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Lamellar junctions in the endolymphatic sac act as a relief valve to regulate inner ear pressure

Ian A. Swinburne, Kishore R. Mosaliganti, Srigokul Upadhyayula, Tsung-Li Liu, View ORCID ProfileDavid G. C. Hildebrand, Tony Y.-C. Tsai, Anzhi Chen, Ebaa Al-Obeidi, Anna K. Fass, Samir Malhotra, Florian Engert, View ORCID ProfileJeff W. Lichtman, Tom Kirchhausen, Eric Betzig, View ORCID ProfileSean G. Megason
doi: https://doi.org/10.1101/143826
Ian A. Swinburne
1Department of Systems Biology, Harvard Medical School, Boston, MA 02115
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Kishore R. Mosaliganti
1Department of Systems Biology, Harvard Medical School, Boston, MA 02115
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Srigokul Upadhyayula
2Department of Pediatrics, Harvard Medical School, Boston, MA 02115
3Program in Cellular and Molecular Medicine, Boston Children’s Hospital, Boston, MA 02115
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Tsung-Li Liu
4Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147
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David G. C. Hildebrand
5Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138
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Tony Y.-C. Tsai
1Department of Systems Biology, Harvard Medical School, Boston, MA 02115
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Anzhi Chen
1Department of Systems Biology, Harvard Medical School, Boston, MA 02115
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Ebaa Al-Obeidi
1Department of Systems Biology, Harvard Medical School, Boston, MA 02115
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Anna K. Fass
1Department of Systems Biology, Harvard Medical School, Boston, MA 02115
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Samir Malhotra
1Department of Systems Biology, Harvard Medical School, Boston, MA 02115
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Florian Engert
5Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138
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Jeff W. Lichtman
5Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138
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Tom Kirchhausen
2Department of Pediatrics, Harvard Medical School, Boston, MA 02115
3Program in Cellular and Molecular Medicine, Boston Children’s Hospital, Boston, MA 02115
6Departments of Cell Biology, Harvard Medical School, Program in Cellular and Molecular Medicine, Boston Children’s Hospital, Boston, MA 02115
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Eric Betzig
4Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147
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Sean G. Megason
1Department of Systems Biology, Harvard Medical School, Boston, MA 02115
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Abstract

The inner ear is a fluid-filled closed-epithelial structure whose normal function requires maintenance of an internal hydrostatic pressure and fluid composition by unknown mechanisms. The endolymphatic sac (ES) is a dead-end epithelial tube connected to the inner ear. ES defects can cause distended ear tissue, a pathology often seen in hearing and balance disorders. Using live imaging of zebrafish larvae, we reveal that the ES undergoes cycles of slow pressure-driven inflation followed by rapid deflation every 1-3 hours. Using serial-section electron microscopy and adaptive optics lattice light-sheet microscopy, we find a pressure relief valve in the ES comprised of thin overlapping basal lamellae that dynamically extend over neighboring cells before rupturing under pressure leading to ES collapse. The unexpected discovery of a physical relief valve in the ear emphasizes the need for further study into how organs control fluid pressure, volume, flow, and ion homeostasis in development and disease.

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Posted May 30, 2017.
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Lamellar junctions in the endolymphatic sac act as a relief valve to regulate inner ear pressure
Ian A. Swinburne, Kishore R. Mosaliganti, Srigokul Upadhyayula, Tsung-Li Liu, David G. C. Hildebrand, Tony Y.-C. Tsai, Anzhi Chen, Ebaa Al-Obeidi, Anna K. Fass, Samir Malhotra, Florian Engert, Jeff W. Lichtman, Tom Kirchhausen, Eric Betzig, Sean G. Megason
bioRxiv 143826; doi: https://doi.org/10.1101/143826
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Lamellar junctions in the endolymphatic sac act as a relief valve to regulate inner ear pressure
Ian A. Swinburne, Kishore R. Mosaliganti, Srigokul Upadhyayula, Tsung-Li Liu, David G. C. Hildebrand, Tony Y.-C. Tsai, Anzhi Chen, Ebaa Al-Obeidi, Anna K. Fass, Samir Malhotra, Florian Engert, Jeff W. Lichtman, Tom Kirchhausen, Eric Betzig, Sean G. Megason
bioRxiv 143826; doi: https://doi.org/10.1101/143826

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