Synaptotagmin- 11 inhibits spontaneous neurotransmission through vti1a
dc.contributor.author | Li, Wan‐ru | |
dc.contributor.author | Wang, Ya‐Long | |
dc.contributor.author | Li, Chao | |
dc.contributor.author | Gao, Pei | |
dc.contributor.author | Zhang, Fei‐Fan | |
dc.contributor.author | Hu, Meiqin | |
dc.contributor.author | Li, Jing‐chen | |
dc.contributor.author | Zhang, Shuli | |
dc.contributor.author | Li, Rena | |
dc.contributor.author | Zhang, Claire Xi | |
dc.date.accessioned | 2021-12-02T02:32:13Z | |
dc.date.available | 2022-12-01 21:32:12 | en |
dc.date.available | 2021-12-02T02:32:13Z | |
dc.date.issued | 2021-11 | |
dc.identifier.citation | Li, Wan‐ru ; Wang, Ya‐Long ; Li, Chao; Gao, Pei; Zhang, Fei‐Fan ; Hu, Meiqin; Li, Jing‐chen ; Zhang, Shuli; Li, Rena; Zhang, Claire Xi (2021). "Synaptotagmin- 11 inhibits spontaneous neurotransmission through vti1a." Journal of Neurochemistry (4): 729-741. | |
dc.identifier.issn | 0022-3042 | |
dc.identifier.issn | 1471-4159 | |
dc.identifier.uri | https://hdl.handle.net/2027.42/171049 | |
dc.description.abstract | Recent work has revealed that spontaneous release plays critical roles in the central nervous system, but how it is regulated remains elusive. Here, we report that synaptotagmin- 11 (Syt11), a Ca2+- independent Syt isoform associated with schizophrenia and Parkinson’s disease, suppressed spontaneous release. Syt11- knockout hippocampal neurons showed an increased frequency of miniature excitatory post- synaptic currents while over- expression of Syt11 inversely decreased the frequency. Neither knockout nor over- expression of Syt11 affected the average amplitude, suggesting the pre- synaptic regulation of spontaneous neurotransmission by Syt11. Glutathione S- transferase pull- down, co- immunoprecipitation, and affinity- purification experiments demonstrated a direct interaction of Syt11 with vps10p- tail- interactor- 1a (vti1a), a non- canonical SNARE protein that maintains spontaneous release. Importantly, knockdown of vti1a reversed the phenotype of Syt11Â knockout, identifying vti1a as the main target of Syt11 inhibition. Domain analysis revealed that the C2A domain of Syt11 bound vti1a with high affinity. Consistently, expression of the C2A domain alone rescued the phenotype of elevated spontaneous release in Syt11- knockout neurons similar to the full- length protein. Altogether, our results suggest that Syt11 inhibits vti1a- containing vesicles during spontaneous release.Spontaneous neurotransmission plays important roles in the maturation of primeval synapses, post- synaptic signal transduction and synaptic plasticity. Here, we report that synaptotagmin- 11 (Syt11)- knockout in hippocampal neurons increases the frequency of miniature excitatory post- synaptic currents while over- expression reduces it. Mechanistically, Syt11 directly interacts with vps10p- tail- interactor- 1a (vti1a), and knockdown of vti1a reverses the Syt11- knockout phenotype, identifying vti1a as the main target of Syt11 inhibition. The C2A domain of Syt11 binds vti1a with high affinity. Expression of the C2A domain rescues the knockout phenotype similar to full- length Syt11. Altogether, we have identified Syt11 as a novel inhibitor of spontaneous neurotransmission via interaction with vti1a. | |
dc.publisher | Wiley Periodicals, Inc. | |
dc.subject.other | vti1a | |
dc.subject.other | spontaneous release | |
dc.subject.other | synaptotagmin | |
dc.subject.other | SNARE | |
dc.title | Synaptotagmin- 11 inhibits spontaneous neurotransmission through vti1a | |
dc.type | Article | |
dc.rights.robots | IndexNoFollow | |
dc.subject.hlbsecondlevel | Neurosciences | |
dc.subject.hlbtoplevel | Health Sciences | |
dc.description.peerreviewed | Peer Reviewed | |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/171049/1/jnc15523_am.pdf | |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/171049/2/jnc15523.pdf | |
dc.identifier.doi | 10.1111/jnc.15523 | |
dc.identifier.source | Journal of Neurochemistry | |
dc.identifier.citedreference | Raingo, J., Khvotchev, M., Liu, P., Darios, F., Li, Y. C., Ramirez, D. M. O., Adachi, M., Lemieux, P., Toth, K., Davletov, B., & Kavalali, E. T. ( 2012 ). VAMP4 directs synaptic vesicles to a pool that selectively maintains asynchronous neurotransmission. Nature Neuroscience, 15, 738 - 745. https://doi.org/10.1038/nn.3067 | |
dc.identifier.citedreference | Nishiki, T., & Augustine, G. J. ( 2004 ). Synaptotagmin I synchronizes transmitter release in mouse hippocampal neurons. Journal of Neuroscience, 24, 6127 - 6132. https://doi.org/10.1523/JNEUROSCI.1563- 04.2004 | |
dc.identifier.citedreference | Pallanck, L. ( 2003 ). A tale of two C2 domains. Trends in Neurosciences, 26, 2 - 4. https://doi.org/10.1016/S0166- 2236(02)00007- 3 | |
dc.identifier.citedreference | Pang, Z. P., Bacaj, T., Yang, X., Zhou, P., Xu, W., & Sudhof, T. C. ( 2011 ). Doc2 supports spontaneous synaptic transmission by a Ca(2+)- independent mechanism. Neuron, 70, 244 - 251. | |
dc.identifier.citedreference | Pang, Z. P., & Sudhof, T. C. ( 2010 ). Cell biology of Ca 2+ - triggered exocytosis. Current Opinion in Cell Biology, 22, 496 - 505. https://doi.org/10.1016/j.ceb.2010.05.001 | |
dc.identifier.citedreference | Pang, Z. P., Sun, J., Rizo, J., Maximov, A., & Sudhof, T. C. ( 2006 ). Genetic analysis of synaptotagmin 2 in spontaneous and Ca 2+ - triggered neurotransmitter release. EMBO Journal, 25, 2039 - 2050. https://doi.org/10.1038/sj.emboj.7601103 | |
dc.identifier.citedreference | Pihlstrøm, L., Axelsson, G., BjørnarÃ¥, K. A., Dizdar, N., Fardell, C., Forsgren, L., Holmberg, B., Larsen, J. P., Linder, J., Nissbrandt, H., Tysnes, O.- B., à hman, E., Dietrichs, E., & Toft, M. ( 2013 ). Supportive evidence for 11 loci from genome- wide association studies in Parkinson’s disease. Neurobiology of Aging, 34 ( 6 ), 1708.e7 - 1708.e13. https://doi.org/10.1016/j.neurobiolaging.2012.10.019 | |
dc.identifier.citedreference | Pratt, K. G., Zhu, P., Watari, H., Cook, D. G., & Sullivan, J. M. ( 2011 ). A novel role for γ- secretase: selective regulation of spontaneous neurotransmitter release from hippocampal neurons. Journal of Neuroscience, 31, 899 - 906. | |
dc.identifier.citedreference | Ramirez, D. M., Khvotchev, M., Trauterman, B., & Kavalali, E. T. ( 2012 ). Vti1a identifies a vesicle pool that preferentially recycles at rest and maintains spontaneous neurotransmission. Neuron, 73, 121 - 134. https://doi.org/10.1016/j.neuron.2011.10.034 | |
dc.identifier.citedreference | Regehr, W. G. ( 2012 ). Short- term presynaptic plasticity. Cold Spring Harbor Perspectives in Biology, 4, a005702. https://doi.org/10.1101/cshperspect.a005702 | |
dc.identifier.citedreference | Sara, Y., Virmani, T., Deak, F., Liu, X., & Kavalali, E. T. ( 2005 ). An isolated pool of vesicles recycles at rest and drives spontaneous neurotransmission. Neuron, 45, 563 - 573. https://doi.org/10.1016/j.neuron.2004.12.056 | |
dc.identifier.citedreference | Schupp, M., Malsam, J., Ruiter, M., Scheutzow, A., Wierda, K. D., Sollner, T. H., & Sorensen, J. B. ( 2016 ). Interactions between SNAP- 25 and synaptotagmin- 1 are involved in vesicle priming, clamping spontaneous and stimulating evoked neurotransmission. Journal of Neuroscience, 36, 11865 - 11880. https://doi.org/10.1523/JNEUROSCI.1011- 16.2016 | |
dc.identifier.citedreference | Sesar, A., Cacheiro, P., López- López, M., Camiña- Tato, M., Quintáns, B., Monroy- Jaramillo, N., Alonso- Vilatela, M.- E., Cebrián, E., Yescas- Gómez, P., Ares, B., Rivas, M.- T., Castro, A., Carracedo, A., & Sobrido, M.- J. ( 2016 ). Synaptotagmin XI in Parkinson’s disease: New evidence from an association study in Spain and Mexico. Journal of the Neurological Sciences, 362, 321 - 325. https://doi.org/10.1016/j.jns.2016.02.014 | |
dc.identifier.citedreference | Shimojo, M., Madara, J., Pankow, S., Liu, X., Yates, J. 3rd, Sudhof, T. C., & Maximov, A. ( 2019 ). Synaptotagmin- 11 mediates a vesicle trafficking pathway that is essential for development and synaptic plasticity. Genes and Development, 33, 365 - 376. https://doi.org/10.1101/gad.320077.118 | |
dc.identifier.citedreference | Sreetama, S. C., Takano, T., Nedergaard, M., Simon, S. M., & Jaiswal, J. K. ( 2016 ). Injured astrocytes are repaired by Synaptotagmin XI- regulated lysosome exocytosis. Cell Death and Differentiation, 23, 596 - 607. https://doi.org/10.1038/cdd.2015.124 | |
dc.identifier.citedreference | Sudhof, T. C., & Rothman, J. E. ( 2009 ). Membrane fusion: grappling with SNARE and SM proteins. Science, 323, 474 - 477. https://doi.org/10.1126/science.1161748 | |
dc.identifier.citedreference | Sun, J., Pang, Z. P., Qin, D., Fahim, A. T., Adachi, R., & Sudhof, T. C. ( 2007 ). A dual- Ca 2+ - sensor model for neurotransmitter release in a central synapse. Nature, 450, 676 - 682. https://doi.org/10.1038/nature06308 | |
dc.identifier.citedreference | Takamori, S., Holt, M., Stenius, K., Lemke, E. A., Grønborg, M., Riedel, D., Urlaub, H., Schenck, S., Brügger, B., Ringler, P., Müller, S. A., Rammner, B., Gräter, F., Hub, J. S., De Groot, B. L., Mieskes, G., Moriyama, Y., Klingauf, J., Grubmüller, H., - ¦ Jahn, R. ( 2006 ). Molecular anatomy of a trafficking organelle. Cell, 127, 831 - 846. https://doi.org/10.1016/j.cell.2006.10.030 | |
dc.identifier.citedreference | Truckenbrodt, S., & Rizzoli, S. O. ( 2014 ). Spontaneous vesicle recycling in the synaptic bouton. Frontiers in Cellular Neuroscience, 8, 409. https://doi.org/10.3389/fncel.2014.00409 | |
dc.identifier.citedreference | von Poser, C., Ichtchenko, K., Shao, X., Rizo, J., & Sudhof, T. C. ( 1997 ). The evolutionary pressure to inactivate. A subclass of synaptotagmins with an amino acid substitution that abolishes Ca 2+ binding. Journal of Biological Chemistry, 272, 14314 - 14319. | |
dc.identifier.citedreference | Walter, A. M., Kurps, J., de Wit, H., Schöning, S., Toft- Bertelsen, T. L., Lauks, J., Ziomkiewicz, I., Weiss, A. N., Schulz, A., Fischer von Mollard, G., & Verhage, M. ( 2014 ). The SNARE protein vti1a functions in dense- core vesicle biogenesis. EMBO Journal, 33, 1681 - 1697. | |
dc.identifier.citedreference | Wang, C., Kang, X., Zhou, L. I., Chai, Z., Wu, Q., Huang, R., Xu, H., Hu, M., Sun, X., Sun, S., Li, J., Jiao, R., Zuo, P., Zheng, L., Yue, Z., & Zhou, Z. ( 2018 ). Synaptotagmin- 11 is a critical mediator of parkin- linked neurotoxicity and Parkinson’s disease- like pathology. Nature Communications, 9, 81. https://doi.org/10.1038/s41467- 017- 02593- y | |
dc.identifier.citedreference | Wang, C., Wang, Y., Hu, M., Chai, Z., Wu, Q., Huang, R., Han, W., Zhang, C. X., & Zhou, Z. ( 2016 ). Synaptotagmin- 11 inhibits clathrin- mediated and bulk endocytosis. EMBO Reports, 17, 47 - 63. https://doi.org/10.15252/embr.201540689 | |
dc.identifier.citedreference | Wierda, K. D., & Sorensen, J. B. ( 2014 ). Innervation by a GABAergic neuron depresses spontaneous release in glutamatergic neurons and unveils the clamping phenotype of synaptotagmin- 1. Journal of Neuroscience, 34, 2100 - 2110. https://doi.org/10.1523/JNEUROSCI.3934- 13.2014 | |
dc.identifier.citedreference | Williams, C. L., & Smith, S. M. ( 2018 ). Calcium dependence of spontaneous neurotransmitter release. Journal of Neuroscience Research, 96, 335 - 347. https://doi.org/10.1002/jnr.24116 | |
dc.identifier.citedreference | Xu, J., Mashimo, T., & Sudhof, T. C. ( 2007 ). Synaptotagmin- 1, - 2, and - 9: Ca(2+) sensors for fast release that specify distinct presynaptic properties in subsets of neurons. Neuron, 54, 567 - 581. https://doi.org/10.1016/j.neuron.2007.05.004 | |
dc.identifier.citedreference | Xu, J., Pang, Z. P., Shin, O. H., & Sudhof, T. C. ( 2009 ). Synaptotagmin- 1 functions as a Ca 2+ sensor for spontaneous release. Nature Neuroscience, 12, 759 - 766. https://doi.org/10.1038/nn.2320 | |
dc.identifier.citedreference | Yan, S., Wang, Y., Zhang, Y., Wang, L. E., Zhao, X., Du, C., Gao, P., Yan, F., Liu, F., Gong, X., Guan, Y., Cui, X., Wang, X., & Xi Zhang, C. ( 2020 ). Synaptotagmin- 11 regulates the functions of caveolae and responds to mechanical stimuli in astrocytes. The FASEB Journal, 34, 2609 - 2624. https://doi.org/10.1096/fj.201901715R | |
dc.identifier.citedreference | Yang, X., Cao, P., & Sudhof, T. C. ( 2013 ). Deconstructing complexin function in activating and clamping Ca 2+ - triggered exocytosis by comparing knockout and knockdown phenotypes. Proceedings of the National Academy of Sciences, 110, 20777 - 20782. https://doi.org/10.1073/pnas.1321367110 | |
dc.identifier.citedreference | Advani, R. J., Bae, H. R., Bock, J. B., Chao, D. S., Doung, Y. C., Prekeris, R., Yoo, J. S., & Scheller, R. H. ( 1998 ). Seven novel mammalian SNARE proteins localize to distinct membrane compartments. Journal of Biological Chemistry, 273, 10317 - 10324. https://doi.org/10.1074/jbc.273.17.10317 | |
dc.identifier.citedreference | Andreae, L. C., & Burrone, J. ( 2018 ). The role of spontaneous neurotransmission in synapse and circuit development. Journal of Neuroscience Research, 96, 354 - 359. https://doi.org/10.1002/jnr.24154 | |
dc.identifier.citedreference | Antonin, W., Fasshauer, D., Becker, S., Jahn, R., & Schneider, T. R. ( 2002 ). Crystal structure of the endosomal SNARE complex reveals common structural principles of all SNAREs. Natural Structural Biology, 9, 107 - 111. https://doi.org/10.1038/nsb746 | |
dc.identifier.citedreference | Bacaj, T., Wu, D., Yang, X., Morishita, W., Zhou, P., Xu, W., Malenka, R. C., & Sudhof, T. C. ( 2013 ). Synaptotagmin- 1 and synaptotagmin- 7 trigger synchronous and asynchronous phases of neurotransmitter release. Neuron, 80, 947 - 959. https://doi.org/10.1016/j.neuron.2013.10.026 | |
dc.identifier.citedreference | Bal, M., Leitz, J., Reese, A. L., Ramirez, D. M., Durakoglugil, M., Herz, J., Monteggia, L. M., & Kavalali, E. T. ( 2013 ). Reelin mobilizes a VAMP7- dependent synaptic vesicle pool and selectively augments spontaneous neurotransmission. Neuron, 80, 934 - 946. https://doi.org/10.1016/j.neuron.2013.08.024 | |
dc.identifier.citedreference | Bento, C. F., Ashkenazi, A., Jimenez- Sanchez, M., & Rubinsztein, D. C. ( 2016 ). The Parkinson’s disease- associated genes ATP13A2 and SYT11 regulate autophagy via a common pathway. Nature Communications, 7, 11803. https://doi.org/10.1038/ncomms11803 | |
dc.identifier.citedreference | Cornelisse, L. N., Tsivtsivadze, E., Meijer, M., Dijkstra, T. M., Heskes, T., & Verhage, M. ( 2012 ). Molecular machines in the synapse: overlapping protein sets control distinct steps in neurosecretion. PLoS Computational Biology, 8, e1002450. https://doi.org/10.1371/journal.pcbi.1002450 | |
dc.identifier.citedreference | Crawford, D. C., Ramirez, D. M., Trauterman, B., Monteggia, L. M., & Kavalali, E. T. ( 2017 ). Selective molecular impairment of spontaneous neurotransmission modulates synaptic efficacy. Nature Communications, 8, 14436. https://doi.org/10.1038/ncomms14436 | |
dc.identifier.citedreference | Dean, C., Liu, H., Dunning, F. M., Chang, P. Y., Jackson, M. B., & Chapman, E. R. ( 2009 ). Synaptotagmin- IV modulates synaptic function and long- term potentiation by regulating BDNF release. Nature Neuroscience, 12, 767 - 776. https://doi.org/10.1038/nn.2315 | |
dc.identifier.citedreference | Du, C., Wang, Y., Zhang, F., Yan, S., Guan, Y., Gong, X., Zhang, T., Cui, X., Wang, X., & Zhang, C. X. ( 2017 ). Synaptotagmin- 11 inhibits cytokine secretion and phagocytosis in microglia. Glia, 65, 1656 - 1667. https://doi.org/10.1002/glia.23186 | |
dc.identifier.citedreference | Emperador- Melero, J., Huson, V., van Weering, J., Bollmann, C., Fischer von Mollard, G., Toonen, R. F., & Verhage, M. ( 2018 ). Vti1a/b regulate synaptic vesicle and dense core vesicle secretion via protein sorting at the Golgi. Nature Communications, 9, 3421. https://doi.org/10.1038/s41467- 018- 05699- z | |
dc.identifier.citedreference | Emperador- Melero, J., Toonen, R. F., & Verhage, M. ( 2019 ). Vti proteins: Beyond endolysosomal trafficking. Neuroscience, 420, 32 - 40. https://doi.org/10.1016/j.neuroscience.2018.11.014. | |
dc.identifier.citedreference | Fatt, P., & Katz, B. ( 1950 ). Some observations on biological noise. Nature, 166, 597 - 598. https://doi.org/10.1038/166597a0 | |
dc.identifier.citedreference | Fatt, P., & Katz, B. ( 1952 ). Spontaneous subthreshold activity at motor nerve endings. Journal of Physiology, 117, 109 - 128. | |
dc.identifier.citedreference | Fawley, J. A., Hofmann, M. E., & Andresen, M. C. ( 2014 ). Cannabinoid 1 and transient receptor potential vanilloid 1 receptors discretely modulate evoked glutamate separately from spontaneous glutamate transmission. Journal of Neuroscience, 34, 8324 - 8332. https://doi.org/10.1523/JNEUROSCI.0315- 14.2014 | |
dc.identifier.citedreference | Fredj, N. B., & Burrone, J. ( 2009 ). A resting pool of vesicles is responsible for spontaneous vesicle fusion at the synapse. Nature Neuroscience, 12, 751 - 758. https://doi.org/10.1038/nn.2317 | |
dc.identifier.citedreference | Geppert, M., Goda, Y., Hammer, R. E., Li, C., Rosahl, T. W., Stevens, C. F., & Sudhof, T. C. ( 1994 ). Synaptotagmin I: a major Ca 2+ sensor for transmitter release at a central synapse. Cell, 79, 717 - 727. https://doi.org/10.1016/0092- 8674(94)90556- 8 | |
dc.identifier.citedreference | Glitsch, M. ( 2006 ). Selective inhibition of spontaneous but not Ca 2+ - dependent release machinery by presynaptic group II mGluRs in rat cerebellar slices. Journal of Neurophysiology, 96, 86 - 96. | |
dc.identifier.citedreference | Gonzalez- Islas, C., Bulow, P., & Wenner, P. ( 2018 ). Regulation of synaptic scaling by action potential- independent miniature neurotransmission. Journal of Neuroscience Research, 96, 348 - 353. https://doi.org/10.1002/jnr.24138 | |
dc.identifier.citedreference | Groemer, T. W., & Klingauf, J. ( 2007 ). Synaptic vesicles recycling spontaneously and during activity belong to the same vesicle pool. Nature Neuroscience, 10, 145 - 147. https://doi.org/10.1038/nn1831 | |
dc.identifier.citedreference | Groffen, A. J., Martens, S., Arazola, R. D., Cornelisse, L. N., Lozovaya, N., de Jong, A. P., Goriounova, N. A., Habets, R. L., Takai, Y., Borst, J. G., & Brose, N. ( 2010 ). Doc2b is a high- affinity Ca 2+ sensor for spontaneous neurotransmitter release. Science, 327, 1614 - 1618. | |
dc.identifier.citedreference | Hu, H., Wang, X., Li, C., Li, Y., Hao, J., Zhou, Y., Yang, X., Chen, P., Shen, X., & Zhang, S. ( 2021 ). Loss of Dysbindin implicates synaptic vesicle replenishment dysregulation as a potential pathogenic mechanism in schizophrenia. Neuroscience, 452, 138 - 152. https://doi.org/10.1016/j.neuroscience.2020.10.020 | |
dc.identifier.citedreference | Hua, Z., Leal- Ortiz, S., Foss, S. M., Waites, C. L., Garner, C. C., Voglmaier, S. M., & Edwards, R. H. ( 2011 ). v- SNARE composition distinguishes synaptic vesicle pools. Neuron, 71, 474 - 487. https://doi.org/10.1016/j.neuron.2011.06.010 | |
dc.identifier.citedreference | Huntwork, S., & Littleton, J. T. ( 2007 ). A complexin fusion clamp regulates spontaneous neurotransmitter release and synaptic growth. Nature Neuroscience, 10, 1235 - 1237. https://doi.org/10.1038/nn1980 | |
dc.identifier.citedreference | Huynh, D. P., Scoles, D. R., Nguyen, D., & Pulst, S. M. ( 2003 ). The autosomal recessive juvenile Parkinson disease gene product, parkin, interacts with and ubiquitinates synaptotagmin XI. Human Molecular Genetics, 12, 2587 - 2597. https://doi.org/10.1093/hmg/ddg269 | |
dc.identifier.citedreference | Ikeda, K., & Bekkers, J. M. ( 2009 ). Counting the number of releasable synaptic vesicles in a presynaptic terminal. Proceedings of the National Academy of Sciences, 106, 2945 - 2950. https://doi.org/10.1073/pnas.0811017106 | |
dc.identifier.citedreference | Inoue, S., Imamura, A., Okazaki, Y., Yokota, H., Arai, M., Hayashi, N., Furukawa, A., Itokawa, M., & Oishi, M. ( 2007 ). Synaptotagmin XI as a candidate gene for susceptibility to schizophrenia. American Journal of Medical Genetics. Part B, Neuropsychiatric Genetics: The Official Publication of the International Society of Psychiatric Genetics, 144B, 332 - 340. https://doi.org/10.1002/ajmg.b.30465 | |
dc.identifier.citedreference | International Parkinson Disease Genomics Consortium, Nalls, M. A., Plagnol, V., Hernandez, D. G., Sharma, M., Sheerin, U.- M., Saad, M., Simón- Sánchez, J., Schulte, C., Lesage, S., Sveinbjörnsdóttir, S., Stefánsson, K., Martinez, M., Hardy, S., Heutink, P., Brice, A., Gasser, T., Singleton, A. B., & Wood, N. W. ( 2011 ). Imputation of sequence variants for identification of genetic risks for Parkinson’s disease: A meta- analysis of genome- wide association studies. Lancet, 377, 641 - 649. https://doi.org/10.1016/S0140- 6736(10)62345- 8 | |
dc.identifier.citedreference | Kaeser, P. S., & Regehr, W. G. ( 2014 ). Molecular mechanisms for synchronous, asynchronous, and spontaneous neurotransmitter release. Annual Review of Physiology, 76, 333 - 363. https://doi.org/10.1146/annurev- physiol- 021113- 170338 | |
dc.identifier.citedreference | Kavalali, E. T. ( 2015 ). The mechanisms and functions of spontaneous neurotransmitter release. Nature Reviews Neuroscience, 16, 5 - 16. https://doi.org/10.1038/nrn3875 | |
dc.identifier.citedreference | Kavalali, E. T. ( 2018 ). Spontaneous neurotransmission: A form of neural communication comes of age. Journal of Neuroscience Research, 96, 331 - 334. https://doi.org/10.1002/jnr.24207 | |
dc.identifier.citedreference | Kononenko, N. L., & Haucke, V. ( 2012 ). Spontaneous neurotransmission: a SNARE for the rest. Neuron, 73, 3 - 5. https://doi.org/10.1016/j.neuron.2011.12.015 | |
dc.identifier.citedreference | Kullmann, D. M. ( 1994 ). Amplitude fluctuations of dual- component EPSCs in hippocampal pyramidal cells: implications for long- term potentiation. Neuron, 12, 1111 - 1120. https://doi.org/10.1016/0896- 6273(94)90318- 2 | |
dc.identifier.citedreference | Liu, H., Dean, C., Arthur, C. P., Dong, M., & Chapman, E. R. ( 2009 ). Autapses and networks of hippocampal neurons exhibit distinct synaptic transmission phenotypes in the absence of synaptotagmin I. Journal of Neuroscience, 29, 7395 - 7403. https://doi.org/10.1523/JNEUROSCI.1341- 09.2009 | |
dc.identifier.citedreference | Mathew, S. S., Pozzo- Miller, L., & Hablitz, J. J. ( 2008 ). Kainate modulates presynaptic GABA release from two vesicle pools. Journal of Neuroscience, 28, 725 - 731. https://doi.org/10.1523/JNEUROSCI.3625- 07.2008 | |
dc.identifier.citedreference | Maximov, A., Shin, O. H., Liu, X., & Sudhof, T. C. ( 2007 ). Synaptotagmin- 12, a synaptic vesicle phosphoprotein that modulates spontaneous neurotransmitter release. Journal of Cell Biology, 176, 113 - 124. https://doi.org/10.1083/jcb.200607021 | |
dc.identifier.citedreference | Maximov, A., & Sudhof, T. C. ( 2005 ). Autonomous function of synaptotagmin 1 in triggering synchronous release independent of asynchronous release. Neuron, 48, 547 - 554. https://doi.org/10.1016/j.neuron.2005.09.006 | |
dc.identifier.citedreference | Milochau, A., Lagree, V., Benassy, M. N., Chaignepain, S., Papin, J., Garcia- Arcos, I., Lajoix, A., Monterrat, C., Coudert, L., Schmitter, J. M., & Ochoa, B. ( 2014 ). Synaptotagmin 11 interacts with components of the RNA- induced silencing complex RISC in clonal pancreatic beta- cells. FEBS Letters, 588, 2217 - 2222. | |
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dc.owningcollname | Interdisciplinary and Peer-Reviewed |
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