Insulin-like growth factor 1 promotes cochlear synapse regeneration after excitotoxic trauma in vitro

Yamahara, Kohei; Asaka, Nakarin; Kita, Tomoko; Kishimoto, Ippei; Matsunaga, Mami; Yamamoto, Norio; Omori, Koichi; Nakagawa, Takayuki

doi:10.1016/j.heares.2019.01.008

Cited by 30 publications

(36 citation statements)

References 42 publications

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“…In the cochlea, IGF1R is expressed on the surface of OHCs, IHCs, and all supporting cells, including pillar cells, Hensen’s and Claudius’ cells, inner sulcus cells, and Deiters’ cells (Okano et al, 2011 ; Hayashi et al, 2013 ), as well as SGNs (Sanchez-Calderon et al, 2010 ). Our previous study confirmed that IGF1 induced the regeneration of ribbon synapses in cochlear explant cultures of postnatal day (P) two mice (Yamahara et al, 2019 ). In this study, we examined the roles of IGF1 signaling in the maintenance of cochlear ribbon synapses using explant cultures.…”

Section: Introductionsupporting

confidence: 85%

“…JB1 is a highly selective IGF-IR antagonist, which interferes with the efficacy of IGF1 by competitively inhibiting the binding of IGF1 to IGF1R (Pietrzkowski et al, 1992 ). Our previous study demonstrated the efficacy of JB1 in attenuating IGF1-mediated regeneration of ribbon synapses in P2 cochlear explants that had been damaged by excitatory amino acids (Yamahara et al, 2019 ). JB1 has also been used to antagonize IGF1 effects in various organs including the hippocampus (Nelson et al, 2014 ) and retina (Landi et al, 2009 ).…”

Section: Discussionmentioning

confidence: 98%

“…The present results demonstrated that JB1 decreased the number of both presynaptic ribbons and postsynaptic receptor patches in a dose-dependent manner, indicating that IGF1 is an inevitable factor for the maintenance of ribbon synapses in cochlear explants. Our previous study (Yamahara et al, 2019 ) used explant cultures of P2 mouse cochleae, while in the present study, we used P4 mouse cochleae for a couple of reasons. One is the maturation process of ribbon synapses.…”

Section: Discussionmentioning

confidence: 99%

“…Cochlear explant cultures were performed as previously described (Yamahara et al, 2019 ). Briefly, P4 mice were killed with carbon dioxide (CO 2 ), after which they were decapitated.…”

Section: Methodsmentioning

confidence: 99%

“…In an aminoglycoside-induced degeneration model, the protection of cochlear ribbon synapses by the local application of fibroblast growth factor 22 has also been reported (Li et al, 2016 ). Although still controversial (Wagner and Shin, 2019 ), the capacity to regenerate ribbon synapses in the mammalian cochlea was demonstrated in vitro (Wang and Green, 2011 ; Yamahara et al, 2019 ) and in vivo (Wan et al, 2014 ; Suzuki et al, 2016 ).…”

Section: Introductionmentioning

confidence: 99%

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Insulin-Like Growth Factor 1 on the Maintenance of Ribbon Synapses in Mouse Cochlear Explant Cultures

Gao

Kita

Katsuno

et al. 2020

Front. Cell. Neurosci.

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Hearing loss has become one of the most common disabilities worldwide. The synaptic connections between inner hair cells (IHCs) and spiral ganglion neurons have specialized synaptic constructions, termed ribbon synapses, which are important for auditory function. The ribbon synapses in the cochlea are quite vulnerable to various insults. As such, the maintenance of ribbon synapses is important for ensuring hearing function. Insulin-like growth factor 1 (IGF1) plays a critical role in the development and maintenance of the cochlea and has the potential to protect cochlear hair cells from various insults. In this study, we examined the role of IGF1 in the maintenance of ribbon synapses in cochlear explants of postnatal day four mice. We cultured cochlear explants with an IGF1 receptor antagonist, JB1, which is an IGF1 peptide analog. Results showed that exposure to JB1 for 24 h resulted in the loss of ribbon synapses. After an additional 24-h culture without JB1, the number of ribbon synapses spontaneously recovered. The application of exogenous IGF1 showed two different aspects of ribbon synapses. Low doses of exogenous IGF1 promoted the recovery of ribbon synapses, while it compromised the spontaneous recovery of ribbon synapses at high doses. Altogether, these results indicate that the paracrine or autocrine release of IGF1 in the cochlea plays a crucial role in the maintenance of cochlear ribbon synapses.

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Section: Introductionsupporting

confidence: 85%

Section: Discussionmentioning

confidence: 98%

Section: Discussionmentioning

confidence: 99%

“…Cochlear explant cultures were performed as previously described (Yamahara et al, 2019 ). Briefly, P4 mice were killed with carbon dioxide (CO 2 ), after which they were decapitated.…”

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Insulin-Like Growth Factor 1 on the Maintenance of Ribbon Synapses in Mouse Cochlear Explant Cultures

Gao

Kita

Katsuno

et al. 2020

Front. Cell. Neurosci.

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Patterns of Teprotumumab‐Induced Hearing Dysfunction: A Systematic Review

Wong,

Arya,

Salmeron

et al. 2024

Otolaryngol.--head neck surg.

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ObjectiveHearing loss has been reported after administration of the monoclonal antibody teprotumumab. The purpose of this study was to review available evidence regarding the patterns of teprotumumab‐related ototoxicity.Data SourcesPubMed, EMBASE, and Cochrane Library.Review MethodsA systematic review was performed using standardized methodology. Studies were included if they included subjects who were prescribed teprotumumab. Exclusion criteria included non‐English articles, abstracts, letters/commentaries, case reports, and reviews. Subjects without both pre‐ and posttreatment audiometric data were also excluded. Bias was assessed using the Mixed Methods Appraisal Tool.ResultsFrom an initial search of 76 articles, 7 studies reporting on 109 unique patients were included. Four studies were level 4 evidence, 1 study was level 3 evidence, and 2 studies were level 2 evidence. Mean age was 55 ± 14 years with a female predominance (64%). The most commonly reported symptoms were hearing loss (22%), followed by fullness (18%) and tinnitus (14%). In total, 41% of patients with available data met criteria for ototoxicity, all exhibiting shifts in the middle frequencies or higher. Fifteen (14%) patients underwent ultrahigh frequency audiometric testing and 8 (53%, 8/15) demonstrated shifts exclusively in this range.ConclusionOtotoxicity may occur in patients treated with teprotumumab. Hearing loss occurs primarily in higher frequencies, and routine hearing screening with ultrahigh frequency testing may be warranted. The true incidence of ototoxicity with teprotumumab remains unknown, and more data is needed to elucidate underlying mechanisms and develop strategies to minimize risks.

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Hearing loss: The final frontier of pharmacology

Foster

Jacques

Piu

2022

Pharmacology Res & Perspec

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Despite a prevalence greater than cancer or diabetes, there are no currently approved drugs for the treatment of hearing loss. Research over the past two decades has led to a vastly improved understanding of the cellular and molecular mechanisms in the cochlea that lead to hearing deficits and the advent of novel strategies to combat them. Combined with innovative methods that enable local drug delivery to the inner ear, these insights have paved the way for promising therapies that are now under clinical investigation. In this review, we will outline this renaissance of cochlear biology and drug development, focusing on noise, age‐related, and chemotherapy‐induced hearing dysfunction.

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Insulin-like growth factor 1 promotes cochlear synapse regeneration after excitotoxic trauma in vitro

Cited by 30 publications

References 42 publications

Insulin-Like Growth Factor 1 on the Maintenance of Ribbon Synapses in Mouse Cochlear Explant Cultures

Insulin-Like Growth Factor 1 on the Maintenance of Ribbon Synapses in Mouse Cochlear Explant Cultures

Patterns of Teprotumumab‐Induced Hearing Dysfunction: A Systematic Review

Hearing loss: The final frontier of pharmacology

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