The ARMS/Kidins220 Scaffold Protein Modulates Synaptic Transmission

Overview

Journal Mol Cell Neurosci

Specialties Cell Biology
Molecular Biology
Neurology

Date 2010 Jun 16

PMID 20547223

Citations 22

Authors

Juan Carlos Arevalo

Synphen H Wu

Takuya Takahashi

Hong Zhang

Tao Yu

Hiroko Yano

Teresa A Milner

Lino Tessarollo

Ipe Ninan

Ottavio Arancio

Moses V Chao

Affiliations

Soon will be listed here.

Abstract

Activity-dependent changes of synaptic connections are facilitated by a variety of scaffold proteins, including PSD-95, Shank, SAP97 and GRIP, which serve to organize ion channels, receptors and enzymatic activities and to coordinate the actin cytoskeleton. The abundance of these scaffold proteins raises questions about the functional specificity of action of each protein. Here we report that basal synaptic transmission is regulated in an unexpected manner by the ankyrin repeat-rich membrane-spanning (ARMS/Kidins220) scaffold protein. In particular, decreases in the levels of ARMS/Kidins220 in vivo led to an increase in basal synaptic transmission in the hippocampus, without affecting paired pulse facilitation. One explanation to account for the effects of ARMS/Kidins220 is an interaction with the AMPA receptor subunit, GluA1, which could be observed after immunoprecipitation. Importantly, shRNA and cell surface biotinylation experiments indicate that ARMS/Kidins220 levels have an impact on GluA1 phosphorylation and localization. Moreover, ARMS/Kidins220 is a negative regulator of AMPAR function, which was confirmed by inward rectification assays. These results provide evidence that modulation of ARMS/Kidins220 levels can regulate basal synaptic strength in a specific manner in hippocampal neurons.

Citing Articles

Morphogenetic theory of mental and cognitive disorders: the role of neurotrophic and guidance molecules.

Primak A, Bozov K, Rubina K, Dzhauari S, Neyfeld E, Illarionova M Front Mol Neurosci. 2024; 17:1361764.

PMID: 38646100 PMC: 11027769. DOI: 10.3389/fnmol.2024.1361764.

Kidins220 and Aiolos promote thymic iNKT cell development by reducing TCR signals.

Herr L, Fiala G, Sagar , Schaffer A, Hummel J, Zintchenko M Sci Adv. 2024; 10(11):eadj2802.

PMID: 38489359 PMC: 10942104. DOI: 10.1126/sciadv.adj2802.

Mechanisms Controlling the Expression and Secretion of BDNF.

Arevalo J, Deogracias R Biomolecules. 2023; 13(5).

PMID: 37238659 PMC: 10216319. DOI: 10.3390/biom13050789.

ARMS-NF-κB signaling regulates intracellular ROS to induce autophagy-associated cell death upon oxidative stress.

Liao Y, Wu J, Hsieh I, Lee H, Huang P iScience. 2023; 26(2):106005.

PMID: 36798436 PMC: 9926119. DOI: 10.1016/j.isci.2023.106005.

Transient Receptor Potential Vanilloid 1 Signaling Is Independent on Protein Kinase A Phosphorylation of Ankyrin-Rich Membrane Spanning Protein.

Pellegrino A, Mukusch S, Seitz V, Stein C, Herberg F, Seitz H Med Sci (Basel). 2022; 10(4).

PMID: 36412904 PMC: 9680306. DOI: 10.3390/medsci10040063.

References

Hayashi Y, Shi S, Esteban J, Piccini A, Poncer J, Malinow R . Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science. 2000; 287(5461):2262-7. DOI: 10.1126/science.287.5461.2262. View

Arevalo J, Yano H, Teng K, Chao M . A unique pathway for sustained neurotrophin signaling through an ankyrin-rich membrane-spanning protein. EMBO J. 2004; 23(12):2358-68. PMC: 423292. DOI: 10.1038/sj.emboj.7600253. View

Kamboj S, Swanson G, Cull-Candy S . Intracellular spermine confers rectification on rat calcium-permeable AMPA and kainate receptors. J Physiol. 1995; 486 ( Pt 2):297-303. PMC: 1156521. DOI: 10.1113/jphysiol.1995.sp020812. View

Tomita S, Stein V, Stocker T, Nicoll R, Bredt D . Bidirectional synaptic plasticity regulated by phosphorylation of stargazin-like TARPs. Neuron. 2005; 45(2):269-77. DOI: 10.1016/j.neuron.2005.01.009. View

Wu S, Arevalo J, Sarti F, Tessarollo L, Gan W, Chao M . Ankyrin Repeat-rich Membrane Spanning/Kidins220 protein regulates dendritic branching and spine stability in vivo. Dev Neurobiol. 2009; 69(9):547-57. PMC: 4098644. DOI: 10.1002/dneu.20723. View

Derkach V, Barria A, Soderling T . Ca2+/calmodulin-kinase II enhances channel conductance of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate type glutamate receptors. Proc Natl Acad Sci U S A. 1999; 96(6):3269-74. PMC: 15931. DOI: 10.1073/pnas.96.6.3269. View

Tomita S, Adesnik H, Sekiguchi M, Zhang W, Wada K, Howe J . Stargazin modulates AMPA receptor gating and trafficking by distinct domains. Nature. 2005; 435(7045):1052-8. DOI: 10.1038/nature03624. View

Bracale A, Cesca F, Neubrand V, Newsome T, Way M, Schiavo G . Kidins220/ARMS is transported by a kinesin-1-based mechanism likely to be involved in neuronal differentiation. Mol Biol Cell. 2006; 18(1):142-52. PMC: 1751333. DOI: 10.1091/mbc.e06-05-0453. View

Man H, Sekine-Aizawa Y, Huganir R . Regulation of {alpha}-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. 2007; 104(9):3579-84. PMC: 1805611. DOI: 10.1073/pnas.0611698104. View

10.

Tada T, Sheng M . Molecular mechanisms of dendritic spine morphogenesis. Curr Opin Neurobiol. 2005; 16(1):95-101. DOI: 10.1016/j.conb.2005.12.001. View

11.

Chen L, Chetkovich D, Petralia R, Sweeney N, Kawasaki Y, Wenthold R . Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature. 2001; 408(6815):936-43. DOI: 10.1038/35050030. View

12.

Milner T, Ayoola K, Drake C, Herrick S, Tabori N, McEwen B . Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation. J Comp Neurol. 2005; 491(2):81-95. DOI: 10.1002/cne.20724. View

13.

Beique J, Lin D, Kang M, Aizawa H, Takamiya K, Huganir R . Synapse-specific regulation of AMPA receptor function by PSD-95. Proc Natl Acad Sci U S A. 2006; 103(51):19535-40. PMC: 1748260. DOI: 10.1073/pnas.0608492103. View

14.

Esteban J, Shi S, Wilson C, Nuriya M, Huganir R, Malinow R . PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci. 2003; 6(2):136-43. DOI: 10.1038/nn997. View

15.

Plant K, Pelkey K, Bortolotto Z, Morita D, Terashima A, McBain C . Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nat Neurosci. 2006; 9(5):602-4. DOI: 10.1038/nn1678. View

16.

Kuratomi G, Komuro A, Goto K, Shinozaki M, Miyazawa K, Miyazono K . NEDD4-2 (neural precursor cell expressed, developmentally down-regulated 4-2) negatively regulates TGF-beta (transforming growth factor-beta) signalling by inducing ubiquitin-mediated degradation of Smad2 and TGF-beta type I receptor. Biochem J. 2004; 386(Pt 3):461-70. PMC: 1134864. DOI: 10.1042/BJ20040738. View

17.

Bowie D, Mayer M . Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block. Neuron. 1995; 15(2):453-62. DOI: 10.1016/0896-6273(95)90049-7. View

18.

Shen L, Liang F, Walensky L, Huganir R . Regulation of AMPA receptor GluR1 subunit surface expression by a 4. 1N-linked actin cytoskeletal association. J Neurosci. 2000; 20(21):7932-40. PMC: 6772741. View

19.

Koh D, Burnashev N, Jonas P . Block of native Ca(2+)-permeable AMPA receptors in rat brain by intracellular polyamines generates double rectification. J Physiol. 1995; 486 ( Pt 2):305-12. PMC: 1156522. DOI: 10.1113/jphysiol.1995.sp020813. View

20.

Bolton M, Blanpied T, Ehlers M . Localization and stabilization of ionotropic glutamate receptors at synapses. Cell Mol Life Sci. 2000; 57(11):1517-25. PMC: 11147101. DOI: 10.1007/pl00000636. View