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Nitric oxide in invertebrates

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Abstract

Nitric oxide (NO) is considered an important signaling molecule implied in different physiological processes, including nervous transmission, vascular regulation, immune defense, and in the pathogenesis of several diseases. The presence of NO is well demonstrated in all vertebrates. The recent data on the presence and roles of NO in the main invertebrate groups are reviewed here, showing the widespread diffusion of this signaling molecule throughout the animal kingdom, from higher invertebrates down to coelenterates and even to prokaryotic cells. In invertebrates, the main functional roles described for mammals have been demonstrated, whereas experimental evidence suggests the presence of new NOS isoforms different from those known for higher organisms. Noteworthy is the early appearance of NO throughout evolution and striking is the role played by the nitrergic pathway in the sensorial functions, from coelenterates up to mammals, mainly in olfactory-like systems. All literature data here reported suggest that future research on the biological roles of early signaling molecules in lower living forms could be important for the understanding of the nervous-system evolution.

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References

  • Anbar M. (1995) Nitric oxide: a sinchronizing chem-ical messenger.Experientia 51, 545–550.

    Article  PubMed  CAS  Google Scholar 

  • Bascal Z. A., Montgomery A., Holden Dye L., Williams R. G., and Walker R. J. (1995) Histo-chemical mapping of NADPH diaphorase in the nervous system of the parasitic nematodeAscaris suum.Parasitology 110, 625–637.

    Article  PubMed  CAS  Google Scholar 

  • Bicker G. and Hahnlein I. (1995) NADPH-diaphorase expression in neurones and glial cells of the locust brain.Neuroreport. 6, 325–328.

    Article  PubMed  CAS  Google Scholar 

  • Bicker G. (1996) Transmitter-induced calcium sig-nalling in cultured neurons of the insect brain.J.Neurosci. Methods 69, 33–41.

    Article  PubMed  CAS  Google Scholar 

  • Breer H. and Shepherd G. M. (1993) Implications of the NO/cGMP system in olfaction.Trends Neu-rosci. 16, 5–8.

    Article  CAS  Google Scholar 

  • Champagne D. E., Nussenzveig R. H., and Ribeiro J.M. (1995) Purification, partial characterization,and cloning of nitric oxide-carrying heme pro-teins (nitrophorins) from salivary glands of the blood-sucking insectRhodnius prolixus.J. Biol.Chem. 270, 8691–8695.

    Article  PubMed  CAS  Google Scholar 

  • Chen J. and Rosazza J. P. (1995) Purification and characterization of nitric oxide synthase (NOS-Noc) from aNocardia species.J. Bacteriol. 177, 5122–5128.

    PubMed  CAS  Google Scholar 

  • Chichery R. and Chichery M. P. (1994) NADPH-diaphorase in a cephalopod brain (Sepia): pres-ence in an analogue of the cerebellum.NeuroReport. 5, 1273–1276.

    PubMed  CAS  Google Scholar 

  • Choi S. K., Choi H. K., Kadono Okuda K., Taniai K., Kato Y., Yamamoto M., Chowdhury S., Xu J., Miyanoshita A., Debnath N. C., et al. (1995) Occurrence of novel types of nitric oxide syn-thase in the silkworm,Bombyx mori.Biochem. Bio-phys. Res. Commun. 207, 452–459.

    Article  CAS  Google Scholar 

  • Christensen S. T., Kemp K., Quie H., and Ras-mussen L. (1996) Cell death, survival and prolif-eration inTetrahymena thermophila. Effects of insulin, sodium nitroprusside, 8-Bromo cyclic GMP, NG-methyl-l-arginine and methylene blue.Cell Biol. Int. 20, 653–666.

    Article  PubMed  CAS  Google Scholar 

  • Colasanti M., Lauro G. M., and Venturini G. (1995a)NO in hydra feeding response.Nature 374, 505

    Article  PubMed  CAS  Google Scholar 

  • Colasanti M., Persichini T., Menegazzi M., Mariotto S., Giordano E., Caldarera C. M., Sogos V., Lauro G. M., and Suzuki H. (1995b) Induction of nitric oxide synthase mRNA expression. Suppression by exogenous nitric oxide.J. Biol Chem. 270, 26, 731–26,733.

    Google Scholar 

  • Colasanti M., Venturini G., Merante A., Musci G.,and Lauro G. M. (1997) Nitric oxide involvement inHydra vulgaris very primitive olfactory-like system.J. Neurosci. 17, 493–499.

    PubMed  CAS  Google Scholar 

  • Conte A. and Ottaviani E. (1995) Nitric oxide syn-thase activity in molluscan hemocytes.FEBS Lett. 365, 120–124.

    Article  PubMed  CAS  Google Scholar 

  • Cueto M., Hernandez-Perera O., Martin R., Bentura M. L., Rodrigo J., Lamas S., and Golvano M. P.(1996) Presence of nitric oxide synthase in roots and nodules ofLupinus albus.FEBS Lett. 398, 159–164.

    Article  PubMed  CAS  Google Scholar 

  • D’Alessio G., Di Donato A., Jaffe K., Maldonado H.,and Zabala N. A. (1982) Arginine and memory consolidation in praying mantis.J. Comp. Physiol. A47, 231–235.

    Article  Google Scholar 

  • de Vera M. E., Shapiro R. A., Nussler A. K., Mudgett J. S., Simmons R. L., Morris S. M. Jr., Billiar T. R., and Geller D. A. (1996) Transcriptional regulation of human inducible nitric oxide synthase (NOS2) gene by cytokines: initial analysis of the human NOS2 promoter.Froc. Natl. Acad. Sci. USA 93, 1054–1059.

    Article  Google Scholar 

  • Dow J. A., Maddrell S. H., Davies S. A., Skaer N. J., and Kaiser K. (1994) A novel role for the nitric oxide-cGMP signaling pathway: the control of epithelial function inDrosophila.Am. J. Physiol. 266, R1716–9.

    PubMed  CAS  Google Scholar 

  • Elofsson R., Carlberg M., Moroz L., Nezlin L., and Sakharov D. (1993) Is nitric oxide (NO) produced by invertebrate neurones?NeuroReport. 4, 279–282.

    Article  PubMed  CAS  Google Scholar 

  • Elphick M. R., Green I. C., and O’Shea M. (1993) Nitric oxide synthesis and action in an invertebrate brain.Brain Res. 619, 344–346.

    Article  PubMed  CAS  Google Scholar 

  • Elphick M. R., Kemenes G., Staras K., and O’Shea M. (1995) Behavioral role for nitric oxide in chemosensory activation of feeding in a mollusc.J. Neurosci. 15, 7653–7664.

    PubMed  CAS  Google Scholar 

  • Elphick M. R., Williams L., and O’Shea M. (1996) New features of the locust optic lobe: evidence of a role for nitric oxide in insect vision.J. Exp. Biol. 199, 2395–2407.

    PubMed  CAS  Google Scholar 

  • Ewer J., De Vente J., and Truman J. W. (1994) Neuropeptide induction of cyclic GMP increases in the insect CNS: resolution at the level of single identifiable neurons.J. Neurosci. 14, 7704–7712.

    PubMed  CAS  Google Scholar 

  • Feelisch M. and Martin J. F. (1995) The early role of nitric oxide in evolution.TREE 10, 496–499.

    Google Scholar 

  • Franchini A., Conte A., and Ottaviani E. (1995a) Nitric oxide: an ancestral immunocyte effector molecule.Adv. Neuroimmunol. 5, 463–478.

    Article  PubMed  CAS  Google Scholar 

  • Franchini A., Fontanili P., and Ottaviani E. (1995b) Invertebrate immunocytes: relationship between phagocytosis and nitric oxide production.Comp. Biochem. Physiol. 110B, 403–407.

    CAS  Google Scholar 

  • Garbers D. L. (1992) Guanylyl cyclase receptors and their endocrine, paracrine, and autocrine ligands.Cell 74, 1–4.

    Google Scholar 

  • Garthwaite J. (1991) Glutamate, nitric oxide and cell-cell signalling in the nervous system.Trends Neurosci. 14, 60–67.

    Article  PubMed  CAS  Google Scholar 

  • Gelperin A., Kleinfeld D., Denk W., and Cooke I. R. (1996) Oscillations and gaseous oxides in invertebrate olfaction.J. Neurobiol. 30, 110–122.

    Article  PubMed  CAS  Google Scholar 

  • Gelperin A. (1994) Nitric oxide mediates network oscillations of olfactory interneurons in a terrestrial mollusc.Nature 369, 61–63.

    Article  PubMed  CAS  Google Scholar 

  • Ghigo D., Todde R., Ginsburg H., Costamagna C., Gautret P., Bussolino F., Ulliers D., Giribaldi G., Deharo E., Gabrielli G. et al. (1995) Erythrocyte stages ofPlasmodium falciparum exhibit a high nitric oxide synthase (NOS) activity and release an NOS-inducing soluble factor.J. Exp. Med. 182, 677–688.

    Article  PubMed  CAS  Google Scholar 

  • Goldring C. E., Narayanan R., Lagadec P., and Jeannin J. F. (1995) Transcriptional inhibition of the inducible nitric oxide synthase gene by competitive binding of NF-kappa B/Rel proteins.Biochem. Biophys. Res. Commun. 209, 73–79.

    Article  PubMed  CAS  Google Scholar 

  • Griscavage J. M., Rogers N. E., Sherman M. P., and Ignarro L. J. (1993) Inducible nitric oxide synthase from a rat alveolar macrophage cell line is inhibited by nitric oxide.J. Immunol. 151, 6329–6337.

    PubMed  CAS  Google Scholar 

  • Gustafsson M. K., Lindholm A. M., Terenina N. B., and Reuter M. (1996) NO nerves in a tapeworm. NADPH-diaphorase histochemistry in adultHymenolepis diminuta.Parasitology 113, 559–565.

    PubMed  CAS  Google Scholar 

  • Hall L. R. and Titus R. G. (1995) Sand fly vector saliva selectively modulates macrophage functions that inhibit killing ofLeishmania major and nitric oxide production.J. Immunol. 155, 3501–3506.

    PubMed  CAS  Google Scholar 

  • Huque T. and Brand J. G. (1994) Nitric oxide synthase activity of the taste organ of the channel catfish,Ictalurus punctatus.Comp. Biochem. Physiol. 108B, 481–486.

    CAS  Google Scholar 

  • Jacklet J. W. (1995) Nitric oxide is used as an orthograde cotransmitter at identified histaminergic synapses.J. Neurophysiol. 74, 891–895.

    PubMed  CAS  Google Scholar 

  • Jacklet J. W. and Gruhn M. (1994) Co-localization of NADPH-diaphorase and myomodulin in synaptic glomeruli ofAplysia.Neuro Report.5, 1841–1844.

    CAS  Google Scholar 

  • Jaffe K. and Blanco M. E. (1994) Involvement of amino acids, opioids, nitric oxide, and NMDA receptors in learning and memory consolidation in crickets.Pharmacol. Biochem. Behav. 47, 493–496.

    Article  PubMed  CAS  Google Scholar 

  • Jain B., Rubinstein I., Robbins R. A., Leise K. L., and Sisson J. H. (1993) Modulation of airway epithelial cell ciliary beat frequency by nitric oxide.Biochem. Biophys. Res. Commun. 191, 83–88.

    Article  PubMed  CAS  Google Scholar 

  • Johansson K. U. and Carlberg M. (1995) NO-synthase: what can research on invertebrates add to what is already known?Adv. Neuroimmunol. 5, 431–442.

    Article  PubMed  CAS  Google Scholar 

  • Kamijo R., Harada H., Matsuyama T., Bosland M., Gerecitano J., Shapiro D., Le J., Koh S. I., Kimura T.,and Green S. J. (1994) Requirement for transcription factor IRF-1 in NO synthase induction in macrophages.Science 263, 1612–1615.

    Article  PubMed  CAS  Google Scholar 

  • Kinney G. A. and Slater N. T. (1993) Potentiation of NMDA receptor-mediated transmission in turtle cerebellar granule cells by activation of metabotropic glutamate receptors.J. Neurophysiol. 69, 585–594.

    PubMed  CAS  Google Scholar 

  • Kuzin B., Roberts I., Peunova N. and Enikolopov G. (1996) Nitric oxide regulates cell proliferation duringDrosophila development.Cell 87, 639–649.

    Article  PubMed  CAS  Google Scholar 

  • Leake L. D., Davis M. P., Chen D. and Moroz L. L. (1995) An unique model for the analysis of neuronal nitric oxide signaling: the leech CNS.Acta Biol. Hung. 46, 135–143.

    PubMed  CAS  Google Scholar 

  • Leake L. D. and Moroz L. L. (1996) Putative nitric oxide synthase (NOS)-containing cells in the central nervous system of the leech,Hirudo medicinalis: NADPH-diaphorase histochemistry.Brain Res. 723, 115–124.

    Article  PubMed  CAS  Google Scholar 

  • Lin M. F. and Leise E. M. (1996) NADPHdiaphorase activity changes during gangliogenesis and metamorphosis in the gastropod molluscIlyanassa obsoleta.J. Comp. Neurol. 374, 194–203.

    Article  PubMed  CAS  Google Scholar 

  • Liu Y., Shenouda D., Bilfinger T. V., Stefano M. L., Magazine H. I., and Stefano G. B. (1996) Morphine stimulates nitric oxide release from invertebrate microglia.Brain Res. 722, 125–131.

    Article  PubMed  CAS  Google Scholar 

  • Li Z. S. and Furness J. B. (1993) Nitric oxide synthase in the enteric nervous system of the rainbow trout,Salmo gairdneri.Arch. Histol. Cytol. 56, 185–193.

    PubMed  CAS  Google Scholar 

  • Li Z. S., Murphy S., Furness J. B., Young H. M., and Campbell G. (1993) Relationships between nitric oxide synthase, vasoactive intestinal peptide and substance P immunoreactivities in neurons of the amphibian intestine.J. Auton. Nerv. Syst. 44, 197–206.

    Article  PubMed  CAS  Google Scholar 

  • Loomis W. F. (1955) Glutathione control of the specific feeding reactions of hydra.Ann. NY Acad. Sci. 62, 209–228.

    Article  CAS  Google Scholar 

  • Lyon J. A. and Hinshaw V. S. (1993) Inhibition of nitric oxide induction from avian macrophage cell lines by influenza virus.Avian. Dis. 37, 868–873.

    Article  PubMed  CAS  Google Scholar 

  • Magazine H. I., Liu Y., Bilfinger T. V., Fricchione G.L., and Stefano G. B. (1996) Morphineinduced conformational changes in human monocytes, granulocytes, and endothelial cells and in invertebrate immunocytes and microglia are mediated by nitric oxide.J. Immunol. 156, 4845–4850.

    PubMed  CAS  Google Scholar 

  • Martinez A. (1995) Nitric oxide synthase in invertebrates.Histochem. J. 27, 770–776.

    PubMed  CAS  Google Scholar 

  • Martinez A., Riveros Moreno V., Polak J. M., Moncada S., and Sesma P. (1994) Nitric oxide (NO) synthase immunoreactivity in the starfishMarthasterias glacialis.Cell Tissue Res 275, 599–603.

    Article  CAS  Google Scholar 

  • Meulemans A., Mothet J. P., Schirar A., Fossier P., Taue L., and Baux G. (1995) A nitric oxide synthase activity is involved in the modulation of acetylcholine release inAplysia ganglion neurons: a histological, voltammetric and electrophysiological study.Neuroscience 69, 985–995.

    Article  PubMed  CAS  Google Scholar 

  • Meyer W. (1994) NADPH diaphorase (nitric oxide synthase) in the central nervous system of spiders (Arachnida: Araneida)Neurosci. Lett. 165, 105–108.

    Article  PubMed  CAS  Google Scholar 

  • Moghadam H. F., Winlow W., and Moroz L. L. (1995) Effects of hydrogen peroxide and nitric oxide (NO) on neuronal discharges and intracellular calcium concentration in the molluscan CNS.Acta Biol. Hung. 46, 145–153.

    PubMed  CAS  Google Scholar 

  • Moncada S. and Martin J. F. (1993) Evolution of nitric oxide.Lancet 341, 1511

    Article  PubMed  CAS  Google Scholar 

  • Moroz L. L., Chen D., Gillette M. U., and Gillette R. (1996) Nitric oxide synthase activity in the molluscan CNS.J. Neurochem. 66, 873–876.

    PubMed  CAS  Google Scholar 

  • Moroz L. L. and Gillette R. (1995) From Polyplacophora to Cephalopoda: comparative analysis of nitric oxide signalling in mollusca.Acta Biol. Hung. 46, 169–182.

    PubMed  CAS  Google Scholar 

  • Moroz L. L. and Gillette R. (1996) NADPHdiaphorase localization in the CNS and peripheral tissues of the predatory sea-slugPleurobranchaea californica.J. Comp. Neurol. 367, 607–622.

    Article  PubMed  CAS  Google Scholar 

  • Moroz L. L., Park J. H., and Winlow W. (1993) Nitric oxide activates buccal motor patterns inLymnaea stagnalis.NeuroReport. 4, 643–646.

    Article  PubMed  CAS  Google Scholar 

  • Moroz L. L., Radbourne S., and Winlow W. (1995) The use of NO-sensitive microelectrodes for direct detection of nitric oxide (NO) production in molluscs.Acta Biol. Hung. 46, 155–167.

    PubMed  CAS  Google Scholar 

  • Moroz L. L., Winlow W., Turner R. W., Bulloch A. G., Lukowiak K., and Syed N. I. (1994) Nitric oxide synthase-immunoreactive cells in the CNS and periphery ofLymnaea.NeuroReport.5, 1277–1280.

    PubMed  CAS  Google Scholar 

  • Mothet J. P., Fossier P., Taue L., and Baux G. (1996) NO decreases evoked quantal ACh release at a synapse of Aplysia by a mechanism independent of Ca2+ influx and protein kinase G.J. Physiol. Lond. 493, 769–784.

    PubMed  CAS  Google Scholar 

  • Muller U. and Bicker G. (1994) Calcium-activated release of nitric oxide and cellular distribution of nitric oxide-synthesizing neurons in the nervous system of the locust.J. Neurosci. 14, 7521–7528.

    PubMed  CAS  Google Scholar 

  • Muller U. and Buchner E. (1993) Histochemical localization of NADPH-diaphorase in the adultDrosophila brain. Is nitric oxide a neuronal messenger also in insects?Naturwissenschaften. 80, 524–526.

    Article  PubMed  CAS  Google Scholar 

  • Muller U. (1994) Ca2+/calmodulin-dependent nitric oxide synthase inApis mellifera andDrosophila melanogaster.Eur. J. Neurosci. 6, 1362–1370.

    Article  PubMed  CAS  Google Scholar 

  • Muller U. and Hildebrandt H. (1995) The nitric oxide/cGMP system in the antennal lobe ofApis mellifera is implicated in integrative processing of chemosensory stimuli.Eur. J. Neurosci. 7, 2240–2248.

    Article  PubMed  CAS  Google Scholar 

  • Ottaviani E., Franchini A., Cassanelli S., and Genedani S. (1995) Cytokines and invertebrate immune responses.Biol. Cell 85, 87–91.

    Article  PubMed  CAS  Google Scholar 

  • Ottaviani E., Franchini A., and Franceschi C. (1997) Pro-opiomelanocortin-derived peptides, cytokines, and nitric oxide in immune responses and stress: an evolutionary approach.Int. Rev. Cytol. 170, 79–141.

    PubMed  CAS  Google Scholar 

  • Ottaviani E. and Franchini A. (1995) Immune and neuroendocrine responses in molluscs: the role of cytokines.Acta Biol. Hung. 46, 341–349.

    PubMed  CAS  Google Scholar 

  • Ottaviani E., Paeman L. R., Cadet P. and Stefano G. B. (1993) Evidence for nitric oxide production and utilization as a bacteriocidal agent by invertebrate immunocytes.Eur J. Pharmacol. 248, 319–324.

    PubMed  Google Scholar 

  • Palumbo A., Di Cosmo A., Gesualdo I., and D’Ischia M. (1997) A calcium-dependent Nitric Oxide Synthase and NMDA R1 glutamate receptor in the ink gland ofSepia officinalis: a hint to a regulatory role of nitric oxide in melanogenesis?Biochem. Biophys. Res. Commun. 235, 429–432.

    Article  PubMed  CAS  Google Scholar 

  • Pivovarov A. S. and Egido Villarreal W. (1995) Inhibitors of NO-synthase and guanylate cyclase block the modulation of cholinoreceptor plasticity in snail neurons by 15-hydroxyeicosatetraenoic acid].Zh. Vyssh. Nerv. Deiat. Im. I. P. Pavlova. 45, 558–564.

    PubMed  CAS  Google Scholar 

  • Radomski M. W., Martin J. F., and Moncada S. (1991) Synthesis of nitric oxide by the haemocytes of the american horseshoe crab (Limulus polyphemus) Philos.Trans. R. Soc. Lond. (Biol) 334, 129–133.

    Article  CAS  Google Scholar 

  • Regulski M. and Tully T. (1995) Molecular and biochemical characterization of dNOS: aDrosophila Ca2+/calmodulin-dependent nitric oxide synthase.Proc. Natl. Acad. Sci. USA 92, 9072–9076.

    Article  PubMed  CAS  Google Scholar 

  • Ribeiro J. M., Hazzard J. M., Nussenzveig R. H., Champagne D. E., and Walker F. A. (1993) Reversible binding of nitric oxide by a salivary heme protein from a bloodsucking insect.Science 260, 539–541.

    Article  PubMed  CAS  Google Scholar 

  • Ribeiro J. M., Marinotti O., and Gonzales R. (1990) A salivary vasodilator in the blood-sucking bug,Rhodnius prolixus.British. J. Pharmacol 101, 932–936.

    CAS  Google Scholar 

  • Ribeiro J. M. and Nussenzveig R. H. (1993) Nitric oxide synthase activity from a hematophagous insect salivary gland.FEBS Lett. 330, 165–168.

    Article  PubMed  CAS  Google Scholar 

  • Ribeiro J. M. and Walker F. A. (1994) High affinity histamine-binding and antihistaminic activity of the salivary nitric oxide-carrying heme protein (nitrophorin) ofRhodnius prolixus.J. Exp. Med. 180, 2251–2257.

    Article  PubMed  CAS  Google Scholar 

  • Robertson J. D., Bonaventura J., and Kohm A. P. (1994) Nitric oxide is required for tactile learning inOctopus vulgaris.Proc. R. Soc. Lond. B. Biol. Sci. 256, 269–273.

    Article  CAS  Google Scholar 

  • Salleo A., Musci G., Barra P. F. A., and Calabrese L. (1996) The discharge mechanism of acontial nematocytes involves the release of nitric oxide.J. Exp. Biol. 199, 1261–1267.

    PubMed  CAS  Google Scholar 

  • Sanchez Alvarez M., Leon Olea M., Talavera E., Pellicer F., Sanchez Islas E., and Martinez Lorenzana G. (1994) Distribution of NADPH-diaphorase in the perioesophageal ganglia of the snail,Helix aspersa.Neurosci. Lett. 169, 51–55.

    Article  Google Scholar 

  • Sawada M., Ichinose M., and Hara N. (1995) Nitric oxide induces an increased Na+ conductance in identified neurons ofAplysia.Brain Res. 670, 248–256.

    Article  PubMed  CAS  Google Scholar 

  • Schober A., Malz C. R., and Meyer D. L. (1993) Enzyme histochemical demonstration of nitric oxide synthase in the diencephalon of the rainbow trout (Oncorhynchus mickiss) Neurosci. Lett. 151, 67–70.

    Article  PubMed  CAS  Google Scholar 

  • Schober A., Malz C. R., Schober W., and Meyer D. L. (1994) NADPH-diaphorase in the central nervous system of the larval lamprey (Lampetra planen) J. Comp. Neurol. 345, 94–104.

    Article  PubMed  CAS  Google Scholar 

  • Scholz N. L., Goy M. F., Truman J. W., and Graubard K. (1996) Nitric oxide and peptide neurohormones activate cGMP synthesis in the crab stomatogastric nervous system.J. Neurosci. 16, 1614–1622.

    PubMed  CAS  Google Scholar 

  • Schoor W. P. and Plumb J. A. (1994) Induction of nitric oxide synthase in channel catfishIctalurus punctatus byEdwardsiella ictaluri.Dis. Aquat. Org. 19, 153–155.

    Article  Google Scholar 

  • Snyder S. H. and Bredt D. S. (1991) Nitric oxide as a neuronal messenger.Trends Pharmacol. Sci. 12, 125–128.

    Article  PubMed  CAS  Google Scholar 

  • Stefano G. B., Liu Y., and Goligorsky M. S. (1996) Cannabinoid receptors are coupled to nitric oxide release in invertebrate immunocytes, microglia, and human monocytes.J. Biol. Chem. 271, 19238–19242.

    Article  PubMed  CAS  Google Scholar 

  • Stenger S., Donhauser N., Thuring H., Rollinghoff M., and Bogdan C. (1996) Reactivation of latent leishmaniasis by inhibition of inducible nitric oxide synthase.J. Exp. Med. 183, 1501–1514.

    Article  PubMed  CAS  Google Scholar 

  • Talavera E., Martinez Lorenzana G., Leon Olea M., Sanchez Alvarez M., Sanchez Islas E., and Pellicer F. (1995) Histochemical distribution of NADPH-diaphorase in the cerebral ganglion of the crayfishCambarellus montezumae.Neurosci. Lett. 187, 177–180.

    Article  PubMed  CAS  Google Scholar 

  • Truman J. W., De Vente T., and Ball E. E. (1996) Nitric oxide-sensitive guanylate cyclase activity is associated with the maturational phase of neuronal development in insects.Development 122, 3949–3958.

    PubMed  CAS  Google Scholar 

  • Valenzuela J. G., Walker F. A., and Ribeiro J.M. (1995) A salivary nitrophorin (nitric-oxide-carrying hemoprotein) in the bedbugCimex lectularius.J. Exp. Biol. 198, 1519–1526.

    PubMed  CAS  Google Scholar 

  • Villar M. J., Settembrini B. P., Hokfelt T., and Tramezzani J. H. (1994) NOS is present in the brain ofTriatoma infestans and is colocalized with CCK.NeuroReport. 6, 81–84.

    Article  PubMed  CAS  Google Scholar 

  • Yuda M., Hirai M., Miura K., Matsumura H., Ando K., and Chinzei Y. (1996) cDNA cloning, expression and characterization of nitric-oxide synthase from the salivary glands of the blood-sucking insectRhodnius prolixus.Eur. J. Biochem. 242, 807–812.

    Article  PubMed  CAS  Google Scholar 

  • Yui Y., Hattori R., Kosuga K., Eizawa H., Hiki K., Ohkawa S., Ohnishi K., Terao S. and Kawai C. (1991) Calmodulin-independent nitric oxide synthase from rat polymorphonuclear neutrophils.J. Biol. Chem. 266, 3369–3371.

    PubMed  CAS  Google Scholar 

  • Zielinski B. S., Osahan J. K., Hara T. J., Hosseini M., and Wong E. (1996) Nitric oxide synthase in the olfactory mucosa of the larval sea lamprey (Petromyzon marinus) J. Comp. Neurol. 365, 18–26.

    Article  PubMed  CAS  Google Scholar 

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  1. Department of Biology, University of Rome III, Viale Marconi, 446-00146, Rome, Italy

    Marco Colasanti & Giorgio Venturini

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Colasanti, M., Venturini, G. Nitric oxide in invertebrates. Mol Neurobiol 17, 157–174 (1998). https://doi.org/10.1007/BF02802029

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