Epithelial‐Mesenchymal Transition‐Derived Cells Exhibit Multilineage Differentiation Potential Similar to Mesenchymal Stem Cells

The epithelial‐to‐mesenchymal transition (EMT) is an embryonic process that becomes latent in most normal adult tissues. Recently, we have shown that induction of EMT endows breast epithelial cells with stem cell traits. In this report, we have further characterized the EMT‐derived cells and shown t...

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Published in:	Stem cells (Dayton, Ohio) Vol. 28; no. 8; pp. 1435 - 1445
Main Authors:	Battula, Venkata Lokesh, Evans, Kurt William, Hollier, Brett George, Shi, Yuexi, Marini, Frank C., Ayyanan, Ayyakkannu, Wang, Rui‐yu, Brisken, Cathrin, Guerra, Rudy, Andreeff, Michael, Mani, Sendurai A.
Format:	Journal Article
Language:	English
Published:	Hoboken Wiley Subscription Services, Inc., A Wiley Company 01-08-2010
Subjects:	Adipocytes - cytology CD140b Cell Differentiation - genetics Cell Differentiation - physiology Cells, Cultured Chondrogenesis - genetics Chondrogenesis - physiology Epithelial-Mesenchymal Transition - genetics Epithelial-Mesenchymal Transition - physiology Epithelial‐mesenchymal transition Flow Cytometry Humans Mesenchymal stem cells Mesenchymal Stromal Cells - cytology Mesenchymal Stromal Cells - metabolism MSC Osteoblasts - cytology PDGFR‐β Receptor, Platelet-Derived Growth Factor beta - genetics Receptor, Platelet-Derived Growth Factor beta - metabolism Reverse Transcriptase Polymerase Chain Reaction Snail Twist
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Abstract	The epithelial‐to‐mesenchymal transition (EMT) is an embryonic process that becomes latent in most normal adult tissues. Recently, we have shown that induction of EMT endows breast epithelial cells with stem cell traits. In this report, we have further characterized the EMT‐derived cells and shown that these cells are similar to mesenchymal stem cells (MSCs) with the capacity to differentiate into multiple tissue lineages. For this purpose, we induced EMT by ectopic expression of Twist, Snail, or transforming growth factor‐β in immortalized human mammary epithelial cells. We found that the EMT‐derived cells and MSCs share many properties including the antigenic profile typical of MSCs, that is, CD44+, CD24−, and CD45−. Conversely, MSCs express EMT‐associated genes, such as Twist, Snail, and mesenchyme forkhead 1 (FOXC2). Interestingly, CD140b (platelet‐derived growth factor receptor‐β), a marker for naive MSCs, is exclusively expressed in EMT‐derived cells and not in their epithelial counterparts. Moreover, functional analyses revealed that EMT‐derived cells but not the control cells can differentiate into alizarin red S‐positive mature osteoblasts, oil red O‐positive adipocytes and alcian blue‐positive chondrocytes similar to MSCs. We also observed that EMT‐derived cells but not the control cells invade and migrate towards MDA‐MB‐231 breast cancer cells similar to MSCs. In vivo wound homing assays in nude mice revealed that the EMT‐derived cells home to wound sites similar to MSCs. In conclusion, we have demonstrated that the EMT‐derived cells are similar to MSCs in gene expression, multilineage differentiation, and ability to migrate towards tumor cells and wound sites. STEM CELLS 2010;28:1435–1445
AbstractList	The epithelial‐to‐mesenchymal transition (EMT) is an embryonic process that becomes latent in most normal adult tissues. Recently, we have shown that induction of EMT endows breast epithelial cells with stem cell traits. In this report, we have further characterized the EMT‐derived cells and shown that these cells are similar to mesenchymal stem cells (MSCs) with the capacity to differentiate into multiple tissue lineages. For this purpose, we induced EMT by ectopic expression of Twist, Snail, or transforming growth factor‐β in immortalized human mammary epithelial cells. We found that the EMT‐derived cells and MSCs share many properties including the antigenic profile typical of MSCs, that is, CD44+, CD24−, and CD45−. Conversely, MSCs express EMT‐associated genes, such as Twist, Snail, and mesenchyme forkhead 1 (FOXC2). Interestingly, CD140b (platelet‐derived growth factor receptor‐β), a marker for naive MSCs, is exclusively expressed in EMT‐derived cells and not in their epithelial counterparts. Moreover, functional analyses revealed that EMT‐derived cells but not the control cells can differentiate into alizarin red S‐positive mature osteoblasts, oil red O‐positive adipocytes and alcian blue‐positive chondrocytes similar to MSCs. We also observed that EMT‐derived cells but not the control cells invade and migrate towards MDA‐MB‐231 breast cancer cells similar to MSCs. In vivo wound homing assays in nude mice revealed that the EMT‐derived cells home to wound sites similar to MSCs. In conclusion, we have demonstrated that the EMT‐derived cells are similar to MSCs in gene expression, multilineage differentiation, and ability to migrate towards tumor cells and wound sites. STEM CELLS 2010;28:1435–1445 The epithelial-to-mesenchymal transition (EMT) is an embryonic process that becomes latent in most normal adult tissues. Recently, we have shown that induction of EMT endows breast epithelial cells with stem cell traits. In this report, we have further characterized the EMT-derived cells and shown that these cells are similar to mesenchymal stem cells (MSCs) with the capacity to differentiate into multiple tissue lineages. For this purpose, we induced EMT by ectopic expression of Twist, Snail, or transforming growth factor-beta in immortalized human mammary epithelial cells. We found that the EMT-derived cells and MSCs share many properties including the antigenic profile typical of MSCs, that is, CD44(+), CD24(-), and CD45(-). Conversely, MSCs express EMT-associated genes, such as Twist, Snail, and mesenchyme forkhead 1 (FOXC2). Interestingly, CD140b (platelet-derived growth factor receptor-beta), a marker for naive MSCs, is exclusively expressed in EMT-derived cells and not in their epithelial counterparts. Moreover, functional analyses revealed that EMT-derived cells but not the control cells can differentiate into alizarin red S-positive mature osteoblasts, oil red O-positive adipocytes and alcian blue-positive chondrocytes similar to MSCs. We also observed that EMT-derived cells but not the control cells invade and migrate towards MDA-MB-231 breast cancer cells similar to MSCs. In vivo wound homing assays in nude mice revealed that the EMT-derived cells home to wound sites similar to MSCs. In conclusion, we have demonstrated that the EMT-derived cells are similar to MSCs in gene expression, multilineage differentiation, and ability to migrate towards tumor cells and wound sites. The epithelial-to-mesenchymal transition (EMT) is an embryonic process that becomes latent in most normal adult tissues. Recently, we have shown that induction of EMT endows breast epithelial cells with stem cell traits. In this report, we have further characterized the EMT-derived cells and shown that these cells are similar to mesenchymal stem cells (MSCs) with the capacity to differentiate into multiple tissue lineages. For this purpose, we induced EMT by ectopic expression of Twist, Snail, or transforming growth factor-β in immortalized human mammary epithelial cells. We found that the EMT-derived cells and MSCs share many properties including the antigenic profile typical of MSCs, that is, CD44+, CD24−, and CD45−. Conversely, MSCs express EMT-associated genes, such as Twist, Snail, and mesenchyme forkhead 1 (FOXC2). Interestingly, CD140b (platelet-derived growth factor receptor-β), a marker for naive MSCs, is exclusively expressed in EMT-derived cells and not in their epithelial counterparts. Moreover, functional analyses revealed that EMT-derived cells but not the control cells can differentiate into alizarin red S-positive mature osteoblasts, oil red O-positive adipocytes and alcian blue-positive chondrocytes similar to MSCs. We also observed that EMT-derived cells but not the control cells invade and migrate towards MDA-MB-231 breast cancer cells similar to MSCs. In vivo wound homing assays in nude mice revealed that the EMT-derived cells home to wound sites similar to MSCs. In conclusion, we have demonstrated that the EMT-derived cells are similar to MSCs in gene expression, multilineage differentiation, and ability to migrate towards tumor cells and wound sites.
Author	Shi, Yuexi Ayyanan, Ayyakkannu Marini, Frank C. Battula, Venkata Lokesh Wang, Rui‐yu Andreeff, Michael Brisken, Cathrin Mani, Sendurai A. Guerra, Rudy Evans, Kurt William Hollier, Brett George
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Notes	First published online in STEM CELLS Author contributions: V.L.B.: conception and design, collection and assembly of data, data analysis and interpretation, manuscript writing; K.E.: collection and assembly of data, data analysis and interpretation, manuscript writing; B.G.H.: collection and assembly of data; Y.S.: collection and assembly of data; F.C.M.: collection and assembly of data, provision of study material; A.A.: collection and assembly of data, provision of study material; R.W.: collection and assembly of data, provision of study material; C.B.: provision of study material; M.A.: conception and design, data analysis and interpretation, financial support, final approval of the manuscript; S.A.M.: conception and design, data analysis and interpretation, financial support, manuscript writing, final approval of the manuscript. Disclosure of potential conflicts of interest is found at the end of this article. Telephone: 1‐713‐792‐9638; Fax: 1‐713‐834‐6082 EXPRESS June 22, 2010.
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PublicationYear	2010
Publisher	Wiley Subscription Services, Inc., A Wiley Company
Publisher_xml	– name: Wiley Subscription Services, Inc., A Wiley Company
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Snippet	The epithelial‐to‐mesenchymal transition (EMT) is an embryonic process that becomes latent in most normal adult tissues. Recently, we have shown that induction... The epithelial-to-mesenchymal transition (EMT) is an embryonic process that becomes latent in most normal adult tissues. Recently, we have shown that induction...
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SubjectTerms	Adipocytes - cytology CD140b Cell Differentiation - genetics Cell Differentiation - physiology Cells, Cultured Chondrogenesis - genetics Chondrogenesis - physiology Epithelial-Mesenchymal Transition - genetics Epithelial-Mesenchymal Transition - physiology Epithelial‐mesenchymal transition Flow Cytometry Humans Mesenchymal stem cells Mesenchymal Stromal Cells - cytology Mesenchymal Stromal Cells - metabolism MSC Osteoblasts - cytology PDGFR‐β Receptor, Platelet-Derived Growth Factor beta - genetics Receptor, Platelet-Derived Growth Factor beta - metabolism Reverse Transcriptase Polymerase Chain Reaction Snail Twist
Title	Epithelial‐Mesenchymal Transition‐Derived Cells Exhibit Multilineage Differentiation Potential Similar to Mesenchymal Stem Cells
URI	https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fstem.467 https://www.ncbi.nlm.nih.gov/pubmed/20572012
Volume	28
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