EWS/ATF1 expression induces sarcomas from neural crest-derived cells in mice
Clear cell sarcoma (CCS) is an aggressive soft tissue malignant tumor characterized by a unique t(12;22) translocation that leads to the expression of a chimeric EWS/ATF1 fusion gene. However, little is known about the mechanisms underlying the involvement of EWS/ATF1 in CCS development. In addition...
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| Veröffentlicht in: | The Journal of clinical investigation 2013-02, Vol.123 (2), p.600-610 |
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| creator | Yamada, Kazunari Ohno, Takatoshi Aoki, Hitomi Semi, Katsunori Watanabe, Akira Moritake, Hiroshi Shiozawa, Shunichi Kunisada, Takahiro Kobayashi, Yukiko Toguchida, Junya Shimizu, Katsuji Hara, Akira Yamada, Yasuhiro |
| description | Clear cell sarcoma (CCS) is an aggressive soft tissue malignant tumor characterized by a unique t(12;22) translocation that leads to the expression of a chimeric EWS/ATF1 fusion gene. However, little is known about the mechanisms underlying the involvement of EWS/ATF1 in CCS development. In addition, the cellular origins of CCS have not been determined. Here, we generated EWS/ATF1-inducible mice and examined the effects of EWS/ATF1 expression in adult somatic cells. We found that forced expression of EWS/ATF1 resulted in the development of EWS/ATF1-dependent sarcomas in mice. The histology of EWS/ATF1-induced sarcomas resembled that of CCS, and EWS/ATF1-induced tumor cells expressed CCS markers, including S100, SOX10, and MITF. Lineage-tracing experiments indicated that neural crest-derived cells were subject to EWS/ATF1-driven transformation. EWS/ATF1 directly induced Fos in an ERK-independent manner. Treatment of human and EWS/ATF1-induced CCS tumor cells with FOS-targeted siRNA attenuated proliferation. These findings demonstrated that FOS mediates the growth of EWS/ATF1-associated sarcomas and suggest that FOS is a potential therapeutic target in human CCS. |
| doi_str_mv | 10.1172/JCI63572 |
| format | Article |
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However, little is known about the mechanisms underlying the involvement of EWS/ATF1 in CCS development. In addition, the cellular origins of CCS have not been determined. Here, we generated EWS/ATF1-inducible mice and examined the effects of EWS/ATF1 expression in adult somatic cells. We found that forced expression of EWS/ATF1 resulted in the development of EWS/ATF1-dependent sarcomas in mice. The histology of EWS/ATF1-induced sarcomas resembled that of CCS, and EWS/ATF1-induced tumor cells expressed CCS markers, including S100, SOX10, and MITF. Lineage-tracing experiments indicated that neural crest-derived cells were subject to EWS/ATF1-driven transformation. EWS/ATF1 directly induced Fos in an ERK-independent manner. Treatment of human and EWS/ATF1-induced CCS tumor cells with FOS-targeted siRNA attenuated proliferation. These findings demonstrated that FOS mediates the growth of EWS/ATF1-associated sarcomas and suggest that FOS is a potential therapeutic target in human CCS.</description><identifier>ISSN: 0021-9738</identifier><identifier>EISSN: 1558-8238</identifier><identifier>DOI: 10.1172/JCI63572</identifier><identifier>PMID: 23281395</identifier><language>eng</language><publisher>United States: American Society for Clinical Investigation</publisher><subject>Activating Transcription Factor 1 - genetics ; Animals ; Base Sequence ; Biomedical research ; Care and treatment ; Cell Line, Tumor ; Cell Lineage - genetics ; Cell Proliferation ; Development and progression ; Gene Expression ; Gene Fusion ; Genes ; Genes, fos ; Genetic aspects ; Health aspects ; Humans ; Kinases ; Melanoma ; Mice ; Mice, Transgenic ; Neural Crest - pathology ; Oncogene Proteins, Fusion - genetics ; Physiological aspects ; Proteins ; RNA polymerase ; RNA, Small Interfering - genetics ; RNA-Binding Protein EWS - genetics ; Sarcoma ; Sarcoma, Clear Cell - etiology ; Sarcoma, Clear Cell - genetics ; Sarcoma, Clear Cell - pathology ; Skin cancer ; Transcription factors ; Transcription Factors - genetics ; Transgenic animals ; Tumors</subject><ispartof>The Journal of clinical investigation, 2013-02, Vol.123 (2), p.600-610</ispartof><rights>COPYRIGHT 2013 American Society for Clinical Investigation</rights><rights>Copyright American Society for Clinical Investigation Feb 2013</rights><rights>Copyright © 2013, American Society for Clinical Investigation 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c503t-af0afa5ec3bd6cfa27e0f2926ab94a97ba3098de675aa0db5f8b24f918c601b63</citedby><cites>FETCH-LOGICAL-c503t-af0afa5ec3bd6cfa27e0f2926ab94a97ba3098de675aa0db5f8b24f918c601b63</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3561811/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3561811/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23281395$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yamada, Kazunari</creatorcontrib><creatorcontrib>Ohno, Takatoshi</creatorcontrib><creatorcontrib>Aoki, Hitomi</creatorcontrib><creatorcontrib>Semi, Katsunori</creatorcontrib><creatorcontrib>Watanabe, Akira</creatorcontrib><creatorcontrib>Moritake, Hiroshi</creatorcontrib><creatorcontrib>Shiozawa, Shunichi</creatorcontrib><creatorcontrib>Kunisada, Takahiro</creatorcontrib><creatorcontrib>Kobayashi, Yukiko</creatorcontrib><creatorcontrib>Toguchida, Junya</creatorcontrib><creatorcontrib>Shimizu, Katsuji</creatorcontrib><creatorcontrib>Hara, Akira</creatorcontrib><creatorcontrib>Yamada, Yasuhiro</creatorcontrib><title>EWS/ATF1 expression induces sarcomas from neural crest-derived cells in mice</title><title>The Journal of clinical investigation</title><addtitle>J Clin Invest</addtitle><description>Clear cell sarcoma (CCS) is an aggressive soft tissue malignant tumor characterized by a unique t(12;22) translocation that leads to the expression of a chimeric EWS/ATF1 fusion gene. However, little is known about the mechanisms underlying the involvement of EWS/ATF1 in CCS development. In addition, the cellular origins of CCS have not been determined. Here, we generated EWS/ATF1-inducible mice and examined the effects of EWS/ATF1 expression in adult somatic cells. We found that forced expression of EWS/ATF1 resulted in the development of EWS/ATF1-dependent sarcomas in mice. The histology of EWS/ATF1-induced sarcomas resembled that of CCS, and EWS/ATF1-induced tumor cells expressed CCS markers, including S100, SOX10, and MITF. Lineage-tracing experiments indicated that neural crest-derived cells were subject to EWS/ATF1-driven transformation. EWS/ATF1 directly induced Fos in an ERK-independent manner. Treatment of human and EWS/ATF1-induced CCS tumor cells with FOS-targeted siRNA attenuated proliferation. These findings demonstrated that FOS mediates the growth of EWS/ATF1-associated sarcomas and suggest that FOS is a potential therapeutic target in human CCS.</description><subject>Activating Transcription Factor 1 - genetics</subject><subject>Animals</subject><subject>Base Sequence</subject><subject>Biomedical research</subject><subject>Care and treatment</subject><subject>Cell Line, Tumor</subject><subject>Cell Lineage - genetics</subject><subject>Cell Proliferation</subject><subject>Development and progression</subject><subject>Gene Expression</subject><subject>Gene Fusion</subject><subject>Genes</subject><subject>Genes, fos</subject><subject>Genetic aspects</subject><subject>Health aspects</subject><subject>Humans</subject><subject>Kinases</subject><subject>Melanoma</subject><subject>Mice</subject><subject>Mice, Transgenic</subject><subject>Neural Crest - pathology</subject><subject>Oncogene Proteins, Fusion - genetics</subject><subject>Physiological aspects</subject><subject>Proteins</subject><subject>RNA polymerase</subject><subject>RNA, Small Interfering - genetics</subject><subject>RNA-Binding Protein EWS - genetics</subject><subject>Sarcoma</subject><subject>Sarcoma, Clear Cell - etiology</subject><subject>Sarcoma, Clear Cell - genetics</subject><subject>Sarcoma, Clear Cell - pathology</subject><subject>Skin cancer</subject><subject>Transcription factors</subject><subject>Transcription Factors - genetics</subject><subject>Transgenic animals</subject><subject>Tumors</subject><issn>0021-9738</issn><issn>1558-8238</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BEC</sourceid><sourceid>BENPR</sourceid><recordid>eNqNkkFr3DAQhUVpaDZpob-gGAolFycaybKlS2FZkjZlIYek9ChkeZRVsK2tZIf231dLNiHpKeggkL55mnl6hHwEegrQsLMfq8uai4a9IQsQQpaScfmWLChlUKqGy0NylNIdpVBVonpHDhlnErgSC7I-_3V9try5gAL_bCOm5MNY-LGbLaYimWjDYFLhYhiKEedo-sJmaio7jP4eu8Ji36dcUAze4nty4Eyf8MN-PyY_L85vVt_L9dW3y9VyXVpB-VQaR40zAi1vu9o6wxqkjilWm1ZVRjWt4VTJDutGGEO7VjjZssopkLam0Nb8mHx90N3O7YCdxXHKnelt9IOJf3UwXr-8Gf1G34Z7zUUNEiALnOwFYvg953n04NNuFDNimJMGXslKMsHUK1AOVCpQMqOf_0PvwhzH7IQGJiVVAGL39ukDdWt61H50Ibdo8-owexhGdD6fLznIRjaM0Vzw5VnBBk0_bVLo5yl_VXoJ7lu1MaQU0T05AlTvcqIfc5LRT88dfAIfg8H_Aehytl4</recordid><startdate>20130201</startdate><enddate>20130201</enddate><creator>Yamada, Kazunari</creator><creator>Ohno, Takatoshi</creator><creator>Aoki, Hitomi</creator><creator>Semi, Katsunori</creator><creator>Watanabe, Akira</creator><creator>Moritake, Hiroshi</creator><creator>Shiozawa, Shunichi</creator><creator>Kunisada, Takahiro</creator><creator>Kobayashi, Yukiko</creator><creator>Toguchida, Junya</creator><creator>Shimizu, Katsuji</creator><creator>Hara, Akira</creator><creator>Yamada, Yasuhiro</creator><general>American Society for Clinical Investigation</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>7RV</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BEC</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB0</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>NAPCQ</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>S0X</scope><scope>7X8</scope><scope>7T5</scope><scope>7TK</scope><scope>H94</scope><scope>5PM</scope></search><sort><creationdate>20130201</creationdate><title>EWS/ATF1 expression induces sarcomas from neural crest-derived cells in mice</title><author>Yamada, Kazunari ; Ohno, Takatoshi ; Aoki, Hitomi ; Semi, Katsunori ; Watanabe, Akira ; Moritake, Hiroshi ; Shiozawa, Shunichi ; Kunisada, Takahiro ; Kobayashi, Yukiko ; Toguchida, Junya ; Shimizu, Katsuji ; Hara, Akira ; Yamada, Yasuhiro</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c503t-af0afa5ec3bd6cfa27e0f2926ab94a97ba3098de675aa0db5f8b24f918c601b63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Activating Transcription Factor 1 - genetics</topic><topic>Animals</topic><topic>Base Sequence</topic><topic>Biomedical research</topic><topic>Care and treatment</topic><topic>Cell Line, Tumor</topic><topic>Cell Lineage - genetics</topic><topic>Cell Proliferation</topic><topic>Development and progression</topic><topic>Gene Expression</topic><topic>Gene Fusion</topic><topic>Genes</topic><topic>Genes, fos</topic><topic>Genetic aspects</topic><topic>Health aspects</topic><topic>Humans</topic><topic>Kinases</topic><topic>Melanoma</topic><topic>Mice</topic><topic>Mice, Transgenic</topic><topic>Neural Crest - pathology</topic><topic>Oncogene Proteins, Fusion - genetics</topic><topic>Physiological aspects</topic><topic>Proteins</topic><topic>RNA polymerase</topic><topic>RNA, Small Interfering - genetics</topic><topic>RNA-Binding Protein EWS - genetics</topic><topic>Sarcoma</topic><topic>Sarcoma, Clear Cell - etiology</topic><topic>Sarcoma, Clear Cell - genetics</topic><topic>Sarcoma, Clear Cell - pathology</topic><topic>Skin cancer</topic><topic>Transcription factors</topic><topic>Transcription Factors - 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Academic</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of clinical investigation</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yamada, Kazunari</au><au>Ohno, Takatoshi</au><au>Aoki, Hitomi</au><au>Semi, Katsunori</au><au>Watanabe, Akira</au><au>Moritake, Hiroshi</au><au>Shiozawa, Shunichi</au><au>Kunisada, Takahiro</au><au>Kobayashi, Yukiko</au><au>Toguchida, Junya</au><au>Shimizu, Katsuji</au><au>Hara, Akira</au><au>Yamada, Yasuhiro</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>EWS/ATF1 expression induces sarcomas from neural crest-derived cells in mice</atitle><jtitle>The Journal of clinical investigation</jtitle><addtitle>J Clin Invest</addtitle><date>2013-02-01</date><risdate>2013</risdate><volume>123</volume><issue>2</issue><spage>600</spage><epage>610</epage><pages>600-610</pages><issn>0021-9738</issn><eissn>1558-8238</eissn><abstract>Clear cell sarcoma (CCS) is an aggressive soft tissue malignant tumor characterized by a unique t(12;22) translocation that leads to the expression of a chimeric EWS/ATF1 fusion gene. However, little is known about the mechanisms underlying the involvement of EWS/ATF1 in CCS development. In addition, the cellular origins of CCS have not been determined. Here, we generated EWS/ATF1-inducible mice and examined the effects of EWS/ATF1 expression in adult somatic cells. We found that forced expression of EWS/ATF1 resulted in the development of EWS/ATF1-dependent sarcomas in mice. The histology of EWS/ATF1-induced sarcomas resembled that of CCS, and EWS/ATF1-induced tumor cells expressed CCS markers, including S100, SOX10, and MITF. Lineage-tracing experiments indicated that neural crest-derived cells were subject to EWS/ATF1-driven transformation. EWS/ATF1 directly induced Fos in an ERK-independent manner. Treatment of human and EWS/ATF1-induced CCS tumor cells with FOS-targeted siRNA attenuated proliferation. These findings demonstrated that FOS mediates the growth of EWS/ATF1-associated sarcomas and suggest that FOS is a potential therapeutic target in human CCS.</abstract><cop>United States</cop><pub>American Society for Clinical Investigation</pub><pmid>23281395</pmid><doi>10.1172/JCI63572</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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| source | Journals@Ovid Ovid Autoload; MEDLINE; EZB-FREE-00999 freely available EZB journals; PubMed Central; Alma/SFX Local Collection |
| subjects | Activating Transcription Factor 1 - genetics Animals Base Sequence Biomedical research Care and treatment Cell Line, Tumor Cell Lineage - genetics Cell Proliferation Development and progression Gene Expression Gene Fusion Genes Genes, fos Genetic aspects Health aspects Humans Kinases Melanoma Mice Mice, Transgenic Neural Crest - pathology Oncogene Proteins, Fusion - genetics Physiological aspects Proteins RNA polymerase RNA, Small Interfering - genetics RNA-Binding Protein EWS - genetics Sarcoma Sarcoma, Clear Cell - etiology Sarcoma, Clear Cell - genetics Sarcoma, Clear Cell - pathology Skin cancer Transcription factors Transcription Factors - genetics Transgenic animals Tumors |
| title | EWS/ATF1 expression induces sarcomas from neural crest-derived cells in mice |
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