Temporal and spatial assembly of inner ear hair cell ankle link condensate through phase separation
Stereocilia are actin-based cell protrusions of inner ear hair cells and are indispensable for mechanotransduction. Ankle links connect the ankle region of developing stereocilia, playing an essential role in stereocilia development. WHRN, PDZD7, ADGRV1 and USH2A have been identified to form the so-...
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| Published in | Nature communications Vol. 14; no. 1; pp. 1657 - 15 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
24.03.2023
Nature Publishing Group Nature Portfolio |
| Subjects | |
| Online Access | Get full text |
| ISSN | 2041-1723 2041-1723 |
| DOI | 10.1038/s41467-023-37267-5 |
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| Abstract | Stereocilia are actin-based cell protrusions of inner ear hair cells and are indispensable for mechanotransduction. Ankle links connect the ankle region of developing stereocilia, playing an essential role in stereocilia development. WHRN, PDZD7, ADGRV1 and USH2A have been identified to form the so-called ankle link complex (ALC); however, the detailed mechanism underlying the temporal emergence and degeneration of ankle links remains elusive. Here we show that WHRN and PDZD7 orchestrate ADGRV1 and USH2A to assemble the ALC through liquid-liquid phase separation (LLPS). Disruption of the ALC multivalency for LLPS largely abolishes the distribution of WHRN at the ankle region of stereocilia. Interestingly, high concentration of ADGRV1 inhibits LLPS, providing a potential mechanism for ALC disassembly. Moreover, certain deafness mutations of ALC genes weaken the multivalent interactions of ALC and impair LLPS. In conclusion, our study demonstrates that LLPS mediates ALC formation, providing essential clues for understanding the pathogenesis of deafness.
In this work, the authors demonstrate that LLPS of the quaternary USH2 protein complex initiates the formation of stereociliary ankle link condensates, providing insights into the pathogenesis of deafness. |
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| AbstractList | In this work, the authors demonstrate that LLPS of the quaternary USH2 protein complex initiates the formation of stereociliary ankle link condensates, providing insights into the pathogenesis of deafness. Stereocilia are actin-based cell protrusions of inner ear hair cells and are indispensable for mechanotransduction. Ankle links connect the ankle region of developing stereocilia, playing an essential role in stereocilia development. WHRN, PDZD7, ADGRV1 and USH2A have been identified to form the so-called ankle link complex (ALC); however, the detailed mechanism underlying the temporal emergence and degeneration of ankle links remains elusive. Here we show that WHRN and PDZD7 orchestrate ADGRV1 and USH2A to assemble the ALC through liquid-liquid phase separation (LLPS). Disruption of the ALC multivalency for LLPS largely abolishes the distribution of WHRN at the ankle region of stereocilia. Interestingly, high concentration of ADGRV1 inhibits LLPS, providing a potential mechanism for ALC disassembly. Moreover, certain deafness mutations of ALC genes weaken the multivalent interactions of ALC and impair LLPS. In conclusion, our study demonstrates that LLPS mediates ALC formation, providing essential clues for understanding the pathogenesis of deafness. In this work, the authors demonstrate that LLPS of the quaternary USH2 protein complex initiates the formation of stereociliary ankle link condensates, providing insights into the pathogenesis of deafness. Stereocilia are actin-based cell protrusions of inner ear hair cells and are indispensable for mechanotransduction. Ankle links connect the ankle region of developing stereocilia, playing an essential role in stereocilia development. WHRN, PDZD7, ADGRV1 and USH2A have been identified to form the so-called ankle link complex (ALC); however, the detailed mechanism underlying the temporal emergence and degeneration of ankle links remains elusive. Here we show that WHRN and PDZD7 orchestrate ADGRV1 and USH2A to assemble the ALC through liquid-liquid phase separation (LLPS). Disruption of the ALC multivalency for LLPS largely abolishes the distribution of WHRN at the ankle region of stereocilia. Interestingly, high concentration of ADGRV1 inhibits LLPS, providing a potential mechanism for ALC disassembly. Moreover, certain deafness mutations of ALC genes weaken the multivalent interactions of ALC and impair LLPS. In conclusion, our study demonstrates that LLPS mediates ALC formation, providing essential clues for understanding the pathogenesis of deafness. Stereocilia are actin-based cell protrusions of inner ear hair cells and are indispensable for mechanotransduction. Ankle links connect the ankle region of developing stereocilia, playing an essential role in stereocilia development. WHRN, PDZD7, ADGRV1 and USH2A have been identified to form the so-called ankle link complex (ALC); however, the detailed mechanism underlying the temporal emergence and degeneration of ankle links remains elusive. Here we show that WHRN and PDZD7 orchestrate ADGRV1 and USH2A to assemble the ALC through liquid-liquid phase separation (LLPS). Disruption of the ALC multivalency for LLPS largely abolishes the distribution of WHRN at the ankle region of stereocilia. Interestingly, high concentration of ADGRV1 inhibits LLPS, providing a potential mechanism for ALC disassembly. Moreover, certain deafness mutations of ALC genes weaken the multivalent interactions of ALC and impair LLPS. In conclusion, our study demonstrates that LLPS mediates ALC formation, providing essential clues for understanding the pathogenesis of deafness.In this work, the authors demonstrate that LLPS of the quaternary USH2 protein complex initiates the formation of stereociliary ankle link condensates, providing insights into the pathogenesis of deafness. Stereocilia are actin-based cell protrusions of inner ear hair cells and are indispensable for mechanotransduction. Ankle links connect the ankle region of developing stereocilia, playing an essential role in stereocilia development. WHRN, PDZD7, ADGRV1 and USH2A have been identified to form the so-called ankle link complex (ALC); however, the detailed mechanism underlying the temporal emergence and degeneration of ankle links remains elusive. Here we show that WHRN and PDZD7 orchestrate ADGRV1 and USH2A to assemble the ALC through liquid-liquid phase separation (LLPS). Disruption of the ALC multivalency for LLPS largely abolishes the distribution of WHRN at the ankle region of stereocilia. Interestingly, high concentration of ADGRV1 inhibits LLPS, providing a potential mechanism for ALC disassembly. Moreover, certain deafness mutations of ALC genes weaken the multivalent interactions of ALC and impair LLPS. In conclusion, our study demonstrates that LLPS mediates ALC formation, providing essential clues for understanding the pathogenesis of deafness.Stereocilia are actin-based cell protrusions of inner ear hair cells and are indispensable for mechanotransduction. Ankle links connect the ankle region of developing stereocilia, playing an essential role in stereocilia development. WHRN, PDZD7, ADGRV1 and USH2A have been identified to form the so-called ankle link complex (ALC); however, the detailed mechanism underlying the temporal emergence and degeneration of ankle links remains elusive. Here we show that WHRN and PDZD7 orchestrate ADGRV1 and USH2A to assemble the ALC through liquid-liquid phase separation (LLPS). Disruption of the ALC multivalency for LLPS largely abolishes the distribution of WHRN at the ankle region of stereocilia. Interestingly, high concentration of ADGRV1 inhibits LLPS, providing a potential mechanism for ALC disassembly. Moreover, certain deafness mutations of ALC genes weaken the multivalent interactions of ALC and impair LLPS. In conclusion, our study demonstrates that LLPS mediates ALC formation, providing essential clues for understanding the pathogenesis of deafness. |
| ArticleNumber | 1657 |
| Author | Wei, Xiaoxi Wu, Hao Xu, Zhigang Du, Tingting Du, Haibo Wang, Huang Ren, Rui Feng, Zhe Dong, Tingting Lin, Lin Wang, Hongyang Sun, Jin-Peng Zhao, Dange Zhai, Xiaoyan Lu, Qing |
| Author_xml | – sequence: 1 givenname: Huang surname: Wang fullname: Wang, Huang organization: Key Laboratory for the Genetics of Developmental and Neuropsychiatric Disorders, Ministry of Education, Bio-X Institutes, Shanghai Jiao Tong University – sequence: 2 givenname: Haibo surname: Du fullname: Du, Haibo organization: Shandong Provincial Key Laboratory of Animal Cell and Developmental Biology, School of Life Sciences, Shandong University, Air Force Medical Center, PLA – sequence: 3 givenname: Rui surname: Ren fullname: Ren, Rui organization: Shandong Provincial Key Laboratory of Animal Cell and Developmental Biology, School of Life Sciences, Shandong University – sequence: 4 givenname: Tingting surname: Du fullname: Du, Tingting organization: Department of Otolaryngology-Head and Neck Surgery, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China. Ear Institute, Shanghai Jiao Tong University School of Medicine, Shanghai, China. Shanghai Key Laboratory of Translational Medicine on Ear and Nose Diseases – sequence: 5 givenname: Lin surname: Lin fullname: Lin, Lin organization: Key Laboratory for the Genetics of Developmental and Neuropsychiatric Disorders, Ministry of Education, Bio-X Institutes, Shanghai Jiao Tong University – sequence: 6 givenname: Zhe surname: Feng fullname: Feng, Zhe organization: School of Life Sciences, Fudan University – sequence: 7 givenname: Dange surname: Zhao fullname: Zhao, Dange organization: Key Laboratory for the Genetics of Developmental and Neuropsychiatric Disorders, Ministry of Education, Bio-X Institutes, Shanghai Jiao Tong University – sequence: 8 givenname: Xiaoxi surname: Wei fullname: Wei, Xiaoxi organization: Key Laboratory for the Genetics of Developmental and Neuropsychiatric Disorders, Ministry of Education, Bio-X Institutes, Shanghai Jiao Tong University – sequence: 9 givenname: Xiaoyan surname: Zhai fullname: Zhai, Xiaoyan organization: Shandong Provincial Key Laboratory of Animal Cell and Developmental Biology, School of Life Sciences, Shandong University – sequence: 10 givenname: Hongyang surname: Wang fullname: Wang, Hongyang organization: College of Otolaryngology, Head and Neck Surgery, Department of Audiology and Vestibular Medicine, Chinese PLA Institute of Otolaryngology, Chinese PLA General Hospital, Medical School of Chinese PLA, 28 Fuxing Road, National Clinical Research Center for Otolaryngologic Diseases, Chinese PLA General Hospital, Medical School of Chinese PLA – sequence: 11 givenname: Tingting surname: Dong fullname: Dong, Tingting organization: Department of Otolaryngology-Head and Neck Surgery, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China. Ear Institute, Shanghai Jiao Tong University School of Medicine, Shanghai, China. Shanghai Key Laboratory of Translational Medicine on Ear and Nose Diseases – sequence: 12 givenname: Jin-Peng surname: Sun fullname: Sun, Jin-Peng organization: Key Laboratory Experimental Teratology of the Ministry of Education, Department of Biochemistry and Molecular Biology, School of Basic Medical Sciences, Cheeloo College of Medicine, Shandong University – sequence: 13 givenname: Hao orcidid: 0000-0002-5317-902X surname: Wu fullname: Wu, Hao organization: Department of Otolaryngology-Head and Neck Surgery, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China. Ear Institute, Shanghai Jiao Tong University School of Medicine, Shanghai, China. Shanghai Key Laboratory of Translational Medicine on Ear and Nose Diseases – sequence: 14 givenname: Zhigang orcidid: 0000-0003-0082-7297 surname: Xu fullname: Xu, Zhigang email: xuzg@sdu.edu.cn organization: Shandong Provincial Key Laboratory of Animal Cell and Developmental Biology, School of Life Sciences, Shandong University, Shandong Provincial Collaborative Innovation Center of Cell Biology, Shandong Normal University – sequence: 15 givenname: Qing orcidid: 0000-0002-6956-3333 surname: Lu fullname: Lu, Qing email: luqing67@sjtu.edu.cn organization: Key Laboratory for the Genetics of Developmental and Neuropsychiatric Disorders, Ministry of Education, Bio-X Institutes, Shanghai Jiao Tong University, Department of Otolaryngology-Head and Neck Surgery, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China. Ear Institute, Shanghai Jiao Tong University School of Medicine, Shanghai, China. Shanghai Key Laboratory of Translational Medicine on Ear and Nose Diseases, Bio-X-Renji Hospital Research Center, School of Medicine, Renji Hospital, Shanghai Jiao Tong University |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36964137$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_3389_fcell_2023_1199069 crossref_primary_10_3390_antiox13050598 crossref_primary_10_1016_j_bbcan_2024_189206 crossref_primary_10_3389_fauot_2024_1423853 crossref_primary_10_1007_s11427_024_2661_3 crossref_primary_10_1038_s41467_024_52580_3 crossref_primary_10_1021_acsnano_4c07514 |
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| Snippet | Stereocilia are actin-based cell protrusions of inner ear hair cells and are indispensable for mechanotransduction. Ankle links connect the ankle region of... In this work, the authors demonstrate that LLPS of the quaternary USH2 protein complex initiates the formation of stereociliary ankle link condensates,... |
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| SubjectTerms | 14/19 631/136/1425 631/45/612 692/699 82/16 82/29 82/80 82/83 Actin Ankle Carrier Proteins - metabolism Condensates Deafness Degeneration Ear Hair Hair - metabolism Hair cells Hair Cells, Auditory - metabolism Humanities and Social Sciences Humans Inner ear Liquid phases Mechanotransduction Mechanotransduction, Cellular multidisciplinary Pathogenesis Phase separation Science Science (multidisciplinary) Stereocilia - metabolism USH2A protein Usher Syndromes - genetics |
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| Title | Temporal and spatial assembly of inner ear hair cell ankle link condensate through phase separation |
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