PIKE-mediated PI3-kinase activity is required for AMPA receptor surface expression

EMBO Journal

Volumn 30, Issue 20, 2011, Pages 4274-4286

  Chan, Chi Bun ^a   Chen, Yongjun ^b   Liu, Xia ^a   Tang, Xiaoling ^a   Lee, Chi Wai ^a   Mei, Lin ^b   Ye, Keqiang ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

GluA2; GRIP1; LTP; PI3K; PIKE

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR; GLYCINE; GUANOSINE TRIPHOSPHATASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NUCLEAR RECEPTOR COACTIVATOR 2; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE ENHANCER; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ASSOCIATION; HIPPOCAMPUS; HUMAN; HUMAN CELL; LONG TERM POTENTIATION; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BRAIN; CARRIER PROTEINS; CELLS, CULTURED; GLYCINE; GTP PHOSPHOHYDROLASES; GTP-BINDING PROTEINS; GTPASE-ACTIVATING PROTEINS; HEK293 CELLS; HUMANS; LONG-TERM POTENTIATION; MICE; MONOMERIC GTP-BINDING PROTEINS; NERVE TISSUE PROTEINS; NEURONS; PHOSPHATIDYLINOSITOL 3-KINASES; RATS; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 80054913696     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.281     Document Type: Article

References (54)

1. Ahn JY, Rong R, Kroll TG, Van Meir EG, Snyder SH, Ye K (2004) PIKE (phosphatidylinositol 3-kinase enhancer)-A GTPase stimulates Akt activity and mediates cellular invasion. J Biol Chem 279: 16441-16451 (Pubitemid 38509342)
2. Arendt KL, Royo M, Fernandez-Monreal M, Knafo S, Petrok CN, Martens JR, Esteban JA (2010) PIP3 controls synaptic function by maintaining AMPA receptor clustering at the postsynaptic membrane. Nat Neurosci 13: 36-44
3. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31-39 (Pubitemid 23020772)
4. Burnashev N, Monyer H, Seeburg PH, Sakmann B (1992) Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron 8: 189-198
5. Capocchi G, Zampolini M, Larson J (1992) Theta burst stimulation is optimal for induction of LTP at both apical and basal dendritic synapses on hippocampal CA1 neurons. Brain Res 591: 332-336
6. Chan CB, Ye K (2007) PIKE GTPase are phosphoinositide-3-kinase enhancers, suppressing programmed cell death. J Cell Mol Med 11 : 39-53 (Pubitemid 46439624)
7. Chen YJ, Zhang M, Yin DM, Wen L, Ting A, Wang P, Lu YS, Zhu XH, Li SJ, Wu CY, Wang XM, Lai C, Xiong WC, Mei L, Gao TM (2010) ErbB4 in parvalbumin-positive interneurons is critical for neu-regulin 1 regulation of long-term potentiation. Proc Natl Acad Sci USA 107: 21818-21823
8. Choi SY, Chang J, Jiang B, Seol GH, Min SS, Han JS, Shin HS, Gallagher M, Kirkwood A (2005) Multiple receptors coupled to phospholipase C gate long-term depression in visual cortex. J Neurosci 25: 11433-11443 (Pubitemid 43083715)
9. Costa-Mattioli M, Sossin WS, Klann E, Sonenberg N (2009) Translational control of long-lasting synaptic plasticity and memory. Neuron 61: 10-26
10. Dong H, O'Brien RJ, Fung ET, Lanahan AA, Worley PF, Huganir RL (1997) GRIP: a synaptic PDZ domain-containing protein that interacts with AMPA receptors. Nature 386: 279-284 (Pubitemid 27142513)
11. Genoux D, Montgomery JM (2007) Glutamate receptor plasticity at excitatory synapses in the brain. Clin Exp Pharmacol Physiol 34: 1058-1063 (Pubitemid 47274556)
12. Gurd JW, Bissoon N (1997) The N-methyl-D-aspartate receptor subunits NR2A and NR2B bind to the SH2 domains of phospho-lipase C-gamma. J Neurochem 69: 623-630 (Pubitemid 27327963)
13. Hoogenraad CC, Milstein AD, Ethell IM, Henkemeyer M, Sheng M (2005) GRIP1 controls dendrite morphogenesis by regulating EphB receptor trafficking. Nat Neurosci 8: 906-915
14. Horne EA, Dell'Acqua ML (2007) Phospholipase C is required for changes in postsynaptic structure and function associated with NMDA receptor-dependent long-term depression. J Neurosci 27: 3523-3534 (Pubitemid 46515123)
15. Horwood JM, Dufour F, Laroche S, Davis S (2006) Signalling mechanisms mediated by the phosphoinositide 3-kinase/Akt cascade in synaptic plasticity and memory in the rat. Eur J Neurosci 23: 3375-3384
16. Johnson JW, Ascher P (1987) Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325: 529-531 (Pubitemid 17056733)
17. 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 (Pubitemid 16046186)
18. Lin DT, Makino Y, Sharma K, Hayashi T, Neve R, Takamiya K, Huganir RL (2009) Regulation of AMPA receptor extrasynaptic insertion by 4.1N, phosphorylation and palmitoylation. Nat Neurosci 12: 879-887
19. Lissin DV, Gomperts SN, Carroll RC, Christine CW, Kalman D, Kitamura M, Hardy S, Nicoll RA, Malenka RC, von Zastrow M (1998) Activity differentially regulates the surface expression of synaptic AMPA and NMDA glutamate receptors. Proc Natl Acad Sci USA 95: 7097-7102 (Pubitemid 28278113)
20. Liu Z, Jang SW, Liu X, Cheng D, Peng J, Yepes M, Li XJ, Matthews S, Watts C, Asano M, Hara-Nishimura I, Luo HR, Ye K (2008) Neuroprotective actions of PIKE-L by inhibition of SET proteo-lytic degradation by asparagine endopeptidase. Mol Cell 29: 665-678 (Pubitemid 351400928)
21. Lu W, Man H, Ju W, Trimble WS, MacDonald JF, Wang YT (2001) Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron 29: 243-254 (Pubitemid 32108736)
22. Lu W, Ziff EB (2005) PICK1 interacts with ABP/GRIP to regulate AMPA receptor trafficking. Neuron 47: 407-421 (Pubitemid 41073881)
23. Man HY, Sekine-Aizawa Y, Huganir RL (2007) Regulation of {alpha}-amino-3-hydroxy-5-methyl-4-isoxazolepropioni. Proc Natl Acad Sci USA 104: 3579-3584
24. Man HY, Wang Q, Lu WY, Ju W, Ahmadian G, Liu L, D'Souza S, Wong TP, Taghibiglou C, Lu J, Becker LE, Pei L, Liu F, Wymann MP, MacDonald JF, Wang YT (2003) Activation of PI3-kinase is required for AMPA receptor insertion during LTP of mEPSCs in cultured hippocampal neurons. Neuron 38: 611-624 (Pubitemid 36645035)
25. Matsuda S, Mikawa S, Hirai H (1999) Phosphorylation of serine-880 in GluR2 by protein kinase C prevents its C terminus from binding with glutamate receptor-interacting protein. J Neurochem 73: 1765-1768 (Pubitemid 29440182)
26. Muller D, Toni N, Buchs PA (2000) Spine changes associated with long-term potentiation. Hippocampus 10: 596-604
27. Nishimoto T, Kihara T, Akaike A, Niidome T, Sugimoto H (2008) alpha-Amino-3-hydroxy-5-methyl-4-isoxazole propionate attenuates glutamate-induced caspase-3 cleavage via regulation of glycogen synthase kinase 3beta. J Neurosci Res 86: 1096-1105 (Pubitemid 351441307)
28. Nishimune A, Isaac JT, Molnar E, Noel J, Nash SR, Tagaya M, Collingridge GL, Nakanishi S, Henley JM (1998) NSF binding to GluR2 regulates synaptic transmission. Neuron 21 : 87-97 (Pubitemid 28355694)
29. Opazo P, Watabe AM, Grant SG, O'Dell TJ (2003) Phosphatidyl-inositol 3-kinase regulates the induction of long-term potentiation through extracellular signal-related kinase-independent mechanisms. J Neurosci 23: 3679-3688 (Pubitemid 36958476)
30. Osten P, Khatri L, Perez JL, Kohr G, Giese G, Daly C, Schulz TW, Wensky A, Lee LM, Ziff EB (2000) Mutagenesis reveals a role for ABP/GRIP binding to GluR2 in synaptic surface accumulation of the AMPA receptor. Neuron 27: 313-325
31. Palmer CL, Cotton L, Henley JM (2005) The molecular pharmacology and cell biology of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors. Pharmacol Rev 57: 253-277 (Pubitemid 41043886)
32. 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 (Pubitemid 46283369)
33. Perestenko PV, Henley JM (2003) Characterization of the intra-cellular transport of GluR1 and GluR2 alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptor subunits in hippocampal neurons. J Biol Chem 278: 43525-43532 (Pubitemid 37345976)
34. Reyes-Harde M, Stanton PK (1998) Postsynaptic phospholipase C activity is required for the induction of homosynaptic long-term depression in rat hippocampus. Neurosci Lett 252: 155-158 (Pubitemid 28400647)
35. Rong R, Ahn JY, Huang H, Nagata E, Kalman D, Kapp JA, Tu J, Worley PF, Snyder SH, Ye K (2003) PI3 kinase enhancer-Homer complex couples mGluRI to PI3 kinase, preventing neuronal apoptosis. Nat Neurosci 6: 1153-1161 (Pubitemid 37346035)
36. Rosenmund C, Stern-Bach Y, Stevens CF (1998) The tetrameric structure of a glutamate receptor channel. Science 280: 1596-1599 (Pubitemid 28277703)
37. Sanna PP, Cammalleri M, Berton F, Simpson C, Lutjens R, Bloom FE, Francesconi W (2002) Phosphatidylinositol 3-kinase is required for the expression but not for the induction or the maintenance of long-term potentiation in the hippocampal CA1 region. J Neurosci 22: 3359-3365 (Pubitemid 37465741)
38. 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 hippo-campal neurons of mice lacking the GluR2 AMPA receptor subunit. J Neurosci 23: 9367-9373 (Pubitemid 37323036)
39. Santos SD, Carvalho AL, Caldeira MV, Duarte CB (2009) Regulation of AMPA receptors and synaptic plasticity. Neuroscience 158: 105-125
40. Setou M, Seog DH, Tanaka Y, Kanai Y, Takei Y, Kawagishi M, Hirokawa N (2002) Glutamate-receptor-interacting protein GRIP1 directly steers kinesin to dendrites. Nature 417: 83-87 (Pubitemid 34498820)
41. Shen L, Liang F, Walensky LD, Huganir RL (2000) Regulation of AMPA receptor GluR1 subunit surface expression by a 4. 1N-linked actin cytoskeletal association. J Neurosci 20: 7932-7940
42. Shi SH, Hayashi Y, Petralia RS, Zaman SH, Wenthold RJ, Svoboda K, Malinow R (1999) Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284: 1811-1816
43. Song I, Huganir RL (2002) Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci 25: 578-588 (Pubitemid 35254182)
44. Srivastava S, Osten P, Vilim FS, Khatri L, Inman G, States B, Daly C, DeSouza S, Abagyan R, Valtschanoff JG, Weinberg RJ, Ziff EB (1998) Novel anchorage of GluR2/3 to the postsynaptic density by the AMPA receptor-binding protein ABP. Neuron 21: 581-591 (Pubitemid 28475509)
45. Tang X, Jang SW, Okada M, Chan CB, Feng Y, Liu Y, Luo SW, Hong Y, Rama N, Xiong WC, Mehlen P, Ye K (2008) Netrin-1 mediates neuronal survival through PIKE-L interaction with the dependence receptor UNC5B. Nat Cell Biol 10 : 698-706 (Pubitemid 351772935)
46. Wu X, Zhu D, Jiang X, Okagaki P, Mearow K, Zhu G, McCall S, Banaudha K, Lipsky RH, Marini AM (2004) AMPA protects cultured neurons against glutamate excitotoxicity through a phosphatidylinositol 3-kinase-dependent activation in extracellular signal-regulated kinase to upregulate BDNF gene expression. J Neurochem 90: 807-818 (Pubitemid 39099962)
47. Wyszynski M, Valtschanoff JG, Naisbitt S, Dunah AW, Kim E, Standaert DG, Weinberg R, Sheng M (1999) Association of AMPA receptors with a subset of glutamate receptor-interacting protein in vivo. J Neurosci 19: 6528-6537 (Pubitemid 29347452)
48. Xia J, Zhang X, Staudinger J, Huganir RL (1999) Clustering of AMPA receptors by the synaptic PDZ domain-containing protein PICK1. Neuron 22: 179-187 (Pubitemid 29070104)
49. Ye K, Aghdasi B, Luo HR, Moriarity JL, Wu FY, Hong JJ, Hurt KJ, Bae SS, Suh PG, Snyder SH (2002) Phospholipase C gamma 1 is a physiological guanine nucleotide exchange factor for the nuclear GTPase PIKE. Nature 415: 541-544 (Pubitemid 34130610)
50. Ye K, Compton DA, Lai MM, Walensky LD, Snyder SH (1999) Protein 4.1N binding to nuclear mitotic apparatus protein in PC12 cells mediates the antiproliferative actions of nerve growth factor. J Neurosci 19: 10747-10756 (Pubitemid 30235721)
51. Ye K, Hurt KJ, Wu FY, Fang M, Luo HR, Hong JJ, Blackshaw S, Ferris CD, Snyder SH (2000) Pike. A nuclear GTPase that enhances PI3kinase activity and is regulated by protein 4.1N. Cell 103: 919-930
52. Zhang J, Wang Y, Chi Z, Keuss MJ, Pai YM, Kang HC, Shin JH, Bugayenko A, Wang H, Xiong Y, Pletnikov MV, Mattson MP, Dawson TM, Dawson VL (2011) The AAA(+) ATPase thorase regulates AMPA receptor-dependent synaptic plasticity and behavior. Cell 145: 284-299
53. Zhang Q, Fan JS, Zhang M (2001) Interdomain chaperoning between PSD-95, Dlg, and Zo-1 (PDZ) domains of glutamate receptor-interacting proteins. J Biol Chem 276: 43216-43220
54. Ziff EB (2007) TARPs and the AMPA receptor trafficking paradox. Neuron 53: 627-633 (Pubitemid 46283374)