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Research Articles, Cellular/Molecular

CIB2 and CIB3 Regulate Stereocilia Maintenance and Mechanoelectrical Transduction in Mouse Vestibular Hair Cells

Xiaoying Wang, Shuang Liu, Qi Cheng, Chengli Qu, Rui Ren, Haibo Du, Nana Li, Keji Yan, Yanfei Wang, Wei Xiong and Zhigang Xu
Journal of Neuroscience 3 May 2023, 43 (18) 3219-3231; DOI: https://doi.org/10.1523/JNEUROSCI.1807-22.2023
Xiaoying Wang
1Shandong Provincial Key Laboratory of Animal Cells and Developmental Biology and Key Laboratory for Experimental Teratology of the Ministry of Education, School of Life Sciences, Shandong University, Qingdao, Shandong 266237, People's Republic of China
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Shuang Liu
2School of Life Sciences, IDG/McGovern Institute for Brain Research, Tsinghua University, Beijing 100084, People's Republic of China
3Chinese Institute for Brain Research, Beijing 102206, People's Republic of China
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Qi Cheng
1Shandong Provincial Key Laboratory of Animal Cells and Developmental Biology and Key Laboratory for Experimental Teratology of the Ministry of Education, School of Life Sciences, Shandong University, Qingdao, Shandong 266237, People's Republic of China
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Chengli Qu
1Shandong Provincial Key Laboratory of Animal Cells and Developmental Biology and Key Laboratory for Experimental Teratology of the Ministry of Education, School of Life Sciences, Shandong University, Qingdao, Shandong 266237, People's Republic of China
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Rui Ren
1Shandong Provincial Key Laboratory of Animal Cells and Developmental Biology and Key Laboratory for Experimental Teratology of the Ministry of Education, School of Life Sciences, Shandong University, Qingdao, Shandong 266237, People's Republic of China
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Haibo Du
1Shandong Provincial Key Laboratory of Animal Cells and Developmental Biology and Key Laboratory for Experimental Teratology of the Ministry of Education, School of Life Sciences, Shandong University, Qingdao, Shandong 266237, People's Republic of China
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Nana Li
1Shandong Provincial Key Laboratory of Animal Cells and Developmental Biology and Key Laboratory for Experimental Teratology of the Ministry of Education, School of Life Sciences, Shandong University, Qingdao, Shandong 266237, People's Republic of China
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Keji Yan
1Shandong Provincial Key Laboratory of Animal Cells and Developmental Biology and Key Laboratory for Experimental Teratology of the Ministry of Education, School of Life Sciences, Shandong University, Qingdao, Shandong 266237, People's Republic of China
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Yanfei Wang
1Shandong Provincial Key Laboratory of Animal Cells and Developmental Biology and Key Laboratory for Experimental Teratology of the Ministry of Education, School of Life Sciences, Shandong University, Qingdao, Shandong 266237, People's Republic of China
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Wei Xiong
2School of Life Sciences, IDG/McGovern Institute for Brain Research, Tsinghua University, Beijing 100084, People's Republic of China
3Chinese Institute for Brain Research, Beijing 102206, People's Republic of China
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Zhigang Xu
1Shandong Provincial Key Laboratory of Animal Cells and Developmental Biology and Key Laboratory for Experimental Teratology of the Ministry of Education, School of Life Sciences, Shandong University, Qingdao, Shandong 266237, People's Republic of China
4Shandong Provincial Collaborative Innovation Center of Cell Biology, Shandong Normal University, Jinan, Shandong 250014, People's Republic of China
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Abstract

The mechanoelectrical transduction (MET) protein complex in the inner-ear hair cells is essential for hearing and balance perception. Calcium and integrin-binding protein 2 (CIB2) has been reported to be a component of MET complex, and loss of CIB2 completely abolishes MET currents in auditory hair cells, causing profound congenital hearing loss. However, loss of CIB2 does not affect MET currents in vestibular hair cells (VHCs) as well as general balance function. Here, we show that CIB2 and CIB3 act redundantly to regulate MET in VHCs, as MET currents are completely abolished in the VHCs of Cib2/Cib3 double knock-out mice of either sex. Furthermore, we show that Cib2 and Cib3 transcripts have complementary expression patterns in the vestibular maculae, and that they play different roles in stereocilia maintenance in VHCs. Cib2 transcripts are highly expressed in the striolar region, and knock-out of Cib2 affects stereocilia maintenance in striolar VHCs. In contrast, Cib3 transcripts are highly expressed in the extrastriolar region, and knock-out of Cib3 mainly affects stereocilia maintenance in extrastriolar VHCs. Simultaneous knock-out of Cib2 and Cib3 affects stereocilia maintenance in all VHCs and leads to severe balance deficits. Taken together, our present work reveals that CIB2 and CIB3 are important for stereocilia maintenance as well as MET in mouse VHCs.

SIGNIFICANCE STATEMENT Calcium and integrin-binding protein 2 (CIB2) is an important component of mechanoelectrical transduction (MET) complex, and loss of CIB2 completely abolishes MET in auditory hair cells. However, MET is unaffected in Cib2 knock-out vestibular hair cells (VHCs). In the present work, we show that CIB3 could compensate for the loss of CIB2 in VHCs, and Cib2/Cib3 double knock-out completely abolishes MET in VHCs. Interestingly, CIB2 and CIB3 could also regulate VHC stereocilia maintenance in a nonredundant way. Cib2 and Cib3 transcripts are highly expressed in the striolar and extrastriolar regions, respectively. Stereocilia maintenance and balance function are differently affected in Cib2 or Cib3 knock-out mice. In conclusion, our data suggest that CIB2 and CIB3 are important for stereocilia maintenance and MET in mouse VHCs.

  • CIB2
  • CIB3
  • mechanoelectrical transduction
  • stereocilia
  • vestibular hair cells

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The Journal of Neuroscience: 43 (18)
Journal of Neuroscience
Vol. 43, Issue 18
3 May 2023
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CIB2 and CIB3 Regulate Stereocilia Maintenance and Mechanoelectrical Transduction in Mouse Vestibular Hair Cells
Xiaoying Wang, Shuang Liu, Qi Cheng, Chengli Qu, Rui Ren, Haibo Du, Nana Li, Keji Yan, Yanfei Wang, Wei Xiong, Zhigang Xu
Journal of Neuroscience 3 May 2023, 43 (18) 3219-3231; DOI: 10.1523/JNEUROSCI.1807-22.2023

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CIB2 and CIB3 Regulate Stereocilia Maintenance and Mechanoelectrical Transduction in Mouse Vestibular Hair Cells
Xiaoying Wang, Shuang Liu, Qi Cheng, Chengli Qu, Rui Ren, Haibo Du, Nana Li, Keji Yan, Yanfei Wang, Wei Xiong, Zhigang Xu
Journal of Neuroscience 3 May 2023, 43 (18) 3219-3231; DOI: 10.1523/JNEUROSCI.1807-22.2023
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Keywords

  • CIB2
  • CIB3
  • mechanoelectrical transduction
  • stereocilia
  • vestibular hair cells

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