{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T06:40:03Z","timestamp":1791355203928,"version":"4.3.1"},"reference-count":147,"publisher":"MDPI AG","issue":"19","license":[{"start":{"date-parts":[[2021,10,6]],"date-time":"2021-10-06T00:00:00Z","timestamp":1633478400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["FOR2289, Schm797\/8-1 and SFB 894 TP A7"],"award-info":[{"award-number":["FOR2289, Schm797\/8-1 and SFB 894 TP A7"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100020027","name":"Dr. Rolf M. Schwiete Foundation","doi-asserted-by":"publisher","award":["2020-002"],"award-info":[{"award-number":["2020-002"]}],"id":[{"id":"10.13039\/501100020027","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Multiple sclerosis (MS) is an inflammatory disease of the central nervous system that finally leads to demyelination. Demyelinating optic neuritis is a frequent symptom in MS. Recent studies also revealed synapse dysfunctions in MS patients and MS mouse models. We previously reported alterations of photoreceptor ribbon synapses in the experimental auto-immune encephalomyelitis (EAE) mouse model of MS. In the present study, we found that the previously observed decreased imunosignals of photoreceptor ribbons in early EAE resulted from a decrease in synaptic ribbon size, whereas the number\/density of ribbons in photoreceptor synapses remained unchanged. Smaller photoreceptor ribbons are associated with fewer docked and ribbon-associated vesicles. At a functional level, depolarization-evoked exocytosis as monitored by optical recording was diminished even as early as on day 7 after EAE induction. Moreover compensatory, post-depolarization endocytosis was decreased. Decreased post-depolarization endocytosis in early EAE correlated with diminished synaptic enrichment of dynamin3. In contrast, basal endocytosis in photoreceptor synapses of resting non-depolarized retinal slices was increased in early EAE. Increased basal endocytosis correlated with increased de-phosphorylation of dynamin1. Thus, multiple endocytic pathways in photoreceptor synapse are differentially affected in early EAE and likely contribute to the observed synapse pathology in early EAE.<\/jats:p>","DOI":"10.3390\/ijms221910789","type":"journal-article","created":{"date-parts":[[2021,10,7]],"date-time":"2021-10-07T16:23:58Z","timestamp":1633623838000},"page":"10789","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":17,"title":["Early Changes in Exo- and Endocytosis in the EAE Mouse Model of Multiple Sclerosis Correlate with Decreased Synaptic Ribbon Size and Reduced Ribbon-Associated Vesicle Pools in Rod Photoreceptor Synapses"],"prefix":"10.3390","volume":"22","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6001-842X","authenticated-orcid":false,"given":"Ajay","family":"Kesharwani","sequence":"first","affiliation":[{"name":"Department of Neuroanatomy, Institute of Anatomy and Cell Biology, Medical School, Saarland University, 66421 Homburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7328-1427","authenticated-orcid":false,"given":"Karin","family":"Schwarz","sequence":"additional","affiliation":[{"name":"Department of Neuroanatomy, Institute of Anatomy and Cell Biology, Medical School, Saarland University, 66421 Homburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ekta","family":"Dembla","sequence":"additional","affiliation":[{"name":"Department of Neuroanatomy, Institute of Anatomy and Cell Biology, Medical School, Saarland University, 66421 Homburg, Germany"},{"name":"Department of Ophthalmology, Duke University School of Medicine, Durham, NC 27710, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mayur","family":"Dembla","sequence":"additional","affiliation":[{"name":"Department of Neuroanatomy, Institute of Anatomy and Cell Biology, Medical School, Saarland University, 66421 Homburg, Germany"},{"name":"Department of Ophthalmology, Duke University School of Medicine, Durham, NC 27710, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1457-6222","authenticated-orcid":false,"given":"Frank","family":"Schmitz","sequence":"additional","affiliation":[{"name":"Department of Neuroanatomy, Institute of Anatomy and Cell Biology, Medical School, Saarland University, 66421 Homburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,10,6]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1111\/j.1750-3639.2007.00064.x","article-title":"The immunopathology of multiple sclerosis: An overview","volume":"17","author":"Lassmann","year":"2007","journal-title":"Brain Pathol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1038\/nrneurol.2014.37","article-title":"Neurodegeneration and axonal dysfunction in multiple sclerosis","volume":"10","author":"Friese","year":"2014","journal-title":"Nat. Rev. Neurol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1038\/nri3871","article-title":"Immunopathology of multiple sclerosis","volume":"15","author":"Dendrou","year":"2015","journal-title":"Nat. Rev. Immunol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"905","DOI":"10.1038\/s41573-019-0035-2","article-title":"Progressive multiple sclerosis: From pathophysiology to therapeutic strategies","volume":"18","author":"Faissner","year":"2019","journal-title":"Nat. Rev. Drug Discov."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2628","DOI":"10.1093\/brain\/awl222","article-title":"Grey matter damage predicts the evolution of primary progressive multiple sclerosis at 5 years","volume":"129","author":"Rovaris","year":"2006","journal-title":"Brain"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1002\/ana.22337","article-title":"Demyelination causes synaptic alterations in hippocampi from multiple sclerosis patients","volume":"69","author":"Dutta","year":"2011","journal-title":"Ann. Neurol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1093\/brain\/awq346","article-title":"Primary retinal pathology in multiple sclerosis as detected by optical coherence tomography","volume":"134","author":"Saidha","year":"2011","journal-title":"Brain"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"558","DOI":"10.1089\/brain.2014.0265","article-title":"Anatomic connectivity assessed using pathway radial diffusivity is related to functional connectivity in monosynaptic pathways","volume":"4","author":"Lowe","year":"2014","journal-title":"Brain Connect."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1386","DOI":"10.1136\/jnnp-2014-307712","article-title":"Multiple sclerosis deep grey matter: The relation between demyelination, neurodegeneration, inflammation and iron","volume":"85","author":"Haider","year":"2014","journal-title":"J. Neurol. Neurosurg. Psychol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1093\/brain\/awv353","article-title":"Reconstruction of single cortical projection neurons reveals primary spine loss in multiple sclerosis","volume":"139","author":"Jafari","year":"2016","journal-title":"Brain"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1038\/s41593-020-00780-7","article-title":"Phagocyte-mediated synapse removal in cortical neuroinflammation is promoted by local calcium accumulation","volume":"24","author":"Jafari","year":"2021","journal-title":"Nat. Neurosci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1730","DOI":"10.1016\/j.cell.2015.11.023","article-title":"Neuroinflammatory TNF\u03b1 impairs memory via astrocyte signaling","volume":"163","author":"Habbas","year":"2015","journal-title":"Cell"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1148","DOI":"10.1016\/j.clinph.2017.04.006","article-title":"Neurophysiology of synaptic functioning in multiple sclerosis","volume":"128","author":"Mori","year":"2017","journal-title":"Clin. Neurophysiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"8430123","DOI":"10.1155\/2018\/8430123","article-title":"Tumor Necrosis Factor and Interleukin-1\u03b2 Modulate Synaptic Plasticity during Neuroinflammation","volume":"2018","author":"Rizzo","year":"2018","journal-title":"Neural Plast."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"887","DOI":"10.1038\/s41593-019-0385-4","article-title":"Bassoon proteinopathy drives neurodegeneration in multiple sclerosis","volume":"22","author":"Schattling","year":"2019","journal-title":"Nat. Neurosci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1007","DOI":"10.1002\/ana.24398","article-title":"Complement C1q-C3-associated synaptic changes in multiple sclerosis hippocampus","volume":"77","author":"Michailidou","year":"2015","journal-title":"Ann. Neurol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1038\/s41583-018-0053-9","article-title":"Multiple sclerosis and cognition: Synaptic failure and network dysfunction","volume":"19","author":"Portaccio","year":"2018","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"711","DOI":"10.1038\/nrneurol.2015.222","article-title":"Synaptopathy connects inflammation and neuro-degeneration in multiple sclerosis","volume":"11","author":"Mandolesi","year":"2015","journal-title":"Nat. Rev. Neurol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1038\/nrn3900","article-title":"Exploring the origins of grey matter damage in multiple sclerosis","volume":"16","author":"Calabrese","year":"2015","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/S1474-4422(13)70259-X","article-title":"Optic neuritis","volume":"13","author":"Toosy","year":"2014","journal-title":"Lancet Neurol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1079","DOI":"10.1111\/j.1476-5381.2011.01302.x","article-title":"Experimental autoimmune encephalomyelitis (EAE) as a model system for multiple sclerosis (MS)","volume":"164","author":"Constantinescu","year":"2011","journal-title":"Br. J. Pharmacol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1016\/B978-0-444-52001-2.00008-X","article-title":"The experimental autoimmune encephalomyelitis (EAE) model of MS: Utility for understanding disease pathophysiology and treatment","volume":"122","author":"Robinson","year":"2014","journal-title":"Handb. Clin. Neurol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/j.jaut.2014.06.004","article-title":"From classic to spontaneous and humanized models of multiple sclerosis: Impact on understanding pathogenesis and drug development","volume":"54","author":"Kaushansky","year":"2014","journal-title":"J. Autoimmun."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Dembla, M., Kesharwani, A., Natarajan, S., Fecher-Trost, C., Fairless, R., Williams, S.K., Flockerzi, V., Diem, R., Schwarz, K., and Schmitz, F. (2018). Early auto-immune targeting of photoreceptor ribbon synapses in mouse models of multiple sclerosis. EMBO Mol. Med., 10.","DOI":"10.15252\/emmm.201808926"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"101830","DOI":"10.1016\/j.isci.2020.101830","article-title":"Disturbed Presynaptic Ca2+ Signaling in Photoreceptors in the EAE Mouse Model of Multiple Sclerosis","volume":"23","author":"Mukherjee","year":"2020","journal-title":"iScience"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"812","DOI":"10.1038\/nrn2924","article-title":"The diverse roles of ribbon synapses in sensory neurotransmission","volume":"11","author":"Matthews","year":"2010","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1146\/annurev-vision-082114-035709","article-title":"Ribbon synapses and visual processing in the retina","volume":"1","author":"Lagnado","year":"2015","journal-title":"Annu. Rev. Vis. Sci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1152\/physrev.00026.2018","article-title":"Sensory processing at ribbon synapses in the retina and the cochlea","volume":"100","author":"Moser","year":"2010","journal-title":"Physiol. Rev."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1016\/S0896-6273(00)00159-8","article-title":"RIBEYE, a component of synaptic ribbons: A protein\u2019s journey through evolution provides insight into synaptic ribbon function","volume":"28","author":"Schmitz","year":"2000","journal-title":"Neuron"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1098","DOI":"10.15252\/embj.201592701","article-title":"How to make a synaptic ribbon: RIBEYE deletion abolishes ribbons in retinal synapses and disrupts neurotransmitter release","volume":"35","author":"Maxeiner","year":"2016","journal-title":"EMBO J."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"611","DOI":"10.1177\/1073858409340253","article-title":"The making of synaptic ribbons: How they are built and what they do","volume":"15","author":"Schmitz","year":"2009","journal-title":"Neuroscientist"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"682","DOI":"10.1016\/j.preteyeres.2005.04.002","article-title":"Synaptic transmission at retinal ribbon synapses","volume":"24","author":"Heidelberger","year":"2005","journal-title":"Prog. Ret. Eye Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2330","DOI":"10.1523\/JNEUROSCI.21-07-02330.2001","article-title":"Synapse formation is arrested in retinal photoreceptors of the zebrafish nrc mutant","volume":"21","author":"Allwardt","year":"2001","journal-title":"J. Neurosci."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"8641","DOI":"10.1523\/JNEUROSCI.2892-04.2004","article-title":"The zebrafish nrc mutant reveals a role for the polyphosphoinositide phosphatase synaptojanin in cone photoreceptor ribbon anchoring","volume":"24","author":"Hayashi","year":"2004","journal-title":"J. Neurosci."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Trapani, J.G., Obholzer, N., Mo, W., Brockerhoff, S.E., and Nicolson, T. (2009). Synaptojanin is required for temporal fidelity of synaptic transmission in hair cells. PLoS Genet., 5.","DOI":"10.1371\/journal.pgen.1000480"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"2686","DOI":"10.15252\/embj.201591885","article-title":"Disruption of adapter protein 2mu (AP-2mu) in cochlear hair cells impairs vesicle reloading of synaptic release sites and hearing","volume":"34","author":"Jung","year":"2015","journal-title":"EMBO J."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"2473","DOI":"10.1523\/JNEUROSCI.2275-15.2016","article-title":"The disease protein Tulp1 is essential for periactive zone endocytosis in photoreceptor ribbon synapses","volume":"36","author":"Wahl","year":"2016","journal-title":"J. Neurosci."},{"key":"ref_38","first-page":"3394","article-title":"Viral transfer of mini-otoferlins partially restores the fast component of exocytosis and uncovers ultrafast endocytosis in auditory hair cells of otoferlin knock-out mice","volume":"39","author":"Tertrais","year":"2019","journal-title":"J. Neurosci."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Kroll, J., Jaime Tob\u00f3n, L.M., Vogl, C., Neef, J., Kondratiuk, I., K\u00f6nig, M., Strenzke, N., Wichmann, C., Milosevic, I., and Moser, T. (2019). Endophilin-A regulates presynaptic Ca2+ influx and synaptic vesicle recycling in auditory hair cells. EMBO J., 38.","DOI":"10.15252\/embj.2018100116"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"236737","DOI":"10.1242\/jcs.236737","article-title":"AP180 promotes release site clearance and clathrin-dependent vesicle reformation in mouse cochlear inner hair cells","volume":"133","author":"Kroll","year":"2020","journal-title":"J. Cell Sci."},{"key":"ref_41","first-page":"7354","article-title":"Loss of cochlear ribbon synapses in the early stage of aging causes initial hearing impairment","volume":"12","author":"Xiong","year":"2020","journal-title":"Am. J. Transl. Res."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"3633","DOI":"10.1002\/1873-3468.13258","article-title":"Balancing presynaptic release and endocytic membrane retrieval at hair cell ribbon synapses","volume":"592","author":"Pangrsic","year":"2018","journal-title":"FEBS Lett."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1146\/annurev.biochem.78.081307.110540","article-title":"Mechanisms of endocytosis","volume":"78","author":"Doherty","year":"2009","journal-title":"Annu. Rev. Biochem."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1038\/nrm3151","article-title":"Molecular mechanism and physiological functions of clathrin-mediated endocytosis","volume":"12","author":"McMahon","year":"2011","journal-title":"Nat. Rev. Cell Biol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1038\/nrm3266","article-title":"Dynamin, a membrane remodelling GTPase","volume":"13","author":"Ferguson","year":"2012","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"882","DOI":"10.1016\/j.cell.2014.02.017","article-title":"BAR domain scaffolds in dynamin-mediated membrane fission","volume":"156","author":"Daumke","year":"2014","journal-title":"Cell"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"2270","DOI":"10.15252\/embj.201694613","article-title":"Membrane fission by dynamin: What we know and what we need to know","volume":"35","author":"Antonny","year":"2016","journal-title":"EMBO J."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1016\/j.tcb.2018.11.003","article-title":"Structural insights into the mechanisms of dynamin superfamily proteins","volume":"29","author":"Jimah","year":"2019","journal-title":"Trends Cell Biol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1146\/annurev-cellbio-100617-062710","article-title":"Spoiled for choice: Diverse endocytic pathways function at the cell surface","volume":"35","author":"Thottacherry","year":"2019","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"484","DOI":"10.1016\/j.neuron.2014.12.016","article-title":"Molecular mechanisms of presynaptic membrane retrieval and synaptic vesicle reformation","volume":"45","author":"Kononenko","year":"2015","journal-title":"Neuron"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"171","DOI":"10.3389\/fncel.2018.00171","article-title":"Synaptic vesicle endocytosis in different model systems","volume":"12","author":"Gan","year":"2018","journal-title":"Front. Cell. Neurosci."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"60","DOI":"10.3389\/fncel.2014.00060","article-title":"Evidence for a Clathrin-independent mode of endocytosis at a continuously active sensory synapse","volume":"8","author":"Fuchs","year":"2014","journal-title":"Front. Cell. Neurosci."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"30195","DOI":"10.1074\/jbc.M111.273110","article-title":"Calcineurin selectively docks with the dynamin1xb slice variant to regulate activity-dependent bulk endocytosis","volume":"286","author":"Xue","year":"2011","journal-title":"J. Biol. Chem."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1085","DOI":"10.1016\/j.neuron.2011.04.025","article-title":"Isoform-specific dephosphorylation of dynamin1 by calcineurin couples neurotrophin receptor endocytosis to axonal growth","volume":"70","author":"Bodmer","year":"2011","journal-title":"Neuron"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"230","DOI":"10.3389\/fnmol.2017.00230","article-title":"The calcineurin-binding, activity-dependent splice variant dynamin1xb is highly enriched in synapses in various regions of the central nervous system","volume":"10","author":"Eich","year":"2017","journal-title":"Front. Mol. Neurosci."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"348","DOI":"10.1016\/0166-2236(94)90179-1","article-title":"Phosphorylation of dynamin1 and synaptic vesicel recycling","volume":"17","author":"Robinson","year":"1994","journal-title":"Trends Neurosci."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"659","DOI":"10.1016\/S0166-2236(00)01930-5","article-title":"The dephosphins: Dephosphorylation by calcineurin triggers synaptic vesicle endocytosis","volume":"24","author":"Cousin","year":"2001","journal-title":"Trends Neurosci."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"570","DOI":"10.1126\/science.1140621","article-title":"A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis","volume":"316","author":"Ferguson","year":"2007","journal-title":"Science"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1100","DOI":"10.1016\/j.neuron.2011.04.031","article-title":"Overlapping Role of Dynamin Isoforms in Synaptic Vesicle Endocytosis","volume":"70","author":"Raimondi","year":"2011","journal-title":"Neuron"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1016\/j.mcn.2015.03.016","article-title":"Differential targeting of dynamin-1 and dynamin-3 to nerve terminals during chronic suppression of neuronal activity","volume":"68","author":"Calabrese","year":"2015","journal-title":"Mol. Cell. Neurosci."},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Zampighi, G.A., Schietroma, C., Zampighi, L.M., Woodruff, M., Wright, E.M., and Brecha, N.C. (2011). Conical tomography of a ribbon synapse: Structural evidence for vesicle fusion. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0016944"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"7578","DOI":"10.1073\/pnas.91.16.7578","article-title":"Clustering of Ca2+ channels and Ca2+ activated K+ channels at fluorescently labeled presynaptic active zones of hair cells","volume":"91","author":"Issa","year":"1994","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"514","DOI":"10.4161\/chan.26376","article-title":"Dysregulation of Ca(v)1.4 channels disrupts the maturation of photoreceptor synaptic ribbons in congenital stationary night blindness type 2","volume":"7","author":"Liu","year":"2013","journal-title":"Channels"},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Zabouri, N., and Haverkamp, S. (2013). Calcium channel-dependent molecular maturation of photoreceptor synapses. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0063853"},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Regus-Leidig, H., Atorf, J., Feigenspan, A., Kremers, J., Maw, M.A., and Brandst\u00e4tter, J.H. (2014). Photoreceptor degeneration in two mouse models for congenital stationary night blindness type 2. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0086769"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"17273","DOI":"10.1523\/JNEUROSCI.3005-12.2012","article-title":"Presynaptic Cav1.3 channels regulate synaptic ribbon size and are required for synaptic maintenance in sensory hair cells","volume":"32","author":"Sheets","year":"2012","journal-title":"J. Neurosci."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"6299","DOI":"10.1523\/JNEUROSCI.2878-16.2017","article-title":"Enlargement of ribbons in zebrafish hair cells increases calcium currents but disrupts afferent spontaneous activity and timing of stimulus onset","volume":"37","author":"Sheets","year":"2017","journal-title":"J. Neurosci."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"5957","DOI":"10.1038\/s41598-020-62734-0","article-title":"Synaptic ribbons foster active zone stability and illumination-dependent active zone enrichment of RIM2 and Cav1.4 in photoreceptor synapses","volume":"10","author":"Dembla","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"143","DOI":"10.2174\/1874467208666150507104937","article-title":"Voltage-gated Cav1 channels in disorders of vision and hearing","volume":"8","author":"Joiner","year":"2015","journal-title":"Curr. Mol. Pharmacol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"2063","DOI":"10.1152\/physrev.00030.2017","article-title":"Calcium channels: Key players in sensory coding in the retina and the inner ear","volume":"98","author":"Pangrsic","year":"2018","journal-title":"Physiol. Rev."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"724","DOI":"10.1016\/j.neuron.2010.10.027","article-title":"Bassoon and the synaptic ribbon organize Ca2+ channels and vesicles to add release sites and promote refilling","volume":"68","author":"Frank","year":"2010","journal-title":"Neuron"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"604","DOI":"10.1016\/j.neuron.2010.11.015","article-title":"The cytomatrix protein bassoon contributes to fast neurotransmission at conventional and ribbon synapses","volume":"68","author":"Joselevitch","year":"2010","journal-title":"Neuron"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"14273","DOI":"10.1038\/s41598-019-50710-2","article-title":"Otoferlin depletion results in abnormal synaptic ribbons and altered intracellular calcium levels in zebrafish","volume":"9","author":"Manchanda","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"7954","DOI":"10.1523\/JNEUROSCI.1964-08.2008","article-title":"Multiple RIBEYE-RIBEYE interactions create a dynamic scaffold for the formation of synaptic ribbons","volume":"28","author":"Magupalli","year":"2008","journal-title":"J. Neurosci."},{"key":"ref_75","doi-asserted-by":"crossref","unstructured":"Wong, H.C., Zhang, Q., Beirl, A.J., Petralia, R.S., Wang, Y.-X., and Kindt, K. (2019). Synaptic mitochondria regulate hair-cell synapse size and function. eLife, 8.","DOI":"10.7554\/eLife.48914"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41514-019-0040-z","article-title":"Short-term NAD+ supplementation prevents hearing loss in mouse models of Cockayne syndrome","volume":"6","author":"Okur","year":"2020","journal-title":"NPJ Aging Mech. Dis."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1042\/bj1280161","article-title":"Stimulation by calcium ions of pyruvate dehydrogenase phosphate phosphatase","volume":"128","author":"Denton","year":"1972","journal-title":"Biochem. J."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"899","DOI":"10.1042\/bj1760899","article-title":"Calcium ions and the regulation of NAD+-linked isocitrate dehydrogenase from the mitochondria of rat heart and other tissues","volume":"176","author":"Denton","year":"1978","journal-title":"Biochem. J."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1042\/bj1800533","article-title":"The effect of calcium ions and adenine nucleotides on the activity of pig heart 2-oxoglutarate dehydrogenase complex","volume":"180","author":"McCormack","year":"1979","journal-title":"Biochem. J."},{"key":"ref_80","first-page":"E543","article-title":"Ca2+ transport by mammalian mitochondria and its role in hormone secretion","volume":"249","author":"Denton","year":"1985","journal-title":"Am. J. Physiol."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"C313","DOI":"10.1152\/ajpcell.1994.267.2.C313","article-title":"Mitochondrial calcium transport: Physiological and pathological relevance","volume":"267","author":"Gunter","year":"1994","journal-title":"Am. J. Physiol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1259","DOI":"10.1006\/jmcc.2002.2082","article-title":"Cardiac energy metabolism homeostasis: Role of cytosolic calcium","volume":"34","author":"Balaban","year":"2002","journal-title":"J. Mol. Cell. Cardiol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"2959","DOI":"10.1021\/bi2018909","article-title":"Role of mitochondrial Ca2+ in the regulation of cellular kinetics","volume":"51","author":"Glancy","year":"2012","journal-title":"Biochemistry"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"2890","DOI":"10.1128\/MCB.00068-14","article-title":"Mitochondrial matrix accumulation regulates cytosolic NAD+\/NADH metabolism, protein acetylation, and sirtuin expression","volume":"34","author":"Marcu","year":"2014","journal-title":"Mol. Cell Biol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"1336","DOI":"10.1161\/CIRCRESAHA.116.304881","article-title":"The mitochondrial permeability transition pore regulates endothelial bioenergetics and angiogenesis","volume":"116","author":"Marcu","year":"2015","journal-title":"Circ. Res."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/j.molmed.2013.11.007","article-title":"Mitochondrial dysfunction contributes to neurodegeneration in multiple sclerosis","volume":"20","author":"Witte","year":"2014","journal-title":"Trends Mol. Med."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"1806","DOI":"10.1177\/1352458514544537","article-title":"The central role of mitochondria in axonal degeneration in multiple sclerosis","volume":"20","author":"Campbell","year":"2014","journal-title":"Mult. Scler."},{"key":"ref_88","doi-asserted-by":"crossref","unstructured":"Peixoto de Barcelos, I., Troxell, R.M., and Graves, J.R. (2019). Mitochondrial dysfunction and multiple sclerosis. Biology, 8.","DOI":"10.3390\/biology8020037"},{"key":"ref_89","doi-asserted-by":"crossref","unstructured":"Jensen, J.B., Lysaght, A.C., Liberman, M.C., Qvortrup, K., and Stankovic, K.M. (2015). Immediate and delayed cochlear neuropathy after noise exposure in pubescent mice. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0125160"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"635201","DOI":"10.3389\/fcell.2020.635201","article-title":"Differences in calcium clearance at inner hair cell active zones may underlie the difference in susceptibility to noise-induced cochlea synaptopathy of C57BL\/6J and CBA\/CaJ mice","volume":"8","author":"Liu","year":"2021","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"1062","DOI":"10.1097\/AUD.0000000000001009","article-title":"Decreased reemerging auditory brainstem responses under ipsilateral broadband masking as a marker of noise-induced cochlear synaptopathy","volume":"42","author":"Giraudet","year":"2021","journal-title":"Ear Hear."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1523\/JNEUROSCI.3389-10.2011","article-title":"Opposing gradients of ribbon size and AMPA receptor expression underlie sensitivity differences among cochlear-nerve\/hair-cell synapses","volume":"31","author":"Liberman","year":"2011","journal-title":"J. Neurosci."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"3260","DOI":"10.1002\/cne.23345","article-title":"Quantitative analysis of ribbons, vesicles, and cisterns at the cat inner hair cell synapse: Correlation with spontaneous rate","volume":"521","author":"Kantardzhieva","year":"2013","journal-title":"J. Comp. Neurol."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"107531","DOI":"10.15252\/embj.2020107531","article-title":"Divide and conquer acoustic diversity","volume":"40","author":"Goutman","year":"2021","journal-title":"EMBO J."},{"key":"ref_95","first-page":"2165","article-title":"Ultrastructural changes of photoreceptor synaptic ribbons in relation to time of day and illumination","volume":"40","author":"Adly","year":"1999","journal-title":"Investig. Ophthalmol. Vis. Sci."},{"key":"ref_96","first-page":"499","article-title":"Synaptic ribbon dynamics in photoreceptors of mice","volume":"106","author":"Vollrath","year":"2001","journal-title":"Ital. J. Anat. Embryol."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"1559","DOI":"10.1111\/j.1460-9568.2004.03198.x","article-title":"Mouse photoreceptor synaptic ribbons lose and regain material in response to illumination changes","volume":"19","author":"Glas","year":"2004","journal-title":"Eur. J. Neurosci."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"28","DOI":"10.3389\/fnmol.2012.00026","article-title":"EF hand\u2014Mediated Ca2+- and cGMP-signaling in photoreceptor terminals","volume":"5","author":"Schmitz","year":"2012","journal-title":"Front. Mol. Neurosci."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"1411","DOI":"10.1016\/S0960-9822(00)80087-1","article-title":"The endocytic machinery in nerve terminals surrounds sites of exocytosis","volume":"9","author":"Roos","year":"1999","journal-title":"Curr. Biol."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"18446","DOI":"10.1074\/jbc.274.26.18446","article-title":"EHSH1\/intersectin, a protein that contains EH and SH3 domains and binds to dynamin and SNAP25","volume":"274","author":"Okamoto","year":"1999","journal-title":"J. Biol. Chem."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/j.neuron.2004.07.001","article-title":"Dap160\/Intersectin scaffolds the active zone to achieve high-fidelity endocytosis and normal synaptic growth","volume":"43","author":"Marie","year":"2004","journal-title":"Neuron"},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"8266","DOI":"10.1073\/pnas.1219234110","article-title":"Fast neurotransmitter release regulated by the endocytic scaffold intersectin","volume":"110","author":"Sakaba","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"12","DOI":"10.3389\/fnsyn.2016.00012","article-title":"The active and periactive zone organization and the functional properties of small and large synapses","volume":"8","author":"Cano","year":"2016","journal-title":"Front. Synaptic Neurosci."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.neures.2017.09.013","article-title":"Coupling of exocytosis and endocytosis at the presynaptic active zone","volume":"127","author":"Maritzen","year":"2018","journal-title":"Neurosci. Res."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"10278","DOI":"10.1523\/JNEUROSCI.5048-12.2013","article-title":"A local, periactive zone endocytic machinery of photoreceptor synapses in close vicinity to synaptic ribbons","volume":"33","author":"Wahl","year":"2013","journal-title":"J. Neurosci."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1016\/S0896-6273(04)00254-5","article-title":"A highly Ca2+ sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse","volume":"42","author":"Thoreson","year":"2004","journal-title":"Neuron"},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"1469","DOI":"10.1007\/s00424-021-02548-9","article-title":"Transmission at rod and cone ribbon synapses in the retina","volume":"473","author":"Thoreson","year":"2021","journal-title":"Pflug. Arch."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"1003","DOI":"10.1038\/nn.2355","article-title":"Ca2+ and calmodulin initiate all forms of endocytosis during depolarization of a nerve terminal","volume":"12","author":"Wu","year":"2009","journal-title":"Nat. Neurosci."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"838","DOI":"10.1038\/nn.2576","article-title":"Developmental shift to a mechanism to a mechanism of synaptic vesicle endocytosis requiring nanodomain Ca2+","volume":"13","author":"Yamashita","year":"2010","journal-title":"Nat. Neurosci."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"464","DOI":"10.1177\/1073858415588265","article-title":"Ca2+ dependence of synaptic vesicle endocytosis","volume":"22","author":"Leitz","year":"2016","journal-title":"Neuroscientist"},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"740","DOI":"10.1016\/S0960-9822(98)70297-0","article-title":"Calcium triggers calcineurin-dependent synaptic vesicle recycling in mammalian nerve terminals","volume":"8","author":"Marks","year":"1998","journal-title":"Curr. Biol."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1042\/bss0720087","article-title":"Dynamin1 phosphorylation and the control of synaptic vesicle endocytosis","volume":"72","author":"Smillie","year":"2005","journal-title":"Biochem. Soc. Symp."},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"752","DOI":"10.1038\/nn1695","article-title":"Syndapin 1 is the phosphorylation-regulated dynamin1 partner in synaptic vesicle endocytosis","volume":"9","author":"Anggono","year":"2006","journal-title":"Nat. Neurosci."},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"687","DOI":"10.1113\/jphysiol.2007.137539","article-title":"Activity-dependent control of bulk endocytosis by protein dephosphorylation in central nerve terminals","volume":"585","author":"Clayton","year":"2007","journal-title":"J. Physiol."},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"7706","DOI":"10.1523\/JNEUROSCI.1976-09.2009","article-title":"The phospho-dependent dynamin\u2014Syndapin interaction triggers activity-dependent bulk endocytosis of synaptic vesicles","volume":"29","author":"Clayton","year":"2009","journal-title":"J. Neurosci."},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"901","DOI":"10.1111\/j.1471-4159.2009.06384.x","article-title":"The molecular physiology of activity-dependent bulk endocytosis of synaptic vesicles","volume":"111","author":"Clayton","year":"2009","journal-title":"J. Neurochem."},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1021\/acscentsci.8b00230","article-title":"A friend or foe: Calcineurin across the gamut of neurological disorders","volume":"4","author":"Saraf","year":"2018","journal-title":"ACS Cent. Sci."},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"570","DOI":"10.1111\/jnc.14862","article-title":"Synaptic vesicle generation from activity\u2014Dependent bulk endosomes requires a dephosphorylation\u2014Dependent dynamin\u2014Syndapin interaction","volume":"151","author":"Cheung","year":"2019","journal-title":"J. Neurochem."},{"key":"ref_119","doi-asserted-by":"crossref","unstructured":"Engholm-Keller, K., Waardenberg, A.J., M\u00fcller, J.A., Wark, J.R., Fernando, R.N., Arthur, J.W., Robinson, P.J., Dietrich, D., Schoch, S., and Graham, M.E. (2019). The temporal profile of activity-dependent phosphor-signalling reveals long-lasting patterns of poststimulus regulation. PLoS Biol., 2.","DOI":"10.1371\/journal.pbio.3000170"},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"100061","DOI":"10.1016\/j.mcpro.2021.100061","article-title":"Protein phosphorylation in depolarized synaptosomes: Dissecting primary effects of calcium from synaptic vesicle cycling","volume":"20","author":"Silbern","year":"2021","journal-title":"Mol. Cell. Proteom."},{"key":"ref_121","doi-asserted-by":"crossref","first-page":"679","DOI":"10.1074\/mcp.M113.033340","article-title":"Discovery of novel disease-specific and membrane-associated candidate markers in a mouse model of multiple sclerosis","volume":"13","author":"Dagley","year":"2014","journal-title":"Mol. Cell. Proteom."},{"key":"ref_122","doi-asserted-by":"crossref","unstructured":"Sen, M.K., Almuslehi, M.S.M., Shortland, P.J., Mahns, D.A., and Coorssen, J.R. (2021). Proteomics of multiple sclerosis: Inherent issues in defining the pathoetiology and identifying (early) biomarkers. Int. Mol. Sci., 22.","DOI":"10.3390\/ijms22147377"},{"key":"ref_123","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1007\/s00441-013-1758-8","article-title":"Dysfunctions of neuronal calcium signalling in neuroinflammation and neurodegeneration","volume":"357","author":"Fairless","year":"2014","journal-title":"Cell Tiss. Res."},{"key":"ref_124","doi-asserted-by":"crossref","first-page":"E127","DOI":"10.1055\/s-0043-109031","article-title":"Calcium homeostasis in multiple sclerosis","volume":"1","author":"Hundehege","year":"2017","journal-title":"Neurol. Int. Open"},{"key":"ref_125","doi-asserted-by":"crossref","first-page":"5245","DOI":"10.1523\/JNEUROSCI.3837-13.2014","article-title":"ArfGAP3 is a component of the photoreceptor synaptic ribbon complex and forms a NAD(H)-regulated, redox-sensitive complex with RIBEYE that is important for endocytosis","volume":"34","author":"Dembla","year":"2014","journal-title":"J. Neurosci."},{"key":"ref_126","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1038\/365163a0","article-title":"Dynamin GTPase regulated by protein kinase C phosphorylation in nerve terminals","volume":"365","author":"Robinson","year":"1993","journal-title":"Nature"},{"key":"ref_127","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1038\/nmeth.2089","article-title":"NIH Image to ImageJ: 25 years of image analysis","volume":"9","author":"Schneider","year":"2012","journal-title":"Nat. Methods"},{"key":"ref_128","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1038\/nmeth.2019","article-title":"Fiji: An open source platform for biological-image analysis","volume":"9","author":"Schindelin","year":"2012","journal-title":"Nat. Methods"},{"key":"ref_129","doi-asserted-by":"crossref","first-page":"3993","DOI":"10.1529\/biophysj.103.038422","article-title":"Automatic and quantitative measurement of protein-protein colocalization in live cells","volume":"86","author":"Costes","year":"2004","journal-title":"Biophys. J."},{"key":"ref_130","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1111\/j.1365-2818.2006.01706.x","article-title":"A guided tour into subcellular colocalization analysis in light microscopy","volume":"224","author":"Bolte","year":"2006","journal-title":"J. Microsc."},{"key":"ref_131","doi-asserted-by":"crossref","first-page":"C723","DOI":"10.1152\/ajpcell.00462.2010","article-title":"A practical guide to evaluating colocalization in biological microscopy","volume":"300","author":"Dunn","year":"2011","journal-title":"Am. J. Physiol. Cell. Physiol."},{"key":"ref_132","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1083\/jcb.201002018","article-title":"A guide to super-resolution fluorescence microscopy","volume":"190","author":"Schermelleh","year":"2010","journal-title":"J. Cell Biol."},{"key":"ref_133","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1083\/jcb.4.3.233","article-title":"Thin sections: I. a study of section thickness and physical distortion produced during microtomy","volume":"4","author":"Peachey","year":"1958","journal-title":"J. Biophys. Biochem. Cytol."},{"key":"ref_134","first-page":"369","article-title":"Relation between thickness and interference colors of biological ultrathin sections","volume":"29","author":"Sakai","year":"1980","journal-title":"J. Electron. Microsc."},{"key":"ref_135","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1016\/S0896-6273(00)00062-3","article-title":"The murine cone photoreceptor: A single cone type expresses both S and M opsins with retinal spatial patterning","volume":"27","author":"Applebury","year":"2000","journal-title":"Neuron"},{"key":"ref_136","doi-asserted-by":"crossref","first-page":"7670","DOI":"10.1523\/JNEUROSCI.0629-11.2011","article-title":"Spectral and temporal sensitivity of cone-mediated responses in mouse retinal ganglion cells","volume":"31","author":"Wang","year":"2011","journal-title":"J. Neurosci."},{"key":"ref_137","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1242\/jeb.200.1.1","article-title":"Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases","volume":"200","author":"Altendorf","year":"1997","journal-title":"J. Exp. Biol."},{"key":"ref_138","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1038\/83949","article-title":"Calcium accelerates endocytosis of vSNAREs at hippocampal synapses","volume":"4","author":"Sankaranarayanan","year":"2001","journal-title":"Nat. Neurosci."},{"key":"ref_139","doi-asserted-by":"crossref","first-page":"5969","DOI":"10.1113\/jphysiol.2008.159715","article-title":"The role of endocytosis in regulating the strength of hippocampal synapses","volume":"586","author":"Granseth","year":"2008","journal-title":"J. Physiol."},{"key":"ref_140","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1113\/expphysiol.2009.051953","article-title":"Optical reporters of synaptic activity in neural circuits","volume":"96","author":"Dreosti","year":"2011","journal-title":"Exp. Physiol."},{"key":"ref_141","first-page":"10","article-title":"Measurement of vesicle recycling in central neurons","volume":"16","author":"Ryan","year":"2001","journal-title":"News Physiol. Sci."},{"key":"ref_142","doi-asserted-by":"crossref","first-page":"16401","DOI":"10.1073\/pnas.0407390101","article-title":"Synaptotagmin promotes vesicle fusion and recycling","volume":"101","author":"Schwarz","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_143","doi-asserted-by":"crossref","first-page":"1109","DOI":"10.1016\/j.neuron.2013.01.021","article-title":"Developmental refinement of vesicle cycling at Schaffer collateral synapses","volume":"77","author":"Rose","year":"2013","journal-title":"Neuron"},{"key":"ref_144","doi-asserted-by":"crossref","first-page":"849","DOI":"10.4161\/auto.6845","article-title":"Does bafilomycin A1 block the fusion of autophagosomes with lysosomes","volume":"4","author":"Klionsky","year":"2008","journal-title":"Autophagy"},{"key":"ref_145","doi-asserted-by":"crossref","first-page":"2247","DOI":"10.1021\/acschemneuro.7b00152","article-title":"The importance of mitophagy in maintaining mitochondrial function in U373MG cells. Bafilomycin A1 restores aminochrome-induced mitochondrial damage","volume":"8","author":"Huenchuguala","year":"2017","journal-title":"ACS Chem. Neurosci."},{"key":"ref_146","doi-asserted-by":"crossref","first-page":"903","DOI":"10.1007\/s00018-010-0502-8","article-title":"Bafilomycin A1 activates respiration of neuronal cells via uncoupling associated with flickering depolarization of mitochondria","volume":"68","author":"Zhdanov","year":"2011","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_147","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1007\/s004410050799","article-title":"A simple assay for quantification of protein in tissue sections, cell cultures, and cell homogenates, and of protein immobilized on solid surfaces","volume":"288","author":"Schnittler","year":"1997","journal-title":"Cell Tiss. Res."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/19\/10789\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:09:45Z","timestamp":1760166585000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/22\/19\/10789"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,10,6]]},"references-count":147,"journal-issue":{"issue":"19","published-online":{"date-parts":[[2021,10]]}},"alternative-id":["ijms221910789"],"URL":"https:\/\/doi.org\/10.3390\/ijms221910789","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,10,6]]}}}