SOX18 meditates the resistance of Bmi1‐expressing cells to cetuximab in HNSCC
Objective Head and neck squamous cell carcinoma (HNSCC) is the most common type of malignancy in the head and neck region worldwide. The therapeutic strategies for HNSCC remain unsatisfying and limited. Here, we found a population of resistant Bmi1‐expressing cells in the presence of cetuximab treat...
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| creator | Zhang, Caihua Chen, Zhi Gao, Nailin Xiong, Gan Chen, Peng Li, Hui Chen, Demeng He, Qianting Peng, Liang |
| description | Objective
Head and neck squamous cell carcinoma (HNSCC) is the most common type of malignancy in the head and neck region worldwide. The therapeutic strategies for HNSCC remain unsatisfying and limited. Here, we found a population of resistant Bmi1‐expressing cells in the presence of cetuximab treatment and reported a novel role of SRY‐box transcription factor 18 (SOX18), a member of the SOX family, in promoting HNSCC resistance to cetuximab. This study aimed to investigate the regulatory mechanism of Sox18 in Bmi1‐positive cells and to search for better therapeutic targets.
Methods
We successfully obtained Bmi1CreER, RosatdTomato, and RosaDTA mice and identified Bmi1‐expressing cells through lineage tracing. SOX18 expression in HNSCC and normal tissues was analyzed by immunohistochemistry, colocalization of Sox18, and Bmi1‐expressing cells was analyzed by immunofluorescence, and SOX18 expression in SCC9 cell lines was quantified by western blotting and quantitative real‐time PCR. The investigation of the mechanism of SOX18‐mediated cetuximab resistance in Bmi1‐positive cells was based on the analysis of single‐cell RNA‐seq data obtained from the Gene Expression Omnibus (GEO) database. Western blotting was performed to verify the results obtained from the single‐cell RNA‐seq analysis.
Results
In our study, we demonstrated that Bmi1‐expressing cells were resistant to cetuximab treatment and that depletion of Bmi1‐expressing cells improved cetuximab efficacy in HNSCC. We then discovered that Sox18 mediated the stem cell‐like properties of Bmi1‐expressing cells and promoted cellular cetuximab resistance through an oxidative phosphorylation pathway. There was a significant downregulation of key genes in the oxidative phosphorylation pathway in Sox18 knockout cell lines.
Conclusions
Taken together, the findings of our study suggest that Sox18 mediates the resistance of Bmi1‐expressing cells to cetuximab in HNSCC via the oxidative phosphorylation pathway. |
| doi_str_mv | 10.1111/odi.14596 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2813888894</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>3054015107</sourcerecordid><originalsourceid>FETCH-LOGICAL-c3536-8a23f3eda9a68297d4612426ee0ba637e9449107d2b9bad8747550213aa1928a3</originalsourceid><addsrcrecordid>eNp1kEtOwzAQhi0EoqWw4AIoEhtYpPUzsZcQHq1UkUVB6s5yEgdcpUmJE9HuOAJn5CS4pLBAYjYzsj79M_4AOEVwiFyNqswMEWUi2AN9FEDkQ47ZvpsJoz7DZN4DR9YuIEShIPgQ9EiIOIUE90E8i-eIe0udmUY12nrNi_ZqbY1tVJlqr8q966VBn-8fer1y79aUz16qi8KRlRuadm2WKvFM6Y0fZlF0DA5yVVh9susD8HR3-xiN_Wl8P4mupn5KGAl8rjDJic6UUAHHIsxogDDFgdYwUQEJtaBUIBhmOBGJynhIQ8YgRkQpJDBXZAAuutxVXb222jZyaez2LlXqqrUSc0S4K0Edev4HXVRtXbrrJIGMQsTcIkdddlRaV9bWOper2v2s3kgE5daydJblt2XHnu0S28SZ-yV_tDpg1AFvptCb_5NkfDPpIr8AxbKEGw</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>3054015107</pqid></control><display><type>article</type><title>SOX18 meditates the resistance of Bmi1‐expressing cells to cetuximab in HNSCC</title><source>MEDLINE</source><source>Wiley Online Library All Journals</source><creator>Zhang, Caihua ; Chen, Zhi ; Gao, Nailin ; Xiong, Gan ; Chen, Peng ; Li, Hui ; Chen, Demeng ; He, Qianting ; Peng, Liang</creator><creatorcontrib>Zhang, Caihua ; Chen, Zhi ; Gao, Nailin ; Xiong, Gan ; Chen, Peng ; Li, Hui ; Chen, Demeng ; He, Qianting ; Peng, Liang</creatorcontrib><description>Objective
Head and neck squamous cell carcinoma (HNSCC) is the most common type of malignancy in the head and neck region worldwide. The therapeutic strategies for HNSCC remain unsatisfying and limited. Here, we found a population of resistant Bmi1‐expressing cells in the presence of cetuximab treatment and reported a novel role of SRY‐box transcription factor 18 (SOX18), a member of the SOX family, in promoting HNSCC resistance to cetuximab. This study aimed to investigate the regulatory mechanism of Sox18 in Bmi1‐positive cells and to search for better therapeutic targets.
Methods
We successfully obtained Bmi1CreER, RosatdTomato, and RosaDTA mice and identified Bmi1‐expressing cells through lineage tracing. SOX18 expression in HNSCC and normal tissues was analyzed by immunohistochemistry, colocalization of Sox18, and Bmi1‐expressing cells was analyzed by immunofluorescence, and SOX18 expression in SCC9 cell lines was quantified by western blotting and quantitative real‐time PCR. The investigation of the mechanism of SOX18‐mediated cetuximab resistance in Bmi1‐positive cells was based on the analysis of single‐cell RNA‐seq data obtained from the Gene Expression Omnibus (GEO) database. Western blotting was performed to verify the results obtained from the single‐cell RNA‐seq analysis.
Results
In our study, we demonstrated that Bmi1‐expressing cells were resistant to cetuximab treatment and that depletion of Bmi1‐expressing cells improved cetuximab efficacy in HNSCC. We then discovered that Sox18 mediated the stem cell‐like properties of Bmi1‐expressing cells and promoted cellular cetuximab resistance through an oxidative phosphorylation pathway. There was a significant downregulation of key genes in the oxidative phosphorylation pathway in Sox18 knockout cell lines.
Conclusions
Taken together, the findings of our study suggest that Sox18 mediates the resistance of Bmi1‐expressing cells to cetuximab in HNSCC via the oxidative phosphorylation pathway.</description><identifier>ISSN: 1354-523X</identifier><identifier>ISSN: 1601-0825</identifier><identifier>EISSN: 1601-0825</identifier><identifier>DOI: 10.1111/odi.14596</identifier><identifier>PMID: 37184032</identifier><language>eng</language><publisher>Denmark: Wiley Subscription Services, Inc</publisher><subject>Animals ; Antineoplastic Agents, Immunological - pharmacology ; Antineoplastic Agents, Immunological - therapeutic use ; cancer stem cells ; Cell Line, Tumor ; cetuximab ; Cetuximab - pharmacology ; Cetuximab - therapeutic use ; Drug Resistance, Neoplasm - genetics ; Gene expression ; Head & neck cancer ; Head and neck carcinoma ; Head and Neck Neoplasms - drug therapy ; Head and Neck Neoplasms - genetics ; Head and Neck Neoplasms - metabolism ; HNSCC ; Humans ; Immunofluorescence ; Immunohistochemistry ; Malignancy ; Mice ; Oxidative phosphorylation ; Phosphorylation ; Polycomb Repressive Complex 1 - genetics ; Polycomb Repressive Complex 1 - metabolism ; Sox18 ; SOXF Transcription Factors - genetics ; SOXF Transcription Factors - metabolism ; Squamous cell carcinoma ; Squamous Cell Carcinoma of Head and Neck - drug therapy ; Squamous Cell Carcinoma of Head and Neck - genetics ; Squamous Cell Carcinoma of Head and Neck - metabolism ; Therapeutic targets ; Western blotting</subject><ispartof>Oral diseases, 2024-04, Vol.30 (3), p.1100-1113</ispartof><rights>2023 Wiley Periodicals LLC.</rights><rights>2024 Wiley Periodicals LLC.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3536-8a23f3eda9a68297d4612426ee0ba637e9449107d2b9bad8747550213aa1928a3</citedby><cites>FETCH-LOGICAL-c3536-8a23f3eda9a68297d4612426ee0ba637e9449107d2b9bad8747550213aa1928a3</cites><orcidid>0000-0002-7457-2816 ; 0000-0001-7230-2495 ; 0000-0002-4741-0053 ; 0000-0003-0657-9650</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fodi.14596$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fodi.14596$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37184032$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Caihua</creatorcontrib><creatorcontrib>Chen, Zhi</creatorcontrib><creatorcontrib>Gao, Nailin</creatorcontrib><creatorcontrib>Xiong, Gan</creatorcontrib><creatorcontrib>Chen, Peng</creatorcontrib><creatorcontrib>Li, Hui</creatorcontrib><creatorcontrib>Chen, Demeng</creatorcontrib><creatorcontrib>He, Qianting</creatorcontrib><creatorcontrib>Peng, Liang</creatorcontrib><title>SOX18 meditates the resistance of Bmi1‐expressing cells to cetuximab in HNSCC</title><title>Oral diseases</title><addtitle>Oral Dis</addtitle><description>Objective
Head and neck squamous cell carcinoma (HNSCC) is the most common type of malignancy in the head and neck region worldwide. The therapeutic strategies for HNSCC remain unsatisfying and limited. Here, we found a population of resistant Bmi1‐expressing cells in the presence of cetuximab treatment and reported a novel role of SRY‐box transcription factor 18 (SOX18), a member of the SOX family, in promoting HNSCC resistance to cetuximab. This study aimed to investigate the regulatory mechanism of Sox18 in Bmi1‐positive cells and to search for better therapeutic targets.
Methods
We successfully obtained Bmi1CreER, RosatdTomato, and RosaDTA mice and identified Bmi1‐expressing cells through lineage tracing. SOX18 expression in HNSCC and normal tissues was analyzed by immunohistochemistry, colocalization of Sox18, and Bmi1‐expressing cells was analyzed by immunofluorescence, and SOX18 expression in SCC9 cell lines was quantified by western blotting and quantitative real‐time PCR. The investigation of the mechanism of SOX18‐mediated cetuximab resistance in Bmi1‐positive cells was based on the analysis of single‐cell RNA‐seq data obtained from the Gene Expression Omnibus (GEO) database. Western blotting was performed to verify the results obtained from the single‐cell RNA‐seq analysis.
Results
In our study, we demonstrated that Bmi1‐expressing cells were resistant to cetuximab treatment and that depletion of Bmi1‐expressing cells improved cetuximab efficacy in HNSCC. We then discovered that Sox18 mediated the stem cell‐like properties of Bmi1‐expressing cells and promoted cellular cetuximab resistance through an oxidative phosphorylation pathway. There was a significant downregulation of key genes in the oxidative phosphorylation pathway in Sox18 knockout cell lines.
Conclusions
Taken together, the findings of our study suggest that Sox18 mediates the resistance of Bmi1‐expressing cells to cetuximab in HNSCC via the oxidative phosphorylation pathway.</description><subject>Animals</subject><subject>Antineoplastic Agents, Immunological - pharmacology</subject><subject>Antineoplastic Agents, Immunological - therapeutic use</subject><subject>cancer stem cells</subject><subject>Cell Line, Tumor</subject><subject>cetuximab</subject><subject>Cetuximab - pharmacology</subject><subject>Cetuximab - therapeutic use</subject><subject>Drug Resistance, Neoplasm - genetics</subject><subject>Gene expression</subject><subject>Head & neck cancer</subject><subject>Head and neck carcinoma</subject><subject>Head and Neck Neoplasms - drug therapy</subject><subject>Head and Neck Neoplasms - genetics</subject><subject>Head and Neck Neoplasms - metabolism</subject><subject>HNSCC</subject><subject>Humans</subject><subject>Immunofluorescence</subject><subject>Immunohistochemistry</subject><subject>Malignancy</subject><subject>Mice</subject><subject>Oxidative phosphorylation</subject><subject>Phosphorylation</subject><subject>Polycomb Repressive Complex 1 - genetics</subject><subject>Polycomb Repressive Complex 1 - metabolism</subject><subject>Sox18</subject><subject>SOXF Transcription Factors - genetics</subject><subject>SOXF Transcription Factors - metabolism</subject><subject>Squamous cell carcinoma</subject><subject>Squamous Cell Carcinoma of Head and Neck - drug therapy</subject><subject>Squamous Cell Carcinoma of Head and Neck - genetics</subject><subject>Squamous Cell Carcinoma of Head and Neck - metabolism</subject><subject>Therapeutic targets</subject><subject>Western blotting</subject><issn>1354-523X</issn><issn>1601-0825</issn><issn>1601-0825</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kEtOwzAQhi0EoqWw4AIoEhtYpPUzsZcQHq1UkUVB6s5yEgdcpUmJE9HuOAJn5CS4pLBAYjYzsj79M_4AOEVwiFyNqswMEWUi2AN9FEDkQ47ZvpsJoz7DZN4DR9YuIEShIPgQ9EiIOIUE90E8i-eIe0udmUY12nrNi_ZqbY1tVJlqr8q966VBn-8fer1y79aUz16qi8KRlRuadm2WKvFM6Y0fZlF0DA5yVVh9susD8HR3-xiN_Wl8P4mupn5KGAl8rjDJic6UUAHHIsxogDDFgdYwUQEJtaBUIBhmOBGJynhIQ8YgRkQpJDBXZAAuutxVXb222jZyaez2LlXqqrUSc0S4K0Edev4HXVRtXbrrJIGMQsTcIkdddlRaV9bWOper2v2s3kgE5daydJblt2XHnu0S28SZ-yV_tDpg1AFvptCb_5NkfDPpIr8AxbKEGw</recordid><startdate>202404</startdate><enddate>202404</enddate><creator>Zhang, Caihua</creator><creator>Chen, Zhi</creator><creator>Gao, Nailin</creator><creator>Xiong, Gan</creator><creator>Chen, Peng</creator><creator>Li, Hui</creator><creator>Chen, Demeng</creator><creator>He, Qianting</creator><creator>Peng, Liang</creator><general>Wiley Subscription Services, Inc</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>7QP</scope><scope>K9.</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-7457-2816</orcidid><orcidid>https://orcid.org/0000-0001-7230-2495</orcidid><orcidid>https://orcid.org/0000-0002-4741-0053</orcidid><orcidid>https://orcid.org/0000-0003-0657-9650</orcidid></search><sort><creationdate>202404</creationdate><title>SOX18 meditates the resistance of Bmi1‐expressing cells to cetuximab in HNSCC</title><author>Zhang, Caihua ; Chen, Zhi ; Gao, Nailin ; Xiong, Gan ; Chen, Peng ; Li, Hui ; Chen, Demeng ; He, Qianting ; Peng, Liang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3536-8a23f3eda9a68297d4612426ee0ba637e9449107d2b9bad8747550213aa1928a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Animals</topic><topic>Antineoplastic Agents, Immunological - pharmacology</topic><topic>Antineoplastic Agents, Immunological - therapeutic use</topic><topic>cancer stem cells</topic><topic>Cell Line, Tumor</topic><topic>cetuximab</topic><topic>Cetuximab - pharmacology</topic><topic>Cetuximab - therapeutic use</topic><topic>Drug Resistance, Neoplasm - genetics</topic><topic>Gene expression</topic><topic>Head & neck cancer</topic><topic>Head and neck carcinoma</topic><topic>Head and Neck Neoplasms - drug therapy</topic><topic>Head and Neck Neoplasms - genetics</topic><topic>Head and Neck Neoplasms - metabolism</topic><topic>HNSCC</topic><topic>Humans</topic><topic>Immunofluorescence</topic><topic>Immunohistochemistry</topic><topic>Malignancy</topic><topic>Mice</topic><topic>Oxidative phosphorylation</topic><topic>Phosphorylation</topic><topic>Polycomb Repressive Complex 1 - genetics</topic><topic>Polycomb Repressive Complex 1 - metabolism</topic><topic>Sox18</topic><topic>SOXF Transcription Factors - genetics</topic><topic>SOXF Transcription Factors - metabolism</topic><topic>Squamous cell carcinoma</topic><topic>Squamous Cell Carcinoma of Head and Neck - drug therapy</topic><topic>Squamous Cell Carcinoma of Head and Neck - genetics</topic><topic>Squamous Cell Carcinoma of Head and Neck - metabolism</topic><topic>Therapeutic targets</topic><topic>Western blotting</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhang, Caihua</creatorcontrib><creatorcontrib>Chen, Zhi</creatorcontrib><creatorcontrib>Gao, Nailin</creatorcontrib><creatorcontrib>Xiong, Gan</creatorcontrib><creatorcontrib>Chen, Peng</creatorcontrib><creatorcontrib>Li, Hui</creatorcontrib><creatorcontrib>Chen, Demeng</creatorcontrib><creatorcontrib>He, Qianting</creatorcontrib><creatorcontrib>Peng, Liang</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><jtitle>Oral diseases</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhang, Caihua</au><au>Chen, Zhi</au><au>Gao, Nailin</au><au>Xiong, Gan</au><au>Chen, Peng</au><au>Li, Hui</au><au>Chen, Demeng</au><au>He, Qianting</au><au>Peng, Liang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>SOX18 meditates the resistance of Bmi1‐expressing cells to cetuximab in HNSCC</atitle><jtitle>Oral diseases</jtitle><addtitle>Oral Dis</addtitle><date>2024-04</date><risdate>2024</risdate><volume>30</volume><issue>3</issue><spage>1100</spage><epage>1113</epage><pages>1100-1113</pages><issn>1354-523X</issn><issn>1601-0825</issn><eissn>1601-0825</eissn><abstract>Objective
Head and neck squamous cell carcinoma (HNSCC) is the most common type of malignancy in the head and neck region worldwide. The therapeutic strategies for HNSCC remain unsatisfying and limited. Here, we found a population of resistant Bmi1‐expressing cells in the presence of cetuximab treatment and reported a novel role of SRY‐box transcription factor 18 (SOX18), a member of the SOX family, in promoting HNSCC resistance to cetuximab. This study aimed to investigate the regulatory mechanism of Sox18 in Bmi1‐positive cells and to search for better therapeutic targets.
Methods
We successfully obtained Bmi1CreER, RosatdTomato, and RosaDTA mice and identified Bmi1‐expressing cells through lineage tracing. SOX18 expression in HNSCC and normal tissues was analyzed by immunohistochemistry, colocalization of Sox18, and Bmi1‐expressing cells was analyzed by immunofluorescence, and SOX18 expression in SCC9 cell lines was quantified by western blotting and quantitative real‐time PCR. The investigation of the mechanism of SOX18‐mediated cetuximab resistance in Bmi1‐positive cells was based on the analysis of single‐cell RNA‐seq data obtained from the Gene Expression Omnibus (GEO) database. Western blotting was performed to verify the results obtained from the single‐cell RNA‐seq analysis.
Results
In our study, we demonstrated that Bmi1‐expressing cells were resistant to cetuximab treatment and that depletion of Bmi1‐expressing cells improved cetuximab efficacy in HNSCC. We then discovered that Sox18 mediated the stem cell‐like properties of Bmi1‐expressing cells and promoted cellular cetuximab resistance through an oxidative phosphorylation pathway. There was a significant downregulation of key genes in the oxidative phosphorylation pathway in Sox18 knockout cell lines.
Conclusions
Taken together, the findings of our study suggest that Sox18 mediates the resistance of Bmi1‐expressing cells to cetuximab in HNSCC via the oxidative phosphorylation pathway.</abstract><cop>Denmark</cop><pub>Wiley Subscription Services, Inc</pub><pmid>37184032</pmid><doi>10.1111/odi.14596</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-7457-2816</orcidid><orcidid>https://orcid.org/0000-0001-7230-2495</orcidid><orcidid>https://orcid.org/0000-0002-4741-0053</orcidid><orcidid>https://orcid.org/0000-0003-0657-9650</orcidid></addata></record> |
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| subjects | Animals Antineoplastic Agents, Immunological - pharmacology Antineoplastic Agents, Immunological - therapeutic use cancer stem cells Cell Line, Tumor cetuximab Cetuximab - pharmacology Cetuximab - therapeutic use Drug Resistance, Neoplasm - genetics Gene expression Head & neck cancer Head and neck carcinoma Head and Neck Neoplasms - drug therapy Head and Neck Neoplasms - genetics Head and Neck Neoplasms - metabolism HNSCC Humans Immunofluorescence Immunohistochemistry Malignancy Mice Oxidative phosphorylation Phosphorylation Polycomb Repressive Complex 1 - genetics Polycomb Repressive Complex 1 - metabolism Sox18 SOXF Transcription Factors - genetics SOXF Transcription Factors - metabolism Squamous cell carcinoma Squamous Cell Carcinoma of Head and Neck - drug therapy Squamous Cell Carcinoma of Head and Neck - genetics Squamous Cell Carcinoma of Head and Neck - metabolism Therapeutic targets Western blotting |
| title | SOX18 meditates the resistance of Bmi1‐expressing cells to cetuximab in HNSCC |
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