Nitric oxide synthesis and action in an invertebrate brain

Elphick, Maurice R.; Green, Irene C.; O’Shea, Michael

doi:10.1016/0006-8993(93)91632-3

Cited by 140 publications

(76 citation statements)

References 9 publications

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“…Consistent with this view are existing histochemical data. NOS activity has been detected in several invertebrate tissue extracts, including Drosophila brain (49)(50)(51)(52)(53). Applications of NOS inhibitors or NO-generating substances have been shown to modulate the activity of buccal motoneurones in Lymnaea stagnalis (52) and the oscillatory dynamics of olfactory neurons in procerebral lobe of Limax maximus (54).…”

Section: Discussionmentioning

confidence: 99%

Molecular and biochemical characterization of dNOS: a Drosophila Ca2+/calmodulin-dependent nitric oxide synthase.

Regulski

Tully²

1995

Proc. Natl. Acad. Sci. U.S.A.

227

144

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Nitric oxide (NO) is an intercellular messenger involved with various aspects of mammalian physiology ranging from vasodilation and macrophage cytotoxicity to neuronal transmission. NO is synthesized from L-arginine by NO synthase (NOS). Here, we report the cloning of a Drosophila NOS gene, dNOS, located at cytological position 32B.The dNOS cDNA encodes a protein of 152 kDa, with 43% amino acid sequence identity to rat neuronal NOS. Like mammalian NOSs, DNOS protein contains putative binding sites for calmodulin, FMN, FAD, and NADPH. DNOS activity is Ca2+/calmodulin dependent when expressed in cell culture. An alternative RNA splicing pattern also exists for dNOS, which is identical to that for vertebrate neuronal NOS. These structural and functional observations demonstrate remarkable conservation of NOS between vertebrates and invertebrates.Nitric oxide (NO) is synthesized by NO synthases (NOSs) during conversion of L-arginine to L-citrulline (for reviews, see refs. 1 and 2). Biochemical characterization of NOSs has distinguished two general classes: (i) constitutive, dependent on exogenous Ca2+/calmodulin, and (ii) inducible, independent of exogenous Ca2+/calmodulin. Analyses of cDNA clones have identified three distinct NOS genes in mammals (3-6): neuronal, endothelial, and macrophage. The neuronal and endothelial NOSs are constitutive, and the macrophage NOS is inducible. The nomenclature for these different isoforms used here is historical, as it is clear now that one or more isoforms can be present in the same tissue (7).As a diffusible, free-radical gas, NO is a multifunctional messenger affecting many diverse aspects of mammalian physiology (for review, see ref. 8), such as regulation of vascular tone, macrophage-mediated cytotoxicity, and cell-cell interactions in the nervous system, including synaptogenesis and apoptosis during development of the rat central nervous system (9) and during neuronal cell differentiation (10). NO also appears to be involved with long-term potentiation in hippocampus and with long-term depression in cerebellum, two forms of synaptic plasticity that may underlie behavioral plasticity (11-15). Consistent with these cellular studies, inhibition of NOS activity may disrupt learning (refs. 16-19, but see refs. 20 and 21).Many of the above results are based on pharmacological studies using inhibitors of NOS or donors of NO. Interpretations of such studies usually are limited because the drugs interact with more than one target and cannot be delivered to specific sites. A molecular genetic approach can overcome these problems, however, by disrupting a specific gene, the product of which may be one of the drug's targets. Recently, such an approach has been attempted in mice via generation of a knockout mutation of the neuronal NOS (nNOS) (22).While nNOS mutants appeared fully viable and fertile, minor defects in stomach morphology and hippocampal long-term potentiation were detected (22, 23). Taken together, the above reports suggest roles for NO in developmental and behav...

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Section: Discussionmentioning

confidence: 99%

Molecular and biochemical characterization of dNOS: a Drosophila Ca2+/calmodulin-dependent nitric oxide synthase.

Regulski

Tully²

1995

Proc. Natl. Acad. Sci. U.S.A.

227

144

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“…؉ injection In the CNS of invertebrates and vertebrates, NO-activated soluble guanylate cyclase is one of the enzymes responsible for the production of cGMP and subsequent activation of PKG (Moncada et al, 1991;Elphick et al, 1993), although other activators of PKG do exist (Morton and Giunta, 1992;Müller, 1997). Histochemical techniques and immunocytochemistry have been used to identify cells in the locust thoracic nerve cord that contain NOS, the key enzyme that produces NO as it converts L-arginine to L-citrulline (Moncada et al, 1991;Müller, 1997;Bullerjahn and Pflüger, 2003).…”

Section: Inhibition Of Nos Attenuates Sd-like Events Evoked By Extracmentioning

confidence: 99%

Suppression of Spreading Depression-Like Events in Locusts by Inhibition of the NO/cGMP/PKG Pathway

Armstrong¹,

Rodgers²,

Money³

et al. 2009

Journal of Neuroscience

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Despite considerable research attention focused on mechanisms underlying neural spreading depression (SD), because of its association with important human CNS pathologies, such as stroke and migraine, little attention has been given to explaining its occurrence and regulation in invertebrates. In the locust metathoracic ganglion (MTG), an SD-like event occurs during heat and anoxia stress, which results in cessation of neuronal output for the duration of the applied stress. SD-like events were characterized by an abrupt rise in extracellular potassium ion concentration ([K ϩ ] o ) from a baseline concentration of ϳ8 to Ͼ30 mM, which returned to near baseline concentrations after removal of the applied stress. After return to baseline [K ϩ ] o , neuronal output (ventilatory motor pattern activity) from the MTG recovered. Unlike mammalian neurons, which depolarize almost completely during SD, locust neurons only partially depolarized. SD-like events in the locust CNS were suppressed by pharmacological inhibition of the nitric oxide/cyclic guanosine monophosphate/protein kinase G (NO/cGMP/PKG) pathway and were exacerbated by its activation. Also, environmental stressors such as heat and anoxia increased production of nitric oxide in the locust CNS. Finally, for the intact animal, manipulation of the pathway affected the speed of recovery from suffocation by immersion under water. We propose that SD-like events in locusts provide an adaptive mechanism for surviving extreme environmental conditions. The highly conserved nature of the NO/cGMP/PKG signaling pathway suggests that it may be involved in modulating SD in other organisms, including mammals.

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“…The numerous studies using NADPHd histochemistry cited above, biochemical measurements of NOS activity in tissue extracts (Elphick et al, 1993(Elphick et al, , 1995bElofsson et al, 1993;Muller, 1994;Willer and Bicker, 1994), electrophysiological (Moroz and Park, 1993;Moroz et al, 1993a,b;Gelperin, 1994a,b;Jacklet and Gruhn, 1994b;Elphick et al, 1995a;Jacklet, 1995;Sawada et al, 1995), and behavioral studies (Robertson et al, 1994(Robertson et al, , 1995Elphick et al, 1995a) all support the idea that NO is an intercellular messenger in nervous systems of the more evolutionarily advanced invertebrates. In arthropods, such as the fruit fly, Drosophila melanogaster, the honey bee, Apis mellifera, the locust, Schistocerca gregaria, and the crayfish, Pacifastacus leniusculus and Cambarellus montezumae, the greatest NOS activity has been detected in the glomeruli and somata of the antennal lobes where olfactory receptor neurons make synaptic connections with local and relay interneurons (Müller and Buchner, 1993;Johansson and Carlberg, 1994;Meyer, 1994;Miller, 1994;Müller and Bicker, 1994;Bicker and Hahnlein, 1995;Elphick et al, 1995;Talavera et al, 1995).…”

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confidence: 91%

NADPH-Diaphorase activity changes during gangliogenesis and metamorphosis in the gastropod molluscIlyanassa obsoleta

Lin

Leise

1996

J. Comp. Neurol.

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Gaseous nitric oxide (NO) is produced through the action of the enzyme nitric oxide synthase (NOS) and acts as a neurotransmitter (Jacklet and Gruhn, 1994b;Elphick et al., 1995a;Jacklet, 1995) in the nervous systems of adult gastropod molluscs. By comparison, little or no information appears to exist about the ontogeny of molluscan NOS-containing neurons. NADPH-diaphorase (NADPHd) has been determined biochemically and histochemically to colocalize with NOS immunoreactivity in neurons; NOS is an isoform of NADPHd (Dawson et al., 1991;Hope et al., 1991). We used NADPHd histochemistry to map the distribution of NOS activity in the nervous systems of larvae, including metamorphosing individuals, and juveniles of the marine snail Ilyanassa obsoleta. Several ganglionic neuropils displayed reaction product throughout development. The most intense NADPHd staining occurred in the neuropil of the apical ganglion, a specialized larval structure. Intermediate staining levels occurred in neuropils of the cerebral, pedal, and pleural ganglia. Larval buccal and intestinal ganglia showed little reaction product, with slight increases arising in metamorphically competent larvae. NADPHd activity conspicuously decreased in the central nervous systems of metamorphosing larvae. The osphradial ganglion, which was present in young larvae, showed only weak NADPHd activity. Our results provide evidence for the existence of a nitrergic signalling system in molluscan larvae and juveniles.

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Nitric oxide synthesis and action in an invertebrate brain

Cited by 140 publications

References 9 publications

Molecular and biochemical characterization of dNOS: a Drosophila Ca2+/calmodulin-dependent nitric oxide synthase.

Molecular and biochemical characterization of dNOS: a Drosophila Ca2+/calmodulin-dependent nitric oxide synthase.

Suppression of Spreading Depression-Like Events in Locusts by Inhibition of the NO/cGMP/PKG Pathway

NADPH-Diaphorase activity changes during gangliogenesis and metamorphosis in the gastropod molluscIlyanassa obsoleta

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