 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
Previous Article | Next Article
The Journal of Neuroscience, May 15, 1999, 19(10):3818-3826
Nitric Oxide Stimulates cGMP Production and Mimics Synaptic Responses in Metacerebral Neurons of Aplysia
Hae-Young Koh and Jon W. Jacklet Department of Biological Sciences, University at Albany, State University of New York, Albany, New York 12222
Nitric oxide (NO) acts as a neurotransmitter and neuromodulator in the nervous systems of many vertebrates and invertebrates. We investigated the mechanism of NO action at an identified synapse between a mechanoafferent neuron, C2, and the serotonergic metacerebral cell (MCC) in the cerebral ganglion of the mollusc Aplysia californica. Stimulation of C2 produces a decreasing conductance, very slow EPSP in the MCC. C2 is thought to use histamine and NO as cotransmitters at this synapse, because both agents mimic the membrane responses. Now we provide evidence that treatment with NO donors stimulates soluble guanylyl cyclase (sGC) in the MCC, and as a result cGMP increases. S-Nitrosocysteine (SNC, an NO donor) and 8-bromo-cGMP (8-Br-cGMP) both induced the membrane depolarization and increase in input resistance that are characteristic of the very slow EPSP. Two inhibitors of sGC, 6-anilino-5,8-quinolinequinone (LY83583) and 1H-[1,2,4]oxadiazolo[4,3-a]quinoxaline-1-one (ODQ), suppressed both the very slow EPSP and the membrane responses to SNC but not the histamine membrane responses. NO-induced cGMP production was determined in the MCC using cGMP immunocytochemistry (cGMP-IR). In the presence of 3-isobutyl-1-methylxanthine (IBMX), 10 µM SNC was sufficient to induce cGMP-IR, and the staining intensity increased as the SNC dose was increased. This cGMP-IR was suppressed by ODQ in a dose-dependent manner and completely blocked by 10 µM ODQ. Histamine did not induce cGMP-IR. The results suggest that NO stimulates sGC-dependent cGMP synthesis in the MCC and that cGMP mediates the membrane responses. The cotransmitter histamine induces essentially the same membrane responses but seems to use a separate and distinct second messenger pathway.
Key words: Aplysia; cGMP; nitric oxide; soluble guanylyl cyclase; immunoreactivity; histamine; cotransmitters; synapses; EPSP
Copyright © 1999 Society for Neuroscience 0270-6474/99/19103818-09$05.00/0
This article has been cited by other articles:
J. Jing, F. S. Vilim, E. C. Cropper, and K. R. Weiss
Neural Analog of Arousal: Persistent Conditional Activation of a Feeding Modulator by Serotonergic Initiators of Locomotion
J. Neurosci., November 19, 2008; 28(47): 12349 - 12361.
[Abstract] [Full Text] [PDF]
I. Antonov, T. Ha, I. Antonova, L. L. Moroz, and R. D. Hawkins
Role of Nitric Oxide in Classical Conditioning of Siphon Withdrawal in Aplysia
J. Neurosci., October 10, 2007; 27(41): 10993 - 11002.
[Abstract] [Full Text] [PDF]
V. A. Straub, J. Grant, M. O'Shea, and P. R. Benjamin
Modulation of Serotonergic Neurotransmission by Nitric Oxide
J Neurophysiol, February 1, 2007; 97(2): 1088 - 1099.
[Abstract] [Full Text] [PDF]
N. G. Hatcher, L. C. Sudlow, L. L. Moroz, and R. Gillette
Nitric Oxide Potentiates cAMP-Gated Cation Current in Feeding Neurons of Pleurobranchaea californica Independent of cAMP and cGMP Signaling Pathways
J Neurophysiol, May 1, 2006; 95(5): 3219 - 3227.
[Abstract] [Full Text] [PDF]
J. W. Jacklet and D. G. Tieman
Nitric Oxide and Histamine Induce Neuronal Excitability by Blocking Background Currents in Neuron MCC of Aplysia
J Neurophysiol, February 1, 2004; 91(2): 656 - 665.
[Abstract] [Full Text] [PDF]
L. F. Gainey Jr and M. J. Greenberg
Nitric oxide mediates seasonal muscle potentiation in clam gills
J. Exp. Biol., October 1, 2003; 206(19): 3507 - 3520.
[Abstract] [Full Text] [PDF]
V. Abudara, A. F. Alvarez, M. H. Chase, and F. R. Morales
Nitric Oxide as an Anterograde Neurotransmitter in the Trigeminal Motor Pool
J Neurophysiol, July 1, 2002; 88(1): 497 - 506.
[Abstract] [Full Text] [PDF]
C. J. H. Elliott and A. J. Susswein
Comparative neuroethology of feeding control in molluscs
J. Exp. Biol., April 1, 2002; 205(7): 877 - 896.
[Abstract] [Full Text] [PDF]
I. Kemenes, G. Kemenes, R. J. Andrew, P. R. Benjamin, and M. O'Shea
Critical Time-Window for NO-cGMP-Dependent Long-Term Memory Formation after One-Trial Appetitive Conditioning
J. Neurosci., February 15, 2002; 22(4): 1414 - 1425.
[Abstract] [Full Text] [PDF]
J. W. Jacklet and H.-Y. Koh
Nitric Oxide as an Orthograde Cotransmitter at Central Synapses of Aplysia: Responses of Isolated Neurons in Culture
Integr. Comp. Biol., April 1, 2001; 41(2): 282 - 291.
[Abstract] [Full Text] [PDF]
N. L. Scholz
NO/cGMP Signaling and the Flexible Organization of Motor Behavior in Crustaceans
Integr. Comp. Biol., April 1, 2001; 41(2): 292 - 303.
[Abstract] [Full Text] [PDF]
A. Gelperin, J. P. Y. Kao, and I. R. C. Cooke
Gaseous Oxides and Olfactory Computation
Integr. Comp. Biol., April 1, 2001; 41(2): 332 - 345.
[Abstract] [Full Text] [PDF]
H Aonuma and P. Newland
Opposing actions of nitric oxide on synaptic inputs of identified interneurones in the central nervous system of the crayfish
J. Exp. Biol., January 4, 2001; 204(7): 1319 - 1332.
[Abstract] [PDF]
S. A. Korneev, J.-H. Park, and M. O'Shea
Neuronal Expression of Neural Nitric Oxide Synthase (nNOS) Protein Is Suppressed by an Antisense RNA Transcribed from an NOS Pseudogene
J. Neurosci., September 15, 1999; 19(18): 7711 - 7720.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|