Structural Basis of Arc Binding to Synaptic Proteins: Implications for Cognitive Disease

Zhang, Wenchi; Wu, Jing; Ward, Matthew D.; Yang, Sunggu; Chuang, Yang-An; Xiao, Meifang; Li, Ruojing; Leahy, Daniel J.; Worley, Paul F.

doi:10.1016/j.neuron.2015.03.030

Title: Structural Basis of Arc Binding to Synaptic Proteins: Implications for Cognitive Disease

Journal Article · Thu Apr 09 00:00:00 EDT 2015 · Neuron

DOI: https://doi.org/10.1016/j.neuron.2015.03.030 · OSTI ID:1213728

Zhang, Wenchi ^[1]; Wu, Jing ^[1]; Ward, Matthew D. ^[2]; Yang, Sunggu ^[3]; Chuang, Yang-An ^[1]; Xiao, Meifang ^[1]; Li, Ruojing ^[4]; Leahy, Daniel J. ^[2]; Worley, Paul F. ^[1]

Johns Hopkins Univ., Baltimore, MD (United States). School of Medicine, Solomon H. Snyder Dept. of Neuroscience
Johns Hopkins Univ., Baltimore, MD (United States). School of Medicine, Dept. of Biophysics and Biophysical Chemistry
Incheon National Univ. (Korea). Dept. of Nano-Bioengineering
Johns Hopkins Univ., Baltimore, MD (United States). School of Medicine, Dept. of Pharmacology and Molecular Sciences

Arc is a cellular immediate-early gene (IEG) that functions at excitatory synapses and is required for learning and memory. Here we report crystal structures of Arc subdomains that form a bi-lobar architecture remarkably similar to the capsid domain of human immunodeficiency virus (HIV) gag protein. Analysis indicates Arc originated from the Ty3/Gypsy retrotransposon family and was “domesticated” in higher vertebrates for synaptic functions. The Arc N-terminal lobe evolved a unique hydrophobic pocket that mediates intermolecular binding with synaptic proteins as resolved in complexes with TARPγ2 (Stargazin) and CaMKII peptides and is essential for Arc’s synaptic function. A consensus sequence for Arc binding identifies several additional partners that include genes implicated in schizophrenia. Arc N-lobe binding is inhibited by small chemicals suggesting Arc’s synaptic action may be druggable. Finally, these studies reveal the remarkable evolutionary origin of Arc and provide a structural basis for understanding Arc’s contribution to neural plasticity and disease.

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Research Organization:: Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

OSTI ID:: 1213728

Journal Information:: Neuron, Journal Name: Neuron Journal Issue: 2 Vol. 86; ISSN 0896-6273

Publisher:: Cell Press / ElsevierCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Role of Immediate-Early Genes in Synaptic Plasticity and Neuronal Ensembles Underlying the Memory Trace Minatohara, Keiichiro; Akiyoshi, Mika; Okuno, Hiroyuki Frontiers in Molecular Neuroscience, Vol. 8 https://doi.org/10.3389/fnmol.2015.00078	journal	January 2016
GSK3α and GSK3β Phosphorylate Arc and Regulate its Degradation Gozdz, Agata; Nikolaienko, Oleksii; Urbanska, Malgorzata Frontiers in Molecular Neuroscience, Vol. 10 https://doi.org/10.3389/fnmol.2017.00192	journal	June 2017
Dynamic Arc SUMOylation and Selective Interaction with F-Actin-Binding Protein Drebrin A in LTP Consolidation In Vivo Nair, Rajeevkumar R.; Patil, Sudarshan; Tiron, Adrian Frontiers in Synaptic Neuroscience, Vol. 9 https://doi.org/10.3389/fnsyn.2017.00008	journal	May 2017
Therapeutic Potential of Selectively Targeting the α2C-Adrenoceptor in Cognition, Depression, and Schizophrenia—New Developments and Future Perspective Uys, Madeleine Monique; Shahid, Mohammed; Harvey, Brian Herbert Frontiers in Psychiatry, Vol. 8 https://doi.org/10.3389/fpsyt.2017.00144	journal	August 2017
Chemogenomic analysis reveals key role for lysine acetylation in regulating Arc stability Lalonde, Jasmin; Reis, Surya A.; Sivakumaran, Sudhir Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01750-7	journal	November 2017
Structures of virus-like capsids formed by the Drosophila neuronal Arc proteins Erlendsson, Simon; Morado, Dustin R.; Cullen, Harrison B. Nature Neuroscience, Vol. 23, Issue 2 https://doi.org/10.1038/s41593-019-0569-y	journal	January 2020
Structure of an Arc-ane virus-like capsid Budnik, Vivian; Thomson, Travis Nature Neuroscience, Vol. 23, Issue 2 https://doi.org/10.1038/s41593-019-0580-3	journal	January 2020
Structure of the Ty3/Gypsy retrotransposon capsid and the evolution of retroviruses Dodonova, Svetlana O.; Prinz, Simone; Bilanchone, Virginia Proceedings of the National Academy of Sciences, Vol. 116, Issue 20 https://doi.org/10.1073/pnas.1900931116	journal	April 2019
Structure of monomeric full-length ARC sheds light on molecular flexibility, protein interactions, and functional modalities Hallin, Erik I.; Eriksen, Maria S.; Baryshnikov, Sergei bioRxiv https://doi.org/10.1101/332015	posted_content	May 2018
Molecular determinants of Arc oligomerization and formation of virus-like capsids Eriksen, Maria Steene; Nikolaienko, Oleksii; Hallin, Erik Ingmar https://doi.org/10.1101/667956	preprint	November 2019
Transposon expression in the Drosophila brain is driven by neighboring genes and diversifies the neural transcriptome Treiber, Christoph D.; Waddell, Scott bioRxiv https://doi.org/10.1101/838045	posted_content	November 2019
Transposon expression in the Drosophila brain is driven by neighboring genes and diversifies the neural transcriptome Treiber, Christoph D.; Waddell, Scott Genome Research, Vol. 30, Issue 11 https://doi.org/10.1101/gr.259200.119	journal	September 2020
Structural basis for PDZ domain interactions in the post-synaptic density scaffolding protein Shank3 Ponna, Srinivas Kumar; Ruskamo, Salla; Myllykoski, Matti Journal of Neurochemistry, Vol. 145, Issue 6 https://doi.org/10.1111/jnc.14322	journal	June 2018
Structure of monomeric full-length ARC sheds light on molecular flexibility, protein interactions, and functional modalities Hallin, Erik I.; Eriksen, Maria S.; Baryshnikov, Sergei Journal of Neurochemistry, Vol. 147, Issue 3 https://doi.org/10.1111/jnc.14556	journal	September 2018
Structure of Drosophila melanogaster ARC1 reveals a repurposed molecule with characteristics of retroviral Gag Cottee, Matthew A.; Letham, Suzanne C.; Young, George R. Science Advances, Vol. 6, Issue 1 https://doi.org/10.1126/sciadv.aay6354	journal	January 2020
A comparative analysis of the foamy and ortho virus capsid structures reveals an ancient domain duplication Taylor, William R.; Stoye, Jonathan P.; Taylor, Ian A. BMC Structural Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s12900-017-0073-0	journal	April 2017
Association of SNPs in EGR3 and ARC with Schizophrenia Supports a Biological Pathway for Schizophrenia Risk Huentelman, Matthew J.; Muppana, Leela; Corneveaux, Jason J. PLOS ONE, Vol. 10, Issue 10 https://doi.org/10.1371/journal.pone.0135076	journal	October 2015
Structure of Drosophila melanogaster ARC1 reveals a repurposed molecule with characteristics of retroviral Gag. Cottee, Matthew A.; Letham, Suzanne C.; Young, George R. The Francis Crick Institute https://doi.org/10.25418/crick.11695380	text	January 2020
Human Endogenous Retroviruses Are Ancient Acquired Elements Still Shaping Innate Immune Responses Grandi, Nicole; Tramontano, Enzo Frontiers in Immunology, Vol. 9 https://doi.org/10.3389/fimmu.2018.02039	journal	September 2018
Reward Network Immediate Early Gene Expression in Mood Disorders Manning, Claire E.; Williams, Elizabeth S.; Robison, Alfred J. Frontiers in Behavioral Neuroscience, Vol. 11 https://doi.org/10.3389/fnbeh.2017.00077	journal	April 2017
Role of Immediate-Early Genes in Synaptic Plasticity and Neuronal Ensembles Underlying the Memory Trace Minatohara, Keiichiro; Akiyoshi, Mika; Okuno, Hiroyuki Frontiers in Molecular Neuroscience, Vol. 8 https://doi.org/10.3389/fnmol.2015.00078	journal	January 2016
Therapeutic Potential of Selectively Targeting the α2C-Adrenoceptor in Cognition, Depression, and Schizophrenia—New Developments and Future Perspective Uys, Madeleine Monique; Shahid, Mohammed; Harvey, Brian Herbert Frontiers in Psychiatry, Vol. 8 https://doi.org/10.3389/fpsyt.2017.00144	journal	August 2017

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