Inducible formation of leader cells driven by CD44 switching gives rise to collective invasion and metastases in luminal breast carcinomas
Collective invasion into adjacent tissue is a hallmark of luminal breast cancer, and ~20% of these cases eventually undergo metastasis. How less aggressive luminal-like breast cancer transitions to invasive cancer remains unclear. Our study revealed that CD44 hi cancer cells are the leading subpopul...
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| Veröffentlicht in: | Oncogene 2019-11, Vol.38 (46), p.7113-7132 |
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| creator | Yang, Cuixia Cao, Manlin Liu, Yiwen He, Yiqing Du, Yan Zhang, Guoliang Gao, Feng |
| description | Collective invasion into adjacent tissue is a hallmark of luminal breast cancer, and ~20% of these cases eventually undergo metastasis. How less aggressive luminal-like breast cancer transitions to invasive cancer remains unclear. Our study revealed that CD44
hi
cancer cells are the leading subpopulation in collectively invading luminal cancer cells and efficiently promote the collective invasion of CD44
lo
/follower cells. The CD44
hi
/leader subpopulation showed a specific gene signature of various hybrid epithelial/mesenchymal genes and key functional coregulators of collective invasion, which was distinct from that of CD44
lo
/follower cells. However, the CD44
hi
/leader cells, which showed a partial epithelial–mesenchymal transition (EMT) phenotype, readily switched to the CD44
lo
phenotype along with collective migration and vice versa; this phenomenon was spontaneous and sensitive to the tumor microenvironment. The CD44
lo
-to-CD44
hi
conversion was accompanied by a shift in CD44s to CD44v but not a conversion of non-cancer stem cells to cancer stem cells (CSCs). Therefore, the CD44
hi
leader cells, as currently identified, are not a stable subpopulation in breast tumors. This plasticity and ability to generate CD44
hi
carcinoma cells with enhanced migratory and invasive behavior might be responsible for the transition from in situ to invasive behavior of luminal-type breast cancer. |
| doi_str_mv | 10.1038/s41388-019-0899-y |
| format | Article |
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hi
cancer cells are the leading subpopulation in collectively invading luminal cancer cells and efficiently promote the collective invasion of CD44
lo
/follower cells. The CD44
hi
/leader subpopulation showed a specific gene signature of various hybrid epithelial/mesenchymal genes and key functional coregulators of collective invasion, which was distinct from that of CD44
lo
/follower cells. However, the CD44
hi
/leader cells, which showed a partial epithelial–mesenchymal transition (EMT) phenotype, readily switched to the CD44
lo
phenotype along with collective migration and vice versa; this phenomenon was spontaneous and sensitive to the tumor microenvironment. The CD44
lo
-to-CD44
hi
conversion was accompanied by a shift in CD44s to CD44v but not a conversion of non-cancer stem cells to cancer stem cells (CSCs). Therefore, the CD44
hi
leader cells, as currently identified, are not a stable subpopulation in breast tumors. This plasticity and ability to generate CD44
hi
carcinoma cells with enhanced migratory and invasive behavior might be responsible for the transition from in situ to invasive behavior of luminal-type breast cancer.</description><identifier>ISSN: 0950-9232</identifier><identifier>EISSN: 1476-5594</identifier><identifier>DOI: 10.1038/s41388-019-0899-y</identifier><identifier>PMID: 31417182</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>38 ; 38/1 ; 38/35 ; 38/39 ; 38/77 ; 631/67/1347 ; 631/67/322 ; 64 ; 64/60 ; 96/10 ; 96/31 ; Animals ; Apoptosis ; Breast cancer ; Breast carcinoma ; Breast Neoplasms - metabolism ; Breast Neoplasms - pathology ; Cancer ; Carcinoma - metabolism ; Carcinoma - pathology ; CD44 antigen ; Cell Biology ; Cell migration ; Cell Movement - physiology ; Female ; Human Genetics ; Humans ; Hyaluronan Receptors - metabolism ; Internal Medicine ; Invasiveness ; Medicine ; Medicine & Public Health ; Mesenchyme ; Metastases ; Metastasis ; Mice ; Neoplasm Invasiveness - pathology ; Oncology ; Oncology, Experimental ; Phenotypes ; Stem cells ; Tumors</subject><ispartof>Oncogene, 2019-11, Vol.38 (46), p.7113-7132</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited 2019</rights><rights>COPYRIGHT 2019 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Nov 2019</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c553t-6fea524c8c9484fb4b2e2c8b87454b6e6c8c88e26d8e62b15bee011737fcb8a03</citedby><cites>FETCH-LOGICAL-c553t-6fea524c8c9484fb4b2e2c8b87454b6e6c8c88e26d8e62b15bee011737fcb8a03</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s41388-019-0899-y$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41388-019-0899-y$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,776,780,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31417182$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yang, Cuixia</creatorcontrib><creatorcontrib>Cao, Manlin</creatorcontrib><creatorcontrib>Liu, Yiwen</creatorcontrib><creatorcontrib>He, Yiqing</creatorcontrib><creatorcontrib>Du, Yan</creatorcontrib><creatorcontrib>Zhang, Guoliang</creatorcontrib><creatorcontrib>Gao, Feng</creatorcontrib><title>Inducible formation of leader cells driven by CD44 switching gives rise to collective invasion and metastases in luminal breast carcinomas</title><title>Oncogene</title><addtitle>Oncogene</addtitle><addtitle>Oncogene</addtitle><description>Collective invasion into adjacent tissue is a hallmark of luminal breast cancer, and ~20% of these cases eventually undergo metastasis. How less aggressive luminal-like breast cancer transitions to invasive cancer remains unclear. Our study revealed that CD44
hi
cancer cells are the leading subpopulation in collectively invading luminal cancer cells and efficiently promote the collective invasion of CD44
lo
/follower cells. The CD44
hi
/leader subpopulation showed a specific gene signature of various hybrid epithelial/mesenchymal genes and key functional coregulators of collective invasion, which was distinct from that of CD44
lo
/follower cells. However, the CD44
hi
/leader cells, which showed a partial epithelial–mesenchymal transition (EMT) phenotype, readily switched to the CD44
lo
phenotype along with collective migration and vice versa; this phenomenon was spontaneous and sensitive to the tumor microenvironment. The CD44
lo
-to-CD44
hi
conversion was accompanied by a shift in CD44s to CD44v but not a conversion of non-cancer stem cells to cancer stem cells (CSCs). Therefore, the CD44
hi
leader cells, as currently identified, are not a stable subpopulation in breast tumors. This plasticity and ability to generate CD44
hi
carcinoma cells with enhanced migratory and invasive behavior might be responsible for the transition from in situ to invasive behavior of luminal-type breast cancer.</description><subject>38</subject><subject>38/1</subject><subject>38/35</subject><subject>38/39</subject><subject>38/77</subject><subject>631/67/1347</subject><subject>631/67/322</subject><subject>64</subject><subject>64/60</subject><subject>96/10</subject><subject>96/31</subject><subject>Animals</subject><subject>Apoptosis</subject><subject>Breast cancer</subject><subject>Breast carcinoma</subject><subject>Breast Neoplasms - metabolism</subject><subject>Breast Neoplasms - pathology</subject><subject>Cancer</subject><subject>Carcinoma - metabolism</subject><subject>Carcinoma - pathology</subject><subject>CD44 antigen</subject><subject>Cell Biology</subject><subject>Cell migration</subject><subject>Cell Movement - physiology</subject><subject>Female</subject><subject>Human Genetics</subject><subject>Humans</subject><subject>Hyaluronan Receptors - metabolism</subject><subject>Internal Medicine</subject><subject>Invasiveness</subject><subject>Medicine</subject><subject>Medicine & Public Health</subject><subject>Mesenchyme</subject><subject>Metastases</subject><subject>Metastasis</subject><subject>Mice</subject><subject>Neoplasm Invasiveness - pathology</subject><subject>Oncology</subject><subject>Oncology, Experimental</subject><subject>Phenotypes</subject><subject>Stem cells</subject><subject>Tumors</subject><issn>0950-9232</issn><issn>1476-5594</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>BENPR</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNp1kd1qFTEUhYMotlYfwBsJeOPN1PzOJJfl-FcoeKPXIcnsOaZkkprMtJxX8KnNcKpFURIIrHx7Ze8shF5Sck4JV2-roFypjlDdEaV1d3iETqkY-k5KLR6jU6Il6TTj7AQ9q_WaEDJowp6iE04FHahip-jHZRpXH1wEPOUy2yXkhPOEI9gRCvYQY8VjCbeQsDvg3TshcL0Li_8W0h7vm15xCRXwkrHPMYJfmoZDurV1s7JpxDMstrbd0JBwXOeQbMSuQFOxt8WHlGdbn6Mnk40VXtyfZ-jrh_dfdp-6q88fL3cXV52Xki9dP4GVTHjltVBicsIxYF45NQgpXA99u1EKWD8q6Jmj0gEQSgc-TN4pS_gZenP0vSn5-wp1MXOo26A2QV6rYWyQTCtNaENf_4Ve57W07hvV_pATwTh_oPY2gglpykuxfjM1Fz2RQ0-E3p49_wfV1ghz8DnBFJr-RwE9FviSay0wmZsSZlsOhhKz5W-O-ZuWv9nyN4dW8-q-4dXNMP6u-BV4A9gRqO0q7aE8TPR_158j_7vO</recordid><startdate>201911</startdate><enddate>201911</enddate><creator>Yang, Cuixia</creator><creator>Cao, Manlin</creator><creator>Liu, Yiwen</creator><creator>He, Yiqing</creator><creator>Du, Yan</creator><creator>Zhang, Guoliang</creator><creator>Gao, Feng</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>201911</creationdate><title>Inducible formation of leader cells driven by CD44 switching gives rise to collective invasion and metastases in luminal breast carcinomas</title><author>Yang, Cuixia ; Cao, Manlin ; Liu, Yiwen ; He, Yiqing ; Du, Yan ; Zhang, Guoliang ; Gao, Feng</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c553t-6fea524c8c9484fb4b2e2c8b87454b6e6c8c88e26d8e62b15bee011737fcb8a03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>38</topic><topic>38/1</topic><topic>38/35</topic><topic>38/39</topic><topic>38/77</topic><topic>631/67/1347</topic><topic>631/67/322</topic><topic>64</topic><topic>64/60</topic><topic>96/10</topic><topic>96/31</topic><topic>Animals</topic><topic>Apoptosis</topic><topic>Breast cancer</topic><topic>Breast carcinoma</topic><topic>Breast Neoplasms - metabolism</topic><topic>Breast Neoplasms - pathology</topic><topic>Cancer</topic><topic>Carcinoma - metabolism</topic><topic>Carcinoma - pathology</topic><topic>CD44 antigen</topic><topic>Cell Biology</topic><topic>Cell migration</topic><topic>Cell Movement - physiology</topic><topic>Female</topic><topic>Human Genetics</topic><topic>Humans</topic><topic>Hyaluronan Receptors - metabolism</topic><topic>Internal Medicine</topic><topic>Invasiveness</topic><topic>Medicine</topic><topic>Medicine & Public Health</topic><topic>Mesenchyme</topic><topic>Metastases</topic><topic>Metastasis</topic><topic>Mice</topic><topic>Neoplasm Invasiveness - pathology</topic><topic>Oncology</topic><topic>Oncology, Experimental</topic><topic>Phenotypes</topic><topic>Stem cells</topic><topic>Tumors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yang, Cuixia</creatorcontrib><creatorcontrib>Cao, Manlin</creatorcontrib><creatorcontrib>Liu, Yiwen</creatorcontrib><creatorcontrib>He, Yiqing</creatorcontrib><creatorcontrib>Du, Yan</creatorcontrib><creatorcontrib>Zhang, Guoliang</creatorcontrib><creatorcontrib>Gao, Feng</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Health & Medical Collection (Proquest)</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database (Proquest)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech 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>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</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>Research Library Prep (ProQuest)</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biological Sciences</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>ProQuest research library</collection><collection>Biological Science Database</collection><collection>Research Library (Corporate)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Oncogene</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yang, Cuixia</au><au>Cao, Manlin</au><au>Liu, Yiwen</au><au>He, Yiqing</au><au>Du, Yan</au><au>Zhang, Guoliang</au><au>Gao, Feng</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Inducible formation of leader cells driven by CD44 switching gives rise to collective invasion and metastases in luminal breast carcinomas</atitle><jtitle>Oncogene</jtitle><stitle>Oncogene</stitle><addtitle>Oncogene</addtitle><date>2019-11</date><risdate>2019</risdate><volume>38</volume><issue>46</issue><spage>7113</spage><epage>7132</epage><pages>7113-7132</pages><issn>0950-9232</issn><eissn>1476-5594</eissn><abstract>Collective invasion into adjacent tissue is a hallmark of luminal breast cancer, and ~20% of these cases eventually undergo metastasis. How less aggressive luminal-like breast cancer transitions to invasive cancer remains unclear. Our study revealed that CD44
hi
cancer cells are the leading subpopulation in collectively invading luminal cancer cells and efficiently promote the collective invasion of CD44
lo
/follower cells. The CD44
hi
/leader subpopulation showed a specific gene signature of various hybrid epithelial/mesenchymal genes and key functional coregulators of collective invasion, which was distinct from that of CD44
lo
/follower cells. However, the CD44
hi
/leader cells, which showed a partial epithelial–mesenchymal transition (EMT) phenotype, readily switched to the CD44
lo
phenotype along with collective migration and vice versa; this phenomenon was spontaneous and sensitive to the tumor microenvironment. The CD44
lo
-to-CD44
hi
conversion was accompanied by a shift in CD44s to CD44v but not a conversion of non-cancer stem cells to cancer stem cells (CSCs). Therefore, the CD44
hi
leader cells, as currently identified, are not a stable subpopulation in breast tumors. This plasticity and ability to generate CD44
hi
carcinoma cells with enhanced migratory and invasive behavior might be responsible for the transition from in situ to invasive behavior of luminal-type breast cancer.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>31417182</pmid><doi>10.1038/s41388-019-0899-y</doi><tpages>20</tpages></addata></record> |
| fulltext | fulltext |
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| ispartof | Oncogene, 2019-11, Vol.38 (46), p.7113-7132 |
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| language | eng |
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| source | MEDLINE; SpringerLink (Online service) |
| subjects | 38 38/1 38/35 38/39 38/77 631/67/1347 631/67/322 64 64/60 96/10 96/31 Animals Apoptosis Breast cancer Breast carcinoma Breast Neoplasms - metabolism Breast Neoplasms - pathology Cancer Carcinoma - metabolism Carcinoma - pathology CD44 antigen Cell Biology Cell migration Cell Movement - physiology Female Human Genetics Humans Hyaluronan Receptors - metabolism Internal Medicine Invasiveness Medicine Medicine & Public Health Mesenchyme Metastases Metastasis Mice Neoplasm Invasiveness - pathology Oncology Oncology, Experimental Phenotypes Stem cells Tumors |
| title | Inducible formation of leader cells driven by CD44 switching gives rise to collective invasion and metastases in luminal breast carcinomas |
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