{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T05:36:30Z","timestamp":1790141790856,"version":"4.0.1"},"reference-count":77,"publisher":"The Company of Biologists","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:p>The conserved Ca2+-binding protein Frequenin\/Neuronal Calcium Sensor 1 (Frq\/NCS-1) is involved in pathologies that result from abnormal synapse number and probability of neurotransmitter release per synapse. Both synaptic features are likely co-regulated but the intervening mechanisms remain poorly understood. We show here that Drosophila Ric8a\/Synembryn, a receptor-independent activator of G protein complexes, binds Frq2 but not the virtually identical duplicate Frq1. Based on crystallographic data on Frq2 and site directed mutagenesis on Frq1, the differential amino acids R94 and T138 account for this specificity. Human NCS-1 and Ric8a reproduce the binding and maintain the structural requirements at these key positions. Ric8a and G\u03b1s regulate synapse number and neurotransmitter release and both are functionally linked to Frq2. Frq2 negatively regulates Ric8a to control synapse number. However, the regulation of neurotransmitter release by Ric8a is independent from the Frq2 binding. Thus, the antagonistic regulation of these two synaptic properties shares a common pathway, Frq2,Ric8a,G\u03b1s which diverges downstream. These mechanisms expose the Frq2-Ric8a interacting surface as a potential pharmacological target for NCS-1 related diseases and provide key data towards the corresponding drug design.<\/jats:p>","DOI":"10.1242\/jcs.152603","type":"journal-article","created":{"date-parts":[[2014,7,30]],"date-time":"2014-07-30T03:41:58Z","timestamp":1406691718000},"source":"Crossref","is-referenced-by-count":26,"title":["The guanine-exchange factor Ric8a binds the calcium sensor NCS-1 to regulate synapse number and probability of release"],"prefix":"10.1242","author":[{"given":"Jes\u00fas","family":"Romero-Pozuelo","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeffrey S.","family":"Dason","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alicia","family":"Mansilla","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Soledad","family":"Ba\u00f1os-Mateos","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jos\u00e9 L.","family":"Sardina","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antonio","family":"Chaves-Sanju\u00e1n","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jaime","family":"Jurado-G\u00f3mez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elena","family":"Santana","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Harold L.","family":"Atwood","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"\u00c1ngel","family":"Hern\u00e1ndez-Hern\u00e1ndez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mar\u00eda-Jos\u00e9","family":"S\u00e1nchez-Barrena","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alberto","family":"Ferr\u00fas","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"237","published-online":{"date-parts":[[2014,1,1]]},"reference":[{"key":"2021042613341767500_b1","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1016\/j.cell.2004.09.026","article-title":"RIC-8 is required for GPR-1\/2-dependent Galpha function during asymmetric division of C. elegans embryos.","volume":"119","author":"Afshar","year":"2004","journal-title":"Cell"},{"key":"2021042613341767500_b2","doi-asserted-by":"publisher","first-page":"1205","DOI":"10.1016\/j.bbagen.2011.10.003","article-title":"Molecular structure and target recognition of neuronal calcium sensor proteins.","volume":"1820","author":"Ames","year":"2012","journal-title":"Biochim. Biophys. Acta"},{"key":"2021042613341767500_b3","doi-asserted-by":"publisher","first-page":"12149","DOI":"10.1021\/bi0012890","article-title":"Structure and calcium-binding properties of Frq1, a novel calcium sensor in the yeast Saccharomyces cerevisiae.","volume":"39","author":"Ames","year":"2000","journal-title":"Biochemistry"},{"key":"2021042613341767500_b4","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1186\/1750-2187-2-13","article-title":"Scaffolding proteins in G-protein signaling.","volume":"2","author":"Andreeva","year":"2007","journal-title":"J. Mol. Signal."},{"key":"2021042613341767500_b5","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1113\/jphysiol.1986.sp016347","article-title":"Calcium dependence of presynaptic calcium current and post-synaptic response at the squid giant synapse.","volume":"381","author":"Augustine","year":"1986","journal-title":"J. Physiol."},{"key":"2021042613341767500_b6","doi-asserted-by":"publisher","first-page":"1415","DOI":"10.1093\/hmg\/ddg147","article-title":"IL1 receptor accessory protein like, a protein involved in X-linked mental retardation, interacts with Neuronal Calcium Sensor-1 and regulates exocytosis.","volume":"12","author":"Bahi","year":"2003","journal-title":"Hum. Mol. Genet."},{"key":"2021042613341767500_b7","doi-asserted-by":"publisher","first-page":"1790","DOI":"10.1111\/j.1742-4658.2009.06926.x","article-title":"Compartmentalized signalling: spatial regulation of cAMP by the action of compartmentalized phosphodiesterases.","volume":"276","author":"Baillie","year":"2009","journal-title":"FEBS J."},{"key":"2021042613341767500_b1a","doi-asserted-by":"publisher","first-page":"530","DOI":"10.1107\/S2053230X14005408","article-title":"Frq2 from Drosophila melanogaster: cloning, expression, purification, crystallization and preliminary X-ray analysis.","volume":"70","author":"Banos-Mateos","year":"2014","journal-title":"Acta crystallographica. Section F, Structural biology communications"},{"key":"2021042613341767500_b8","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1093\/chemse\/bjp095","article-title":"Expression analysis of the 3 G-protein subunits, Galpha, Gbeta, and Ggamma, in the olfactory receptor organs of adult Drosophila melanogaster.","volume":"35","author":"Boto","year":"2010","journal-title":"Chem. Senses"},{"key":"2021042613341767500_b9","doi-asserted-by":"publisher","first-page":"11949","DOI":"10.1074\/jbc.M009373200","article-title":"Immunocytochemical localization and crystal structure of human frequenin (neuronal calcium sensor 1).","volume":"276","author":"Bourne","year":"2001","journal-title":"J. Biol. Chem."},{"key":"2021042613341767500_b10","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1242\/dev.118.2.401","article-title":"Targeted gene expression as a means of altering cell fates and generating dominant phenotypes.","volume":"118","author":"Brand","year":"1993","journal-title":"Development"},{"key":"2021042613341767500_b11","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1107\/S0907444909042073","article-title":"MolProbity: all-atom structure validation for macromolecular crystallography.","volume":"66","author":"Chen","year":"2010","journal-title":"Acta Crystallogr. D Biol. Crystallogr."},{"key":"2021042613341767500_b12","doi-asserted-by":"publisher","first-page":"2104","DOI":"10.1126\/science.274.5295.2104","article-title":"Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies.","volume":"274","author":"Connolly","year":"1996","journal-title":"Science"},{"key":"2021042613341767500_b13","doi-asserted-by":"publisher","first-page":"4109","DOI":"10.1242\/jcs.055095","article-title":"Frequenin\/NCS-1 and the Ca2+-channel alpha1-subunit co-regulate synaptic transmission and nerve-terminal growth.","volume":"122","author":"Dason","year":"2009","journal-title":"J. Cell Sci."},{"key":"2021042613341767500_b14","doi-asserted-by":"publisher","first-page":"388","DOI":"10.1007\/s12035-012-8250-4","article-title":"Multiple roles for frequenin\/NCS-1 in synaptic function and development.","volume":"45","author":"Dason","year":"2012","journal-title":"Mol. Neurobiol."},{"key":"2021042613341767500_b15","doi-asserted-by":"publisher","first-page":"4319","DOI":"10.1074\/jbc.M110.196436","article-title":"A molecular and structural mechanism for G protein-mediated microtubule destabilization.","volume":"286","author":"Dav\u00e9","year":"2011","journal-title":"J. Biol. Chem."},{"key":"2021042613341767500_b16","doi-asserted-by":"publisher","first-page":"2126","DOI":"10.1107\/S0907444904019158","article-title":"Coot: model-building tools for molecular graphics.","volume":"60","author":"Emsley","year":"2004","journal-title":"Acta Crystallogr. D Biol. Crystallogr."},{"key":"2021042613341767500_b17","doi-asserted-by":"publisher","first-page":"72","DOI":"10.1107\/S0907444905036693","article-title":"Scaling and assessment of data quality.","volume":"62","author":"Evans","year":"2006","journal-title":"Acta Crystallogr. D Biol. Crystallogr."},{"key":"2021042613341767500_b18","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1016\/j.bbamem.2011.09.028","article-title":"Electrostatic interaction between inactivation ball and T1-S1 linker region of Kv1.4 channel.","volume":"1818","author":"Fan","year":"2012","journal-title":"Biochim. Biophys. Acta"},{"key":"2021042613341767500_b19","doi-asserted-by":"publisher","first-page":"40","DOI":"10.3389\/fncel.2014.00040","article-title":"How voltage-gated calcium channels gate forms of homeostatic synaptic plasticity.","volume":"8","author":"Frank","year":"2014","journal-title":"Front. Cell. Neurosci."},{"key":"2021042613341767500_b20","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1016\/S0896-6273(01)00276-8","article-title":"Ca2+ signaling via the neuronal calcium sensor-1 regulates associative learning and memory in C. elegans.","volume":"30","author":"Gomez","year":"2001","journal-title":"Neuron"},{"key":"2021042613341767500_b21","doi-asserted-by":"publisher","first-page":"1133","DOI":"10.1002\/cne.22268","article-title":"Immunocytochemical localization of synaptic proteins to photoreceptor synapses of Drosophila melanogaster.","volume":"518","author":"Hamanaka","year":"2010","journal-title":"J. Comp. Neurol."},{"key":"2021042613341767500_b22","doi-asserted-by":"publisher","first-page":"1099","DOI":"10.1038\/ncb1318","article-title":"Drosophila Ric-8 is essential for plasma-membrane localization of heterotrimeric G proteins.","volume":"7","author":"Hampoelz","year":"2005","journal-title":"Nat. Cell Biol."},{"key":"2021042613341767500_b23","doi-asserted-by":"publisher","first-page":"e10534","DOI":"10.1371\/journal.pone.0010534","article-title":"Structural and functional deficits in a neuronal calcium sensor-1 mutant identified in a case of autistic spectrum disorder.","volume":"5","author":"Handley","year":"2010","journal-title":"PLoS ONE"},{"key":"2021042613341767500_b24","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1016\/j.jmb.2011.12.049","article-title":"The C-terminal tail of human neuronal calcium sensor 1 regulates the conformational stability of the Ca2+- activated state.","volume":"417","author":"Heidarsson","year":"2012","journal-title":"J. Mol. Biol."},{"key":"2021042613341767500_b25","doi-asserted-by":"publisher","first-page":"234","DOI":"10.1038\/12058","article-title":"Yeast homologue of neuronal frequenin is a regulator of phosphatidylinositol-4-OH kinase.","volume":"1","author":"Hendricks","year":"1999","journal-title":"Nat. Cell Biol."},{"key":"2021042613341767500_b26","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1113\/jphysiol.2005.102889","article-title":"Calcium-sensing mechanism in TRPC5 channels contributing to retardation of neurite outgrowth.","volume":"572","author":"Hui","year":"2006","journal-title":"J. Physiol."},{"key":"2021042613341767500_b27","doi-asserted-by":"publisher","first-page":"1095","DOI":"10.1016\/j.neuron.2008.10.050","article-title":"Metabotropic glutamate receptor-mediated LTD involves two interacting Ca(2+) sensors, NCS-1 and PICK1.","volume":"60","author":"Jo","year":"2008","journal-title":"Neuron"},{"key":"2021042613341767500_b28","doi-asserted-by":"publisher","first-page":"3621","DOI":"10.1242\/jcs.102806","article-title":"Presynaptic PI3K activity triggers the formation of glutamate receptors at neuromuscular terminals of Drosophila.","volume":"125","author":"Jord\u00e1n-\u00c1lvarez","year":"2012","journal-title":"J. Cell Sci."},{"key":"2021042613341767500_b29","doi-asserted-by":"crossref","first-page":"8476","DOI":"10.1523\/JNEUROSCI.22-19-08476.2002","article-title":"Interaction with neuronal calcium sensor NCS-1 mediates desensitization of the D2 dopamine receptor.","volume":"22","author":"Kabbani","year":"2002","journal-title":"J. Neurosci."},{"key":"2021042613341767500_b30","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1002\/jcp.10300","article-title":"Human brain synembryn interacts with Gsalpha and Gqalpha and is translocated to the plasma membrane in response to isoproterenol and carbachol.","volume":"195","author":"Klattenhoff","year":"2003","journal-title":"J. Cell. Physiol."},{"key":"2021042613341767500_b31","doi-asserted-by":"publisher","first-page":"14724","DOI":"10.1523\/JNEUROSCI.3612-10.2010","article-title":"Peptide-induced modulation of synaptic transmission and escape response in Drosophila requires two G-protein-coupled receptors.","volume":"30","author":"Klose","year":"2010","journal-title":"J. Neurosci."},{"key":"2021042613341767500_b32","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1073\/pnas.232693499","article-title":"Up-regulation of neuronal calcium sensor-1 (NCS-1) in the prefrontal cortex of schizophrenic and bipolar patients.","volume":"100","author":"Koh","year":"2003","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2021042613341767500_b33","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1016\/S0896-6273(00)80159-2","article-title":"Intracellular Ca2+ fluctuations modulate the rate of neuronal migration.","volume":"17","author":"Komuro","year":"1996","journal-title":"Neuron"},{"key":"2021042613341767500_b34","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1107\/S0907444905039107","article-title":"The integration of macromolecular diffraction data.","volume":"62","author":"Leslie","year":"2006","journal-title":"Acta Crystallogr. D Biol. Crystallogr."},{"key":"2021042613341767500_b35","doi-asserted-by":"publisher","first-page":"e27779","DOI":"10.1371\/journal.pone.0027779","article-title":"Characterisation of the interaction of the C-terminus of the dopamine D2 receptor with neuronal calcium sensor-1.","volume":"6","author":"Lian","year":"2011","journal-title":"PLoS ONE"},{"key":"2021042613341767500_b36","doi-asserted-by":"publisher","first-page":"2659","DOI":"10.1152\/jn.00515.2002","article-title":"Fast calcium signals in Drosophila motor neuron terminals.","volume":"88","author":"Macleod","year":"2002","journal-title":"J. Neurophysiol."},{"key":"2021042613341767500_b37","doi-asserted-by":"publisher","first-page":"587","DOI":"10.1139\/o90-084","article-title":"Calcium binding proteins. Elucidating the contributions to calcium affinity from an analysis of species variants and peptide fragments.","volume":"68","author":"Marsden","year":"1990","journal-title":"Biochem. Cell Biol."},{"key":"2021042613341767500_b38","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1186\/1756-6606-6-39","article-title":"Identification of key structural elements for neuronal calcium sensor-1 function in the regulation of the temperature-dependency of locomotion in C. elegans.","volume":"6","author":"Martin","year":"2013","journal-title":"Mol. Brain"},{"key":"2021042613341767500_b39","doi-asserted-by":"crossref","first-page":"446","DOI":"10.1128\/JB.134.2.446-457.1978","article-title":"Genetic control of galactokinase synthesis in Saccharomyces cerevisiae: evidence for constitutive expression of the positive regulatory gene gal4.","volume":"134","author":"Matsumoto","year":"1978","journal-title":"J. Bacteriol."},{"key":"2021042613341767500_b40","doi-asserted-by":"publisher","first-page":"804","DOI":"10.1126\/science.2536957","article-title":"Splice variants of the alpha subunit of the G protein Gs activate both adenylyl cyclase and calcium channels.","volume":"243","author":"Mattera","year":"1989","journal-title":"Science"},{"key":"2021042613341767500_b41","doi-asserted-by":"publisher","first-page":"658","DOI":"10.1107\/S0021889807021206","article-title":"Phaser crystallographic software.","volume":"40","author":"McCoy","year":"2007","journal-title":"J. Appl. Crystallogr."},{"key":"2021042613341767500_b42","doi-asserted-by":"publisher","first-page":"386","DOI":"10.1107\/S0907444911007281","article-title":"Presenting your structures: the CCP4mg molecular-graphics software.","volume":"67","author":"McNicholas","year":"2011","journal-title":"Acta Crystallogr. D Biol. Crystallogr."},{"key":"2021042613341767500_b43","doi-asserted-by":"crossref","first-page":"3159","DOI":"10.1113\/jphysiol.2012.248625","article-title":"Organization and function of transmitter release sites at the neuromuscular junction.","volume":"591","author":"Meriney","year":"2013","journal-title":"J. Physiol."},{"key":"2021042613341767500_b44","doi-asserted-by":"publisher","first-page":"323","DOI":"10.1016\/S0896-6273(00)80847-8","article-title":"Goalpha and diacylglycerol kinase negatively regulate the Gqalpha pathway in C. elegans.","volume":"24","author":"Miller","year":"1999","journal-title":"Neuron"},{"key":"2021042613341767500_b45","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1016\/S0896-6273(00)00037-4","article-title":"RIC-8 (Synembryn): a novel conserved protein that is required for G(q)alpha signaling in the C. elegans nervous system.","volume":"27","author":"Miller","year":"2000","journal-title":"Neuron"},{"key":"2021042613341767500_b46","doi-asserted-by":"publisher","first-page":"42","DOI":"10.1159\/000186689","article-title":"Functions and regulatory mechanisms of Gq-signaling pathways.","volume":"17","author":"Mizuno","year":"2009","journal-title":"Neurosignals"},{"key":"2021042613341767500_b47","doi-asserted-by":"publisher","first-page":"240","DOI":"10.1107\/S0907444996012255","article-title":"Refinement of macromolecular structures by the maximum-likelihood method.","volume":"53","author":"Murshudov","year":"1997","journal-title":"Acta Crystallogr. D Biol. Crystallogr."},{"key":"2021042613341767500_b48","doi-asserted-by":"publisher","first-page":"565","DOI":"10.1083\/jcb.200908055","article-title":"A Syd-1 homologue regulates pre- and postsynaptic maturation in Drosophila.","volume":"188","author":"Owald","year":"2010","journal-title":"J. Cell Biol."},{"key":"2021042613341767500_b49","doi-asserted-by":"publisher","first-page":"496","DOI":"10.1016\/j.ceb.2010.05.001","article-title":"Cell biology of Ca2+-triggered exocytosis.","volume":"22","author":"Pang","year":"2010","journal-title":"Curr. Opin. Cell Biol."},{"key":"2021042613341767500_b50","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1016\/j.cub.2009.12.030","article-title":"A postsynaptic signaling pathway that may account for the cognitive defect due to IL1RAPL1 mutation.","volume":"20","author":"Pavlowsky","year":"2010","journal-title":"Curr. Biol."},{"key":"2021042613341767500_b51","doi-asserted-by":"publisher","first-page":"987","DOI":"10.1038\/nsmb1164","article-title":"Three-dimensional structure of the KChIP1-Kv4.3 T1 complex reveals a cross-shaped octamer.","volume":"13","author":"Pioletti","year":"2006","journal-title":"Nat. Struct. Mol. Biol."},{"key":"2021042613341767500_b52","doi-asserted-by":"publisher","first-page":"3965","DOI":"10.1093\/hmg\/ddn300","article-title":"Mutations in the calcium-related gene IL1RAPL1 are associated with autism.","volume":"17","author":"Piton","year":"2008","journal-title":"Hum. Mol. Genet."},{"key":"2021042613341767500_b53","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1016\/0896-6273(93)90267-U","article-title":"Frequenin\u2014a novel calcium-binding protein that modulates synaptic efficacy in the Drosophila nervous system.","volume":"11","author":"Pongs","year":"1993","journal-title":"Neuron"},{"key":"2021042613341767500_b54","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1186\/1471-2148-5-28","article-title":"Subfunctionalization of duplicated genes as a transition state to neofunctionalization.","volume":"5","author":"Rastogi","year":"2005","journal-title":"BMC Evol. Biol."},{"key":"2021042613341767500_b55","doi-asserted-by":"publisher","first-page":"2620","DOI":"10.1152\/jn.01072.2002","article-title":"Mutation and activation of Galpha s similarly alters pre- and postsynaptic mechanisms modulating neurotransmission.","volume":"89","author":"Renden","year":"2003","journal-title":"J. Neurophysiol."},{"key":"2021042613341767500_b56","doi-asserted-by":"publisher","first-page":"2428","DOI":"10.1111\/j.1460-9568.2007.05877.x","article-title":"Chronic and acute alterations in the functional levels of Frequenins 1 and 2 reveal their roles in synaptic transmission and axon terminal morphology.","volume":"26","author":"Romero-Pozuelo","year":"2007","journal-title":"Eur. J. Neurosci."},{"key":"2021042613341767500_b57","doi-asserted-by":"publisher","first-page":"R777","DOI":"10.1016\/j.cub.2008.07.035","article-title":"Coordinating speed and amplitude in G-protein signaling.","volume":"18","author":"Ross","year":"2008","journal-title":"Curr. Biol."},{"key":"2021042613341767500_b58","doi-asserted-by":"publisher","first-page":"4654","DOI":"10.1111\/j.1742-4658.2008.06614.x","article-title":"Submembraneous microtubule cytoskeleton: regulation of microtubule assembly by heterotrimeric Gproteins.","volume":"275","author":"Roychowdhury","year":"2008","journal-title":"FEBS J."},{"key":"2021042613341767500_b59","doi-asserted-by":"publisher","first-page":"643","DOI":"10.1016\/j.neuron.2009.08.014","article-title":"NCS-1 in the dentate gyrus promotes exploration, synaptic plasticity, and rapid acquisition of spatial memory.","volume":"63","author":"Saab","year":"2009","journal-title":"Neuron"},{"key":"2021042613341767500_b60","doi-asserted-by":"publisher","first-page":"54","DOI":"10.1186\/1471-2148-10-54","article-title":"Two frequenins in Drosophila: unveiling the evolutionary history of an unusual neuronal calcium sensor (NCS) duplication.","volume":"10","author":"S\u00e1nchez-Gracia","year":"2010","journal-title":"BMC Evol. Biol."},{"key":"2021042613341767500_b61","doi-asserted-by":"publisher","first-page":"9253","DOI":"10.1073\/pnas.93.17.9253","article-title":"Direct modulation of calmodulin targets by the neuronal calcium sensor NCS-1.","volume":"93","author":"Schaad","year":"1996","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2021042613341767500_b62","doi-asserted-by":"publisher","first-page":"3","DOI":"10.3389\/fnmol.2014.00003","article-title":"Presynaptic [Ca(2+)] and GCAPs: aspects on the structure and function of photoreceptor ribbon synapses.","volume":"7","author":"Schmitz","year":"2014","journal-title":"Front. Mol. Neurosci."},{"key":"2021042613341767500_b63","doi-asserted-by":"publisher","first-page":"30949","DOI":"10.1074\/jbc.M705499200","article-title":"Structural insights into activation of phosphatidylinositol 4-kinase (Pik1) by yeast frequenin (Frq1).","volume":"282","author":"Strahl","year":"2007","journal-title":"J. Biol. Chem."},{"key":"2021042613341767500_b64","doi-asserted-by":"publisher","first-page":"8356","DOI":"10.1074\/jbc.M211862200","article-title":"Mammalian Ric-8A (synembryn) is a heterotrimeric Galpha protein guanine nucleotide exchange factor.","volume":"278","author":"Tall","year":"2003","journal-title":"J. Biol. Chem."},{"key":"2021042613341767500_b65","doi-asserted-by":"publisher","first-page":"591","DOI":"10.1016\/S1567-133X(03)00119-4","article-title":"Expression of ric-8 (synembryn) gene in the nervous system of developing and adult mouse.","volume":"3","author":"T\u00f5nissoo","year":"2003","journal-title":"Gene Expr. Patterns"},{"key":"2021042613341767500_b66","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1016\/j.pnpbp.2008.11.011","article-title":"Expression of neuronal calcium sensor-1 (NCS-1) is decreased in leukocytes of schizophrenia and bipolar disorder patients.","volume":"33","author":"Torres","year":"2009","journal-title":"Prog. Neuropsychopharmacol. Biol. Psychiatry"},{"key":"2021042613341767500_b67","doi-asserted-by":"publisher","first-page":"2276","DOI":"10.1126\/science.1068278","article-title":"Neuronal calcium sensor 1 and activity-dependent facilitation of P\/Q-type calcium currents at presynaptic nerve terminals.","volume":"295","author":"Tsujimoto","year":"2002","journal-title":"Science"},{"key":"2021042613341767500_b68","doi-asserted-by":"publisher","first-page":"833","DOI":"10.1016\/j.neuron.2006.02.008","article-title":"Bruchpilot, a protein with homology to ELKS\/CAST, is required for structural integrity and function of synaptic active zones in Drosophila.","volume":"49","author":"Wagh","year":"2006","journal-title":"Neuron"},{"key":"2021042613341767500_b69","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1016\/S0896-6273(01)00434-2","article-title":"Ca(2+) binding protein frequenin mediates GDNF-induced potentiation of Ca(2+) channels and transmitter release.","volume":"32","author":"Wang","year":"2001","journal-title":"Neuron"},{"key":"2021042613341767500_b70","doi-asserted-by":"publisher","first-page":"1091","DOI":"10.1038\/ncb1317","article-title":"Ric-8 controls Drosophila neural progenitor asymmetric division by regulating heterotrimeric G proteins.","volume":"7","author":"Wang","year":"2005","journal-title":"Nat. Cell Biol."},{"key":"2021042613341767500_b71","doi-asserted-by":"publisher","first-page":"32","DOI":"10.1038\/nn1822","article-title":"Structural basis for modulation of Kv4 K+ channels by auxiliary KChIP subunits.","volume":"10","author":"Wang","year":"2007","journal-title":"Nat. Neurosci."},{"key":"2021042613341767500_b72","doi-asserted-by":"publisher","first-page":"40082","DOI":"10.1074\/jbc.M008603200","article-title":"Neuronal Ca2+ sensor-1\/frequenin functions in an autocrine pathway regulating Ca2+ channels in bovine adrenal chromaffin cells.","volume":"275","author":"Weiss","year":"2000","journal-title":"J. Biol. Chem."},{"key":"2021042613341767500_b73","doi-asserted-by":"publisher","first-page":"965","DOI":"10.1152\/physrev.00049.2006","article-title":"Organization and Ca2+ regulation of adenylyl cyclases in cAMP microdomains.","volume":"87","author":"Willoughby","year":"2007","journal-title":"Physiol. Rev."},{"key":"2021042613341767500_b74","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1107\/S0907444910045749","article-title":"Overview of the CCP4 suite and current developments.","volume":"67","author":"Winn","year":"2011","journal-title":"Acta Crystallogr. D Biol. Crystallogr."},{"key":"2021042613341767500_b75","doi-asserted-by":"publisher","first-page":"295","DOI":"10.1016\/j.ydbio.2004.01.007","article-title":"Signaling through Gs alpha is required for the growth and function of neuromuscular synapses in Drosophila.","volume":"268","author":"Wolfgang","year":"2004","journal-title":"Dev. Biol."},{"key":"2021042613341767500_b76","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1038\/47501","article-title":"Turning of nerve growth cones induced by localized increases in intracellular calcium ions.","volume":"403","author":"Zheng","year":"2000","journal-title":"Nature"}],"container-title":["Journal of Cell Science"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/journals.biologists.com\/jcs\/article-pdf\/127\/19\/4246\/1959722\/jcs-127-19-4246.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/jcs\/article-pdf\/doi\/10.1242\/jcs.152603\/2046824\/jcs152603.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/jcs\/article-pdf\/doi\/10.1242\/jcs.152603\/2046824\/jcs152603.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,5,18]],"date-time":"2021-05-18T18:11:10Z","timestamp":1621361470000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/jcs\/article\/doi\/10.1242\/jcs.152603\/259186\/The-guanine-exchange-factor-Ric8a-binds-the"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2014,1,1]]},"references-count":77,"URL":"https:\/\/doi.org\/10.1242\/jcs.152603","relation":{},"ISSN":["1477-9137","0021-9533"],"issn-type":[{"value":"1477-9137","type":"electronic"},{"value":"0021-9533","type":"print"}],"subject":[],"published":{"date-parts":[[2014,1,1]]},"article-number":"jcs.152603"}}