Synaptic stimulation of mTOR is mediated by Wnt signaling and regulation of glycogen synthetase kinase-3

Journal of Neuroscience

Volumn 31, Issue 48, 2011, Pages 17537-17546

  Ma, Tao ^a,b   Tzavaras, Nikos ^a   Tsokas, Panayiotis ^a,c   Landau, Emmanuel M ^a   Blitzer, Robert D ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c SUNY Downstate Medical Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1, 4 DIAMINO 1, 4 BIS (2 AMINOPHENYLTHIO) 2, 3 DICYANOBUTADIENE; 2 (2 AMINO 3 METHOXYPHENYL) CHROMONE; 2 AMINO 5 PHOSPHONOVALERIC ACID; EMETINE; FRIZZLED PROTEIN; GLYCOGEN SYNTHASE KINASE 3; ISOPRENALINE; KENPAULLONE; LITHIUM CHLORIDE; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NIFEDIPINE; PROTEIN KINASE B; PROTEIN KINASE B INHIBITOR; RAPAMYCIN; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; WNT PROTEIN;

ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTROPHYSIOLOGY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NERVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; GLYCOGEN SYNTHASE KINASE 3; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; NEURONS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES; TOR SERINE-THREONINE KINASES; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 82555174660     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4761-11.2011     Document Type: Article

References (40)

1. Asuni AA, Hooper C, Reynolds CH, Lovestone S, Anderton BH, Killick R (2006) GSK3α exhibits β-catenin and tau directed kinase activities that are modulated by Wnt. Eur J Neurosci 24:3387-3392.
2. Brown EJ, Beal PA, Keith CT, Chen J, Shin TB, Schreiber SL (1995) Control of p70 s6 kinase by kinase activity of FRAP in vivo. Nature 377:441-446.
3. Cai X, Liang CW, Muralidharan S, Kao JP, Tang CM, Thompson SM (2004) Unique roles of SK and Kv4.2 potassium channels in dendritic integration. Neuron 44:351-364.
4. Cammalleri M, Lütjens R, Berton F, King AR, Simpson C, Francesconi W, Sanna PP (2003) Time-restricted role for dendritic activation of the mTOR-p70S6K pathway in the induction of late-phase long-term potentiation in the CA1. Proc Natl Acad Sci U S A 100:14368-14373.
5. Chen J, Park CS, Tang SJ (2006) Activity-dependent synaptic Wnt release regulates hippocampal long term potentiation. J Biol Chem 281:11910-11916.
6. Decker MW, McGaugh JL (1991) The role of interactions between the cholinergic system and other neuromodulatory systems in learning and memory. Synapse 7:151-168.
7. Doble BW, Patel S, Wood GA, Kockeritz LK, Woodgett JR (2007) Functional redundancy of GSK-3alpha and GSK-3beta in Wnt/beta-catenin signaling shown by using an allelic series of embryonic stem cell lines. Developmental cell 12:957-971.
8. Frey U, Morris RG (1997) Synaptic tagging and long-term potentiation. Nature 385:533-536.
9. Frödin M, Jensen CJ, Merienne K, Gammeltoft S (2000) A phosphoserineregulated docking site in the protein kinase RSK2 that recruits and activates PDK1. EMBO J 19:2924-2934.
10. Gafford GM, Parsons RG, Helmstetter FJ (2011) Consolidation and reconsolidation of contextual fear memory requires mammalian target of rapamycin-dependent translation in the dorsal hippocampus. Neuroscience 182:98-104.
11. Gelinas JN, Banko JL, Hou L, Sonenberg N, Weeber EJ, Klann E, Nguyen PV (2007) ERK and mTOR signaling couple beta-adrenergic receptors to translation initiation machinery to gate induction of protein synthesisdependent long-term potentiation. J Biol Chem 282:27527-27535.
12. Hahn-Windgassen A, Nogueira V, Chen CC, Skeen JE, Sonenberg N, Hay N (2005) Akt activates the mammalian target of rapamycin by regulating cellular ATP level and AMPK activity. J Biol Chem 280:32081-32089.
13. Hernández F, Borrell J, Guaza C, Avila J, Lucas JJ (2002) Spatial learning deficit in transgenic mice that conditionally over-express GSK-3beta in the brain but do not form tau filaments. J Neurochem 83:1529-1533.
14. 2+ channels in dendritic spines by activation of beta2 adrenergic receptors. J Neurosci 24:8416-8427.
15. Hooper C, Killick R, Lovestone S (2008) The GSK3 hypothesis of Alzheimer's disease. J Neurochem 104:1433-1439.
16. Inoki K, Ouyang H, Zhu T, Lindvall C, Wang Y, Zhang X, Yang Q, Bennett C, Harada Y, Stankunas K, Wang CY, He X, MacDougald OA, You M, Williams BO, Guan KL (2006) TSC2 integrates Wnt and energy signals via a coordinated phosphorylation byAMPKand GSK3 to regulate cell growth. Cell 126:955-968.
17. Kwon G, Marshall CA, Liu H, Pappan KL, Remedi MS, McDaniel ML (2006) Glucose-stimulated DNA synthesis through mammalian target of rapamycin (mTOR) is regulated by KATP channels: effects on cell cycle progression in rodent islets. J Biol Chem 281:3261-3267.
18. Lenz G, Avruch J (2005) Glutamatergic regulation of the p70S6 kinase in primary mouse neurons. J Biol Chem 280:38121-38124.
19. Logan CY, Nusse R (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20:781-810.
20. Ma T, Hoeffer CA, Capetillo-Zarate E, Yu F, Wong H, Lin MT, Tampellini D, Klann E, Blitzer RD, Gouras GK (2010) Dysregulation of the mTOR pathway mediates impairment of synaptic plasticity in a mouse model of Alzheimer's disease. PloS One 5:e12845
21. MacDonald BT, Tamai K, He X (2009) Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 17:9-26.
22. Manning BD, Cantley LC (2007) AKT/PKB signaling: navigating downstream. Cell 129:1261-1274.
23. Meyuhas O, Hornstein E (2000) Translational control of TOP mRNAs. In: Translational control of gene expression (Sonenberg N, Hershey JWB, Mathews MB, eds), pp 671-693.
24. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory. O'Dell TJ, Connor SA, Gelinas JN, Nguyen PV (2010) Viagra for your synapses: enhancement of hippocampal long-term potentiation by activation of beta-adrenergic receptors. Cell Signal 22:728-736.
25. Peineau S, Taghibiglou C, Bradley C, Wong TP, Liu L, Lu J, Lo E, Wu D, Saule E, Bouschet T, Matthews P, Isaac JT, Bortolotto ZA, Wang YT, Collingridge GL (2007) LTP inhibits LTD in the hippocampus via regulation of GSK3beta. Neuron 53:703-717.
26. Peterson RT, Beal PA, Comb MJ, Schreiber SL (2000) FKBP12-rapamycinassociated protein (FRAP) autophosphorylates at serine 2481 under translationally repressive conditions. J Biol Chem 275:7416-7423.
27. Sancak Y, Thoreen CC, Peterson TR, Lindquist RA, Kang SA, Spooner E, Carr SA, Sabatini DM (2007) PRAS40 is an insulin-regulated inhibitor of the mTORC1 protein kinase. Mol Cell 25:903-915.
28. Schrader LA, Birnbaum SG, Nadin BM, Ren Y, Bui D, Anderson AE, Sweatt JD (2006) ERK/MAPK regulates the Kv4.2 potassium channel by direct phosphorylation of the pore-forming subunit. Am J Physiol Cell Physiol 290:C852-861.
29. Srivastava AK, Pandey SK (1998) Potential mechanism(s) involved in the regulation of glycogen synthesis by insulin. Mol Cell Biochem 182: 135-141.
30. Stoica L, Zhu PJ, Huang W, Zhou H, Kozma SC, Costa-Mattioli M (2011) Selective pharmacogenetic inhibition of mammalian target of Rapamycin complex I (mTORC1) blocks long-term synaptic plasticity and memory storage. Proc Natl Acad Sci U S A 108:3791-3796.
31. Tang X, Wang L, Proud CG, Downes CP (2003) Muscarinic receptormediated activation of p70 S6 kinase 1 (S6K1) in 1321N1 astrocytoma cells: permissive role of phosphoinositide 3-kinase. Biochem J 374: 137-143.
32. Teyler TJ, Cavus I, Coussens C, DiScenna P, Grover L, Lee YP, Little Z (1994) Multideterminant role of calcium in hippocampal synaptic plasticity. Hippocampus 4:623-634.
33. Tsokas P, Grace EA, Chan P, Ma T, Sealfon SC, Iyengar R, Landau EM, Blitzer RD (2005) Local protein synthesis mediates a rapid increase in dendritic elongation factor 1A after induction of late long-term potentiation. J Neurosci 25:5833-5843.
34. Tsokas P, Ma T, Iyengar R, Landau EM, Blitzer RD (2007) Mitogenactivated protein kinase upregulates the dendritic translation machinery in long-term potentiation by controlling the mammalian target of rapamycin pathway. J Neurosci 27:5885-5894.
35. Tully K, Bolshakov VY (2010) Emotional enhancement of memory: how norepinephrine enables synaptic plasticity. Mol Brain 3:15.
36. Vander Haar E, Lee SI, Bandhakavi S, Griffin TJ, Kim DH (2007) Insulin signalling tomTORmediated by the Akt/PKB substrate PRAS40. Nat Cell Biol 9:316-323.
37. Vigneron F, Dos Santos P, Lemoine S, Bonnet M, Tariosse L, Couffinhal T, Duplaa C, Jaspard-Vinassa B (2011) GSK-3b at the crossroads in the signalling of heart preconditioning: implication of mTOR and Wnt pathways. Cardiovasc Res 90:49-56.
38. Wang L, Harris TE, Roth RA, Lawrence JC Jr (2007) PRAS40 regulates mTORC1 kinase activity by functioning as a direct inhibitor of substrate binding. J Biol Chem 282:20036-20044.
39. Woodgett JR (1990) Molecular cloning and expression of glycogen synthase kinase-3/factor A. EMBO J 9:2431-2438.
40. + channels in hippocampus involves a mitogen-activated protein kinase pathway. J Neurosci 22:4860-4868.