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Cell‐extracellular matrix interactions in the fluidic phase direct the topology and polarity of self‐organized epithelial structures

Ouyang, Mingxing and Yu, Jiun-Yann and Chen, Yenyu and Deng, Linhong and Guo, Chin-Lin (2021) Cell‐extracellular matrix interactions in the fluidic phase direct the topology and polarity of self‐organized epithelial structures. Cell Proliferation, 54 (4). Art. No. e13014. ISSN 0960-7722. doi:10.1111/cpr.13014. https://resolver.caltech.edu/CaltechAUTHORS:20200515-090423680

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Abstract

Introduction: In vivo, cells are surrounded by extracellular matrix (ECM). To build organs from single cells, it is generally believed that ECM serves as scaffolds to coordinate cell positioning and differentiation. Nevertheless, how cells utilize cell‐ECM interactions for the spatiotemporal coordination to different ECM at the tissue scale is not fully understood. Methods: Here, using in vitro assay with engineered MDCK cells expressing H2B‐mCherry (nucleus) and gp135/Podocalyxin‐GFP (apical marker), we show in multi‐dimensions that such coordination for epithelial morphogenesis can be determined by cell‐soluble ECM interaction in the fluidic phase. Results: The coordination depends on the native topology of ECM components such as sheet‐like basement membrane (BM) and type I collagen (COL) fibres: scaffold formed by BM (COL) facilitates a close‐ended (open‐ended) coordination that leads to the formation of lobular (tubular) epithelium. Further, cells form apicobasal polarity throughout the entire lobule/tubule without a complete coverage of ECM at the basal side, and time‐lapse two‐photon scanning imaging reveals the polarization occurring early and maintained through the lobular expansion. During polarization, gp135‐GFP was converged to the apical surface collectively in the lobular/tubular structures, suggesting possible intercellular communications. Under suspension culture, the polarization was impaired with multi‐lumen formation in the tubules, implying the importance of ECM biomechanical microenvironment. Conclusion: Our results suggest a biophysical mechanism for cells to form polarity and coordinate positioning at tissue scale, and in engineering epithelium through cell‐soluble ECM interaction and self‐assembly.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1111/cpr.13014DOIArticle
https://doi.org/10.1101/2020.05.12.090068DOIDiscussion Paper
ORCID:
AuthorORCID
Ouyang, Mingxing0000-0002-2910-0713
Deng, Linhong0000-0003-1970-8239
Alternate Title:Extracellular matrix directs the topology and polarity of epithelium, ECM guides the epithelium topology and polarity
Additional Information:© 2021 The Authors. Cell Proliferation Published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Issue Online: 01 April 2021; Version of Record online: 21 February 2021; Manuscript accepted: 09 February 2021; Manuscript revised: 04 February 2021; Manuscript received: 12 January 2021. We want to thank Dr Joachim Füllekrug (Max Planck Institute of Molecular Cell Biology and Genetics) for pcDNA3‐gp135‐GFP construct, and Dr Rusty Lansford and David Huss (Biology, California Institute of Technology) for Lentivirus encoding H2B‐mCherry. This work is financially supported by Ellison Medical Foundation and Western Heaven Funds (CG); National Natural Science Foundation of China (11872129) and Natural Science Foundation of Jiangsu Province (BK20181416) (MO); National Natural Science Foundation of China (11532003) (LD). The authors declare no conflict of interest in this work. Author Contributions: M. Ouyang and C. Guo designed the research and performed data analysis; M. Ouyang, J‐Y. Yu, C. Guo conducted the experiments; J‐Y. Yu, Y. Chen and C. Guo constructed the microscopes and developed the imaging programs; L. Deng provided discussion and certain fund support; M. Ouyang, L. Deng and C. Guo prepared the manuscript. Data Availability Statement: The data that support the findings of this study are available from the corresponding author upon reasonable request.
Funders:
Funding AgencyGrant Number
Ellison Medical FoundationUNSPECIFIED
Western Heaven FundsUNSPECIFIED
National Natural Science Foundation of China11872129
Natural Science Foundation of Jiangsu ProvinceBK20181416
National Natural Science Foundation of China11532003
Subject Keywords:cell‐ECM interaction; epithelial polarity; epithelial self‐assembly; epithelial topology; fluidic phase; tubulogenesis
Issue or Number:4
DOI:10.1111/cpr.13014
Record Number:CaltechAUTHORS:20200515-090423680
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200515-090423680
Official Citation: Ouyang, M, Yu, J‐Y, Chen, Y, Deng, L, Guo, C‐L. Cell‐extracellular matrix interactions in the fluidic phase direct the topology and polarity of self‐organized epithelial structures. Cell Prolif. 2021; 54:e13014. https://doi.org/10.1111/cpr.13014
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:103227
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:15 May 2020 16:14
Last Modified:07 Apr 2021 17:09

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