{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,8]],"date-time":"2026-10-08T01:46:58Z","timestamp":1791424018838,"version":"4.3.3"},"update-to":[{"DOI":"10.1371\/journal.pgen.1010827","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2023,7,14]],"date-time":"2023-07-14T00:00:00Z","timestamp":1689292800000}}],"reference-count":66,"publisher":"Public Library of Science (PLoS)","issue":"7","license":[{"start":{"date-parts":[[2023,7,3]],"date-time":"2023-07-03T00:00:00Z","timestamp":1688342400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100002855","name":"Ministry of Science and Technology of the People's Republic of China","doi-asserted-by":"publisher","award":["2021ZD0203200-02"],"award-info":[{"award-number":["2021ZD0203200-02"]}],"id":[{"id":"10.13039\/501100002855","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31930021"],"award-info":[{"award-number":["31930021"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32022035"],"award-info":[{"award-number":["32022035"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosgenetics.org"],"crossmark-restriction":false},"short-container-title":["PLoS Genet"],"abstract":"<jats:p>Sleep disruptions are quite common in psychological disorders, but the underlying mechanism remains obscure. Wolfram syndrome 1 (WS1) is an autosomal recessive disease mainly characterized by diabetes insipidus\/mellitus, neurodegeneration and psychological disorders. It is caused by loss-of function mutations of the <jats:italic>WOLFRAM SYNDROME 1<\/jats:italic> (<jats:italic>WFS1<\/jats:italic>) gene, which encodes an endoplasmic reticulum (ER)-resident transmembrane protein. Heterozygous mutation carriers do not develop WS1 but exhibit 26-fold higher risk of having psychological disorders. Since WS1 patients display sleep abnormalities, we aimed to explore the role of WFS1 in sleep regulation so as to help elucidate the cause of sleep disruptions in psychological disorders. We found in <jats:italic>Drosophila<\/jats:italic> that knocking down <jats:italic>wfs1<\/jats:italic> in all neurons and <jats:italic>wfs1<\/jats:italic> mutation lead to reduced sleep and dampened circadian rhythm. These phenotypes are mainly caused by lack of <jats:italic>wfs1<\/jats:italic> in dopamine 2-like receptor (Dop2R) neurons which act to promote wake. Consistently, the influence of <jats:italic>wfs1<\/jats:italic> on sleep is blocked or partially rescued by inhibiting or knocking down the rate-limiting enzyme of dopamine synthesis, suggesting that <jats:italic>wfs1<\/jats:italic> modulates sleep via dopaminergic signaling. Knocking down <jats:italic>wfs1<\/jats:italic> alters the excitability of Dop2R neurons, while genetic interactions reveal that lack of <jats:italic>wfs1<\/jats:italic> reduces sleep via perturbation of ER-mediated calcium homeostasis. Taken together, we propose a role for <jats:italic>wfs1<\/jats:italic> in modulating the activities of Dop2R neurons by impinging on intracellular calcium homeostasis, and this in turn influences sleep. These findings provide a potential mechanistic insight for pathogenesis of diseases associated with <jats:italic>WFS1<\/jats:italic> mutations.<\/jats:p>","DOI":"10.1371\/journal.pgen.1010827","type":"journal-article","created":{"date-parts":[[2023,7,3]],"date-time":"2023-07-03T17:27:19Z","timestamp":1688405239000},"page":"e1010827","update-policy":"https:\/\/doi.org\/10.1371\/journal.pgen.corrections_policy","source":"Crossref","is-referenced-by-count":12,"title":["Wolfram syndrome 1 regulates sleep in dopamine receptor neurons by modulating calcium homeostasis"],"prefix":"10.1371","volume":"19","author":[{"given":"Huanfeng","family":"Hao","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li","family":"Song","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5996-6975","authenticated-orcid":true,"given":"Luoying","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2023,7,3]]},"reference":[{"issue":"4","key":"pgen.1010827.ref001","doi-asserted-by":"crossref","first-page":"743","DOI":"10.1016\/j.psc.2015.07.006","article-title":"Sleep Disturbances in Mood Disorders.","volume":"38","author":"ME Rumble","year":"2015","journal-title":"Psychiatr Clin North Am."},{"issue":"2","key":"pgen.1010827.ref002","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1038\/2441","article-title":"A gene encoding a transmembrane protein is mutated in patients with diabetes mellitus and optic atrophy (Wolfram syndrome).","volume":"20","author":"H Inoue","year":"1998","journal-title":"Nat Genet"},{"issue":"13","key":"pgen.1010827.ref003","doi-asserted-by":"crossref","first-page":"2021","DOI":"10.1093\/hmg\/7.13.2021","article-title":"Diabetes insipidus, diabetes mellitus, optic atrophy and deafness (DIDMOAD) caused by mutations in a novel gene (wolframin) coding for a predicted transmembrane protein.","volume":"7","author":"TM Strom","year":"1998","journal-title":"Hum Mol Genet"},{"issue":"5","key":"pgen.1010827.ref004","doi-asserted-by":"crossref","first-page":"921","DOI":"10.1038\/pr.2018.17","article-title":"Genetic and clinical aspects of Wolfram syndrome 1, a severe neurodegenerative disease","volume":"83","author":"L Rigoli","year":"2018","journal-title":"Pediatr Res"},{"issue":"1","key":"pgen.1010827.ref005","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1038\/sj.mp.4000344","article-title":"Predisposition of Wolfram syndrome heterozygotes to psychiatric illness","volume":"3","author":"RG Swift","year":"1998","journal-title":"Mol Psychiatry"},{"issue":"9","key":"pgen.1010827.ref006","doi-asserted-by":"crossref","first-page":"787","DOI":"10.1016\/S0006-3223(00)00244-4","article-title":"Psychiatric disorders and mutations at the Wolfram syndrome locus","volume":"47","author":"M Swift","year":"2000","journal-title":"Biol Psychiatry"},{"key":"pgen.1010827.ref007","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.08752","article-title":"Layer 2\/3 pyramidal cells in the medial prefrontal cortex moderate stress induced depressive behaviors.","volume":"4","author":"P Shrestha","year":"2015","journal-title":"eLife"},{"key":"pgen.1010827.ref008","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1186\/s13023-015-0282-1","article-title":"Selective cognitive and psychiatric manifestations in Wolfram Syndrome.","volume":"10","author":"AN Bischoff","year":"2015","journal-title":"Orphanet J Rare Dis"},{"issue":"6","key":"pgen.1010827.ref009","doi-asserted-by":"crossref","first-page":"775","DOI":"10.1176\/ajp.148.6.775","article-title":"Psychiatric disorders in 36 families with Wolfram syndrome.","volume":"148","author":"RG Swift","year":"1991","journal-title":"Am J Psychiatry"},{"issue":"52","key":"pgen.1010827.ref010","doi-asserted-by":"crossref","first-page":"52755","DOI":"10.1074\/jbc.M310331200","article-title":"Wolframin expression induces novel ion channel activity in endoplasmic reticulum membranes and increases intracellular calcium","volume":"278","author":"AA Osman","year":"2003","journal-title":"J Biol Chem"},{"issue":"47","key":"pgen.1010827.ref011","doi-asserted-by":"crossref","first-page":"39609","DOI":"10.1074\/jbc.M507426200","article-title":"WFS1 is a novel component of the unfolded protein response and maintains homeostasis of the endoplasmic reticulum in pancreatic beta-cells","volume":"280","author":"SG Fonseca","year":"2005","journal-title":"J Biol Chem"},{"issue":"7","key":"pgen.1010827.ref012","doi-asserted-by":"crossref","first-page":"e1002511","DOI":"10.1371\/journal.pbio.1002511","article-title":"Role of Mitochondrial Dynamics in Neuronal Development: Mechanism for Wolfram Syndrome","volume":"14","author":"M Cagalinec","year":"2016","journal-title":"PLoS Biol"},{"issue":"553","key":"pgen.1010827.ref013","doi-asserted-by":"crossref","DOI":"10.1126\/scisignal.aaq1380","article-title":"ER-mitochondria cross-talk is regulated by the Ca(2+) sensor NCS1 and is impaired in Wolfram syndrome.","volume":"11","author":"C Angebault","year":"2018","journal-title":"Sci Signal."},{"issue":"11","key":"pgen.1010827.ref014","doi-asserted-by":"crossref","first-page":"1159","DOI":"10.1093\/hmg\/ddh125","article-title":"Disruption of the WFS1 gene in mice causes progressive beta-cell loss and impaired stimulus-secretion coupling in insulin secretion","volume":"13","author":"H Ishihara","year":"2004","journal-title":"Hum Mol Genet"},{"issue":"11","key":"pgen.1010827.ref015","doi-asserted-by":"crossref","first-page":"2313","DOI":"10.1007\/s00125-005-1947-4","article-title":"Mice conditionally lacking the Wolfram gene in pancreatic islet beta cells exhibit diabetes as a result of enhanced endoplasmic reticulum stress and apoptosis","volume":"48","author":"AC Riggs","year":"2005","journal-title":"Diabetologia"},{"issue":"10","key":"pgen.1010827.ref016","doi-asserted-by":"crossref","first-page":"1600","DOI":"10.1093\/hmg\/ddl081","article-title":"WFS1-deficiency increases endoplasmic reticulum stress, impairs cell cycle progression and triggers the apoptotic pathway specifically in pancreatic beta-cells","volume":"15","author":"T Yamada","year":"2006","journal-title":"Hum Mol Genet"},{"issue":"1","key":"pgen.1010827.ref017","doi-asserted-by":"crossref","first-page":"e1007196","DOI":"10.1371\/journal.pgen.1007196","article-title":"Knockdown of wfs1, a fly homolog of Wolfram syndrome 1, in the nervous system increases susceptibility to age- and stress-induced neuronal dysfunction and degeneration in Drosophila.","volume":"14","author":"Y Sakakibara","year":"2018","journal-title":"PLoS Genet."},{"issue":"3","key":"pgen.1010827.ref018","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1152\/physrev.1994.74.3.595","article-title":"Molecular and cellular physiology of intracellular calcium stores","volume":"74","author":"T Pozzan","year":"1994","journal-title":"Physiol Rev"},{"issue":"3","key":"pgen.1010827.ref019","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1016\/0896-6273(94)90022-1","article-title":"Ectopic and increased expression of Fasciclin II alters motoneuron growth cone guidance","volume":"13","author":"DM Lin","year":"1994","journal-title":"Neuron"},{"issue":"1","key":"pgen.1010827.ref020","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1006\/dbio.2001.0411","article-title":"Peripheral glia direct axon guidance across the CNS\/PNS transition zone","volume":"238","author":"KJ Sepp","year":"2001","journal-title":"Dev Biol"},{"issue":"220","key":"pgen.1010827.ref021","doi-asserted-by":"crossref","first-page":"pl6","DOI":"10.1126\/stke.2202004pl6","article-title":"Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila","volume":"2004","author":"SE McGuire","year":"2004","journal-title":"Sci STKE"},{"issue":"1","key":"pgen.1010827.ref022","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3109\/01677068909107096","article-title":"Reciprocal behaviour associated with altered homeostasis and photosensitivity of Drosophila clock mutants","volume":"6","author":"RJ Konopka","year":"1989","journal-title":"J Neurogenet"},{"key":"pgen.1010827.ref023","doi-asserted-by":"crossref","first-page":"4044","DOI":"10.1002\/j.1460-2075.1995.tb00075.x","article-title":"Suppression of PERIOD protein abundance and circadian cycling by the Drosophila clock mutation timeless","volume":"14","author":"JL Price","year":"1995","journal-title":"EMBO J"},{"issue":"24","key":"pgen.1010827.ref024","doi-asserted-by":"crossref","first-page":"5173","DOI":"10.1523\/JNEUROSCI.3074-19.2021","article-title":"Weekend Light Shifts Evoke Persistent Drosophila Circadian Neural Network Desynchrony","volume":"41","author":"C Nave","year":"2021","journal-title":"J Neurosci"},{"issue":"2","key":"pgen.1010827.ref025","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1038\/s41580-019-0179-2","article-title":"Molecular mechanisms and physiological importance of circadian rhythms","volume":"21","author":"A Patke","year":"2020","journal-title":"Nature reviews Molecular cell biology"},{"issue":"4","key":"pgen.1010827.ref026","doi-asserted-by":"crossref","first-page":"849","DOI":"10.1016\/j.pbb.2005.06.008","article-title":"A developmental role for catecholamines in Drosophila behavior","volume":"81","author":"RG Pendleton","year":"2005","journal-title":"Pharmacol Biochem Behav"},{"issue":"1707","key":"pgen.1010827.ref027","first-page":"906","article-title":"Dopamine in Drosophila: setting arousal thresholds in a miniature brain","volume":"278","author":"B Van Swinderen","year":"2011","journal-title":"Proc Biol Sci"},{"key":"pgen.1010827.ref028","article-title":"Sleep-promoting effects of threonine link amino acid metabolism in Drosophila neuron to GABAergic control of sleep drive","volume":"8","author":"Y Ki","year":"2019","journal-title":"eLife"},{"issue":"1","key":"pgen.1010827.ref029","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/j.nbd.2010.02.012","article-title":"Dopamine-dependent neurodegeneration in Drosophila models of familial and sporadic Parkinson\u2019s disease","volume":"40","author":"F Bayersdorfer","year":"2010","journal-title":"Neurobiol Dis"},{"issue":"5","key":"pgen.1010827.ref030","doi-asserted-by":"crossref","first-page":"876","DOI":"10.1016\/j.neuron.2019.01.045","article-title":"Chemoconnectomics: Mapping Chemical Transmission in Drosophila","volume":"101","author":"B Deng","year":"2019","journal-title":"Neuron"},{"issue":"1","key":"pgen.1010827.ref031","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1093\/chemse\/bjq100","article-title":"Go alpha is involved in sugar perception in Drosophila","volume":"36","author":"N Bredendiek","year":"2011","journal-title":"Chem Senses"},{"issue":"11","key":"pgen.1010827.ref032","doi-asserted-by":"crossref","first-page":"5118","DOI":"10.1073\/pnas.1812342116","article-title":"Suppression of GABAergic neurons through D2-like receptor secures efficient conditioning in Drosophila aversive olfactory learning","volume":"116","author":"M Zhou","year":"2019","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"5","key":"pgen.1010827.ref033","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1016\/S0092-8674(00)81637-2","article-title":"CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity","volume":"95","author":"P Emery","year":"1998","journal-title":"Cell"},{"issue":"6777","key":"pgen.1010827.ref034","doi-asserted-by":"crossref","first-page":"456","DOI":"10.1038\/35006558","article-title":"A unique circadian-rhythm photoreceptor","volume":"404","author":"P Emery","year":"2000","journal-title":"Nature"},{"issue":"7201","key":"pgen.1010827.ref035","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1038\/nature07001","article-title":"An internal thermal sensor controlling temperature preference in Drosophila","volume":"454","author":"FN Hamada","year":"2008","journal-title":"Nature"},{"issue":"2","key":"pgen.1010827.ref036","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1523\/JNEUROSCI.3915-05.2006","article-title":"Electrical hyperexcitation of lateral ventral pacemaker neurons desynchronizes downstream circadian oscillators in the fly circadian circuit and induces multiple behavioral periods","volume":"26","author":"MN Nitabach","year":"2006","journal-title":"J Neurosci"},{"issue":"1","key":"pgen.1010827.ref037","doi-asserted-by":"crossref","first-page":"89","DOI":"10.3109\/01677063.2011.642910","article-title":"Mapping neural circuits with activity-dependent nuclear import of a transcription factor","volume":"26","author":"K Masuyama","year":"2012","journal-title":"J Neurogenet"},{"issue":"7094","key":"pgen.1010827.ref038","doi-asserted-by":"crossref","first-page":"757","DOI":"10.1038\/nature04811","article-title":"Sleep in Drosophila is regulated by adult mushroom bodies","volume":"441","author":"WJ Joiner","year":"2006","journal-title":"Nature"},{"issue":"7094","key":"pgen.1010827.ref039","doi-asserted-by":"crossref","first-page":"753","DOI":"10.1038\/nature04739","article-title":"A dynamic role for the mushroom bodies in promoting sleep in Drosophila","volume":"441","author":"JL Pitman","year":"2006","journal-title":"Nature"},{"issue":"22","key":"pgen.1010827.ref040","doi-asserted-by":"crossref","first-page":"2915","DOI":"10.1016\/j.cub.2015.09.017","article-title":"Propagation of Homeostatic Sleep Signals by Segregated Synaptic Microcircuits of the Drosophila Mushroom Body","volume":"25","author":"D Sitaraman","year":"2015","journal-title":"Curr Biol"},{"issue":"2","key":"pgen.1010827.ref041","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1101\/pdb.ip067827","article-title":"Synapto-pHluorins: genetically encoded reporters of synaptic transmission","volume":"2012","author":"G. Miesenbock","year":"2012","journal-title":"Cold Spring Harb Protoc"},{"issue":"7458","key":"pgen.1010827.ref042","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1038\/nature12354","article-title":"Ultrasensitive fluorescent proteins for imaging neuronal activity","volume":"499","author":"TW Chen","year":"2013","journal-title":"Nature"},{"issue":"3","key":"pgen.1010827.ref043","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1016\/S0896-6273(00)80701-1","article-title":"Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis","volume":"22","author":"T Lee","year":"1999","journal-title":"Neuron"},{"issue":"5","key":"pgen.1010827.ref044","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1016\/S0092-8674(00)00183-5","article-title":"The amnesiac gene product is expressed in two neurons in the Drosophila brain that are critical for memory","volume":"103","author":"S Waddell","year":"2000","journal-title":"Cell"},{"key":"pgen.1010827.ref045","doi-asserted-by":"crossref","first-page":"128","DOI":"10.3389\/fmed.2019.00128","article-title":"Genetically Encoded Calcium Indicators: A New Tool in Renal Hypertension Research.","volume":"6","author":"C Zhong","year":"2019","journal-title":"Front Med (Lausanne)."},{"issue":"49","key":"pgen.1010827.ref046","first-page":"E5292","article-title":"A calcium-dependent protease as a potential therapeutic target for Wolfram syndrome","volume":"111","author":"S Lu","year":"2014","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"4","key":"pgen.1010827.ref047","doi-asserted-by":"crossref","first-page":"1112","DOI":"10.1111\/j.1476-5381.2009.00369.x","article-title":"Regulation by FK506 and rapamycin of Ca2+ release from the sarcoplasmic reticulum in vascular smooth muscle: the role of FK506 binding proteins and mTOR","volume":"158","author":"D MacMillan","year":"2009","journal-title":"Br J Pharmacol"},{"issue":"3","key":"pgen.1010827.ref048","doi-asserted-by":"crossref","first-page":"758","DOI":"10.1210\/en.2013-1519","article-title":"Calcium efflux from the endoplasmic reticulum leads to beta-cell death","volume":"155","author":"T Hara","year":"2014","journal-title":"Endocrinology"},{"issue":"4","key":"pgen.1010827.ref049","doi-asserted-by":"crossref","first-page":"764","DOI":"10.1016\/j.neuron.2014.09.030","article-title":"A TRPV channel in Drosophila motor neurons regulates presynaptic resting Ca2+ levels, synapse growth, and synaptic transmission","volume":"84","author":"CO Wong","year":"2014","journal-title":"Neuron"},{"issue":"3","key":"pgen.1010827.ref050","doi-asserted-by":"crossref","first-page":"814","DOI":"10.1093\/hmg\/ddu499","article-title":"Sarco(endo)plasmic reticulum ATPase is a molecular partner of Wolfram syndrome 1 protein, which negatively regulates its expression.","volume":"24","author":"M Zatyka","year":"2015","journal-title":"Hum Mol Genet"},{"issue":"3","key":"pgen.1010827.ref051","doi-asserted-by":"crossref","first-page":"e0172825","DOI":"10.1371\/journal.pone.0172825","article-title":"Wfs1 is expressed in dopaminoceptive regions of the amniote brain and modulates levels of D1-like receptors.","volume":"12","author":"T Tekko","year":"2017","journal-title":"PLoS One."},{"issue":"1","key":"pgen.1010827.ref052","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1007\/s13105-010-0048-0","article-title":"Impaired striatal dopamine output of homozygous Wfs1 mutant mice in response to [K+] challenge","volume":"67","author":"V Matto","year":"2011","journal-title":"J Physiol Biochem"},{"key":"pgen.1010827.ref053","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1016\/j.bbr.2013.01.046","article-title":"Evidence for impaired function of dopaminergic system in Wfs1-deficient mice.","volume":"244","author":"T Visnapuu","year":"2013","journal-title":"Behav Brain Res"},{"key":"pgen.1010827.ref054","first-page":"73","article-title":"Control of Sleep by Dopaminergic Inputs to the Drosophila Mushroom Body.","volume":"9","author":"D Sitaraman","year":"2015","journal-title":"Front Neural Circuits."},{"issue":"5","key":"pgen.1010827.ref055","doi-asserted-by":"crossref","first-page":"780","DOI":"10.1016\/j.conb.2013.02.001","article-title":"Role of the basal ganglia in the control of sleep and wakefulness","volume":"23","author":"M Lazarus","year":"2013","journal-title":"Curr Opin Neurobiol"},{"issue":"2","key":"pgen.1010827.ref056","doi-asserted-by":"crossref","first-page":"737","DOI":"10.1534\/genetics.104.031930","article-title":"Analysis of conditional paralytic mutants in Drosophila sarco-endoplasmic reticulum calcium ATPase reveals novel mechanisms for regulating membrane excitability","volume":"169","author":"S Sanyal","year":"2005","journal-title":"Genetics"},{"issue":"18","key":"pgen.1010827.ref057","doi-asserted-by":"crossref","first-page":"3946","DOI":"10.1021\/bi900260y","article-title":"Identification and characterization of wolframin, the product of the wolfram syndrome gene (WFS1), as a novel calmodulin-binding protein.","volume":"48","author":"S Yurimoto","year":"2009","journal-title":"Biochemistry"},{"issue":"5","key":"pgen.1010827.ref058","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1093\/hmg\/10.5.477","article-title":"WFS1 (Wolfram syndrome 1) gene product: predominant subcellular localization to endoplasmic reticulum in cultured cells and neuronal expression in rat brain.","volume":"10","author":"K Takeda","year":"2001","journal-title":"Hum Mol Genet"},{"issue":"6","key":"pgen.1010827.ref059","doi-asserted-by":"crossref","first-page":"642","DOI":"10.1002\/cne.21777","article-title":"Distribution of Wfs1 protein in the central nervous system of the mouse and its relation to clinical symptoms of the Wolfram syndrome","volume":"509","author":"H Luuk","year":"2008","journal-title":"J Comp Neurol"},{"issue":"2","key":"pgen.1010827.ref060","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1016\/j.neures.2009.03.005","article-title":"Wolfram syndrome 1 (Wfs1) mRNA expression in the normal mouse brain during postnatal development.","volume":"64","author":"J Kawano","year":"2009","journal-title":"Neurosci Res"},{"key":"pgen.1010827.ref061","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1016\/j.ijdevneu.2014.03.009","article-title":"Initiation and developmental dynamics of Wfs1 expression in the context of neural differentiation and ER stress in mouse forebrain.","volume":"35","author":"T Tekko","year":"2014","journal-title":"Int J Dev Neurosci"},{"key":"pgen.1010827.ref062","doi-asserted-by":"crossref","first-page":"52","DOI":"10.3389\/fncel.2017.00052","article-title":"Blockade of RyRs in the ER Attenuates 6-OHDA-Induced Calcium Overload, Cellular Hypo-Excitability and Apoptosis in Dopaminergic Neurons.","volume":"11","author":"L Huang","year":"2017","journal-title":"Front Cell Neurosci"},{"issue":"24","key":"pgen.1010827.ref063","doi-asserted-by":"crossref","first-page":"5635","DOI":"10.1016\/j.febslet.2006.09.007","article-title":"WFS1 protein modulates the free Ca(2+) concentration in the endoplasmic reticulum.","volume":"580","author":"D Takei","year":"2006","journal-title":"FEBS Lett"},{"issue":"2","key":"pgen.1010827.ref064","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/S1534-5807(01)00118-6","article-title":"Two isoforms of the Drosophila RNA binding protein, how, act in opposing directions to regulate tendon cell differentiation","volume":"2","author":"H Nabel-Rosen","year":"2002","journal-title":"Developmental cell"},{"issue":"11","key":"pgen.1010827.ref065","article-title":"Processing sleep data created with the Drosophila Activity Monitoring (DAM) System.","volume":"2010","author":"C Pfeiffenberger","year":"2010","journal-title":"Cold Spring Harb Protoc."},{"issue":"6","key":"pgen.1010827.ref066","doi-asserted-by":"crossref","first-page":"969","DOI":"10.1007\/s12264-019-00404-6","article-title":"Nuclear Envelope Protein MAN1 Regulates the Drosophila Circadian Clock via Period.","volume":"35","author":"B Bu","year":"2019","journal-title":"Neurosci Bull."}],"updated-by":[{"DOI":"10.1371\/journal.pgen.1010827","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2023,7,14]],"date-time":"2023-07-14T00:00:00Z","timestamp":1689292800000}}],"container-title":["PLOS Genetics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pgen.1010827","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,7,14]],"date-time":"2023-07-14T17:48:27Z","timestamp":1689356907000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pgen.1010827"}},"subtitle":[],"editor":[{"given":"John","family":"Ewer","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2023,7,3]]},"references-count":66,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2023,7,3]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pgen.1010827","relation":{"new_version":[{"id-type":"doi","id":"10.1371\/journal.pgen.1010827","asserted-by":"object"}]},"ISSN":["1553-7404"],"issn-type":[{"value":"1553-7404","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,7,3]]}}}