Signaling Cascade Regulating Long-Term Potentiation of GABAA Receptor Responsiveness in Cerebellar Purkinje Neurons

Journal of Neuroscience

Volumn 22, Issue 10, 2002, Pages 3969-3976

  Kawaguchi, Shin Ya ^b   Hirano, Tomoo ^a  

^a KYOTO UNIVERSITY   (Japan)

^b NONE

Author keywords

Calcineurin; CaMKII; DARPP 32; GABA; Inhibitory synapse; PKA; PP 1; Purkinje neuron; Synaptic plasticity

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ANTISENSE OLIGONUCLEOTIDE; CALCINEURIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; PHOSPHOPROTEIN DARPP 32; PHOSPHOPROTEIN PHOSPHATASE 1; PROTEIN KINASE (CALCIUM,CALMODULIN) II; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; CALMODULIN DEPENDENT PROTEIN KINASE II; CALMODULIN-DEPENDENT PROTEIN KINASE II; ENZYME INHIBITOR; NERVE PROTEIN; PHOSPHOPROTEIN; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN KINASE (CALCIUM,CALMODULIN);

ANIMAL CELL; ARTICLE; CEREBELLUM; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME SUBSTRATE; INHIBITORY POSTSYNAPTIC POTENTIAL; LONG TERM POTENTIATION; NERVE CELL INHIBITION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PURKINJE CELL; RAT; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; METABOLISM; PATCH CLAMP; PHOSPHORYLATION; PHYSIOLOGY; WISTAR RAT;

ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCINEURIN; CELLS, CULTURED; CEREBELLUM; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DOPAMINE AND CAMP-REGULATED PHOSPHOPROTEIN 32; ENZYME INHIBITORS; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; LONG-TERM POTENTIATION; NERVE TISSUE PROTEINS; NEURAL INHIBITION; NEURONAL PLASTICITY; OLIGONUCLEOTIDES, ANTISENSE; PATCH-CLAMP TECHNIQUES; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHOPROTEINS; PHOSPHORYLATION; PURKINJE CELLS; RATS; RATS, WISTAR; RECEPTORS, GABA-A; RECEPTORS, GABA-B; SIGNAL TRANSDUCTION;

EID: 0037095666     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-10-03969.2002     Document Type: Article

References (45)

1. Aiba A, Kano M, Chen C, Stanton ME, Fox GD, Herrup K, Zwingman TA, Tonegawa S (1994) Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell 7:377-388.
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. Blitzer RD, Wong T, Nouranifar R, Iyengar R, Landau EM (1995) Postsynaptic cAMP pathway gates early LTP in hippocampal CA1 region. Neuron 15:1403-1414.
4. Blitzer RD, Connor JH, Brown GP, Wong T, Shenolikar S, Iyengar R, Landau EM (1998) Gating of CaMKII by cAMP-regulated protein phosphatase activity during LTP. Science 280:1940-1942.
5. Braun AP, Schulman H (1995) The multifunctional calcium/calmodulin-dependent protein kinase: from form to function. Annu Rev Physiol 57:417-445.
6. Calabresi P, Gubellini P, Centonze D, Picconi B, Bernardi G, Chergui K, Svenningsson P, Fienberg AA, Greengard P (2000) Dopamine and cAMP-regulated phosphoprotein 32 kDa controls both striatal long-term depression and long-term potentiation, opposing forms of synaptic plasticity. J Neurosci 20:8443-8451.
7. Conquet F, Bashir ZI, Davies CH, Daniel H, Ferraguti F, Bordi F, Franz Bacon K, Reggiani A, Matarese V, Conde F (1994) Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1. Nature 372:237-243.
8. Cooper DM, Mons N, Karpen JW (1995) Adenylyl cyclases and the interaction between calcium and cAMP signalling. Nature 374:421-424.
9. Ehrlich ME, Kurihara T, Greengard P (1990) Rat DARPP-32: cloning, sequencing, and characterization of the cDNA. J Mol Neurosci 2:1-10.
10. Fukunaga K, Stoppini L, Miyamoto E, Muller D (1993) Long-term potentiation is associated with an increased activity of Ca2+/calmodulin-dependent protein kinase II. J Biol Chem 268:7863-7867.
11. Giese KP, Fedorov NB, Filipkowski RK, Silva AJ (1998) Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. Science 279:870-873.
12. Greengard P, Allen PB, Nairn AC (1999) Beyond the dopamine receptor: the DARPP-32/protein phosphatase-1 cascade. Neuron 23:435-447.
13. Hansel C, Linden DJ, D'Angelo E (2001) Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum. Nat Neurosci 4:467-475.
14. 2+ is the crucial step for the potentiation of IPSCs in the cultured cerebellar Purkinje cells of the rat. J Physiol (Lond) 497:611-627.
15. 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.
16. Hemmings Jr HC, Greengard P, Tung HY, Cohen P (1984) DARPP-32, a dopamine-regulated neuronal phosphoprotein, is a potent inhibitor of protein phosphatase-1. Nature 310:503-505.
17. Hirano T, Kasono K (1993) Spatial distribution of excitatory and inhibitory synapses on a Purkinje cell in a rat cerebellar culture. J Neurophysiol 70:1316-1325.
18. Ingebritsen TS, Cohen P (1983) Protein phosphatases: properties and role in cellular regulation. Science 221:331-338.
19. Ito M (2001) Cerebellar long-term depression: characterization, signal transduction, and functional roles. Physiol Rev 81:1143-1195.
20. Jones MV, Westbrook GL (1997) Shaping of IPSCs by endogenous calcineurin activity. J Neurosci 17:7626-7633.
21. Kano M (1995) Plasticity of inhibitory synapses in the brain: a possible memory mechanism that has been overlooked. Neurosci Res 21: 177-182.
22. Kano M, Konnerth A (1992) Potentiation of GABA-mediated currents by cAMP-dependent protein kinase. NeuroReport 3:563-566.
23. Kano M, Rexhausen U, Dreessen J, Konnerth A (1992) Synaptic excitation produces a long-lasting rebound potentiation of inhibitory synaptic signals in cerebellar Purkinje cells. Nature 356:601-604.
24. 2+/calmodulin-dependent kinase II. Proc Natl Acad Sci USA 93:13351-13356.
25. B receptors in Purkinje neuron. Neuron 27:339-347.
26. 2+ release are involved in the induction of long-term potentiation at visual cortical inhibitory synapses. J Neurosci 16:6342-6352.
27. Kwon YG, Huang HB, Desdouits F, Girault JA, Greengard P, Nairn AC (1997) Characterization of the interaction between DARPP-32 and protein phosphatase 1 (PP-1): DARPP-32 peptides antagonize the interaction of PP-1 with binding proteins. Proc Natl Acad Sci USA 94:3536-3541.
28. Lee HK, Barbarosie M, Kameyama K, Bear MF, Huganir RL (2000) Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature 405:955-959.
29. Lisman JE, Zhabotinsky AM (2001) A model of synaptic memory: a CaMKII/ PP1 switch that potentiates transmission by organizing an AMPA receptor anchoring assembly. Neuron 31:191-201.
30. MacDonald BJ, Moss SJ (1994) Differential phosphorylation of intracellular domains of gamma-aminobutyric acid type A receptor subunits by calcium/calmodulin type 2-dependent protein kinase and cGMP-dependent protein kinase. J Biol Chem 269:18111-18117.
31. Makhinson M, Chotiner JK, Watson JB, O'Dell TJ (1999) Adenylyl cyclase activation modulates activity-dependent changes in synaptic strength and Ca2+/calmodulin-dependent kinase II autophosphorylation. J Neurosci 19:2500-2510.
32. Malenka RC (1994) Synaptic plasticity in the hippocampus: LTP and LTD. Cell 78:535-538.
33. Malenka RC, Nicoll RA (1999) Long-term potentiation: a decade of progress? Science 285:1870-1874.
34. Miyashita T, Kubo Y (2000) Extracellular Ca2+ sensitivity of mGluR1alpha induces an increase in the basal cAMP level by direct coupling with Gs protein in transfected CHO cells. Receptors Channels 7:77-91.
35. Moss SJ, Smart TG (1996) Modulation of amino acid-gated ion channels by protein phosphorylation. Int Rev Neurobiol 39:1-52.
36. Mulkey RM, Endo S, Shenolikar S, Malenka RC (1994) Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369:486-488.
37. Nusser Z, Hajos N, Somogyi P, Mody I (1998) Increased number of synaptic GABA(A) receptors underlies potentiation at hippocampal inhibitory synapses. Nature 395:172-177.
38. Oda Y, Kawasaki K, Morita M, Korn H, Matsui H (1998) Inhibitory long-term potentiation underlies auditory conditioning of goldfish escape behavior. Nature 394:182-185.
39. Otmakhova NA, Otmakhov N, Mortenson LH, Lisman JE (2000). Inhibition of the cAMP pathway decreases early long-term potentiation at CA1 hippocampal synapses. J Neurosci 20:4446-4451.
40. Schalling M, Djurfeldt M, Hokfelt T, Ehrlich M, Kurihara T, Greengard P (1990) Distribution and cellular localization of DARPP-32 mRNA in rat brain. Brain Res Mol Brain Res 7:139-149.
41. Shigemoto R, Abe T, Nomura S, Nakanishi S, Hirano T (1994) Antibodies inactivating mGluR1 metabotropic glutamate receptor block long-term depression in cultured Purkinje cells. Neuron 12:1245-1255.
42. Smart TG (1997) Regulation of excitatory and inhibitory neurotransmitter-gated ion channels by protein phosphorylation. Curr Opin Neurobiol 7:358-367.
43. Soderling TR (2000) CaM-kinases: modulators of synaptic plasticity. Curr Opin Neurobiol 10:375-380.
44. Strack S, Barban MA, Wadzinski BE, Colbran RJ (1997) Differential inactivation of postsynaptic density-associated and soluble Ca2+/calmodulin-dependent protein kinase II by protein phosphatases 1 and 2A. J Neurochem 68:2119-2128.
45. Wong ST, Athos J, Figueroa XA, Pineda VV, Schaefer ML, Chavkin CC, Muglia LJ, Storm DR (1999) Calcium-stimulated adenylyl cyclase activity is critical for hippocampus-dependent long-term memory and late phase LTP. Neuron 23:787-798.