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

Author

Listed:
  • Tian Wang

    (Stanford University School of Medicine
    The Second Xiangya Hospital, Central South University)

  • Angela H. Ling

    (Stanford University School of Medicine
    Epithelial Biology Center, Vanderbilt University Medical Center)

  • 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
    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)

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.

Suggested Citation

  • 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 Schei, 2024. "Single-cell transcriptomic atlas reveals increased regeneration in diseased human inner ear balance organs," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48491-y
    DOI: 10.1038/s41467-024-48491-y
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    References listed on IDEAS

    as
    1. Tian Wang & Renjie Chai & Grace S. Kim & Nicole Pham & Lina Jansson & Duc-Huy Nguyen & Bryan Kuo & Lindsey A. May & Jian Zuo & Lisa L. Cunningham & Alan G. Cheng, 2015. "Lgr5+ cells regenerate hair cells via proliferation and direct transdifferentiation in damaged neonatal mouse utricle," Nature Communications, Nature, vol. 6(1), pages 1-15, May.
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