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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...

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Autores principales: 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.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2018
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.
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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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