EMT Subtype Influences Epithelial Plasticity and Mode of Cell Migration
Epithelial-mesenchymal transition (EMT) is strongly implicated in tumor cell invasion and metastasis. EMT is thought to be regulated primarily at the transcriptional level through the repressive activity of EMT transcription factors. However, these classical mechanisms have been parsed out almost ex...
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| Published in | Developmental cell Vol. 45; no. 6; pp. 681 - 695.e4 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
18.06.2018
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Epithelial-mesenchymal transition (EMT) is strongly implicated in tumor cell invasion and metastasis. EMT is thought to be regulated primarily at the transcriptional level through the repressive activity of EMT transcription factors. However, these classical mechanisms have been parsed out almost exclusively in vitro, leaving questions about the programs driving EMT in physiological contexts. Here, using a lineage-labeled mouse model of pancreatic ductal adenocarcinoma to study EMT in vivo, we found that most tumors lose their epithelial phenotype through an alternative program involving protein internalization rather than transcriptional repression, resulting in a “partial EMT” phenotype. Carcinoma cells utilizing this program migrate as clusters, contrasting with the single-cell migration pattern associated with traditionally defined EMT mechanisms. Moreover, many breast and colorectal cancer cell lines utilize this alternative program to undergo EMT. Collectively, these results suggest that carcinoma cells have different ways of losing their epithelial program, resulting in distinct modes of invasion and dissemination.
[Display omitted]
•Pancreatic carcinoma cells use two distinct programs to undergo EMT•Transcriptional repression of epithelial genes mediates EMT in a minority of tumors•Re-localization of epithelial proteins mediates EMT in a majority of tumors•Different EMT programs are associated with different modes of invasion
Using a lineage-traced tumor model, Aiello et al. describe a program of epithelial-to-mesenchymal transition (EMT), conserved across several carcinomas, involving re-localization of epithelial proteins rather than transcriptional repression. This alternative program leads to a “partial EMT” phenotype that promotes collective tumor cell migration and formation of circulating tumor cell clusters. |
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| AbstractList | Epithelial-mesenchymal-transition (EMT) is strongly implicated in tumor cell invasion and metastasis. EMT is thought to be regulated primarily at the transcriptional level through the repressive activity of EMT transcription factors. However, these classical mechanisms have been parsed out almost exclusively
in vitro
, leaving questions about the programs driving EMT in physiological contexts. Here, using a lineage-labeled mouse model of pancreatic ductal adenocarcinoma to study EMT
in vivo
, we found that most tumors lose their epithelial phenotype through an alternative program involving protein internalization rather than transcriptional repression, resulting in a “partial EMT” phenotype. Carcinoma cells utilizing this program migrate as clusters, contrasting with the single-cell migration pattern associated with traditionally-defined EMT mechanisms. Moreover, many breast and colorectal cancer cell lines utilize this alternative program to undergo EMT. Collectively, these results suggest that carcinoma cells have different ways of losing their epithelial program, resulting in distinct modes of invasion and dissemination.
Using a lineage-traced tumor model, Aiello et al. describe a program of epithelial-to-mesenchymal transition (EMT), conserved across several carcinomas, involving re-localization of epithelial proteins rather than transcriptional repression. This alternative program leads to a “partial EMT” phenotype that promotes collective tumor cell migration and formation of circulating tumor cell clusters. Epithelial-mesenchymal transition (EMT) is strongly implicated in tumor cell invasion and metastasis. EMT is thought to be regulated primarily at the transcriptional level through the repressive activity of EMT transcription factors. However, these classical mechanisms have been parsed out almost exclusively in vitro, leaving questions about the programs driving EMT in physiological contexts. Here, using a lineage-labeled mouse model of pancreatic ductal adenocarcinoma to study EMT in vivo, we found that most tumors lose their epithelial phenotype through an alternative program involving protein internalization rather than transcriptional repression, resulting in a “partial EMT” phenotype. Carcinoma cells utilizing this program migrate as clusters, contrasting with the single-cell migration pattern associated with traditionally defined EMT mechanisms. Moreover, many breast and colorectal cancer cell lines utilize this alternative program to undergo EMT. Collectively, these results suggest that carcinoma cells have different ways of losing their epithelial program, resulting in distinct modes of invasion and dissemination. [Display omitted] •Pancreatic carcinoma cells use two distinct programs to undergo EMT•Transcriptional repression of epithelial genes mediates EMT in a minority of tumors•Re-localization of epithelial proteins mediates EMT in a majority of tumors•Different EMT programs are associated with different modes of invasion Using a lineage-traced tumor model, Aiello et al. describe a program of epithelial-to-mesenchymal transition (EMT), conserved across several carcinomas, involving re-localization of epithelial proteins rather than transcriptional repression. This alternative program leads to a “partial EMT” phenotype that promotes collective tumor cell migration and formation of circulating tumor cell clusters. Epithelial-mesenchymal transition (EMT) is strongly implicated in tumor cell invasion and metastasis. EMT is thought to be regulated primarily at the transcriptional level through the repressive activity of EMT transcription factors. However, these classical mechanisms have been parsed out almost exclusively in vitro, leaving questions about the programs driving EMT in physiological contexts. Here, using a lineage-labeled mouse model of pancreatic ductal adenocarcinoma to study EMT in vivo, we found that most tumors lose their epithelial phenotype through an alternative program involving protein internalization rather than transcriptional repression, resulting in a "partial EMT" phenotype. Carcinoma cells utilizing this program migrate as clusters, contrasting with the single-cell migration pattern associated with traditionally defined EMT mechanisms. Moreover, many breast and colorectal cancer cell lines utilize this alternative program to undergo EMT. Collectively, these results suggest that carcinoma cells have different ways of losing their epithelial program, resulting in distinct modes of invasion and dissemination.Epithelial-mesenchymal transition (EMT) is strongly implicated in tumor cell invasion and metastasis. EMT is thought to be regulated primarily at the transcriptional level through the repressive activity of EMT transcription factors. However, these classical mechanisms have been parsed out almost exclusively in vitro, leaving questions about the programs driving EMT in physiological contexts. Here, using a lineage-labeled mouse model of pancreatic ductal adenocarcinoma to study EMT in vivo, we found that most tumors lose their epithelial phenotype through an alternative program involving protein internalization rather than transcriptional repression, resulting in a "partial EMT" phenotype. Carcinoma cells utilizing this program migrate as clusters, contrasting with the single-cell migration pattern associated with traditionally defined EMT mechanisms. Moreover, many breast and colorectal cancer cell lines utilize this alternative program to undergo EMT. Collectively, these results suggest that carcinoma cells have different ways of losing their epithelial program, resulting in distinct modes of invasion and dissemination. Epithelial-mesenchymal transition (EMT) is strongly implicated in tumor cell invasion and metastasis. EMT is thought to be regulated primarily at the transcriptional level through the repressive activity of EMT transcription factors. However, these classical mechanisms have been parsed out almost exclusively in vitro, leaving questions about the programs driving EMT in physiological contexts. Here, using a lineage-labeled mouse model of pancreatic ductal adenocarcinoma to study EMT in vivo, we found that most tumors lose their epithelial phenotype through an alternative program involving protein internalization rather than transcriptional repression, resulting in a "partial EMT" phenotype. Carcinoma cells utilizing this program migrate as clusters, contrasting with the single-cell migration pattern associated with traditionally defined EMT mechanisms. Moreover, many breast and colorectal cancer cell lines utilize this alternative program to undergo EMT. Collectively, these results suggest that carcinoma cells have different ways of losing their epithelial program, resulting in distinct modes of invasion and dissemination. |
| Author | Aiello, Nicole M. Norgard, Robert J. Yuan, Salina Li, Jinyang Black, Taylor Stanger, Ben Z. Sahmoud, Amine Balli, David Maddipati, Ravikanth Yamazoe, Taiji Bar-Sagi, Dafna Furth, Emma E. |
| AuthorAffiliation | d Department of Cell and Developmental Biology, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA 19104, USA a Department of Medicine, Gastroenterology Division, and Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA c Department of Biochemistry and Molecular Pharmacology, New York University School of Medicine, New York, NY 10016, USA b Department of Pathology and Laboratory Medicine, Hospital of the University of Pennsylvania, Philadelphia, PA 19104 USA |
| AuthorAffiliation_xml | – name: b Department of Pathology and Laboratory Medicine, Hospital of the University of Pennsylvania, Philadelphia, PA 19104 USA – name: d Department of Cell and Developmental Biology, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA 19104, USA – name: c Department of Biochemistry and Molecular Pharmacology, New York University School of Medicine, New York, NY 10016, USA – name: a Department of Medicine, Gastroenterology Division, and Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA |
| Author_xml | – sequence: 1 givenname: Nicole M. surname: Aiello fullname: Aiello, Nicole M. organization: Department of Medicine, Gastroenterology Division, Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Pennsylvania, 421 Curie Blvd, 512 BRB II/III, Philadelphia, PA 19104, USA – sequence: 2 givenname: Ravikanth surname: Maddipati fullname: Maddipati, Ravikanth organization: Department of Medicine, Gastroenterology Division, Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Pennsylvania, 421 Curie Blvd, 512 BRB II/III, Philadelphia, PA 19104, USA – sequence: 3 givenname: Robert J. surname: Norgard fullname: Norgard, Robert J. organization: Department of Medicine, Gastroenterology Division, Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Pennsylvania, 421 Curie Blvd, 512 BRB II/III, Philadelphia, PA 19104, USA – sequence: 4 givenname: David surname: Balli fullname: Balli, David organization: Department of Medicine, Gastroenterology Division, Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Pennsylvania, 421 Curie Blvd, 512 BRB II/III, Philadelphia, PA 19104, USA – sequence: 5 givenname: Jinyang surname: Li fullname: Li, Jinyang organization: Department of Medicine, Gastroenterology Division, Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Pennsylvania, 421 Curie Blvd, 512 BRB II/III, Philadelphia, PA 19104, USA – sequence: 6 givenname: Salina surname: Yuan fullname: Yuan, Salina organization: Department of Medicine, Gastroenterology Division, Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Pennsylvania, 421 Curie Blvd, 512 BRB II/III, Philadelphia, PA 19104, USA – sequence: 7 givenname: Taiji surname: Yamazoe fullname: Yamazoe, Taiji organization: Department of Medicine, Gastroenterology Division, Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Pennsylvania, 421 Curie Blvd, 512 BRB II/III, Philadelphia, PA 19104, USA – sequence: 8 givenname: Taylor surname: Black fullname: Black, Taylor organization: Department of Medicine, Gastroenterology Division, Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Pennsylvania, 421 Curie Blvd, 512 BRB II/III, Philadelphia, PA 19104, USA – sequence: 9 givenname: Amine surname: Sahmoud fullname: Sahmoud, Amine organization: Department of Medicine, Gastroenterology Division, Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Pennsylvania, 421 Curie Blvd, 512 BRB II/III, Philadelphia, PA 19104, USA – sequence: 10 givenname: Emma E. surname: Furth fullname: Furth, Emma E. organization: Department of Pathology and Laboratory Medicine, Hospital of the University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 11 givenname: Dafna surname: Bar-Sagi fullname: Bar-Sagi, Dafna organization: Department of Biochemistry and Molecular Pharmacology, New York University School of Medicine, New York, NY 10016, USA – sequence: 12 givenname: Ben Z. surname: Stanger fullname: Stanger, Ben Z. email: bstanger@exchange.upenn.edu organization: Department of Medicine, Gastroenterology Division, Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Pennsylvania, 421 Curie Blvd, 512 BRB II/III, Philadelphia, PA 19104, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29920274$$D View this record in MEDLINE/PubMed |
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| Keywords | pancreatic cancer partial EMT metastasis tumor cell clusters epithelial-mesenchymal transition lineage tracing circulating tumor cells collective migration E-cadherin |
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| Snippet | Epithelial-mesenchymal transition (EMT) is strongly implicated in tumor cell invasion and metastasis. EMT is thought to be regulated primarily at the... Epithelial-mesenchymal-transition (EMT) is strongly implicated in tumor cell invasion and metastasis. EMT is thought to be regulated primarily at the... |
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| SubjectTerms | Animals Cadherins - metabolism Cadherins - physiology Cell Line, Tumor Cell Movement - genetics Cell Plasticity - physiology circulating tumor cells collective migration E-cadherin Epithelial Cells - physiology epithelial-mesenchymal transition Epithelial-Mesenchymal Transition - physiology Gene Expression Regulation, Neoplastic - genetics Humans lineage tracing metastasis Mice Neoplasm Invasiveness - genetics pancreatic cancer Pancreatic Neoplasms Pancreatic Neoplasms - metabolism partial EMT Signal Transduction Transcription Factors - metabolism tumor cell clusters |
| Title | EMT Subtype Influences Epithelial Plasticity and Mode of Cell Migration |
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