Pentylenetetrazol-Induced Epileptiform Activity Affects Basal Synaptic Transmission and Short-Term Plasticity in Monosynaptic Connections

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Giachello, Carlo Natale Giuseppe ^a   Premoselli, Federica ^a   Montarolo, Pier Giorgio ^a,b   Ghirardi, Mirella ^a,b  

^a UNIVERSITY OF TURIN   (Italy)

^b Istituto Nazionale di Neuroscienze   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE I; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE IV; CYCLIC AMP DEPENDENT PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE; PENTETRAZOLE; SYNAPSIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EPILEPSY; HELIX (SNAIL); IN VITRO STUDY; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; POST TETANIC POTENTIATION; PROTEIN PHOSPHORYLATION; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

ANIMALS; CELL CULTURE TECHNIQUES; COCULTURE TECHNIQUES; EPILEPSY; HELIX (SNAILS); HUMANS; NEURONAL PLASTICITY; NEURONS; PENTYLENETETRAZOLE; PHOSPHORYLATION; SYNAPSINS; SYNAPTIC POTENTIALS; SYNAPTIC TRANSMISSION;

EID: 84874239803     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056968     Document Type: Article

References (128)

1. Altrup U, (2004) Epileptogenicity and epileptic activity: Mechanisms in an invertebrate model nervous system. Curr Drug Targets 5: 473-484.
2. Altrup U, Lehmenkuhler A, Speckmann EJ, (1991) Effects of the hypnotic drug etomidate in a model nervous system (buccal ganglia, Helix pomatia). Comp Biochem Physiol C 99: 579-587.
3. Chalazonitis N, Takeuchi H, (1968) Wide variations in membrane potential induced by metrazol (auto-active nerve fibers of Helix pomatia). C R Séances Soc Biol Fil 162: 1552-1554.
4. Schulze H, Speckmann EJ, Kuhlmann D, Caspers H, (1975) Topography and bioelectrical properties of identifiable neurons in buccal ganglion of Helix pomatia. Neurosci Lett 1: 277-281.
5. Steffens H, (1980) The buccal ganglia of Helix pomatia L. (Gastropoda, Pulmonata). Zoomorphologie 95: 195-212.
6. Altrup U, Speckmann EJ, (1988) Epileptic discharges induced by pentylenetetrazol: changes of shape of dendrites. Brain Res 456: 401-405.
7. Madeja M, Altrup U, Speckmann EJ, (1989) Synchronization of epileptic discharges: temporal coupling of paroxysmal depolarizations in the buccal ganglia of Helix pomatia. Comp Biochem Physiol 94: 585-590.
8. Schulze-Bonhage A, Altrup U, Speckmann EJ, Wittkowski W, (1993) Structure and bioelectricity of single neurons of Helix pomatia in the intact nervous tissue during epileptic activity: Simultaneous evaluations by confocal microscopy and intracellular recordings of membrane potential changes. Comp Biochem Physiol A Mol Integr Physiol 106: 537-545.
9. Speckman EJ, Caspers H, (1973) Paroxysmal depolarization and changes in action potentials induced by pentylenetetrazol in isolated neurons of Helix pomatia. Epilepsia 14: 397-408.
10. Matsumoto H, Marsan CA, (1964) Cellular mechanisms in experimental epileptic seizures. Science 144: 193-194.
11. Prince DA, (1969) Electrophysiology of "epileptic" neurons: spike generation. Electroencephalogr Clin Neurophysiol 26: 476-487.
12. Purpura DP, McMurtry JG, Leonard CF, (1966) Evidence for dendritic origin of spikes without depolarizing prepotentials in hippocampal neurons during and after seizure. J Neurophysiol 29: 954-979.
13. Giachello CNG, Montarolo PG, Ghirardi M, (2012) Synaptic functions of invertebrate varicosities: what molecular mechanisms lie beneath. Neural Plast 2012: 670821.
14. Ghirardi M, Casadio A, Santarelli L, Montarolo PG, (1996) Aplysia hemolymph promotes neurite outgrowth and synaptogenesis of identified Helix neurons in cell culture. Invert Neurosci 2: 41-49.
15. Li L, Chin LS, Shupliakov O, Brodin L, Sihra TS, et al. (1995) Impairment of synaptic vesicle clustering and of synaptic transmission, and increased seizure propensity, in synapsin I-deficient mice. Proc Natl Acad Sci USA 92: 9235-9239.
16. Rosahl TW, Spillane D, Missler M, Herz J, Selig DK, et al. (1995) Essential functions of synapsin-I and synapsin-II in synaptic vesicle regulation. Nature 375: 488-493.
17. Garcia CC, Blair HJ, Seager M, Coulthard A, Tennant S, et al. (2004) Identification of a mutation in synapsin I, a synaptic vesicle protein, in a family with epilepsy. J Med Genet 41: 183-186.
18. Gitler D, Takagishi Y, Feng J, Ren Y, Rodriguiz RM, et al. (2004) Different presynaptic roles of synapsins at excitatory and inhibitory synapses. J Neurosci 24: 11368-11380.
19. Etholm L, Heggelund P, (2009) Seizure elements and seizure element transitions during tonic-clonic seizure activity in the synapsin I/II double knockout mouse: A neuroethological description. Epilepsy Behav 14: 582-590.
20. Fassio A, Patry L, Congia S, Onofri F, Piton A, et al. (2011) SYN1 loss-of-function mutations in autism and partial epilepsy cause impaired synaptic function. Hum Mol Genet 20: 2297-2307.
21. Etholm L, Bahonjic E, Walaas SI, Kao H-T, Heggelund P, (2012) Neuroethologically delineated differences in the seizure behavior of Synapsin 1 and Synapsin 2 knock-out mice. Epilepsy Res 99: 252-259.
22. Cesca F, Baldelli P, Valtorta F, Benfenati F, (2010) The synapsins: Key actors of synapse function and plasticity. Prog Neurobiol 91: 313-348.
23. Benfenati F, Bahler M, Jahn R, Greengard P, (1989) Interactions of synapsin I with small synaptic vesicles: distinct sites in synapsin I bind to vesicle phospholipids and vesicle proteins. J Cell Biol 108: 1863-1872.
24. Benfenati F, Valtorta F, Chieregatti E, Greengard P, (1992) Interaction of free and synaptic vesicle bound synapsin-I with F-actin. Neuron 8: 377-386.
25. Greengard P, Valtorta F, Czernik AJ, Benfenati F, (1993) Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 259: 780-785.
26. Huttner WB, Schiebler W, Greengard P, De Camilli P, (1983) Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J Cell Biol 96: 1374-1388.
27. Matsubara M, Kusubata M, Ishiguro K, Uchida T, Titani K, et al. (1996) Site-specific phosphorylation of synapsin I by mitogen-activated protein kinase and Cdk5 and its effects on physiological functions. J Biol Chem 271: 21108-21113.
28. Pieribone VA, Shupliakov O, Brodin L, Hilfiker-Rothenfluh S, Czernik AJ, et al. (1995) Distinct pools of synaptic vesicles in neurotransmitter release. Nature 375: 493-497.
29. Rizzoli SO, Betz WJ, (2005) Synaptic vesicle pools. Nat Rev Neurosci 6: 57-69.
30. Schweizer FE, Ryan TA, (2006) The synaptic vesicle: cycle of exocytosis and endocytosis. Curr Opin Neurobiol 16: 298-304.
31. Richards DA, Guatimosim C, Betz WJ, (2000) Two endocytic recycling routes selectively fill two vesicle pools in frog motor nerve terminals. Neuron 27: 551-559.
32. Kuromi H, Kidokoro Y, (2000) Tetanic stimulation recruits vesicles from reserve pool via a cAMP-mediated process in Drosophila synapses. Neuron 27: 133-143.
33. Kuromi H, Kidokoro Y, (2003) Two synaptic vesicle pools, vesicle recruitment and replenishment of pools at the Drosophila neuromuscular junction. J Neurocytol 32: 551-565.
34. Gaffield MA, Rizzoli SO, Betz WJ, (2006) Mobility of synaptic vesicles in different pools in resting and stimulated frog motor nerve terminals. Neuron 51: 317-325.
35. Rosenmund C, Stevens CF, (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16: 1197-1207.
36. Sakaba T, Neher E, (2001) Preferential potentiation of fast-releasing synaptic vesicles by cAMP at the calyx of Held. Proc Natl Acad Sci USA 98: 331-336.
37. Rizzoli SO, Betz WJ, (2004) The structural organization of the readily releasable pool of synaptic vesicles. Science 303: 2037-2039.
38. Jovanovic JN, Sihra TS, Nairn AC, Hemmings HC, Greengard P, et al. (2001) Opposing changes in phosphorylation of specific sites in synapsin I during Ca2+-dependent glutamate release in isolated nerve terminals. J Neurosci 21: 7944-7953.
39. Chi P, Greengard P, Ryan TA, (2003) Synaptic vesicle mobilization is regulated by distinct synapsin I phosphorylation pathways at different frequencies. Neuron 38: 69-78.
40. Fioravante D, Liu RY, Netek AK, Cleary LJ, Byrne JH, (2007) Synapsin regulates basal synaptic strength, synaptic depression, and serotonin-induced facilitation of sensorimotor synapses in Aplysia. J Neurophysiol 98: 3568-3580.
41. Orenbuch A, Shalev L, Marra V, Sinai I, Lavy Y, et al. (2012) Synapsin selectively controls the mobility of resting pool vesicles at hippocampal terminals. J Neurosci 32: 3969-3980.
42. Vasileva M, Horstmann H, Geumann C, Gitler D, Kuner T (2012) Synapsin-dependent reserve pool of synaptic vesicles supports replenishment of the readily releasable pool under intense synaptic transmission. Eur J Neurosci doi:10.1111/j.1460-9568.2012.08225.x.
43. Fiumara F, Milanese C, Corradi A, Giovedi S, Leitinger G, et al. (2007) Phosphorylation of synapsin domain A is required for post-tetanic potentiation. J Cell Sci 120: 3228-3237.
44. Giachello CNG, Fiumara F, Giacomini C, Corradi A, Milanese C, et al. (2010) MAPK/Erk-dependent phosphorylation of synapsin mediates formation of functional synapses and short-term homosynaptic plasticity. J Cell Sci 123: 881-893.
45. Altrup U, (1987) Inputs and outputs of giant neuron-B1 and neuron-B2 in the buccal ganglia of Helix pomatia- an electrophysiological and morphological study. Brain Res 414: 271-284.
46. Altrup U, Speckmann EJ, (1994) Identified neuronal individuals in the buccal ganglia of Helix pomatia. Neurosci Behav Physiol 24: 23-32.
47. Massobrio P, Tedesco M, Giachello C, Ghirardi M, Fiumara F, et al. (2009) Helix neuronal ensembles with controlled cell type composition and placement develop functional polysynaptic circuits on Micro-Electrode Arrays. Neurosci Lett 467: 121-126.
48. Altrup U, Hader M, Storz U, (2003) Endogenous pacemaker potentials develop into paroxysmal depolarization shifts (PDSs) with application of an epileptogenic drug. Brain Res 975: 73-84.
49. Schneggenburger R, Meyer AC, Neher E, (1999) Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23: 399-409.
50. Schneggenburger R, Sakaba T, Neher E, (2002) Vesicle pools and short-term synaptic depression: lessons from a large synapse. Trends Neurosci 25: 206-212.
51. Manabe T, Wyllie DJA, Perkel DJ, Nicoll RA, (1993) Modulation of synaptic transmission and long-term potentiation- Effects on paired-pulse facilitation and EPSC variance in the CA1 region of the hippocampus. J Neurophysiol 70: 1451-1459.
52. Debanne D, Guerineau NC, Gahwiler BH, Thompson SM, (1996) Paired-pulse facilitation and depression at unitary synapses in rat hippocampus: Quantal fluctuation affects subsequent release. J Physiol 491: 163-176.
53. Dobrunz LE, Stevens CF, (1997) Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18: 995-1008.
54. Bloom FE, Ueda T, Battenberg E, Greengard P, (1979) Immunocytochemical localization, in synapses, of protein I, an endogenous substrate for protein kinases in mammalian brain. Proc Natl Acad Sci USA 76: 5982-5986.
55. De Camilli P, Ueda T, Bloom FE, Battenberg E, Greengard P, (1979) Widespread distribution of protein I in the central and peripheral nervous systems. Proc Natl Acad Sci USA 76: 5977-5981.
56. De Camilli P, Cameron R, Greengard P, (1983) Synapsin I (protein I), a nerve terminal-specific phosphoprotein. I. Its general distribution in synapses of the central and peripheral nervous system demonstrated bv immunofluorescence in frozen and plastic sections. J Cell Biol 96: 1337-1354.
57. De Camilli P, Harris SM, Huttner WB, Greengard P, (1983) Synapsin I (Protein I), a nerve terminal-specific phosphoprotein. II. Its specific association with synaptic vesicles demonstrated by immunocytochemistry in agarose-embedded synaptosomes. J Cell Biol 96: 1355-1373.
58. Fried G, Nestler EJ, De Camilli P, Stjarne L, Olson L, et al. (1982) Cellular and subcellular localization of protein I in the peripheral nervous system. Proc Natl Acad Sci USA 79: 2717-2721.
59. Valtorta F, Villa A, Jahn R, De Camilli P, Greengard P, et al. (1988) Localization of synapsin-I at the frog neuromuscular-junction. Neuroscience 24: 593-603.
60. Hirokawa N, Sobue K, Kanda K, Harada A, Yorifuji H, (1989) The cytoskeletal architecture of the presynaptic terminal and molecular structure of synapsin I. J Cell Biol. 108: 111-126.
61. Bloom O, Evergren E, Tomilin N, Kjaerulff O, Low P, et al. (2003) Colocalization of synapsin and actin during synaptic vesicle recycling. J Cell Biol 161: 737-747.
62. Tao-Cheng JH, (2006) Activity-related redistribution of presynaptic proteins at the active zone. Neuroscience 141: 1217-1224.
63. Gitler D, Xu YM, Kao HT, Lin DY, Lim SM, et al. (2004) Molecular determinants of synapsin targeting to presynaptic terminals. J Neurosci 24: 3711-3720.
64. Langmeier M, Mares J, Fischer J, (1983) Number of synaptic vesicles in rat cortex immediately after cessation of the self-sustained afterdischarge during kindling. Epilepsia 24: 616-627.
65. Applegate MD, Landfield PW, (1988) Synaptic vesicle redistribution during hippocampal frequency potentiation and depression in young and aged rats. J Neurosci 8: 1096-1111.
66. Ceccarelli B, Hurlbut WP, (1980) Vesicle hypothesis of the release of quanta of acetylcholine. Physiol Rev 60: 396-441.
67. Fischer J, Langmeier M, (1980) Changes in the number, size, and shape of synaptic vesicles in an experimental, projected cortical epileptic focus in the rat. Epilepsia 21: 571-585.
68. Langmeier M, Fischer J, Mares J, (1980) Number of synaptic vesicles in the rat somatosensory cortex after repetitive electrical stimulation prolonging self-sustained after-discharges. Epilepsia 21: 255-260.
69. Hovorka J, Langmeier M, Mares P, (1989) Are there morphological-changes in presynaptic terminals of kindled rats? Neurosci Lett 107: 179-183.
70. Doussau F, Clabecq A, Henry JP, Darchen F, Poulain B, (1998) Calcium-dependent regulation of Rab3 in short-term plasticity. J Neurosci 18: 3147-3157.
71. Humeau Y, Doussau F, Popoff MR, Benfenati F, Poulain B, (2007) Fast changes in the functional status of release sites during short-term plasticity: involvement of a frequency-dependent bypass of Rac at Aplysia synapses. J Physiol 583: 983-1004.
72. Zucker RS, (1993) Calcium and transmitter release. J Physiol Paris 87: 25-36.
73. Kim JH, Udo H, Li HL, Youn TY, Chen M, et al. (2003) Presynaptic activation of silent synapses and growth of new synapses contribute to intermediate and long-term facilitation in Aplysia. Neuron 40: 151-165.
74. Shoji Y, Tanaka E, Yamamoto S, Maeda H, Higashi H, (1998) Mechanisms underlying the enhancement of excitatory synaptic transmission in basolateral amygdala neurons of the kindling rat. J Neurophysiol 80: 638-646.
75. Castellucci V, Pinsker H, Kupfermann I, Kandel ER, (1970) Neuronal mechanisms of habituation and dishabituation of the gill-withdrawal reflex in Aplysia. Science 167: 1745-1748.
76. Christoffersen GRJ, (1997) Habituation: Events in the history of its characterization and linkage to synaptic depression. A new proposed kinetic criterion for its identification. Prog Neurobiol 53: 45-66.
77. Casadio A, Fiumara F, Sonetti D, Montarolo PG, Ghirardi M, (2004) Distribution of sensorin immunoreactivity in the central nervous system of Helix pomatia: Functional aspects. J Neurosci Res 75: 32-43.
78. Millar AG, Bradacs H, Charlton MP, Atwood HL, (2002) Inverse relationship between release probability and readily releasable vesicles in depressing and facilitating synapses. J Neurosci 22: 9661-9667.
79. Pivovarov AS, Drozdova EI, (2002) Ca-dependent regulation of the Na-K-pump by post-tetanic sensitization of extrasynaptic cholinoreceptors in common snail neurons. Neurosci Behav Physiol 32: 223-229.
80. Kopanitsa MV, (1997) Extrasynaptic receptors of neurotransmitters: Distribution, mechanisms of activation, and physiological role. Neurophysiology 29: 357-365.
81. Lu WY, Man HY, Ju W, Trimble WS, MacDonald JF, et al. (2001) Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron 29: 243-254.
82. Massey PV, Johnson BE, Moult PR, Auberson YP, Brown MW, et al. (2004) Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J Neurosci 24: 7821-7828.
83. Luk CC, Naruo H, Prince D, Hassan A, Doran SA, et al. (2011) A novel form of presynaptic CaMKII-dependent short-term potentiation between Lymnaea neurons. Eur J Neurosci 34: 569-577.
84. Volianskis A, Jensen MS, (2003) Transient and sustained types of long-term potentiation in the CA1 area of the rat hippocampus. J Physiol 550: 459-492.
85. Zhao Y, Klein M, (2004) Changes in the readily releasable pool of transmitter and in efficacy of release induced by high-frequency firing at Aplysia sensorimotor synapses in culture. J Neurophysiol 91: 1500-1509.
86. Habets RLP, Borst JGG, (2005) Post-tetanic potentiation in the rat calyx of Held synapse. J Physiol 564: 173-187.
87. Korogod N, Lou XL, Schneggenburger R, (2005) Presynaptic Ca2+ requirements and developmental regulation of posttetanic potentiation at the calyx of Held. J Neurosci 25: 5127-5137.
88. Zucker RS, Regehr WG, (2002) Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405.
89. Felmy F, von Gersdorff H, (2006) Late switch for post-tetanic potentiation: Once again it's Ca2+. Focus on "An increase in calcium influx contributes to post-tetanic potentiation at the rat calyx of held synapse". J Neurophysiol 96: 2840-2841.
90. Delgado R, Maureira C, Oliva C, Kidokoro Y, Labarca P, (2000) Size of vesicle pools, rates of mobilization, and recycling at neuromuscular synapses of a Drosophila mutant, shibire. Neuron 28: 941-953.
91. Kidokoro Y, Kuromi H, Delgado R, Maureira C, Oliva C, et al. (2004) Synaptic vesicle pools and plasticity of synaptic transmission at the Drosophila synapse. Brain Res Brain Res Rev 47: 18-32.
92. Habets RLP, Borst JGG, (2007) Dynamics of the readily releasable pool during post-tetanic potentiation in the rat calyx of Held synapse. J Physiol 581: 467-478.
93. Kim SM, Kumar V, Lin Y-Q, Karunanithi S, Ramaswami M, (2009) Fos and Jun potentiate individual release sites and mobilize the reserve synaptic-vesicle pool at the Drosophila larval motor synapse. Proc Natl Acad Sci USA 106: 4000-4005.
94. Humeau Y, Doussau F, Vitiello F, Greengard P, Benfenati F, et al. (2001) Synapsin controls both reserve and releasable synaptic vesicle pools during neuronal activity and short-term plasticity in Aplysia. J Neurosci 21: 4195-4206.
95. Cousin MA, Malladi CS, Tan TC, Raymond CR, Smillie KJ, et al. (2003) Synapsin I-associated phosphatidylinositol 3-kinase mediates synaptic vesicle delivery to the readily releasable pool. J Biol Chem 278: 29065-29071.
96. Giovedì S, Vaccaro P, Valtorta F, Darchen F, Greengard P, et al. (2004) Synapsin is a novel Rab3 effector protein on small synaptic vesicles- I. Identification and characterization of the synapsin I-Rab3 interactions in vitro and in intact nerve terminals. J Biol Chem 279: 43760-43768.
97. Giovedì S, Darchen F, Valtorta F, Greengard P, Benfenati F, (2004) Synapsin is a novel Rab3 effector protein on small synaptic vesicles- II. Functional effects of the Rab3A-synapsin I interaction. J Biol Chem 279: 43769-43779.
98. Fornasiero EF, Raimondi A, Guarnieri FC, Orlando M, Fesce R, et al. (2012) Synapsins contribute to the dynamic spatial organization of synaptic vesicles in an activity-dependent manner. J Neurosci 32: 12214-12227.
99. Spillane DM, Rosahl TW, Sudhof TC, Malenka RC, (1995) Long-term potentiation in mice lacking synapsins. Neuropharmacol 34: 1573-1579.
100. Valente P, Casagrande S, Nieus T, Verstegen AMJ, Valtorta F, et al. (2012) Site-specific synapsin I phosphorylation participates in the expression of post-tetanic potentiation and its enhancement by BDNF. J Neurosci 32: 5868-5879.
101. Onozuka M, Imai S, Sugaya E, (1986) Pentylenetetrazole-induced bursting activity and cellular protein phosphorylation in snail neurons. Brain Res 362: 33-39.
102. Onozuka M, Imai S, Kishii K, Furuichi H, Ozono S, (1986) Stimulation of synapsin I phosphorylation in synaptosomes by convulsants. Exp Neurol 94: 802-807.
103. Sugaya E, Onozuka M, (1978) Intracellular calcium: its movement during pentylenetetrazole-induced bursting activity. Science 200: 797-799.
104. Onozuka M, Imai S, Ozono S, (1987) Involvement of pentylenetetrazole in synapsin I phosphorylation associated with calcium influx in synaptosomes from rat cerebral cortex. Biochem Pharmacol 36: 1407-1415.
105. Sugaya E, Furuichi H, Takagi T, Kajiwara K, Komatsubara J, (1987) Intracellular calcium concentration during pentylenetetrazol-induced bursting activity in snail neurons. Brain Res 416: 183-186.
106. Onozuka M, Nakagaki I, Sasaki S, (1989) Pentylenetetrazole-induced seizure activity produces an increased release of calcium from endoplasmic reticulum by mediating cyclic AMP-dependent protein phosphorylation in rat cerebral cortex. Gen Pharmacol 20: 627-634.
107. Bahler M, Greengard P, (1987) Synapsin-I bundles F-actin in a phosphorylation-dependent manner. Nature 326: 704-707.
108. Jovanovic JN, Benfenati F, Siow YL, Sihra TS, Sanghera JS, et al. (1996) Neurotrophins stimulate phosphorylation of synapsin I by MAP kinase and regulate synapsin I-actin interactions. Proc Natl Acad Sci USA 93: 3679-3683.
109. Chi P, Greengard P, Ryan TA, (2001) Synapsin dispersion and reclustering during synaptic activity. Nature Neurosci 4: 1187-1193.
110. Jovanovic JN, Czernik AJ, Fienberg AA, Greengard P, Sihra TS, (2000) Synapsins as mediators of BDNF-enhanced neurotransmitter release. Nature Neurosci 3: 323-329.
111. Kushner SA, Elgersma Y, Murphy GG, Jaarsma D, Hojjati MR, et al. (2005) Modulation of presynaptic plasticity and learning by the H-ras/extracellular signal-regulated kinase/synapsin I signaling pathway. J Neurosci 25: 9721-9734.
112. Menegon A, Bonanomi D, Albertinazzi C, Lotti F, Ferrari G, et al. (2006) Protein kinase A-mediated synapsin I phosphorylation is a central modulator of Ca2+-dependent synaptic activity. J Neurosci 26: 11670-11681.
113. Fiumara F, Giovedi S, Menegon A, Milanese C, Merlo D, et al. (2004) Phosphorylation by cAMP-dependent protein kinase is essential for synapsin-induced enhancement of neurotransmitter release in invertebrate neurons. J Cell Sci 117: 5145-5154.
114. Boulton CL, McCrohan CR, Oshaughnessy CT, (1993) Cyclic-AMP analogs increase excitability and enhance epileptiform activity in rat neocortex in vitro. Eur J Pharmacol 236: 131-136.
115. Higashima M, Ohno K, Koshino Y, (2002) Cyclic AMP-mediated modulation of epileptiform afterdischarge generation in rat hippocampal slices. Brain Res 949: 157-161.
116. Tehrani MHJ, Barnes EM, (1995) Reduced function of gamma-aminobutyric acidA receptors in tottering mouse brain: role of cAMP-dependent protein kinase. Epilepsy Res 22: 13-21.
117. Yechikhov S, Morenkov E, Chulanova T, Godukhin O, Shchipakina T, (2001) Involvement of cAMP- and Ca2+/calmodulin-dependent neuronal protein phosphorylation in mechanisms underlying genetic predisposition to audiogenic seizures in rats. Epilepsy Res 46: 15-25.
118. Ure A, Altrup U, (2006) Block of spontaneous termination of paroxysmal depolarizations by forskolin (buccal ganglia, Helix pomatia). Neurosci Lett 392: 10-15.
119. Bracey JM, Kurz JE, Low B, Churn SB, (2009) Prolonged seizure activity leads to increased Protein Kinase A activation in the rat pilocarpine model of status epilepticus. Brain Res 1283: 167-176.
120. Reijmers L, Hernando F, Van Ree JM, Spruijt BM, Burbach JPH, (2000) Differential responses of phosphorylated mitogen-activated protein kinase and phosphorylated cyclic-AMP response element-binding protein immunoreactivity in the rat brain to sub-convulsive pentylenetetrazol. Neurosci 101: 1023-1028.
121. Berkeley JL, Decker MJ, Levey AI, (2002) The role of muscarinic acetylcholine receptor-mediated activation of extracellular signal-regulated kinase 1/2 in pilocarpine-induced seizures. J Neurochem 82: 192-201.
122. Merlo D, Cifelli P, Cicconi S, Tancredi V, Avoli M, (2004) 4 Aminopyridine-induced epileptogenesis depends on activation of mitogen-activated protein kinase ERK. J Neurochem 89: 654-659.
123. Nateri AS, Raivich G, Gebhardt C, Da Costa C, Naumann H, et al. (2007) ERK activation causes epilepsy by stimulating NMDA receptor activity. EMBO J 26: 4891-4901.
124. Xi ZQ, Wang XF, He RQ, Li MW, Liu XZ, et al. (2007) Extracellular signal-regulated protein kinase in human intractable epilepsy. Eur J Neurol 14: 865-872.
125. Hagler DJ, Goda Y, (2001) Properties of synchronous and asynchronous release during pulse train depression in cultured hippocampal neurons. J Neurophysiol 85: 2324-2334.
126. Otsu Y, Shahrezaei V, Li B, Raymond LA, Delaney KR, et al. (2004) Competition between phasic and asynchronous release for recovered synaptic vesicles at developing hippocampal autaptic synapses. J Neurosci 24: 420-433.
127. Sennepin AD, Charpentier S, Normand T, Sarre C, Legrand A, et al. (2009) Multiple reprobing of Western blots after inactivation of peroxidase activity by its substrate, hydrogen peroxide. Anal Biochem 393: 129-131.
128. Upadhaya R, Mizunoya W, Anderson JE, (2011) Detecting multiple proteins by Western blotting using same-species primary antibodies, precomplexed serum, and hydrogen peroxide. Anal Biochem 419: 342-344.