Inhibition of the cAMP pathway decreases early long-term potentiation at CA1 hippocampal synapses

Journal of Neuroscience

Volumn 20, Issue 12, 2000, Pages 4446-4451

  Otmakhova, Nonna A ^a   Otmakhov, Nikolai ^a   Mortenson, Lindsay H ^a   Lisman, John E ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

Adenylyl cyclase; CA1; CAMP dependent protein kinase; Early LTP; H89; PKI(6 22) amide; SQ 22536

Indexed keywords

9 (TETRAHYDRO 2 FURYL)ADENINE; ADENYLATE CYCLASE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HIPPOCAMPUS; LONG TERM POTENTIATION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; SYNAPSE; TETANUS;

EID: 0034660162     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-12-04446.2000     Document Type: Article

References (34)

1. Abel T, Nguyen PV, Barad M, Deuel TA, Kandel ER, Bourtchouladze R (1997) Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88:615-626.
2. Abraham WC, Bear MF (1996) Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 19:126-130.
3. Barad M, Bourtchouladze R, Winder DG, Golan H, Kandel E. (1998) Rolipram, a type IV-specific phosphodiesterase inhibitor, facilitates the establishment of long-lasting long-term potentiation and improves memory. Proc Natl Acad Sci USA 95:15020-15025.
4. 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.
5. 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.
6. Bolshakov VY, Golan H, Kandel ER, Siegelbaum SA (1997) Recruitment of new sites of synaptic transmission during the cAMP-dependent late phase of LTP at CA3-CA1 synapses in the hippocampus. Neuron 19:635-651.
7. Bourtchouladze R, Abel T, Berman N, Gordon R, Lapidus K, Kandel ER (1998) Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA. Learn Mem 5:365-374.
8. Brandon EP, Zhuo M, Huang YY, Qi M, Gerhold KA, Burton KA, Kandel ER, McKnight GS, Idzerda RL (1995) Hippocampal long-term depression and depotentiation are defective in mice carrying a targeted disruption of the gene encoding the RI beta subunit of cAMP-dependent protein kinase. Proc Natl Acad Sci USA 92:8851-8855.
9. Carr DW, Stofko-Hahn RE, Fraser ID, Cone RD, Scott JD (1992) Localization of the cAMP-dependent protein kinase to the postsynaptic densities by A-kinase anchoring proteins. Characterization of AKAP 79. J Biol Chem 267:16816-16823.
10. Chetkovich DM, Sweatt JD (1993) NMDA receptor activation increases cyclic Amp in area Ca1 of the hippocampus via calcium/calmodulin stimulation of adenylyl cyclase. J Neurochem 61:1933-1942.
11. Chijiwa T, Mishima A, Hagiwara M, Sano M, Hayashi K, Inoue T, Naito K, Toshioka T, Hidaka H (1990) Inhibition of forskolin-induced neurite outgrowth and protein phosphorylation by a newly synthesized selective inhibitor of cyclic AMP-dependent protein kinase. N-[2-(p-bromocinnamylamino)ethyl]-5- isoquinolinesulfonamide (H-89), of PC12D pheochromocytoma cells. J Biol Chem 265:5267-5272.
12. Coussens CM, Teyler TJ (1996) Protein kinase and phosphatase activity regulate the form of synaptic plasticity expressed. Synapse 24:97-103.
13. Frey U, Huang YY, Kandel ER (1993) Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260:1661-1664.
14. Huang Y-Y, Kandel ER (1994) Recruitment of long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of hippocampus requires repeated tetanization. Learn Mem 1:74-82.
15. Lisman J (1994) The CaM kinase II hypothesis for the storage of synaptic memory. Trends Neurosci 17:406-412.
16. Ma L, Zablow L, Kandel ER, Siegelbaum SA (1999) Cyclic AMP induces functional presynaptic boutons in hippocampal CA3-CA1 neuronal cultures [see comments]. Nat Neurosci 2:24-30.
17. Madison DV, Nicoll RA (1986) Cyclic adenosine 3′,5′-monophosphate mediates beta-receptor actions of noradrenaline in rat hippocampal pyramidal cells. J Physiol (Lond) 372:245-59.
18. Malenka RC, Nicoll RA (1999) Long-term potentiation-A decade of progress? Science 285:1870-1874.
19. Otmakhov N, Griffith LC, Lisman JE (1997) Postsynaptic inhibitors of calcium/calmodulin-dependent protein kinase type II block induction but not maintenance of pairing-induced long-term potentiation. J Neurosci 17:5357-5365.
20. Otmakhov N, Chen H-X, Lisman J (1999) Postynaptically applied cAMP analogs block induction of pairing-induced LTP, possibly by a PKA independent mechanism. Soc Neurosci Abstr 25:989.
21. Otmakhova NA, Lisman JE (1996) D1/D5 dopamine receptor activation increases the magnitude of early long-term potentiation at CA1 hippocampal synapses. J Neurosci 16:7478-7486.
22. Otmakhova NA, Lisman JE (1998) D1/D5 dopamine receptors inhibit depotentiation at CA1 synapses via cAMP-dependent mechanism. J Neurosci 18:1270-1279.
23. + current underlying the slow spike frequency adaptation in hippocampal neurons. Neuron 11:1023-1035.
24. 2+-dependent K+ current, IAHP, by acetylcholine, but not by glutamate, in hippocampal neurons. Pflügers Arch 431:723-728.
25. Qi M, Zhuo M, Skalhegg BS, Brandon EP, Kandel ER, McKnight GS, Idzerda RL (1996) Impaired hippocampal plasticity in mice lacking the Cbeta1 catalytic subunit of cAMP-dependent protein kinase. Proc Natl Acad Sci USA 93:1571-1576.
26. Roberson ED, Sweatt JD (1996) Transient activation of cyclic AMP-dependent protein kinase during hippocampal long-term potentiation. J Biol Chem 271:30436-30441.
27. Rosenmund C, Carr DW, Bergeson SE, Nilaver G, Scott JD, Westbrook GL (1994) Anchoring of protein kinase A is required for modulation of AMPA/kainate receptors on hippocampal neurons. Nature 368:853-856.
28. Sah P, Bekkers JM (1996) Apical dendritic location of slow afterhyperpolarization current in hippocampal pyramidal neurons: implications for the integration of long-term potentiation. J Neurosci 16:4537-4542.
29. Sanes JR, Lichtman JW (1999) Can molecules explain long-term potentiation? Nat Neurosci 2:597-604.
30. Thomas MJ, Moody TD, Makhinson M, O'Dell TJ (1996) Activity-dependent beta-adrenergic modulation of low frequency stimulation induced LTP in the hippocampal CA1 region. Neuron 17:475-482.
31. Westphal RS, Tavalin SJ, Lin JW, Alto NM, Fraser ID, Langeberg LK, Sheng M, Scott JD (1999) Regulation of NMDA receptors by an associated phosphatase-kinase signaling complex. Science 285:93-96.
32. Winder DG, Mansuy IM, Osman M, Moallem TM, Kandel ER (1998) Genetic and pharmacological evidence for a novel, intermediate phase of long-term potentiation suppressed by calcineurin. Cell 92:25-37.
33. 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.
34. Wu ZL, Thomas SA, Villacres EC, Xia Z, Simmons ML, Chavkin C, Palmiter RD, Storm DR (1995) Altered behavior and long-term potentiation in type I adenylyl cyclase mutant mice. Proc Natl Acad Sci USA 92:220-224.