The role of nitric oxide and GluR1 in presynaptic and postsynaptic components of neocortical potentiation

Journal of Neuroscience

Volumn 26, Issue 28, 2006, Pages 7395-7404

  Hardingham, Neil ^a   Fox, Kevin ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; CALCIUM; CALMODULIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; STRONTIUM; CALMODULIN DEPENDENT PROTEIN KINASE II; CALMODULIN-DEPENDENT PROTEIN KINASE II; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 1; N(G) NITROARGININE; PROTEIN KINASE (CALCIUM,CALMODULIN);

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CONTROLLED STUDY; LONG TERM POTENTIATION; MOUSE; NEOCORTEX; NERVE CELL PLASTICITY; NERVE CONDUCTION; NEUROTRANSMISSION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN INTERACTION; QUANTITATIVE ASSAY; SIGNAL TRANSDUCTION; SOMATOSENSORY CORTEX; SYNAPSE; SYNAPTIC INHIBITION; ACTION POTENTIAL; ANIMAL; C57BL MOUSE; DRUG ANTAGONISM; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETICS; IN VITRO STUDY; MOUSE MUTANT; PATCH CLAMP; PHYSIOLOGY; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; EXCITATORY POSTSYNAPTIC POTENTIALS; LONG-TERM POTENTIATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOCORTEX; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITROARGININE; PATCH-CLAMP TECHNIQUES; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 33746079663     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0652-06.2006     Document Type: Article

References (50)

1. Abbott LF, Regehr WG (2004) Synaptic computation. Nature 431:796-803.
2. Allen PB, Hvalby O, Jensen V, Errington ML, Ramsay M, Chaudhry FA, Bliss TV, Storm-Mathisen J, Morris RG, Andersen P, Greengard P (2000) Protein phosphatase-1 regulation in the induction of long-term potentiation: heterogeneous molecular mechanisms. J Neurosci 20:3537-3543.
3. Barria A, Muller D, Derkach V, Griffith LC, Soderling TR (1997) Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science 276:2042-2045.
4. Bredt DS, Ferris CD, Snyder SH (1992) Nitric oxide synthase regulatory sites. Phosphorylation by cyclic AMP-dependent protein kinase, protein kinase C, and calcium/calmodulin protein kinase; identification of flavin and calmodulin binding sites. J Biol Chem 267:10976-10981.
5. Brenman JE, Chao DS, Gee SH, McGee AW, Craven SE, Santillano DR, Wu Z, Huang F, Xia H, Peters MF, Froehner SC, Bredt DS (1996) Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha1-syntrophin mediated by PDZ domains. Cell 84:757-767.
6. Buonomano DV (1999) Distinct functional types of associative long-term potentiation in neocortical and hippocampal pyramidal neurons. J Neurosci 19:6748-6754.
7. Buonomano DV, Merzenich MM (1998) Cortical plasticity: from synapses to maps. Annu Rev Neurosci 21:149-186.
8. Busconi L, Michel T (1993) Endothelial nitric oxide synthase. N-terminal myristoylation determines subcellular localization. J Biol Chem 268:8410-8413.
9. Carpenter GA, Milenova BL (2002) Redistribution of synaptic efficacy supports stable pattern learning in neural networks. Neural Comput 14:873-888.
10. Celikel T, Szostak VA, Feldman DE (2004) Modulation of spike timing by sensory deprivation during induction of cortical map plasticity. Nat Neurosci 7:534-541.
11. Feldman DE (2000) Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron 27:45-56.
12. Feldmeyer D, Lubke J, Silver RA, Sakmann B (2002) Synaptic connections between layer 4 spiny neurone-layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column. J Physiol (Lond) 538:803-822.
13. Finnerty GT, Roberts LS, Connors BW (1999) Sensory experience modifies the short-term dynamics of neocortical synapses. Nature 400:367-371.
14. Fox K (1994) The cortical component of experience-dependent synaptic plasticity in the rat barrel cortex. J Neurosci 14:7665-7679.
15. Fox K (2002) Anatomical pathways and molecular mechanisms for plasticity in the barrel cortex. Neuroscience 111:799-814.
16. Glazewski S, Chen CM, Silva A, Fox K (1996) Requirement for alpha-CaMKII in experience-dependent plasticity of the barrel cortex. Science 272:421-423.
17. Hardingham NR, Larkman AU (1998) Rapid report: the reliability of excitatory synaptic transmission in slices of rat visual cortex in vitro is temperature dependent. J Physiol (Lond) 507:249-256.
18. Hardingham N, Glazewski S, Pakhotin P, Mizuno K, Chapman PF, Giese KP, Fox K (2003) Neocortical long-term potentiation and experience-dependent synaptic plasticity require α-calcium/calmodulin-dependent protein kinase II autophosphorylation. J Neurosci 23:4428-4436.
19. Haul S, Godecke A, Schrader J, Haas HL, Luhmann HJ (1999) Impairment of neocortical long-term potentiation in mice deficient of endothelial nitric oxide synthase. J Neurophysiol 81:494-497.
20. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R (2000) Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287:2262-2267.
21. Hoffman DA, Sprengel R, Sakmann B (2002) Molecular dissection of hippocampal theta-burst pairing potentiation. Proc Natl Acad Sci USA 99:7740-7745.
22. Imura T, Kanatani S, Fukuda S, Miyamoto Y, Hisatsune T (2005) Layer-specific production of nitric oxide during cortical circuit formation in postnatal mouse brain. Cereb Cortex 15:332-340.
23. Isaac JT, Crair MC, Nicoll RA, Malenka RC (1997) Silent synapses during development of thalamocortical inputs. Neuron 18:269-280.
24. Ishida A, Shigeri Y, Tatsu Y, Uegaki K, Kameshita I, Okuno S, Kitani T, Yumoto N, Fujisawa H (1998) Critical amino acid residues of AIP, a highly specific inhibitory peptide of calmodulin-dependent protein kinase II. FEBS Lett 427:115-118.
25. Kantor DB, Lanzrein M, Stary SJ, Sandoval GM, Smith WB, Sullivan BM, Davidson N, Schuman EM (1996) A role for endothelial NO synthase in LTP revealed by adenovirus-mediated inhibition and rescue. Science 274:1744-1748.
26. Koester HJ, Johnston D (2005) Target cell-dependent normalization of transmitter release at neocortical synapses. Science 308:863-866.
27. Kolleker A, Zhu JJ, Schupp BJ, Qin Y, Mack V, Borchardt T, Kohr G, Malinow R, Seeburg PH, Osten P (2003) Glutamatergic plasticity by synaptic delivery of GluR-B(long)-containing AMPA receptors. Neuron 40:1199-1212.
28. Lancaster Jr JR (1997) A tutorial on the diffusibility and reactivity of free nitric oxide. Nitric Oxide 1:18-30.
29. Larkman AU, Jack JJ, Stratford KJ (1997a) Assessment of the reliability or amplitude histograms from excitatory synapses in rat hippocampal CA1 in vitro. J Physiol (Lond) 505:443-456.
30. Larkman AU, Jack JJ, Stratford KJ (1997b) Quantal analysis of excitatory synapses in rat hippocampal CA1 in vitro during low-frequency depression. J Physiol (Lond) 505:457-471.
31. Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44:5-21.
32. Malinow R, Tsien RW (1990) Presynaptic enhancement shown by wholecell recordings of long-term potentiation in hippocampal slices. Nature 346:177-180.
33. Markram H, Tsodyks M (1996) Redistribution of synaptic efficacy between neocortical pyramidal neurons. Nature 382:807-810.
34. Nicoll RA, Malenka RC (1995) Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature 377:115-118.
35. Philippides A, Ott SR, Husbands P, Lovick TA, O'Shea M (2005) Modeling cooperative volume signaling in a plexus of nitric-oxide-synthase-expressing neurons. J Neurosci 25:6520-6532.
36. Reyes A, Sakmann B (1999) Developmental switch in the short-term modification of unitary EPSPs evoked in layer 2/3 and layer 5 pyramidal neurons of rat neocortex. J Neurosci 19:3827-3835.
37. Rossner S, Kumar A, Kues W, Witzemann V, Schliebs R (1993) Differential laminar expression of AMPA receptor genes in the developing rat visual cortex using in situ hybridization histochemistry. Effect of visual deprivation. Int J Dev Neurosci 11:411-424.
38. Rumpel S, Kattenstroth G, Gottmann K (2004) Silent synapses in the immature visual cortex: layer-specific developmental regulation. J Neurophysiol 91:1097-1101.
39. Schmitt WB, Sprengel R, Mack V, Draft RW, Seeburg PH, Deacon RM, Rawlins JN, Bannerman DM (2005) Restoration of spatial working memory by genetic rescue of GluR-A-deficient mice. Nat Neurosci 8:270-272.
40. Sjostrom PJ, Turrigiano GG, Nelson SB (2003) Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39:641-654.
41. Son H, Hawkins RD, Martin K, Kiebler M, Huang PL, Fishman MC, Kandel ER (1996) Long-term potentiation is reduced in mice that are doubly mutant in endothelial and neuronal nitric oxide synthase. Cell 87:1015-1023.
42. Stratford KJ, Jack JJ, Larkman AU (1997) Calibration of an autocorrelation-based method for determining amplitude histogram reliability and quantal size. J Physiol (Lond) 505:425-442.
43. Takahashi T, Svoboda K, Malinow R (2003) Experience strengthening transmission by driving AMPA receptors into synapses. Science 299:1585-1588.
44. Volgushev M, Balaban P, Chistiakova M, Eysel UT (2000) Retrograde signalling with nitric oxide at neocortical synapses. Eur J Neurosci 12:4255-4267.
45. Wall MJ, Usowicz MM (1998) Development of the quantal properties of evoked and spontaneous synaptic currents at a brain synapse. Nat Neurosci 1:675-682.
46. Wang HG, Lu FM, Jin I, Udo H, Kandel ER, de Vente J, Walter U, Lohmann SM, Hawkins RD, Antonova I (2005) Presynaptic and postsynaptic roles of NO, cGK, and RhoA in long-lasting potentiation and aggregation of synaptic proteins. Neuron 45:389-403.
47. Watanabe Y, Song T, Sugimoto K, Horii M, Araki N, Tokumitsu H, Tezuka T, Yamamoto T, Tokuda M (2003) Post-synaptic density-95 promotes calcium/calmodulin-dependent protein kinase II-mediated Ser847 phosphorylation of neuronal nitric oxide synthase. Biochem J 372:465-471.
48. Woolsey TA, Van der Loos H (1970) The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res 17:205-242.
49. Yasuda H, Barth AL, Stellwagen D, Malenka RC (2003) A developmental switch in the signaling cascades for LTP induction. Nat Neurosci 6:15-16.
50. 2+/calmodulin-dependent protein kinase II in the postsynaptic density by protein sequencing and mass spectrometry. Biochem Biophys Res Commun 290:948-954.