Elevated synaptic vesicle release probability in synaptophysin/gyrin family quadruple knockouts
Synaptophysins 1 and 2 and synaptogyrins 1 and 3 constitute a major family of synaptic vesicle membrane proteins. Unlike other widely expressed synaptic vesicle proteins such as vSNAREs and synaptotagmins, the primary function has not been resolved. Here, we report robust elevation in the probabilit...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2019-05-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/40744 |
| _version_ | 1811236812780208128 |
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| author | Mathan K Raja Julia Preobraschenski Sergio Del Olmo-Cabrera Rebeca Martinez-Turrillas Reinhard Jahn Isabel Perez-Otano John F Wesseling |
| author_facet | Mathan K Raja Julia Preobraschenski Sergio Del Olmo-Cabrera Rebeca Martinez-Turrillas Reinhard Jahn Isabel Perez-Otano John F Wesseling |
| author_sort | Mathan K Raja |
| collection | DOAJ |
| description | Synaptophysins 1 and 2 and synaptogyrins 1 and 3 constitute a major family of synaptic vesicle membrane proteins. Unlike other widely expressed synaptic vesicle proteins such as vSNAREs and synaptotagmins, the primary function has not been resolved. Here, we report robust elevation in the probability of release of readily releasable vesicles with both high and low release probabilities at a variety of synapse types from knockout mice missing all four family members. Neither the number of readily releasable vesicles, nor the timing of recruitment to the readily releasable pool was affected. The results suggest that family members serve as negative regulators of neurotransmission, acting directly at the level of exocytosis to dampen connection strength selectively when presynaptic action potentials fire at low frequency. The widespread expression suggests that chemical synapses may play a frequency filtering role in biological computation that is more elemental than presently envisioned.Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (see decision letter). |
| first_indexed | 2024-04-12T12:14:34Z |
| format | Article |
| id | doaj.art-6b102a56568d45b68882ed2b104af202 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T12:14:34Z |
| publishDate | 2019-05-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-6b102a56568d45b68882ed2b104af2022022-12-22T03:33:28ZengeLife Sciences Publications LtdeLife2050-084X2019-05-01810.7554/eLife.40744Elevated synaptic vesicle release probability in synaptophysin/gyrin family quadruple knockoutsMathan K Raja0https://orcid.org/0000-0001-7727-6994Julia Preobraschenski1Sergio Del Olmo-Cabrera2Rebeca Martinez-Turrillas3Reinhard Jahn4https://orcid.org/0000-0003-1542-3498Isabel Perez-Otano5John F Wesseling6https://orcid.org/0000-0002-7565-2594Department of Neuroscience, Universidad de Navarra, Pamplona, SpainDepartment of Neurobiology, Max Planck Institute for Biophysical Chemistry, Göttingen, GermanyInstitute for Neurosciences CSIC-UMH, San Juan de Alicante, SpainDepartment of Neuroscience, Universidad de Navarra, Pamplona, SpainDepartment of Neurobiology, Max Planck Institute for Biophysical Chemistry, Göttingen, GermanyDepartment of Neuroscience, Universidad de Navarra, Pamplona, Spain; Institute for Neurosciences CSIC-UMH, San Juan de Alicante, SpainDepartment of Neuroscience, Universidad de Navarra, Pamplona, Spain; Institute for Neurosciences CSIC-UMH, San Juan de Alicante, SpainSynaptophysins 1 and 2 and synaptogyrins 1 and 3 constitute a major family of synaptic vesicle membrane proteins. Unlike other widely expressed synaptic vesicle proteins such as vSNAREs and synaptotagmins, the primary function has not been resolved. Here, we report robust elevation in the probability of release of readily releasable vesicles with both high and low release probabilities at a variety of synapse types from knockout mice missing all four family members. Neither the number of readily releasable vesicles, nor the timing of recruitment to the readily releasable pool was affected. The results suggest that family members serve as negative regulators of neurotransmission, acting directly at the level of exocytosis to dampen connection strength selectively when presynaptic action potentials fire at low frequency. The widespread expression suggests that chemical synapses may play a frequency filtering role in biological computation that is more elemental than presently envisioned.Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (see decision letter).https://elifesciences.org/articles/40744vesicleRRPshort-term plasticitySTP |
| spellingShingle | Mathan K Raja Julia Preobraschenski Sergio Del Olmo-Cabrera Rebeca Martinez-Turrillas Reinhard Jahn Isabel Perez-Otano John F Wesseling Elevated synaptic vesicle release probability in synaptophysin/gyrin family quadruple knockouts eLife vesicle RRP short-term plasticity STP |
| title | Elevated synaptic vesicle release probability in synaptophysin/gyrin family quadruple knockouts |
| title_full | Elevated synaptic vesicle release probability in synaptophysin/gyrin family quadruple knockouts |
| title_fullStr | Elevated synaptic vesicle release probability in synaptophysin/gyrin family quadruple knockouts |
| title_full_unstemmed | Elevated synaptic vesicle release probability in synaptophysin/gyrin family quadruple knockouts |
| title_short | Elevated synaptic vesicle release probability in synaptophysin/gyrin family quadruple knockouts |
| title_sort | elevated synaptic vesicle release probability in synaptophysin gyrin family quadruple knockouts |
| topic | vesicle RRP short-term plasticity STP |
| url | https://elifesciences.org/articles/40744 |
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