A novel pathway for presynaptic mitogen-activated kinase activation via AMPA receptors

Journal of Neuroscience

Volumn 25, Issue 7, 2005, Pages 1654-1663

  Schenk, Ursula ^a   Menna, Elisabetta ^a   Kim, Taeyong ^b   Passafaro, Maria ^a,d   Chang, Sunghoe ^b   De Camilli, Pietro ^c   Matteoli, Michela ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b Gwangju Institute of Science and Technology (GIST)   (South Korea)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d DULBECCO TELETHON INSTITUTE   (Italy)

Author keywords

Growth cone; MAP kinase; Presynaptic AMPA receptor; Synaptic plasticity; Synaptogenesis; Vesicle recycling

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; AMPA RECEPTOR; GLUTAMATE RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; SYNAPSIN I;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; EVOKED RESPONSE; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SYNAPSE VESICLE; SYNAPTOSOME;

ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; CELLS, CULTURED; CYTOSKELETON; ENZYME ACTIVATION; EXOCYTOSIS; GROWTH CONES; HIPPOCAMPUS; MAP KINASE SIGNALING SYSTEM; NEURONAL PLASTICITY; NEURONS; PHOSPHORYLATION; PRESYNAPTIC TERMINALS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RECEPTORS, AMPA; RECEPTORS, PRESYNAPTIC; SUBCELLULAR FRACTIONS; SYNAPSINS; SYNAPTIC VESICLES; SYNAPTOSOMES;

EID: 14044270862     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3074-04.2005     Document Type: Article

References (50)

1. Angers A, Fioravante D, Chin J, Cleary L, Bean A, Byrne J (2002) Serotonin stimulates phosphorylation of Aplysia synapsin and alters its subcellular distribution in sensory neurons. J Neurosci 22:5412-5422.
2. Bartlett W, Banker G (1984) An electron microscopic study of the development of axons and dendrites by hippocampal neurons in culture. II. Synaptic relationships. J Neurosci 4:1954-1965.
3. Betz W, Mao F, Bewick G (1992) Activity-dependent fluorescent staining and destaining of living vertebrate motor nerve terminals. J Neurosci 12:363-375.
4. Brummelkamp TR, Bernards R, Agami R (2002) A system for stable expression of short interfering RNAs in mammalian cells. Science 296:550-553.
5. Casey M, Maguire C, Kelly A, Gooney M, Lynch M (2002) Analysis of the presynaptic signaling mechanisms underlying the inhibition of LTP in rat dentate gyms by the tyrosine kinase inhibitor, genistein. Hippocampus 12:377-385.
6. Chang L, Karin M (2001) Mammalian MAP kinase signalling cascades. Nature 410:37-40.
7. Chang S, De Camilli P (2001) Glutamate regulates actin-based motility in axonal filopodia. Nat Neurosci 4:787-793.
8. Chi P, Greengard P, Ryan T (2001) Synapsin dispersion and reclustering during synaptic activity. Nat Neurosci 4:1187-1193.
9. Chi P, Greengard P, Ryan T (2003) Synaptic vesicle mobilization is regulated by distinct synapsin I phosphorylation pathways at different frequencies. Neuron 38:69-78.
10. Chin J, Angers A, Cleary L, Eskin A, Byrne J (2002) Transforming growth factor β1 alters synapsin distribution and modulates synaptic depression in Aplysia. J Neurosci 22:RC220(1-6).
11. Choi S, Klingauf I, Tsien RW (2000) Postfusional regulation of cleft glutamate concentration during LTP at "silent synapses." Nat Neurosci 3:330-336.
12. Clements JD (1996) Transmitter timecourse in the synaptic cleft: its role in central synaptic function. Trends Neurosci 19:163-171.
13. Coco S, Raposo G, Martinez S, Fontaine JJ, Takamori S, Zahraoui A, Jahn R, Matteoli M, Louvard D, Galli T (1999) Subcellular localization of tetanus neurotoxin-insensitive vesicle-associated membrane protein (VAMP)/VAMP7 in neuronal cells: evidence for a novel membrane compartment. J Neurosci 19:9803-9812.
14. Diamond JS, Jahr CE (1997) Transporters buffer synaptically released glutamate on a submillisecond time scale. J Neurosci 17:4672-4687.
15. Fabian-Fine R, Volknandt W, Fine A, Stewart M (2000) Age-dependent pre- and postsynaptic distribution of AMPA receptors at synapses in CA3 stratum radiatum of hippocampal slice cultures compared with intact brain. Eur J Neurosci 12:3687-3700.
16. Fremeau Jr RT, Kam K, Qureshi T, Johnson J, Copenhagen DR, Storm-Mathisen J, Chaudhry FA, Nicoll RA, Edwards RH (2004) Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 304:1815-1819.
17. Goda Y, Davis GW (2003) Mechanisms of synapse assembly and disassembly. Neuron 40:243-264.
18. Grewal S, York R, Stork P (1999) Extracellular-signal-regulated kinase signalling in neurons. Curr Opin Neurobiol 9:544-553.
19. Hayashi T, Umemori H, Mishira M, Yamamoto T (1999) The AMPA receptor interacts with and signals through the protein tyrosine kinase Lyn. Nature 397:72-76.
20. Helmke S, Pfenninger K (1995) Growth cone enrichment and cytoskeletal association of non-receptor tyrosine kinases. Cell Motil Cytoskeleton 30:194-207.
21. Hilfiker S, Pieribone V, Czernik A, Kao H, Augustine G, Greengard P (1999) Synapsins as regulators of neurotransmitter release. Philos Trans R Soc Lond B Biol Sci 354:269-279.
22. Huttner W, Schiebler W, Greengard P, De CP (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.
23. Jovanovic J, Benfenati F, Siow Y, Sihra T, Sanghera J, Pelech S, Greengard P, Czernik A (1996) Neurotrophins stimulate phosphorylation of synapsin I by MAP kinase and regulate synapsin I-actin interactions. Proc Natl Acad Sci USA 93:3679-3683.
24. Jovanovic J, Czernik A, Fienberg A, Greengard P, Sihra T (2000) Synapsins as mediators of BDNF-enhanced neurotransmitter release. Nat Neurosci 3:323-329.
25. Koh TW, Verstreken P, Bellen HJ (2004) Dap160/Intersectin acts as a stabilizing scaffold required for synaptic development and vesicle endocytosis. Neuron 43:193-205.
26. Krueger SR, Kolar A, Fitzsimonds RM (2003) The presynaptic release apparatus is functional in the absence of dendritic contact and highly mobile within isolated axons. Neuron 40:945-957.
27. Lee C, Bardoni R, Tong C, Engelman H, Joseph D, Magherini P, MacDermott A (2002) Functional expression of AMPA receptors on central terminals of rat dorsal root ganglion neurons and presynaptic inhibition of glutamate release. Neuron 35:135-146.
28. Lockerbie R, Miller V, Pfenninger K (1991) Regulated plasmalemmal expansion in nerve growth cones. J Cell Biol 112:1215-1227.
29. Lohse K, Helmke SM, Wood MR, Quiroga S, de la Houssaye BA, Miller VE, Negre-Aminou P, Pfenninger KH (1996) Axonal origin and purity of growth cones isolated from fetal rat brain. Brain Res Dev Brain Res 96:83-96.
30. Lu C, Hwang S, Phend K, Rustioni A, Valtschanoff J (2002) Primary afferent terminals in spinal cord express presynaptic AMPA receptors. J Neurosci 22:9522-9529.
31. MacDermott A, Role L, Siegelbaum S (1999) Presynaptic ionotropic receptors and the control of transmitter release. Annu Rev Neurosci 22:443-485.
32. Malinow R, Malenka R (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
33. Marie B, Sweeney ST, Poskanzer KE, Roos J, Kelly RB, Davis GW (2004) Dap160/Intersectin scaffolds the periactive zone to achieve high-fidelity endocytosis and normal synaptic growth. Neuron 43:207-219.
34. Matsubara M, Kusubata M, Ishiguro K, Uchida T, Titani K, Taniguchi H (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.
35. Matteoli M, Takei K, Perin MS, Sudhof TC, De Camilli P (1992) Exoendocytotic recycling of synaptic vesicles in developing processes of cultured hippocampal neurons. J Cell Biol 117:849-861.
36. Matteoli M, Coco S, Schenk U, Verderio C (2004) Vesicle turnover in developing neurons: how to build a presynaptic terminal. Trends Cell Biol 14:133-140.
37. Passafaro M, Nakagawa T, Sala C, Sheng M (2003) Induction of dendritic spines by an extracellular domain of AMPA receptor subunit GluR2. Nature 424:677-681.
38. 2+-permeable AMPA receptors induce phosphorylation of cAMP response element-binding protein through a phosphatidylinositol 3-kinase-dependent stimulation of the mitogen-activated protein kinase signaling cascade in neurons. J Neurosci 19:5861-5874.
39. Pfenninger K, Ellis L, Johnson M, Friedman L, Somlo S (1983) Nerve growth cones isolated from fetal rat brain: subcellular fractionation and characterization. Cell 35:573-584.
40. Sabo S, McAllister A (2003) Mobility and cycling of synaptic protein-containing vesicles in axonal growth cone filopodia. Nat Neurosci 6:1264-1269.
41. Sans N, Vissel B, Petralia RS, Wang YX, Chang K, Royle GA, Wang CY, O'Gorman S, Heinemann SF, Wenthold RJ (2003) Aberrant formation of glutamate receptor complexes in hippocampal neurons of mice lacking the GluR2 AMPA receptor subunit. J Neurosci 23:9367-9373.
42. Satake S, Saitow F, Yamada J, Konishi S (2000) Synaptic activation of AMPA receptors inhibits GABA release from cerebellar interneurons. Nat Neurosci 3:551-558.
43. Satake S, Saitow F, Rusakov D, Konishi S (2004) AMPA receptor-mediated presynaptic inhibition at cerebellar GABAergic synapses: a characterization of molecular mechanisms. Eur J Neurosci 19:2464-2474.
44. Schenk U, Matteoli M (2004) Presynaptic AMPA receptors: more than just ion channels? Biol Cell 96:257-260.
45. Schenk U, Verderio C, Benfenati F, Matteoli M (2003) Regulated delivery of AMPA receptor subunits to the presynaptic membrane. EMBO J 22:558-568.
46. Tashiro A, Dunaevsky A, Blazeski R, Mason C, Yuste R (2003) Bidirectional regulation of hippocampal mossy fiber filopodial motility by kainate receptors: a two-step model of synaptogenesis. Neuron 38:773-784.
47. Verderio C, Coco S, Fumagalli G, Matteoli M (1994) Spatial changes in calcium signaling during the establishment of neuronal polarity and synaptogenesis. J Cell Biol 126:1527-1536.
48. Verderio C, Coco S, Bacci A, Rossetto O, De CP, Montecucco C, Matteoli M (1999) Tetanus toxin blocks the exocytosis of synaptic vesicles clustered at synapses but not of synaptic vesicles in isolated axons. J Neurosci 19:6723-6732.
49. Wang Y, Durkin J (1995) alpha-Amino-3-hydroxy-5-methyl-4- isoxazolepropionic acid, but not N-methyl-D-aspartate, activates mitogen-activated protein kinase through G-protein beta gamma subunits in rat cortical neurons. J Biol Chem 270:22783-22787.
50. Wang Y, Small D, Stanimirovic D, Morley P, Durkin J (1997) AMPA receptor-mediated regulation of a Gi-protein in cortical neurons. Nature 389:502-504.