Palmitoylation of A-Kinase anchoring protein 79/150 regulates dendritic endosomal targeting and synaptic plasticity mechanisms

Journal of Neuroscience

Volumn 32, Issue 21, 2012, Pages 7119-7136

  Keith, Dove J ^b,c   Sanderson, Jennifer L ^a   Gibson, Emily S ^a   Woolfrey, Kevin M ^a   Robertson, Holly R ^a,d   Olszewski, Kyle ^a   Kang, Rujun ^b   El Husseini, Alaa ^b   Dell'Acqua, Mark L ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c OREGON STATE UNIVERSITY   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; CALCINEURIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN 150; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN 79; EARLY ENDOSOME ANTIGEN 1; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; POSTSYNAPTIC DENSITY PROTEIN 95; RAB11 PROTEIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITIC SPINE; ELECTROPHYSIOLOGY; ENDOSOME; FEMALE; FLUORESCENCE IMAGING; IMMUNOHISTOCHEMISTRY; LIPID RAFT; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NONHUMAN; PALMITOYLATION; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SEIZURE; STIMULATION;

A KINASE ANCHOR PROTEINS; ANIMALS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; DENDRITES; DENDRITIC SPINES; ENDOSOMES; FEMALE; GENE KNOCKDOWN TECHNIQUES; HIPPOCAMPUS; KAINIC ACID; LIPOYLATION; LONG-TERM POTENTIATION; LONG-TERM SYNAPTIC DEPRESSION; MALE; NEURONAL PLASTICITY; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR; RECEPTORS, AMPA; SEIZURES;

EID: 84861322293     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0784-12.2012     Document Type: Article

References (64)

1. Beattie EC, Carroll RC, Yu X, Morishita W, Yasuda H, von Zastrow M, Malenka RC (2000) Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nat Neurosci 3:1291-1300.
2. Bhattacharyya S, Biou V, Xu W, Schlüter O, Malenka RC (2009) A critical role for PSD-95/AKAP interactions in endocytosis of synaptic AMPA receptors. Nat Neurosci 12:172-181.
3. Boehm J, Kang MG, Johnson RC, Esteban J, Huganir RL, Malinow R (2006) Synaptic incorporation of AMPA receptors during LTP is controlled by a PKC phosphorylation site on GluR1. Neuron 51:213-225.
4. Brandao KE, Dell'Acqua ML, Levinson SR (2012) A-kinase anchoring protein 150 expression in a specific subset of TRPV1- and CaV 1.2-positive nociceptive rat dorsal root ganglion neurons. J Comp Neurol 520:81-99.
5. Colledge M, Dean RA, Scott GK, Langeberg LK, Huganir RL, Scott JD (2000) Targeting of PKA to glutamate receptors through a MAGUK-AKAP complex. Neuron 27:107-119.
6. Delint-Ramirez I, Willoughby D, Hammond GV, Ayling LJ, Cooper DM (2011) Palmitoylation targets AKAP79 to lipid rafts and promotes its regulation of the calcium sensitive adenylyl cyclase type 8. J Biol Chem 286:32962-32975.
7. Dell'Acqua ML, Faux MC, Thorburn J, Thorburn A, Scott JD (1998) Membrane-targeting sequences on AKAP79 bind phosphatidylinositol-4,5-bisphosphate. EMBO J 17:2246-2260.
8. Derkach VA, Oh MC, Guire ES, Soderling TR (2007) Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat Rev Neurosci 8:101-113.
9. Ehlers MD (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28:511-525.
10. El-Husseini Ael-D, Schnell E, Dakoji S, Sweeney N, Zhou Q, Prange O, Gauthier-Campbell C, Aguilera-Moreno A, Nicoll RA, Bredt DS (2002) Synaptic strength regulated by palmitate cycling on PSD-95. Cell 108:849-863.
11. Esteban JA, Shi SH, Wilson C, Nuriya M, Huganir RL, Malinow R (2003) PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 6:136-143.
12. Faux MC, Rollins EN, Edwards AS, Langeberg LK, Newton AC, Scott JD (1999) Mechanism of A-kinase-anchoring protein 79 (AKAP79) and protein kinase C interaction. Biochem J 343:443-452.
13. 2+-permeable AMPA receptors recruited by CaM-kinase I. J Neurosci 30:11565-11575.
14. Fukata Y, Fukata M (2010) Protein palmitoylation in neuronal development and synaptic plasticity. Nat Rev Neurosci 11:161-175.
15. Gomez LL, Alam S, Smith KE, Horne E, Dell'Acqua ML (2002) Regulation of A-kinase anchoring protein 79/150-cAMP-dependent protein kinase postsynaptic targeting by NMDA receptor activation of calcineurin and remodeling of dendritic actin. J Neurosci 22:7027-7044.
16. Gorski JA, Gomez LL, Scott JD, Dell'Acqua ML (2005) Association of an A-kinase-anchoring protein signaling scaffold with cadherin adhesion molecules in neurons and epithelial cells. Mol Biol Cell 16:3574-3590.
17. Greaves J, Gorleku OA, Salaun C, Chamberlain LH (2010) Palmitoylation of the SNAP25 protein family: specificity and regulation byDHHCpalmitoyl transferases. J Biol Chem 285:24629-24638.
18. Greaves J, Carmichael JA, Chamberlain LH (2011) The palmitoyl transferase DHHC2 targets a dynamic membrane cycling pathway: regulation by a C-terminal domain. Mol Biol Cell 22:1887-1895.
19. 2+-permeable AMPA receptors at perisynaptic sites by GluR1-S845 phosphorylation. Proc Natl Acad Sci U S A 106: 20033-20038.
20. Horne EA, Dell'Acqua ML (2007) Phospholipase C is required for changes in postsynaptic structure and function associated with NMDA receptordependent long-term depression. J Neurosci 27:3523-3534.
21. Hoshi N, Langeberg LK, Scott JD (2005) Distinct enzyme combinations in AKAP signalling complexes permit functional diversity. Nat Cell Biol 7:1066-1073.
22. Jurado S, Biou V, Malenka RC (2010) A calcineurin/AKAP complex is required for NMDA receptor-dependent long-term depression. Nat Neurosci 13:1053-1055.
23. Kang R, Swayze R, Lise MF, Gerrow K, Mullard A, Honer WG, El-Husseini A (2004) Presynaptic trafficking of synaptotagmin I is regulated by protein palmitoylation. J Biol Chem 279:50524-50536.
24. Kang R, Wan J, Arstikaitis P, Takahashi H, Huang K, Bailey AO, Thompson JX, Roth AF, Drisdel RC, Mastro R, Green WN, Yates JR 3rd, Davis NG, El-Husseini A (2008) Neural palmitoyl-proteomics reveals dynamic synaptic palmitoylation. Nature 456:904-909.
25. Kasai H, Fukuda M, Watanabe S, Hayashi-Takagi A, Noguchi J (2010) Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci 33:121-129.
26. Kennedy MJ, Davison IG, Robinson CG, Ehlers MD (2010) Syntaxin-4 defines a domain for activity-dependent exocytosis in dendritic spines. Cell 141:524-535.
27. Lee HK (2006) Synaptic plasticity and phosphorylation. Pharmacol Ther 112:810-832.
28. Lee HK, Takamiya K, He K, Song L, Huganir RL (2010) Specific roles of AMPA receptor subunit GluR1 (GluA1) phosphorylation sites in regulating synaptic plasticity in the CA1 region of hippocampus. J Neurophysiol 103:479-489.
29. Li Y, Hu J, Höfer K, Wong AM, Cooper JD, Birnbaum SG, Hammer RE, Hofmann SL (2010) DHHC5 interacts with PDZ domain 3 of postsynaptic density-95 (PSD-95) protein and plays a role in learning and memory. J Biol Chem 285:13022-13031.
30. 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.
31. + channel trafficking. J Neurosci 31:1323-1332.
32. 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.
33. Lu Y, Allen M, Halt AR, Weisenhaus M, Dallapiazza RF, Hall DD, Usachev YM, McKnight GS, Hell JW (2007) Age-dependent requirement of AKAP150-anchored PKA and GluR2-lacking AMPA receptors in LTP. EMBO J 26:4879-4890.
34. Lu Y, Zhang M, Lim IA, Hall DD, Allen M, Medvedeva Y, McKnight GS, Usachev YM, Hell JW (2008) AKAP150-anchored PKA activity is important for LTD during its induction phase. J Physiol 586:4155-4164.
35. Lu Y, Zha XM, Kim EY, Schachtele S, Dailey ME, Hall DD, Strack S, Green SH, Hoffman DA, Hell JW (2011) A-kinase anchor protein 150 (AKAP150)- associated protein kinase A limits dendritic spine density. J Biol Chem 286:26496-26506.
36. Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44:5-21.
37. Man HY, Sekine-Aizawa Y, Huganir RL (2007) Regulation of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor trafficking through PKA phosphorylation of the Glu receptor 1 subunit. Proc Natl Acad Sci U S A 104:3579-3584.
38. Mukai J, Liu H, Burt RA, Swor DE, Lai WS, Karayiorgou M, Gogos JA (2004) Evidence that the gene encoding ZDHHC8 contributes to the risk of schizophrenia. Nat Genet 36:725-731.
39. Mukai J, Dhilla A, Drew LJ, Stark KL, Cao L, MacDermott AB, Karayiorgou M, Gogos JA (2008) Palmitoylation-dependent neurodevelopmental deficits in a mouse model of 22q11 microdeletion. Nat Neurosci 11:1302-1310.
40. Newpher TM, Ehlers MD (2009) Spine microdomains for postsynaptic signaling and plasticity. Trends Cell Biol 19:218-227.
41. Nicot AS, Laporte J (2008) Endosomal phosphoinositides and human diseases. Traffic 9:1240-1249.
42. Noritake J, Fukata Y, Iwanaga T, Hosomi N, Tsutsumi R, Matsuda N, Tani H, Iwanari H, Mochizuki Y, Kodama T, Matsuura Y, Bredt DS, Hamakubo T, Fukata M (2009) Mobile DHHC palmitoylating enzyme mediates activity-sensitive synaptic targeting of PSD-95. J Cell Biol 186:147-160.
43. Oh MC, Derkach VA, Guire ES, Soderling TR (2006) Extrasynaptic membrane trafficking regulated by GluR1 serine 845 phosphorylation primes AMPA receptors for long-term potentiation. J Biol Chem 281:752-758.
44. Oliveria SF, Gomez LL, Dell'Acqua ML (2003) Imaging kinase-AKAP79- phosphatase scaffold complexes at the plasma membrane in living cells using FRET microscopy. J Cell Biol 160:101-112.
45. 2+ channel activity and nuclear signaling. Neuron 55:261-275.
46. Opazo P, Choquet D (2011) A three-step model for the synaptic recruitment of AMPA receptors. Mol Cell Neurosci 46:1-8.
47. Opazo P, Labrecque S, Tigaret CM, Frouin A, Wiseman PW, De Koninck P, Choquet D (2010) CaMKII triggers the diffusional trapping of surface AMPARs through phosphorylation of Stargazin. Neuron 67:239-252.
48. Park M, Penick EC, Edwards JG, Kauer JA, Ehlers MD (2004) Recycling endosomes supply AMPA receptors for LTP. Science 305:1972-1975.
49. Park M, Salgado JM, Ostroff L, Helton TD, Robinson CG, Harris KM, Ehlers MD (2006) Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes. Neuron 52:817-830.
50. Penzes P, Cahill ME, Jones KA, VanLeeuwen JE, Woolfrey KM (2011) Dendritic spine pathology in neuropsychiatric disorders. Nat Neurosci 14:285-293.
51. Petrini EM, Lu J, Cognet L, Lounis B, Ehlers MD, Choquet D (2009) Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation. Neuron 63:92-105.
52. Racine RJ (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281-294.
53. Robertson HR, Gibson ES, Benke TA, Dell'Acqua ML (2009) Regulation of postsynaptic structure and function by an A-kinase anchoring proteinmembrane-associated guanylate kinase scaffolding complex. J Neurosci 29:7929-7943.
54. Sanderson JL, Dell'Acqua ML (2011) AKAP signaling complexes in regulation of excitatory synaptic plasticity. Neuroscientist 17:321-336.
55. Sheng M, Hoogenraad CC (2007) The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu Rev Biochem 76:823-847.
56. Smith KE, Gibson ES, Dell'Acqua ML (2006) cAMP-dependent protein kinase postsynaptic localization regulated by NMDA receptor activation through translocation of an A-kinase anchoring protein scaffold protein. J Neurosci 26:2391-2402.
57. 2+-calmodulin-dependent protein kinase II/protein kinase C site. J Biol Chem 283:11445-11452.
58. Tavalin SJ, Colledge M, Hell JW, Langeberg LK, Huganir RL, Scott JD (2002) Regulation of GluR1 by the A-kinase anchoring protein 79 (AKAP79) signaling complex shares properties with long-term depression. J Neurosci 22:3044-3051.
59. Thomas GM, Hayashi T, Chiu SL, Chen CM, Huganir RL (2012) Palmitoylation by DHHC5/8 targets GRIP1 to dendritic endosomes to regulate AMPA-R trafficking. Neuron 73:482-496.
60. 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.
61. Tunquist BJ, Hoshi N, Guire ES, Zhang F, Mullendorff K, Langeberg LK, Raber J, Scott JD (2008) Loss of AKAP150 perturbs distinct neuronal processes in mice. Proc Natl Acad Sci U S A 105:12557-12562.
62. Weisenhaus M, Allen ML, Yang L, Lu Y, Nichols CB, Su T, Hell JW, McKnight GS (2010) Mutations in AKAP5 disrupt dendritic signaling complexes and lead to electrophysiological and behavioral phenotypes in mice. PLoS One 5:e10325.
63. Xu W, Schlüter OM, Steiner P, Czervionke BL, Sabatini B, Malenka RC (2008) Molecular dissociation of the role of PSD-95 in regulating synaptic strength and LTD. Neuron 57:248-262.
64. Yudowski GA, Puthenveedu MA, Leonoudakis D, Panicker S, Thorn KS, Beattie EC, von Zastrow M (2007) Real-time imaging of discrete exocytic events mediating surface delivery of AMPA receptors. J Neurosci 27:11112-11121.