ASPP2 suppresses squamous cell carcinoma via RelA/p65–mediated repression of p63
Squamous cell carcinoma (SCC) is highly malignant and refractory to therapy. The majority of existing mouse SCC models involve multiple gene mutations. Very few mouse models of spontaneous SCC have been generated by a single gene deletion. Here we report a haploinsufficient SCC mouse model in which...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2013-10, Vol.110 (44), p.17969-17974 |
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| creator | Tordella, Luca Koch, Sofia Salter, Victoria Pagotto, Anna Doondeea, Jessica B Feller, Stephan M Ratnayaka, Indrika Zhong, Shan Goldin, Robert D Lozano, Guillermina McKeon, Frank D Tavassoli, Mahvash Fritzsche, Florian Huber, Gerhard F Rössle, Matthias Moch, Holger Lu, Xin |
| description | Squamous cell carcinoma (SCC) is highly malignant and refractory to therapy. The majority of existing mouse SCC models involve multiple gene mutations. Very few mouse models of spontaneous SCC have been generated by a single gene deletion. Here we report a haploinsufficient SCC mouse model in which exon 3 of the Tp53BP2 gene (a p53 binding protein) was deleted in one allele in a BALB/c genetic background. Tp53BP2 encodes ASPP2 (ankyrin repeats, SH3 domain and protein rich region containing protein 2). Keratinocyte differentiation induces ASPP2 and its expression is inversely correlated with p63 protein in vitro and in vivo. Up-regulation of p63 expression is required for ASPP2 Δᵉˣᵒⁿ³/⁺ BALB/c mice to develop SCC, as heterozygosity of p63 but not p53 prevents them from developing it. Mechanistically, ASPP2 inhibits ΔNp63 expression through its ability to bind IκB and enhance nuclear Rel/A p65, a component of the NF-κB transcription complex, which mediates the repression of p63. Reduced ASPP2 expression associates with tumor metastasis and increased p63 expression in human head and neck SCCs. This study identifies ASPP2 as a tumor suppressor that suppresses SCC via inflammatory signaling through NF-κB–mediated repression of p63. |
| doi_str_mv | 10.1073/pnas.1309362110 |
| format | Article |
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The majority of existing mouse SCC models involve multiple gene mutations. Very few mouse models of spontaneous SCC have been generated by a single gene deletion. Here we report a haploinsufficient SCC mouse model in which exon 3 of the Tp53BP2 gene (a p53 binding protein) was deleted in one allele in a BALB/c genetic background. Tp53BP2 encodes ASPP2 (ankyrin repeats, SH3 domain and protein rich region containing protein 2). Keratinocyte differentiation induces ASPP2 and its expression is inversely correlated with p63 protein in vitro and in vivo. Up-regulation of p63 expression is required for ASPP2 Δᵉˣᵒⁿ³/⁺ BALB/c mice to develop SCC, as heterozygosity of p63 but not p53 prevents them from developing it. Mechanistically, ASPP2 inhibits ΔNp63 expression through its ability to bind IκB and enhance nuclear Rel/A p65, a component of the NF-κB transcription complex, which mediates the repression of p63. Reduced ASPP2 expression associates with tumor metastasis and increased p63 expression in human head and neck SCCs. This study identifies ASPP2 as a tumor suppressor that suppresses SCC via inflammatory signaling through NF-κB–mediated repression of p63.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1309362110</identifier><identifier>PMID: 24127607</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Animals ; Biological Sciences ; Cancer ; Carcinoma, Squamous Cell - genetics ; Carcinoma, Squamous Cell - immunology ; Cell Line ; Crosses, Genetic ; Disease Models, Animal ; DNA Primers - genetics ; Gene expression ; Genetics ; Haploinsufficiency ; Humans ; Immunoblotting ; Immunoprecipitation ; Mice ; Mice, Inbred BALB C ; Microarray Analysis ; Oncology ; Phosphoproteins - metabolism ; Proteins ; Real-Time Polymerase Chain Reaction ; RNA, Small Interfering - genetics ; Rodents ; Signal Transduction - immunology ; Trans-Activators - metabolism ; Transcription Factor RelA - metabolism ; Tumor Suppressor Proteins - genetics ; Tumor Suppressor Proteins - immunology ; Tumor Suppressor Proteins - metabolism ; Tumors</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2013-10, Vol.110 (44), p.17969-17974</ispartof><rights>Copyright National Academy of Sciences Oct 30, 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c536t-de0b29f2dad2b94585e6ae61c9afcf2492048863e3df0634c153e8a2aee2d90c3</citedby><cites>FETCH-LOGICAL-c536t-de0b29f2dad2b94585e6ae61c9afcf2492048863e3df0634c153e8a2aee2d90c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/110/44.cover.gif</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3816480/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3816480/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24127607$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Tordella, Luca</creatorcontrib><creatorcontrib>Koch, Sofia</creatorcontrib><creatorcontrib>Salter, Victoria</creatorcontrib><creatorcontrib>Pagotto, Anna</creatorcontrib><creatorcontrib>Doondeea, Jessica B</creatorcontrib><creatorcontrib>Feller, Stephan M</creatorcontrib><creatorcontrib>Ratnayaka, Indrika</creatorcontrib><creatorcontrib>Zhong, Shan</creatorcontrib><creatorcontrib>Goldin, Robert D</creatorcontrib><creatorcontrib>Lozano, Guillermina</creatorcontrib><creatorcontrib>McKeon, Frank D</creatorcontrib><creatorcontrib>Tavassoli, Mahvash</creatorcontrib><creatorcontrib>Fritzsche, Florian</creatorcontrib><creatorcontrib>Huber, Gerhard F</creatorcontrib><creatorcontrib>Rössle, Matthias</creatorcontrib><creatorcontrib>Moch, Holger</creatorcontrib><creatorcontrib>Lu, Xin</creatorcontrib><title>ASPP2 suppresses squamous cell carcinoma via RelA/p65–mediated repression of p63</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Squamous cell carcinoma (SCC) is highly malignant and refractory to therapy. The majority of existing mouse SCC models involve multiple gene mutations. Very few mouse models of spontaneous SCC have been generated by a single gene deletion. Here we report a haploinsufficient SCC mouse model in which exon 3 of the Tp53BP2 gene (a p53 binding protein) was deleted in one allele in a BALB/c genetic background. Tp53BP2 encodes ASPP2 (ankyrin repeats, SH3 domain and protein rich region containing protein 2). Keratinocyte differentiation induces ASPP2 and its expression is inversely correlated with p63 protein in vitro and in vivo. Up-regulation of p63 expression is required for ASPP2 Δᵉˣᵒⁿ³/⁺ BALB/c mice to develop SCC, as heterozygosity of p63 but not p53 prevents them from developing it. Mechanistically, ASPP2 inhibits ΔNp63 expression through its ability to bind IκB and enhance nuclear Rel/A p65, a component of the NF-κB transcription complex, which mediates the repression of p63. Reduced ASPP2 expression associates with tumor metastasis and increased p63 expression in human head and neck SCCs. This study identifies ASPP2 as a tumor suppressor that suppresses SCC via inflammatory signaling through NF-κB–mediated repression of p63.</description><subject>Animals</subject><subject>Biological Sciences</subject><subject>Cancer</subject><subject>Carcinoma, Squamous Cell - genetics</subject><subject>Carcinoma, Squamous Cell - immunology</subject><subject>Cell Line</subject><subject>Crosses, Genetic</subject><subject>Disease Models, Animal</subject><subject>DNA Primers - genetics</subject><subject>Gene expression</subject><subject>Genetics</subject><subject>Haploinsufficiency</subject><subject>Humans</subject><subject>Immunoblotting</subject><subject>Immunoprecipitation</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Microarray Analysis</subject><subject>Oncology</subject><subject>Phosphoproteins - metabolism</subject><subject>Proteins</subject><subject>Real-Time Polymerase Chain Reaction</subject><subject>RNA, Small Interfering - genetics</subject><subject>Rodents</subject><subject>Signal Transduction - immunology</subject><subject>Trans-Activators - metabolism</subject><subject>Transcription Factor RelA - metabolism</subject><subject>Tumor Suppressor Proteins - genetics</subject><subject>Tumor Suppressor Proteins - immunology</subject><subject>Tumor Suppressor Proteins - metabolism</subject><subject>Tumors</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkc1u1DAUhS1ERaeFNTuwxIZNOtc_cewN0qjiT6rUqqVry-PclFRJnNqTSux4B96QJ6nDTAfK6i7ud47uuYeQ1wxOGFRiOQ4unTABRijOGDwjCwaGFUoaeE4WALwqtOTykByldAsAptTwghxyyXiloFqQy9XVxQWnaRrHiClhoulucn2YEvXYddS76Nsh9I7et45eYrdajqr8_fNXj3XrNljTiH-UbRhoaOioxEty0Lgu4avdPCbXnz5-O_1SnJ1__nq6Oit8KdSmqBHW3DS8djVfG1nqEpVDxbxxjW-4NByk1kqgqBtQQnpWCtSOO0ReG_DimHzY-o7TOl_jcdhE19kxtr2LP2xwrX26Gdrv9ibcW6GZkhqywfudQQx3E6aN7ds0p3YD5gdYJmUljaoqntF3_6G3YYpDjjdThhmjSpWp5ZbyMaQUsdkfw8DOfdm5L_u3r6x482-GPf9YUAboDpiVe7vsJ6VllVEmI2-3SOOCdTexTfb6igNTAEwyabR4AByTpbk</recordid><startdate>20131029</startdate><enddate>20131029</enddate><creator>Tordella, Luca</creator><creator>Koch, Sofia</creator><creator>Salter, Victoria</creator><creator>Pagotto, Anna</creator><creator>Doondeea, Jessica B</creator><creator>Feller, Stephan M</creator><creator>Ratnayaka, Indrika</creator><creator>Zhong, Shan</creator><creator>Goldin, Robert D</creator><creator>Lozano, Guillermina</creator><creator>McKeon, Frank D</creator><creator>Tavassoli, Mahvash</creator><creator>Fritzsche, Florian</creator><creator>Huber, Gerhard F</creator><creator>Rössle, Matthias</creator><creator>Moch, Holger</creator><creator>Lu, Xin</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><scope>FBQ</scope><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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20131029</creationdate><title>ASPP2 suppresses squamous cell carcinoma via RelA/p65–mediated repression of p63</title><author>Tordella, Luca ; Koch, Sofia ; Salter, Victoria ; Pagotto, Anna ; Doondeea, Jessica B ; Feller, Stephan M ; Ratnayaka, Indrika ; Zhong, Shan ; Goldin, Robert D ; Lozano, Guillermina ; McKeon, Frank D ; Tavassoli, Mahvash ; Fritzsche, Florian ; Huber, Gerhard F ; Rössle, Matthias ; Moch, Holger ; Lu, Xin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c536t-de0b29f2dad2b94585e6ae61c9afcf2492048863e3df0634c153e8a2aee2d90c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Animals</topic><topic>Biological Sciences</topic><topic>Cancer</topic><topic>Carcinoma, Squamous Cell - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Tordella, Luca</au><au>Koch, Sofia</au><au>Salter, Victoria</au><au>Pagotto, Anna</au><au>Doondeea, Jessica B</au><au>Feller, Stephan M</au><au>Ratnayaka, Indrika</au><au>Zhong, Shan</au><au>Goldin, Robert D</au><au>Lozano, Guillermina</au><au>McKeon, Frank D</au><au>Tavassoli, Mahvash</au><au>Fritzsche, Florian</au><au>Huber, Gerhard F</au><au>Rössle, Matthias</au><au>Moch, Holger</au><au>Lu, Xin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>ASPP2 suppresses squamous cell carcinoma via RelA/p65–mediated repression of p63</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2013-10-29</date><risdate>2013</risdate><volume>110</volume><issue>44</issue><spage>17969</spage><epage>17974</epage><pages>17969-17974</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Squamous cell carcinoma (SCC) is highly malignant and refractory to therapy. The majority of existing mouse SCC models involve multiple gene mutations. Very few mouse models of spontaneous SCC have been generated by a single gene deletion. Here we report a haploinsufficient SCC mouse model in which exon 3 of the Tp53BP2 gene (a p53 binding protein) was deleted in one allele in a BALB/c genetic background. Tp53BP2 encodes ASPP2 (ankyrin repeats, SH3 domain and protein rich region containing protein 2). Keratinocyte differentiation induces ASPP2 and its expression is inversely correlated with p63 protein in vitro and in vivo. Up-regulation of p63 expression is required for ASPP2 Δᵉˣᵒⁿ³/⁺ BALB/c mice to develop SCC, as heterozygosity of p63 but not p53 prevents them from developing it. Mechanistically, ASPP2 inhibits ΔNp63 expression through its ability to bind IκB and enhance nuclear Rel/A p65, a component of the NF-κB transcription complex, which mediates the repression of p63. Reduced ASPP2 expression associates with tumor metastasis and increased p63 expression in human head and neck SCCs. This study identifies ASPP2 as a tumor suppressor that suppresses SCC via inflammatory signaling through NF-κB–mediated repression of p63.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>24127607</pmid><doi>10.1073/pnas.1309362110</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Biological Sciences Cancer Carcinoma, Squamous Cell - genetics Carcinoma, Squamous Cell - immunology Cell Line Crosses, Genetic Disease Models, Animal DNA Primers - genetics Gene expression Genetics Haploinsufficiency Humans Immunoblotting Immunoprecipitation Mice Mice, Inbred BALB C Microarray Analysis Oncology Phosphoproteins - metabolism Proteins Real-Time Polymerase Chain Reaction RNA, Small Interfering - genetics Rodents Signal Transduction - immunology Trans-Activators - metabolism Transcription Factor RelA - metabolism Tumor Suppressor Proteins - genetics Tumor Suppressor Proteins - immunology Tumor Suppressor Proteins - metabolism Tumors |
| title | ASPP2 suppresses squamous cell carcinoma via RelA/p65–mediated repression of p63 |
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