M. (2001). Multireceptor GABAergic regulation of synaptic communication in amphibian retina. Journal of Physiology 530, 55–67.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle Scholar
White, W.F. (1985). The glycine receptor in the mutant mouse spastic (spa): Strychnine binding characteristics and pharmacology. Brain Research 329, 1–6.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.CrossRefGoogle Scholar
Yang, C.Y., Lukasiewicz, P., Maguire, G., Werblin, F.S., & Yazulla, S. (1991). Amacrine cells in the tiger salamander retina: Morphology, physiology, and neurotransmitter identification. Journal of Comparative Neurology 312, 19–32.CrossRefGoogle Scholar
Yu, D. & Eldred, W.D. (2003). GABAA and GABAC receptor antagonists increase retinal cyclic GMP levels through nitric oxide synthase. Visual Neuroscience 20, 627–638.CrossRefGoogle Scholar
Yu, D. & Eldred, W.D. (2005). Nitric oxide stimulates GABA release and inhibits glycine release in retina. Journal of Comparative Neurology 483, 278–291.CrossRefGoogle Scholar
Zabel, U., Kleinschnitz, C., Oh, P., Nedvetsky, P., Smolenski, A., Muller, H., Kronich, P., Kugler, P., Walter, U., Schnitzer, J.E., & Schmidt, H.H. (2002). Calcium-dependent membrane association sensitizes soluble guanylyl cyclase to nitric oxide. Nature Cell Biology 4, 307–311.CrossRefGoogle Scholar
Zhang, J., Jung, C.S., & Slaughter, M.M. (1997). Serial inhibitory synapses in retina. Visual Neuroscience 14, 553–563.CrossRefGoogle Scholar