Concepts of neural nitric oxide‐mediated transmission

Abstract

As a chemical transmitter in the mammalian central nervous system, nitric oxide (NO) is still thought a bit of an oddity, yet this role extends back to the beginnings of the evolution of the nervous system, predating many of the more familiar neurotransmitters. During the 20 years since it became known, evidence has accumulated for NO subserving an increasing number of functions in the mammalian central nervous system, as anticipated from the wide distribution of its synthetic and signal transduction machinery within it. This review attempts to probe beneath those functions and consider the cellular and molecular mechanisms through which NO evokes short‐ and long‐term modifications in neural performance. With any transmitter, understanding its receptors is vital for decoding the language of communication. The receptor proteins specialised to detect NO are coupled to cGMP formation and provide an astonishing degree of amplification of even brief, low amplitude NO signals. Emphasis is given to the diverse ways in which NO receptor activation initiates changes in neuronal excitability and synaptic strength by acting at pre‐ and/or postsynaptic locations. Signalling to non‐neuronal cells and an unexpected line of communication between endothelial cells and brain cells are also covered. Viewed from a mechanistic perspective, NO conforms to many of the rules governing more conventional neurotransmission, particularly of the metabotropic type, but stands out as being more economical and versatile, attributes that presumably account for its spectacular evolutionary success.

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    Garthwaite J. Dynamics of cellular NO-cGMP signaling. Front. Biosci. 2005;10:1868-1880.

    Not in our library10.2741/1666

98. 98.

    Garthwaite J. Neuronal nitric oxide synthase and the serotonin transporter get harmonious. Proc. Natl Acad. Sci. USA. 2007;104:7739-7740.

    Not in our library10.1073/pnas.0702508104

99. 99.

    Garthwaite J, Boulton CL. Nitric oxide signaling in the central nervous system. Annu. Rev. Physiol. 1995;57:683-706.

    Not in our library10.1146/annurev.ph.57.030195.003343

100. 100.

     Garthwaite J, Garthwaite G. Cellular origins of cyclic GMP responses to excitatory amino acid receptor agonists in rat cerebellum in vitro. J. Neurochem. 1987;48:29-39.

     Not in our library10.1111/j.1471-4159.1987.tb13123.x

101. 101.

     Garthwaite J, Charles SL, Chess Williams R. Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature. 1988;336:385-388.

     Not in our library10.1038/336385a0

102. 102.

     Garthwaite J, Southam E, Boulton CL, Nielsen EB, Schmidt K, Mayer B. Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one. Mol. Pharmacol. 1995;48:184-188.

     Not in our library

103. 103.

     Garthwaite G, Bartus K, Malcolm D, Goodwin DA, Kollb-Sielecka M, Dooldeniya C, Garthwaite J. Signaling from blood vessels to CNS axons through nitric oxide. J. Neurosci. 2006;26:7730-7740.

     Not in our library10.1523/jneurosci.1528-06.2006

104. 104.

     Geiselhoringer A, Gaisa M, Hofmann F, Schlossmann J. Distribution of IRAG and cGKI-isoforms in murine tissues. FEBS Lett. 2004;575:19-22.

     Not in our library10.1016/j.febslet.2004.08.030

105. 105.

     Gibb BJ, Garthwaite J. Subunits of the nitric oxide receptor, soluble guanylyl cyclase, expressed in rat brain. Eur. J. Neurosci. 2001;13:539-544.

     Not in our library10.1046/j.1460-9568.2001.01421.x

106. 106.

     Gibb BJ, Wykes V, Garthwaite J. Properties of NO-activated guanylyl cyclases expressed in cells. Br. J. Pharmacol. 2003;139:1032-1040.

     Not in our library10.1038/sj.bjp.0705318

107. 107.

     Godfrey EW, Schwarte RC. The role of nitric oxide signaling in the formation of the neuromuscular junction. J. Neurocytol. 2003;32:591-602.

     Not in our library10.1023/b:neur.0000020612.87729.98

108. 108.

     Golombek DA, Agostino PV, Plano SA, Ferreyra GA. Signaling in the mammalian circadian clock: the NO/cGMP pathway. Neurochem. Int. 2004;45:929-936.

     Not in our library10.1016/j.neuint.2004.03.023

109. 109.

     Gonzalez-Forero D, Portillo F, Gomez L, Montero F, Kasparov S, Moreno-Lopez B. Inhibition of resting potassium conductances by long-term activation of the NO/cGMP/protein kinase G pathway: a new mechanism regulating neuronal excitability. J. Neurosci. 2007;27:6302-6312.

     Not in our library10.1523/jneurosci.1019-07.2007

110. 110.

     Grassi S, Pettorossi VE. Role of nitric oxide in long-term potentiation of the rat medial vestibular nuclei. Neuroscience. 2000;101:157-164.

     Not in our library10.1016/s0306-4522(00)00334-1

111. 111.

     Grassi S, Pettorossi VE. Synaptic plasticity in the medial vestibular nuclei: role of glutamate receptors and retrograde messengers in rat brainstem slices. Prog. Neurobiol. 2001;64:527-553.

     Not in our library10.1016/s0301-0082(00)00070-8

112. 112.

     Grassi C, D’Ascenzo M, Azzena GB. Modulation of Ca(v)1 and Ca(v)2.2 channels induced by nitric oxide via cGMP-dependent protein kinase. Neurochem. Int. 2004;45:885-893.

     Not in our library10.1016/j.neuint.2004.03.019

113. 113.

     Graves AR, Lewin KA, Lindgren A. Nitric oxide, cAMP and the biphasic muscarinic modulation of ACh release at the lizard neuromuscular junction. J. Physiol. 2004;559:423-432.

     Not in our library10.1113/jphysiol.2004.064469

114. 114.

     Griffiths C, Garthwaite G, Goodwin DA, Garthwaite J. Dynamics of nitric oxide during simulated ischaemia-reperfusion in rat striatal slices measured using an intrinsic biosensor, soluble guanylyl cyclase. Eur. J. Neurosci. 2002;15:962-968.

     Not in our library10.1046/j.1460-9568.2002.01930.x

115. 115.

     Gyurko R, Leupen S, Huang PL. Deletion of exon 6 of the neuronal nitric oxide synthase gene in mice results in hypogonadism and infertility. Endocrinology. 2002;143:2767-2774.

     Not in our library10.1210/endo.143.7.8921

116. 116.

     Haghikia A, Mergia E, Friebe A, Eysel UT, Koesling D, Mittmann T. Long-term potentiation in the visual cortex requires both nitric oxide receptor guanylyl cyclases. J. Neurosci. 2007;27:818-823.

     Not in our library10.1523/jneurosci.4706-06.2007

117. 117.

     Hall CN, Garthwaite J. Inactivation of nitric oxide by rat cerebellar slices. J. Physiol. 2006;577:549-567.

     Not in our library10.1113/jphysiol.2006.118380

118. 118.

     Han NL, Ye JS, Yu AC, Sheu FS. Differential mechanisms underlying the modulation of delayed-rectifier K+ channel in mouse neocortical neurons by nitric oxide. J. Neurophysiol. 2006;95:2167-2178.

     Not in our library10.1152/jn.01185.2004

119. 119.

     Hardingham N, Fox K. The role of nitric oxide and GluR1 in presynaptic and postsynaptic components of neocortical potentiation. J. Neurosci. 2006;26:7395-7404.

     Not in our library10.1523/jneurosci.0652-06.2006

120. 120.

     Hartell NA. Parallel fiber plasticity. Cerebellum. 2002;1:3-18.

     Not in our library10.1080/147342202753203041

121. 121.

     Hashimotodani Y, Ohno-Shosaku T, Kano M. Endocannabinoids and synaptic function in the CNS. Neuroscientist. 2007;13:127-137.

     Not in our library10.1177/1073858406296716

122. 122.

     Haul S, Godecke A, Schrader J, Haas HL, Luhmann HJ. Impairment of neocortical long-term potentiation in mice deficient of endothelial nitric oxide synthase. J. Neurophysiol. 1999;81:494-497.

     Not in our library10.1152/jn.1999.81.2.494

123. 123.

     Hawkins RD, Son H, Arancio O. Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus. Prog. Brain Res. 1998;118:155-172.

     Not in our library10.1016/s0079-6123(08)63206-9

124. 124.

     Hayashi Y, Nishio M, Naito Y, Yokokura H, Nimura Y, Hidaka H, Watanabe Y. Regulation of neuronal nitric-oxide synthase by calmodulin kinases. J. Biol. Chem. 1999;274:20597-20602.

     Not in our library10.1074/jbc.274.29.20597

125. 125.

     Hentall ID. Excitation of cells in the rostral medial medulla of the rat by the nitric oxide-cyclic guanosine monophosphate messenger system. Neurosci. Lett. 1995;195:155-158.

     Not in our library10.1016/0304-3940(95)11802-4

126. 126.

     Hepp R, Tricoire L, Hu E, Gervasi N, Paupardin-Tritsch D, Lambolez B, Vincent P. Phosphodiesterase type 2 and the homeostasis of cyclic GMP in living thalamic neurons. J. Neurochem. 2007;102:1875-1886.

     Not in our library10.1111/j.1471-4159.2007.04657.x

127. 127.

     Hervieu GJ, Cluderay JE, Gray CW, Green PJ, Ranson JL, Randall AD, Meadows HJ. Distribution and expression of TREK-1, a two-pore-domain potassium channel, in the adult rat CNS. Neuroscience. 2001;103:899-919.

     Not in our library10.1016/s0306-4522(01)00030-6

128. 128.

     Hofmann F, Feil R, Kleppisch T, Schlossmann J. Function of cGMP-dependent protein kinases as revealed by gene deletion. Physiol. Rev. 2006;86:1-23.

     Not in our library10.1152/physrev.00015.2005

129. 129.

     Hogg N. The biochemistry and physiology of S-nitrosothiols. Annu. Rev. Pharmacol. Toxicol. 2002;42:585-600.

     Not in our library10.1146/annurev.pharmtox.42.092501.104328

130. 130.

     Holscher C. Nitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity. Trends Neurosci. 1997;20:298-303.

     Not in our library10.1016/s0166-2236(97)01065-5

131. 131.

     Hopper RA, Garthwaite J. Tonic and phasic nitric oxide signals in hippocampal long-term potentiation. J. Neurosci. 2006;26:11513-11521.

     Not in our library10.1523/jneurosci.2259-06.2006

132. 132.

     Hopper R, Lancaster B, Garthwaite J. On the regulation of NMDA receptors by nitric oxide. Eur. J. Neurosci. 2004;19:1675-1682.

     Not in our library10.1111/j.1460-9568.2004.03306.x

133. 133.

     Huang PL, Dawson TM, Bredt DS, Snyder SH, Fishman MC. Targeted disruption of the neuronal nitric oxide synthase gene. Cell. 1993;75:1273-1286.

     Not in our library10.1016/0092-8674(93)90615-w

134. 134.

     Huang CC, Chan SH, Hsu KS. cGMP/protein kinase G-dependent potentiation of glutamatergic transmission induced by nitric oxide in immature rat rostral ventrolateral medulla neurons in vitro. Mol. Pharmacol. 2003;64:521-532.

     Not in our library10.1124/mol.64.2.521

135. 135.

     Hwang SJ, O’Kane N, Singer C, Ward SM, Sanders KM, Koh SD. Block of inhibitory junction potentials and TREK-1 channels in murine colon by Ca2+ store-active drugs. J. Physiol. 2008;586:1169-1184.

     Not in our library10.1113/jphysiol.2007.148718

136. 136.

     Iadecola C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat. Rev. Neurosci. 2004;5:347-360.

     Not in our library10.1038/nrn1387

137. 137.

     Ignarro LJ. Nitric oxide: a unique endogenous signaling molecule in vascular biology. Biosci. Rep. 1999;19:51-71.

     Not in our library10.1023/a:1020150124721

138. 138.

     Ignarro LJ, Wood KS, Wolin MS. Activation of purified soluble guanylate cyclase by protoporphyrin IX. Proc. Natl Acad. Sci. USA. 1982;79:2870-2873.

     Not in our library10.1073/pnas.79.9.2870

139. 139.

     Ignarro LJ, Buga GM, Wood KS, Byrns RE, Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl Acad. Sci. USA. 1987;84:9265-9269.

     Not in our library10.1073/pnas.84.24.9265

140. 140.

     Ishikawa T, Nakamura Y, Saitoh N, Li WB, Iwasaki S, Takahashi T. Distinct roles of Kv1 and Kv3 potassium channels at the calyx of Held presynaptic terminal. J. Neurosci. 2003;23:10445-10453.

     Not in our library10.1523/jneurosci.23-32-10445.2003

141. 141.

     Ito M. Cerebellar long-term depression: characterization, signal transduction, and functional roles. Physiol. Rev. 2001;81:1143-1195.

     Not in our library10.1152/physrev.2001.81.3.1143

142. 142.

     Iyer LM, Anantharaman V, Aravind L. Ancient conserved domains shared by animal soluble guanylyl cyclases and bacterial signaling proteins. BMC Genomics. 2003;4:5.

     Not in our library10.1186/1471-2164-4-5

143. 143.

     Jacklet JW, Tieman DG. Nitric oxide and histamine induce neuronal excitability by blocking background currents in neuron MCC of Aplysia. J. Neurophysiol. 2004;91:656-665.

     Not in our library10.1152/jn.00409.2003

144. 144.

     Jacoby S, Sims RE, Hartell NA. Nitric oxide is required for the induction and heterosynaptic spread of long-term potentiation in rat cerebellar slices. J. Physiol. 2001;535:825-839.

     Not in our library10.1111/j.1469-7793.2001.t01-1-00825.x

145. 145.

     Jaffrey SR, Benfenati F, Snowman AM, Czernik AJ, Snyder SH. Neuronal nitric-oxide synthase localization mediated by a ternary complex with synapsin and CAPON. Proc. Natl Acad. Sci. USA. 2002;99:3199-3204.

     Not in our library10.1073/pnas.261705799

146. 146.

     Jones JD, Carney ST, Vrana KE, Norford DC, Howlett AC. Cannabinoid receptor-mediated translocation of NO-sensitive guanylyl cyclase and production of cyclic GMP in neuronal cells. Neuropharmacology. 2008;54:23-30.

     Not in our library10.1016/j.neuropharm.2007.06.027

147. 147.

     Kaehler ST, Singewald N, Sinner C, Philippu A. Nitric oxide modulates the release of serotonin in the rat hypothalamus. Brain Res. 1999;835:346-349.

     Not in our library10.1016/s0006-8993(99)01599-1

148. 148.

     Kang Y, Dempo Y, Ohashi A, Saito M, Toyoda H, Sato H, Koshino H, Maeda Y, Hirai T. Nitric oxide activates leak K+ currents in the presumed cholinergic neuron of basal forebrain. J. Neurophysiol. 2007;98:3397-3410.

     Not in our library10.1152/jn.00536.2007

149. 149.

     Kano T, Shimizu-Sasamata M, Huang PL, Moskowitz MA, Lo EH. Effects of nitric oxide synthase gene knockout on neurotransmitter release in vivo. Neuroscience. 1998;86:695-699.

     Not in our library10.1016/s0306-4522(98)00179-1

150. 150.

     Kantor DB, Lanzrein M, Stary SJ, Sandoval GM, Smith WB, Sullivan BM, Davidson N, Schuman EM. A role for endothelial NO synthase in LTP revealed by adenovirus-mediated inhibition and rescue. Science. 1996;274:1744-1748.

     Not in our library10.1126/science.274.5293.1744

151. 151.

     Kara P, Friedlander MJ. Arginine analogs modify signal detection by neurons in the visual cortex. J. Neurosci. 1999;19:5528-5548.

     Not in our library10.1523/jneurosci.19-13-05528.1999

152. 152.

     Kaupp UB, Seifert R. Cyclic nucleotide-gated ion channels. Physiol. Rev. 2002;82:769-824.

     Not in our library10.1152/physrev.00008.2002

153. 153.

     Kawa F, Sterling P. cGMP modulates spike responses of retinal ganglion cells via a cGMP-gated current. Vis. Neurosci. 2002;19:373-380.

     Not in our library

154. 154.

     Kennedy MB. Signal-processing machines at the postsynaptic density. Science. 2000;290:750-754.

     Not in our library10.1126/science.290.5492.750

155. 155.

     Keynes RG, Garthwaite J. Nitric oxide and its role in ischaemic brain injury. Curr. Mol. Med. 2004;4:179-191.

     Not in our library10.2174/1566524043479176

156. 156.

     Keynes RG, Griffiths C, Garthwaite J. Superoxide-dependent consumption of nitric oxide in biological media may confound in vitro experiments. Biochem. J. 2003;369:399-406.

     Not in our library10.1042/bj20020933

157. 157.

     Keynes RG, Duport S, Garthwaite J. Hippocampal neurons in organotypic slice culture are highly resistant to damage by endogenous and exogenous nitric oxide. Eur. J. Neurosci. 2004;19:1163-1173.

     Not in our library10.1111/j.1460-9568.2004.03217.x

158. 158.

     Keynes RG, Griffiths CH, Hall C, Garthwaite J. Nitric oxide consumption through lipid peroxidation in brain cell suspensions and homogenates. Biochem. J. 2005;387:685-694.

     Not in our library10.1042/bj20041431

159. 159.

     Kimura S, Uchiyama S, Takahashi HE, Shibuki K. cAMP-dependent long-term potentiation of nitric oxide release from cerebellar parallel fibers in rats. J. Neurosci. 1998;18:8551-8558.

     Not in our library10.1523/jneurosci.18-21-08551.1998

160. 160.

     Klyachko VA, Ahern GP, Jackson MB. cGMP-mediated facilitation in nerve terminals by enhancement of the spike afterhyperpolarization. Neuron. 2001;31:1015-1025.

     Not in our library10.1016/s0896-6273(01)00449-4

161. 161.

     Ko FN, Wu CC, Kuo SC, Lee FY, Teng CM. YC-1, a novel activator of platelet guanylate cyclase. Blood. 1994;84:4226-4233.

     Not in our library

162. 162.

     Komeima K, Hayashi Y, Naito Y, Watanabe Y. Inhibition of neuronal nitric-oxide synthase by calcium/calmodulin-dependent protein kinase IIalpha through Ser847 phosphorylation in NG108-15 neuronal cells. J. Biol. Chem. 2000;275:28139-28143.

     Not in our library10.1074/jbc.m003198200

163. 163.

     Koppenol WH. NO nomenclature? Nitric Oxide. 2002;6:96-98.

     Not in our library10.1006/niox.2001.0406

164. 164.

     Kostic TS, Andric SA, Stojilkovic SS. Receptor-controlled phosphorylation of alpha 1 soluble guanylyl cyclase enhances nitric oxide-dependent cyclic guanosine 5’-monophosphate production in pituitary cells. Mol. Endocrinol. 2004;18:458-470.

     Not in our library10.1210/me.2003-0015

165. 165.

     Kotera J, Grimes KA, Corbin JD, Francis SH. cGMP-dependent protein kinase protects cGMP from hydrolysis by phosphodiesterase-5. Biochem. J. 2003;372:419-426.

     Not in our library10.1042/bj20030107

166. 166.

     Krumenacker JS, Hanafy KA, Murad F. Regulation of nitric oxide and soluble guanylyl cyclase. Brain Res. Bull. 2004;62:505-515.

     Not in our library10.1016/s0361-9230(03)00102-3

167. 167.

     Kyriakatos A, El Manira A. Long-term plasticity of the spinal locomotor circuitry mediated by endocannabinoid and nitric oxide signaling. J. Neurosci. 2007;27:12664-12674.

     Not in our library10.1523/jneurosci.3174-07.2007

168. 168.

     Lancaster JR. A tutorial on the diffusibility and reactivity of free nitric oxide. Nitric Oxide. 1997;1:18-30.

     Not in our library10.1006/niox.1996.0112

169. 169.

     Langnaese K, Richter K, Smalla KH, Krauss M, Thomas U, Wolf G, Laube G. Splice-isoform specific immunolocalization of neuronal nitric oxide synthase in mouse and rat brain reveals that the PDZ-complex-building nNOSalpha beta-finger is largely exposed to antibodies. Dev. Neurobiol. 2007;67:422-437.

     Not in our library10.1002/dneu.20317

170. 170.

     Latchford KJ, Ferguson AV. Angiotensin II activates a nitric-oxide-driven inhibitory feedback in the rat paraventricular nucleus. J. Neurophysiol. 2003;89:1238-1244.

     Not in our library10.1152/jn.00914.2002

171. 171.

     Launey T, Endo S, Sakai R, Harano J, Ito M. Protein phosphatase 2A inhibition induces cerebellar long-term depression and declustering of synaptic AMPA receptor. Proc. Natl Acad. Sci. USA. 2004;101:676-681.

     Not in our library10.1073/pnas.0302914101

172. 172.

     Lev-Ram V, Wong ST, Storm DR, Tsien RY. A new form of cerebellar long-term potentiation is postsynaptic and depends on nitric oxide but not cAMP. Proc. Natl Acad. Sci. USA. 2002;99:8389-8993.

     Not in our library10.1073/pnas.122206399

173. 173.

     Li DP, Chen SR, Pan HL. Nitric oxide inhibits spinally projecting paraventricular neurons through potentiation of presynaptic GABA release. J. Neurophysiol. 2002;88:2664-2674.

     Not in our library10.1152/jn.00540.2002

174. 174.

     Li Y, Zhang W, Stern JE. Nitric oxide inhibits the firing activity of hypothalamic paraventricular neurons that innervate the medulla oblongata: role of GABA. Neuroscience. 2003;118:585-601.

     Not in our library10.1016/s0306-4522(03)00042-3

175. 175.

     Li DP, Chen SR, Finnegan TF, Pan HL. Signalling pathway of nitric oxide in synaptic GABA release in the rat paraventricular nucleus. J. Physiol. 2004;554:100-110.

     Not in our library10.1113/jphysiol.2003.053371

176. 176.

     Lin LH, Taktakishvili O, Talman WT. Identification and localization of cell types that express endothelial and neuronal nitric oxide synthase in the rat nucleus tractus solitarii. Brain Res. 2007;1171:42-51.

     Not in our library10.1016/j.brainres.2007.07.057

177. 177.

     Lipton SA, Choi YB, Takahashi H, Zhang D, Li W, Godzik A, Bankston LA. Cysteine regulation of protein function – as exemplified by NMDA-receptor modulation. Trends Neurosci. 2002;25:474-480.

     Not in our library10.1016/s0166-2236(02)02245-2

178. 178.

     Liu X, Miller MJ, Joshi MS, Sadowska-Krowicka H, Clark DA, Lancaster JR. Diffusion-limited reaction of free nitric oxide with erythrocytes. J. Biol. Chem. 1998;273:18709-18713.

     Not in our library10.1074/jbc.273.30.18709

179. 179.

     Liu X, Srinivasan P, Collard E, Grajdeanu P, Zweier JL, Friedman A. Nitric oxide diffusion rate is reduced in the aortic wall. Biophys. J. 2008;94:1880-1889.

     Not in our library10.1529/biophysj.107.120626

180. 180.

     Lovick TA, Brown LA, Key BJ. Neurovascular relationships in hippocampal slices: physiological and anatomical studies of mechanisms underlying flow-metabolism coupling in intraparenchymal microvessels. Neuroscience. 1999;92:47-60.

     Not in our library10.1016/s0306-4522(98)00737-4

181. 181.

     Lu YF, Hawkins RD. Ryanodine receptors contribute to cGMP-induced late-phase LTP and CREB phosphorylation in the hippocampus. J. Neurophysiol. 2002;88:1270-1278.

     Not in our library10.1152/jn.2002.88.3.1270

182. 182.

     Lu YF, Kandel ER, Hawkins RD. Nitric oxide signaling contributes to late-phase LTP and CREB phosphorylation in the hippocampus. J. Neurosci. 1999;19:10250-10261.

     Not in our library10.1523/jneurosci.19-23-10250.1999

183. 183.

     Ma X, Sayed N, Beuve A, van den AF. NO and CO differentially activate soluble guanylyl cyclase via a heme pivot-bend mechanism. EMBO J. 2007;26:578-588.

     Not in our library10.1038/sj.emboj.7601521

184. 184.

     Maffei A, Prestori F, Shibuki K, Rossi P, Taglietti V, D’Angelo E. NO enhances presynaptic currents during cerebellar mossy fiber-granule cell LTP. J. Neurophysiol. 2003;90:2478-2483.

     Not in our library10.1152/jn.00399.2003

185. 185.

     Makara JK, Katona I, Nyiri G, Nemeth B, Ledent C, Watanabe M, de VJ, Freund TF, Hajos N. Involvement of nitric oxide in depolarization-induced suppression of inhibition in hippocampal pyramidal cells during activation of cholinergic receptors. J. Neurosci. 2007;27:10211-10222.

     Not in our library10.1523/jneurosci.2104-07.2007

186. 186.

     Makino R, Matsuda H, Obayashi E, Shiro Y, Iizuka T, Hori H. EPR characterization of axial bond in metal center of native and cobalt-substituted guanylate cyclase. J. Biol. Chem. 1999;274:7714-7723.

     Not in our library10.1074/jbc.274.12.7714

187. 187.

     Marino J, Cudeiro J. Nitric oxide-mediated cortical activation: a diffuse wake-up system. J. Neurosci. 2003;23:4299-4307.

     Not in our library10.1523/jneurosci.23-10-04299.2003

188. 188.

     Martens-Lobenhoffer J, Sulyok E, Czeiter E, Buki A, Kohl J, Firsching R, Troger U, Bode-Boger SM. Determination of cerebrospinal fluid concentrations of arginine and dimethylarginines in patients with subarachnoid haemorrhage. J. Neurosci. Methods. 2007;164:155-160.

     Not in our library10.1016/j.jneumeth.2007.04.005

189. 189.

     Martin E, Berka V, Bogatenkova E, Murad F, Tsai AL. Ligand selectivity of soluble guanylyl cyclase: effect of the hydrogen-bonding tyrosine in the distal heme pocket on binding of oxygen, nitric oxide, and carbon monoxide. J. Biol. Chem. 2006;281:27836-27845.

     Not in our library10.1074/jbc.m601078200

190. 190.

     Matyash V, Filippov V, Mohrhagen K, Kettenmann H. Nitric oxide signals parallel fiber activity to Bergmann glial cells in the mouse cerebellar slice. Mol. Cell. Neurosci. 2001;18:664-670.

     Not in our library10.1006/mcne.2001.1047

191. 191.

     Mergia E, Russwurm M, Zoidl G, Koesling D. Major occurrence of the new alpha(2)beta(1) isoform of NO-sensitive guanylyl cyclase in brain. Cell. Signal. 2003;15:189-195.

     Not in our library10.1016/s0898-6568(02)00078-5

192. 192.

     Mergia E, Friebe A, Dangel O, Russwurm M, Koesling D. Spare guanylyl cyclase NO receptors ensure high NO sensitivity in the vascular system. J. Clin. Invest. 2006;116:1731-1737.

     Not in our library10.1172/jci27657

193. 193.

     Meurer S, Pioch S, Wagner K, Muller-Esterl W, Gross S. AGAP1, a novel binding partner of nitric oxide-sensitive guanylyl cyclase. J. Biol. Chem. 2004;279:49346-49354.

     Not in our library10.1074/jbc.m410565200

194. 194.

     Miki N, Kawabe Y, Kuriyama K. Activation of cerebral guanylate cyclase by nitric oxide. Biochem. Biophys. Res. Commun. 1977;75:851-856.

     Not in our library10.1016/0006-291x(77)91460-7

195. 195.

     Mironov SL, Langohr K. Modulation of synaptic and channel activities in the respiratory network of the mice by NO/cGMP signalling pathways. Brain Res. 2007;1130:73-82.

     Not in our library10.1016/j.brainres.2006.09.114

196. 196.

     Mize RR, Lo F. Nitric oxide, impulse activity, and neurotrophins in visual system development. Brain Res. 2000;886:15-32.

     Not in our library10.1016/s0006-8993(00)02750-5

197. 197.

     Mo E, Amin H, Bianco IH, Garthwaite J. Kinetics of a cellular nitric oxide/cGMP/phosphodiesterase-5 pathway. J. Biol. Chem. 2004;279:26149-26158.

     Not in our library10.1074/jbc.m400916200

198. 198.

     Montague PR, Sejnowski TJ. The predictive brain: temporal coincidence and temporal order in synaptic learning mechanisms. Learn. Mem. 1994;1:1-33.

     Not in our library

199. 199.

     Montoliu C, Llansola M, Kosenko E, Corbalan R, Felipo V. Role of cyclic GMP in glutamate neurotoxicity in primary cultures of cerebellar neurons. Neuropharmacology. 1999;38:1883-1891.

     Not in our library10.1016/s0028-3908(99)00071-4

200. 200.

     Moreno H, Vega-Saenz de ME, Nadal MS, Amarillo Y, Rudy B. Modulation of Kv3 potassium channels expressed in CHO cells by a nitric oxide-activated phosphatase. J. Physiol. 2001;530:345-358.

     Not in our library10.1111/j.1469-7793.2001.0345k.x

201. 201.

     Moroz LL. Gaseous transmission across time and species. Amer. Zool. 2001;41:304-320.

     Not in our library

202. 202.

     Moroz LL, Meech RW, Sweedler JV, Mackie GO. Nitric oxide regulates swimming in the jellyfish Aglantha digitale. J. Comp. Neurol. 2004;471:26-36.

     Not in our library10.1002/cne.20023

203. 203.

     Mullershausen F, Russwurm M, Friebe A, Koesling D. Inhibition of phosphodiesterase type 5 by the activator of nitric oxide-sensitive guanylyl cyclase BAY 41-2272. Circulation. 2004;109:1711-1713.

     Not in our library10.1161/01.cir.0000126286.47618.bd

204. 204.

     Mullershausen F, Lange A, Mergia E, Friebe A, Koesling D. Desensitization of NO/cGMP signaling in smooth muscle: blood vessels versus airways. Mol. Pharmacol. 2006;69:1969-1974.

     Not in our library10.1124/mol.105.020909

205. 205.

     Murphy GJ, Isaacson JS. Presynaptic cyclic nucleotide-gated ion channels modulate neurotransmission in the mammalian olfactory bulb. Neuron. 2003;37:639-647.

     Not in our library10.1016/s0896-6273(03)00057-6

206. 206.

     Murthy KS. Inhibitory phosphorylation of soluble guanylyl cyclase by muscarinic m2 receptors via G{beta}{gamma}-dependent activation of c-Src kinase. J. Pharmacol. Exp. Ther. 2008;325:183-189.

     Not in our library10.1124/jpet.107.132928

207. 207.

     Nakane M, Mitchell J, Forstermann U, Murad F. Phosphorylation by calcium calmodulin-dependent protein kinase II and protein kinase C modulates the activity of nitric oxide synthase. Biochem. Biophys. Res. Commun. 1991;180:1396-1402.

     Not in our library10.1016/s0006-291x(05)81351-8

208. 208.

     Nausch LW, Ledoux J, Bonev AD, Nelson MT, Dostmann WR. Differential patterning of cGMP in vascular smooth muscle cells revealed by single GFP-linked biosensors. Proc. Natl Acad. Sci. USA. 2008;105:365-370.

     Not in our library10.1073/pnas.0710387105

209. 209.

     Nauser T, Koppenol WH. The rate constant of the reaction of superoxide with nitrogen monoxide: approaching the diffusion limit. J. Phys. Chem. A. 2002;106:4084-4086.

     Not in our library

210. 210.

     Nedvetsky PI, Meurer S, Opitz N, Nedvetskaya TY, Muller H, Schmidt HH. Heat shock protein 90 regulates stabilization rather than activation of soluble guanylate cyclase. FEBS Lett. 2008;582:327-331.

     Not in our library10.1016/j.febslet.2007.12.025

211. 211.

     Nelson RJ, Trainor BC, Chiavegatto S, Demas GE. Pleiotropic contributions of nitric oxide to aggressive behavior. Neurosci. Biobehav. Rev. 2006;30:346-355.

     Not in our library10.1016/j.neubiorev.2005.02.002

212. 212.

     Newman Z, Malik P, Wu TY, Ochoa C, Watsa N, Lindgren C. Endocannabinoids mediate muscarine-induced synaptic depression at the vertebrate neuromuscular junction. Eur. J. Neurosci. 2007;25:1619-1630.

     Not in our library10.1111/j.1460-9568.2007.05422.x

213. 213.

     Nikonenko I, Jourdain P, Muller D. Presynaptic remodeling contributes to activity-dependent synaptogenesis. J. Neurosci. 2003;23:8498-8505.

     Not in our library10.1523/jneurosci.23-24-08498.2003

214. 214.

     Ninan I, Arancio O. Presynaptic CaMKII is necessary for synaptic plasticity in cultured hippocampal neurons. Neuron. 2004;42:129-141.

     Not in our library10.1016/s0896-6273(04)00143-6

215. 215.

     Nugent FS, Penick EC, Kauer JA. Opioids block long-term potentiation of inhibitory synapses. Nature. 2007;446:1086-1090.

     Not in our library10.1038/nature05726

216. 216.

     O’Dell TJ, Hawkins RD, Kandel ER, Arancio O. Tests of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible early retrograde messenger. Proc. Natl Acad. Sci. USA. 1991;88:11285-11289.

     Not in our library10.1073/pnas.88.24.11285

217. 217.

     O’Dell TJ, Huang PL, Dawson TM, Dinerman JL, Snyder SH, Kandel ER, Fishman MC. Endothelial NOS and the blockade of LTP by NOS inhibitors in mice lacking neuronal NOS. Science. 1994;265:542-546.

     Not in our library10.1126/science.7518615

218. 218.

     O’Donnell VB, Chumley PH, Hogg N, Bloodsworth A, Darley-Usmar VM, Freeman BA. Nitric oxide inhibition of lipid peroxidation: kinetics of reaction with lipid peroxyl radicals and comparison with alpha-tocopherol. Biochemistry. 1997;36:15216-15223.

     Not in our library10.1021/bi971891z

219. 219.

     Olesen S-P, Drejer J, Axelsson O, Moldt P, Bang L, Nielsen-Kudsk JE, Busse R, Mulsch A. Characterization of NS 2028 as a specific inhibitor of soluble guanylyl cyclase. Br. J. Pharmacol. 1998;123:299-309.

     Not in our library10.1038/sj.bjp.0701603

220. 220.

     Ott SR, Philippides A, Elphick MR, O'shea M. Enhanced fidelity of diffusive nitric oxide signalling by the spatial segregation of source and target neurones in the memory centre of an insect brain. Eur. J. Neurosci. 2007;25:181-190.

     Not in our library10.1111/j.1460-9568.2006.05271.x

221. 221.

     Palmer RM, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature. 1987;327:524-526.

     Not in our library10.1038/327524a0

222. 222.

     Palumbo A. Nitric oxide in marine invertebrates: a comparative perspective. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 2005;142:241-248.

     Not in our library10.1016/j.cbpb.2005.05.043

223. 223.

     Papapetropoulos A, Zhou Z, Gerassimou C, Yetik G, Venema RC, Roussos C, Sessa WC, Catravas JD. Interaction between the 90-kDa heat shock protein and soluble guanylyl cyclase: physiological significance and mapping of the domains mediating binding. Mol. Pharmacol. 2005;68:1133-1141.

     Not in our library10.1124/mol.105.012682

224. 224.

     Park JH, Straub VA, O'shea M. Anterograde signaling by nitric oxide: characterization and in vitro reconstitution of an identified nitrergic synapse. J. Neurosci. 1998;18:5463-5476.

     Not in our library10.1523/jneurosci.18-14-05463.1998

225. 225.

     Patel S, Robb-Gaspers LD, Stellato KA, Shon M, Thomas AP. Coordination of calcium signalling by endothelial-derived nitric oxide in the intact liver. Nat. Cell Biol. 1999;1:467-471.

     Not in our library10.1038/70249

226. 226.

     Paton JF, Waki H, Abdala AP, Dickinson J, Kasparov S. Vascular-brain signaling in hypertension: role of angiotensin II and nitric oxide. Curr. Hypertens. Rep. 2007;9:242-247.

     Not in our library10.1007/s11906-007-0043-1

227. 227.

     Pawlik G, Rackl A, Bing RJ. Quantitative capillary topography and blood flow in the cerebral cortex of cats: an in vivo microscopic study. Brain Res. 1981;208:35-58.

     Not in our library10.1016/0006-8993(81)90619-3

228. 228.

     Pepicelli O, Raiteri M, Fedele E. The NOS/sGC pathway in the rat central nervous system: a microdialysis overview. Neurochem. Int. 2004;45:787-797.

     Not in our library10.1016/j.neuint.2004.03.009

229. 229.

     Persechini A, White HD, Gansz KJ. Different mechanisms for Ca2+ dissociation from complexes of calmodulin with nitric oxide synthase or myosin light chain kinase. J. Biol. Chem. 1996;271:62-67.

     Not in our library10.1074/jbc.271.1.62

230. 230.

     Pfeifer A, Klatt P, Massberg S, Ny L, Sausbier M, Hirneiss C, Wang GX, Korth M, Aszodi A, Andersson KE, Krombach F, Mayerhofer A, Ruth P, Fassler R, Hofmann F. Defective smooth muscle regulation in cGMP kinase I-deficient mice. EMBO J. 1998;17:3045-3051.

     Not in our library10.1093/emboj/17.11.3045

231. 231.

     Philippides A, Ott SR, Husbands P, Lovick TA, O'shea M. Modeling cooperative volume signaling in a plexus of nitric-oxide-synthase-expressing neurons. J. Neurosci. 2005;25:6520-6532.

     Not in our library10.1523/jneurosci.1264-05.2005

232. 232.

     Piet R, Jahr CE. Glutamatergic and purinergic receptor-mediated calcium transients in Bergmann glial cells. J. Neurosci. 2007;27:4027-4035.

     Not in our library10.1523/jneurosci.0462-07.2007

233. 233.

     Pilz RB, Broderick KE. Role of cyclic GMP in gene regulation. Front. Biosci. 2005;10:1239-1268.

     Not in our library10.2741/1616

234. 234.

     Poblete IM, Orliac ML, Briones R, dler-Graschinsky E, Huidobro-Toro JP. Anandamide elicits an acute release of nitric oxide through endothelial TRPV1 receptor activation in the rat arterial mesenteric bed. J. Physiol. 2005;568:539-551.

     Not in our library10.1113/jphysiol.2005.094292

235. 235.

     Podda MV, D’Ascenzo M, Leone L, Piacentini R, Azzena GB, Grassi C. Functional role of cyclic nucleotide-gated channels in rat medial vestibular nucleus neurons. J. Physiol. 2008;586:803-815.

     Not in our library10.1113/jphysiol.2007.146019

236. 236.

     Poulopoulou C, Nowak LM. Extracellular 3’,5’ cyclic guanosine monophosphate inhibits kainate-activated responses in cultured mouse cerebellar neurons. J. Pharmacol. Exp. Ther. 1998;286:99-109.

     Not in our library

237. 237.

     Prast H, Philippu A. Nitric oxide as modulator of neuronal function. Prog. Neurobiol. 2001;64:51-68.

     Not in our library10.1016/s0301-0082(00)00044-7

238. 238.

     Pyriochou A, Papapetropoulos A. Soluble guanylyl cyclase: more secrets revealed. Cell. Signal. 2005;17:407-413.

     Not in our library10.1016/j.cellsig.2004.09.008

239. 239.

     Qiu DL, Knopfel T. An NMDA receptor/nitric oxide cascade in presynaptic parallel fiber-Purkinje neuron long-term potentiation. J. Neurosci. 2007;27:3408-3415.

     Not in our library10.1523/jneurosci.4831-06.2007

240. 240.

     Ramamoorthy S, Samuvel DJ, Buck ER, Rudnick G, Jayanthi LD. Phosphorylation of threonine residue 276 is required for acute regulation of serotonin transporter by cyclic GMP. J. Biol. Chem. 2007;282:11639-11647.

     Not in our library10.1074/jbc.m611353200

241. 241.

     Rameau GA, Chiu LY, Ziff EB. Bidirectional regulation of neuronal nitric-oxide synthase phosphorylation at serine 847 by the N-methyl-d-aspartate receptor. J. Biol. Chem. 2004;279:14307-14314.

     Not in our library10.1074/jbc.m311103200

242. 242.

     Rameau GA, Tukey DS, Garcin-Hosfield ED, Titcombe RF, Misra C, Khatri L, Getzoff ED, Ziff EB. Biphasic coupling of neuronal nitric oxide synthase phosphorylation to the NMDA receptor regulates AMPA receptor trafficking and neuronal cell death. J. Neurosci. 2007;27:3445-3455.

     Not in our library10.1523/jneurosci.4799-06.2007

243. 243.

     Rancillac A, Rossier J, Guille M, Tong XK, Geoffroy H, Amatore C, Arbault S, Hamel E, Cauli B. Glutamatergic control of microvascular tone by distinct GABA neurons in the cerebellum. J. Neurosci. 2006;26:6997-7006.

     Not in our library10.1523/jneurosci.5515-05.2006

244. 244.

     Rand MJ, Li CG. Nitric oxide as a neurotransmitter in peripheral nerves: nature of transmitter and mechanism of transmission. Annu. Rev. Physiol. 1995;57:659-682.

     Not in our library10.1146/annurev.ph.57.030195.003303

245. 245.

     Rauch M, Schmid HA, deVente J, Simon E. Electrophysiological and immunocytochemical evidence for a cGMP-mediated inhibition of subfornical organ neurons by nitric oxide. J. Neurosci. 1997;17:363-371.

     Not in our library10.1523/jneurosci.17-01-00363.1997

246. 246.

     Reif A, Schmitt A, Fritzen S, Chourbaji S, Bartsch C, Urani A, Wycislo M, Mossner R, Sommer C, Gass P, Lesch KP. Differential effect of endothelial nitric oxide synthase (NOS-III) on the regulation of adult neurogenesis and behaviour. Eur. J. Neurosci. 2004;20:885-895.

     Not in our library10.1111/j.1460-9568.2004.03559.x

247. 247.

     Riediger T, Giannini P, Erguven E, Lutz T. Nitric oxide directly inhibits ghrelin-activated neurons of the arcuate nucleus. Brain Res. 2006;1125:37-45.

     Not in our library10.1016/j.brainres.2006.09.049

248. 248.

     Rivadulla C, Grieve KL, Rodriguez R, Martinez-Conde S, Acuna C, Cuderio J. An unusual effect of application of the amino acid l-arginine on cat visual cortical cells. Neuroreport. 1997;8:863-866.

     Not in our library

249. 249.

     Rodriguez-Crespo I, Straub W, Gavilanes F, Ortiz de Montellano PR. Binding of dynein light chain (PIN) to neuronal nitric oxide synthase in the absence of inhibition. Arch. Biochem. Biophys. 1998;359:297-304.

     Not in our library10.1006/abbi.1998.0928

250. 250.

     Romano MR, Lograno MD. Cannabinoid agonists induce relaxation in the bovine ophthalmic artery: evidences for CB1 receptors, nitric oxide and potassium channels. Br. J. Pharmacol. 2006;147:917-925.

     Not in our library10.1038/sj.bjp.0706687

251. 251.

     Roy B, Garthwaite J. Nitric oxide activation of guanylyl cyclase in cells revisited. Proc. Natl Acad. Sci. USA. 2006;103:12185-12190.

     Not in our library10.1073/pnas.0602544103

252. 252.

     Roy B, Mo E, Vernon J, Garthwaite J. Probing the presence of the ligand-binding haem in cellular nitric oxide receptors. Br. J. Pharmacol. 2008;153:1495-1504.

     Not in our library10.1038/sj.bjp.0707687

253. 253.

     Russwurm M, Behrends S, Harteneck C, Koesling D. Functional properties of a naturally occurring isoform of soluble guanylyl cyclase. Biochem. J. 1998;335:125-130.

     Not in our library10.1042/bj3350125

254. 254.

     Russwurm M, Wittau N, Koesling D. Guanylyl cyclase/PSD-95 interaction: targeting of the NO-sensitive alpha2beta1 guanylyl cyclase to synaptic membranes. J. Biol. Chem. 2001;276:44647-44652.

     Not in our library10.1074/jbc.m105587200

255. 255.

     Russwurm M, Mullershausen F, Friebe A, Jager R, Russwurm C, Koesling D. Design of fluorescence resonance energy transfer (FRET)-based cGMP indicators: a systematic approach. Biochem. J. 2007;407:69-77.

     Not in our library10.1042/bj20070348

256. 256.

     Sabatini BL, Oertner TG, Svoboda K. The life cycle of Ca[2+] ions in dendritic spines. Neuron. 2002;33:439-452.

     Not in our library10.1016/s0896-6273(02)00573-1

257. 257.

     Safo PK, Regehr WG. Endocannabinoids control the induction of cerebellar LTD. Neuron. 2005;48:647-659.

     Not in our library10.1016/j.neuron.2005.09.020

258. 258.

     Sager G. Cyclic GMP transporters. Neurochem. Int. 2004;45:865-873.

     Not in our library10.1016/j.neuint.2004.03.017

259. 259.

     Sanders KM, Koh SD. Two-pore-domain potassium channels in smooth muscles: new components of myogenic regulation. J. Physiol. 2006;570:37-43.

     Not in our library10.1113/jphysiol.2005.098897

260. 260.

     Santolini J, Adak S, Curran CM, Stuehr DJ. A kinetic simulation model that describes catalysis and regulation in nitric-oxide synthase. J. Biol. Chem. 2001;276:1233-1243.

     Not in our library10.1074/jbc.m006858200

261. 261.

     Sardo P, Carletti F, D’Agostino S, Rizzo V, Ferraro G. Effects of nitric oxide-active drugs on the discharge of subthalamic neurons: microiontophoretic evidence in the rat. Eur. J. Neurosci. 2006;24:1995-2002.

     Not in our library10.1111/j.1460-9568.2006.05097.x

262. 262.

     Sato M, Hida N, Umezawa Y. Imaging the nanomolar range of nitric oxide with an amplifier-coupled fluorescent indicator in living cells. Proc. Natl Acad. Sci. USA. 2005;102:14515-14520.

     Not in our library10.1073/pnas.0505136102

263. 263.

     Sausbier M, Schubert R, Voigt V, Hirneiss C, Pfeifer A, Korth M, Kleppisch T, Ruth P, Hofmann F. Mechanisms of NO/cGMP-dependent vasorelaxation. Circ. Res. 2000;87:825-830.

     Not in our library10.1161/01.res.87.9.825

264. 264.

     Savchenko A, Barnes S, Kramer RH. Cyclic-nucleotide-gated channels mediate synaptic feedback by nitric oxide. Nature. 1997;390:694-698.

     Not in our library10.1038/37803

265. 265.

     Schindler U, Strobel H, Schonafinger K, Linz W, Lohn M, Martorana PA, Rutten H, Schindler PW, Busch AE, Sohn M, Topfer A, Pistorius A, Jannek C, Mulsch A. Biochemistry and pharmacology of novel anthranilic acid derivatives activating heme-oxidized soluble guanylyl cyclase. Mol. Pharmacol. 2006;69:1260-1268.

     Not in our library10.1124/mol.105.018747

266. 266.

     Schlossmann J, Hofmann F. cGMP-dependent protein kinases in drug discovery. Drug Discov. Today. 2005;10:627-634.

     Not in our library10.1016/s1359-6446(05)03406-9

267. 267.

     Schmid HA, Pehl U. Regional specific effects of nitric oxide donors and cGMP on the electrical activity of neurons in the rat spinal cord. J. Chem. Neuroanat. 1996;10:197-201.

     Not in our library10.1016/0891-0618(96)00143-3

268. 268.

     Schmidt PM, Schramm M, Schroder H, Wunder F, Stasch JP. Identification of residues crucially involved in the binding of the heme moiety of soluble guanylate cyclase. J. Biol. Chem. 2004;279:3025-3032.

     Not in our library10.1074/jbc.m310141200

269. 269.

     Schrammel A, Behrends S, Schmidt K, Koesling D, Mayer B. Characterization of 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one as a heme-site inhibitor of nitric oxide-sensitive guanylyl cyclase. Mol. Pharmacol. 1996;50:1-5.

     Not in our library

270. 270.

     Secondo A, Pannaccione A, Cataldi M, Sirabella R, Formisano L, Di RG, Annunziato L. Nitric oxide induces [Ca2+]i oscillations in pituitary GH3 cells: involvement of IDR and ERG K+ currents. Am. J. Physiol. Cell Physiol. 2006;290:C233-C243.

     Not in our library10.1152/ajpcell.00231.2005

271. 271.

     Seidel B, Stanarius A, Wolf G. Differential expression of neuronal and endothelial nitric oxide synthase in blood vessels of the rat brain. Neurosci. Lett. 1997;239:109-112.

     Not in our library10.1016/s0304-3940(97)00912-9

272. 272.

     Sergeeva OA, Doreulee N, Chepkova AN, Kazmierczak T, Haas HL. Long-term depression of cortico-striatal synaptic transmission by DHPG depends on endocannabinoid release and nitric oxide synthesis. Eur. J. Neurosci. 2007;26:1889-1894.

     Not in our library10.1111/j.1460-9568.2007.05815.x

273. 273.

     Serulle Y, Zhang S, Ninan I, Puzzo D, McCarthy M, Khatri L, Arancio O, Ziff EB. A GluR1-cGKII interaction regulates AMPA receptor trafficking. Neuron. 2007;56:670-688.

     Not in our library10.1016/j.neuron.2007.09.016

274. 274.

     Shaw PJ, Charles SL, Salt TE. Actions of 8-bromo-cyclic-GMP on neurones in the rat thalamus in vivo and in vitro. Brain Res. 1999;833:272-277.

     Not in our library10.1016/s0006-8993(99)01556-5

275. 275.

     Shibuki K, Kimura S. Dynamic properties of nitric oxide release from parallel fibres in rat cerebellar slices. J. Physiol. 1997;498(Pt 2):443-452.

     Not in our library10.1113/jphysiol.1997.sp021870

276. 276.

     Shimizu-Albergine M, Rybalkin SD, Rybalkina IG, Feil R, Wolfsgruber W, Hofmann F, Beavo JA. Individual cerebellar Purkinje cells express different cGMP phosphodiesterases (PDEs): in vivo phosphorylation of cGMP-specific PDE (PDE5) as an indicator of cGMP-dependent protein kinase (PKG) activation. J. Neurosci. 2003;23:6452-6459.

     Not in our library10.1523/jneurosci.23-16-06452.2003

277. 277.

     Shin JH, Linden DJ. An NMDA receptor/nitric oxide cascade is involved in cerebellar LTD but is not localized to the parallel fiber terminal. J. Neurophysiol. 2005;94:4281-4289.

     Not in our library10.1152/jn.00661.2005

278. 278.

     Sjostrom PJ, Turrigiano GG, Nelson SB. Multiple forms of long-term plasticity at unitary neocortical layer 5 synapses. Neuropharmacology. 2007;52:176-184.

     Not in our library10.1016/j.neuropharm.2006.07.021

279. 279.

     Smith KJ, Lassmann H. The role of nitric oxide in multiple sclerosis. Lancet Neurol. 2002;1:232-241.

     Not in our library10.1016/s1474-4422(02)00102-3

280. 280.

     Smith SL, Otis TS. Persistent changes in spontaneous firing of Purkinje neurons triggered by the nitric oxide signaling cascade. J. Neurosci. 2003;23:367-372.

     Not in our library10.1523/jneurosci.23-02-00367.2003

281. 281.

     Son H, Hawkins RD, Martin K, Kiebler M, Huang PL, Fishman MC, Kandel ER. Long-term potentiation is reduced in mice that are doubly mutant in endothelial and neuronal nitric oxide synthase. Cell. 1996;87:1015-1023.

     Not in our library10.1016/s0092-8674(00)81796-1

282. 282.

     Song T, Hatano N, Horii M, Tokumitsu H, Yamaguchi F, Tokuda M, Watanabe Y. Calcium/calmodulin-dependent protein kinase I inhibits neuronal nitric-oxide synthase activity through serine 741 phosphorylation. FEBS Lett. 2004;570:133-137.

     Not in our library10.1016/j.febslet.2004.05.083

283. 283.

     Song T, Hatano N, Kume K, Sugimoto K, Yamaguchi F, Tokuda M, Watanabe Y. Inhibition of neuronal nitric-oxide synthase by phosphorylation at Threonine1296 in NG108-15 neuronal cells. FEBS Lett. 2005;579:5658-5662.

     Not in our library10.1016/j.febslet.2005.09.037

284. 284.

     Song XJ, Wang ZB, Gan Q, Walters ET. cAMP and cGMP contribute to sensory neuron hyperexcitability and hyperalgesia in rats with dorsal root ganglia compression. J. Neurophysiol. 2006;95:479-492.

     Not in our library10.1152/jn.00503.2005

285. 285.

     Southam E, Garthwaite J. Comparative effects of some nitric oxide donors on cyclic GMP levels in rat cerebellar slices. Neurosci. Lett. 1991;130:107-111.

     Not in our library10.1016/0304-3940(91)90239-p

286. 286.

     Southam E, Garthwaite J. The nitric oxide-cyclic GMP signalling pathway in rat brain. Neuropharmacology. 1993;32:1267-1277.

     Not in our library10.1016/0028-3908(93)90021-t

287. 287.

     Southam E, Morris R, Garthwaite J. Sources and targets of nitric oxide in rat cerebellum. Neurosci. Lett. 1992;137:241-244.

     Not in our library10.1016/0304-3940(92)90413-2

288. 288.

     Stamler JS, Lamas S, Fang FC. Nitrosylation: the prototypic redox-based signaling mechanism. Cell. 2001;106:675-683.

     Not in our library10.1016/s0092-8674(01)00495-0

289. 289.

     Stanarius A, Topel I, Schulz S, Noack H, Wolf G. Immunocytochemistry of endothelial nitric oxide synthase in the rat brain: a light and electron microscopical study using the tyramide signal amplification technique. Acta Histochem. 1997;99:411-429.

     Not in our library10.1016/s0065-1281(97)80034-7

290. 290.

     Stasch JP, Becker EM, Alonso-Alija C, Apeler H, Dembowsky K, Feurer A, Gerzer R, Minuth T, Perzborn E, Pleiss U, Schroder H, Schroeder W, Stahl E, Steinke W, Straub A, Schramm M. NO-independent regulatory site on soluble guanylate cyclase. Nature. 2001;410:212-215.

     Not in our library10.1038/35065611

291. 291.

     Stasch JP, Schmidt P, Alonso-Alija C, Apeler H, Dembowsky K, Haerter M, Heil M, Minuth T, Perzborn E, Pleiss U, Schramm M, Schroeder W, Schroder H, Stahl E, Steinke W, Wunder F. NO- and haem-independent activation of soluble guanylyl cyclase: molecular basis and cardiovascular implications of a new pharmacological principle. Br. J. Pharmacol. 2002;136:773-783.

     Not in our library10.1038/sj.bjp.0704778

292. 292.

     Stasch JP, Schmidt PM, Nedvetsky PI, Nedvetskaya TY, AK HS, Meurer S, Deile M, Taye A, Knorr A, Lapp H, Muller H, Turgay Y, Rothkegel C, Tersteegen A, Kemp-Harper B, Muller-Esterl W, Schmidt HH. Targeting the heme-oxidized nitric oxide receptor for selective vasodilatation of diseased blood vessels. J. Clin. Invest. 2006;116:2552-2561.

     Not in our library10.1172/jci28371

293. 293.

     van Staveren WC, Markerink-Van Ittersum M, Steinbusch HW, de Vente J. The effects of phosphodiesterase inhibition on cyclic GMP and cyclic AMP accumulation in the hippocampus of the rat. Brain Res. 2001;888:275-286.

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     Steinberg JP, Takamiya K, Shen Y, Xia J, Rubio ME, Yu S, Jin W, Thomas GM, Linden DJ, Huganir RL. Targeted in vivo mutations of the AMPA receptor subunit GluR2 and its interacting protein PICK1 eliminate cerebellar long-term depression. Neuron. 2006;49:845-860.

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     Stone JR, Marletta MA. Soluble guanylate cyclase from bovine lung: activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states. Biochemistry. 1994;33:5636-5640.

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     Sunahara RK, Beuve A, Tesmer JJ, Sprang SR, Garbers DL, Gilman AG. Exchange of substrate and inhibitor specificities between adenylyl and guanylyl cyclases. J. Biol. Chem. 1998;273:16332-16338.

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     Sung YJ, Walters ET, Ambron RT. A neuronal isoform of protein kinase G couples mitogen-activated protein kinase nuclear import to axotomy-induced long-term hyperexcitability in Aplysia sensory neurons. J. Neurosci. 2004;24:7583-7595.

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300. 300.

     Susswein AJ, Katzoff A, Miller N, Hurwitz I. Nitric oxide and memory. Neuroscientist. 2004;10:153-162.

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303. 303.

     Toda N, Okamura T. The pharmacology of nitric oxide in the peripheral nervous system of blood vessels. Pharmacol. Rev. 2003;55:271-324.

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     Wedel B, Humbert P, Harteneck C, Foerster J, Malkewitz J, Bohme E, Schultz G, Koesling D. Mutation of His-105 in the beta 1 subunit yields a nitric oxide-insensitive form of soluble guanylyl cyclase. Proc. Natl Acad. Sci. USA. 1994;91:2592-2596.

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     West AR, Grace AA. The nitric oxide-guanylyl cyclase signaling pathway modulates membrane activity states and electrophysiological properties of striatal medium spiny neurons recorded in vivo. J. Neurosci. 2004;24:1924-1935.

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     Willmott N, Sethi JK, Walseth TF, Lee HC, White AM, Galione A. Nitric oxide-induced mobilization of intracellular calcium via the cyclic ADP-ribose signaling pathway. J. Biol. Chem. 1996;271:3699-3705.

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     Willmott NJ, Wong K, Strong AJ. A fundamental role for the nitric oxide-G-kinase signaling pathway in mediating intercellular Ca(2+) waves in glia. J. Neurosci. 2000;20:1767-1779.

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326. 326.

     Wilson RI, Godecke A, Brown RE, Schrader J, Haas HL. Mice deficient in endothelial nitric oxide synthase exhibit a selective deficit in hippocampal long-term potentiation. Neuroscience. 1999;90:1157-1165.

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     Wu SY, Dun NJ. Potentiation of IPSCs by nitric oxide in immature rat sympathetic preganglionic neurones in vitro. J. Physiol. Lond. 1996;495:479-490.

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     Wu SY, Dun SL, Forstermann U, Dun NJ. Nitric oxide and excitatory postsynaptic currents in immature rat sympathetic preganglionic neurons in vitro. Neuroscience. 1997;79:237-245.

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330. 330.

     Wykes V, Garthwaite J. Membrane-association and the sensitivity of guanylyl cyclase-coupled receptors to nitric oxide. Br. J. Pharmacol. 2004;141:1087-1090.

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331. 331.

     Wykes V, Bellamy TC, Garthwaite J. Kinetics of nitric oxide-cyclic GMP signalling in CNS cells and its possible regulation by cyclic GMP. J. Neurochem. 2002;83:37-47.

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     Xu ZQ, de VJ, Steinbusch H, Grillner S, Hokfelt T. The NO-cGMP pathway in the rat locus coeruleus: electrophysiological, immunohistochemical and in situ hybridization studies. Eur. J. Neurosci. 1998;10:3508-3516.

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     Yang G, Huard JM, Beitz AJ, Ross ME, Iadecola C. Stellate neurons mediate functional hyperemia in the cerebellar molecular layer. J. Neurosci. 2000;20:6968-6973.

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     Yang Q, Chen SR, Li DP, Pan HL. Kv1.1/1.2 channels are downstream effectors of nitric oxide on synaptic GABA release to preautonomic neurons in the paraventricular nucleus. Neuroscience. 2007;149:315-327.

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     Zabel U, Kleinschnitz C, Oh P, Nedvetsky P, Smolenski A, Muller H, Kronich P, Kugler P, Walter U, Schnitzer JE, Schmidt HH. Calcium-dependent membrane association sensitizes soluble guanylyl cyclase to nitric oxide. Nat. Cell Biol. 2002;4:307-311.

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     Zhang Y, Hogg N. S-Nitrosothiols: cellular formation and transport. Free Radic. Biol. Med. 2005;38:831-838.

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337. 337.

     Zhang L, Dawson VL, Dawson TM. Role of nitric oxide in Parkinson's disease. Pharmacol. Ther. 2006a;109:33-41.

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338. 338.

     Zhang XL, Zhou ZY, Winterer J, Muller W, Stanton PK. NMDA-dependent, but not group I metabotropic glutamate receptor-dependent, long-term depression at Schaffer collateral-CA1 synapses is associated with long-term reduction of release from the rapidly recycling presynaptic vesicle pool. J. Neurosci. 2006b;26:10270-10280.

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     Zhang YW, Gesmonde J, Ramamoorthy S, Rudnick G. Serotonin transporter phosphorylation by cGMP-dependent protein kinase is altered by a mutation associated with obsessive compulsive disorder. J. Neurosci. 2007a;27:10878-10886.

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340. 340.

     Zhang Z, Klyachko V, Jackson MB. Blockade of phosphodiesterase Type 5 enhances rat neurohypophysial excitability and electrically evoked oxytocin release. J. Physiol. 2007b;584:137-147.

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     Zhao Y, Schelvis JP, Babcock GT, Marletta MA. Identification of histidine 105 in the beta1 subunit of soluble guanylate cyclase as the heme proximal ligand. Biochemistry. 1998;37:4502-4509.

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     Zhao Y, Brandish PE, Ballou DP, Marletta MA. A molecular basis for nitric oxide sensing by soluble guanylate cyclase. Proc. Natl Acad. Sci. USA. 1999;96:14753-14758.

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     Zheng JH, Walters ET, Song XJ. Dissociation of dorsal root ganglion neurons induces hyperexcitability that is maintained by increased responsiveness to cAMP and cGMP. J. Neurophysiol. 2007;97:15-25.

     Not in our library10.1152/jn.00559.2006

Cited by papers we hold 6

• Progress and Promise of Nitric Oxide‐Releasing Platforms · 2018
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• Molecular Approaches for Manipulating Astrocytic Signaling In Vivo · 2015
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• Mechanisms in the Bed Nucleus of the Stria Terminalis Involved in Control of Autonomic and Neuroendocrine Functions: A Review · 2013
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• The role of nitric oxide in pre-synaptic plasticity and homeostasis · 2013
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• The changing roles of neurons in the cortical subplate · 2009
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• What is the real physiological NO concentration in vivo? · 2009
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