The role of the t-SNARE SNAP-25 in action potential-dependent calcium signaling and expression in GABAergic and glutamatergic neurons

BMC Neuroscience

Volumn 9, Issue , 2008, Pages

  Tafoya, Lawrence C R ^a   William, C William ^a   Yanagawa, Yuchio ^b   Obata, Kunihiko ^c   Wilson, Michael C ^a  

^a UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

^b GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; GLUTAMIC ACID; SNARE PROTEIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; VOLTAGE GATED CALCIUM CHANNEL; 4 AMINOBUTYRIC ACID; CALCIUM; CALCIUM CHANNEL; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 1; MESSENGER RNA; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BRAIN TISSUE; CALCIUM SIGNALING; CELL CULTURE; CELL FUNCTION; CELL POPULATION; CONTROLLED STUDY; DEPOLARIZATION; EVOKED RESPONSE; GENETIC CODE; GENETIC VARIABILITY; GLIA; HIPPOCAMPUS; HOMOZYGOSITY; MOUSE; MUTANT; NEUROTRANSMISSION; NONHUMAN; PROTEIN EXPRESSION; RNA TRANSCRIPTION; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; WILD TYPE; ANALYSIS OF VARIANCE; ANIMAL; ASTROCYTE; C57BL MOUSE; CYTOLOGY; DRUG EFFECT; FLUORESCENCE; GENETICS; METABOLISM; MOUSE MUTANT; NERVE CELL; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; ASTROCYTES; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; CELLS, CULTURED; FLUORESCENCE; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; GLUTAMIC ACID; HIPPOCAMPUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SNARE PROTEINS; SYNAPTIC TRANSMISSION; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25;

EID: 57749168634     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-9-105     Document Type: Article

References (51)

1. Jahn R Scheller RH SNAREs - engines for membrane fusion Nat Rev Mol Cell Biol 2006, 7(9):631-643. 10.1038/nrm2002 16912714
2. Rizo J Sudhof TC Snares and Munc18 in synaptic vesicle fusion Nat Rev Neurosci 2002, 3(8):641-653. 12154365
3. Washbourne P Thompson PM Carta M Costa ET Mathews JR Lopez-Bendito G Molnar Z Becher MW Valenzuela CF Partridge LD et al. Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis Nat Neurosci 2002, 5(1):19-26. 11753414
4. Sorensen JB Nagy G Varoqueaux F Nehring RB Brose N Wilson MC Neher E Differential control of the releasable vesicle pools by SNAP-25 splice variants and SNAP-23 Cell 2003, 114(1):75-86. 10.1016/ S0092-8674(03)00477-X 12859899
5. Tafoya LC Mameli M Miyashita T Guzowski JF Valenzuela CF Wilson MC Expression and function of SNAP-25 as a universal SNARE component in GABAergic neurons J Neurosci 2006, 26(30):7826-7838. 10.1523/ JNEUROSCI.1866-06.2006 16870728
6. Catterall WA Interactions of presynaptic Ca2+ channels and snare proteins in neurotransmitter release Ann N Y Acad Sci 1999, 868:144-159. 10.1111/j.1749-6632.1999.tb11284.x 10414292
7. Zhong H Yokoyama CT Scheuer T Catterall WA Reciprocal regulation of P/ Q-type Ca2+ channels by SNAP-25, syntaxin and synaptotagmin Nat Neurosci 1999, 2(11):939-941. 10.1038/14721 10526329
8. Verderio C Pozzi D Pravettoni E Inverardi F Schenk U Coco S Proux-Gillardeaux V Galli T Rossetto O Frassoni C et al. SNAP-25 modulation of calcium dynamics underlies differences in GABAergic and glutamatergic responsiveness to depolarization Neuron 2004, 41(4):599-610. 10.1016/S0896-6273(04)00077-7 14980208
9. Collin T Marty A Llano I Presynaptic calcium stores and synaptic transmission Curr Opin Neurobiol 2005, 15(3):275-281. 10.1016/ j.conb.2005.05.003 15919193
10. Bronk P Deak F Wilson MC Liu X Sudhof TC Kavalali ET Differential effects of SNAP-25 deletion on Ca2+-dependent and Ca2+-independent neurotransmission J Neurophysiol 2007, 98(2):794-806. 10.1152/ jn.00226.2007 17553942
11. Delgado-Martinez I Nehring RB Sorensen JB Differential abilities of SNAP-25 homologs to support neuronal function J Neurosci 2007, 27(35):9380-9391. 10.1523/JNEUROSCI.5092-06.2007 17728451
12. Capogna M McKinney RA O'Connor V Gahwiler BH Thompson SM Ca2+ or Sr2+ partially rescues synaptic transmission in hippocampal cultures treated with botulinum toxin A and C, but not tetanus toxin J Neurosci 1997, 17(19):7190-7202. 9295365
13. Trudeau LE Fang Y Haydon PG Modulation of an early step in the secretory machinery in hippocampal nerve terminals Proc Natl Acad Sci USA 1998, 95(12):7163-7168. 22774 9618556 10.1073/pnas.95.12.7163
14. Catsicas S Larhammar D Blomqvist A Sanna PP Milner RJ Wilson MC Expression of a conserved cell-type-specific protein in nerve terminals coincides with synaptogenesis Proc Natl Acad Sci USA 1991, 88(3):785-789. 50898 1992470 10.1073/pnas.88.3.785
15. Bark IC Hahn KM Ryabinin AE Wilson MC Differential expression of SNAP-25 protein isoforms during divergent vesicle fusion events of neural development Proc Natl Acad Sci USA 1995, 92(5):1510-1514. 42549 7878010 10.1073/pnas.92.5.1510
16. Boschert U O'Shaughnessy C Dickinson R Tessari M Bendotti C Catsicas S Pich EM Developmental and plasticity-related differential expression of two SNAP-25 isoforms in the rat brain J Comp Neurol 1996, 367(2):177-193. 10.1002/ (SICI)1096-9861(19960401)367:2<177::AID-CNE2>3.0.CO;2-2 8708003
17. Gonelle-Gispert C Halban PA Niemann H Palmer M Catsicas S Sadoul K SNAP-25a and -25b isoforms are both expressed in insulin-secreting cells and can function in insulin secretion Biochem J 1999, 339(Pt 1):159-165. 1220140 10085240 10.1042/0264-6021:3390159
18. Grant NJ Hepp R Krause W Aunis D Oehme P Langley K Differential expression of SNAP-25 isoforms and SNAP-23 in the adrenal gland J Neurochem 1999, 72(1):363-372. 10.1046/j.1471-4159.1999.0720363.x 9886089
19. Jacobsson G Bark C Meister B Differential expression of SNAP-25a and SNAP-25b RNA transcripts in cranial nerve nuclei J Comp Neurol 1999, 411(4):591-600. 10.1002/ (SICI)1096-9861(19990906)411:4<591::AID-CNE5>3.0.CO;2-0 10421870
20. Jacobsson G Bean AJ Meister B Isoform-specific exocytotic protein mRNA expression in hypothalamic magnocellular neurons: Regulation after osmotic challenge Neuroendocrinology 1999, 70(6):392-401. 10.1159/ 000054501 10657732
21. Jacobsson G Piehl F Bark IC Zhang X Meister B Differential subcellular localization of SNAP-25a and SNAP-25b RNA transcripts in spinal motoneurons and plasticity in expression after nerve injury Brain Res Mol Brain Res 1996, 37(1-2):49-62. 10.1016/0169-328X(95)00272-T 8738135
22. Bark C Bellinger FP Kaushal A Mathews JR Partridge LD Wilson MC Developmentally regulated switch in alternatively spliced SNAP-25 isoforms alters facilitation of synaptic transmission J Neurosci 2004, 24(40):8796-8805. 10.1523/JNEUROSCI.1940-04.2004 15470145
23. Frassoni C Inverardi F Coco S Ortino B Grumelli C Pozzi D Verderio C Matteoli M Analysis of SNAP-25 immunoreactivity in hippocampal inhibitory neurons during development in culture and in situ Neuroscience 2005, 131(4):813-823. 15749336
24. Bacci A Verderio C Pravettoni E Matteoli M Synaptic and intrinsic mechanisms shape synchronous oscillations in hippocampal neurons in culture Eur J Neurosci 1999, 11(2):389-397. 10.1046/ j.1460-9568.1999.00440.x 10051739
25. Lawrie AM Graham ME Thorn P Gallacher DV Burgoyne RD Synchronous calcium oscillations in cerebellar granule cells in culture mediated by NMDA receptors Neuroreport 1993, 4(5):539-542. 10.1097/ 00001756-199305000-00019 8099816
26. Murphy TH Blatter LA Wier WG Baraban JM Spontaneous synchronous synaptic calcium transients in cultured cortical neurons J Neurosci 1992, 12(12):4834-4845. 1361198
27. Nunez L Sanchez A Fonteriz RI Garcia-Sancho J Mechanisms for synchronous calcium oscillations in cultured rat cerebellar neurons Eur J Neurosci 1996, 8(1):192-201. 10.1111/j.1460-9568.1996.tb01180.x 8713463
28. Schoch S Deak F Konigstorfer A Mozhayeva M Sara Y Sudhof TC Kavalali ET SNARE function analyzed in synaptobrevin/VAMP knockout mice Science 2001, 294(5544):1117-1122. 10.1126/science.1064335 11691998
29. Jonas P Bischofberger J Fricker D Miles R Interneuron diversity series: Fast in, fast out - temporal and spatial signal processing in hippocampal interneurons Trends Neurosci 2004, 27(1):30-40. 10.1016/ j.tins.2003.10.010 14698608
30. Bark IC Wilson MC Regulated vesicular fusion in neurons: Snapping together the details Proc Natl Acad Sci USA 1994, 91(11):4621-4624. 43839 8197108 10.1073/pnas.91.11.4621
31. Nagy G Milosevic I Fasshauer D Muller EM de Groot BL Lang T Wilson MC Sorensen JB Alternative splicing of SNAP-25 regulates secretion through nonconservative substitutions in the SNARE domain Mol Biol Cell 2005, 16(12):5675-5685. 1289412 16195346 10.1091/mbc.E05-07-0595
32. Tamamaki N Yanagawa Y Tomioka R Miyazaki J Obata K Kaneko T Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse J Comp Neurol 2003, 467(1):60-79. 10.1002/cne.10905 14574680
33. Montana V Ni Y Sunjara V Hua X Parpura V Vesicular glutamate transporter-dependent glutamate release from astrocytes J Neurosci 2004, 24(11):2633-2642. 10.1523/JNEUROSCI.3770-03.2004 15028755
34. Parpura V Fang Y Basarsky T Jahn R Haydon PG Expression of synaptobrevin II, cellubrevin and syntaxin but not SNAP-25 in cultured astrocytes FEBS Lett 1995, 377(3):489-492. 10.1016/0014-5793(95)01401-2 8549782
35. Madison DL Krueger WH Cheng D Trapp BD Pfeiffer SE SNARE complex proteins, including the cognate pair VAMP-2 and syntaxin-4, are expressed in cultured oligodendrocytes J Neurochem 1999, 72(3):988-998. 10.1046/j.1471-4159.1999.0720988.x 10037470
36. Oyler GA Higgins GA Hart RA Battenberg E Billingsley M Bloom FE Wilson MC The identification of a novel synaptosomal-associated protein, SNAP-25, differentially expressed by neuronal subpopulations J Cell Biol 1989, 109(6 Pt 1):3039-3052. 2115928 2592413 10.1083/jcb.109.6.3039
37. Matteoli M Pozzi D Grumelli C Condliffe S Frassoni C Harkany T Verderio C The synaptic split of SNAP-25: Different roles in glutamatergic and GABAERGIC neurons? Neuroscience 2008. 18514426
38. Branks PL Wilson MC Patterns of gene expression in the murine brain revealed by in situ hybridization of brain-specific mRNAs Brain Res 1986, 387(1):1-16. 3755636
39. Loewenstein Y Mahon S Chadderton P Kitamura K Sompolinsky H Yarom Y Hausser M Bistability of cerebellar Purkinje cells modulated by sensory stimulation Nat Neurosci 2005, 8(2):202-211. 10.1038/nn1393 15665875
40. Hess DT Slater TM Wilson MC Skene JH The 25 kDa synaptosomal-associated protein SNAP-25 is the major methionine-rich polypeptide in rapid axonal transport and a major substrate for palmitoylation in adult CNS J Neurosci 1992, 12(12):4634-4641. 1281490
41. Salaun C Gould GW Chamberlain LH The SNARE proteins SNAP-25 and SNAP-23 display different affinities for lipid rafts in PC12 cells. Regulation by distinct cysteine-rich domains J Biol Chem 2005, 280(2):1236-1240. 2387193 15542596 10.1074/jbc.M410674200
42. Kataoka M Kuwahara R Iwasaki S Shoji-Kasai Y Takahashi M Nerve growth factor-induced phosphorylation of SNAP-25 in PC12 cells: A possible involvement in the regulation of SNAP-25 localization J Neurochem 2000, 74(5):2058-2066. 10.1046/j.1471-4159.2000.0742058.x 10800949
43. Pozzi D Condliffe S Bozzi Y Chikhladze M Grumelli C Proux-Gillardeaux V Takahashi M Franceschetti S Verderio C Matteoli M Activity-dependent phosphorylation of Ser187 is required for SNAP-25-negative modulation of neuronal voltage-gated calcium channels Proc Natl Acad Sci USA 2008, 105:323-328. 2224210 18162553 10.1073/pnas.0706211105
44. Kataoka M Kuwahara R Matsuo R Sekiguchi M Inokuchi K Takahashi M Development- and activity-dependent regulation of SNAP-25 phosphorylation in rat brain Neurosci Lett 2006, 407:258-262. 10.1016/ j.neulet.2006.08.055 16978778
45. Shu Y Liu XB Yang Y Takahashi M Gillis KD Phosphorylation of SNAP-25 at Ser187 mediates enhancement of exocytosis by a phorbol ester in INS-1 cells J Neurosci 2008, 28:21-30. 10.1523/JNEUROSCI.2352-07.2008 18171919
46. Jacobsson G Meister B Molecular components of the exocytotic machinery in the rat pituitary gland Endocrinology 1996, 137(12):5344-5356. 10.1210/en.137.12.5344 8940356
47. Jacobsson G Bean AJ Scheller RH Juntti-Berggren L Deeney JT Berggren PO Meister B Identification of synaptic proteins and their isoform mRNAs in compartments of pancreatic endocrine cells Proc Natl Acad Sci USA 1994, 91(26):12487-12491. 45463 7809063 10.1073/pnas.91.26.12487
48. Hepp R Dupont JL Aunis D Langley K Grant NJ NGF enhances depolarization effects on SNAP-25 expression: Induction of SNAP-25b isoform Neuroreport 2001, 12(4):673-677. 10.1097/00001756-200103260-00011 11277561
49. Gutierrez R Heinemann U Co-existence of GABA and Glu in the hippocampal granule cells: Implications for epilepsy Curr Top Med Chem 2006, 6(10):975-978. 10.2174/156802606777323692 16787272
50. Verkhratsky A Glial calcium signaling in physiology and pathophysiology Acta Pharmacol Sin 2006, 27(7):773-780. 10.1111/j.1745-7254.2006.00396.x 16787559
51. Xiang CC Mezey E Chen M Key S Ma L Brownstein MJ Using DSP, a reversible cross-linker, to fix tissue sections for immunostaining, microdissection and expression profiling Nucleic Acids Res 2004, 32(22):e185. 545482 15604454 10.1093/nar/gnh185