Live-cell imaging of actin dynamics reveals mechanisms of stereocilia length regulation in the inner ear

Meghan C. Drummond, Melanie Barzik, Jonathan E. Bird, Duan-Sun Zhang, Claude P. Lechene, David P. Corey, Lisa L. Cunningham and Thomas B. Friedman ()
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Meghan C. Drummond: Laboratory of Molecular Genetics, Section on Human Genetics, National Institute on Deafness and Other Communication Disorders, National Institutes of Health
Melanie Barzik: Laboratory of Molecular Genetics, Section on Human Genetics, National Institute on Deafness and Other Communication Disorders, National Institutes of Health
Jonathan E. Bird: Laboratory of Molecular Genetics, Section on Human Genetics, National Institute on Deafness and Other Communication Disorders, National Institutes of Health
Duan-Sun Zhang: Harvard Medical School and Howard Hughes Medical Institute
Claude P. Lechene: National Resource for Imaging Mass Spectrometry, Brigham and Women’s Hospital and Harvard Medical School
David P. Corey: Harvard Medical School and Howard Hughes Medical Institute
Lisa L. Cunningham: Section on Sensory Cell Biology, National Institute on Deafness and Other Communication Disorders, National Institutes of Health
Thomas B. Friedman: Laboratory of Molecular Genetics, Section on Human Genetics, National Institute on Deafness and Other Communication Disorders, National Institutes of Health

Nature Communications, 2015, vol. 6, issue 1, 1-10

Abstract: Abstract The maintenance of sensory hair cell stereocilia is critical for lifelong hearing; however, mechanisms of structural homeostasis remain poorly understood. Conflicting models propose that stereocilia F-actin cores are either continually renewed every 24–48 h via a treadmill or are stable, exceptionally long-lived structures. Here to distinguish between these models, we perform an unbiased survey of stereocilia actin dynamics in more than 500 utricle hair cells. Live-imaging EGFP-β-actin or dendra2-β-actin reveal stable F-actin cores with turnover and elongation restricted to stereocilia tips. Fixed-cell microscopy of wild-type and mutant β-actin demonstrates that incorporation of actin monomers into filaments is required for localization to stereocilia tips. Multi-isotope imaging mass spectrometry and live imaging of single differentiating hair cells capture stereociliogenesis and explain uniform incorporation of 15N-labelled protein and EGFP-β-actin into nascent stereocilia. Collectively, our analyses support a model in which stereocilia actin cores are stable structures that incorporate new F-actin only at the distal tips.

Date: 2015
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DOI: 10.1038/ncomms7873

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