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Structural basis of arc binding to synaptic proteins: implications for cognitive disease.

Zhang W, Wu J, Ward MD, Yang S, Chuang YA, Xiao M, Li R, Leahy DJ, Worley PF
Neuron 86 490-500 (2015)
Related entries: 4x3i, 4x3x

Cited: 94 times
EuropePMC logo PMID: 25864631

Abstract

Arc is a cellular immediate-early gene (IEG) that functions at excitatory synapses and is required for learning and memory. 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. These studies reveal the remarkable evolutionary origin of Arc and provide a structural basis for understanding Arc's contribution to neural plasticity and disease.

Articles - 4x3h mentioned but not cited (6)

  1. Structural basis of arc binding to synaptic proteins: implications for cognitive disease. Zhang W, Wu J, Ward MD, Yang S, Chuang YA, Xiao M, Li R, Leahy DJ, Worley PF. Neuron 86 490-500 (2015)
  2. Structures of virus-like capsids formed by the Drosophila neuronal Arc proteins. Erlendsson S, Morado DR, Cullen HB, Feschotte C, Shepherd JD, Briggs JAG. Nat Neurosci 23 172-175 (2020)
  3. Arc Oligomerization Is Regulated by CaMKII Phosphorylation of the GAG Domain: An Essential Mechanism for Plasticity and Memory Formation. Zhang W, Chuang YA, Na Y, Ye Z, Yang L, Lin R, Zhou J, Wu J, Qiu J, Savonenko A, Leahy DJ, Huganir R, Linden DJ, Worley PF. Mol Cell 75 13-25.e5 (2019)
  4. Structure of Drosophila melanogaster ARC1 reveals a repurposed molecule with characteristics of retroviral Gag. Cottee MA, Letham SC, Young GR, Stoye JP, Taylor IA. Sci Adv 6 eaay6354 (2020)
  5. Structural properties and peptide ligand binding of the capsid homology domains of human Arc. Hallin EI, Bramham CR, Kursula P. Biochem Biophys Rep 26 100975 (2021)
  6. PepPro: A Nonredundant Structure Data Set for Benchmarking Peptide-Protein Computational Docking. Xu X, Zou X. J Comput Chem 41 362-369 (2020)


Reviews citing this publication (27)

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  2. Human Endogenous Retroviruses Are Ancient Acquired Elements Still Shaping Innate Immune Responses. Grandi N, Tramontano E. Front Immunol 9 2039 (2018)
  3. Structure, Function, and Pharmacology of Glutamate Receptor Ion Channels. Hansen KB, Wollmuth LP, Bowie D, Furukawa H, Menniti FS, Sobolevsky AI, Swanson GT, Swanger SA, Greger IH, Nakagawa T, McBain CJ, Jayaraman V, Low CM, Dell'Acqua ML, Diamond JS, Camp CR, Perszyk RE, Yuan H, Traynelis SF. Pharmacol Rev 73 298-487 (2021)
  4. Plasticity of Spine Structure: Local Signaling, Translation and Cytoskeletal Reorganization. Nakahata Y, Yasuda R. Front Synaptic Neurosci 10 29 (2018)
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  7. Molecular Architecture of the Retroviral Capsid. Perilla JR, Gronenborn AM. Trends Biochem Sci 41 410-420 (2016)
  8. Roles for Arc in metabotropic glutamate receptor-dependent LTD and synapse elimination: Implications in health and disease. Wilkerson JR, Albanesi JP, Huber KM. Semin Cell Dev Biol 77 51-62 (2018)
  9. Therapeutic Potential of Selectively Targeting the α2C-Adrenoceptor in Cognition, Depression, and Schizophrenia-New Developments and Future Perspective. Uys MM, Shahid M, Harvey BH. Front Psychiatry 8 144 (2017)
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  18. Schizophrenia: What's Arc Got to Do with It? Managò F, Papaleo F. Front Behav Neurosci 11 181 (2017)
  19. Molecular physiology of Arc/Arg3.1: The oligomeric state hypothesis of synaptic plasticity. Eriksen MS, Bramham CR. Acta Physiol (Oxf) 236 e13886 (2022)
  20. mRNA Trafficking in the Nervous System: A Key Mechanism of the Involvement of Activity-Regulated Cytoskeleton-Associated Protein (Arc) in Synaptic Plasticity. Fila M, Diaz L, Szczepanska J, Pawlowska E, Blasiak J. Neural Plast 2021 3468795 (2021)
  21. Molecular Mechanisms of Memory Consolidation That Operate During Sleep. Reyes-Resina I, Samer S, Kreutz MR, Oelschlegel AM. Front Mol Neurosci 14 767384 (2021)
  22. Physiological Roles of Metallothioneins in Central Nervous System Diseases. Nakamura S, Shimazawa M, Hara H. Biol Pharm Bull 41 1006-1013 (2018)
  23. Dysregulated Signaling at Postsynaptic Density: A Systematic Review and Translational Appraisal for the Pathophysiology, Clinics, and Antipsychotics' Treatment of Schizophrenia. de Bartolomeis A, Vellucci L, De Simone G, Mazza B, Barone A, Ciccarelli M. Cells 12 574 (2023)
  24. Arc protein, a remnant of ancient retrovirus, forms virus-like particles, which are abundantly generated by neurons during epileptic seizures, and affects epileptic susceptibility in rodent models. Sibarov DA, Tsytsarev V, Volnova A, Vaganova AN, Alves J, Rojas L, Sanabria P, Ignashchenkova A, Savage ED, Inyushin M. Front Neurol 14 1201104 (2023)
  25. Effect of pharmacological manipulations on Arc function. Yakout DW, Shree N, Mabb AM. Curr Res Pharmacol Drug Discov 2 100013 (2021)
  26. 'Arc'-hitecture of normal cognitive aging. Myrum C, Moreno-Castilla P, Rapp PR. Ageing Res Rev 80 101678 (2022)
  27. Mechanisms and Functions of Activity-Regulated Cytoskeleton-Associated Protein in Synaptic Plasticity. Chen Y, Wang X, Xiao B, Luo Z, Long H. Mol Neurobiol 60 5738-5754 (2023)

Articles citing this publication (61)

  1. Retrovirus-like Gag Protein Arc1 Binds RNA and Traffics across Synaptic Boutons. Ashley J, Cordy B, Lucia D, Fradkin LG, Budnik V, Thomson T. Cell 172 262-274.e11 (2018)
  2. The Neuronal Gene Arc Encodes a Repurposed Retrotransposon Gag Protein that Mediates Intercellular RNA Transfer. Pastuzyn ED, Day CE, Kearns RB, Kyrke-Smith M, Taibi AV, McCormick J, Yoder N, Belnap DM, Erlendsson S, Morado DR, Briggs JAG, Feschotte C, Shepherd JD. Cell 172 275-288.e18 (2018)
  3. Genetic Disruption of Arc/Arg3.1 in Mice Causes Alterations in Dopamine and Neurobehavioral Phenotypes Related to Schizophrenia. Managò F, Mereu M, Mastwal S, Mastrogiacomo R, Scheggia D, Emanuele M, De Luca MA, Weinberger DR, Wang KH, Papaleo F. Cell Rep 16 2116-2128 (2016)
  4. Arc Requires PSD95 for Assembly into Postsynaptic Complexes Involved with Neural Dysfunction and Intelligence. Fernández E, Collins MO, Frank RAW, Zhu F, Kopanitsa MV, Nithianantharajah J, Lemprière SA, Fricker D, Elsegood KA, McLaughlin CL, Croning MDR, Mclean C, Armstrong JD, Hill WD, Deary IJ, Cencelli G, Bagni C, Fromer M, Purcell SM, Pocklington AJ, Choudhary JS, Komiyama NH, Grant SGN. Cell Rep 21 679-691 (2017)
  5. Metabotropic Glutamate Receptors Induce a Form of LTP Controlled by Translation and Arc Signaling in the Hippocampus. Wang H, Ardiles AO, Yang S, Tran T, Posada-Duque R, Valdivia G, Baek M, Chuang YA, Palacios AG, Gallagher M, Worley P, Kirkwood A. J Neurosci 36 1723-1729 (2016)
  6. Activity-Regulated Cytoskeleton-Associated Protein Controls AMPAR Endocytosis through a Direct Interaction with Clathrin-Adaptor Protein 2. DaSilva LL, Wall MJ, P de Almeida L, Wauters SC, Januário YC, Müller J, Corrêa SA. eNeuro 3 ENEURO.0144-15.2016 (2016)
  7. Dynamic Arc SUMOylation and Selective Interaction with F-Actin-Binding Protein Drebrin A in LTP Consolidation In Vivo. Nair RR, Patil S, Tiron A, Kanhema T, Panja D, Schiro L, Parobczak K, Wilczynski G, Bramham CR. Front Synaptic Neurosci 9 8 (2017)
  8. Real-Time Imaging Reveals Properties of Glutamate-Induced Arc/Arg 3.1 Translation in Neuronal Dendrites. Na Y, Park S, Lee C, Kim DK, Park JM, Sockanathan S, Huganir RL, Worley PF. Neuron 91 561-573 (2016)
  9. Association of SNPs in EGR3 and ARC with Schizophrenia Supports a Biological Pathway for Schizophrenia Risk. Huentelman MJ, Muppana L, Corneveaux JJ, Dinu V, Pruzin JJ, Reiman R, Borish CN, De Both M, Ahmed A, Todorov A, Cloninger CR, Zhang R, Ma J, Gallitano AL. PLoS One 10 e0135076 (2015)
  10. Stimulus-evoked ERK-dependent phosphorylation of activity-regulated cytoskeleton-associated protein (Arc) regulates its neuronal subcellular localization. Nikolaienko O, Eriksen MS, Patil S, Bito H, Bramham CR. Neuroscience 360 68-80 (2017)
  11. Structure of the Ty3/Gypsy retrotransposon capsid and the evolution of retroviruses. Dodonova SO, Prinz S, Bilanchone V, Sandmeyer S, Briggs JAG. Proc Natl Acad Sci U S A 116 10048-10057 (2019)
  12. GSK3α and GSK3β Phosphorylate Arc and Regulate its Degradation. Gozdz A, Nikolaienko O, Urbanska M, Cymerman IA, Sitkiewicz E, Blazejczyk M, Dadlez M, Bramham CR, Jaworski J. Front Mol Neurosci 10 192 (2017)
  13. Phylogenetic and Genomic Analyses Resolve the Origin of Important Plant Genes Derived from Transposable Elements. Joly-Lopez Z, Hoen DR, Blanchette M, Bureau TE. Mol Biol Evol 33 1937-1956 (2016)
  14. Structure of monomeric full-length ARC sheds light on molecular flexibility, protein interactions, and functional modalities. Hallin EI, Eriksen MS, Baryshnikov S, Nikolaienko O, Grødem S, Hosokawa T, Hayashi Y, Bramham CR, Kursula P. J Neurochem 147 323-343 (2018)
  15. Structural basis for PDZ domain interactions in the post-synaptic density scaffolding protein Shank3. Ponna SK, Ruskamo S, Myllykoski M, Keller C, Boeckers TM, Kursula P. J Neurochem 145 449-463 (2018)
  16. Transposon expression in the Drosophila brain is driven by neighboring genes and diversifies the neural transcriptome. Treiber CD, Waddell S. Genome Res 30 1559-1569 (2020)
  17. Arc 3' UTR Splicing Leads to Dual and Antagonistic Effects in Fine-Tuning Arc Expression Upon BDNF Signaling. Paolantoni C, Ricciardi S, De Paolis V, Okenwa C, Catalanotto C, Ciotti MT, Cattaneo A, Cogoni C, Giorgi C. Front Mol Neurosci 11 145 (2018)
  18. Arc/Arg3.1 has an activity-regulated interaction with PICK1 that results in altered spatial dynamics. Goo BMSS, Sanstrum BJ, Holden DZY, Yu Y, James NG. Sci Rep 8 14675 (2018)
  19. Carbamoylated erythropoietin induces a neurotrophic gene profile in neuronal cells. Tiwari NK, Sathyanesan M, Schweinle W, Newton SS. Prog Neuropsychopharmacol Biol Psychiatry 88 132-141 (2019)
  20. AMPA receptors control fear extinction through an Arc-dependent mechanism. Trent S, Barnes P, Hall J, Thomas KL. Learn Mem 24 375-380 (2017)
  21. Activity-dependent Signaling and Epigenetic Abnormalities in Mice Exposed to Postnatal Ethanol. Subbanna S, Joshi V, Joshi V, Basavarajappa BS. Neuroscience 392 230-240 (2018)
  22. A comparative analysis of the foamy and ortho virus capsid structures reveals an ancient domain duplication. Taylor WR, Stoye JP, Taylor IA. BMC Struct Biol 17 3 (2017)
  23. Chemogenomic analysis reveals key role for lysine acetylation in regulating Arc stability. Lalonde J, Reis SA, Sivakumaran S, Holland CS, Wesseling H, Sauld JF, Alural B, Zhao WN, Steen JA, Haggarty SJ. Nat Commun 8 1659 (2017)
  24. A biomarker-authenticated model of schizophrenia implicating NPTX2 loss of function. Xiao MF, Roh SE, Zhou J, Chien CC, Lucey BP, Craig MT, Hayes LN, Coughlin JM, Leweke FM, Jia M, Xu D, Zhou W, Conover Talbot C, Arnold DB, Staley M, Jiang C, Reti IM, Sawa A, Pelkey KA, McBain CJ, Savonenko A, Worley PF. Sci Adv 7 eabf6935 (2021)
  25. Arc Interacts with the Integral Endoplasmic Reticulum Protein, Calnexin. Myrum C, Soulé J, Bittins M, Cavagnini K, Goff K, Ziemek SK, Eriksen MS, Patil S, Szum A, Nair RR, Bramham CR. Front Cell Neurosci 11 294 (2017)
  26. Higher Arc Nucleus-to-Cytoplasm Ratio during Sleep in the Superficial Layers of the Mouse Cortex. Honjoh S, de Vivo L, Okuno H, Bito H, Tononi G, Cirelli C. Front Neural Circuits 11 60 (2017)
  27. Membrane Remodeling by Arc/Arg3.1. Hedde PN, Malacrida L, Barylko B, Binns DD, Albanesi JP, Jameson DM. Front Mol Biosci 8 630625 (2021)
  28. Palmitoylated Proteins in Dendritic Spine Remodeling. Albanesi JP, Barylko B, DeMartino GN, Jameson DM. Front Synaptic Neurosci 12 22 (2020)
  29. Phosphorylation-dependent control of Activity-regulated cytoskeleton-associated protein (Arc) protein by TNIK. Walczyk-Mooradally A, Holborn J, Singh K, Tyler M, Patnaik D, Wesseling H, Brandon NJ, Steen J, Graether SP, Haggarty SJ, Lalonde J. J Neurochem 158 1058-1073 (2021)
  30. Arc: building a bridge from viruses to memory. Day C, Shepherd JD. Biochem J 469 e1-3 (2015)
  31. Herpes Simplex Virus Type 1 Enhances Expression of the Synaptic Protein Arc for Its Own Benefit. Acuña-Hinrichsen F, Muñoz M, Hott M, Martin C, Mancilla E, Salazar P, Leyton L, Zambrano A, Concha MI, Burgos PV, Otth C. Front Cell Neurosci 12 505 (2018)
  32. Genetic Feedback Regulation of Frontal Cortical Neuronal Ensembles Through Activity-Dependent Arc Expression and Dopaminergic Input. Mastwal S, Cao V, Wang KH. Front Neural Circuits 10 100 (2016)
  33. Genomic Study of COVID-19 Corona Virus Excludes Its Origin from Recombination or Characterized Biological Sources and Suggests a Role for HERVS in Its Wide Range Symptoms. El-Shehawi AM, Alotaibi SS, Elseehy MM. Cytol Genet 54 588-604 (2020)
  34. Going retro: ancient viral origins of cognition. Campioni MR, Finkbeiner S. Neuron 86 346-348 (2015)
  35. Regulatory Architecture of the Neuronal Cacng2/Tarpγ2 Gene Promoter: Multiple Repressive Domains, a Polymorphic Regulatory Short Tandem Repeat, and Bidirectional Organization with Co-regulated lncRNAs. Corney BPA, Widnall CL, Rees DJ, Davies JS, Crunelli V, Carter DA. J Mol Neurosci 67 282-294 (2019)
  36. Arc weakens synapses by dispersing AMPA receptors from postsynaptic density via modulating PSD phase separation. Chen X, Jia B, Araki Y, Liu B, Ye F, Huganir R, Zhang M. Cell Res 32 914-930 (2022)
  37. Arc-Mediated Plasticity in the Paraventricular Thalamic Nucleus Promotes Habituation to Stress. Corbett BF, Luz S, Arner J, Vigderman A, Urban K, Bhatnagar S. Biol Psychiatry 92 116-126 (2022)
  38. Common variants in the ARC gene are not associated with cognitive abilities. Myrum C, Giddaluru S, Jacobsen K, Espeseth T, Nyberg L, Lundervold AJ, Haavik J, Nilsson LG, Reinvang I, Steen VM, Johansson S, Wibrand K, Le Hellard S, Bramham CR. Brain Behav 5 e00376 (2015)
  39. Crystal and solution structures reveal oligomerization of individual capsid homology domains of Drosophila Arc. Hallin EI, Markússon S, Böttger L, Torda AE, Bramham CR, Kursula P. PLoS One 16 e0251459 (2021)
  40. Development and Validation of Arc Nanobodies: New Tools for Probing Arc Dynamics and Function. Ishizuka Y, Mergiya TF, Baldinotti R, Xu J, Hallin EI, Markússon S, Kursula P, Bramham CR. Neurochem Res 47 2656-2666 (2022)
  41. Structure of an Arc-ane virus-like capsid. Budnik V, Thomson T. Nat Neurosci 23 153-154 (2020)
  42. Bidirectional protein-protein interactions control liquid-liquid phase separation of PSD-95 and its interaction partners. Christensen NR, Pedersen CP, Sereikaite V, Pedersen JN, Vistrup-Parry M, Sørensen AT, Otzen D, Teilum K, Madsen KL, Strømgaard K. iScience 25 103808 (2022)
  43. Characterization of the C-terminal tail of the Arc protein. Boldridge M, Shimabukuro J, Nakamatsu K, Won C, Jansen C, Turner H, Wang L. PLoS One 15 e0239870 (2020)
  44. High-affinity anti-Arc nanobodies provide tools for structural and functional studies. Markússon S, Hallin EI, Bustad HJ, Raasakka A, Xu J, Muruganandam G, Loris R, Martinez A, Bramham CR, Kursula P. PLoS One 17 e0269281 (2022)
  45. Stress Diminishes BDNF-stimulated TrkB Signaling, TrkB-NMDA Receptor Linkage and Neuronal Activity in the Rat Brain. Robinson S, Mogul AS, Taylor-Yeremeeva EM, Khan A, Tirabassi AD, Wang HY. Neuroscience 473 142-158 (2021)
  46. Aberrant hippocampal transmission and behavior in mice with a stargazin mutation linked to intellectual disability. Caldeira GL, Inácio AS, Beltrão N, Barreto CAV, Rodrigues MV, Rondão T, Macedo R, Gouveia RP, Edfawy M, Guedes J, Cruz B, Louros SR, Moreira IS, Peça J, Carvalho AL. Mol Psychiatry 27 2457-2469 (2022)
  47. Prions induce an early Arc response and a subsequent reduction in mGluR5 in the hippocampus. Ojeda-Juárez D, Lawrence JA, Soldau K, Pizzo DP, Wheeler E, Aguilar-Calvo P, Khuu H, Chen J, Malik A, Funk G, Nam P, Sanchez H, Geschwind MD, Wu C, Yeo GW, Chen X, Patrick GN, Sigurdson CJ. Neurobiol Dis 172 105834 (2022)
  48. Remembering and forgetting in sleep: Selective synaptic plasticity during sleep driven by scaling factors Homer1a and Arc. Diering GH. Neurobiol Stress 22 100512 (2023)
  49. An extracellular vesicle targeting ligand that binds to Arc proteins and facilitates Arc transport in vivo. Lee PH, Anaya M, Ladinsky MS, Reitsma JM, Zinn K. Elife 12 e82874 (2023)
  50. Arc ubiquitination regulates endoplasmic reticulum-mediated Ca2+ release and CaMKII signaling. Ghane MA, Wei W, Yakout DW, Allen ZD, Miller CL, Dong B, Yang JJ, Fang N, Mabb AM. Front Cell Neurosci 17 1091324 (2023)
  51. Arc-Mediated Synaptic Plasticity Regulates Cognitive Function in a Migraine Mouse Model. Hu L, Gong Q, Zhou Y, Wang Y, Qiu T, Fang Y, Huang W, Liang J, Xiao Z. Brain Sci 13 331 (2023)
  52. Retroviral Elements in Human Evolution and Neural Development. Wang T, Doucet-O'Hare TT, Henderson L, Abrams RPM, Nath A. J Exp Neurol 2 1-9 (2021)
  53. Structural evidence that MOAP1 and PEG10 are derived from retrovirus/retrotransposon Gag proteins. Zurowska K, Alam A, Ganser-Pornillos BK, Pornillos O. Proteins 90 309-313 (2022)
  54. ARC/Arg3.1 expression in the lateral geniculate body of monocular form deprivation amblyopic kittens. Fan H, Wang Y, Zou Y, Song W, Xie J, Tang X, Chen S. BMC Ophthalmol 23 3 (2023)
  55. Adolescent neurostimulation of dopamine circuit reverses genetic deficits in frontal cortex function. Mastwal S, Li X, Stowell R, Manion M, Zhang W, Kim NS, Yoon KJ, Song H, Ming GL, Wang KH. Elife 12 RP87414 (2023)
  56. Captive ERVWE1 triggers impairment of 5-HT neuronal plasticity in the first-episode schizophrenia by post-transcriptional activation of HTR1B in ALKBH5-m6A dependent epigenetic mechanisms. Wu X, Liu L, Xue X, Li X, Zhao K, Zhang J, Li W, Yao W, Ding S, Jia C, Zhu F. Cell Biosci 13 213 (2023)
  57. Detection of Arc/Arg3.1 oligomers in rat brain: constitutive and synaptic activity-evoked dimer expression in vivo. Mergiya TF, Gundersen JET, Kanhema T, Brighter G, Ishizuka Y, Bramham CR. Front Mol Neurosci 16 1142361 (2023)
  58. Mimicking Protein Kinase C Phosphorylation Inhibits Arc/Arg3.1 Palmitoylation and Its Interaction with Nucleic Acids. Barylko B, Taylor CA, Wang J, Earnest S, Stippec S, Binns DD, Brautigam CA, Jameson DM, DeMartino GN, Cobb MH, Albanesi JP. Int J Mol Sci 25 780 (2024)
  59. NMDA Receptor-Arc Signaling Is Required for Memory Updating and Is Disrupted in Alzheimer's Disease. Yang L, Liu W, Shi L, Wu J, Zhang W, Chuang YA, Redding-Ochoa J, Kirkwood A, Savonenko AV, Worley PF. Biol Psychiatry 94 706-720 (2023)
  60. The CERV protein of Cer1, a C. elegans LTR retrotransposon, is required for nuclear export of viral genomic RNA and can form giant nuclear rods. Sun B, Kim H, Mello CC, Priess JR. PLoS Genet 19 e1010804 (2023)
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