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Trans-epithelial fluid flow and mechanics of epithelial morphogenesis

Choudhury, Mohammad Ikbal and Benson, Morgan A. and Sun, Sean X. (2022) Trans-epithelial fluid flow and mechanics of epithelial morphogenesis. Seminars in Cell and Developmental Biology . ISSN 1084-9521. doi:10.1016/j.semcdb.2022.05.020. (In Press) https://resolver.caltech.edu/CaltechAUTHORS:20220607-425387000

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Abstract

Active fluid transport across epithelial monolayers is emerging as a major driving force of tissue morphogenesis in a variety of healthy and diseased systems, as well as during embryonic development. Cells use directional transport of ions and osmotic gradients to drive fluid flow across the cell surface, in the process also building up fluid pressure. The basic physics of this process is described by the osmotic engine model, which also underlies actin-independent cell migration. Recently, the trans-epithelial fluid flux and the hydraulic pressure gradient have been explicitly measured for a variety of cellular and tissue model systems across various species. For the kidney, it was shown that tubular epithelial cells behave as active mechanical fluid pumps: the trans-epithelial fluid flux depends on the hydraulic pressure difference across the epithelial layer. When a stall pressure is reached, the fluid flux vanishes. Hydraulic forces generated from active fluid pumping are important in tissue morphogenesis and homeostasis, and could also underlie multiple morphogenic events seen in other developmental contexts. In this review, we highlight findings that examined the role of trans-epithelial fluid flux and hydraulic pressure gradient in driving tissue-scale morphogenesis. We also review organ pathophysiology due to impaired fluid pumping and the loss of hydraulic pressure sensing at the cellular scale. Finally, we draw an analogy between cellular fluidic pumps and a connected network of water pumps in a city. The dynamics of fluid transport in an active and adaptive network is determined globally at the systemic level, and transport in such a network is best when each pump is operating at its optimal efficiency.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.semcdb.2022.05.020DOIArticle
ORCID:
AuthorORCID
Choudhury, Mohammad Ikbal0000-0002-3241-9813
Sun, Sean X.0000-0002-9077-7088
Additional Information:© 2022 Elsevier. Received 5 April 2022, Revised 22 May 2022, Accepted 23 May 2022, Available online 31 May 2022. We would like to thank Dr. Owen Woodward and Dr. Feng Qian for helpful discussions. This work has been funded in part by US National Institutes of Health Grant R01GM134542. Conflict of interest statement. S.X.S and M.I.C are co-authors of a patent application WO2021007300A1. The remaining authors declare no competing interests.
Funders:
Funding AgencyGrant Number
NIHR01GM134542
Subject Keywords:Hydraulic pressure; Osmotic engine model; Trans-epithelial flux; Pump performance curve; Lumenogenesis; Morphogenesis
DOI:10.1016/j.semcdb.2022.05.020
Record Number:CaltechAUTHORS:20220607-425387000
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20220607-425387000
Official Citation:Mohammad Ikbal Choudhury, Morgan A. Benson, Sean X. Sun, Trans-epithelial fluid flow and mechanics of epithelial morphogenesis, Seminars in Cell & Developmental Biology, 2022, , ISSN 1084-9521, https://doi.org/10.1016/j.semcdb.2022.05.020.
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:115064
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:07 Jun 2022 20:02
Last Modified:07 Jun 2022 20:02

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