Ca2+ binding to synapsin I regulates resting Ca2+ and recovery from synaptic depression in nerve terminals

Accogli A, Wiegand G, Scala M, Cerminara C, Iacomino M, Riva A, Carlini B, Camerota L, Belcastro V, Prontera P, Fernández-Jaén A, Bebek N, Scudieri P, Baldassari S, Salpietro V, Novelli G, De Luca C, von Stülpnagel C, Kluger F, Kluger GJ, Wohlrab GC, Ramantani G, Lewis-Smith D, Thomas RH, Lai M, Verrotti A, Striano S, Depienne C, Minetti C, Benfenati F, Brancati F, Zara F, Striano P (2021) Clinical and genetic features in patients with reflex bathing epilepsy. Neurology 97:e577–e586

Article  PubMed  PubMed Central  CAS  Google Scholar 

Alabi AA, Tsien RW (2012) Synaptic vesicle pools and dynamics. Cold Spring Harb Perspect Biol 4:a013680

Article  PubMed  PubMed Central  Google Scholar 

Aponte Y, Bischofberger J, Jonas P (2008) Efficient Ca2+ buffering in fast-spiking basket cells of rat hippocampus. J Physiol 586:2061–2075

Article  PubMed  PubMed Central  CAS  Google Scholar 

Ariel P, Ryan TA (2010) Optical mapping of release properties in synapses. Front Neural Circuits 4:18

PubMed  PubMed Central  Google Scholar 

Baldelli P, Fassio A, Valtorta F, Benfenati F (2007) Lack of synapsin I reduces the readily releasable pool of synaptic vesicles at central inhibitory synapses. J Neurosci 27:13520–13531

Article  PubMed  PubMed Central  CAS  Google Scholar 

Bekkers JM, Stevens CF (1991) Excitatory and inhibitory autaptic currents in isolated hippocampal neurons maintained in cell culture. Proc Natl Acad Sci USA 88:7834–7838

Article  PubMed  PubMed Central  CAS  Google Scholar 

Benfenati F, Valtorta F, Chieregatti E, Greengard P (1992) Interaction of free and synaptic vesicle-bound synapsin I with F-actin. Neuron 8:377–386

Article  PubMed  CAS  Google Scholar 

Benfenati F, Valtorta F, Rossi MC, Onofri F, Sihra T, Greengard P (1993) Interactions of synapsin I with phospholipids: possible role in synaptic vesicle clustering and in the maintenance of bilayer structures. J Cell Biol 123:1845–1855

Article  PubMed  CAS  Google Scholar 

Bragina L, Candiracci C, Barbaresi P, Giovedì S, Benfenati F, Conti F (2007) Heterogeneity of glutamatergic and GABAergic release machinery in cerebral cortex. Neuroscience 146:1829–1840

Article  PubMed  CAS  Google Scholar 

Brautigam CA, Chelliah Y, Deisenhofer J (2004) Tetramerization and ATP binding by a protein comprising the A, B, and C domains of rat synapsin I. J Biol Chem 279:11948–11956

Article  PubMed  CAS  Google Scholar 

Cesca F, Baldelli P, Valtorta F, Benfenati F (2010) The synapsins: key actors of synapse function and plasticity. Prog Neurobiol 91:313–348

Article  PubMed  CAS  Google Scholar 

Chi P, Greengard P, Ryan TA (2001) Synapsin dispersion and reclustering during synaptic activity. Nat Neurosci 4:1187–1193

Article  PubMed  CAS  Google Scholar 

Chi P, Greengard P, Ryan TA (2003) Synaptic vesicle mobilization is regulated by distinct synapsin I phosphorylation pathways at different frequencies. Neuron 38:68–78

Article  Google Scholar 

Chiappalone M, Casagrande S, Tedesco M, Valtorta F, Baldelli P, Martinoia S, Benfenati F (2009) Opposite changes in glutamatergic and GABAergic transmission underlie the diffuse hyperexcitability of synapsin I-deficient cortical networks. Cereb Cortex 19:1422–1439

Article  PubMed  Google Scholar 

Coombs ID, Soto D, McGee TP, Gold MG, Farrant M, Cull-Candy SG (2019) Homomeric GluA2(R) AMPA receptors can conduct when desensitized. Nat Commun 10:4312

Article  PubMed  PubMed Central  Google Scholar 

Corradi A, Zanardi A, Giacomini C, Onofri F, Valtorta F, Zoli M, Benfenati F (2008) Synapsin I and synapsin II null mice display an increased age-dependent cognitive impairment. J Cell Sci 121:3042–3051

Article  PubMed  CAS  Google Scholar 

Corradi A, Fadda M, Piton A, Patry L, Marte A, Rossi P, Cadieux-Dion M, Gauthier J, Lapointe L, Mottron L, Valtorta F, Rouleau GA, Fassio A, Benfenati F, Cossette P (2014) SYN2 is an autism predisposing gene: loss-of-function mutations alter synaptic vesicle cycling and axon outgrowth. Hum Mol Genet 23:90–103

Article  PubMed  CAS  Google Scholar 

Crawford DC, Kavalali ET (2015) Molecular underpinnings of synaptic vesicle pool heterogeneity. Traffic 16:338–364

Article  PubMed  PubMed Central  CAS  Google Scholar 

Darden T, York D, Pedersen L (1993) Particle mesh Ewald: a Nlog(N) method for Ewald sums in large systems. J Chem Phys 98:10089–10092

Article  CAS  Google Scholar 

De Camilli P, Benfenati F, Valtorta F, Greengard P (1990) The synapsins. Annu Rev Cell Biol 6:433–460

Article  PubMed  Google Scholar 

De Palma M, Naldini L (2002) Transduction of a gene expression cassette using advanced generation lentiviral vectors. Methods Enzymol 346:514–529

Article  PubMed  Google Scholar 

Eggermann E, Jonas P (2012) How the ‘slow’ Ca2+ buffer parvalbumin affects transmitter release in nanodomain-coupling regimes. Nat Neurosci 15:20–22

Article  CAS  Google Scholar 

Esser L, Wang CR, Hosaka M, Smagula CS, Südhof TC, Deisenhofer J (1998) Synapsin I is structurally similar to ATP-utilizing enzymes. EMBO J 17:977–984

Article  PubMed  PubMed Central  CAS  Google Scholar 

Evergren E, Benfenati F, Shupliakov O (2007) The synapsin cycle: a view from the synaptic endocytic zone. J Neurosci Res 85:2648–2656

Article  PubMed  CAS  Google Scholar 

Farisello P, Boido D, Nieus T, Medrihan L, Cesca F, Valtorta F, Baldelli P, Benfenati F (2013) Synaptic and extrasynaptic origin of the excitation/inhibition imbalance in the hippocampus of 785 synapsin I/II/III knockout mice. Cereb Cortex 23:581–593

Article  PubMed  Google Scholar 

Fassio A, Raimondi A, Lignani G, Benfenati F, Baldelli P (2011) Synapsins: from synapse to network hyperexcitability and epilepsy. Semin Cell Dev Biol 22:408–415

Article  PubMed  CAS  Google Scholar 

Fassio A, Patry L, Congia S, Onofri F, Piton A, Gauthier J, Pozzi D, Messa M, Defranchi E, Fadda M, Corradi A, Baldelli P, Lapointe L, St-Onge J, Meloche C, Mottron L, Valtorta F, Khoa Nguyen D, Rouleau GA, Benfenati F, Cossette P (2011) SYN1 loss-of-function mutations in autism and partial epilepsy cause impaired synaptic function. Hum Mol Genet 20:2297–2307

Article  PubMed  CAS  Google Scholar 

Fornasiero EF, Bonanomi D, Benfenati F, Valtorta F (2010) The role of synapsins in neuronal development. Cell Mol Life Sci 67:1383–1396

Article  PubMed  CAS  Google Scholar 

Forte N, Binda F, Contestabile A, Benfenati F, Baldelli P (2020) Synapsin I synchronizes GABA release in distinct interneuron subpopulations. Cereb Cortex 30:1393–1406

Article  PubMed  CAS  Google Scholar 

Frenkel D, Smit B (2001) Understanding molecular simulation: from algorithms to applications, 2nd edn. Academic Press, San Diego

Google Scholar 

Garcia CC, Blair HJ, Seager M, Coulthard A, Tennant S, Buddles M, Curtis A, Goodship JA (2004) Identification of a mutation in synapsin I, a synaptic vesicle protein, in a family with epilepsy. J Med Genet 41:183–186

Article  PubMed  PubMed Central  CAS  Google Scholar 

Gerth F, Jäpel M, Pechstein A, Kochlamazashvili G, Lehmann M, Puchkov D, Onofri F, Benfenati F, Nikonenko AG, Fredrich K, Shupliakov O, Maritzen T, Freund C, Haucke V (2017) Intersectin associates with synapsin and regulates its nanoscale localization and function. Proc Natl Acad Sci USA 114:12057–12062

Article  PubMed  PubMed Central  CAS  Google Scholar 

Giannandrea M, Guarnieri FC, Gehring NH, Monzani E, Benfenati F, Kulozik AE, Valtorta F (2013) Nonsense-mediated mRNA decay and loss-of-function of the protein underlie the X-linked epilepsy associated with the W356X mutation in synapsin I. PLoS ONE 8:e67724

Article  PubMed  PubMed Central  CAS  Google Scholar 

Gitler D, Takagishi Y, Feng J, Ren Y, Rodriguez RM, Wetsel WC, Greengard P, Augustine GJ (2004) Different presynaptic roles of synapsin at excitatory and inhibitory synapses. J Neurosci 24:11368–11380

Article  PubMed  PubMed Central  CAS  Google Scholar 

Greco B, Managò F, Tucci V, Kao HT, Valtorta F, Benfenati F (2013) Autism-related behavioral abnormalities in synapsin knockout mice. Behav Brain Res 251:65–74

Article  PubMed  PubMed Central  CAS  Google Scholar 

Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260:3440–3450

Article  PubMed 

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