Reduced SNAP-25 alters short-term plasticity at developing glutamatergic synapses

EMBO Reports

Volumn 14, Issue 7, 2013, Pages 645-651

  Antonucci, Flavia ^a,b   Corradini, Irene ^a,c   Morini, Raffaella ^a,d   Fossati, Giuliana ^a,d   Menna, Elisabetta ^b,d   Pozzi, Davide ^e   Pacioni, Simone ^f   Verderio, Claudia ^b   Bacci, Alberto ^f,g   Matteoli, Michela ^a,d  

^a UNIVERSITY OF MILAN   (Italy)

^b CNR   (Italy)

^c Fondazione Filarete   (Italy)

^d HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^e IRCCS   (Italy)

^f EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^g CNRS   (France)

Author keywords

glutamatergic transmission; short term plasticity; SNAP 25

Indexed keywords

PROTEIN; PROTEIN SNAP 25; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL CELL; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; DEPRESSION; FACILITATION; GLUTAMATERGIC SYNAPSE; HUMAN; INTELLECTUAL IMPAIRMENT; MOUSE; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; PHENOTYPE; PLASTICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SYNAPSE; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; WILD TYPE;

ACTION POTENTIALS; ANIMALS; CALCIUM; CALCIUM CHANNELS; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE SILENCING; GLUTAMIC ACID; HIPPOCAMPUS; HUMANS; MICE; NEURONAL PLASTICITY; NEURONS; PRIMARY CELL CULTURE; RATS; RNA, SMALL INTERFERING; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25;

EID: 84879686362     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.1038/embor.2013.75     Document Type: Article

References (37)

1. Jahn RSR (2006) SNAREs-engines for membrane fusion. Nat Rev Mol Cell Biol 7: 631-643
2. Sudhof TC, Rothman JE (2009) Membrane fusion: grappling with SNARE and SM proteins. Science 323: 474-477
3. Washbourne P et al (2002) Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat Neurosci 5: 19-26 (Pubitemid 34038778)
4. Atlas DWO, Trus M (2001) The voltage-gated Ca2 channel is the Ca2 sensor of fast neurotransmitter release. Cell Mol Neurobiol 21: 717-731 (Pubitemid 34538866)
5. Catterall WA, Few AP (2008) Calcium channel regulation and presynaptic plasticity. Neuron 59: 882-901
6. Zamponi GW (2003) The L-type calcium channel C-terminus: sparking interest beyond its role in calcium-dependent inactivation. J Physiol 552: 333 (Pubitemid 37321832)
7. Pozzi DCS, Bozzi Y, Chikhladze M, Grumelli C, Proux-Gillardeaux V, Takahashi M, Franceschetti S, Verderio C, Matteoli M (2008) Activity-dependent phosphorylation of Ser187 is required for SNAP-25-negative modulation of neuronal voltage-gated calcium channels. Proc Natl Acad Sci USA 105: 323-328
8. Condliffe SB, Corradini I, Pozzi D, Verderio C, Matteoli M (2010) Endogenous SNAP-25 regulates native voltage-gated calcium channels in glutamatergic neurons. J Biol Chem 285: 24968-24976
9. Condliffe SBMM (2011) Inactivation kinetics of voltage-gated calcium channels in glutamatergic neurons are influenced by SNAP-25. Channels 5: 304-307
10. Lewis CM et al (2003) Genome scan meta-analysis of schizophrenia and bipolar disorder, part II: schizophrenia. Am J Hum Genet 73: 34-48 (Pubitemid 36793778)
11. Corradini I, Verderio C, Sala M, Wilson MC, Matteoli M (2009) SNAP-25 in neuropsychiatric disorders. Ann N Y Acad Sci 1152: 93-99
12. Young CE, Arima K, Xie J, Hu L, Beach TG, Falkai P, Honer WG (1998) SNAP-25 deficit and hippocampal connectivity in schizophrenia. Cereb Cortex 8: 261-268 (Pubitemid 28226162)
13. Thompson PM, Kelley M, Yao J, Tsai G, van Kammen DP (2003) Elevated cerebrospinal fluid SNAP-25 in schizophrenia. Biol Psychiatry 53: 1132-1137 (Pubitemid 36695088)
14. Thompson PM, Sower AC, Perrone-Bizzozero NI (1998) Altered levels of the synaptosomal associated protein SNAP-25 in schizophrenia. Biol Psychiatry 43: 239-243 (Pubitemid 28085669)
15. Barr CLFY, Wigg K, Bloom S, Roberts W, Malone M, Schachar R, Tannock R, Kennedy JL (2000) Identification of DNA variants in the SNAP-25 gene and linkage study of these polymorphisms and attention-deficit hyperactivity disorder. Mol Psychiatry 5: 405-409 (Pubitemid 30455954)
16. Hess EJ, Rogan PK, Domoto M, Tinker DE, Ladda RL, Ramer JC (1995) Absence of linkage of apparently single gene mediated ADHD with the human syntenic region of the mouse mutant Coloboma. Am J Med Genet 60: 573-579 (Pubitemid 26002131)
17. Faraone SV, Perlis RH, Doyle AE, Smoller JW, Goralnick JJ, Holmgren MA, Sklar P (2005) Molecular genetics of attention-deficit/hyperactivity disorder. Biol Psychiatry 57: 1313-1323 (Pubitemid 40798551)
18. Sharma M, Burre J, Sudhof TC (2011) CSPalpha promotes SNARE-complex assembly by chaperoning SNAP-25 during synaptic activity. Nat Cell Biol 13: 30-39
19. Bronk P, Deak F, Wilson MC, Liu X, Sudhof TC, Kavalali ET (2007) Differential effects of SNAP-25 deletion on Ca2-dependent and Ca2 -independent neurotransmission. J Neurophysiol 98: 794-806 (Pubitemid 47236033)
20. Rosenmund CSC (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16: 1197-1207
21. Tokuoka HGY (2006) Myosin light chain kinase is not a regulator of synaptic vesicle trafficking during repetitive exocytosis in cultured hippocampal neurons. J Neurosci 26: 11606-11614
22. Benagiano VLL, Flace P, Girolamo F, Rizzi A, Bosco L, Cagiano R, Nico B, Ribatti D, Ambrosi G (2011) VAMP-2, SNAP-25A/B and syntaxin-1 in glutamatergic and GABAergic synapses of the rat cerebellar cortex. BMC Neurosci 12: 118
23. Bragina L, Melone M, Fattorini G, Conti F (2007) Clozapine upregulates the expression of the vesicular GABA transporter (VGAT) in rat frontal cortex. Mol Psychiatry 12: 612-613 (Pubitemid 46998254)
24. Mandolesi G, Vanni V, Cesa R, Grasselli G, Puglisi F, Cesare P, Strata P (2009) Distribution of the SNAP25 and SNAP23 synaptosomal-associated protein isoforms in rat cerebellar cortex. Neuroscience 164: 1084-1096
25. Verderio C et al (2004) SNAP-25 modulation of calcium dynamics underlies differences in GABAergic and glutamatergic responsiveness to depolarization. Neuron 41: 599-610 (Pubitemid 38253071)
26. Tafoya LCMM, Miyashita T, Guzowski JF, Valenzuela CF, Wilson MC (2006) Expression and function of SNAP-25 as a universal SNARE component in GABAergic neurons. J Neurosci 26: 7826-7838 (Pubitemid 44315152)
27. Boyken JGM, Riedel D, Urlaub H, Jahn R, Chua JJ (2013) Molecular profiling of synaptic vesicle docking sites reveals novel proteins but few differences between glutamatergic and GABAergic synapses. Neuron 78: 285-297
28. Saviane CSL, Raffaelli G, Voronin LL, Cherubini E (2002) Frequency-dependent shift from paired-pulse facilitation to paired-pulse depression at unitary CA3-CA3 synapses in the rat hippocampus. J Physiol 544: 469-476 (Pubitemid 35244263)
29. Rettig J, Sheng ZH, Kim DK, Hodson CD, Snutch TP, Catterall WA (1996) Isoform-specific interaction of the alpha1A subunits of brain Ca2 + channels with the presynaptic proteins syntaxin and SNAP-25. Proc Natl Acad Sci USA 93: 7363-7368
30. Sippy TC-MA, Jeromin A, Schweizer FE (2003) Acute changes in short-term plasticity at synapses with elevated levels of neuronal calcium sensor-1. Nat Neurosci 6: 1031-1038 (Pubitemid 37186194)
31. Bark CBF, Kaushal A, Mathews JR, Partridge LD, Wilson MC (2004) Developmentally regulated switch in alternatively spliced SNAP-25 isoforms alters facilitation of synaptic transmission. J Neurosci 24: 8796-8805 (Pubitemid 39362974)
32. Corradini IDA et al (2012) Epileptiform Activity and cognitive deficits in SNAP-25 +/- mice are normalized by antiepileptic drugs. Cereb Cortex 12: [Epub ahead of print] doi:10.1093/cercor/bhs316
33. Grumelli C, Corradini I, Matteoli M, Verderio C (2010) Intrinsic calcium dynamics control botulinum toxin A susceptibility in distinct neuronal populations. Cell Calcium 47: 419-424
34. Deng PY, Sojka D, Klyachko VA (2011) Abnormal presynaptic short-term plasticity and information processing in a mouse model of fragile X syndrome. J Neurosci 31: 10971-10982
35. El Idrissi A, Neuwirth LS, L'Amoreaux W (2010) Taurine regulation of short term synaptic plasticity in fragile X mice. J Biomed Sci 17(Suppl 1): S15
36. Rizzi TS et al (2012) Supporting the generalist genes hypothesis for intellectual ability/disability: the case of SNAP25. Genes Brain Behav11: 767-771
37. Bartlett WPBG (1984) An electron microscopic study of the development of axons and dendrites by hippocampal neurons in culture. I. Cells which develop without intercellular contacts. J Neurosci 4: 1944-1953