High-resolution chromatin immunoprecipitation (ChIP) sequencing reveals novel binding targets and prognostic role for SOX11 in mantle cell lymphoma
Sex determining region Y-box 11 (SOX11) expression is specific for mantle cell lymphoma (MCL) as compared with other non-Hodgkin’s lymphomas. However, the function and direct-binding targets of SOX11 in MCL are largely unknown. We used high-resolution chromatin immunoprecipitation sequencing to iden...
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| Veröffentlicht in: | Oncogene 2015-03, Vol.34 (10), p.1231-1240 |
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| creator | Kuo, P-Y Leshchenko, V V Fazzari, M J Perumal, D Gellen, T He, T Iqbal, J Baumgartner-Wennerholm, S Nygren, L Zhang, F Zhang, W Suh, K S Goy, A Yang, D T Chan, W-C Kahl, B S Verma, A K Gascoyne, R D Kimby, E Sander, B Ye, B H Melnick, A M Parekh, S |
| description | Sex determining region Y-box 11 (SOX11) expression is specific for mantle cell lymphoma (MCL) as compared with other non-Hodgkin’s lymphomas. However, the function and direct-binding targets of SOX11 in MCL are largely unknown. We used high-resolution chromatin immunoprecipitation sequencing to identify the direct target genes of SOX11 in a genome-wide, unbiased manner and elucidate its functional significance. Pathway analysis identified WNT, PKA and TGF-beta signaling pathways as significantly enriched by SOX11-target genes. Quantitative chromatin immunoprecipitation sequencing and promoter reporter assays confirmed that SOX11 directly binds to individual genes and modulates their transcription activities in these pathways in MCL. Functional studies using RNA interference demonstrate that SOX11 directly regulates WNT in MCL. We analyzed SOX11 expression in three independent well-annotated tissue microarrays from the University of Wisconsin (UW), Karolinska Institute and British Columbia Cancer Agency. Our findings suggest that high SOX11 expression is associated with improved survival in a subset of MCL patients, particularly those treated with intensive chemotherapy. Transcriptional regulation of WNT and other biological pathways affected by SOX11-target genes may help explain the impact of SOX11 expression on patient outcomes. |
| doi_str_mv | 10.1038/onc.2014.44 |
| format | Article |
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However, the function and direct-binding targets of SOX11 in MCL are largely unknown. We used high-resolution chromatin immunoprecipitation sequencing to identify the direct target genes of SOX11 in a genome-wide, unbiased manner and elucidate its functional significance. Pathway analysis identified WNT, PKA and TGF-beta signaling pathways as significantly enriched by SOX11-target genes. Quantitative chromatin immunoprecipitation sequencing and promoter reporter assays confirmed that SOX11 directly binds to individual genes and modulates their transcription activities in these pathways in MCL. Functional studies using RNA interference demonstrate that SOX11 directly regulates WNT in MCL. We analyzed SOX11 expression in three independent well-annotated tissue microarrays from the University of Wisconsin (UW), Karolinska Institute and British Columbia Cancer Agency. Our findings suggest that high SOX11 expression is associated with improved survival in a subset of MCL patients, particularly those treated with intensive chemotherapy. Transcriptional regulation of WNT and other biological pathways affected by SOX11-target genes may help explain the impact of SOX11 expression on patient outcomes.</description><identifier>ISSN: 0950-9232</identifier><identifier>EISSN: 1476-5594</identifier><identifier>DOI: 10.1038/onc.2014.44</identifier><identifier>PMID: 24681958</identifier><identifier>CODEN: ONCNES</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/1647/2217/2088 ; 631/67/1990/291/1621 ; 631/80/86 ; 692/53/2422 ; Antineoplastic Combined Chemotherapy Protocols ; Apoptosis ; beta Catenin - metabolism ; Binding Sites ; Cancer ; Cell Biology ; Cell Cycle Checkpoints ; Cell Line, Tumor ; Cell Proliferation ; Cell Survival - drug effects ; Chemotherapy ; Chromatin ; Chromatin Immunoprecipitation ; Development and progression ; Drug targeting ; Gene Expression ; Gene Expression Regulation, Neoplastic ; Gene regulation ; Genetic aspects ; Genetic research ; Genomes ; High-Throughput Nucleotide Sequencing ; Human Genetics ; Humans ; Immunoprecipitation ; Innovations ; Internal Medicine ; Lymphoma ; Lymphoma, Mantle-Cell - drug therapy ; Lymphoma, Mantle-Cell - genetics ; Lymphoma, Mantle-Cell - metabolism ; Lymphoma, Mantle-Cell - mortality ; Mantle cell lymphoma ; Medicine ; Medicine & Public Health ; Non-Hodgkin's lymphoma ; Nucleotide Motifs ; Oncology ; Oncology, Experimental ; original-article ; Prognosis ; Protein Binding ; Protein kinase A ; Ribonucleic acid ; RNA ; RNA-mediated interference ; Signal Transduction ; SOXC Transcription Factors - genetics ; SOXC Transcription Factors - metabolism ; Studies ; Transcription ; Transcription, Genetic ; Wnt protein ; Wnt Proteins - metabolism ; Wnt Signaling Pathway</subject><ispartof>Oncogene, 2015-03, Vol.34 (10), p.1231-1240</ispartof><rights>Macmillan Publishers Limited 2015</rights><rights>COPYRIGHT 2015 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Mar 5, 2015</rights><rights>Macmillan Publishers Limited 2015.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c627t-1dfe051215f22f84b0f9dca6ba89b5620d06c23f118d3e84084e1d2a6c722f243</citedby><cites>FETCH-LOGICAL-c627t-1dfe051215f22f84b0f9dca6ba89b5620d06c23f118d3e84084e1d2a6c722f243</cites><orcidid>0000-0003-1141-9790 ; 0000000311419790</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/onc.2014.44$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/onc.2014.44$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,550,776,780,881,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24681958$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttp://kipublications.ki.se/Default.aspx?queryparsed=id:130875280$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Kuo, P-Y</creatorcontrib><creatorcontrib>Leshchenko, V V</creatorcontrib><creatorcontrib>Fazzari, M J</creatorcontrib><creatorcontrib>Perumal, D</creatorcontrib><creatorcontrib>Gellen, T</creatorcontrib><creatorcontrib>He, T</creatorcontrib><creatorcontrib>Iqbal, J</creatorcontrib><creatorcontrib>Baumgartner-Wennerholm, S</creatorcontrib><creatorcontrib>Nygren, L</creatorcontrib><creatorcontrib>Zhang, F</creatorcontrib><creatorcontrib>Zhang, W</creatorcontrib><creatorcontrib>Suh, K S</creatorcontrib><creatorcontrib>Goy, A</creatorcontrib><creatorcontrib>Yang, D T</creatorcontrib><creatorcontrib>Chan, W-C</creatorcontrib><creatorcontrib>Kahl, B S</creatorcontrib><creatorcontrib>Verma, A K</creatorcontrib><creatorcontrib>Gascoyne, R D</creatorcontrib><creatorcontrib>Kimby, E</creatorcontrib><creatorcontrib>Sander, B</creatorcontrib><creatorcontrib>Ye, B H</creatorcontrib><creatorcontrib>Melnick, A M</creatorcontrib><creatorcontrib>Parekh, S</creatorcontrib><title>High-resolution chromatin immunoprecipitation (ChIP) sequencing reveals novel binding targets and prognostic role for SOX11 in mantle cell lymphoma</title><title>Oncogene</title><addtitle>Oncogene</addtitle><addtitle>Oncogene</addtitle><description>Sex determining region Y-box 11 (SOX11) expression is specific for mantle cell lymphoma (MCL) as compared with other non-Hodgkin’s lymphomas. However, the function and direct-binding targets of SOX11 in MCL are largely unknown. We used high-resolution chromatin immunoprecipitation sequencing to identify the direct target genes of SOX11 in a genome-wide, unbiased manner and elucidate its functional significance. Pathway analysis identified WNT, PKA and TGF-beta signaling pathways as significantly enriched by SOX11-target genes. Quantitative chromatin immunoprecipitation sequencing and promoter reporter assays confirmed that SOX11 directly binds to individual genes and modulates their transcription activities in these pathways in MCL. Functional studies using RNA interference demonstrate that SOX11 directly regulates WNT in MCL. We analyzed SOX11 expression in three independent well-annotated tissue microarrays from the University of Wisconsin (UW), Karolinska Institute and British Columbia Cancer Agency. Our findings suggest that high SOX11 expression is associated with improved survival in a subset of MCL patients, particularly those treated with intensive chemotherapy. Transcriptional regulation of WNT and other biological pathways affected by SOX11-target genes may help explain the impact of SOX11 expression on patient outcomes.</description><subject>631/1647/2217/2088</subject><subject>631/67/1990/291/1621</subject><subject>631/80/86</subject><subject>692/53/2422</subject><subject>Antineoplastic Combined Chemotherapy Protocols</subject><subject>Apoptosis</subject><subject>beta Catenin - metabolism</subject><subject>Binding Sites</subject><subject>Cancer</subject><subject>Cell Biology</subject><subject>Cell Cycle Checkpoints</subject><subject>Cell Line, Tumor</subject><subject>Cell Proliferation</subject><subject>Cell Survival - drug effects</subject><subject>Chemotherapy</subject><subject>Chromatin</subject><subject>Chromatin Immunoprecipitation</subject><subject>Development and progression</subject><subject>Drug targeting</subject><subject>Gene Expression</subject><subject>Gene Expression Regulation, Neoplastic</subject><subject>Gene regulation</subject><subject>Genetic aspects</subject><subject>Genetic research</subject><subject>Genomes</subject><subject>High-Throughput Nucleotide Sequencing</subject><subject>Human Genetics</subject><subject>Humans</subject><subject>Immunoprecipitation</subject><subject>Innovations</subject><subject>Internal Medicine</subject><subject>Lymphoma</subject><subject>Lymphoma, Mantle-Cell - drug therapy</subject><subject>Lymphoma, Mantle-Cell - genetics</subject><subject>Lymphoma, Mantle-Cell - metabolism</subject><subject>Lymphoma, Mantle-Cell - mortality</subject><subject>Mantle cell lymphoma</subject><subject>Medicine</subject><subject>Medicine & Public Health</subject><subject>Non-Hodgkin's lymphoma</subject><subject>Nucleotide Motifs</subject><subject>Oncology</subject><subject>Oncology, Experimental</subject><subject>original-article</subject><subject>Prognosis</subject><subject>Protein Binding</subject><subject>Protein kinase A</subject><subject>Ribonucleic 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text</collection><jtitle>Oncogene</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kuo, P-Y</au><au>Leshchenko, V V</au><au>Fazzari, M J</au><au>Perumal, D</au><au>Gellen, T</au><au>He, T</au><au>Iqbal, J</au><au>Baumgartner-Wennerholm, S</au><au>Nygren, L</au><au>Zhang, F</au><au>Zhang, W</au><au>Suh, K S</au><au>Goy, A</au><au>Yang, D T</au><au>Chan, W-C</au><au>Kahl, B S</au><au>Verma, A K</au><au>Gascoyne, R D</au><au>Kimby, E</au><au>Sander, B</au><au>Ye, B H</au><au>Melnick, A M</au><au>Parekh, S</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>High-resolution chromatin immunoprecipitation (ChIP) sequencing reveals novel binding targets and prognostic role for SOX11 in mantle cell lymphoma</atitle><jtitle>Oncogene</jtitle><stitle>Oncogene</stitle><addtitle>Oncogene</addtitle><date>2015-03-05</date><risdate>2015</risdate><volume>34</volume><issue>10</issue><spage>1231</spage><epage>1240</epage><pages>1231-1240</pages><issn>0950-9232</issn><eissn>1476-5594</eissn><coden>ONCNES</coden><abstract>Sex determining region Y-box 11 (SOX11) expression is specific for mantle cell lymphoma (MCL) as compared with other non-Hodgkin’s lymphomas. However, the function and direct-binding targets of SOX11 in MCL are largely unknown. We used high-resolution chromatin immunoprecipitation sequencing to identify the direct target genes of SOX11 in a genome-wide, unbiased manner and elucidate its functional significance. Pathway analysis identified WNT, PKA and TGF-beta signaling pathways as significantly enriched by SOX11-target genes. Quantitative chromatin immunoprecipitation sequencing and promoter reporter assays confirmed that SOX11 directly binds to individual genes and modulates their transcription activities in these pathways in MCL. Functional studies using RNA interference demonstrate that SOX11 directly regulates WNT in MCL. We analyzed SOX11 expression in three independent well-annotated tissue microarrays from the University of Wisconsin (UW), Karolinska Institute and British Columbia Cancer Agency. Our findings suggest that high SOX11 expression is associated with improved survival in a subset of MCL patients, particularly those treated with intensive chemotherapy. Transcriptional regulation of WNT and other biological pathways affected by SOX11-target genes may help explain the impact of SOX11 expression on patient outcomes.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>24681958</pmid><doi>10.1038/onc.2014.44</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0003-1141-9790</orcidid><orcidid>https://orcid.org/0000000311419790</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0950-9232 |
| ispartof | Oncogene, 2015-03, Vol.34 (10), p.1231-1240 |
| issn | 0950-9232 1476-5594 |
| language | eng |
| recordid | cdi_swepub_primary_oai_swepub_ki_se_522616 |
| source | MEDLINE; Springer Nature - Complete Springer Journals; Nature; EZB-FREE-00999 freely available EZB journals; SWEPUB Freely available online |
| subjects | 631/1647/2217/2088 631/67/1990/291/1621 631/80/86 692/53/2422 Antineoplastic Combined Chemotherapy Protocols Apoptosis beta Catenin - metabolism Binding Sites Cancer Cell Biology Cell Cycle Checkpoints Cell Line, Tumor Cell Proliferation Cell Survival - drug effects Chemotherapy Chromatin Chromatin Immunoprecipitation Development and progression Drug targeting Gene Expression Gene Expression Regulation, Neoplastic Gene regulation Genetic aspects Genetic research Genomes High-Throughput Nucleotide Sequencing Human Genetics Humans Immunoprecipitation Innovations Internal Medicine Lymphoma Lymphoma, Mantle-Cell - drug therapy Lymphoma, Mantle-Cell - genetics Lymphoma, Mantle-Cell - metabolism Lymphoma, Mantle-Cell - mortality Mantle cell lymphoma Medicine Medicine & Public Health Non-Hodgkin's lymphoma Nucleotide Motifs Oncology Oncology, Experimental original-article Prognosis Protein Binding Protein kinase A Ribonucleic acid RNA RNA-mediated interference Signal Transduction SOXC Transcription Factors - genetics SOXC Transcription Factors - metabolism Studies Transcription Transcription, Genetic Wnt protein Wnt Proteins - metabolism Wnt Signaling Pathway |
| title | High-resolution chromatin immunoprecipitation (ChIP) sequencing reveals novel binding targets and prognostic role for SOX11 in mantle cell lymphoma |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-10T12%3A56%3A48IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_swepu&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=High-resolution%20chromatin%20immunoprecipitation%20(ChIP)%20sequencing%20reveals%20novel%20binding%20targets%20and%20prognostic%20role%20for%20SOX11%20in%20mantle%20cell%20lymphoma&rft.jtitle=Oncogene&rft.au=Kuo,%20P-Y&rft.date=2015-03-05&rft.volume=34&rft.issue=10&rft.spage=1231&rft.epage=1240&rft.pages=1231-1240&rft.issn=0950-9232&rft.eissn=1476-5594&rft.coden=ONCNES&rft_id=info:doi/10.1038/onc.2014.44&rft_dat=%3Cgale_swepu%3EA405169883%3C/gale_swepu%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1660676658&rft_id=info:pmid/24681958&rft_galeid=A405169883&rfr_iscdi=true |