Localization of putative nitrergic neurons in peripheral chemosensory areas and the central nervous system of Aplysia californica

Journal of Comparative Neurology

Volumn 495, Issue 1, 2006, Pages 10-20

  Moroz, Leonid L ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

Feeding, sensory systems; NADPH diaphorase; Nitric oxide synthase, olfaction

Indexed keywords

NEUROTRANSMITTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

ABDOMINAL GANGLION; ANIMAL ANATOMY; ANIMAL TISSUE; APLYSIA; ARTICLE; BRAIN GANGLION; BUCCAL GANGLION; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; CHEMOSENSITIVITY; CONTROLLED STUDY; ENZYME ACTIVITY; FOOT; FOOT GANGLION; HISTOCHEMISTRY; MOLLUSC; MOUTH; MUSCLE; NERVE CELL; NEURITE; NEUROPIL; NITRERGIC NERVE; NONHUMAN; PLEURAL GANGLION; PRIORITY JOURNAL; RHINOPHORE; SALIVARY GLAND; TENTACLE;

ANIMALS; APLYSIA; BIOLOGICAL MARKERS; BRAIN; CENTRAL NERVOUS SYSTEM; CHEMORECEPTORS; CILIA; EPITHELIAL CELLS; FEEDING BEHAVIOR; GANGLIA, INVERTEBRATE; HISTOCYTOCHEMISTRY; MOUTH; NADPH DEHYDROGENASE; NEURONS, AFFERENT; NEUROPIL; NITRERGIC NEURONS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PERIPHERAL NERVOUS SYSTEM;

EID: 32544442625     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20842     Document Type: Article

References (68)

1. Audesirk TE. 1975. Chemoreception in Aplysia californica. I. Behavioral localization of distance chemoreceptors used in food-finding. Behav Biol 15:45-55.
2. Audesirk TE. 1977. Chemoreception in Aplysia californica. III. Evidence for pheromones influencing reproductive behavior. Behav Biol 20:235-243.
3. Audesirk TE, Audesirk GJ. 1977. Chemoreception in Aplysia californica. II. Electrophysiological evidence for detection of the odor of conspecifics. Comp Biochem Physiol A56:267-270.
4. Bodnarova M, Sadreev RI, Panchin YV, Uvarov P, Jezzini S, Lovell P, Martasek P, Moroz LL. 2003. Biochemical characterization of nitric oxide synthase from the CNS of Aplysia californica and molecular identification of NOS signaling pathways. Society for Neuroscience Meeting, New Orleans [abstract].
5. Bodnarova M, Martasek P, Moroz LL. 2005. Calcium/calmodulin-dependent nitric oxide synthase activity in the CNS of Aplysia californica: biochemical charterization and link to cGMP pathways. J Inorg Biochem 99:922-928.
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. Chase R. 2002. Behavior and its neuronal control in gastropod molluscs. Oxford: Oxford University Press. 314 p.
8. Chase R, Rieling J. 1986. Autoradiographic evidence for receptor cell renewal in the olfactory epithelium of a snail. Brain Res 384:232-239.
9. Chase R, Tolloczko B. 1993. Tracing neural pathways in snail olfaction: from the tip of the tentacles to the brain and beyond. Microsc Res Techniq 24:214-230.
10. Chiel HJ, Weiss KR, Kupfermann I. 1986. An identified histaminergic neuron modulates feeding motor circuitry in Aplysia. J Neurosci 6:2427-2450.
11. Chiel HJ, Weiss KR, Kupfermann I. 1990. Multiple roles of a histaminergic afferent neuron in the feeding behavior of Aplysia. Trends Neurosci 13:223-227.
12. Clifford KT, Gross L, Johnson K, Martin KJ, Shaheen N, Harrington MA. 2003. Slime-trail tracking in the predatory snail, Euglandina rosea. Behav Neurosci 117:1086-1095.
13. Cooke IRC, Edwards SL, Anderson CR. 1994. The distribution of NADPH-diaphorase activity and immunore-activity to nitric oxide synthase in the nervous system of the pulmonate mollusc Helix aspersa. Cell Tissue Res 277:565-572.
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. Elphick M, Rayne R, Riveros-Moreno W, Moncada S, Shea M. 1995a. Nitric oxide synthesis in locust olfactory interneurones. J Exp Biol 198:821-829.
16. Elphick MR, Kemenes G, Staras K, O'Shea M. 1995b. Behavioral role for nitric oxide in chemosensory activation of feeding in a mollusc. J Neurosci 15:7653-7664.
17. Emery DG. 1992. Fine structure of olfactory epithelia of gastropod molluscs. Microsc Res Techniq 22:307-324.
18. Emery DG, Audesirk TE. 1978. Sensory cells in Aplysia. J Neurobiol 9:173-179.
19. Fossier P, Blanchard B, Ducrocq C, Leprince C, Taue L, Baux G. 1999. Nitric oxide transforms serotonin into an inactive form and this affects neuromodulation. Neuroscience 93:597-603.
20. Frings H, Frings C. 1965. Chemosensory bases of food-finding and feeding in Aplysia juliana (Mollusca, Opistobranchia). Biol Bull 128:211-217.
21. Fujie S, Aonuma H, Ito I, Gelperin A, Ito E. 2002. The nitric oxide/cyclic GMP pathway in the olfactory processing system of the terrestrial slug Limax marginatus. Zool Sci 19:15-26.
22. Fukuto JM, Wink DA. 1999. Nitric oxide (NO): formation and biological roles in mammalian systems. Metal Ions Biol Syst 36:547-595.
23. Gelperin A. 1994. Nitric oxide mediates network oscillations of olfactory interneurons in a terrestrial mollusc. Nature 369:61-63.
24. Gelperin A, Kleinfeld D, Denk W, Cooke IR. 1996. Oscillations and gaseous oxides in invertebrate olfaction. J Neurobiol 30:110-122.
25. Grisham MB, Jourd'Heuil D, Wink DA. 1999. Nitric oxide. I. Physiological chemistry of nitric oxide and its metabolites:implications in inflammation. Am J Physiol 276:G315-G321.
26. Hamilton PV, Russell BJ. 1982. Field experiments on the sense organs and directional cues involved in offshore oriented swimming by Aplysia brasiliana (Mollusca, Gastropoda). J Exp Mar Biol Ecol 56:123-143.
27. Hope BT, Vincent SR. 1989. Histochemical localization of neuronal NADPH-diaphorase. J Histochem Cytochem 37:653-661.
28. 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.
29. 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.
30. Jacklet JW. 1995. Nitric oxide is used as an orthograde cotransmitter at identified histaminergic synapses. J Neurophysiol 74:891-895.
31. Jacklet JW, Gruhn M. 1994. Co-localization of NADPH-diaphorase and myomodulin in synaptic glomeruli of Aplysia. Neuroreport 5:1841-1844.
32. Jacklet JW, Tieman DG. 2004. Nitric oxide and histamine induce neuronal excitability by blocking background currents in neuron MCC of Aplysia. J Neurophysiol 91:656-665.
33. Jahan-Parwar B. 1972. Behavioral and electrophysiological studies on chemoreception in Aplysia. Am Zool 12:525-537.
34. Kandel ER. 1976. Cellular basis of behavior. San Francisco: W.H. Freeman and Company. 727 p.
35. Kandel ER. 2001. The molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030-1038.
36. Katzoff A, Ben-Gedalya T, Susswein AJ. 2002. Nitric oxide is necessary for multiple memory processes after learning that a food is inedible in Aplysia. J Neurosci 22:9581-9594.
37. Koh HY, Jacklet JW. 1999. Nitric oxide stimulates cGMP production and mimics synaptic responses in metacerebral neurons of Aplysia. J Neurosci 19:3818-3826.
38. Koh HY, Jacklet JW. 2001. Nitric oxide induces cGMP immunoreactivity and modulates membrane conductance in identified central neurons of Aplysia. Eur J Neurosci 13:553-560.
39. Lancaster JR. 1994. Simulation of the diffusion and reaction of endogenously produced nitric oxide. Proc Natl Acad Sci U S A 91:8137-8141.
40. Leyon H. 1947. Anatomy of the cerebral nerves in Gastropoda. Zool Bidrag Uppsala 25:394-401.
41. Matsumoto T, Nakane M, Pollock JS, 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.
42. Meulemans A, Mothet JP, Schirar A, Fossier P, Taue L, Baux G. 1995. A nitric oxide synthase activity is involved in the modulation of acetylcholine release in Aplysia ganglion neurons: a histological, voltammetric and electrophysiological study. Neuroscience 69:985-995.
43. Moroz LL. 2000a. Giant identified NO-releasing neurons and comparative histochemistry of putative nitrergic systems in gastropod molluscs. Microsc Res Techniq 49:557-569.
44. 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.
45. Moroz LL. 2001. Gaseous transmission across time and species. Am Zool 41:304-320.
46. Moroz LL, Gillette R. 1996. NADPH-diaphorase localization in the CNS and peripheral tissues of the predatory sea-slug Pleurobranchaea californica. J Comp Neurol 367:607-622.
47. Moroz LL, Park JH, Winlow W. 1993a. Nitric oxide activates buccal motor patterns in Lymnaea stagnalis. Neuroreport 4:643-646.
48. Moroz LL, Roger I, Syed NIAGM, Bulloch AGM, Lukowiak K. 1993b. Abundance of putative NO-synthesizing cells in the oesophagus of gastropod molluscs. J Physiol 473.
49. Moroz LL, Bulloch AGM, Lukowiak K, Syed N. 1994a. Putative NO-synthsizing neurons of Lymnaea in vivo and in vitro. Neth J Zool 44:535-549.
50. Moroz LL, Winlow W, Turner KW, Bulloch AG, Lukowiak K, Syed NI. 1994b. Nitric oxide synthase-immunoreactive cells in the CNS and periphery of Lymnaea. Neuroreport 5:1277-1280.
51. Moroz LL, Chen D, Gillette MU, Gillette R. 1996. Nitric oxide synthase activity in the molluscan CNS. J Neurochem 66:873-876.
52. Moroz LL, Gillette R, Sweedler JV. 1999. Single-cell analyses of nitrergic neurons in simple nervous systems. J Exp Biol 202:333-341.
53. 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 molluse, Clione limacina. J Comp Neurol 427:274-284.
54. Moroz LL, Dahlgren RL, Boudko D, Sweedler JV, Lovell P. 2005. Direct single cell determination of nitric oxide synthase related metabolites in identified nitrergic neurons. J Inorg Biochem 99:929-239.
55. Mothet JP, Fossier P, Schirar A, Tauc L, Baux G. 1996a. Opposite effects of nitric oxide on identified inhibitory and excitatory cholinergic synapses of Aplysia californica. Physiol Res 45:177-183.
56. 2+ influx and protein kinase G. J Physiol 493:769-784.
57. Mothet JP, Fossier P, Tauc L, Baux G. 1996c. Opposite actions of nitric oxide on cholinergic synapses: which pathways? Proc Natl Acad Sci U S A 93:8721-8726.
58. Newcomb JM, Watson WH 3rd. 2001. Identifiable nitrergic neurons in the central nervous system of the nudibranch Melibe leonina localized with NADPH-diaphorase histochemistry and nitric oxide synthase immunoreactivity. J Comp Neurol 437:70-78.
59. Preston RJ, Lee RM. 1973. Feeding behavior in Aplysia californica: role of chemical and tactile stimuli. J Comp Physiol Psychol 82:368-381.
60. + current in identified Aplysia neurons. J Neurosci Res 44:21-26.
61. + conductance in identified neurons of Aplysia. Brain Res 670:248-256.
62. + current in B-cluster neurons of Aplysia by nitric oxide donor. Brain Res 740:124-130.
63. + current via guanylate cyclase in Aplysia neurons. J Neurosci Res 50:450-456.
64. Stamler JS, Singel DJ, Loscalzo J. 1992. Biochemistry of nitric oxide and its redox activated forms. Science 258:1898-1902.
65. Walters ET, Byrne JH, Carew TJ, Kandel ER. 1983. Mechanoafferent neurons innervating tail of Aplysia. I. Response properties and synaptic connections. J Neurophysiol 50:1522-1542.
66. Walters ET, Bodnarova M, Billy AJ, Dulin MF, Diaz-Rios M, Miller MW, Moroz LL. 2004. Somatotopic organization and functional properties of mechanosensory neurons expressing sensorin-A mRNA in Aplysia californica. J Comp Neurol 471:219-240.
67. Wink DA, Mitchell JB. 1998. Chemical biology of nitric oxide: Insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radic Biol Med 25:434-456.
68. Wink DA, Miranda KM, Espey MG, Pluta RM, Hewett SJ, Colton C, Vitek M, Feelisch M, Grisham MB. 2001. Mechanisms of the antioxidant effects of nitric oxide. Antioxid Redox Signal 3:203-213.