Nitric oxide-containing neurons in the nervous ganglia of Helix aspersa during rest and activity: Immunocytochemical and enzyme histochemical detection

Journal of Comparative Neurology

Volumn 409, Issue 2, 1999, Pages 274-284

  Pisu, M B ^a   Conforti, E ^a   Fenoglio, C ^a   Necchi, D ^a   Scherini, E ^a   Bernocchi, Graziella ^a,b  

^a UNIVERSITY OF PAVIA   (Italy)

^b Dipartimento di Biologia Animale   (Italy)

Author keywords

Cerebral and buccal ganglia; Inactive and active snails; Nicotinamide adenine dinucleotide phosphate diaphorase activity; Nitric oxide synthase immunoreactivity

Indexed keywords

DIHYDROLIPOAMIDE DEHYDROGENASE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN GANGLION; ENZYME ACTIVITY; ENZYME HISTOCHEMISTRY; HELIX ASPERSA; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; NERVE CELL; NERVE CONDUCTION; NERVOUS SYSTEM; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTIBODY SPECIFICITY; BEHAVIOR, ANIMAL; GANGLIA, INVERTEBRATE; HELIX (SNAILS); IMMUNOHISTOCHEMISTRY; MOTOR ACTIVITY; NADPH DEHYDROGENASE; NERVOUS SYSTEM; NEURONS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; REST;

EID: 0033612532     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19990628)409:2<274::AID-CNE8>3.0.CO;2-E     Document Type: Article

References (101)

1. Aimi Y, Fujimura M, Vincent SR, Kimura H. 1991. Localization of NADPH diaphorase containing neurons in sensory ganglia of the rat. J Comp Neurol 306:382-392.
2. Arévalo R, Alonso JR, Briñón JB, Porteros A, Aijón J. 1993. NADPH-diaphorase histochemical technique in the teleost brain. Zool J Anat 123:403-409.
3. Arévalo R, Alonso JR, García-Ojeda E, Briñón JB, Crespo C, Aijón J. 1995. NADPH-diaphorase in the central nervous system of the tench (Tinca tinea L. 1758). J Comp Neurol 352:398-420.
4. Balaban PM. 1983. Postsynaptic mechanisms of withdrawal reflex sensitization in the snail. J Neurobiol 14:365-375.
5. Balaban P. 1993. Behavioral neurobiology of learning in terrestrial snails. Progr Neurobiol 41:1-19.
6. Balaban P, Chase R. 1990. Stimulation of mesocerebrum in Helix aspersa inhibits the neuronal network underlying avoidance behavior. J Comp Physiol A 166:421-427.
7. Bascal ZA, Montgomery A, Holden-Dye L, Williams RG, Thorndyke MC, Walker RJ. 1996. NADPH diaphorase activity in peptidergic neurons of the parasitic nematode, Ascaris suum. Parasitology 112:125-134.
8. Beesley JE. 1995. Histochemical methods for detecting nitric oxide synthase. Histochem J 27:757-769.
9. Benjamin PR, Rose RM, Slade CT, Lacy MG. 1979. Morphology of identified neurons in the buccal ganglia of Lymnaea stagnalis. J Exp Biol 80:119-135.
10. Bernocchi G, Fenoglio C, Pisu MB, Conforti E, Scherini E, Necchi D. 1997. About the role of nitric oxide (NO): cytochemical detection of NO synthase in snail ganglia during resting and active periods. Eur J Histochem 41(Suppl):22.
11. Bernocchi G, Vignola C, Scherini E, Pisu MB. 1998. Bioactive peptides and serotonin immunocytochemistry in the cerebral ganglia of hibernating Helix aspersa. J Exp Zool 280:354-367.
12. Bicker G, Hähnlein I. 1995. NADPH-diaphorase expression in neurons and glial cells of the locust brain. Neuroreport 6:325-328.
13. Blottner D, Baumgarten HG. 1995. L-NNA inhibits the histochemical NADPH-d reaction in rat spinal cord neurons. Histochemistry 103:379-385.
14. Blottner D, Grozdanovic Z, Gossrau R. 1995. Histochemistry of nitric oxide synthase in the nervous system. Histochem J 27:785-811.
15. Bredt DS, Snyder SH. 1992. Nitric oxide, a novel neuronal messenger. Neuron 8:3-11.
16. Bredt DS, Snyder SH. 1994. Nitric oxide: a physiologic messenger molecule. Annu Rev Biochem 63:175-195.
17. Bredt DS, Glatt CE, Hwang PM, Fotuhi M, Dawson TM, Snyder SH. 1991. Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase. Neuron 7:615-624.
18. Breer H, Shepherd GM. 1993. Implication of the NO/cGMP system for olfaction. TINS 16:5-9.
19. Brüning G. 1993. Localization of NADPH-diaphorase in the brain of the chicken. J Comp Neurol 334:192-208.
20. Brüning G, Funk U, Mayer B. 1994a. Immunocytochemical localization of nitric oxide synthase in the brain of the chicken. Neuroreport 5:2425-2428.
21. Brüning G, Wiese S, Mayer B. 1994b. Nitric oxide synthase in the central nervous system of the turtle, Pseudemys scripta elegans. J Comp Neurol 348:183-206.
22. Chapman PF, Atkins CM, Allen MT, Haley JE, Steinmetz JE. 1992. Inhibition of nitric oxide synthase impairs two different forms of learning. Neuroreport 3:567-570.
23. Chichery R, Chichery M-P. 1994. NADPH-diaphorase in a cephalopod brain (Sepia): presence in an analogue of the cerebellum. Neuroreport 5:1273-1276.
24. Colton CA. 1995. Induction of nitric oxide in cultured microglia: evidence for a cytoprotective role. Adv Neuroimmunol 5:491-503.
25. 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.
26. Cottrell GA, Osborne NN. 1970. Subcellular localization of serotonin in an identified serotonin-containing neuron. Nature 225:470-472.
27. Cruz LA, 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.
28. Dawson TM, Bredt DS, Fotuhi M, Hwang PM, Snyder SH. 1991. Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissue. Proc Natl Acad Sci USA 88:7797-7801.
29. Dun NJ, Dun SL, Wu SY, Förstermann U, Schmidt HHHW, Tseng LF. 1993. Nitric oxide synthase immunoreactivity in the rat, mouse, cat and squirrel monkey spinal cord. Neuroscience 54:845-857.
30. Elekes K. 1991. Serotonin-immunoreactive varicosities in the cell body and neural sheath of the snail, Helix pomatia, ganglia: an electron microscopic immunocytochemical study. Neuroscience 42:583-591.
31. Elofsson R, Carlberg M, Moroz L, Nezlin L, Sakharov D. 1993. Is nitric oxide (NO) produced by invertebrate neurons? Neuroreport 4:279-282.
32. Elphick MR, Green IC, O'Shea M. 1993. Nitric oxide synthesis and action in an invertebrate brain. Brain Res 619:344-346.
33. Elphick MR, Kemenes G, Staras K, O'Shea M. 1995. Behavioral role for nitric oxide in chemosensory activation of feeding in a mollusc. J Neurosci 15:7653-7664.
34. Elphick MR, Williams L, 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.
35. Fenoglio C, Scherini E, Necchi D, Soldani C, Bernocchi G. 1997. Perineuronal glial system in the cerebral ganglion of active and hibernating Helix aspersa. Tissue Cell 29:561-572.
36. Gelperin A. 1994a. Nitric oxide mediates networks oscillations of olfactory interneurons in a terrestrial mollusc. Nature 369:61-63.
37. Gelperin A. 1994b. Nitric oxide, odour processing and plasticity. Neth J Zool 44:159-169.
38. Gelperin A, Kleinfeld D, Denk W, Cooke IRC. 1996. Oscillations and gaseous oxides in invertebrate olfaction. J Neurobiol 30:110-122.
39. Gerlach M, Riederer P, Youdim MBH. 1995. Neuroprotective therapeutic strategies. Comparison of experimental and clinical results. Biochem Pharmacol 50:1-16.
40. Gustafsson MKS, Lindholm AM, Terenina NB, Reuter M. 1996. NO nerves in a tapeworm. NADPH-diaphorase histochemistry in adult Hymenolepis diminuta. Parasitology 113:559-565.
41. Hernádi L. 1992. Relationships between the distribution of serotoninergic cell bodies and the running of vascular elements in the central nervous system of the snail, Helix pomatia. Comp Biochem Phys 103:85-92.
42. Holmqvist BI, Östholm T, Alm P, Ekström P. 1994. Nitric oxide synthase in the brain of a teleost. Neurosci Lett 171:205-208.
43. Hölscher C, Rose SP. 1992. An inhibitor of nitric oxide synthesis prevents memory formation in the chick. Neurosci Lett 145:165-167.
44. Hope BT, Micheal GJ, Knigge KM, Vincent SR. 1991. Neuronal NADPH diaphorase is a nitric oxide synthase. Proc Natl Acad Sci USA 88:2811-2814.
45. Huang S, Kerschbaum HH, Hermann A. 1997. Biochemical characterization of histochemical localization of nitric oxide synthase (NOS) in the central nervous system of the snail, Helix pomatia. J Neurochem 69:2516-2528.
46. Huang S, Kerschbaum HH, Hermann A. 1998. Nitric oxide-mediated cGMP synthesis in Helix neural ganglia. Brain Res 780:329-336.
47. Hunter WR. 1964. Ecology in nonmarine forms. In: Wilbur KM, Yonge CM, editors. Physiology of Mollusca. New York: Academic Press. p83-126.
48. Johansson KUI, Carlberg M. 1994. NADPH-diaphorase histochemistry and nitric oxide synthase activity in deutocerebrum of the crayfish, Pacifastacus leniusculus (Crustacea, Decapoda). Brain Res 649:36-42.
49. Johansson KUI, Carlberg M. 1995. NO-synthase: what can research on invertebrates add to what is already known? Adv Neuroimmunol 5:431-142.
50. Kaufmann W, Kerschbaum HH, Hauser-Kronberger C, Hacker GW, Hermann A. 1995. Distribution of seasonal variation of vasoactive intestinal (VIP)-like peptides in the nervous system of Helix pomatia. Brain Res 695:125-136.
51. Klatt P, Schmidt K, Brunner F, Mayer B. 1994. Inhibitors of brain nitric oxide synthase. Binding kinetics, metabolism and enzyme characterization. J Biol Chem 269:1674-1680.
52. Kurenny DE, Moroz LL, Barnes S. 1993. Subcellular localization of nitric oxide synthase and modulation of calcium channels by nitric oxide in rod photoreceptors. Soc Neurosci Abstr 19:463.18.
53. Leake LD, Davis MP, Chen D, Moroz LL. 1995. An unique model for the analysis of neuronal nitric oxide signaling: the leech CNS. Acta Biol Hungary 46:135-143.
54. Lei SZ, Pan ZH, Aggarwal SK, Chen HS, Hartman J, Sucher NJ, Lipton SA. 1992. Effect of nitric oxide production on the redox modulatory site of the NMDA receptor-channel complex. Neuron 8:1087-1099.
55. Li G, Chase R. 1995. Correlation of axon projections and peptide immunoreactivity in mesocerebral neurons of the snail Helix aspersa. J Comp Neurol 353:9-17.
56. Li ZS, Furness JG, Young HV, Campbell G. 1992. Nitric oxide synthase immunoreactivity and NADPH diaphorase enzyme activity in neurons of the gastrointestinal tract of the toad, Bufo marinus. Arch Histol Cytol 55:333-350.
57. Lin M-F, Leise EM. 1996. NADPH-diaphorase activity changes during gangliogenesis and metamorphosis in the gastropod mollusc Ilyanassa obsoleta. J Comp Neurol 374:194-203.
58. Lipton SA, Choi YB, Pan ZH, Lei SZ, Chen HS, Sucher NJ, Loscalzo J, Singel DJ, Stamler JS. 1993. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 364:626-632.
59. Lipton SA, Singel DJ, Stamler JS. 1994. Nitric oxide in the central nervous system. Progr Brain Res 103:359-364.
60. Loesch A, Burnstock G. 1996. Ultrastructural localization of nitric oxide synthase and endothelin in rat pulmonary artery and vein during postnatal development and ageing. Cell Tissue Res 283:355-365.
61. Machin J. 1975. Water relationships. In: Fretter V, Peake J, editors. Pulmonates: functional anatomy and physiology, vol 1. London: Academic Press. p105-163.
62. Mann HB, Whitney DR. 1947. On a test of whether one of two random variables is stochastically larger than the other. Ann Math Stat 18:50-60.
63. Martinez A. 1995. Nitric oxide synthase in invertebrates. Histochem J 27:770-776.
64. Matsumoto T, Akane M, Polloch GS, Kuk JE, Forstermann U. 1993. A correlation between soluble nitric oxide synthase and NADPH diaphorase activity is only seen after exposure of the tissue to fixative. Neurosci Lett 155:61-64.
65. Mattson MP. 1992. Calcium as sculptor and destroyer of neuronal circuitry. Exp Gerontol 27:29-49.
66. Meyer W. 1994. NADPH diaphorase (nitric oxide synthase) in the central nervous system of spiders (Arachnia: Araneida). Neurosci Lett 165:105-108.
67. Moncada S. 1992. The L-arginine/nitric oxide pathway. Acta Physiol Scand 145:201-227.
68. 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.
69. Moroz LL, Park J-H, Winlow W. 1993. Nitric oxide activates buccal motor patterns in Lymnaea stagnalis. Neuroreport 4:643-646.
70. Moroz LL, Winlow W, Turner RW, Bulloch AGM, Lukowiak K, Syed N. 1994. Nitric oxide synthase immunoreactive cells in the CNS and periphery of Lymnaea. Neuroreport 5:1277-1280.
71. Moroz LL, Chen D, Gillette MU, Gillette R. 1996. Nitric oxide synthase in the molluscan CNS. J Neurochem 66:873-876.
72. Müller U. 1997. The nitric oxide system in insects. Progr Neurobiol 51:363-381.
73. Muñoz M, Muñoz A, Marín O, Alonso JR, Arévalo R, Porteros A, González A. 1996. Typographical distribution of NADPH-diaphorase activity in the central nervous system of the frog, Rana perezi. J Comp Neurol 367:54-69.
74. Neuhuber WL, Wörl J, Berthoud H-R, Conte B. 1994. NADPH-diaphorase positive nerve fibers associated with motor endplates in the rat esophagus: new evidence for co-innervation of striated muscle by enteric neurons. Cell Tissue Res 276:23-30.
75. Panzica GC, Arevalo R, Sánchez R, Alonso JR, Aste N, Viglietta-Panzica C, Aijón J, Vázquez R. 1994. Topographical distribution of reduced nicotinamide adenine dinucleotide phosphate-diaphorase in the brain of the Japanese quail. J Comp Neurol 342:97-114.
76. Pentreath VW, Cottrell GA. 1970. The blood supply to the central nervous system of Helix pomatia. Z Zellforsch 111:160-178.
77. Peunova N, Enikolopov G. 1995. Nitric oxide triggers a switch to growth arrest during differentiation of neuronal cells. Nature 375:68-73.
78. Rodrigo J, Springall DR, Uttenthal O, Bentura ML, Abadia-Molina F, Riveros-Moreno V, Martinez-Murillo R, Polak JM, Moncada S. 1994. Localization of nitric oxide synthase in the adult rat brain. Phil Trans R Soc London B 345:175-221.
79. Sánchez-Alvarez M, León-Olea M, Talavera E, Pellicer F, Sánchez-Islas E, Martínez-Lorenzana G. 1994. Distribution of NADPH-diaphorase in the perioesophageal ganglia of the snail, Helix aspersa. Neurosci Lett 169:51-55.
80. Saxon DW, Beitz AJ. 1996. Induction of NADPH diaphorase/nitric oxide synthase in the brainstem trigeminal system resulting from cerebellar lesions. J Comp Neurol 371:41-71.
81. Schmidt HHHW, Walter U. 1994. NO at work. Cell 78:919-925.
82. Schmidt HHHW, Gagne GD, Nakane M, Pollock JS, Miller MF, Murad F. 1992. Mapping of neural nitric oxide synthase in the rat suggests frequent co-localization with NADPH diaphorase but not with soluble guanylyl cyclase, and novel paraneural functions for nitrinergic signal transduction. J Histochem Cytochem 40:1439-1456.
83. Schottler F, Collins JL, Fergus A, Okonkwo D, Kassell NF, Lee KS. 1996. Structural interactions between NOS-positive neurons and blood vessels in the hippocampus. Neuroreport 7:966-968.
84. Schulze H, Speckmann EJ, Kuhlmann D, Caspers H. 1975. Topography and bioelectrical properties of identifiable neurones in the buccal ganglion of Helix pomatia. Neurosci Lett 1:277-281.
85. Schuman EM, Madison DV. 1994. Nitric oxide and synaptic function. Annu Rev Neurosci 17:153-183.
86. Scott JW, McDonald JK, Pemberton JL. 1987. Short axon cells of the rat olfactory bulb display NADPH diaphorase activity, neuropeptide Y-like immunoreactivity, and somatostatin-like immunoreactivity. J Comp Neurol 260:378-391.
87. Seidel C, Bicker G. 1997. Colocalization of NADPH-diaphorase and GABA-immunoreactivity in the olfactory and visual system of the locust. Brain Res 769:273-280.
88. Sosunov AA, Hassall CJS, Loesch A, Turmaine M, Burnstock G. 1995. Ultrastructural investigation of nitric oxide synthase-immunoreactive nerves associated with coronary blood vessels of rat and guinea-pig. Cell Tissue Res 280:575-582.
89. Spessert R, Wohlgemuth C, Reuss S, Layes EJ. 1994. NADPH diaphorase activity of nitric oxide synthase in the olfactory bulb: co-factor specificity and characterization regarding the interrelation to NO formation. J Histochem Cytochem 42:569-575.
90. Talavera E, Martínez-Lorenzana G, León-Olea M, Sánchez-Alvarez M, Sánchez-Islas E, Pellicer F. 1995. Histochemical distribution of NADPH-diaphorase in the cerebral ganglion of the crayfish, Cambarellus montezumae. Neurosci Lett 187:177-180.
91. Teyke T. 1996. Nitric oxide, but not serotonin, is involved in acquisition of food-attraction conditioning in the snail Helix pomatia. Neurosci Lett 206:29-32.
92. Valtschanoff JG, Weinberg RJ, Kharazia VN, Schmidt HH, Nakame M, Rustioni A. 1993. Neurons in rat cerebral cortex that synthesize nitric oxide: NADPH diaphorase histochemistry, and colocalization with GABA. Neurosci Lett 157:157-161.
93. Van Noorden CJF, Butcher RG. 1984. Histochemical localization of NADP-dependent dehydrogenase activity with four different tetrazolium salts. J Histochem Cytochem 32:998-1004.
94. Van Noorden CJF, Frederiks WM. 1992. Enzyme histochemistry: a laboratory manual of current methods: Royal Microscopy Society. Oxford: Oxford University Press.
95. Vignola C, FenogLio C, Scherini E, Bernocchi G. 1995. The cerebral neurons of Helix aspersa during hibernation. Changes in the cytochemical detection of calmodulin, cytoskeletal components and phosphatases. Tissue Cell 27:185-196.
96. Vincent SR. 1994. Nitric oxide: a radical neurotransmitter in the central nervous system. Progr Neurobiol 42:129-160.
97. Vincent SR, Hope BT. 1992. Neurons that say NO. TINS 15:108-113.
98. Vincent SR, Kimura H. 1992. Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46:755-784.
99. Vincent SR, Satoh K, Armstrong DM, Panula P, Vale W, Fibiger HC. 1986. Neuropeptides and NADPH-diaphorase activity in the ascending cholinergic reticular system of the rat. Neuroscience 17:167-182.
100. Winlow W, Park JHJ, Moroz LL. 1993. Are nitric oxide and free radicals of oxygen intercellular messengers in the molluscan CNS? Soc Neurosci Abstr 19:403.5.
101. Wörl J, Wiesand M, Mayer B, Greskötter KR, Neuhuber WL. 1994. Neuronal and endothelial nitric oxide synthase immunoreactivity and NADPH-diaphorase staining in rat and human pancreas: influence of fixation. Histochemistry 102:353-364.