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DPYSL3 modulates mitosis, migration, and epithelial-to-mesenchymal transition in claudin-low breast cancer
A Clinical Proteomic Tumor Analysis Consortium (CPTAC) proteogenomic analysis prioritized dihydropyrimidinase-like-3 (DPYSL3) as a multilevel (RNA/protein/phosphoprotein) expression outlier specific to the claudin-low (CLOW) subset of triple-negative breast cancers. A PubMed informatics tool indicat...
Autores principales: | , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2018
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6305012/ https://www.ncbi.nlm.nih.gov/pubmed/30498031 http://dx.doi.org/10.1073/pnas.1810598115 |
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author | Matsunuma, Ryoichi Chan, Doug W. Kim, Beom-Jun Singh, Purba Han, Airi Saltzman, Alexander B. Cheng, Chonghui Lei, Jonathan T. Wang, Junkai Roberto da Silva, Leonardo Sahin, Ergun Leng, Mei Fan, Cheng Perou, Charles M. Malovannaya, Anna Ellis, Matthew J. |
author_facet | Matsunuma, Ryoichi Chan, Doug W. Kim, Beom-Jun Singh, Purba Han, Airi Saltzman, Alexander B. Cheng, Chonghui Lei, Jonathan T. Wang, Junkai Roberto da Silva, Leonardo Sahin, Ergun Leng, Mei Fan, Cheng Perou, Charles M. Malovannaya, Anna Ellis, Matthew J. |
author_sort | Matsunuma, Ryoichi |
collection | PubMed |
description | A Clinical Proteomic Tumor Analysis Consortium (CPTAC) proteogenomic analysis prioritized dihydropyrimidinase-like-3 (DPYSL3) as a multilevel (RNA/protein/phosphoprotein) expression outlier specific to the claudin-low (CLOW) subset of triple-negative breast cancers. A PubMed informatics tool indicated a paucity of data in the context of breast cancer, which further prioritized DPYSL3 for study. DPYSL3 knockdown in DPYSL3-positive ([Formula: see text]) CLOW cell lines demonstrated reduced proliferation, yet enhanced motility and increased expression of epithelial-to-mesenchymal transition (EMT) markers, suggesting that DPYSL3 is a multifunctional signaling modulator. Slower proliferation in DPYSL3-negative ([Formula: see text]) CLOW cells was associated with accumulation of multinucleated cells, indicating a mitotic defect that was associated with a collapse of the vimentin microfilament network and increased vimentin phosphorylation. DPYSL3 also suppressed the expression of EMT regulators SNAIL and TWIST and opposed p21 activated kinase 2 (PAK2)-dependent migration. However, these EMT regulators in turn induce DPYSL3 expression, suggesting that DPYSL3 participates in negative feedback on EMT. In conclusion, DPYSL3 expression identifies CLOW tumors that will be sensitive to approaches that promote vimentin phosphorylation during mitosis and inhibitors of PAK signaling during migration and EMT. |
format | Online Article Text |
id | pubmed-6305012 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-63050122018-12-28 DPYSL3 modulates mitosis, migration, and epithelial-to-mesenchymal transition in claudin-low breast cancer Matsunuma, Ryoichi Chan, Doug W. Kim, Beom-Jun Singh, Purba Han, Airi Saltzman, Alexander B. Cheng, Chonghui Lei, Jonathan T. Wang, Junkai Roberto da Silva, Leonardo Sahin, Ergun Leng, Mei Fan, Cheng Perou, Charles M. Malovannaya, Anna Ellis, Matthew J. Proc Natl Acad Sci U S A PNAS Plus A Clinical Proteomic Tumor Analysis Consortium (CPTAC) proteogenomic analysis prioritized dihydropyrimidinase-like-3 (DPYSL3) as a multilevel (RNA/protein/phosphoprotein) expression outlier specific to the claudin-low (CLOW) subset of triple-negative breast cancers. A PubMed informatics tool indicated a paucity of data in the context of breast cancer, which further prioritized DPYSL3 for study. DPYSL3 knockdown in DPYSL3-positive ([Formula: see text]) CLOW cell lines demonstrated reduced proliferation, yet enhanced motility and increased expression of epithelial-to-mesenchymal transition (EMT) markers, suggesting that DPYSL3 is a multifunctional signaling modulator. Slower proliferation in DPYSL3-negative ([Formula: see text]) CLOW cells was associated with accumulation of multinucleated cells, indicating a mitotic defect that was associated with a collapse of the vimentin microfilament network and increased vimentin phosphorylation. DPYSL3 also suppressed the expression of EMT regulators SNAIL and TWIST and opposed p21 activated kinase 2 (PAK2)-dependent migration. However, these EMT regulators in turn induce DPYSL3 expression, suggesting that DPYSL3 participates in negative feedback on EMT. In conclusion, DPYSL3 expression identifies CLOW tumors that will be sensitive to approaches that promote vimentin phosphorylation during mitosis and inhibitors of PAK signaling during migration and EMT. National Academy of Sciences 2018-12-18 2018-11-29 /pmc/articles/PMC6305012/ /pubmed/30498031 http://dx.doi.org/10.1073/pnas.1810598115 Text en Copyright © 2018 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . |
spellingShingle | PNAS Plus Matsunuma, Ryoichi Chan, Doug W. Kim, Beom-Jun Singh, Purba Han, Airi Saltzman, Alexander B. Cheng, Chonghui Lei, Jonathan T. Wang, Junkai Roberto da Silva, Leonardo Sahin, Ergun Leng, Mei Fan, Cheng Perou, Charles M. Malovannaya, Anna Ellis, Matthew J. DPYSL3 modulates mitosis, migration, and epithelial-to-mesenchymal transition in claudin-low breast cancer |
title | DPYSL3 modulates mitosis, migration, and epithelial-to-mesenchymal transition in claudin-low breast cancer |
title_full | DPYSL3 modulates mitosis, migration, and epithelial-to-mesenchymal transition in claudin-low breast cancer |
title_fullStr | DPYSL3 modulates mitosis, migration, and epithelial-to-mesenchymal transition in claudin-low breast cancer |
title_full_unstemmed | DPYSL3 modulates mitosis, migration, and epithelial-to-mesenchymal transition in claudin-low breast cancer |
title_short | DPYSL3 modulates mitosis, migration, and epithelial-to-mesenchymal transition in claudin-low breast cancer |
title_sort | dpysl3 modulates mitosis, migration, and epithelial-to-mesenchymal transition in claudin-low breast cancer |
topic | PNAS Plus |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6305012/ https://www.ncbi.nlm.nih.gov/pubmed/30498031 http://dx.doi.org/10.1073/pnas.1810598115 |
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