Molecular switches at the synapse emerge from receptor and kinase traffic

PLoS Computational Biology

Volumn 1, Issue 2, 2005, Pages 0137-0154

  Hayer, Arnold ^a,b,c   Bhalla, Upinder S ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMES;

BIOCHEMICAL DATA; BIOCHEMICAL EXPERIMENTS; COMPUTER MODELS; MEMORY FORMATION; MOLECULAR SWITCHES; RECEPTORS PROTEINS; REGULATORY PROTEIN; STABLE STATE; SYNAPTIC CONNECTION STRENGTHS; SYNAPTIC STRENGTHS;

MOLECULES;

EID: 33749370872     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.0010020     Document Type: Article

References (63)

1. Ehlers MD (2003) Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat Neurosci 6: 231-242.
2. Roberson ED, Sweatt JD (1999) A biochemical blueprint for long-term memory. Learn Mem 6: 381-388.
3. Lisman JE, McIntyre CC (2001) Synaptic plasticity: A molecular memory switch. Curr Biol 11: R788-R791.
4. Bhalla US, Iyengar R (1999) Emergent properties of networks of biological signaling pathways. Science 283: 381-387.
5. Kuroda S, Schweighofer N, Kawato M (2001) Exploration of signal transduction pathways in cerebellar long-term depression by kinetic simulation. J Neurosci 21: 5693-5702.
6. Blitzer RD, Iyengar R, Landau EM (2005) Postsynaptic signaling networks: Cellular cogwheels underlying long-term plasticity. Biol Psychiatry 57: 113-119.
7. Bhalla US (2004) Signaling in small subcellular volumes. II. Stochastic and diffusion effects on synaptic network properties. Biophys J 87: 745-753.
8. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25: 103-126.
9. Shi S, Hayashi Y, Esteban JA, Malinow R (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105: 331-343.
10. Ehlers MD (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28: 511-525.
11. Esteban JA, Shi SH, Wilson C, Nuriya M, Huganir RL, et al. (2003) PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 6: 136-143.
12. Lee HK, Takamiya K, Han JS, Man H, Kim CH, et al. (2003) Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell 112: 631-643.
13. Wikstrom MA, Matthews P, Roberts D, Collingridge GL, Bortolotto ZA (2003) Parallel kinase cascades are involved in the induction of LTP at hippocampal CA1 synapses. Neuropharmacology 45: 828-836.
14. Shen K, Teruel MN, Connor JH, Shenolikar S, Meyer T (2000) Molecular memory by reversible translocation of calcium/calmodulin-dependent protein kinase II. Nat Neurosci 3: 881-886.
15. Meyer T, Shen K (2000) In and out of the postsynaptic region: Signalling proteins on the move. Trends Cell Biol 10: 238-244.
16. Harris KM, Kater SB (1994) Dendritic spines: Cellular specializations imparting both stability and flexibility to synaptic function. Annu Rev Neurosci 17: 341-371.
17. Bialek W (2001) Stability and noise in biochemical switches. Adv Neural Inf Process Sys 13: 103-109.
18. Montgomery JM, Madison DV (2004) Discrete synaptic states define a major mechanism of synapse plasticity. Trends Neurosci 27: 744-750.
19. Sivakumaran S, Hariharaputran S, Mishra J, Bhalla US (2003) The database of quantitative cellular signaling: Repository and analysis tools for chemical kinetic models of signaling networks. Bioinformatics 19: 408-415.
20. Passafaro M, Piech V, Sheng M (2001) Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat Neurosci 4: 917-926.
21. Lin JW, Ju W, Foster K, Lee SH, Ahmadian G, et al. (2000) Distinct molecular mechanisms and divergent endocytotic pathways of AMPA receptor internalization. Nat Neurosci 3: 1282-1290.
22. Bienenstock EL, Cooper LN, Munro PW (1982) Theory for the development of neuron selectivity: Orientation specificity and binocular interaction in visual cortex. J Neurosci 2: 32-48.
23. Dudek SM, Bear MF (1993) Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J Neurosci 13: 2910-2918.
24. Yang SN, Tang YG, Zucker RS (1999) Selective induction of LTP and LTD by postsynaptic [Ca2+]i elevation. J Neurophysiol 81: 781-787.
25. Bliss TVP, Collingridge GL (1993) A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361: 31-39.
26. Genoux D, Haditsch U, Knobloch M, Michalon A, Storm D, et al. (2002) Protein phosphatase 1 is a molecular constraint on learning and memory. Nature 418: 970-975.
27. Gillespie DT (1977) Exact stochastic simulation of coupled chemical reactions. J Phys Chem 81: 2340-2361.
28. Grutzendler J, Kasthuri N, Gan WB (2002) Long-term dendritic spine stability in the adult cortex. Nature 420: 812-816.
29. 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.
30. Nayak A, Zastrow DJ, Lickteig R, Zahniser NR, Browning MD (1998) Maintenance of late-phase LTP is accompanied by PKA-dependent increase in AMPA receptor synthesis. Nature 394: 680-683.
31. Ju W, Morishita W, Tsui J, Gaietta G, Deerinck TJ, et al. (2004) Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors. Nat Neurosci 7: 244-253.
32. Smith WB, Starck SR, Roberts RW, Schuman EM (2005) Dopaminergic stimulation of local protein synthesis enhances surface expression of GluR1 and synaptic transmission in hippocampal neurons. Neuron 45: 765-779.
33. Bayer KU, De Koninck P, Leonard AS, Hell JW, Schulman H (2001) Interaction with the NMDA receptor locks CaMKII in an active conformation. Nature 411: 801-805.
34. Zhabotinsky AM (2000) Bistability in the Ca(2+)/calmodulin-dependent protein kinase-phosphatase system. Biophys J 79: 2211-2221.
35. Holmes WR (2000) Models of calmodulin trapping and CaM kinase II activation in a dendritic spine. J Comput Neurosci 8: 65-85.
36. Bhalla US (2004) Signaling in small subcellular volumes. I. Stochastic and diffusion effects on individual pathways. Biophys J 87: 733-744.
37. Tomita S, Stein V, Stocker TJ, Nicoll RA, Bredt DS (2005) Bidirectional synaptic plasticity regulated by phosphorylation of stargazin-like TARPs. Neuron 45: 269-277.
38. Bhalla US, Ram PT, Iyengar R (2002) MAP Kinase phosphatase as a locus of flexibility in a mitogen-activated protein kinase signaling network. Science 297: 1018-1023.
39. Wu GY, Deisseroth K, Tsien RW (2001) Spaced stimuli stabilize MAPK pathway activation and its effects on dendritic morphology. Nat Neurosci 4: 151-158.
40. Ajay SM, Bhalla US (2004) A role for ERKII in synaptic pattern selectivity on the time-scale of minutes. Eur J Neurosci 20: 2671-2680.
41. Markevich NI, Hoek JB, Kholodenko BN (2004) Signaling switches and bistability arising from multisite phosphorylation in protein kinase cascades. J Cell Biol 164: 353-359.
42. Miller P, Zhabotinsky AM, Lisman JE, Wang XJ (2005) The stability of a stochastic CaMKII switch: Dependence on the number of enzyme molecules and protein turnover. PLoS Biol 3: el07. DOI: 10.1371/journal. pbio.0030107
43. Groc L, Heine M, Cognet L, Brickley K, Stephenson FA, et al. (2004) Differential activity-dependent regulation of the lateral mobilities of AMPA and NMDA receptors. Nat Neurosci 7: 695-696.
44. Rosenmund C, Stern-Bach Y, Stevens CF (1998) The tetrameric structure of a glutamate receptor channel. Science 280: 1596-1599.
45. Rosenmund C, Carr DW, Bergeson SE, Nilaver G, Scott JD, et al. (1994) Anchoring of protein kinase A is required for modulation of AMPA/kainate receptors on hippocampal neurons. Nature 368: 853-856.
46. Morishita W, Connor JH, Xia H, Quinlan EM, Shenolikar S, et al. (2001) Regulation of synaptic strength by protein phosphatase 1. Neuron 32: 1133-1148.
47. Zeng H, Chattarji S, Barbarosie M, Rondi-Reig L, Philpot BD, et al. (2001) Forebrain-speciflc calcineurin knockout selectively impairs bidirectional synaptic plasticity and working/episodic-like memory. Cell 107: 617-629.
48. Beattie EC, Carroll RC, Yu X, Morishita W, Yasuda H, et al. (2000) Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nat Neurosci 3: 1291-1300.
49. Derkach V, Barria A, Soderling TR (1999) Ca2+/calmodulin-kinase II enhances channel conductance of alpha-amino-3-hydroxy-5-methyl-4- isoxazolepropionate type glutamate receptors. Proc Natl Acad Sci USA 96: 3269-3274.
50. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, lino M, et al. (2001) Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci 4: 1086-1092.
51. Bhalla US (2002) Mechanisms for temporal tuning and filtering by postsynaptic signaling pathways. Biophys J 83: 740-752.
52. Colbran RJ, Bass MA, McNeill RB, Bollen M, Zhao S, et al. (1997) Association of brain protein phosphatase 1 with cytoskeletal targeting/ regulatory subunits. J Neurochem 69: 920-929.
53. Sim AT, Ratcliffe E, Mumby MC, Villa-Moruzzi E, Rostas JA (1994) Differential activities of protein phosphatase types 1 and 2A in cytosolic and particulate fractions from rat forebrain. J Neurochem 62: 1552-1559.
54. Strack S, Barban MA, Wadzinski BE, Colbran RJ (1997) Differential inactivation of postsynaptic density-associated and soluble Ca2+/Cal-modulin- dependent protein kinase II by protein phosphatases 1 and 2A. J Neurochem 68: 2119-2128.
55. Shen K, Meyer T (1999) Dynamic control of CaMKII translocation and localization in hippocampal neurons by NMDA receptor stimulation. Science 284: 162-166.
56. Gardoni F, Caputi A, Cimino M, Pastorino L, Cattabeni F, et al. (1998) Calcium/calmodulin-dependent protein kinase II is associated with NR2A/B subunits of NMDA receptor in postsynaptic densities. J Neurochem 71: 1733-1741.
57. Gardoni F, Schrama LH, van DalenJJ, Gispen WH, Cattabeni F, et al. (1999) AlphaCaMKII binding to the C-terminal tail of NMDA receptor subunit NR2A and its modulation by autophosphorylation. FEBS Lett 456: 394-398.
58. Suzuki T, Okumura-Noji K, Tanaka R, Tada T (1994) Rapid translocation of cytosolic Ca2+/calmodulin-dependent protein kinase II into postsynaptic density after decapitation. J Neurochem 63: 1529-1537.
59. Elgersma Y, Fedorov NB, Ikonen S, Choi ES, Elgersma M, et al. (2002) Inhibitory autophosphorylation of CaMKII controls PSD association, plasticity, and learning. Neuron 36: 493-505.
60. Chen C, Nakamura T, Koutalos Y (1999) Cyclic AMP diffusion coefficient in frog olfactory cilia. Biophys J 76: 2861-2867.
61. Bhalla US (2002) Use of Kinetikit and GENESIS for modeling signaling pathways. In: Hildebrandt JD, Iyengar R, editors. Methods in enzymology, Volume 345. San Diego: Academic Press, pp. 3-23
62. Vasudeva K, Bhalla US (2004) Adaptive stochastic-deterministic chemical kinetic simulations. Bioinformatics 20: 78-84.
63. Matsumoto M, Nishimura T (1998) Mersenne Twister: A 623-dimensionally equidistributed uniform pseudorandom number generator. ACM Trans Model Comput Simul 8: 3-30.