Nitric oxide synthase in tiger salamander retina

Abstract

Previous studies have indicated that nitric oxide, a labile freely diffusible biological messenger synthesized by nitric oxide synthase, may modulate light transduction and signal transmission in the retina. In the present work, the large size of retinal cells in tiger salamander (Ambystoma tigrinum) allowed the utilization of nicotinamide adenine dinucleotide phosphate (NADPH)-diaphorase histochemistry and nitric oxide synthase immunocytochemistry to delineate the cell-specific intracellular localization of nitric oxide synthase. NADPH-diaphorase activity was highly concentrated in the outer retina, in rod and cone inner segment ellipsoids, and between and adjacent to the photoreceptor cell bodies in the outer nuclear layer. Examination of enzymatically isolated retinal cells indicated that outer nuclear layer NADPH-diaphorase activity was localized to the distal processes of the retinal glial (Müller) cells and to putative bipolar cell Landolt clubs. Less intense NADPH-diaphorase activity was seen in the photoreceptor inner segment myoid region, in a small number of inner nuclear layer cells, in cap-like configurations at the distal poles of cells in the ganglion cell layer and surrounding ganglion cell layer somata, and in punctate form within both plexiform layers, the pigment epithelium, and the optic nerve. Nitric oxide synthase-like immunoreactivity was similarly localized, but was also concentrated along a thin sublamina centered within the inner plexiform layer. The potential for nitric oxide generation at multiple retinal sites suggests that this molecule may play a number of roles in the processing of visual information in the retina.

Cellular localization of neuronal nitric oxide synthase (NOS-1) in the human and rat retina

“…Note that the NOS-1 protein localizes to the outer segments of cones in the human retina, but not to the outer segments of rods, to the inner segments, and to the terminals of the photoreceptors. Nitric oxide, presumably synthesized by the constitutive NOS-1 in photoreceptors, may stimulate the soluble guanylate cyclase found in photoreceptors (Koch et al, 1994), causing increases in the cyclic GMP-gated conductances (Schmidt et al, 1992;Kurenni et al, 1995) and modifying events in the visual transduction pathway. In the terminals of the photoreceptors, nitric oxide, synthesized by NOS-1 may contribute to neuromodulation (Koch et al, 1994) by increasing transmitter release (Savchenko et al, 1997).…”

Pattern of Nitrergic Neuronal System Organization in the Brain of Two Holostean Fishes (Actinopterygii: Ginglymodi)

“…Thus, nitrergic ganglion cells and photoreceptors have been reported in the retina of teleosts Pottek et al, 1997;Ota et al, 1999;Haamedi and Djamgoz, 2002;Gaikwad et al, 2009], amphibians [Nöll et al, 1994;Kurenni et al, 1995;Blom et al, 2009], reptiles [Blute et al, 1997], birds [Fischer and Stell, 1999;Wilson et al, 2011;Tekmen-Clark and Gleason, 2013], and mammals [Blom et al, 2012], where protoreceptor cells always lack nitrergic labeling. Furthermore, nitrergic bipolar neurons have been described in the retina of chondrichthyes [Shiells and Falk, 1992], amphibians [Nöll et al, 1994;Kurenni et al, 1995;Blom et al, 2009], and reptiles [Cao and Eldred, 2001], whereas horizontal nitrergic cells have been reported only in teleosts [Ota et al, 1999;Haamedi and Djamgoz, 2002] and reptiles [Haverkamp and Eldred, 1998;Cuenca et al, 2000].…”

“…Retinal NO might modulate the neuronal communication between bipolar and ganglion cells, like the transient conversion of synaptic inhibition to excitation [Hoffpauir et al, 2006]. Amacrine cells, either NADPH-d reactive or NOSir, have been thoroughly reported in the retina of teleosts Pottek et al, 1997;Haamedi and Djamgoz, 2002], amphibians [Nöll et al, 1994;Kurenni et al, 1995;Blom et al, 2009], reptiles , birds [Fischer and Stell, 1999;Wilson et al, 2011;Tekmen-Clark and Gleason, 2013], and mammals [Vielma et al, 2012], representing a feature shared in all osteichthyes studied. Of note, holosteans, like cladistians, lack other nitrergic cells in the retina [López et al, 2016;present results].…”

“…References: agnathans: Schober et al, 1994a;Kyriakatos et al, 2009;chondrichthyes: Shiells and Falk, 1992;Pérez et al, 1995;Álvarez-Otero et al, 1996;Funakoshi et al, 1997;Ferrando et al, 2012;Pose-Mendez et al, 2014;cladistians: López et al, 2016;chondrosteans: Pushchina and Obukhov, 2012;teleosts: Holmqvist et al, 1994teleosts: Holmqvist et al, , 2000Ostholm et al, 1994;Arévalo et al, 1995;Brüning et al, 1995;Anken and Rahmann, 1996;Cioni et al, 1997;Pottek et al, 1997;Funakoshi et al, 1999;Baby et al, 2000;Oyan et al, 2000;Haamedi and Djamgoz, 2002;Bordieri et al, 2003Bordieri et al, , 2005Singru et al, 2003;Ando et al, 2004;Bordieri and Cioni, 2004;Pushchina and Diuĭzen, 2004;Pushchina, 2007;Pushchina et al, 2007;Giráldez-Pérez et al, 2008Gaikwad et al, 2009;Pushchina and Obukhov, 2010;Ganz et al, 2012;lungfishes: Schober et al, 1994b;Northcutt, 2009;amphibians: Nöll et al, 1994;Crowe et al, 1995;Kurenni et al, 1995;Brüning and Mayer, 1996;González et al, 1996González et al, , 2002b…”

Nitric Oxide as an Efferent Modulator of Circadian Pacemaker Neurones in the Eye of the Marine Mollusc Bulla gouldiana~!2008-04-11~!2008-06-27~!2008-08-26~!

“…NO may also influence light-evoked CAPs by modulating calcium channels, as shown for lizard cone terminals [72] and salamander rod terminals [73]. In snail feeding neurones, NO modulates voltage dependent Ltype calcium channels, which have also been identified in Bulla BRNs [74], via cGMP induction of channel phosphorylation by protein kinases [37].…”