Modulation of presynaptic plasticity and learning by the H-ras/extracellular signal-regulated kinase/synapsin I signaling pathway

Journal of Neuroscience

Volumn 25, Issue 42, 2005, Pages 9721-9734

  Kushner, Steven A ^a   Elgersma, Ype ^a,b   Murphy, Geoffrey G ^a   Jaarsma, Dick ^b   Van Woerden, Geeske M ^b   Hojjati, Mohammad Reza ^b   Cui, Yijun ^a   LeBoutillier, Janelle C ^c   Marrone, Diano F ^c   Choi, Esther S ^a   De Zeeuw, Chris I ^b   Petit, Ted L ^c   Pozzo Miller, Lucas ^d   Silva, Alcino J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF TORONTO   (Canada)

^d University of Alabama at Birmingham   (United States)

Author keywords

ERK; Learning; LTP; mEPSCs; Miniature excitatory postsynaptic currents; Presynaptic; Ras; Synapsin

Indexed keywords

GLUTAMIC ACID; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; NEUROTRANSMITTER; SYNAPSIN I;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; EXCITATORY POSTSYNAPTIC POTENTIAL; FACILITATION; GENE LOCATION; HIPPOCAMPUS; INVERTEBRATE; LEARNING; LONG TERM POTENTIATION; MEMBRANE VESICLE; MEMORY; MOUSE; NERVE CELL PLASTICITY; NERVE ENDING; NEUROMODULATION; NEUROTRANSMITTER RELEASE; NONHUMAN; ONCOGENE H RAS; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; WILD TYPE;

ANIMALS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; LEARNING; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEURONAL PLASTICITY; PRESYNAPTIC TERMINALS; PROTO-ONCOGENE PROTEINS P21(RAS); SYNAPSINS;

EID: 27144548450     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2836-05.2005     Document Type: Article

References (82)

1. Adams JP, Sweatt JD (2002) Molecular psychology: roles for the ERK MAP kinase cascade in memory. Annu Rev Pharmacol Toxicol 42:135-163.
2. Adams JP, Anderson AE, Varga AW, Dineley KT, Cook RG, Pfaffinger PJ, Sweatt JD (2000) The A-type potassium channel Kv4.2 is a substrate for the mitogen-activated protein kinase ERK. J Neurochem 75:2277-2287.
3. Anagnostaras SG, Josselyn SA, Frankland PW, Silva AJ (2000) Computer-assisted behavioral assessment of Pavlovian fear conditioning in mice. Learn Mem 7:58-72.
4. Antonov I, Antonova I, Kandel ER, Hawkins RD (2003) Activity-dependent presynaptic facilitation and hebbian LTP are both required and interact during classical conditioning in Aplysia. Neuron 37:135-147.
5. Atkins CM, Selcher JC, Petraitis J, Trzaskos J, Sweatt J (1998) The MAPK cascade is required for mammalian associative learning. Nat Neurosci 1:602-609.
6. Bahler M, Greengard P (1987) Synapsin I bundles F-actin in a phosphorylation-dependent manner. Nature 326:704-707.
7. 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.
8. 2+/calmodulin-dependent protein kinase II is a binding protein for synapsin I. Nature 359:417-420.
9. Brager DH, Capogna M, Thompson SM (2002) Short-term synaptic plasticity, simulation of nerve terminal dynamics, and the effects of protein kinase C activation in rat hippocampus. J Physiol (Lond) 541:545-559.
10. Brandeis R, Brandys Y, Yehuda S (1989) The use of the Morris water maze in the study of memory and learning. Int J Neurosci 48:29-69.
11. Burrell BD, Sahley CL (2001) Learning in simple systems. Curr Opin Neurobiol 11:757-764.
12. 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.
13. Chin J, Angers A, Cleary LJ, Eskin A, Byrne JH (2002) Transforming growth factor β-1 alters synapsin distribution and modulates synaptic depression in Aplysia. J Neurosci 22:1-6.
14. Costa RM, Yang T, Huynh DP, Pulst SM, Viskochil DH, Silva AJ, Brannan CI (2001) Learning deficits, but normal development and tumor predisposition, in mice lacking exon 23a of Nf1. Nat Genet 27:399-405.
15. Daniels RW, Collins CA, Gelfand MV, Dant J, Brooks ES, Krantz DE, DiAntonio A (2004) Increased expression of the Drosophila vesicular glutamate transporter leads to excess glutamate release and a compensatory decrease in quantal content. J Neurosci 24:10466-10474.
16. Davis GW, Goodman CS (1998) Synapse-specific control of synaptic efficacy at the terminals of a single neuron. Nature 392:82-86.
17. Dickinson-Nelson A, Reese TS (1983) Structural changes during transmitter release at synapses in the frog sympathetic ganglion. J Neurosci 3:42-52.
18. Dobrunz LE, Stevens CF (1997) Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18:995-1008.
19. Dobrunz LE, Stevens CF (1999) Response of hippocampal synapses to natural stimulation patterns. Neuron 22:157-166.
20. Dobrunz LE, Huang EP, Stevens CF (1997) Very short-term plasticity in hippocampal synapses. Proc Natl Acad Sci USA 94:14843-14847.
21. Elgersma Y, Fedorov N, Ikonen S, Choi E, Elgersma M, Carvalho O, Giese K, Silva A (2002) Inhibitory autophosphorylation of CaMKII controls PSD association, plasticity and learning. Neuron 36:493-505.
22. English JD, Sweatt JD (1996) Activation of p42 mitogen-activated protein kinase in hippocampal long term potentiation. J Biol Chem 271:24329-24332.
23. Fanselow MS (1990) Factors governing one-trial contextual conditioning. Anim Learn Behav 18:264-270.
24. Frankland P, O'Brien C, Ohno M, Kirkwood A, Silva A (2001) Alpha-CaMKI1-dependent plasticity in the cortex is required for permanent memory. Nature 411:309-313.
25. Frankland PW, Josselyn SA, Anagnostaras SG, Kogan JH, Takahashi E, Silva AJ (2004) Consolidation of CS and US representations in associative fear conditioning. Hippocampus 14:557-569.
26. Frick A, Magee J, Johnston D (2004) LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat Neurosci 7:126-135.
27. Gartner U, Alpar A, Seeger G, Heumann R, Arendt T (2004) Enhanced Ras activity in pyramidal neurons induces cellular hypertrophy and changes in afferent and intrinsic connectivity in synRas mice. Int J Dev Neurosci 22:165-173.
28. Gottschalk W, Pozzo-Miller LD, Figurov A, Lu B (1998) Presynaptic modulation of synaptic transmission and plasticity by brain-derived neurotrophic factor in the developing hippocampus. J Neurosci 18:6830-6839.
29. Gottschalk WA, Jiang H, Tartaglia N, Feng L, Figurov A, Lu B (1999) Signaling mechanisms mediating BDNF modulation of synaptic plasticity in the hippocampus. Learn Mem 6:243-256.
30. Heumann R, Goemans C, Bartsch D, Lingenhohl K, Waldmeier PC, Hengerer B, Allegrini PR, Schellander K, Wagner EF, Arendt T, Kamdem RH, Obst-Pernberg K, Narz F, Wahle P, Berns H (2000) Transgenic activation of Ras in neurons promotes hypertrophy and protects from lesion-induced degeneration. J Cell Biol 151:1537-1548.
31. Hilfiker S, Pieribone VA, Czernik AJ, Kao HT, Augustine GJ, Greengard P (1999) Synapsins as regulators of neurotransmitter release. Philos Trans R Soc Lond B Biol Sci 354:269-279.
32. Humeau Y, Doussau F, Vitiello F, Greengard P, Benfenati F, Poulain B (2001) Synapsin controls both reserve and releasable synaptic vesicle pools during neuronal activity and short-term plasticity in Aplysia. J Neurosci 21:4195-4206.
33. Husi H, Ward MA, Choudhary JS, Blackstock WP, Grant SG (2000) Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat Neurosci 3:661-669.
34. Iida N, Namikawa K, Kiyama H, Ueno H, Nakamura S, Hattori S (2001) Requirement of Ras for the activation of mitogen-activated protein kinase by calcium influx, cAMP, and neurotrophin in hippocampal neurons. J Neurosci 21:6459-6466.
35. Jaarsma D, Rognoni F, van Duijn W, Verspaget HW, Haasdijk ED, Holstege JC (2001) CuZn superoxide dismutase (SOD1) accumulates in vacuolated mitochondria in transgenic mice expressing amyotrophic lateral sclerosis-linked SOD1 mutations. Acta Neuropathol (Berl) 102:293-305.
36. Jones SR, Gainetdinov RR, Jaber M, Giros B, Wightman RM, Caron MG (1998) Profound neuronal plasticity in response to inactivation of the dopamine transporter. Proc Natl Acad Sci USA 95:4029-4034.
37. Jovanovic JN, Benfenati F, Siow YL, Sihra TS, Sanghera JS, Pelech SL, Greengard P, Czernik AJ (1996) Neurotrophins stimulate phosphorylation of synapsin I by MAP kinase and regulate synapsin I-actin interactions. Proc Natl Acad Sci USA 93:3679-3683.
38. Jovanovic JN, Czernik AJ, Fienberg AA, Greengard P, Sihra TS (2000) Synapsins as mediators of BDNF-enhanced neurotransmitter release. Nat Neurosci 3:323-329.
39. 2+-dependent glutamate release in isolated nerve terminals. J Neurosci 21:7944-7953.
40. Kim JJ, Fanselow MS (1992) Modality-specific retrograde amnesia of fear. Science 256:675-677.
41. Koh YH, Ruiz-Canada C, Gorczyca M, Budnik V (2002) The Ras1-mitogen-activated protein kinase signal transduction pathway regulates synaptic plasticity through fasciclin II-mediated cell adhesion. J Neurosci 22:2496-2504.
42. Komiyama NH, Watabe AM, Carlisle HJ, Porter K, Charlesworth P, Monti J, Strathdee DJ, O'Carroll CM, Martin SJ, Morris RG, O'Dell TJ, Grant SG (2002) SynGAP regulates ERK/MAPK signaling, synaptic plasticity, and learning in the complex with postsynaptic density 95 and NMDA receptor. J Neurosci 22:9721-9732.
43. Larson J, Wong D, Lynch G (1986) Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res 368:347-350.
44. Li L, Chin LS, Shupliakov O, Brodin L, Sihra TS, Hvalby O, Jensen V, Zheng D, McNamara JO, Greengard P, Andersen P (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.
45. Lisman JE (1997) Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci 20:38-43.
46. Malenka RC, Nicoll RA (1999) Long-term potentiation-a decade of progress? Science 285:1870-1874.
47. Manabe T, Aiba A, Yamada A, Ichise T, Sakagami H, Kondo H, Katsuki M (2000) Regulation of long-term potentiation by H-ras through NMDA receptor phosphorylation. J Neurosci 20:2504-2511.
48. Martin KC, Michael D, Rose JC, Barad M, Casadio A, Zhu H, Kandel ER (1997) MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia. Neuron 18:899-912.
49. Martin SJ, Grimwood PD, Morris RG (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649-711.
50. Mayford M, Wang J, Kandel ER, O'Dell TJ (1995) CaMKII regulates the frequency-response function of hippocampal synapses for the production of both LTD and LTP. Cell 81:891-904.
51. Morris RG, Garrud P, Rawlins JN, O'Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
52. Otto T, Eichenbaum H, Wiener SI, Wible CG (1991) Learning-related patterns of CA1 spike trains parallel stimulation parameters optimal for inducing hippocampal long-term potentiation. Hippocampus 1:181-192.
53. Phend KD, Rustioni A, Weinberg RJ (1995) An osmium-free method of epon embedment that preserves both ultrastructure and antigenicity for post-embedding immunocytochemistry. J Histochem Cytochem 43:283-292.
54. 2+ entry pathway. Proc Natl Acad Sci USA 101:3609-3614.
55. Pieribone VA, Shupliakov O, Brodin L, Hilfiker-Rothenfluh S, Czernik AJ, Greengard P (1995) Distinct pools of synaptic vesicles in neurotransmitter release. Nature 375:493-497.
56. Powell CM, Schoch S, Monteggia L, Barrot M, Matos MF, Feldmann N, Sudhof TC, Nestler EJ (2004) The presynaptic active zone protein RIM1 alpha is critical for normal learning and memory. Neuron 42:143-153.
57. Pozzo-Miller LD, Gottschalk W, Zhang L, McDermott K, Du J, Gopalakrishnan R, Oho C, Sheng ZH, Lu B (1999) Impairments in high-frequency transmission, synaptic vesicle docking, and synaptic protein distribution in the hippocampus of BDNF knock-out mice. J Neurosci 19:4972-4983.
58. Roberts AC, Glanzman DL (2003) Learning in Aplysia: looking at synaptic plasticity from both sides. Trends Neurosci 26:662-670.
59. Rosahl TW, Geppert M, Spillane D, Herz J, Hammer RE, Malenka RC, Sudhof TC (1993) Short-term synaptic plasticity is altered in mice lacking synapsin I. Cell 75:661-670.
60. Rosahl TW, Spillane D, Missler M, Herz J, Selig DK, Wolff JR, Hammer RE, Malenka RC, Sudhof TC (1995) Essential functions of synapsins I and II in synaptic vesicle regulation. Nature 375:488-493.
61. Rosen LB, Ginty DD, Weber MJ, Greenberg ME (1994) Membrane depolarization and calcium influx stimulate MEK and MAP kinase via activation of Ras. Neuron 12:1207-1221.
62. Rudy JW, Barrientos RM, O'Reilly RC (2002) Hippocampal formation supports conditioning to memory of a context. Behav Neurosci 116:530 -538.
63. Schiebler W, Jahn R, Doucet JP, Rothlein J, Greengard P (1986) Characterization of synapsin I binding to small synaptic vesicles. J Biol Chem 261:8383-8390.
64. Schikorski T, Stevens CF (1997) Quantitative ultrastructural analysis of hippocampal excitatory synapses. J Neurosci 17:5858-5867.
65. Schikorski T, Stevens CF (2001) Morphological correlates of functionally defined synaptic vesicle populations. Nat Neurosci 4:391-395.
66. Schnell E, Nicoll RA (2001) Hippocampal synaptic transmission and plasticity are preserved in myosin Va mutant mice. J Neurophysiol 85:1498-1501.
67. Selcher JC, Weeber EJ, Christian J, Nekrasova T, Landreth GE, Sweatt JD (2003) A role for ERK MAP kinase in physiologic temporal integration in hippocampal area CA1. Learn Mem 10:26-39.
68. Sharma SK, Sherff CM, Shobe J, Bagnall MW, Sutton MA, Carew TJ (2003) Differential role of mitogen-activated protein kinase in three distinct phases of memory for sensitization in Aplysia. J Neurosci 23:3899-3907.
69. Silva AJ, Rosahl TW, Chapman PF, Marowitz Z, Friedman E, Frankland PW, Cestari V, Cioffi D, Sudhof TC, Bourtchuladze R (1996) Impaired learning in mice with abnormal short-lived plasticity. Curr Biol 6:1509-1518.
70. Tsodyks MV, Markram H (1997) The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci USA 94:719-723.
71. Tyler WJ, Pozzo-Miller LD (2001) BDNF enhances quantal neurotransmitter release and increases the number of docked vesicles at the active zones of hippocampal excitatory synapses. J Neurosci 21:4249-4258.
72. Tyler WJ, Alonso M, Bramham CR, Pozzo-Miller LD (2002) From acquisition to consolidation: on the role of brain-derived neurotrophic factor signaling in hippocampal-dependent learning. Learn Mem 9:224-237.
73. Varela JA, Sen K, Gibson J, Post J, Abbott LF, Nelson SB (1997) A quantitative description of short-term plasticity at excitatory synapses in layer 2/3 of rat primary visual cortex. J Neurosci 17:7926-7940.
74. + channels contribute to spike-timing dependent long-term potentiation in hippocampal pyramidal neurons. Proc Natl Acad Sci USA 99:8366-8371.
75. Winder DG, Martin KC, Muzzio IA, Rohrer D, Chruscinski A, Kobilka B, Kandel ER (1999) ERK plays a regulatory role in induction of LTP by theta frequency stimulation and its modulation by beta-adrenergic receptors. Neuron 24:715-726.
76. Wisden W, Errington ML, Williams S, Dunnett SB, Waters C, Hitchcock D, Evan G, Bliss TVP, Hunt SP (1990) Differential expression of immediate early genes in the hippocampus and spinal cord. Neuron 4:603-614.
77. Xu B, Gottschalk W, Chow A, Wilson RI, Schnell E, Zang K, Wang D, Nicoll RA, Lu B, Reichardt LF (2000) The role of brain-derived neurotrophic factor receptors in the mature hippocampus: modulation of long-term potentiation through a presynaptic mechanism involving TrkB. J Neurosci 20:6888-6897.
78. + channels in hippocampus involves a mitogen-activated protein kinase pathway. J Neurosci 22:4860-4868.
79. 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.
80. Zhang X, Poo MM (2002) Localized synaptic potentiation by BDNF requires local protein synthesis in the developing axon. Neuron 36:675-688.
81. Zhu JJ, Qin Y, Zhao M, Van Aelst L, Malinow R (2002) Ras and Rap control AMPA receptor trafficking during synaptic plasticity. Cell 110:443-455.
82. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405.