Single-cell transcriptomic atlas reveals increased regeneration in diseased human inner ear balance organs

Tian Wang, Angela H. Ling, Sara E. Billings, Davood K. Hosseini, Yona Vaisbuch, Grace S. Kim, Patrick J. Atkinson, Zahra N. Sayyid, Ksenia A. Aaron, Dhananjay Wagh, Nicole Pham, Mirko Scheibinger, Ruiqi Zhou, Akira Ishiyama, Lindsay S. Moore, Peter Santa Maria, Nikolas H. Blevins, Robert K. Jackler, Jennifer C. Alyono, John Kveton, Dhasakumar Navaratnam, Stefan Heller, Ivan A. Lopez, Nicolas Grillet, Taha A. Jan () and Alan G. Cheng ()
Additional contact information
Tian Wang: Stanford University School of Medicine
Angela H. Ling: Stanford University School of Medicine
Sara E. Billings: Stanford University School of Medicine
Davood K. Hosseini: Stanford University School of Medicine
Yona Vaisbuch: Stanford University School of Medicine
Grace S. Kim: Stanford University School of Medicine
Patrick J. Atkinson: Stanford University School of Medicine
Zahra N. Sayyid: Stanford University School of Medicine
Ksenia A. Aaron: Stanford University School of Medicine
Dhananjay Wagh: Stanford University School of Medicine
Nicole Pham: Stanford University School of Medicine
Mirko Scheibinger: Stanford University School of Medicine
Ruiqi Zhou: Epithelial Biology Center, Vanderbilt University Medical Center
Akira Ishiyama: University of California Los Angeles
Lindsay S. Moore: Stanford University School of Medicine
Peter Santa Maria: Stanford University School of Medicine
Nikolas H. Blevins: Stanford University School of Medicine
Robert K. Jackler: Stanford University School of Medicine
Jennifer C. Alyono: Stanford University School of Medicine
John Kveton: Yale University School of Medicine
Dhasakumar Navaratnam: Yale University School of Medicine
Stefan Heller: Stanford University School of Medicine
Ivan A. Lopez: University of California Los Angeles
Nicolas Grillet: Stanford University School of Medicine
Taha A. Jan: Epithelial Biology Center, Vanderbilt University Medical Center
Alan G. Cheng: Stanford University School of Medicine

Nature Communications, 2024, vol. 15, issue 1, 1-19

Abstract: Abstract Mammalian inner ear hair cell loss leads to permanent hearing and balance dysfunction. In contrast to the cochlea, vestibular hair cells of the murine utricle have some regenerative capacity. Whether human utricular hair cells regenerate in vivo remains unknown. Here we procured live, mature utricles from organ donors and vestibular schwannoma patients, and present a validated single-cell transcriptomic atlas at unprecedented resolution. We describe markers of 13 sensory and non-sensory cell types, with partial overlap and correlation between transcriptomes of human and mouse hair cells and supporting cells. We further uncover transcriptomes unique to hair cell precursors, which are unexpectedly 14-fold more abundant in vestibular schwannoma utricles, demonstrating the existence of ongoing regeneration in humans. Lastly, supporting cell-to-hair cell trajectory analysis revealed 5 distinct patterns of dynamic gene expression and associated pathways, including Wnt and IGF-1 signaling. Our dataset constitutes a foundational resource, accessible via a web-based interface, serving to advance knowledge of the normal and diseased human inner ear.

Date: 2024
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DOI: 10.1038/s41467-024-48491-y

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