Regulation of Synaptic Structure and Function by Palmitoylated AMPA Receptor Binding Protein

Overview

Journal Mol Cell Neurosci

Specialties Cell Biology
Molecular Biology
Neurology

Date 2010 Jan 20

PMID 20083202

Citations 17

Authors

Charu Misra

Sophie Restituito

Jainne Ferreira

Gerald A Rameau

Jie Fu

Edward B Ziff

Affiliations

Soon will be listed here.

Abstract

AMPA receptor binding protein (ABP) is a multi-PDZ domain scaffold that binds and stabilizes AMPA receptor (AMPAR) GluR2/3 subunits at synapses. A palmitoylated N-terminal splice variant (pABP-L) concentrates in spine heads, whereas a non-palmitoylated form (ABP-L) is intracellular. We show that postsynaptic Sindbis viral expression of pABP-L increased AMPAR mediated mEPSC amplitude and frequency and elevated surface levels of GluR1 and GluR2, suggesting an increase in AMPA receptors at individual synapses. Spines were enlarged and more numerous and nerve terminals contacting these cells displayed enlarged synaptophysin puncta. A non-palmitoylated pABP-L mutant (C11A) did not change spine density or size. Exogenous pABP-L and endogenous GRIP, a related scaffold, colocalized with NPRAP (delta-catenin), to which ABP and GRIP bind, and with cadherins, which bind NPRAP. Thus postsynaptic pABP-L induces pre and postsynaptic changes that are dependent on palmitoylation and likely achieved through ABP association with a multi-molecular cell surface signaling complex.

Citing Articles

S-Palmitoylation of Synaptic Proteins in Neuronal Plasticity in Normal and Pathological Brains.

Buszka A, Pytys A, Colvin D, Wlodarczyk J, Wojtowicz T Cells. 2023; 12(3).

PMID: 36766729 PMC: 9913408. DOI: 10.3390/cells12030387.

Discovery of new therapeutic targets in ovarian cancer through identifying significantly non-mutated genes.

Al-Farsi H, Al-Azwani I, Malek J, Chouchane L, Rafii A, Halabi N J Transl Med. 2022; 20(1):244.

PMID: 35619151 PMC: 9134657. DOI: 10.1186/s12967-022-03440-5.

Roles of palmitoylation in structural long-term synaptic plasticity.

Ji B, Skup M Mol Brain. 2021; 14(1):8.

PMID: 33430908 PMC: 7802216. DOI: 10.1186/s13041-020-00717-y.

Acute Regulation of Habituation Learning via Posttranslational Palmitoylation.

Nelson J, Witze E, Ma Z, Ciocco F, Frerotte A, Randlett O Curr Biol. 2020; 30(14):2729-2738.e4.

PMID: 32502414 PMC: 8446937. DOI: 10.1016/j.cub.2020.05.016.

Post-translational protein modifications in schizophrenia.

Mueller T, Meador-Woodruff J NPJ Schizophr. 2020; 6(1):5.

PMID: 32123175 PMC: 7051976. DOI: 10.1038/s41537-020-0093-9.

References

Yamazaki M, Fukaya M, Abe M, Ikeno K, Kakizaki T, Watanabe M . Differential palmitoylation of two mouse glutamate receptor interacting protein 1 forms with different N-terminal sequences. Neurosci Lett. 2001; 304(1-2):81-4. DOI: 10.1016/s0304-3940(01)01766-9. View

Shi S, Hayashi Y, Esteban J, Malinow R . Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell. 2001; 105(3):331-43. DOI: 10.1016/s0092-8674(01)00321-x. View

Penzes P, Johnson R, Sattler R, Zhang X, Huganir R, Kambampati V . The neuronal Rho-GEF Kalirin-7 interacts with PDZ domain-containing proteins and regulates dendritic morphogenesis. Neuron. 2001; 29(1):229-42. DOI: 10.1016/s0896-6273(01)00193-3. View

Chetkovich D, Chen L, Stocker T, Nicoll R, Bredt D . Phosphorylation of the postsynaptic density-95 (PSD-95)/discs large/zona occludens-1 binding site of stargazin regulates binding to PSD-95 and synaptic targeting of AMPA receptors. J Neurosci. 2002; 22(14):5791-6. PMC: 6757934. DOI: 20026591. View

Chung H, Xia J, Scannevin R, Zhang X, Huganir R . Phosphorylation of the AMPA receptor subunit GluR2 differentially regulates its interaction with PDZ domain-containing proteins. J Neurosci. 2000; 20(19):7258-67. PMC: 6772789. View

Ochiishi T, Futai K, Okamoto K, Kameyama K, Kosik K . Regulation of AMPA receptor trafficking by delta-catenin. Mol Cell Neurosci. 2008; 39(4):499-507. DOI: 10.1016/j.mcn.2008.06.002. View

Wyszynski M, Kim E, Dunah A, Passafaro M, Valtschanoff J, Serra-Pages C . Interaction between GRIP and liprin-alpha/SYD2 is required for AMPA receptor targeting. Neuron. 2002; 34(1):39-52. DOI: 10.1016/s0896-6273(02)00640-2. View

Wyszynski M, Valtschanoff J, Naisbitt S, Dunah A, Kim E, Standaert D . Association of AMPA receptors with a subset of glutamate receptor-interacting protein in vivo. J Neurosci. 1999; 19(15):6528-37. PMC: 6782830. View

Dev K, Nishimune A, Henley J, Nakanishi S . The protein kinase C alpha binding protein PICK1 interacts with short but not long form alternative splice variants of AMPA receptor subunits. Neuropharmacology. 1999; 38(5):635-44. DOI: 10.1016/s0028-3908(98)00230-5. View

10.

Braithwaite S, Xia H, Malenka R . Differential roles for NSF and GRIP/ABP in AMPA receptor cycling. Proc Natl Acad Sci U S A. 2002; 99(10):7096-101. PMC: 124534. DOI: 10.1073/pnas.102156099. View

11.

Daw M, Chittajallu R, Bortolotto Z, Dev K, Duprat F, Henley J . PDZ proteins interacting with C-terminal GluR2/3 are involved in a PKC-dependent regulation of AMPA receptors at hippocampal synapses. Neuron. 2001; 28(3):873-86. DOI: 10.1016/s0896-6273(00)00160-4. View

12.

Xu W, Schluter O, Steiner P, Czervionke B, Sabatini B, Malenka R . Molecular dissociation of the role of PSD-95 in regulating synaptic strength and LTD. Neuron. 2008; 57(2):248-62. PMC: 3147180. DOI: 10.1016/j.neuron.2007.11.027. View

13.

Silverman J, Restituito S, Lu W, Lee-Edwards L, Khatri L, Ziff E . Synaptic anchorage of AMPA receptors by cadherins through neural plakophilin-related arm protein AMPA receptor-binding protein complexes. J Neurosci. 2007; 27(32):8505-16. PMC: 6672939. DOI: 10.1523/JNEUROSCI.1395-07.2007. View

14.

Penzes P, Beeser A, Chernoff J, Schiller M, Eipper B, Mains R . Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin. Neuron. 2003; 37(2):263-74. DOI: 10.1016/s0896-6273(02)01168-6. View

15.

Henkemeyer M, Itkis O, Ngo M, Hickmott P, Ethell I . Multiple EphB receptor tyrosine kinases shape dendritic spines in the hippocampus. J Cell Biol. 2003; 163(6):1313-26. PMC: 1435730. DOI: 10.1083/jcb.200306033. View

16.

El-Husseini A, Schnell E, Chetkovich D, Nicoll R, Bredt D . PSD-95 involvement in maturation of excitatory synapses. Science. 2000; 290(5495):1364-8. View

17.

Saglietti L, Dequidt C, Kamieniarz K, Rousset M, Valnegri P, Thoumine O . Extracellular interactions between GluR2 and N-cadherin in spine regulation. Neuron. 2007; 54(3):461-77. DOI: 10.1016/j.neuron.2007.04.012. View

18.

Rumbaugh G, Sia G, Garner C, Huganir R . Synapse-associated protein-97 isoform-specific regulation of surface AMPA receptors and synaptic function in cultured neurons. J Neurosci. 2003; 23(11):4567-76. PMC: 6740810. View

19.

Bredt D, Nicoll R . AMPA receptor trafficking at excitatory synapses. Neuron. 2003; 40(2):361-79. DOI: 10.1016/s0896-6273(03)00640-8. View

20.

Osten P, Khatri L, Perez J, Kohr G, Giese G, Daly C . Mutagenesis reveals a role for ABP/GRIP binding to GluR2 in synaptic surface accumulation of the AMPA receptor. Neuron. 2000; 27(2):313-25. DOI: 10.1016/s0896-6273(00)00039-8. View