Cell position within human pluripotent stem cell colonies determines apical specialization via an actin cytoskeleton-based mechanism

Youngju Kim; Hwanseok Jang; Kyubin Seo; June Hoan Kim; Boram Lee; Hyo Min Cho; Hyun Jung Kim; Esther Yang; Hyun Kim; Jeong An Gim; Yongdoo Park; Jae Ryun Ryu; Woong Sun

doi:10.1016/j.stemcr.2021.11.005

Cell position within human pluripotent stem cell colonies determines apical specialization via an actin cytoskeleton-based mechanism

Youngju Kim, Hwanseok Jang, Kyubin Seo, June Hoan Kim, Boram Lee, Hyo Min Cho, Hyun Jung Kim, Esther Yang, Hyun Kim, Jeong An Gim, Yongdoo Park, Jae Ryun Ryu, Woong Sun

Department of Biomedical Sciences

Research output: Contribution to journal › Article › peer-review

9 Citations (Scopus)

Abstract

Human pluripotent stem cells (hPSCs) grow as colonies with epithelial-like features including cell polarity and position-dependent features that contribute to symmetry breaking during development. Our study provides evidence that hPSC colonies exhibit position-dependent differences in apical structures and functions. With this apical difference, edge cells were preferentially labeled with amphipathic dyes, which enabled separation of edge and center cells by fluorescence-activated cell sorting. Transcriptome comparison between center and edge cells showed differential expression of genes related to apicobasal polarization, cell migration, and endocytosis. Accordingly, different kinematics and mechanical dynamics were found between center and edge cells, and perturbed actin dynamics disrupted the position-dependent apical polarity. In addition, our dye-labeling approach could be utilized to sort out a certain cell population in differentiated micropatterned colonies. In summary, hPSC colonies have position-dependent differences in apical structures and properties, and actin dynamics appear to play an important role in the establishment of this position-dependent cell polarity.

Original language	English
Pages (from-to)	68-81
Number of pages	14
Journal	Stem Cell Reports
Volume	17
Issue number	1
DOIs	https://doi.org/10.1016/j.stemcr.2021.11.005
Publication status	Published - 2022 Jan 11

Bibliographical note

Funding Information:
This research was funded by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIP) ( NRF-2019M3D1A1078940 , NRF-2017M3A9B3061308 , NRF-2017M3C7A1047654 , and NRF-2016R1D1A1B01011346 ). We thank Hyun-Wook Kim for sample preparation and imaging with a scanning electron microscope and Eun-Ok Kim for FACSAriaIII sorting at the Medical Science Research Center.

Publisher Copyright:
© 2021 The Author(s)

Keywords

actin dynamics
apical specialization
cell polarity
human pluripotent stem cells
stem cell colony
topology
transcriptome analysis

ASJC Scopus subject areas

Biochemistry
Genetics
Developmental Biology
Cell Biology

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10.1016/j.stemcr.2021.11.005

Cite this

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title = "Cell position within human pluripotent stem cell colonies determines apical specialization via an actin cytoskeleton-based mechanism",

abstract = "Human pluripotent stem cells (hPSCs) grow as colonies with epithelial-like features including cell polarity and position-dependent features that contribute to symmetry breaking during development. Our study provides evidence that hPSC colonies exhibit position-dependent differences in apical structures and functions. With this apical difference, edge cells were preferentially labeled with amphipathic dyes, which enabled separation of edge and center cells by fluorescence-activated cell sorting. Transcriptome comparison between center and edge cells showed differential expression of genes related to apicobasal polarization, cell migration, and endocytosis. Accordingly, different kinematics and mechanical dynamics were found between center and edge cells, and perturbed actin dynamics disrupted the position-dependent apical polarity. In addition, our dye-labeling approach could be utilized to sort out a certain cell population in differentiated micropatterned colonies. In summary, hPSC colonies have position-dependent differences in apical structures and properties, and actin dynamics appear to play an important role in the establishment of this position-dependent cell polarity.",

keywords = "actin dynamics, apical specialization, cell polarity, human pluripotent stem cells, stem cell colony, topology, transcriptome analysis",

author = "Youngju Kim and Hwanseok Jang and Kyubin Seo and Kim, {June Hoan} and Boram Lee and Cho, {Hyo Min} and Kim, {Hyun Jung} and Esther Yang and Hyun Kim and Gim, {Jeong An} and Yongdoo Park and Ryu, {Jae Ryun} and Woong Sun",

note = "Funding Information: This research was funded by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIP) ( NRF-2019M3D1A1078940 , NRF-2017M3A9B3061308 , NRF-2017M3C7A1047654 , and NRF-2016R1D1A1B01011346 ). We thank Hyun-Wook Kim for sample preparation and imaging with a scanning electron microscope and Eun-Ok Kim for FACSAriaIII sorting at the Medical Science Research Center. Publisher Copyright: {\textcopyright} 2021 The Author(s)",

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doi = "10.1016/j.stemcr.2021.11.005",

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AU - Kim, Youngju

AU - Jang, Hwanseok

AU - Seo, Kyubin

AU - Kim, June Hoan

AU - Lee, Boram

AU - Cho, Hyo Min

AU - Kim, Hyun Jung

AU - Yang, Esther

AU - Kim, Hyun

AU - Gim, Jeong An

AU - Park, Yongdoo

AU - Ryu, Jae Ryun

AU - Sun, Woong

N1 - Funding Information: This research was funded by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIP) ( NRF-2019M3D1A1078940 , NRF-2017M3A9B3061308 , NRF-2017M3C7A1047654 , and NRF-2016R1D1A1B01011346 ). We thank Hyun-Wook Kim for sample preparation and imaging with a scanning electron microscope and Eun-Ok Kim for FACSAriaIII sorting at the Medical Science Research Center. Publisher Copyright: © 2021 The Author(s)

PY - 2022/1/11

Y1 - 2022/1/11

N2 - Human pluripotent stem cells (hPSCs) grow as colonies with epithelial-like features including cell polarity and position-dependent features that contribute to symmetry breaking during development. Our study provides evidence that hPSC colonies exhibit position-dependent differences in apical structures and functions. With this apical difference, edge cells were preferentially labeled with amphipathic dyes, which enabled separation of edge and center cells by fluorescence-activated cell sorting. Transcriptome comparison between center and edge cells showed differential expression of genes related to apicobasal polarization, cell migration, and endocytosis. Accordingly, different kinematics and mechanical dynamics were found between center and edge cells, and perturbed actin dynamics disrupted the position-dependent apical polarity. In addition, our dye-labeling approach could be utilized to sort out a certain cell population in differentiated micropatterned colonies. In summary, hPSC colonies have position-dependent differences in apical structures and properties, and actin dynamics appear to play an important role in the establishment of this position-dependent cell polarity.

AB - Human pluripotent stem cells (hPSCs) grow as colonies with epithelial-like features including cell polarity and position-dependent features that contribute to symmetry breaking during development. Our study provides evidence that hPSC colonies exhibit position-dependent differences in apical structures and functions. With this apical difference, edge cells were preferentially labeled with amphipathic dyes, which enabled separation of edge and center cells by fluorescence-activated cell sorting. Transcriptome comparison between center and edge cells showed differential expression of genes related to apicobasal polarization, cell migration, and endocytosis. Accordingly, different kinematics and mechanical dynamics were found between center and edge cells, and perturbed actin dynamics disrupted the position-dependent apical polarity. In addition, our dye-labeling approach could be utilized to sort out a certain cell population in differentiated micropatterned colonies. In summary, hPSC colonies have position-dependent differences in apical structures and properties, and actin dynamics appear to play an important role in the establishment of this position-dependent cell polarity.

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Cell position within human pluripotent stem cell colonies determines apical specialization via an actin cytoskeleton-based mechanism

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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