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

Swinburne, Ian A.; Mosaliganti, Kishore; Upadhyayula, Srigokul; Liu, Tsung Li; Hildebrand, David G. C.; Tsai, Tony; Chen, Anzhi; Al-Obeidi, Ebaa; Fass, Anna K.; Malhotra, Samir; Engert, Florian; Lichtman, Jeff W.; Kirchhausen, Tomas; Betzig, Eric; Megason, Sean G.

doi:10.7554/elife.37131

Cited by 27 publications

(31 citation statements)

References 91 publications

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“…In the inner ear, pressure is initially regulated by feedback between pressure and lumenal fluid flux. However later in development, we have found that a physical pressure relief valve is necessary for pressure homeostasis in the inner ear (Swinburne et al, 2018). Together, we expect that these new insights on ear development and physiology will be critical to the development of effective clinical therapies for hearing and balance disorders, and for understanding size control in closed epithelial tissues.…”

Section: Discussionmentioning

confidence: 99%

Size control of the inner ear via hydraulic feedback

Mosaliganti

Swinburne

Chan

et al. 2019

eLife

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Animals make organs of precise size, shape, and symmetry but how developing embryos do this is largely unknown. Here, we combine quantitative imaging, physical theory, and physiological measurement of hydrostatic pressure and fluid transport in zebrafish to study size control of the developing inner ear. We find that fluid accumulation creates hydrostatic pressure in the lumen leading to stress in the epithelium and expansion of the otic vesicle. Pressure, in turn, inhibits fluid transport into the lumen. This negative feedback loop between pressure and transport allows the otic vesicle to change growth rate to control natural or experimentally-induced size variation. Spatiotemporal patterning of contractility modulates pressure-driven strain for regional tissue thinning. Our work connects molecular-driven mechanisms, such as osmotic pressure driven strain and actomyosin tension, to the regulation of tissue morphogenesis via hydraulic feedback to ensure robust control of organ size.Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (<xref ref-type="decision-letter" rid="SA1">see decision letter</xref>).

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Section: Discussionmentioning

confidence: 99%

Size control of the inner ear via hydraulic feedback

Mosaliganti

Swinburne

Chan

et al. 2019

eLife

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“…One mechanism may involve the transient rupture of tight junctions through mitosis, as in the case of mouse blastocysts (Chan et al, 2019;Leonavicius et al, 2018). Excessive pressure can also lead to a breach of epithelial permeability and pressure relief, as shown in the endolymphatic sac of the inner ear (Swinburne et al, 2018). Other mechanisms may include the active regulation of ion pumping activity and endo-or exocytosis to modulate the lumen volume and pressure, as shown during zebrafish inner ear formation (Hoijman et al, 2015;Mosaliganti et al, 2019).…”

Section: Biomechanical Control Of Luminogenesismentioning

confidence: 99%

Integration of luminal pressure and signalling in tissue self-organization

Chan

Hiiragi

2020

Development

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Many developmental processes involve the emergence of intercellular fluid-filled lumina. This process of luminogenesis results in a build up of hydrostatic pressure and signalling molecules in the lumen. However, the potential roles of lumina in cellular functions, tissue morphogenesis and patterning have yet to be fully explored. In this Review, we discuss recent findings that describe how pressurized fluid expansion can provide both mechanical and biochemical cues to influence cell proliferation, migration and differentiation. We also review emerging techniques that allow for precise quantification of fluid pressure in vivo and in situ. Finally, we discuss the intricate interplay between luminogenesis, tissue mechanics and signalling, which provide a new dimension for understanding the principles governing tissue self-organization in embryonic development.

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“…In addition to creating new mutant models, CRISPR-Cas9 methods have been optimized to create biallelic mutations that enable detection of phenotypes in G 0 CRISPR-Cas9 injected embryos or larvae (Burger et al 2016 ; Hoshijima et al 2019 ; Kroll et al 2021 ; Swinburne et al 2018 ). These CRISPR-Cas9 injected zebrafish are referred to as “CRISPants” or G 0 knockouts.…”

Section: Main Bodymentioning

confidence: 99%

How Zebrafish Can Drive the Future of Genetic-based Hearing and Balance Research

Sheets

Holmgren

Kindt

2021

JARO

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Over the last several decades, studies in humans and animal models have successfully identified numerous molecules required for hearing and balance. Many of these studies relied on unbiased forward genetic screens based on behavior or morphology to identify these molecules. Alongside forward genetic screens, reverse genetics has further driven the exploration of candidate molecules. This review provides an overview of the genetic studies that have established zebrafish as a genetic model for hearing and balance research. Further, we discuss how the unique advantages of zebrafish can be leveraged in future genetic studies. We explore strategies to design novel forward genetic screens based on morphological alterations using transgenic lines or behavioral changes following mechanical or acoustic damage. We also outline how recent advances in CRISPR-Cas9 can be applied to perform reverse genetic screens to validate large sequencing datasets. Overall, this review describes how future genetic studies in zebrafish can continue to advance our understanding of inherited and acquired hearing and balance disorders.

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

Cited by 27 publications

References 91 publications

Size control of the inner ear via hydraulic feedback

Size control of the inner ear via hydraulic feedback

Integration of luminal pressure and signalling in tissue self-organization

How Zebrafish Can Drive the Future of Genetic-based Hearing and Balance Research

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