Genetic disruption of protein kinase a anchoring reveals a role for compartmentalized kinase signaling in theta-burst long-term potentiation and spatial memory

Journal of Neuroscience

Volumn 27, Issue 38, 2007, Pages 10278-10288

  Nie, Ting ^a,c   McDonough, Conor B ^a   Huang, Ted ^a   Nguyen, Peter V ^b   Abel, Ted ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

A kinase anchoring proteins; cAMP dependent protein kinase; Hippocampus; LTP; Spatial memory; Synaptic plasticity

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; DOXYCYCLINE; PROTEIN HT31; UNCLASSIFIED DRUG;

ANALYSIS OF VARIANCE; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DNA MODIFICATION; DRUG INHIBITION; FEMALE; GENE DISRUPTION; GENE EXPRESSION; GENE REPRESSION; GENOTYPE; HIPPOCAMPUS; IN SITU HYBRIDIZATION; LONG TERM POTENTIATION; MALE; MEMORY CONSOLIDATION; MOUSE; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPATIAL MEMORY; SYNAPSE;

AMINO ACID SEQUENCE; ANIMALS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; FEMALE; LONG-TERM POTENTIATION; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; SIGNAL TRANSDUCTION; SPATIAL BEHAVIOR; SYNAPSES;

EID: 34548860619     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1602-07.2007     Document Type: Article

References (48)

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. Alto NM, Soderling SH, Hoshi N, Langeberg LK, Fayos R, Jennings PA, Scott JD (2003) Bioinformatic design of A-kinase anchoring protein-in silico: a potent and selective peptide antagonist of type II protein kinase A anchoring. Proc Natl Acad Sci USA 100:4445-4450.
3. 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.
4. Buzsaki G (2002) Theta oscillations in the hippocampus. Neuron 33:325-340.
5. Diviani D, Abuin L, Cotecchia S, Pansier L (2004) Anchoring of both PKA and 14-3-3 inhibits the Rho-GEF activity of the AKAP-Lbc signaling complex. EMBO J 23:2811-2820.
6. Duffy SN, Nguyen PV (2003) Postsynaptic application of a peptide inhibitor of cAMP-dependent protein kinase blocks expression of long-lasting synaptic potentiation in hippocampal neurons. J Neurosci 23:1142-1150.
7. Fink MA, Zakhary DR, Mackey JA, Desnoyer RW, Apperson-Hansen C, Damron DS, Bond M (2001) AKAP-mediated targeting of protein kinase A regulates contractility in cardiac myocytes. Circ Res 88:291-297.
8. Frey U, Morris RG (1997) Synaptic tagging and long-term potentiation. Nature 385:533-536.
9. Frey U, Krug M, Reymann KG, Matthies H (1988) Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res 452:57-65.
10. Frey U, Huang YY, Kandel ER (1993) Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260:1661-1664.
11. Gruart A, Munoz MD, Delgado-Garcia JM (2006) Involvement of the CA3-CA1 synapse in the acquisition of associative learning in behaving mice. J Neurosci 26:1077-1087.
12. Huang T, McDonough CB, Abel T (2006) Compartmentalized PKA signaling events are required for synaptic tagging and capture during hippocampal late-phase long-term potentiation. Eur J Cell Biol 85:635-642.
13. Huang YY, 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.
14. Huang YY, Zakharenko SS, Schoch S, Kaeser PS, Janz R, Sudhof TC, Siegelbaum SA, Kandel ER (2005) Genetic evidence for a protein-kinase-A-mediated presynaptic component in NMDA-receptor-dependent forms of long-term synaptic potentiation. Proc Natl Acad Sci USA 102:9365-9370.
15. Klussmann E, Edemir B, Pepperle B, Tamma G, Henn V, Klauschenz E, Hundsrucker C, Maric K, Rosenthal W (2001) Ht31: the first protein kinase A anchoring protein to integrate protein kinase A and Rho signaling. FEBS Lett 507:264-268.
16. Lattal KM, Mullen MT, Abel T (2003) Extinction, renewal, and spontaneous recovery of a spatial preference in the water maze. Behav Neurosci 117:1017-1028.
17. Lester LB, Langeberg LK, Scott JD (1997) Anchoring of protein kinase A facilitates hormone-mediated insulin secretion. Proc Natl Acad Sci USA 94:14942-14947.
18. Liu J, Hu JY, Schacher S, Schwartz JH (2004) The two regulatory subunits of Aplysia cAMP-dependent protein kinase mediate distinct functions in producing synaptic plasticity. J Neurosci 24:2465-2474.
19. Lynch G, Larson J, Kelso S, Barrionuevo G, Schottler F (1983) Intracellular injections of EGTA block induction of hippocampal long-term potentiation. Nature 305:719-721.
20. Lynch MA (2004) Long-term potentiation and memory. Physiol Rev 84:87-136.
21. Malenka RC, Nicoll RA (1999) Long-term potentiation - a decade of progress? Science 285:1870-1874.
22. Martin SJ, Grimwood PD, Morris RG (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649-711.
23. Matthies H, Frey U, Reymann K, Krug M, Jork R, Schroeder H (1990) Different mechanisms and multiple stages of LTP. Adv Exp Med Biol 268:359-368.
24. Mayford M, Bach ME, Huang YY, Wang L, Hawkins RD, Kandel ER (1996) Control of memory formation through regulated expression of a CaMKII transgene. Science 274:1678-1683.
25. 2+-dependent synaptic activity. J Neurosci 26:11670-11681.
26. Moita MA, Lamprecht R, Nader K, LeDoux JE (2002) A-kinase anchoring proteins in amygdala are involved in auditory fear memory. Nat Neurosci 5:837-838.
27. Nguyen PV, Woo NH (2003) Regulation of hippocampal synaptic plasticity by cyclic AMP-dependent protein kinases. Prog Neurobiol 71:401-437.
28. Nguyen PV, Abel T, Kandel ER (1994) Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265:1104-1107.
29. Nijholt IM, Ostroveanu A, de Bruyn M, Luiten PGM, Eisel ULM, Van der Zee EA (2007) Both exposure to a novel context and associative learning induce an upregulation of AKAP150 protein in mouse hippocampus. Neurobiol Learn Mem 87:693-696.
30. Powell CM, Schoch S, Monteggia L, Barrot M, Matos MF, Feldmann N, Sudhof TC, Nestler EJ (2004) The presynaptic active zone protein RIM1alpha is critical for normal learning and memory. Neuron 42:143-153.
31. Reymann KG, Frey JU (2007) The late maintenance of hippocampal LTP: requirements, phases, "synaptic tagging," "late- associativity" and implications. Neuropharmacology 52:24-40.
32. 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.
33. Sajikumar S, Navakkode S, Frey JU (2007) Identification of compartment-and process-specific molecules required for "synaptic tagging" during long-term potentiation and long-term depression in hippocampal CA1. J Neurosci 27:5068-5080.
34. Schenk F, Morris RG (1985) Dissociation between components of spatial memory in rats after recovery from the effects of retrohippocampal lesions. Exp Brain Res 58:11-28.
35. Schmitt JM, Guire ES, Saneyoshi T, Soderling TR (2005) Calmodulin-dependent kinase kinase/calmodulin kinase I activity gates extracellular-regulated kinase-dependent long-term potentiation. J Neurosci 25:1281-1290.
36. Schulz PE, Cook EP, Johnston D (1994) Changes in paired-pulse facilitation suggest presynaptic involvement in long-term potentiation. J Neurosci 14:5325-5337.
37. Schulz PE, Cook EP, Johnston D (1995) Using paired-pulse facilitation to probe the mechanisms for long-term potentiation (LTP). J Physiol (Paris) 89:3-9.
38. Skalhegg BS, Tasken K (2000) Specificity in the cAMP/PKA signaling pathway. Differential expression, regulation, and subcellular localization of subunits of PKA. Front Biosci 5:D678-D693.
39. Skeberdis VA, Chevaleyre V, Lau CG, Goldberg JH, Pettit DL, Suadicani SO, Lin Y, Bennett MV, Yuste R, Castillo PE, Zukin RS (2006) Protein kinase A regulates calcium permeability of NMDA receptors. Nat Neurosci 9:501-510.
40. Smith FD, Scott JD (2006) Anchored cAMP signaling: onward and upward - a short history of compartmentalized cAMP signal transduction. Eur J Cell Biol 85:585-592.
41. Snyder EM, Colledge M, Crozier RA, Chen WS, Scott JD, Bear MF (2005) Role for A kinase-anchoring proteins (AKAPS) in glutamate receptor trafficking and long term synaptic depression. J Biol Chem 280:16962-16968.
42. Tavalin SJ, Colledge M, Hell JW, Langeberg LK, Huganir RL, Scott JD (2002) Regulation of GluR1 by the A-kinase anchoring protein 79 (AKAP79) signaling complex shares properties with long-term depression. J Neurosci 22:3044-3051.
43. Vijayaraghavan S, Goueli SA, Davey MP, Carr DW (1997) Protein kinase A-anchoring inhibitor peptides arrest mammalian sperm motility. J Biol Chem 272:4747-4752.
44. 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.
45. Whitlock JR, Heynen AJ, Shuler MG, Bear MF (2006) Learning induces long-term potentiation in the hippocampus. Science 313:1093-1097.
46. Woo NH, Duffy SN, Abel T, Nguyen PV (2000) Genetic and pharmacological demonstration of differential recruitment of cAMP-dependent protein kinases by synaptic activity. J Neurophysiol 84:2739-2745.
47. Young JZ, Nguyen PV (2005) Homosynaptic and heterosynaptic inhibition of synaptic tagging and capture of long-term potentiation by previous synaptic activity. J Neurosci 25:7221-7231.
48. Zakharenko SS, Patterson SL, Dragatsis I, Zeitlin SO, Siegelbaum SA, Kandel ER, Morozov A (2003) Presynaptic BDNF required for a presynaptic but not postsynaptic component of LTP at hippocampal CA1-CA3 synapses. Neuron 39:975-990.