Syntaxin 1B, but not syntaxin 1A, is necessary for the regulation of synaptic vesicle exocytosis and of the readily releasable pool at central synapses

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Mishima, Tatsuya ^a   Fujiwara, Tomonori ^a   Sanada, Masumi ^a   Kofuji, Takefumi ^a   Kanai Azuma, Masami ^a   Akagawa, Kimio ^a  

^a KYORIN UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

SNARE PROTEIN; SYNTAXIN; SYNTAXIN 1A; SYNTAXIN 1B; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; EVOKED RESPONSE; EXOCYTOSIS; FEMALE; FREQUENCY MODULATION; GABAERGIC SYSTEM; GENE OVEREXPRESSION; GLUTAMATERGIC SYNAPSE; MOUSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PROTEIN DETERMINATION; PROTEIN FUNCTION; SYNAPSE; SYNAPTIC TRANSMISSION;

ANIMALS; EVOKED POTENTIALS; EXOCYTOSIS; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION; GLUTAMIC ACID; MALE; MICE; MICE, KNOCKOUT; NEURONS; SYNAPSES; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; SYNTAXIN 1;

EID: 84896540220     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0090004     Document Type: Article

References (42)

1. Lin RC, Scheller RH (2000) Mechanisms of synaptic vesicle exocytosis. Annu Rev Cell Dev Biol 16: 19-49. (Pubitemid 32037499)
2. Rizo J, Südhof TC (2002) Snares and Munc18 in synaptic vesicle fusion. Nat Rev Neurosci 3: 641-653. (Pubitemid 135706672)
3. Kasai H, Takahashi N, Tokumaru H (2012) Distinct initial SNARE configurations underlying the diversity of exocytosis. Physiol Rev 92: 1915-1964.
4. Hata Y, Slaughter CA, Südhof TC (1993) Synaptic vesicle fusion complex contains unc-18 homologue bound to syntaxin. Nature 366: 347-351.
5. Bennett MK, Calakos N, Scheller RH (1992) Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science 257: 255-259.
6. Sheng ZH, Rettig J, Takahashi M, Catterall WA (1994) Identification of a syntaxin-binding site on N-type calcium channels. Neuron 13: 1303-1313.
7. Pabst S, Hazzard JW, Antonin W, Südhof TC, Jahn R, et al. (2000) Selective interaction of complexin with the neuronal SNARE complex. Determination of the binding regions. J Biol Chem 275: 19808-19818.
8. Inoue a, Obata K, Akagawa K (1992) Cloning and sequence analysis of cDNA for a neuronal cell membrane antigen, HPC-1. J Biol Chem 267: 10613-10619.
9. Kushima Y, Fujiwara T, Sanada M, Akagawa K (1997) Characterization of HPC-1 antigen, an isoform of syntaxin-1, with the isoform-specific monoclonal antibody, 14D8. J Mol Neurosci 8: 19-27. (Pubitemid 127721712)
10. Washbourne P, Thompson PM, Carta M, Costa ET, Mathews JR, et al. (2002) Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat Neurosci 5: 19-26. (Pubitemid 34038778)
11. Schoch S, Deák F, Königstorfer A, Mozhayeva M, Sara Y, et al. (2001) SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 294: 1117-1122. (Pubitemid 33041870)
12. Mishima T, Fujiwara T, Kofuji T, Akagawa K (2012) Impairment of catecholamine systems during induction of long-term potentiation at hippocampal CA1 synapses in HPC-1/syntaxin 1A knock-out mice. J Neurosci 32: 381-389.
13. Fujiwara T, Mishima T, Kofuji T, Chiba T, Tanaka K, et al. (2006) Analysis of knock-out mice to determine the role of HPC-1/syntaxin 1A in expressing synaptic plasticity. J Neurosci 26: 5767-5776. (Pubitemid 44315269)
14. Fujiwara T, Sanada M, Kofuji T, Mishima T, Kanai-Azuma M, et al. (2009) Phenotype analysis of syntaxin1B knockout mice. Neurosci Res 65: S79.
15. Mishima T, Fujiwara T, Akagawa K (2002) Reduction of neurotransmitter release by the exogenous H3 domain peptide of HPC-1/syntaxin 1A in cultured rat hippocampal neurons. Neurosci Lett 329: 273-276. (Pubitemid 35245340)
16. Koh S, Yamamoto A, Inoue A, Inoue Y, Akagawa K, et al. (1993) Immunoelectron microscopic localization of the HPC-1 antigen in rat cerebellum. J Neurocytol 22: 995-1005. (Pubitemid 23343023)
17. Leenders a G, Lopes da Silva FH, Ghijsen WE, Verhage M (2001) Rab3a is involved in transport of synaptic vesicles to the active zone in mouse brain nerve terminals. Mol Biol Cell 12: 3095-3102. (Pubitemid 33062964)
18. Schneggenburger R, Meyer a C, Neher E (1999) Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23: 399-409. (Pubitemid 29315733)
19. Moulder KL, Mennerick S (2005) Reluctant vesicles contribute to the total readily releasable pool in glutamatergic hippocampal neurons. J Neurosci 25: 3842-3850. (Pubitemid 40570417)
20. Hua Z, Leal-Ortiz S, Foss SM, Waites CL, Garner CC, et al. (2011) v-SNARE composition distinguishes synaptic vesicle pools. Neuron 71: 474-487.
21. Ramirez DMO, Khvotchev M, Trauterman B, Kavalali ET (2012) Vti1a identifies a vesicle pool that preferentially recycles at rest and maintains spontaneous neurotransmission. Neuron 73: 121-134.
22. Raingo J, Khvotchev M, Liu P, Darios F, Li YC, et al. (2012) VAMP4 directs synaptic vesicles to a pool that selectively maintains asynchronous neurotransmission. Nat Neurosci 15.
23. Rosenmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16: 1197-1207. (Pubitemid 26227241)
24. Stevens CF, Tsujimoto T (1995) Estimates for the pool size of releasable quanta at a single central synapse and for the time required to refill the pool. Proc Natl Acad Sci U S A 92: 846-849.
25. Zhou P, Pang ZP, Yang X, Zhang Y, Rosenmund C, et al. (2012) Syntaxin-1 Npeptide and H(abc)-domain perform distinct essential functions in synaptic vesicle fusion. EMBO J: 1-13.
26. Ruiz-Montasell B, Aguado F, Majó G, Chapman ER, Canals JM, et al. (1996) Differential distribution of syntaxin isoforms 1A and 1B in the rat central nervous system. Eur J Neurosci 8: 2544-2552. (Pubitemid 27011330)
27. Aguado F, Majó G, Ruiz-Montasell B, Llorens J, Marsal J, et al. (1999) Syntaxin 1A and 1B display distinct distribution patterns in the rat peripheral nervous system. Neuroscience 88: 437-446. (Pubitemid 28480005)
28. Gerber SH, Rah J, Min S, Liu X, de Wit H, et al. (2008) Conformational switch of syntaxin-1 controls synaptic vesicle fusion. Science 321: 1507-1510.
29. Arancillo M, Min S-W, Gerber SH, Munster-Wandowski A., Wu Y-J, et al. (2013) Titration of Syntaxin1 in Mammalian Synapses Reveals Multiple Roles in Vesicle Docking, Priming, and Release Probability. J Neurosci 33: 16698-16714.
30. Pérez-Brangul?́ F, Muhaisen A, Blasi J (2002) Munc 18a binding to syntaxin 1A and 1B isoforms defines its localization at the plasma membrane and blocks SNARE assembly in a three-hybrid system assay. Mol Cell Neurosci 20: 169-180. (Pubitemid 34762129)
31. Prange O, Murphy TH (1999) Correlation of miniature synaptic activity and evoked release probability in cultures of cortical neurons. J Neurosci 19: 6427-6438. (Pubitemid 29347442)
32. Xu J, Luo F, Zhang Z, Xue L, Wu X-S, et al. (2013) SNARE Proteins Synaptobrevin, SNAP-25, and Syntaxin Are Involved in Rapid and Slow Endocytosis at Synapses. Cell Rep: 1-8.
33. Ma H, Cai Q, Lu W, Sheng Z-H, Mochida S (2009) KIF5B motor adaptor syntabulin maintains synaptic transmission in sympathetic neurons. J Neurosci 29: 13019-13029.
34. Su Q, Cai Q, Gerwin C, Smith CL, Sheng Z-H (2004) Syntabulin is a microtubule-associated protein implicated in syntaxin transport in neurons. Nat Cell Biol 6: 941-953. (Pubitemid 39359847)
35. Bronk P, Deák F, Wilson MC, Liu X, Südhof TC, et al. (2007) Differential effects of SNAP-25 deletion on Ca2+-dependent and Ca2+-independent neurotransmission. J Neurophysiol 98: 794-806. (Pubitemid 47236033)
36. Delgado-Mart?́nez I, Nehring RB, Sørensen JB (2007) Differential abilities of SNAP-25 homologs to support neuronal function. J Neurosci 27: 9380-9391. (Pubitemid 47358199)
37. Peng L, Liu H, Ruan H, Tepp WH, Stoothoff WH, et al. (2013) Cytot oxicity of botulinum neurotoxins reveals a direct role of syntaxin 1 and SNAP-25 in neuron survival. Nat Commun 4: 1472.
38. Curtis L, Datta P, Liu X, Bogdanova N, Heidelberger R, et al. (2010) Syntaxin 3B is essential for the exocytosis of synaptic vesicles in ribbon synapses of the retina. Neuroscience 166: 832-841.
39. Curtis LB, Doneske B, Liu X, Thaller C, McNew Ja, et al. (2008) Syntaxin 3b is a t-SNARE specific for ribbon synapses of the retina. J Comp Neurol 510: 550-559.
40. Jurado S, Goswami D, Zhang Y, Molina AJM, Südhof TC, et al. (2013) LTP Requires a Unique Postsynaptic SNARE Fusion Machinery. Neuron 77: 542-558.
41. Maximov A, Südhof TC (2005) Autonomous function of synaptotagmin 1 in triggering synchronous release independent of asynchronous release. Neuron 48: 547-554 (Pubitemid 41654677)
42. Nishiki T, Augustine GJ (2004) Synaptotagmin I synchronizes transmitter release in mouse hippocampal neurons. J 24: 6127-6132. (Pubitemid 38891103)