TRIOBP-5 sculpts stereocilia rootlets and stiffens supporting cells enabling hearing.


Journal

JCI insight
ISSN: 2379-3708
Titre abrégé: JCI Insight
Pays: United States
ID NLM: 101676073

Informations de publication

Date de publication:
20 06 2019
Historique:
received: 04 03 2019
accepted: 08 05 2019
entrez: 21 6 2019
pubmed: 21 6 2019
medline: 25 8 2020
Statut: epublish

Résumé

TRIOBP remodels the cytoskeleton by forming unusually dense F-actin bundles and is implicated in human cancer, schizophrenia, and deafness. Mutations ablating human and mouse TRIOBP-4 and TRIOBP-5 isoforms are associated with profound deafness, as inner ear mechanosensory hair cells degenerate after stereocilia rootlets fail to develop. However, the mechanisms regulating formation of stereocilia rootlets by each TRIOBP isoform remain unknown. Using 3 new Triobp mouse models, we report that TRIOBP-5 is essential for thickening bundles of F-actin in rootlets, establishing their mature dimensions and for stiffening supporting cells of the auditory sensory epithelium. The coiled-coil domains of this isoform are required for reinforcement and maintenance of stereocilia rootlets. A loss of TRIOBP-5 in mouse results in dysmorphic rootlets that are abnormally thin in the cuticular plate but have increased widths and lengths within stereocilia cores, and causes progressive deafness recapitulating the human phenotype. Our study extends the current understanding of TRIOBP isoform-specific functions necessary for life-long hearing, with implications for insight into other TRIOBPopathies.

Identifiants

pubmed: 31217345
pii: 128561
doi: 10.1172/jci.insight.128561
pmc: PMC6629139
doi:
pii:

Substances chimiques

Actins 0
Microfilament Proteins 0
Protein Isoforms 0
TRIOBP protein, mouse 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Intramural NIH HHS
ID : ZIC DC000081
Pays : United States
Organisme : NIDCD NIH HHS
ID : R01 DC014658
Pays : United States
Organisme : Intramural NIH HHS
ID : ZIA MH002946
Pays : United States
Organisme : NIDCD NIH HHS
ID : T32 DC000039
Pays : United States
Organisme : Intramural NIH HHS
ID : Z01 DC000039
Pays : United States

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Auteurs

Tatsuya Katsuno (T)

Department of Otolaryngology-Head and Neck Surgery, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Inna A Belyantseva (IA)

Laboratory of Molecular Genetics, National Institute on Deafness and Other Communication Disorders, NIH, Bethesda, Maryland, USA.

Alexander X Cartagena-Rivera (AX)

Section on Auditory Mechanics, National Institute on Deafness and Other Communication Disorders, NIH, Bethesda, Maryland, USA.

Keisuke Ohta (K)

Advanced Imaging Research Center, Kurume University School of Medicine, Kurume, Japan.

Shawn M Crump (SM)

Department of Physiology, University of Kentucky, Lexington, Kentucky, USA.

Ronald S Petralia (RS)

Advanced Imaging Core, National Institute on Deafness and Other Communication Disorders, NIH, Bethesda, Maryland, USA.

Kazuya Ono (K)

Department of Otolaryngology-Head and Neck Surgery, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Risa Tona (R)

Department of Otolaryngology-Head and Neck Surgery, Kyoto University Graduate School of Medicine, Kyoto, Japan.
Laboratory of Molecular Genetics, National Institute on Deafness and Other Communication Disorders, NIH, Bethesda, Maryland, USA.

Ayesha Imtiaz (A)

Laboratory of Molecular Genetics, National Institute on Deafness and Other Communication Disorders, NIH, Bethesda, Maryland, USA.

Atteeq Rehman (A)

Laboratory of Molecular Genetics, National Institute on Deafness and Other Communication Disorders, NIH, Bethesda, Maryland, USA.

Hiroshi Kiyonari (H)

Laboratory for Animal Resources and Genetic Engineering, Riken Center for Biosystems Dynamics Research, Kobe, Japan.

Mari Kaneko (M)

Laboratory for Animal Resources and Genetic Engineering, Riken Center for Biosystems Dynamics Research, Kobe, Japan.

Ya-Xian Wang (YX)

Advanced Imaging Core, National Institute on Deafness and Other Communication Disorders, NIH, Bethesda, Maryland, USA.

Takaya Abe (T)

Laboratory for Animal Resources and Genetic Engineering, Riken Center for Biosystems Dynamics Research, Kobe, Japan.

Makoto Ikeya (M)

Department of Clinical Application, Center for iPS Cell Research and Application, Kyoto University, Kyoto, Japan.

Cristina Fenollar-Ferrer (C)

Laboratory of Molecular Genetics, National Institute on Deafness and Other Communication Disorders, NIH, Bethesda, Maryland, USA.
Laboratory of Molecular and Cellular Neurobiology, National Institute of Mental Health, NIH, Bethesda, Maryland, USA.

Gavin P Riordan (GP)

Laboratory of Molecular Genetics, National Institute on Deafness and Other Communication Disorders, NIH, Bethesda, Maryland, USA.

Elisabeth A Wilson (EA)

Laboratory of Molecular Genetics, National Institute on Deafness and Other Communication Disorders, NIH, Bethesda, Maryland, USA.

Tracy S Fitzgerald (TS)

Mouse Auditory Testing Core Facility, National Institute on Deafness and Other Communication Disorders, NIH, Bethesda, Maryland, USA.

Kohei Segawa (K)

Department of Otolaryngology-Head and Neck Surgery, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Koichi Omori (K)

Department of Otolaryngology-Head and Neck Surgery, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Juichi Ito (J)

Department of Otolaryngology-Head and Neck Surgery, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Gregory I Frolenkov (GI)

Department of Physiology, University of Kentucky, Lexington, Kentucky, USA.

Thomas B Friedman (TB)

Laboratory of Molecular Genetics, National Institute on Deafness and Other Communication Disorders, NIH, Bethesda, Maryland, USA.

Shin-Ichiro Kitajiri (SI)

Department of Otolaryngology-Head and Neck Surgery, Kyoto University Graduate School of Medicine, Kyoto, Japan.
Department of Otorhinolaryngology, Shinshu University School of Medicine, Matsumoto, Japan.

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