Nitric oxide signaling in invertebrates

Abstract

Nitric oxide (NO) is an unconventional neurotransmitter and neuromodulator molecule that is increasingly found to have important signaling functions in animals from nematodes to mammals. NO signaling mechanisms in the past were identified largely through experiments on mammals, after the discovery of NO's vasodilatory functions. The use of gene knock out mice has been particularly important in revealing the functions of the several isoforms of nitric oxide synthase (NOS), the enzyme that produces NO. Recent studies have revealed rich diversity in NO signaling. In addition to the well-established pathway in which NO activates guanylyl cyclase and cGMP production, redox mechanisms involving protein nitrosylation are important contributors to modulation of neurotransmitter release and reception. NO signaling studies in invertebrates are now generating a wealth of comparative information. Invertebrate NOS isoforms have been identified in insects and molluscs, and the conserved and variable amino acid sequences evaluated. Calcium-calmodulin dependence and cofactor requirements are conserved. NADPH diaphorase studies show that NOS is found in echinoderms, coelenterates, nematodes, annelids, insects, crustaceans and molluscs. Accumulating evidence reveals that NO is used as an orthograde transmitter and cotransmitter, and as a modulator of conventional transmitter release. NO appears to be used in diverse animals for certain neuronal functions, such as chemosensory signaling, learning, and development, suggesting that these NO functions have been conserved during evolution. The discovery of NO's diverse and unconventional signaling functions has stimulated a plethora of enthusiastic investigations into its uses. We can anticipate the discovery of many more interesting and some surprising NO signaling functions.

Serotonin and nitric oxide interaction in the control of bioluminescence in northern krill, Meganyctiphanes norvegica (M. Sars)

“…NO donors [sodium nitroprusside (SNP) and S-nitroso-N-acetylpenicillamine (SNAP)] injected in live specimens significantly reduced light production stimulated by 5-HT, whereas inhibition of the enzyme NO synthase (NOS) with L-NAME (N is a molecule with a short half-life that can diffuse through cell membranes and have different intracellular effects. In many systems, the physiological effects of NO are mediated through the production of cyclic guanosine monophosphate (cGMP), by stimulation of the enzyme guanylyl cyclase in the target cell (Jacklet, 1997). NO can also control physiological mechanisms in the target cell by inhibiting mitochondrial respiration through a cGMP-independent pathway (Brown, 1994).…”

Nitric oxide in control of luminescence from hatchetfish(Argyropelecus hemigymnus) photophores

“…Nitric oxide (NO) is a freely diffusible unconventional neurotransmitter and neuromodulator molecule that is increasingly found to play an important role in several physiological systems, from invertebrates to mammals (Jacklet, 1997). Since the presence of an NO system has been described in several fish species (Schober et al, 1993;Olsson and Holmgren, 1997;Nilsson and Söderström, 1997;Cox et al, 2001), we investigated the possible role of NO as a neurotransmitter and/or modulator of the adrenergic control of bioluminescence, using isolated ventral photophores of Argyropelecus hemigymnus.…”

Nitric oxide modulates peristaltic muscle activity associated with fluid circulation in the sea pansyRenilla koellikeri

“…Nitric oxide (NO) has emerged in the last two decades as an important signalling molecule with various functions in both vertebrates and invertebrates (Jacklet, 1997;Colasanti and Venturini, 1998; for a review see Moroz, 2001). In many invertebrates, and particularly in mollusks Elphick et al, 1995;Moroz, 2000;Gelperin et al, 2000;Cole et al, 2002) and in arthropods (Truman et al, 1996;Muller, 1997;Scholz et al, 1998Scholz et al, , 2001, NO synthase (NOS) activity is concentrated in the nervous system except that of the salivary gland of a blood-feeding insect (Ribeiro and Nussenzveig, 1993) and the firefly lantern (Trimmer et al, 2001).…”