Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts

Suling Liu; Yang Cong; Dong Wang; Yu Sun; Lu Deng; Yajing Liu; Rachel Martin-Trevino; Li Shang; Sean P. McDermott; Melissa D. Landis; Suhyung Hong; April Adams; Rosemarie D'Angelo; Christophe Ginestier; Emmanuelle Charafe-Jauffret; Shawn G. Clouthier; Daniel Birnbaum; Stephen T. Wong; Ming Zhan; Jenny C. Chang; Max S. Wicha

doi:10.1016/j.stemcr.2013.11.009

Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts

Suling Liu
, Yang Cong
, Dong Wang
, Yu Sun
, Lu Deng
, Yajing Liu
, Rachel Martin-Trevino
, Li Shang
, Sean P. McDermott
, Melissa D. Landis
, Suhyung Hong
, April Adams
, Rosemarie D'Angelo
, Christophe Ginestier
, Emmanuelle Charafe-Jauffret
, Shawn G. Clouthier
, Daniel Birnbaum
, Stephen T. Wong
, Ming Zhan
, Jenny C. Chang

Max S. Wicha

Department of Dentistry

University of Science and Technology of China
Houston Methodist
University of Michigan, Ann Arbor
Centre de Recherche en Cancérologie de Marseille

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

873 Scopus citations

Abstract

Previous studies have suggested that breast cancer stem cells (BCSCs) mediate metastasis, are resistant to radiation and chemotherapy, and contribute to relapse. Although several BCSC markers have been described, it is unclear whether these markers identify the same or independent BCSCs. Here, we show that BCSCs exist in distinct mesenchymal-like (epithelial-mesenchymal transition [EMT]) and epithelial-like (mesenchymal-epithelial transition [MET]) states. Mesenchymal-like BCSCs characterized as CD24^-CD44⁺ are primarily quiescent and localized at the tumor invasive front, whereas epithelial-like BCSCs express aldehyde dehydrogenase (ALDH), are proliferative, and are located more centrally. The gene-expression profiles of mesenchymal-like and epithelial-like BCSCs are remarkably similar across different molecular subtypes of breast cancer, and resemble those of distinct basal and luminal stem cells found in the normal breast. We propose that the plasticity of BCSCs that allows them to transition between EMT- and MET-like states endows these cells with the capacity for tissue invasion, dissemination, and growth at metastatic sites.

Original language	English
Pages (from-to)	78-91
Number of pages	14
Journal	Stem Cell Reports
Volume	2
Issue number	1
DOIs	https://doi.org/10.1016/j.stemcr.2013.11.009
State	Published - 14 Jan 2014

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10.1016/j.stemcr.2013.11.009

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Liu, S., Cong, Y., Wang, D., Sun, Y., Deng, L., Liu, Y., Martin-Trevino, R., Shang, L., McDermott, S. P., Landis, M. D., Hong, S., Adams, A., D'Angelo, R., Ginestier, C., Charafe-Jauffret, E., Clouthier, S. G., Birnbaum, D., Wong, S. T., Zhan, M., ... Wicha, M. S. (2014). Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts. Stem Cell Reports, 2(1), 78-91. https://doi.org/10.1016/j.stemcr.2013.11.009

@article{8cf5504500274c4d96e2f114f1c01f5a,

title = "Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts",

abstract = "Previous studies have suggested that breast cancer stem cells (BCSCs) mediate metastasis, are resistant to radiation and chemotherapy, and contribute to relapse. Although several BCSC markers have been described, it is unclear whether these markers identify the same or independent BCSCs. Here, we show that BCSCs exist in distinct mesenchymal-like (epithelial-mesenchymal transition [EMT]) and epithelial-like (mesenchymal-epithelial transition [MET]) states. Mesenchymal-like BCSCs characterized as CD24-CD44+ are primarily quiescent and localized at the tumor invasive front, whereas epithelial-like BCSCs express aldehyde dehydrogenase (ALDH), are proliferative, and are located more centrally. The gene-expression profiles of mesenchymal-like and epithelial-like BCSCs are remarkably similar across different molecular subtypes of breast cancer, and resemble those of distinct basal and luminal stem cells found in the normal breast. We propose that the plasticity of BCSCs that allows them to transition between EMT- and MET-like states endows these cells with the capacity for tissue invasion, dissemination, and growth at metastatic sites.",

author = "Suling Liu and Yang Cong and Dong Wang and Yu Sun and Lu Deng and Yajing Liu and Rachel Martin-Trevino and Li Shang and McDermott, \{Sean P.\} and Landis, \{Melissa D.\} and Suhyung Hong and April Adams and Rosemarie D'Angelo and Christophe Ginestier and Emmanuelle Charafe-Jauffret and Clouthier, \{Shawn G.\} and Daniel Birnbaum and Wong, \{Stephen T.\} and Ming Zhan and Chang, \{Jenny C.\} and Wicha, \{Max S.\}",

year = "2014",

month = jan,

day = "14",

doi = "10.1016/j.stemcr.2013.11.009",

language = "English",

volume = "2",

pages = "78--91",

journal = "Stem Cell Reports",

issn = "2213-6711",

publisher = "Cell Press",

number = "1",

}

Liu, S, Cong, Y, Wang, D, Sun, Y, Deng, L, Liu, Y, Martin-Trevino, R, Shang, L, McDermott, SP, Landis, MD, Hong, S, Adams, A, D'Angelo, R, Ginestier, C, Charafe-Jauffret, E, Clouthier, SG, Birnbaum, D, Wong, ST, Zhan, M, Chang, JC & Wicha, MS 2014, 'Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts', Stem Cell Reports, vol. 2, no. 1, pp. 78-91. https://doi.org/10.1016/j.stemcr.2013.11.009

TY - JOUR

T1 - Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts

AU - Liu, Suling

AU - Cong, Yang

AU - Wang, Dong

AU - Sun, Yu

AU - Deng, Lu

AU - Liu, Yajing

AU - Martin-Trevino, Rachel

AU - Shang, Li

AU - McDermott, Sean P.

AU - Landis, Melissa D.

AU - Hong, Suhyung

AU - Adams, April

AU - D'Angelo, Rosemarie

AU - Ginestier, Christophe

AU - Charafe-Jauffret, Emmanuelle

AU - Clouthier, Shawn G.

AU - Birnbaum, Daniel

AU - Wong, Stephen T.

AU - Zhan, Ming

AU - Chang, Jenny C.

AU - Wicha, Max S.

PY - 2014/1/14

Y1 - 2014/1/14

N2 - Previous studies have suggested that breast cancer stem cells (BCSCs) mediate metastasis, are resistant to radiation and chemotherapy, and contribute to relapse. Although several BCSC markers have been described, it is unclear whether these markers identify the same or independent BCSCs. Here, we show that BCSCs exist in distinct mesenchymal-like (epithelial-mesenchymal transition [EMT]) and epithelial-like (mesenchymal-epithelial transition [MET]) states. Mesenchymal-like BCSCs characterized as CD24-CD44+ are primarily quiescent and localized at the tumor invasive front, whereas epithelial-like BCSCs express aldehyde dehydrogenase (ALDH), are proliferative, and are located more centrally. The gene-expression profiles of mesenchymal-like and epithelial-like BCSCs are remarkably similar across different molecular subtypes of breast cancer, and resemble those of distinct basal and luminal stem cells found in the normal breast. We propose that the plasticity of BCSCs that allows them to transition between EMT- and MET-like states endows these cells with the capacity for tissue invasion, dissemination, and growth at metastatic sites.

AB - Previous studies have suggested that breast cancer stem cells (BCSCs) mediate metastasis, are resistant to radiation and chemotherapy, and contribute to relapse. Although several BCSC markers have been described, it is unclear whether these markers identify the same or independent BCSCs. Here, we show that BCSCs exist in distinct mesenchymal-like (epithelial-mesenchymal transition [EMT]) and epithelial-like (mesenchymal-epithelial transition [MET]) states. Mesenchymal-like BCSCs characterized as CD24-CD44+ are primarily quiescent and localized at the tumor invasive front, whereas epithelial-like BCSCs express aldehyde dehydrogenase (ALDH), are proliferative, and are located more centrally. The gene-expression profiles of mesenchymal-like and epithelial-like BCSCs are remarkably similar across different molecular subtypes of breast cancer, and resemble those of distinct basal and luminal stem cells found in the normal breast. We propose that the plasticity of BCSCs that allows them to transition between EMT- and MET-like states endows these cells with the capacity for tissue invasion, dissemination, and growth at metastatic sites.

UR - https://www.scopus.com/pages/publications/84892619683

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DO - 10.1016/j.stemcr.2013.11.009

M3 - Article

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AN - SCOPUS:84892619683

SN - 2213-6711

VL - 2

SP - 78

EP - 91

JO - Stem Cell Reports

JF - Stem Cell Reports

IS - 1

ER -

Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts

Abstract

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