Cochlear ribbon synapse maturation requires Nlgn1 and Nlgn3
Summary: Hearing depends on precise synaptic transmission between cochlear inner hair cells and spiral ganglion neurons through afferent ribbon synapses.Neuroligins (Nlgns) facilitate synapse maturation in the brain, but they have gone unstudied in the cochlea. We report Nlgn3 and Nlgn1 knockout (KO...
| Main Authors: | , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2022-08-01
|
| Series: | iScience |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2589004222010756 |
| _version_ | 1828149877837660160 |
|---|---|
| author | Miguel A. Ramirez Yuzuru Ninoyu Cayla Miller Leonardo R. Andrade Seby Edassery Ewa Bomba-Warczak Briana Ortega Uri Manor Mark A. Rutherford Rick A. Friedman Jeffrey N. Savas |
| author_facet | Miguel A. Ramirez Yuzuru Ninoyu Cayla Miller Leonardo R. Andrade Seby Edassery Ewa Bomba-Warczak Briana Ortega Uri Manor Mark A. Rutherford Rick A. Friedman Jeffrey N. Savas |
| author_sort | Miguel A. Ramirez |
| collection | DOAJ |
| description | Summary: Hearing depends on precise synaptic transmission between cochlear inner hair cells and spiral ganglion neurons through afferent ribbon synapses.Neuroligins (Nlgns) facilitate synapse maturation in the brain, but they have gone unstudied in the cochlea. We report Nlgn3 and Nlgn1 knockout (KO) cochleae have fewer ribbon synapses and have impaired hearing. Nlgn3 KO is more vulnerable to noise trauma with limited activity at high frequencies one day after noise. Furthermore, Nlgn3 KO cochleae have a 5-fold reduction in synapse number compared to wild type after two weeks of recovery. Double KO cochlear phenotypes are more prominent than the KOs, for example, 5-fold smaller synapses, 25% reduction in synapse density, and 30% less synaptic output. These observations indicate Nlgn3 and Nlgn1 are essential to cochlear ribbon synapse maturation and function. |
| first_indexed | 2024-04-11T21:35:34Z |
| format | Article |
| id | doaj.art-2d83c1d5d98a4ed9a50479488748c93e |
| institution | Directory Open Access Journal |
| issn | 2589-0042 |
| language | English |
| last_indexed | 2024-04-11T21:35:34Z |
| publishDate | 2022-08-01 |
| publisher | Elsevier |
| record_format | Article |
| series | iScience |
| spelling | doaj.art-2d83c1d5d98a4ed9a50479488748c93e2022-12-22T04:01:45ZengElsevieriScience2589-00422022-08-01258104803Cochlear ribbon synapse maturation requires Nlgn1 and Nlgn3Miguel A. Ramirez0Yuzuru Ninoyu1Cayla Miller2Leonardo R. Andrade3Seby Edassery4Ewa Bomba-Warczak5Briana Ortega6Uri Manor7Mark A. Rutherford8Rick A. Friedman9Jeffrey N. Savas10Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USADivision of Otolaryngology, Department of Surgery, University of California, San Diego, 9500 Gilman Drive, Mail Code 0666, La Jolla, CA 92093, USAWaitt Advanced Biophotonics Core, Salk Institute for Biological Studies, 10010 N. Torrey Pines Road, La Jolla, CA 92037, USAWaitt Advanced Biophotonics Core, Salk Institute for Biological Studies, 10010 N. Torrey Pines Road, La Jolla, CA 92037, USADepartment of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USADepartment of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USADivision of Otolaryngology, Department of Surgery, University of California, San Diego, 9500 Gilman Drive, Mail Code 0666, La Jolla, CA 92093, USAWaitt Advanced Biophotonics Core, Salk Institute for Biological Studies, 10010 N. Torrey Pines Road, La Jolla, CA 92037, USADepartment of Otolaryngology, Washington University in St. Louis School of Medicine, St. Louis, MO, USADivision of Otolaryngology, Department of Surgery, University of California, San Diego, 9500 Gilman Drive, Mail Code 0666, La Jolla, CA 92093, USADepartment of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA; Corresponding authorSummary: Hearing depends on precise synaptic transmission between cochlear inner hair cells and spiral ganglion neurons through afferent ribbon synapses.Neuroligins (Nlgns) facilitate synapse maturation in the brain, but they have gone unstudied in the cochlea. We report Nlgn3 and Nlgn1 knockout (KO) cochleae have fewer ribbon synapses and have impaired hearing. Nlgn3 KO is more vulnerable to noise trauma with limited activity at high frequencies one day after noise. Furthermore, Nlgn3 KO cochleae have a 5-fold reduction in synapse number compared to wild type after two weeks of recovery. Double KO cochlear phenotypes are more prominent than the KOs, for example, 5-fold smaller synapses, 25% reduction in synapse density, and 30% less synaptic output. These observations indicate Nlgn3 and Nlgn1 are essential to cochlear ribbon synapse maturation and function.http://www.sciencedirect.com/science/article/pii/S2589004222010756genomicsneurosciencecellular neurosciencesensory neuroscience |
| spellingShingle | Miguel A. Ramirez Yuzuru Ninoyu Cayla Miller Leonardo R. Andrade Seby Edassery Ewa Bomba-Warczak Briana Ortega Uri Manor Mark A. Rutherford Rick A. Friedman Jeffrey N. Savas Cochlear ribbon synapse maturation requires Nlgn1 and Nlgn3 iScience genomics neuroscience cellular neuroscience sensory neuroscience |
| title | Cochlear ribbon synapse maturation requires Nlgn1 and Nlgn3 |
| title_full | Cochlear ribbon synapse maturation requires Nlgn1 and Nlgn3 |
| title_fullStr | Cochlear ribbon synapse maturation requires Nlgn1 and Nlgn3 |
| title_full_unstemmed | Cochlear ribbon synapse maturation requires Nlgn1 and Nlgn3 |
| title_short | Cochlear ribbon synapse maturation requires Nlgn1 and Nlgn3 |
| title_sort | cochlear ribbon synapse maturation requires nlgn1 and nlgn3 |
| topic | genomics neuroscience cellular neuroscience sensory neuroscience |
| url | http://www.sciencedirect.com/science/article/pii/S2589004222010756 |
| work_keys_str_mv | AT miguelaramirez cochlearribbonsynapsematurationrequiresnlgn1andnlgn3 AT yuzuruninoyu cochlearribbonsynapsematurationrequiresnlgn1andnlgn3 AT caylamiller cochlearribbonsynapsematurationrequiresnlgn1andnlgn3 AT leonardorandrade cochlearribbonsynapsematurationrequiresnlgn1andnlgn3 AT sebyedassery cochlearribbonsynapsematurationrequiresnlgn1andnlgn3 AT ewabombawarczak cochlearribbonsynapsematurationrequiresnlgn1andnlgn3 AT brianaortega cochlearribbonsynapsematurationrequiresnlgn1andnlgn3 AT urimanor cochlearribbonsynapsematurationrequiresnlgn1andnlgn3 AT markarutherford cochlearribbonsynapsematurationrequiresnlgn1andnlgn3 AT rickafriedman cochlearribbonsynapsematurationrequiresnlgn1andnlgn3 AT jeffreynsavas cochlearribbonsynapsematurationrequiresnlgn1andnlgn3 |