Mechanical overstimulation causes acute injury and synapse loss followed by fast recovery in lateral-line neuromasts of larval zebrafish

Excess noise damages sensory hair cells, resulting in loss of synaptic connections with auditory nerves and, in some cases, hair-cell death. The cellular mechanisms underlying mechanically induced hair-cell damage and subsequent repair are not completely understood. Hair cells in neuromasts of larva...

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Autores principales:	Melanie Holmgren, Michael E Ravicz, Kenneth E Hancock, Olga Strelkova, Dorina Kallogjeri, Artur A Indzhykulian, Mark E Warchol, Lavinia Sheets
Formato:	article
Lenguaje:	EN
Publicado:	eLife Sciences Publications Ltd 2021
Materias:	mechanical damage hair cell ribbon synapse inflammation repair Medicine R Science Q Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/054f1334e50d48d3b96da9188ffa6f0f
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spelling	oai:doaj.org-article:054f1334e50d48d3b96da9188ffa6f0f2021-11-26T11:14:27ZMechanical overstimulation causes acute injury and synapse loss followed by fast recovery in lateral-line neuromasts of larval zebrafish10.7554/eLife.692642050-084Xe69264https://doaj.org/article/054f1334e50d48d3b96da9188ffa6f0f2021-10-01T00:00:00Zhttps://elifesciences.org/articles/69264https://doaj.org/toc/2050-084XExcess noise damages sensory hair cells, resulting in loss of synaptic connections with auditory nerves and, in some cases, hair-cell death. The cellular mechanisms underlying mechanically induced hair-cell damage and subsequent repair are not completely understood. Hair cells in neuromasts of larval zebrafish are structurally and functionally comparable to mammalian hair cells but undergo robust regeneration following ototoxic damage. We therefore developed a model for mechanically induced hair-cell damage in this highly tractable system. Free swimming larvae exposed to strong water wave stimulus for 2 hr displayed mechanical injury to neuromasts, including afferent neurite retraction, damaged hair bundles, and reduced mechanotransduction. Synapse loss was observed in apparently intact exposed neuromasts, and this loss was exacerbated by inhibiting glutamate uptake. Mechanical damage also elicited an inflammatory response and macrophage recruitment. Remarkably, neuromast hair-cell morphology and mechanotransduction recovered within hours following exposure, suggesting severely damaged neuromasts undergo repair. Our results indicate functional changes and synapse loss in mechanically damaged lateral-line neuromasts that share key features of damage observed in noise-exposed mammalian ear. Yet, unlike the mammalian ear, mechanical damage to neuromasts is rapidly reversible.Melanie HolmgrenMichael E RaviczKenneth E HancockOlga StrelkovaDorina KallogjeriArtur A IndzhykulianMark E WarcholLavinia SheetseLife Sciences Publications Ltdarticlemechanical damagehair cellribbon synapseinflammationrepairMedicineRScienceQBiology (General)QH301-705.5ENeLife, Vol 10 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	mechanical damage hair cell ribbon synapse inflammation repair Medicine R Science Q Biology (General) QH301-705.5
spellingShingle	mechanical damage hair cell ribbon synapse inflammation repair Medicine R Science Q Biology (General) QH301-705.5 Melanie Holmgren Michael E Ravicz Kenneth E Hancock Olga Strelkova Dorina Kallogjeri Artur A Indzhykulian Mark E Warchol Lavinia Sheets Mechanical overstimulation causes acute injury and synapse loss followed by fast recovery in lateral-line neuromasts of larval zebrafish
description	Excess noise damages sensory hair cells, resulting in loss of synaptic connections with auditory nerves and, in some cases, hair-cell death. The cellular mechanisms underlying mechanically induced hair-cell damage and subsequent repair are not completely understood. Hair cells in neuromasts of larval zebrafish are structurally and functionally comparable to mammalian hair cells but undergo robust regeneration following ototoxic damage. We therefore developed a model for mechanically induced hair-cell damage in this highly tractable system. Free swimming larvae exposed to strong water wave stimulus for 2 hr displayed mechanical injury to neuromasts, including afferent neurite retraction, damaged hair bundles, and reduced mechanotransduction. Synapse loss was observed in apparently intact exposed neuromasts, and this loss was exacerbated by inhibiting glutamate uptake. Mechanical damage also elicited an inflammatory response and macrophage recruitment. Remarkably, neuromast hair-cell morphology and mechanotransduction recovered within hours following exposure, suggesting severely damaged neuromasts undergo repair. Our results indicate functional changes and synapse loss in mechanically damaged lateral-line neuromasts that share key features of damage observed in noise-exposed mammalian ear. Yet, unlike the mammalian ear, mechanical damage to neuromasts is rapidly reversible.
format	article
author	Melanie Holmgren Michael E Ravicz Kenneth E Hancock Olga Strelkova Dorina Kallogjeri Artur A Indzhykulian Mark E Warchol Lavinia Sheets
author_facet	Melanie Holmgren Michael E Ravicz Kenneth E Hancock Olga Strelkova Dorina Kallogjeri Artur A Indzhykulian Mark E Warchol Lavinia Sheets
author_sort	Melanie Holmgren
title	Mechanical overstimulation causes acute injury and synapse loss followed by fast recovery in lateral-line neuromasts of larval zebrafish
title_short	Mechanical overstimulation causes acute injury and synapse loss followed by fast recovery in lateral-line neuromasts of larval zebrafish
title_full	Mechanical overstimulation causes acute injury and synapse loss followed by fast recovery in lateral-line neuromasts of larval zebrafish
title_fullStr	Mechanical overstimulation causes acute injury and synapse loss followed by fast recovery in lateral-line neuromasts of larval zebrafish
title_full_unstemmed	Mechanical overstimulation causes acute injury and synapse loss followed by fast recovery in lateral-line neuromasts of larval zebrafish
title_sort	mechanical overstimulation causes acute injury and synapse loss followed by fast recovery in lateral-line neuromasts of larval zebrafish
publisher	eLife Sciences Publications Ltd
publishDate	2021
url	https://doaj.org/article/054f1334e50d48d3b96da9188ffa6f0f
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Mechanical overstimulation causes acute injury and synapse loss followed by fast recovery in lateral-line neuromasts of larval zebrafish

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