Identification of the SUMO E3 ligase PIAS1 as a potential survival biomarker in breast cancer
Metastasis is the ultimate cause of breast cancer related mortality. Epithelial-mesenchymal transition (EMT) is thought to play a crucial role in the metastatic potential of breast cancer. Growing evidence has implicated the SUMO E3 ligase PIAS1 in the regulation of EMT in mammary epithelial cells a...
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| creator | Chanda, Ayan Chan, Angela Deng, Lili Kornaga, Elizabeth N Enwere, Emeka K Morris, Donald G Bonni, Shirin |
| description | Metastasis is the ultimate cause of breast cancer related mortality. Epithelial-mesenchymal transition (EMT) is thought to play a crucial role in the metastatic potential of breast cancer. Growing evidence has implicated the SUMO E3 ligase PIAS1 in the regulation of EMT in mammary epithelial cells and breast cancer metastasis. However, the relevance of PIAS1 in human cancer and mechanisms by which PIAS1 might regulate breast cancer metastasis remain to be elucidated. Using tissue-microarray analysis (TMA), we report that the protein abundance and subcellular localization of PIAS1 correlate with disease specific overall survival of a cohort of breast cancer patients. In mechanistic studies, we find that PIAS1 acts via sumoylation of the transcriptional regulator SnoN to suppress invasive growth of MDA-MB-231 human breast cancer cell-derived organoids. Our studies thus identify the SUMO E3 ligase PIAS1 as a prognostic biomarker in breast cancer, and suggest a potential role for the PIAS1-SnoN sumoylation pathway in controlling breast cancer metastasis. |
| doi_str_mv | 10.1371/journal.pone.0177639 |
| format | Article |
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Epithelial-mesenchymal transition (EMT) is thought to play a crucial role in the metastatic potential of breast cancer. Growing evidence has implicated the SUMO E3 ligase PIAS1 in the regulation of EMT in mammary epithelial cells and breast cancer metastasis. However, the relevance of PIAS1 in human cancer and mechanisms by which PIAS1 might regulate breast cancer metastasis remain to be elucidated. Using tissue-microarray analysis (TMA), we report that the protein abundance and subcellular localization of PIAS1 correlate with disease specific overall survival of a cohort of breast cancer patients. In mechanistic studies, we find that PIAS1 acts via sumoylation of the transcriptional regulator SnoN to suppress invasive growth of MDA-MB-231 human breast cancer cell-derived organoids. Our studies thus identify the SUMO E3 ligase PIAS1 as a prognostic biomarker in breast cancer, and suggest a potential role for the PIAS1-SnoN sumoylation pathway in controlling breast cancer metastasis.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0177639</identifier><identifier>PMID: 28493978</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Abundance ; Adult ; Aged ; Aged, 80 and over ; Analysis ; Biochemistry ; Biology and life sciences ; Biomarkers ; Biomarkers, Tumor - metabolism ; Breast cancer ; Breast Neoplasms - enzymology ; Breast Neoplasms - pathology ; Cancer ; Cancer metastasis ; Cell cycle ; Cell Line, Tumor ; Cell Nucleus - drug effects ; Cell Nucleus - metabolism ; Cell Proliferation - drug effects ; Cohort Studies ; Diagnosis ; DNA microarrays ; Epithelial cells ; Female ; Growth factors ; Health aspects ; Health services ; HEK293 Cells ; Humans ; Invasiveness ; Laboratories ; Ligases ; Localization ; Mammary gland ; Medicine and Health Sciences ; Mesenchyme ; Metastases ; Metastasis ; Middle Aged ; Molecular biology ; Neoplasm Invasiveness ; Organoids ; Organoids - drug effects ; Patients ; Plasmids ; Protein Inhibitors of Activated STAT - metabolism ; Protein Stability - drug effects ; Protein Transport - drug effects ; Proteins ; Research and Analysis Methods ; Risk factors ; Skin cancer ; Small Ubiquitin-Related Modifier Proteins - metabolism ; SUMO protein ; Sumoylation - drug effects ; Survival ; Survival Analysis ; Tissue analysis ; Tissue Array Analysis ; Transcription ; Transforming Growth Factor beta - pharmacology ; Transforming growth factors ; Ubiquitin-protein ligase</subject><ispartof>PloS one, 2017-05, Vol.12 (5), p.e0177639-e0177639</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Chanda et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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Epithelial-mesenchymal transition (EMT) is thought to play a crucial role in the metastatic potential of breast cancer. Growing evidence has implicated the SUMO E3 ligase PIAS1 in the regulation of EMT in mammary epithelial cells and breast cancer metastasis. However, the relevance of PIAS1 in human cancer and mechanisms by which PIAS1 might regulate breast cancer metastasis remain to be elucidated. Using tissue-microarray analysis (TMA), we report that the protein abundance and subcellular localization of PIAS1 correlate with disease specific overall survival of a cohort of breast cancer patients. In mechanistic studies, we find that PIAS1 acts via sumoylation of the transcriptional regulator SnoN to suppress invasive growth of MDA-MB-231 human breast cancer cell-derived organoids. 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metabolism</topic><topic>Breast cancer</topic><topic>Breast Neoplasms - enzymology</topic><topic>Breast Neoplasms - pathology</topic><topic>Cancer</topic><topic>Cancer metastasis</topic><topic>Cell cycle</topic><topic>Cell Line, Tumor</topic><topic>Cell Nucleus - drug effects</topic><topic>Cell Nucleus - metabolism</topic><topic>Cell Proliferation - drug effects</topic><topic>Cohort Studies</topic><topic>Diagnosis</topic><topic>DNA microarrays</topic><topic>Epithelial cells</topic><topic>Female</topic><topic>Growth factors</topic><topic>Health aspects</topic><topic>Health services</topic><topic>HEK293 Cells</topic><topic>Humans</topic><topic>Invasiveness</topic><topic>Laboratories</topic><topic>Ligases</topic><topic>Localization</topic><topic>Mammary gland</topic><topic>Medicine and Health Sciences</topic><topic>Mesenchyme</topic><topic>Metastases</topic><topic>Metastasis</topic><topic>Middle Aged</topic><topic>Molecular biology</topic><topic>Neoplasm Invasiveness</topic><topic>Organoids</topic><topic>Organoids - drug effects</topic><topic>Patients</topic><topic>Plasmids</topic><topic>Protein Inhibitors of Activated STAT - metabolism</topic><topic>Protein Stability - drug effects</topic><topic>Protein Transport - drug effects</topic><topic>Proteins</topic><topic>Research and Analysis Methods</topic><topic>Risk factors</topic><topic>Skin cancer</topic><topic>Small Ubiquitin-Related Modifier Proteins - metabolism</topic><topic>SUMO protein</topic><topic>Sumoylation - drug effects</topic><topic>Survival</topic><topic>Survival Analysis</topic><topic>Tissue analysis</topic><topic>Tissue Array Analysis</topic><topic>Transcription</topic><topic>Transforming Growth Factor beta - pharmacology</topic><topic>Transforming growth factors</topic><topic>Ubiquitin-protein ligase</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chanda, Ayan</creatorcontrib><creatorcontrib>Chan, Angela</creatorcontrib><creatorcontrib>Deng, Lili</creatorcontrib><creatorcontrib>Kornaga, Elizabeth N</creatorcontrib><creatorcontrib>Enwere, Emeka K</creatorcontrib><creatorcontrib>Morris, Donald G</creatorcontrib><creatorcontrib>Bonni, Shirin</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chanda, Ayan</au><au>Chan, Angela</au><au>Deng, Lili</au><au>Kornaga, Elizabeth N</au><au>Enwere, Emeka K</au><au>Morris, Donald G</au><au>Bonni, Shirin</au><au>Agoulnik, Irina U</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Identification of the SUMO E3 ligase PIAS1 as a potential survival biomarker in breast cancer</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2017-05-11</date><risdate>2017</risdate><volume>12</volume><issue>5</issue><spage>e0177639</spage><epage>e0177639</epage><pages>e0177639-e0177639</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Metastasis is the ultimate cause of breast cancer related mortality. Epithelial-mesenchymal transition (EMT) is thought to play a crucial role in the metastatic potential of breast cancer. Growing evidence has implicated the SUMO E3 ligase PIAS1 in the regulation of EMT in mammary epithelial cells and breast cancer metastasis. However, the relevance of PIAS1 in human cancer and mechanisms by which PIAS1 might regulate breast cancer metastasis remain to be elucidated. Using tissue-microarray analysis (TMA), we report that the protein abundance and subcellular localization of PIAS1 correlate with disease specific overall survival of a cohort of breast cancer patients. In mechanistic studies, we find that PIAS1 acts via sumoylation of the transcriptional regulator SnoN to suppress invasive growth of MDA-MB-231 human breast cancer cell-derived organoids. Our studies thus identify the SUMO E3 ligase PIAS1 as a prognostic biomarker in breast cancer, and suggest a potential role for the PIAS1-SnoN sumoylation pathway in controlling breast cancer metastasis.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>28493978</pmid><doi>10.1371/journal.pone.0177639</doi><tpages>e0177639</tpages><orcidid>https://orcid.org/0000-0002-2692-8558</orcidid><oa>free_for_read</oa></addata></record> |
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| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1897800403 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS); PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Abundance Adult Aged Aged, 80 and over Analysis Biochemistry Biology and life sciences Biomarkers Biomarkers, Tumor - metabolism Breast cancer Breast Neoplasms - enzymology Breast Neoplasms - pathology Cancer Cancer metastasis Cell cycle Cell Line, Tumor Cell Nucleus - drug effects Cell Nucleus - metabolism Cell Proliferation - drug effects Cohort Studies Diagnosis DNA microarrays Epithelial cells Female Growth factors Health aspects Health services HEK293 Cells Humans Invasiveness Laboratories Ligases Localization Mammary gland Medicine and Health Sciences Mesenchyme Metastases Metastasis Middle Aged Molecular biology Neoplasm Invasiveness Organoids Organoids - drug effects Patients Plasmids Protein Inhibitors of Activated STAT - metabolism Protein Stability - drug effects Protein Transport - drug effects Proteins Research and Analysis Methods Risk factors Skin cancer Small Ubiquitin-Related Modifier Proteins - metabolism SUMO protein Sumoylation - drug effects Survival Survival Analysis Tissue analysis Tissue Array Analysis Transcription Transforming Growth Factor beta - pharmacology Transforming growth factors Ubiquitin-protein ligase |
| title | Identification of the SUMO E3 ligase PIAS1 as a potential survival biomarker in breast cancer |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-05T14%3A09%3A47IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Identification%20of%20the%20SUMO%20E3%20ligase%20PIAS1%20as%20a%20potential%20survival%20biomarker%20in%20breast%20cancer&rft.jtitle=PloS%20one&rft.au=Chanda,%20Ayan&rft.date=2017-05-11&rft.volume=12&rft.issue=5&rft.spage=e0177639&rft.epage=e0177639&rft.pages=e0177639-e0177639&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0177639&rft_dat=%3Cgale_plos_%3EA491534945%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1897800403&rft_id=info:pmid/28493978&rft_galeid=A491534945&rft_doaj_id=oai_doaj_org_article_73cf0300ae144afcbf3fc1ec1ee89d5b&rfr_iscdi=true |