Literature DB >> 31571582

Size control of the inner ear via hydraulic feedback.

Kishore R Mosaliganti1, Ian A Swinburne1, Chon U Chan2, Nikolaus D Obholzer1, Amelia A Green1, Shreyas Tanksale1, L Mahadevan2,3,4,5, Sean G Megason1.   

Abstract

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 (see decision letter).
© 2019, Mosaliganti et al.

Entities:  

Keywords:  computational biology; developmental biology; growth; inner ear; pressure; size control; systems biology; systems modeling; transepithelial flow; zebrafish

Mesh:

Year:  2019        PMID: 31571582      PMCID: PMC6773445          DOI: 10.7554/eLife.39596

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.140


  80 in total

1.  Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member.

Authors:  A C McPherron; A M Lawler; S J Lee
Journal:  Nature       Date:  1997-05-01       Impact factor: 49.962

2.  Hydraulic control of mammalian embryo size and cell fate.

Authors:  Chii Jou Chan; Maria Costanzo; Teresa Ruiz-Herrero; Gregor Mönke; Ryan J Petrie; Martin Bergert; Alba Diz-Muñoz; L Mahadevan; Takashi Hiiragi
Journal:  Nature       Date:  2019-06-12       Impact factor: 49.962

3.  Route of passive ion permeation in epithelia.

Authors:  E Frömter; J Diamond
Journal:  Nat New Biol       Date:  1972-01-05

4.  Intrinsic growth control in the imaginal primordia of Drosophila, and the autonomous action of a lethal mutation causing overgrowth.

Authors:  P J Bryant; P Levinson
Journal:  Dev Biol       Date:  1985-02       Impact factor: 3.582

5.  Recovery of shape and size in a developing organ pair.

Authors:  Amelia A Green; Kishore R Mosaliganti; Ian A Swinburne; Nikolaus D Obholzer; Sean G Megason
Journal:  Dev Dyn       Date:  2017-04-03       Impact factor: 3.780

6.  Fundamental limits on the suppression of molecular fluctuations.

Authors:  Ioannis Lestas; Glenn Vinnicombe; Johan Paulsson
Journal:  Nature       Date:  2010-09-09       Impact factor: 49.962

7.  Early ear development in the embryo of the zebrafish, Danio rerio.

Authors:  C Haddon; J Lewis
Journal:  J Comp Neurol       Date:  1996-01-29       Impact factor: 3.215

8.  Cell volume changes contribute to epithelial morphogenesis in zebrafish Kupffer's vesicle.

Authors:  Agnik Dasgupta; Matthias Merkel; Madeline J Clark; Andrew E Jacob; Jonathan Edward Dawson; M Lisa Manning; Jeffrey D Amack
Journal:  Elife       Date:  2018-01-29       Impact factor: 8.140

9.  Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein.

Authors:  G M Preston; T P Carroll; W B Guggino; P Agre
Journal:  Science       Date:  1992-04-17       Impact factor: 47.728

Review 10.  Organ Size Control: Lessons from Drosophila.

Authors:  Iswar K Hariharan
Journal:  Dev Cell       Date:  2015-08-10       Impact factor: 12.270

View more
  11 in total

Review 1.  Programmed and self-organized flow of information during morphogenesis.

Authors:  Claudio Collinet; Thomas Lecuit
Journal:  Nat Rev Mol Cell Biol       Date:  2021-01-22       Impact factor: 94.444

Review 2.  Polarized transport of membrane and secreted proteins during lumen morphogenesis.

Authors:  Daniel S Levic; Michel Bagnat
Journal:  Semin Cell Dev Biol       Date:  2022-03-17       Impact factor: 7.499

Review 3.  The mechanical forces that shape our senses.

Authors:  Anh Phuong Le; Jin Kim; Karl R Koehler
Journal:  Development       Date:  2022-03-31       Impact factor: 6.862

Review 4.  Hydrostatic pressure as a driver of cell and tissue morphogenesis.

Authors:  Mayank Chugh; Akankshi Munjal; Sean G Megason
Journal:  Semin Cell Dev Biol       Date:  2022-05-06       Impact factor: 7.499

Review 5.  Mechanics of Development.

Authors:  Katharine Goodwin; Celeste M Nelson
Journal:  Dev Cell       Date:  2020-12-14       Impact factor: 12.270

6.  Extracellular hyaluronate pressure shaped by cellular tethers drives tissue morphogenesis.

Authors:  Akankshi Munjal; Edouard Hannezo; Tony Y-C Tsai; Timothy J Mitchison; Sean G Megason
Journal:  Cell       Date:  2021-12-22       Impact factor: 41.582

Review 7.  Mechanical forces shaping the development of the inner ear.

Authors:  Roie Cohen; David Sprinzak
Journal:  Biophys J       Date:  2021-07-07       Impact factor: 3.699

8.  Inflation-collapse dynamics drive patterning and morphogenesis in intestinal organoids.

Authors:  Naren P Tallapragada; Hailey M Cambra; Tomas Wald; Samantha Keough Jalbert; Diana M Abraham; Ophir D Klein; Allon M Klein
Journal:  Cell Stem Cell       Date:  2021-04-28       Impact factor: 25.269

9.  Mechanical oscillations orchestrate axial patterning through Wnt activation in Hydra.

Authors:  Jaroslav Ferenc; Panagiotis Papasaikas; Jacqueline Ferralli; Yukio Nakamura; Sebastien Smallwood; Charisios D Tsiairis
Journal:  Sci Adv       Date:  2021-12-10       Impact factor: 14.136

Review 10.  The Shape and Function of Solid Fascias Depend on the Presence of Liquid Fascias.

Authors:  Bruno Bordoni
Journal:  Cureus       Date:  2020-02-10
View more

北京卡尤迪生物科技股份有限公司 © 2022-2023.