Multiple roles for mammalian target of rapamycin signaling in both glutamatergic and GABAergic synaptic transmission

Journal of Neuroscience

Volumn 32, Issue 33, 2012, Pages 11441-11452

  Weston, Matthew C ^a,b   Chen, Hongmei ^a,b   Swann, John W ^a,b  

^a Cain Foundation Laboratories   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMIC ACID; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3, 4, 5 TRISPHOSPHATE 3 PHOSPHATASE; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EVOKED RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; GABAERGIC TRANSMISSION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; MINIATURE ENDPLATE POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BIOPHYSICS; CORPUS STRIATUM; DENDRITES; DNA-BINDING PROTEINS; ELECTRIC STIMULATION; FEMALE; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATES; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; HUMANS; MALE; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURONS; NUCLEAR PROTEINS; PATCH-CLAMP TECHNIQUES; PTEN PHOSPHOHYDROLASE; SIGNAL TRANSDUCTION; SIROLIMUS; SODIUM CHANNEL BLOCKERS; SYNAPSES; SYNAPTIC TRANSMISSION; TETRODOTOXIN; TIME FACTORS; TOR SERINE-THREONINE KINASES; TRANSFECTION; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS;

EID: 84864965624     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1283-12.2012     Document Type: Article

References (45)

1. Akerman CJ, Cline HT (2007) Refining the roles of GABAergic signaling during neural circuit formation. Trends Neurosci 30:382-389.
2. Backman SA, Stambolic V, Suzuki A, Haight J, Elia A, Pretorius J, Tsao MS, Shannon P, Bolon B, Ivy GO, Mak TW (2001) Deletion of Pten in mouse brain causes seizures, ataxia and defects in soma size resembling Lhermitte-Duclos disease. Nat Genet 29:396-403.
3. Bateup HS, Takasaki KT, Saulnier JL, Denefrio CL, Sabatini BL (2011) Loss of Tsc1 in vivo impairs hippocampal mGluR-LTD and increases excit- atory synaptic function. J Neurosci 31:8862-8869.
4. Bekkers JM, Stevens CF (1991) Excitatory and inhibitory autaptic currents in isolated hippocampal neurons maintained in cell culture. Proc Natl Acad Sci U S A 88:7834-7838.
5. Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL (1989) Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol, 416:303-325.
6. Buckmaster PS, Wen X (2011) Rapamycin suppresses axon sprouting by somatostatin interneurons in a mouse model of temporal lobe epilepsy. Epilepsia, 52:2057-2064.
7. Cohen I, Navarro V, Clemenceau S, Baulac M, Miles R (2002) On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 298:1418-1421.
8. Costa-Mattioli M, Sossin WS, Klann E, Sonenberg N (2009) Translational control of long-lasting synaptic plasticity and memory. Neuron 61:10-26.
9. del Castillo J, Katz B (1954) Quantal components of the end-plate potential. J Physiol, 124:560-573.
10. Fraser MM, Bayazitov IT, Zakharenko SS, Baker SJ (2008) Phosphatase and tensin homolog, deleted on chromosome 10 deficiency in brain causes defects in synaptic structure, transmission and plasticity, and myelination abnormalities. Neuroscience, 151:476-488.
11. Fu C, Cawthon B, Clinkscales W, Bruce A, Winzenburger P, Ess KC (2011) GABAergic interneuron development and function is modulated by the tsc1 gene. Cereb Cortex. Advance online publication. Retrieved October 20, 2011. doi:10.1093/cercor/bhr300.
12. Greenwood JS, Wang Y, Estrada RC, Ackerman L, Ohara PT, Baraban SC (2009) Seizures, enhanced excitation, and increased vesicle number in Lis1 mutant mice. Ann Neurol 66:644-653.
13. Habets RL, Borst JG (2005) Post-tetanic potentiation in the rat calyx of Held synapse. J Physiol, 564:173-187.
14. Heitman J, Movva NR, Hall MN (1991) Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science, 253:905-909.
15. Hoeffer CA, Klann E (2010) mTOR signaling: at the crossroads of plasticity, memory and disease. Trends Neurosci, 33:67-75.
16. Jaworski J, Spangler S, Seeburg DP, Hoogenraad CC, Sheng M (2005) Control of dendritic arborization by the phosphoinositide-3 -kinase-Aktmammalian target of rapamycin pathway. J Neurosci, 25:11300-11312.
17. Jones DL, Baraban SC (2007) Characterization of inhibitory circuits in the malformed hippocampus of Lis1 mutant mice. J Neurophysiol, 98:2737-2746.
18. Jurado S, Benoist M, Lario A, Knafo S, Petrok CN, Esteban JA (2010) PTEN is recruited to the postsynaptic terminal for NMDA receptor-dependentlong-term depression. EMBO J, 29:2827-2840.
19. Khalilov I, Le Van Quyen M, Gozlan H, Ben-Ari Y (2005) Epileptogenic actions of GABA and fast oscillations in the developing hippocampus. Neuron, 48:787-796.
20. Kwon CH, Zhu X, Zhang J, Knoop LL, Tharp R, Smeyne RJ, Eberhart CG, Burger PC, Baker SJ (2001) Pten regulates neuronal soma size: a mouse model of Lhermitte-Duclos disease. Nat Genet, 29:404-411.
21. Kwon CH, Luikart BW, Powell CM, Zhou J, Matheny SA, Zhang W, Li Y, Baker SJ, Parada LF (2006) Pten regulates neuronal arborization and social interaction in mice. Neuron, 50:377-388.
22. Ljungberg MC, Sunnen CN, Lugo JN, Anderson AE, D'Arcangelo G (2009) Rapamycin suppresses seizures and neuronal hypertrophy in a mouse model of cortical dysplasia. Dis Model Mech, 2:389 -398.
23. Lois C, Hong EJ, Pease S, Brown EJ, Baltimore D (2002) Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science, 295:868-872.
24. Luikart BW, Schnell E, Washburn EK, Bensen AL, Tovar KR, Westbrook GL (2011) Pten knockdown in vivo increases excitatory drive onto dentate granule cells. J Neurosci, 31:4345-4354.
25. Meikle L, Talos DM, Onda H, Pollizzi K, Rotenberg A, Sahin M, Jensen FE, Kwiatkowski DJ (2007) A mouse model of tuberous sclerosis: neuronal loss of Tsc1 causes dysplastic and ectopic neurons, reduced myelination, seizure activity, and limited survival. J Neurosci, 27:5546-5558.
26. Moult PR, Cross A, Santos SD, Carvalho AL, Lindsay Y, Connolly CN, Irving AJ, Leslie NR, Harvey J (2010) Leptin regulates AMPA receptor trafficking via PTEN inhibition. J Neurosci, 30:4088-4101.
27. Mueller AL, Taube JS, Schwartzkroin PA (1984) Development of hyperpolarizing inhibitory postsynaptic potentials and hyperpolarizing response to gamma-aminobutyric acid in rabbit hippocampus studied in vitro. J Neurosci, 4:860-867.
28. Murthy VN, Schikorski T, Stevens CF, Zhu Y (2001) Inactivity produces increases in neurotransmitter release and synaptic size. Neuron 32:673-682.
29. Orlova KA, Parker WE, Heuer GG, Tsai V, Yoon J, Baybis M, Fenning RS, Strauss K, Crino PB (2010) STRADalpha deficiency results in aberrant mTORC1 signaling during corticogenesis in humans and mice. J Clin Invest, 120:1591-1602.
30. Reim K, Mansour M, Varoqueaux F, McMahon HT, Sudhof TC, Brose N, Rosenmund C (2001) Complexins regulate a late step in Ca2 dependent neurotransmitter release. Cell 104:71-81.
31. Rosenmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16:1197-1207.
32. Rost BR, Breustedt J, Schoenherr A, Grosse G, Ahnert-Hilger G, Schmitz D (2010) Autaptic cultures of single hippocampal granule cells of mice and rats. Eur J Neurosci, 32:939-947.
33. Sarbassov DD, Ali SM, Sengupta S, Sheen JH, Hsu PP, Bagley AF, Markhard AL, Sabatini DM (2006) Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol Cell, 22:159-168.
34. Stevens CF (2003) Neurotransmitter release at central synapses. Neuron, 39:381-388.
35. Tabuchi K, Blundell J, Etherton MR, Hammer RE, Liu X, Powell CM, Sudhof TC (2007) A neuroligin-3 mutation implicated in autism increases in-hibitory synaptic transmission in mice. Science 318:71-76.
36. Tavazoie SF, Alvarez VA, Ridenour DA, Kwiatkowski DJ, Sabatini BL (2005) Regulation of neuronal morphology and function by the tumor suppressors Tsc1 and Tsc2. Nat Neurosci, 8:1727-1734.
37. Tyler WJ, Pozzo-Miller LD (2001) BDNF enhances quantal neurotransmit ter release and increases the number of docked vesicles at the active zones of hippocampal excitatory synapses. J Neurosci, 21:4249-4258.
38. van Spronsen M, Hoogenraad CC (2010) Synapse pathology in psychiatric and neurologic disease. Curr Neurol Neurosci Rep 10:207-214.
39. Waites CL, Garner CC (2011) Presynaptic function in health and disease. Trends Neurosci, 34:326-337.
40. Wang Y, Barbaro MF, Baraban SC (2006) A role for the mTOR pathway in surface expression of AMPA receptors. Neurosci Lett 401:35-39.
41. Wang Y, Greenwood JS, Calcagnotto ME, Kirsch HE, Barbaro NM, Baraban SC (2007) Neocortical hyperexcitability in a human case of tuberous sclerosis complex and mice lacking neuronal expression of TSC1. Ann Neurol, 61:139-152.
42. Xiong Q, Oviedo HV, Trotman LC, Zador AM (2012) PTEN regulation of local and long-range connections in mouse auditory cortex. J Neurosci 32:1643-1652.
43. Xue M, Stradomska A, Chen H, Brose N, Zhang W, Rosenmund C, Reim K (2008) Complexins facilitate neurotransmitter release at excitatory and inhibitory synapses in mammalian central nervous system. Proc Natl Acad Sci U S A 105:7875-7880.
44. Zhou J, Blundell J, Ogawa S, Kwon CH, Zhang W, Sinton C, Powell CM, Parada LF (2009) Pharmacological inhibition of mTORC1 suppresses anatomical, cellular, and behavioral abnormalities in neural-specific Pten knockout mice. J Neurosci 29:1773-1783.
45. Zoghbi HY (2003) Postnatal neurodevelopmental disorders: meeting at the synapse? Science 302:826-830.