Co-induction of LTP and LTD and its regulation by protein kinases and phosphatases

Journal of Neurophysiology

Volumn 103, Issue 5, 2010, Pages 2737-2746

  Grey, Kathryn B ^a   Burrell, Brian D ^a  

^a UNIVERSITY OF SOUTH DAKOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

7 CHLOROKYNURENIC ACID; AMPA RECEPTOR ANTAGONIST; BOTULINUM TOXIN; CALCINEURIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM ION; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; DIZOCILPINE; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; GLUTAMIC ACID; GLYCINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; OKADAIC ACID; PHOSPHATASE; PROTEIN KINASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CALCIUM CELL LEVEL; CELL STIMULATION; CONTROLLED STUDY; DEPOLARIZATION; ENDOCYTOSIS; ENZYME ACTIVATION; ENZYME REGULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; LEECH; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESSURE; PRESSURE CHAMBER; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; SYNAPTIC TRANSMISSION;

ANIMALS; CALCIUM; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENDOCYTOSIS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; LEECHES; LONG-TERM POTENTIATION; LONG-TERM SYNAPTIC DEPRESSION; MECHANORECEPTORS; MICROELECTRODES; NEURONS; PHOSPHOPROTEIN PHOSPHATASES; PRESSURE; PRESYNAPTIC TERMINALS; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTIC TRANSMISSION; TIME FACTORS;

EID: 77953005418     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01112.2009     Document Type: Article

References (74)

1. Antonov I, Ha T, Antonova I, Moroz LL, Hawkins RD. Role of nitric oxide in classical conditioning of siphon withdrawal in Aplysia. J Neurosci 27: 10993-11002, 2007.
2. Anwyl R. Induction and expression mechanisms of postsynaptic NMDA receptor-independent homosynaptic long-term depression. Prog Neurobiol 78: 17-37, 2006.
3. Balschun D, Wolfer DP, Bertocchini F, Barone V, Conti A, Zuschratter W, Missiaen L, Lipp HP, Frey JU, Sorrentino V. Deletion of the ryanodine receptor type 3 (RyR3) impairs forms of synaptic plasticity and spatial learning. EMBO J 18: 5264-5273, 1999.
4. Beattie EC, Carroll RC, Yu X, Morishita W, Yasuda H, von Zastrow M, Malenka RC. Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nat Neurosci 3: 1291-1300, 2000.
5. Beck A, Lohr C, Deitmer JW. Calcium transients in subcompartments of the leech Retzius neuron as induced by single action potentials. J Neurobiol 48: 1-18, 2001.
6. Bi GQ, Poo MM. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18: 10464-10472, 1998.
7. Blitzer RD, Connor JH, Brown GP, Wong T, Shenolikar S, Iyengar R, Landau EM. Gating of CaMKII by cAMP-regulated protein phosphatase activity during LTP. Science 280: 1940-1942, 1998.
8. Brockie PJ, Mellem JE, Hills T, Madsen DM, Maricq AV. The C. elegans glutamate receptor subunit NMR-1 is required for slow NMDA-activated currents that regulate reversal frequency during locomotion. Neuron 31: 617-630, 2001.
9. Bruns D, Engers S, Yang C, Ossig R, Jeromin A, Jahn R. Inhibition of transmitter release correlates with the proteolytic activity of tetanus toxin and botulinus toxin A in individual cultured synapses of Hirudo medicinalis. J Neurosci 17: 1898-1910, 1997.
10. Burrell BD, Sahley CL. Multiple forms of long-term potentiation and long-term depression converge on a single interneuron in the leech CNS. J Neurosci 24: 4011-4019, 2004.
11. Burrell BD, Sahley CL. Serotonin mediates learning-induced potentiation of excitability. J Neurophysiol 94: 4002-4010, 2005.
12. Butts DA, Kanold PO, Shatz CJ. A burst-based "Hebbian" learning rule at retinogeniculate synapses links retinal waves to activity-dependent refinement. PLoS Biol 5: , 2007.
13. Chang HC, Rongo C. Cytosolic tail sequences and subunit interactions are critical for synaptic localization of glutamate receptors. J Cell Sci 118: 1945-1956, 2005.
14. Chitwood RA, Li Q, Glanzman DL. Serotonin facilitates AMPA-type responses in isolated siphon motor neurons of Aplysia in culture. J Physiol 534: 501-510, 2001.
15. Clapper DL, Lee HC. Inositol trisphosphate induces calcium release from nonmitochondrial stores in sea urchin egg homogenates. J Biol Chem 260: 13947-13954, 1985.
16. Daw MI, Chittajallu R, Bortolotto ZA, Dev KK, Duprat F, Henley JM, Collingridge GL, Isaac JT. PDZ proteins interacting with C-terminal GluR2/3 are involved in a PKC-dependent regulation of AMPA receptors at hippocampal synapses. Neuron 28: 873-886, 2000.
17. 2+ channels in identified neurons. Brain Res 1013: 159-167, 2004.
18. Endo S, Shenolikar S, Eskin A, Zwartjes RE, Byrne JH. Characterization of neuronal protein phosphatases in Aplysia californica. J Neurochem 58: 975-982, 1992.
19. Ezzeddine Y, Glanzman DL. Prolonged habituation of the gill-withdrawal reflex in Aplysia depends on protein synthesis, protein phosphatase activity, and postsynaptic glutamate receptors. J Neurosci 23: 9585-9594, 2003. (Pubitemid 37352058)
20. 2+ influx in presynaptic facilitation. Nature 361: 634-637, 1993.
21. Feldman DE. Synaptic mechanisms for plasticity in neocortex. Annu Rev Neurosci 32: 33-55, 2009.
22. Frey MC, Sprengel R, Nevian T. Activity pattern-dependent long-term potentiation in neocortex and hippocampus of GluA1 (GluR-A) subunit-deficient mice. J Neurosci 29: 5587-5596, 2009.
23. Fukunaga K, Muller D, Ohmitsu M, Bako E, DePaoli-Roach AA, Miyamoto E. Decreased protein phosphatase 2A activity in hippocampal longterm potentiation. J Neurochem 74: 807-817, 2000.
24. 2+ release in Aplysia bag cell neurons requires interaction between mitochondrial and endoplasmic reticulum stores. J Neurophysiol 100: 24-37, 2008.
25. Giese KP, Fedorov NB, Filipkowski RK, Silva AJ. Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. Science 279: 870-873, 1998.
26. Graupner M, Brunel N. STDP in a bistable synapse model based on CaMKII and associated signaling pathways. PLoS Comput Biol 3: , 2007.
27. Grey KB, Burrell BD. Forskolin induces NMDA receptor-dependent potentiation at a central synapse in the leech. J Neurophysiol 99: 2719-2724, 2008.
28. Grey KB, Moss BL, Burrell BD. Molecular identification and expression of the NMDA receptor NR1 subunit in the leech. Invert Neurosci 9: 11-20, 2009.
29. Gu XN. Effect of conduction block at axon bifurcations on synaptic transmission to different postsynaptic neurones in the leech. J Physiol 441: 755-778, 1991.
30. Ha TJ, Kohn AB, Bobkova YV, Moroz LL. Molecular characterization of NMDA-like receptors in Aplysia and Lymnaea: relevance to memory mechanisms. Biol Bull 210: 255-270, 2006.
31. + current in the pleural sensory neurons of Aplysia by serotonin and cAMP: implications for spike broadening. Proc Natl Acad Sci USA 89: 11476-11480, 1992.
32. Ivanov AI, Calabrese RL. Spike-mediated and graded inhibitory synaptic transmission between leech interneurons: evidence for shared release sites. J Neurophysiol 96: 235-251, 2006.
33. Jin I, Hawkins RD. Presynaptic and postsynaptic mechanisms of a novel form of homosynaptic potentiation at Aplysia sensory-motor neuron synapses. J Neurosci 23: 7288-7297, 2003. (Pubitemid 36999518)
34. Kapur A, Yeckel MF, Gray R, Johnston D. L-Type calcium channels are required for one form of hippocampal mossy fiber LTP. J Neurophysiol 79: 2181-2190, 1998. (Pubitemid 28183347)
35. Kessels HW, Malinow R. Synaptic AMPA receptor plasticity and behavior. Neuron 61: 340-350, 2009.
36. Kleinhaus AL, Angstadt JD. Diversity and modulation of ionic conductances in leech neurons. J Neurobiol 27: 419-433, 1995.
37. Kristan WB Jr, Calabrese RL, Friesen WO. Neuronal control of leech behavior. Prog Neurobiol 76: 279-327, 2005.
38. Li Q, Burrell BD. CNQX and AMPA inhibit electrical synaptic transmission: a potential interaction between electrical and glutamatergic synapses. Brain Res 1228: 43-57, 2008.
39. Li Q, Burrell BD. Two forms of long-term depression in a polysynaptic pathway in the leech CNS: one NMDA receptor-dependent and the other cannabinoid-dependent. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 195: 831-841, 2009.
40. 2+ from postsynaptic intracellular stores, postsynaptic exocytosis, and modulation of postsynaptic AMPA receptor efficacy. J Neurosci 25: 5623-5637, 2005.
41. Lin XY, Glanzman DL. Hebbian induction of long-term potentiation of Aplysia sensorimotor synapses: partial requirement for activation of an NMDA-related receptor. Proc Biol Sci 255: 215-221, 1994.
42. Lin XY, Glanzman DL. Effect of interstimulus interval on pairing-induced LTP of Aplysia sensorimotor synapses in cell culture. J Neurophysiol 77: 667-674, 1997.
43. Luscher C, Xia H, Beattie EC, Carroll RC, von Zastrow M, Malenka RC, Nicoll RA. Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron 24: 649-658, 1999.
44. Lynch G, Larson J, Kelso S, Barrionuevo G, Schottler F. Intracellular injections of EGTA block induction of hippocampal long-term potentiation. Nature 305: 719-721, 1983. (Pubitemid 13021524)
45. Massey PV, Bashir ZI. Long-term depression: multiple forms and implications for brain function. Trends Neurosci 30: 176-184, 2007.
46. Miyamoto E. Molecular mechanism of neuronal plasticity: induction and maintenance of long-term potentiation in the hippocampus. J Pharmacol Sci 100: 433-442, 2006.
47. Montecucco C, Schiavo G. Structure and function of tetanus and botulinum neurotoxins. Q Rev Biophys 28: 423-472, 1995. (Pubitemid 26015975)
48. Montgomery JM, Pavlidis P, Madison DV. Pair-recordings reveal all-silent synaptic connections and the postysnaptic expression of long term potentiation. Neuron 29: 691-701, 2001.
49. Moroz LL, Edwards JR, Puthanveettil SV, Kohn AB, Ha T, Heyland A, Knudsen B, Sahni A, Yu F, Liu L, Jezzini S, Lovell P, Iannucculli W, Chen M, Nguyen T, Sheng H, Shaw R, Kalachikov S, Panchin YV, Farmerie W, Russo JJ, Ju J, Kandel ER. Neuronal transcriptome of Aplysia: neuronal compartments and circuitry. Cell 127: 1453-1467, 2006.
50. Mulkey RM, Herron CE, Malenka RC. An essential role for protein phosphatases in hippocampal long-term depression. Science 261: 1051-1055, 1993.
51. Murphy GG, Glanzman DL. Enhancement of sensorimotor connections by conditioning-related stimulation in Aplysia depends upon postsynaptic Ca2+. Proc Natl Acad Sci USA 93: 9931-9936, 1996. (Pubitemid 126585338)
52. Murphy GG, Glanzman DL. Mediation of classical conditioning in Aplysia californica by long-term potentiation of sensorimotor synapses. Science 278: 467-471, 1997.
53. Murphy GG, Glanzman DL. Cellular analog of differential classical conditioning in Aplysia: disruption by the NMDA receptor antagonist DL-2-amino-5-phosphonovalerate. J Neurosci 19: 10595-10602, 1999.
54. Nayak A, Zastrow DJ, Lickteig R, Zahniser NR, Browning MD. Maintenance of late-phase LTP is accompanied by PKA-dependent increase in AMPA receptor synthesis. Nature 394: 680-683, 1998.
55. 2+ signaling in spike-timing-dependent plasticity. J Neurosci 26: 11001-11013, 2006.
56. Nishiyama M, Hong K, Mikoshiba K, Poo MM, Kato K. Calcium stores regulate the polarity and input specificity of synaptic modification. Nature 408: 584-588, 2000.
57. Pi HJ, Lisman JE. Coupled phosphatase and kinase switches produce the tristability required for long-term potentiation and long-term depression. J Neurosci 28: 13132-13138, 2008.
58. Ryan TJ, Emes RD, Grant SGN, Komiyama NH. Evolution of NMDA receptor interaction domains: implications for organisation of synaptic signaling complexes. BMC Neurosci 9: 6, 2008.
59. Ryan TJ, Grant SGN. The origin and evolution of synapses. Nat Rev Neurosci 10: 701-712.
60. Siddall ME, Trontelj P, Utevsky SY, Nkamany M, Macdonald KS. Diverse molecular data demonstrate that commercially available medicinal leeches are not Hirudo medicinalis. Proc Biol Sci 274: 1481-1487, 2007.
61. Sutko L, Airey JA, Welch W, Ruest L. The pharmacology of ryanodine and related compounds. Pharmacol Rev 49: 53-98, 1997.
62. Trueta C, Sanchez-Armass S, Morales MA, De Miguel FF. Calcium-induced calcium release contributes to somatic secretion of serotonin in leech Retzius neurons. J Neurobiol 61: 309-316, 2004.
63. van Woerden GM, Hoebeek FE, Gao Z, Nagaraja RY, Hoogenraad CC, Kushner SA, Hansel C, De Zeeuw CI, Elgersma Y. betaCaMKII controls the direction of plasticity at parallel fiber-Purkinje cell synapses. Nat Neurosci 12: 823-825, 2009.
64. Vargas R, Cifuentes F, Morales MA. Differential contribution of extracellular and intracellular calcium sources to basal transmission and long-term potentiation in the sympathetic ganglion of the rat. Dev Neurobiol 67: 589-602, 2007.
65. Walker CS, Brockie PJ, Madsen DM, Francis MM, Zheng Y, Koduri S, Mellem JE, Strutz-Seebohm N, Maricq AV. Reconstitution of invertebrate glutamate receptor function depends on stargazin-like proteins. Proc Natl Acad Sci USA 103: 10781-10786, 2006.
66. Wessel R, Kristan WB, Jr, Kleinfeld D. Supralinear summation of synaptic inputs by an invertebrate neuron: dendritic gain is mediated by an "inward rectifier" K(+) current. J Neurosci 19: 5875-5888, 1999.
67. Willoughby D, Thomas R, Schwiening C. The effects of intracellular pH changes on resting cytosolic calcium in voltage-clamped snail neurones. J Physiol 530: 405-416, 2001.
68. Xu X, Bhat MB, Nishi M, Takeshima H, Ma J. Molecular cloning of cDNA encoding a drosophila ryanodine receptor and functional studies of the carboxyl-terminal calcium release channel. Biophys J 78: 1270-1281, 2000. (Pubitemid 30141554)
69. Xu Z, Chen RQ, Gu QH, Yan JZ, Wang SH, Liu SY, Lu W. Metaplastic regulation of long-term potentiation/long-term depression threshold by activity-dependent changes of NR2A/NR2B ratio. J Neurosci 29: 8764-8773, 2009.
70. Yang HW, Hu XD, Zhang HM, Xin WJ, Li MT, Zhang T, Zhou LJ, Liu XG. Roles of CaMKII, PKA, and PKC in the induction and maintenance of LTP of C-fiber-evoked field potentials in rat spinal dorsal horn. J Neurophysiol 91: 1122-1133, 2004.
71. 2+/calmodulin-dependent protein kinase II from postsynaptic densities. FEBS Lett 446: 239-242, 1999.
72. Zannat MT, Locatelli F, Rybak J, Menzel R, Leboulle G. Identification and localisation of the NR1 sub-unit homologue of the NMDA glutamate receptor in the honeybee brain. Neurosci Lett 398: 274-279, 2006.
73. Zhabotinsky AM. Bistability in the Ca(2+)/calmodulin-dependent protein kinase-phosphatase system. Biophys J 79: 2211-2221, 2000.
74. Zheng Z, Keifer J. PKA has a critical role in synaptic delivery of GluR1- and GluR4-containing AMPARs during initial stages of acquisition of in vitro classical conditioning.. J Neurophysiol 101: 2539-2549, 2009.