Activity-dependent synaptic GRIP1 accumulation drives synaptic scaling up in response to action potential blockade

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 27, 2015, Pages E3590-E3599

  Gainey, Melanie A ^a,b   Tatavarty, Vedakumar ^a   Nahmani, Marc ^a   Lin, Heather ^a   Turrigiano, Gina G ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b University of California Berkeley   (United States)

Author keywords

AMPAR; GluA2; GRIP1; Synaptic plasticity; Synaptic scaling

Indexed keywords

AMPA RECEPTOR; BINDING PROTEIN; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR 2; GLUTAMATE RECEPTOR INTERACTING PROTEIN 1; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; CARRIER PROTEIN; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 2; GRIP1 PROTEIN, RAT; NERVE PROTEIN; PROTEIN BINDING; TETRODOTOXIN;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; GENE OVEREXPRESSION; GENE SILENCING; HIPPOCAMPAL NEURONAL CULTURE; IN VITRO STUDY; INTRACELLULAR MEMBRANE; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PYRAMIDAL NERVE CELL; RAT; SCALE UP; SYNAPTIC MEMBRANE; ANIMAL; CELL CULTURE; CONFOCAL MICROSCOPY; DRUG EFFECTS; GENETICS; IMMUNOELECTRON MICROSCOPY; LONG EVANS RAT; METABOLISM; NERVE CELL; NEWBORN; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; RNA INTERFERENCE; SYNAPSE; ULTRASTRUCTURE;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; CARRIER PROTEINS; CELLS, CULTURED; EXCITATORY POSTSYNAPTIC POTENTIALS; MICROSCOPY, CONFOCAL; MICROSCOPY, IMMUNOELECTRON; NERVE TISSUE PROTEINS; NEURONS; PATCH-CLAMP TECHNIQUES; PROTEIN BINDING; RATS, LONG-EVANS; RECEPTORS, AMPA; RNA INTERFERENCE; SYNAPSES; TETRODOTOXIN;

EID: 84935426296     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1510754112     Document Type: Article

References (51)

1. Abbott LF, Nelson SB (2000) Synaptic plasticity: Taming the beast. Nat Neurosci 3 (Suppl):1178-1183.
2. Pozo K, Goda Y (2010) Unraveling mechanisms of homeostatic synaptic plasticity. Neuron 66(3):337-351.
3. Turrigiano GG, Nelson SB (2004) Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5(2):97-107.
4. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB (1998) Activitydependent scaling of quantal amplitude in neocortical neurons. Nature 391(6670): 892-896.
5. Ibata K, Sun Q, Turrigiano GG (2008) Rapid synaptic scaling induced by changes in postsynaptic firing. Neuron 57(6):819-826.
6. Goold CP, Nicoll RA (2010) Single-cell optogenetic excitation drives homeostatic synaptic depression. Neuron 68(3):512-528.
7. Pratt KG, Zimmerman EC, Cook DG, Sullivan JM (2011) Presenilin 1 regulates homeostatic synaptic scaling through Akt signaling. Nat Neurosci 14(9):1112-1114.
8. Trasande CA, Ramirez JM (2007) Activity deprivation leads to seizures in hippocampal slice cultures: Is epilepsy the consequence of homeostatic plasticity? J Clin Neurophysiol 24(2):154-164.
9. Anggono V, Huganir RL (2012) Regulation of AMPA receptor trafficking and synaptic plasticity. Curr Opin Neurobiol 22(3):461-469.
10. O'Brien RJ, et al. (1998) Activity-dependent modulation of synaptic AMPA receptor accumulation. Neuron 21(5):1067-1078.
11. Wierenga CJ, Ibata K, Turrigiano GG (2005) Postsynaptic expression of homeostatic plasticity at neocortical synapses. J Neurosci 25(11):2895-2905.
12. Gainey MA, Hurvitz-Wolff JR, Lambo ME, Turrigiano GG (2009) Synaptic scaling requires the GluR2 subunit of the AMPA receptor. J Neurosci 29(20):6479-6489.
13. Diering GH, Gustina AS, Huganir RL (2014) PKA-GluA1 coupling via AKAP5 controls AMPA receptor phosphorylation and cell-surface targeting during bidirectional homeostatic plasticity. Neuron 84(4):790-805.
14. Altimimi HF, Stellwagen D (2013) Persistent synaptic scaling independent of AMPA receptor subunit composition. J Neurosci 33(29):11763-11767.
15. Dong H, et al. (1997) GRIP: A synaptic PDZ domain-containing protein that interacts with AMPA receptors. Nature 386(6622):279-284.
16. Dev KK, Nishimune A, Henley JM, Nakanishi S (1999) The protein kinase C alpha binding protein PICK1 interacts with short but not long form alternative splice variants of AMPA receptor subunits. Neuropharmacology 38(5):635-644.
17. Osten P, et al. (2000) Mutagenesis reveals a role for ABP/GRIP binding to GluR2 in synaptic surface accumulation of the AMPA receptor. Neuron 27(2):313-325.
18. Daw MI, et al. (2000) PDZ proteins interacting with C-terminal GluR2/3 are involved in a PKC-dependent regulation of AMPA receptors at hippocampal synapses. Neuron 28(3):873-886.
19. Braithwaite SP, Xia H, Malenka RC (2002) Differential roles for NSF and GRIP/ABP in AMPA receptor cycling. Proc Natl Acad Sci USA 99(10):7096-7101.
20. Lin DT, Huganir RL (2007) PICK1 and phosphorylation of the glutamate receptor 2 (GluR2) AMPA receptor subunit regulates GluR2 recycling after NMDA receptorinduced internalization. J Neurosci 27(50):13903-13908.
21. Mejias R, et al. (2011) Gain-of-function glutamate receptor interacting protein 1 variants alter GluA2 recycling and surface distribution in patients with autism. Proc Natl Acad Sci USA 108(12):4920-4925.
22. Mao L, Takamiya K, Thomas G, Lin DT, Huganir RL (2010) GRIP1 and 2 regulate activity-dependent AMPA receptor recycling via exocyst complex interactions. Proc Natl Acad Sci USA 107(44):19038-19043.
23. Anggono V, Clem RL, Huganir RL (2011) PICK1 loss of function occludes homeostatic synaptic scaling. J Neurosci 31(6):2188-2196.
24. Dong H, et al. (1999) Characterization of the glutamate receptor-interacting proteins GRIP1 and GRIP2. J Neurosci 19(16):6930-6941.
25. Srivastava S, Ziff EB (1999) ABP: A novel AMPA receptor binding protein. Ann N Y Acad Sci 868:561-564.
26. Torres R, et al. (1998) PDZ proteins bind, cluster, and synaptically colocalize with Eph receptors and their ephrin ligands. Neuron 21(6):1453-1463.
27. Ye B, et al. (2000) GRASP-1: A neuronal RasGEF associated with the AMPA receptor/ GRIP complex. Neuron 26(3):603-617.
28. Wyszynski M, et al. (2002) Interaction between GRIP and liprin-alpha/SYD2 is required for AMPA receptor targeting. Neuron 34(1):39-52.
29. Setou M, et al. (2002) Glutamate-receptor-interacting protein GRIP1 directly steers kinesin to dendrites. Nature 417(6884):83-87.
30. Steiner P, et al. (2005) Interactions between NEEP21, GRIP1 and GluR2 regulate sorting and recycling of the glutamate receptor subunit GluR2. EMBO J 24(16): 2873-2884.
31. Kulangara K, et al. (2007) Phosphorylation of glutamate receptor interacting protein1 regulates surface expression of glutamate receptors. J Biol Chem 282(4):2395-2404.
32. Chung HJ, Xia J, Scannevin RH, Zhang X, Huganir RL (2000) Phosphorylation of the AMPA receptor subunit GluR2 differentially regulates its interaction with PDZ domain-containing proteins. J Neurosci 20(19):7258-7267.
33. Xia J, Chung HJ, Wihler C, Huganir RL, Linden DJ (2000) Cerebellar long-term depression requires PKC-regulated interactions between GluR2/3 and PDZ domaincontaining proteins. Neuron 28(2):499-510.
34. Takamiya K, Mao L, Huganir RL, Linden DJ (2008) The glutamate receptor-interacting protein family of GluR2-binding proteins is required for long-term synaptic depression expression in cerebellar Purkinje cells. J Neurosci 28(22):5752-5755.
35. Steinmetz CC, Turrigiano GG (2010) Tumor necrosis factor-α signaling maintains the ability of cortical synapses to express synaptic scaling. J Neurosci 30(44):14685-14690.
36. Watt AJ, van Rossum MC, MacLeod KM, Nelson SB, Turrigiano GG (2000) Activity coregulates quantal AMPA and NMDA currents at neocortical synapses. Neuron 26(3): 659-670.
37. Wyszynski M, et al. (1999) Association of AMPA receptors with a subset of glutamate receptor-interacting protein in vivo. J Neurosci 19(15):6528-6537.
38. Bladt F, Tafuri A, Gelkop S, Langille L, Pawson T (2002) Epidermolysis bullosa and embryonic lethality in mice lacking the multi-PDZ domain protein GRIP1. Proc Natl Acad Sci USA 99(10):6816-6821.
39. Takamiya K, et al. (2004) A direct functional link between the multi-PDZ domain protein GRIP1 and the Fraser syndrome protein Fras1. Nat Genet 36(2):172-177.
40. Hoogenraad CC, Milstein AD, Ethell IM, Henkemeyer M, Sheng M (2005) GRIP1 controls dendrite morphogenesis by regulating EphB receptor trafficking. Nat Neurosci 8(7):906-915.
41. Chung HJ, Steinberg JP, Huganir RL, Linden DJ (2003) Requirement of AMPA receptor GluR2 phosphorylation for cerebellar long-term depression. Science 300(5626): 1751-1755.
42. 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 receptorinteracting protein. J Neurochem 73(4):1765-1768.
43. Hayashi T, Huganir RL (2004) Tyrosine phosphorylation and regulation of the AMPA receptor by SRC family tyrosine kinases. J Neurosci 24(27):6152-6160.
44. Seidenman KJ, Steinberg JP, Huganir R, Malinow R (2003) Glutamate receptor subunit 2 Serine 880 phosphorylation modulates synaptic transmission and mediates plasticity in CA1 pyramidal cells. J Neurosci 23(27):9220-9228.
45. Perez JL, et al. (2001) PICK1 targets activated protein kinase Calpha to AMPA receptor clusters in spines of hippocampal neurons and reduces surface levels of the AMPAtype glutamate receptor subunit 2. J Neurosci 21(15):5417-5428.
46. Hsu SC, TerBush D, Abraham M, Guo W (2004) The exocyst complex in polarized exocytosis. Int Rev Cytol 233:243-265.
47. Bakshi K, et al. (2009) Prenatal cocaine reduces AMPA receptor synaptic expression through hyperphosphorylation of the synaptic anchoring protein GRIP. J Neurosci 29(19):6308-6319.
48. Steinberg JP, et al. (2006) Targeted in vivo mutations of the AMPA receptor subunit GluR2 and its interacting protein PICK1 eliminate cerebellar long-term depression. Neuron 49(6):845-860.
49. Turrigiano GG (2008) The self-tuning neuron: Synaptic scaling of excitatory synapses. Cell 135(3):422-435.
50. Pratt KG, Watt AJ, Griffith LC, Nelson SB, Turrigiano GG (2003) Activity-dependent remodeling of presynaptic inputs by postsynaptic expression of activated CaMKII. Neuron 39(2):269-281.
51. Rutherford LC, DeWan A, Lauer HM, Turrigiano GG (1997) Brain-derived neurotrophic factor mediates the activity-dependent regulation of inhibition in neocortical cultures. JNeurosci17(12):4527-4535.