Uncoordinated maturation of developing and regenerating postnatal mammalian vestibular hair cells

Tian Wang, Mamiko Niwa, Zahra N. Sayyid, Davood K. Hosseini, Nicole Pham, Sherri M Jones, Anthony J. Ricci, Alan G. Cheng

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

Sensory hair cells are mechanoreceptors required for hearing and balance functions. From embryonic development, hair cells acquire apical stereociliary bundles for mechanosensation, basolateral ion channels that shape receptor potential, and synaptic contacts for conveying information centrally. These key maturation steps are sequential and presumed coupled; however, whether hair cells emerging postnatally mature similarly is unknown. Here, we show that in vivo postnatally generated and regenerated hair cells in the utricle, a vestibular organ detecting linear acceleration, acquired some mature somatic features but hair bundles appeared nonfunctional and short. The utricle consists of two hair cell subtypes with distinct morphological, electrophysiological and synaptic features. In both the undamaged and damaged utricle, fate-mapping and electrophysiology experiments showed that Plp1+ supporting cells took on type II hair cell properties based on molecular markers, basolateral conductances and synaptic properties yet stereociliary bundles were absent, or small and nonfunctional. By contrast, Lgr5+ supporting cells regenerated hair cells with type I and II properties, representing a distinct hair cell precursor subtype. Lastly, direct physiological measurements showed that utricular function abolished by damage was partially regained during regeneration. Together, our data reveal a previously unrecognized aberrant maturation program for hair cells generated and regenerated postnatally and may have broad implications for inner ear regenerative therapies.

Original languageEnglish (US)
Article numbere3000326
JournalPLoS biology
Volume17
Issue number7
DOIs
StatePublished - Jul 1 2019

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Vestibular Hair Cells
hairs
Cells
Saccule and Utricle
cells
Electrophysiology
Synaptic Potentials
Mechanoreceptors
Neurotransmitter Receptor
Audition
Conveying
electrophysiology
mechanoreceptors
Ion Channels
Inner Ear
ion channels
hearing
Hearing
Embryonic Development
Regeneration

ASJC Scopus subject areas

  • Neuroscience(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Uncoordinated maturation of developing and regenerating postnatal mammalian vestibular hair cells. / Wang, Tian; Niwa, Mamiko; Sayyid, Zahra N.; Hosseini, Davood K.; Pham, Nicole; Jones, Sherri M; Ricci, Anthony J.; Cheng, Alan G.

In: PLoS biology, Vol. 17, No. 7, e3000326, 01.07.2019.

Research output: Contribution to journalArticle

Wang, T, Niwa, M, Sayyid, ZN, Hosseini, DK, Pham, N, Jones, SM, Ricci, AJ & Cheng, AG 2019, 'Uncoordinated maturation of developing and regenerating postnatal mammalian vestibular hair cells', PLoS biology, vol. 17, no. 7, e3000326. https://doi.org/10.1371/journal.pbio.3000326
Wang, Tian ; Niwa, Mamiko ; Sayyid, Zahra N. ; Hosseini, Davood K. ; Pham, Nicole ; Jones, Sherri M ; Ricci, Anthony J. ; Cheng, Alan G. / Uncoordinated maturation of developing and regenerating postnatal mammalian vestibular hair cells. In: PLoS biology. 2019 ; Vol. 17, No. 7.
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