Nitric Oxide Regulates Swimming in the Jellyfish Aglantha digitale

Journal of Comparative Neurology

Volumn 471, Issue 1, 2004, Pages 26-36

  Moroz, Leonid L ^a   Meech, Robert W ^b   Sweedler, Jonathan V ^c   Mackie, George O ^d  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d UNIVERSITY OF VICTORIA   (Canada)

Author keywords

Cnidaria and invertebrates; Cyclic GMP; Evolution; Feeding locomotion; NADPH diaphorase; Sensory system

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; ARGININE; CYCLIC GMP; DIPHENYLIODONIUM SALT; GUANYLATE CYCLASE INHIBITOR; N(G) NITRO DEXTRO ARGININE METHYL ESTER; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; NITROGEN DIOXIDE; NITROGEN OXIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

ANIMAL TISSUE; ARTICLE; CAPILLARY ELECTROPHORESIS; COELENTERATE; ECTODERM; ENZYME ACTIVITY; EVOLUTION; FEEDING; INVERTEBRATE; JELLYFISH; LOCOMOTION; NERVOUS SYSTEM; NEURITE; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SWIMMING;

ANIMALS; HYDROZOA; NADPH DEHYDROGENASE; NEURITES; NEURONS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; SIGNAL TRANSDUCTION; SWIMMING; TISSUE DISTRIBUTION;

EID: 1442285303     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20023     Document Type: Article

References (81)

1. Akaike T, Yoshida M, Miyamoto Y, Sato K, Kohno M, Sasamoto K, Miyazaki K, Ueda S, Maeda H. 1993. Antagonistic action of imidazolineoxyl N-oxides against endothelium-derived relaxing factor/NO through a radical reaction. Biochemistry 32:827-832.
2. Archer S. 1993. Measurement of nitric oxide in biological models. FASEB J 7:349-360.
3. Arkett SA, Mackie GO, Meech RW. 1988. Hair cell mechanoreception in the jellyfish Aglantha digitale. J Exp Biol 135:329-342.
4. Bickell-Page LR, Mackie GO. 1991. Tentacle autotomy in the hydromedusa Aglantha digitale (Cnidaria): an ultrastructural and neurophysiological analysis. Philos Trans R Soc Lond 331:155-170.
5. Bishop CD, Brandhorst BP. 2001. NO/cGMP signaling and HSP90 activity represses metamorphosis in the sea urchin Lytechinus pictus. Biol Bull 201:394-404.
6. Bredt DS, Glatt CE, Hwang PM, Fotuhi M, Dawson TM, Snyder SH. 1991. Nitric oxide synthase protein and mRNA are discretely localized in neuronal population of the mammalian CNS together with NADPH diaphorase. Neuron 7:615-624.
7. Chandok MR, Ytterberg AJ, van Wijk KJ, Klessig DF. 2003. The pathogen-inducible nitric oxide synthase (iNOS) in plants is a variant of the P protein of the glycine decarboxylase complex. Cell 113:469-482.
8. Choi YH, Furuse M, Okumura J, Denbow DM. 1994. Nitric oxide controls feeding behavior in the chicken. Brain Res 654:163-166.
9. Colasanti M, Lauro G, Venturini G. 1995. NO in Hydra feeding response. Nature 374:505.
10. Colasanti M, Venturini G, Merante A, Musci G, Lauro GM. 1997. Nitric oxide involvement in Hydra vulgaris very primitive olfactory-like system. J Neurosci 17:493-499.
11. Cooke IRC, Edwards SL, Anderson CR. 1994. The distribution of NADPH-diaphorase activity and immunoreactivity to nitric oxide synthase in the nervous system of the pulmonate mollusc Helix aspersa. Cell Tissue Res 277:565-572.
12. Cox RL, Mariano T, Heck DE, Laskin JD, Stegeman JJ. 2001. Nitric oxide synthase sequences in the marine fish Stenotomus chrysops and the sea urchin Arbacia punctulata, and phylogenetic analysis of nitric oxide synthase calmodulin-binding domains. Comp Biochem Physiol B Biochem Mol Biol 130:479-491.
13. Cruz L, Moroz LL, Gillette R, Sweedler JV. 1997. Nitrite and nitrate levels in individual molluscan neurons: single-cell capillary electrophoresis analysis. J Neurochem 69:110-115.
14. Dawson TM, Bredt DS, Fotuhi M, Hwang PM, Snyder SH. 1991. Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc Natl Acad Sci U S A 88:7797-7801.
15. Dinerman JL, Dawson TM, Schell MJ, Snowman A, Snyder SH. 1994. Endothelial nitric oxide synthase localized to hippocampal pyramidal cells: implications for synaptic plasticity. Proc Natl Acad Sci U S A 91:4214-4218.
16. Donaldson S, Mackie GO, Roberts A. 1980. Preliminary observations on escape swimming in Aglantha digitale (Hydromedusae: Trachylina). Ca J Zool 58:549-552.
17. Elofsson R, Carlberg M, Moroz L, Nezlin L, Sakharov D. 1993. Is nitric oxide (NO) produced by invertebrate neurones? Neuroreport 4:279-282.
18. Elphick MR, Kemenes G, Staras K, O'Shea M. 1995. Behavioural role for nitric oxide in chemosensory activation of feeding in a mollusc. J Neurosci 15:7653-7664.
19. Feelisch M, Martin JE. 1995. The early role of nitric oxide in evolution. Trends Ecol Evol 10:496-499.
20. Floyd PD, Moroz LL, Gillette R, Sweedler JV. 1998. Capillary electrophoresis analysis of nitric oxide synthase related metabolites in single identified neurons. Anal Chem 70:2243-2247.
21. Franchini A, Conte A, Ottaviani E. 1995. Nitric oxide: an ancestral immunocyte effector molecule. Adv Neuroimmunol 5:463-478.
22. Garthwaite J, Boulton CL. 1995. Nitric oxide signaling in the central nervous system. Annu Rev Physiol 57:683-706.
23. Garthwaite J, Southam E, Boulton CL, Nielsen EB, Schmidt K, Mayer B. 1995. Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one. Mol Pharmacol 48:184-188.
24. Golderer G, Werner ER, Leitner S, Grobner P, Werner-Felmayer G. 2001. Nitric oxide synthase is induced in sporulation of Physarum polycephalum. Genes Dev 15:1299-1309.
25. Gruetter CA, Kadovitz PJ, Ignarro LJ. 1981. Methylene blue inhibits coronary arterial relaxation and guanylate cyclase activation by nitroglycerin, sodium nitrite and amyl nitrite. Can J Physiol Pharmacol 59:150-162.
26. Hogg N, Singh RJ, Joseph J, Neese F, Kalyanaraman B. 1995. Reactions of nitric oxide with nitronyl nitroxides and oxygen: prediction of nitrite and nitrate formation by kinetic simulation. Free Radic Res 22:47-56.
27. Hope BT, Michael GJ, Knigge KM, Vincent SR. 1991. Neuronal NADPH-diaphorase is a nitric oxide synthase. Proc Natl Acad Sci U S A 88:2811-2814.
28. Huang S, Kerschbaum HH, Engel E, Hermann A. 1997. Biochemical characterization and histochemical localization of nitric oxide synthase in the nervous system of the snail, Helix pomatia. J Neurochem 69:2516-2528.
29. Jacklet JW. 1995. Nitric oxide is used as an orthograde cotransmitter at identified histaminergic synapses. J Neurophysiol 74:891-895.
30. Kerfoot PA, Mackie GO, Meech RW, Roberts A, Singla CL. 1985. Neuromuscular transmission in the jellyfish Aglantha digitale. J Exp Biol 116:1-25.
31. Knowles RG, Moncada S. 1994. Nitric oxide synthases in mammals. Biochem J 298:249-258.
32. Korneev SA, Piper MR, Picot J, Phillips R, Korneeva EI, O'Shea M. 1998. Molecular characterization of NOS in a mollusc: expression in a giant modulatory neuron. J Neurobiol 35:65-76.
33. Kuzin B, Roberts I, Peunova N, Enikolopov G. 1996. Nitric oxide regulates cell proliferation during Drosophila development. Cell 87:639-649.
34. Lancaster JR Jr. 1994. Simulation of the diffusion and reaction of endogenously produced nitric oxide. Proc Natl Acad Sci U S A 91:8137-8141.
35. Leake LD, Moroz LL. 1996. Putative nitric oxide synthase (NOS) -containing cells in the central nervous system of the leech, Hirudo medicinals: NADPH-diaphorase histochemistry. Brain Res 723:115-124.
36. Leake LD, Davis MP, Chen D, Moroz LL. 1996. An unique model for the analysis of neuronal nitric oxide signaling: the leech CNS. In: Salanki J, S-Rozsa K, Elekes K, editors. Neurobiology of invertebrates: simple and complex regulatory systems. Budapest: Akademia Kiado. p 135-143.
37. Leckie C, Empson R, Becchetti A, Thomas J, Galione A, Whitaker M. 2003. The NO pathway acts late during the fertilization response in sea urchin eggs. J Biol Chem 278:12247-12254.
38. Levine W, Giuditta A, Englard S, Strecker J. 1960. Brain diaphorases. J Neurochem. 6:28-36.
39. Lewis RS, Deen WM. 1994. Kinetics of the reaction of nitric oxide with oxygen in aqueous solutions. Chem Res Toxicol 7:568-574.
40. Luca De B, Monda M, Sullo A. 1995. Changes in eating behavior and termogenic activity following inhibition of nitric oxide formation. Am J Physiol 268:R1533-R1538.
41. Mackie GO. 1980. Slow swimming and cyclical "fishing" behavior in Aglantha digitale (Hydromedusae: Trachylina). Can J Fish Aquat Sci 37:1550-1556.
42. Mackie GO. 2004a. Central neural circuitry in the jellyfish Aglantha: a model "simple nervous system". Neurosignals 55 (in press).
43. Mackie GO. 2004b. Epithelial conduction: recent findings, old questions, and where do we go from here? Hydrobiologia (in press).
44. Mackie GO, Meech RW. 1985. Separate sodium and calcium spikes in the same axon. Nature 313:791-793.
45. Mackie GO, Meech RW. 1995a. Central circuitry in the jellyfish Aglantha. I. The relay system. J Exp Biol 198:2261-2270.
46. Mackie GO, Meech RW. 1995b. Central circuitry in the jellyfish Aglantha. II. The ring giant and carrier systems. J Exp Biol 198:2271-2278.
47. Mackie GO, Meech RW. 2000. Central circuitry in the jellyfish Aglantha digitale. III. The rootlet and pacemaker systems. J Exp Biol 203(Pt 12):1797-1807.
48. Mackie GO, Singla CL, Stell WK. 1985. Distribution of nerve elements showing FMRFamide-like immunoreactivity in Hydromedusae. Acta Zool Stockh 66:199-210.
49. Mackie GO, Nielsen C, Singla CL. 1989. The tentacle cilia of Aglantha digitale (Hydrozoa: Trachylina) and their control. Acta Zool 70:133-141.
50. Mackie GO, Marx RM, Meech RW. 2003. Central circuitry in the jellyfish Aglantha digitale. IV. Pathways coordinating feeding behaviour. J Exp Biol 206:2487-2505.
51. Matsumoto T, Nakane M, Pollock JS, Kuk JE, Forstermann U. 1993. A correlation between soluble brain nitric oxide synthase and NADPH-diaphorase activity is only seen after exposure of the tissue to fixative. Neurosci Lett 155:61-64.
52. Meech RW, Mackie GO. 1993a. Ionic currents in giant motor axons of the jellyfish, Aglantha digitale. J Neurophysiol 69:884-893.
53. Meech RW, Mackie GO. 1993b. Potassium channel family in giant motor axons of Aglantha digitale. J Neurophysiol 69:894-901.
54. Meech RW, Mackie GO. 1995. Synaptic events underlying the production of calcium and sodium spikes in motor giant axons of Aglantha digitale. J Neurophysiol 74:1662-1669.
55. Moncada S, Martin JF. 1993. Evolution of nitric oxide. Lancet 341:1511.
56. Moroz LL. 2000a. Giant identified NO-releasing neurons and comparative histochemistry of putative nitrergic systems in gastropod molluscs. Microsc Res Tech 49:557-569.
57. Moroz LL. 2000b. On the origin and early evolution of neuronal NO signaling: a comparative analysis. In: Kalsner S, editor. Nitric oxide and free radicals in peripheral neurotransmission. New York: Springer-Verlag. p 1-34.
58. Moroz LL. 2001. Gaseous transmission across time and species. Am Zool 41:304-320.
59. Moroz LL, Gillette R. 1996a. From Polyplacophora to Cephalopoda: comparative analysis of nitric oxide signalling in Mollusca. In: Salanki J, S-Rozsa K, Elekes K, editors. Neurobiology of invertebrates: simple and complex regulatory systems. Budapest: Akademia Kiado. p 169-182.
60. Moroz LL, Gillette R. 1996b. NADPH-diaphorase localization in the CNS and peripheral tissues of the predatory sea-slug Pleurobranchaea californica. J Comp Neurol 367:607-622.
61. Moroz LL, Park JH, Winlow W. 1993. Nitric oxide activates buccal motor patterns in Lymnaea stagnalis. Neuroreport 4:643-646.
62. Moroz LL, Winlow W, Turner RW, Bulloch AG, Lukowiak K, Syed NI. 1994. Nitric oxide synthase-immunoreactive cells in the CNS and periphery of Lymnaea. Neuroreport 5:1277-1280.
63. Moroz LL, Norby SW, Cruz L, Sweedler JV, Gillette R, Clarkson RB. 1998. Non-enzymatic production of nitric oxide (NO) from NO synthase inhibitors. Biochem Biophys Res Commun 253:571-576.
64. Moroz LL, Gillette R, Sweedler JV. 1999. Single-cell analyses of nitrergic neurons in simple nervous systems. J Exp Biol 202(Pt 4):333-341.
65. Moroz LL, Norekian TP, Pirtle TJ, Robertson KJ, Satterlie RA. 2000. Distribution of NADPH-diaphorase reactivity and effects of nitric oxide on feeding and locomotory circuitry in the pteropod mollusc, Clione limacina. J Comp Neurol 427:274-284.
66. Morrall CE, Galloway TS, Trapido-Rosenthal HG, Depledge MH. 2000. Characterisation of nitric oxide synthase activity in the tropical sea anemone Aiptasia pallida. Comp Biochem Physiol B Biochem Mol Biol 125:483-491.
67. 2+/calmodulin-dependent nitric oxide synthase in Apis mellifera and Drosophila melanogaster. Eur J Neurosci 6:1362-1370.
68. Muller U. 1997. The nitric oxide system in insects. Prog Neurobiol 51:363-381.
69. Muller U, 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.
70. Ninnemann H, Maier J. 1996. Indications for the occurrence of nitric oxide synthases in fungi and plants and the involvement in photoconidiation of Neurospora crassa. Photochem Photobiol 64:393-398.
71. Ottaviani E, Paemen LR, Cadet P, Stefano GB. 1993. Evidence for nitric oxide production and utilization as a bacteriocidal agent by invertebrate immunocytes. Eur J Pharmacol 248:319-324.
72. Radomski MW, Martin JF, Moncada S. 1991. Synthesis of nitric oxide by the haemocytes of the americam horseshoe crab (Limulus polyphemus). Philos Trans R Soc Lond 334B:129-133.
73. Regulski M, Tully T. 1995. Molecular and biochemical characterization of dNOS: a Drosophila Ca2+/calmodulin-dependent nitric oxide synthase. Proc Natl Acad Sci U S A 92:9072-9076.
74. Richardson KC, Jarrett L, Finke EH. 1960. Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technology 35:313-323.
75. Salleo A, Giovanni M, Barra P, Calabrese L. 1996. The discharge mechanism of acomitial nematocytes involves the release of nitric oxide. J Exp Biol 199:1261-1267.
76. Salter M, Duffy C, Garthwaite J, Strigbos PJLM. 1996. Ex vivo measurement of brain tissue nitrite and nitrate accurately reflects nitric oxide synthase activity in vivo. J Neurochem 66:1683-1690.
77. Stamler JS, Singel DJ, Loscalzo J. 1992. Biochemistry of nitric oxide and its redox activated forms. Science 258:1898-1902.
78. Tao YP, Misko TP, Howlett AC, Klein C. 1997. Nitric oxide, an endogenous regulator of Dictyostelium discoideum differentiation. Development 124:3587-3595.
79. Weber C, Singla CL, Kerfoot PA. 1982. Microanatomy of the subumbrellar motor innervation in Aglantha digitale (Hydromedusae: Trachylina). Cell Tissue Res 223:305-312.
80. Werner-Felmayer G, Golderer G, Werner ER, Grobner P, Wachter H. 1994. Pteridine biosynthesis and nitric oxide synthase in Physarum polycephalum. Biochem J 304:105-111.
81. Westfall JA. 1973. Ultrastructural evidence for a granule-containing sensory-motor-interneuron in Hydra littoralis. J Ultrastruct Res 42:268-282.