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


Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
19 10 2021
Historique:
received: 09 04 2021
accepted: 18 10 2021
pubmed: 20 10 2021
medline: 20 11 2021
entrez: 19 10 2021
Statut: epublish

Résumé

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.

Identifiants

pubmed: 34665127
doi: 10.7554/eLife.69264
pii: 69264
pmc: PMC8555980
doi:
pii:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIDCD NIH HHS
ID : R01 DC016066
Pays : United States
Organisme : NIDCD NIH HHS
ID : R01 DC006283
Pays : United States
Organisme : NIDCD NIH HHS
ID : R01 DC017166
Pays : United States

Informations de copyright

© 2021, Holmgren et al.

Déclaration de conflit d'intérêts

MH, MR, KH, OS, DK, AI, MW, LS No competing interests declared

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Auteurs

Melanie Holmgren (M)

Department of Otolaryngology, Washington University School of Medicine, St Louis, United States.

Michael E Ravicz (ME)

Eaton-Peabody Laboratory, Massachusetts Eye and Ear, Boston, United States.
Department of Otolaryngology-Head and Neck Surgery, Harvard Medical School, Boston, United States.

Kenneth E Hancock (KE)

Eaton-Peabody Laboratory, Massachusetts Eye and Ear, Boston, United States.
Department of Otolaryngology-Head and Neck Surgery, Harvard Medical School, Boston, United States.

Olga Strelkova (O)

Eaton-Peabody Laboratory, Massachusetts Eye and Ear, Boston, United States.
Department of Otolaryngology-Head and Neck Surgery, Harvard Medical School, Boston, United States.

Dorina Kallogjeri (D)

Department of Otolaryngology, Washington University School of Medicine, St Louis, United States.

Artur A Indzhykulian (AA)

Eaton-Peabody Laboratory, Massachusetts Eye and Ear, Boston, United States.
Department of Otolaryngology-Head and Neck Surgery, Harvard Medical School, Boston, United States.

Mark E Warchol (ME)

Department of Otolaryngology, Washington University School of Medicine, St Louis, United States.
Department of Neuroscience, Washington University School of Medicine, St Louis, United States.

Lavinia Sheets (L)

Department of Otolaryngology, Washington University School of Medicine, St Louis, United States.
Department of Developmental Biology, Washington University School of Medicine, St. Louis, United States.

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