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Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2018,2,13]]},"abstract":"<jats:p>\n                    Capicua (CIC) regulates a transcriptional network downstream of the RAS\/MAPK signaling cascade. In\n                    <jats:italic>Drosophila<\/jats:italic>\n                    , CIC is important for many developmental processes, including embryonic patterning and specification of wing veins. In humans, CIC has been implicated in neurological diseases, including spinocerebellar ataxia type 1 (SCA1) and a neurodevelopmental syndrome. Additionally, we and others have reported mutations in\n                    <jats:italic>CIC<\/jats:italic>\n                    in several cancers. However, whether CIC is a tumor suppressor remains to be formally tested. In this study, we found that deletion of\n                    <jats:italic>Cic<\/jats:italic>\n                    in adult mice causes T cell acute lymphoblastic leukemia\/lymphoma (T-ALL). Using hematopoietic-specific deletion and bone marrow transplantation studies, we show that loss of\n                    <jats:italic>Cic<\/jats:italic>\n                    from hematopoietic cells is sufficient to drive T-ALL.\n                    <jats:italic>Cic<\/jats:italic>\n                    -null tumors show up-regulation of the KRAS pathway as well as activation of the NOTCH1 and MYC transcriptional programs. In sum, we demonstrate that loss of CIC causes T-ALL, establishing it as a tumor suppressor for lymphoid malignancies. Moreover, we show that mouse models lacking CIC in the hematopoietic system are robust models for studying the role of RAS signaling as well as NOTCH1 and MYC transcriptional programs in T-ALL.\n                  <\/jats:p>","DOI":"10.1073\/pnas.1716452115","type":"journal-article","created":{"date-parts":[[2018,1,30]],"date-time":"2018-01-30T12:05:13Z","timestamp":1517313913000},"update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":34,"title":["Loss of Capicua alters early T cell development and predisposes mice to T cell lymphoblastic leukemia\/lymphoma"],"prefix":"10.1073","volume":"115","author":[{"given":"Qiumin","family":"Tan","sequence":"first","affiliation":[{"name":"Jan and Dan Duncan Neurological Research Institute at Texas Children\u2019s Hospital, Houston, TX 77030;"},{"name":"Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lorenzo","family":"Brunetti","sequence":"additional","affiliation":[{"name":"Stem Cells and Regenerative Medicine Center, Baylor College of Medicine, Houston, TX 77030;"},{"name":"Center for Cell and Gene Therapy, Baylor College of Medicine, Houston, TX 77030;"},{"name":"Centro di Ricerca Emato-Oncologica, University of Perugia, 06156 Perugia, Italy;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maxime W. C.","family":"Rousseaux","sequence":"additional","affiliation":[{"name":"Jan and Dan Duncan Neurological Research Institute at Texas Children\u2019s Hospital, Houston, TX 77030;"},{"name":"Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hsiang-Chih","family":"Lu","sequence":"additional","affiliation":[{"name":"Jan and Dan Duncan Neurological Research Institute at Texas Children\u2019s Hospital, Houston, TX 77030;"},{"name":"Program in Developmental Biology, Baylor College of Medicine, Houston, TX 77030;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ying-Wooi","family":"Wan","sequence":"additional","affiliation":[{"name":"Jan and Dan Duncan Neurological Research Institute at Texas Children\u2019s Hospital, Houston, TX 77030;"},{"name":"Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jean-Pierre","family":"Revelli","sequence":"additional","affiliation":[{"name":"Jan and Dan Duncan Neurological Research Institute at Texas Children\u2019s Hospital, Houston, TX 77030;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7608-0831","authenticated-orcid":false,"given":"Zhandong","family":"Liu","sequence":"additional","affiliation":[{"name":"Jan and Dan Duncan Neurological Research Institute at Texas Children\u2019s Hospital, Houston, TX 77030;"},{"name":"Department of Pediatrics, Baylor College of Medicine, Houston, TX 77030;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Margaret A.","family":"Goodell","sequence":"additional","affiliation":[{"name":"Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030;"},{"name":"Stem Cells and Regenerative Medicine Center, Baylor College of Medicine, Houston, TX 77030;"},{"name":"Center for Cell and Gene Therapy, Baylor College of Medicine, Houston, TX 77030;"},{"name":"Department of Pediatrics, Baylor College of Medicine, Houston, TX 77030;"},{"name":"Texas Children\u2019s Hospital and Houston Methodist Hospital, Houston, TX 77030;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huda Y.","family":"Zoghbi","sequence":"additional","affiliation":[{"name":"Jan and Dan Duncan Neurological Research Institute at Texas Children\u2019s Hospital, Houston, TX 77030;"},{"name":"Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030;"},{"name":"Program in Developmental Biology, Baylor College of Medicine, Houston, TX 77030;"},{"name":"Department of Pediatrics, Baylor College of Medicine, Houston, TX 77030;"},{"name":"Howard Hughes Medical Institute, Baylor College of Medicine, Houston, TX 77030"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"341","published-online":{"date-parts":[[2018,1,30]]},"reference":[{"key":"e_1_3_4_1_2","doi-asserted-by":"crossref","first-page":"e1006622","DOI":"10.1371\/journal.pgen.1006622","article-title":"A new mode of DNA binding distinguishes Capicua from other HMG-box factors and explains its mutation patterns in cancer","volume":"13","author":"For\u00e9s M","year":"2017","unstructured":"M For\u00e9s, , A new mode of DNA binding distinguishes Capicua from other HMG-box factors and explains its mutation patterns in cancer. PLoS Genet 13, e1006622 (2017).","journal-title":"PLoS Genet"},{"key":"e_1_3_4_2_2","doi-asserted-by":"crossref","first-page":"1335","DOI":"10.1016\/j.cell.2006.11.038","article-title":"ATAXIN-1 interacts with the repressor Capicua in its native complex to cause SCA1 neuropathology","volume":"127","author":"Lam YC","year":"2006","unstructured":"YC Lam, , ATAXIN-1 interacts with the repressor Capicua in its native complex to cause SCA1 neuropathology. Cell 127, 1335\u20131347 (2006).","journal-title":"Cell"},{"key":"e_1_3_4_3_2","doi-asserted-by":"crossref","first-page":"746","DOI":"10.1016\/j.devcel.2011.08.017","article-title":"ATXN1 protein family and CIC regulate extracellular matrix remodeling and lung alveolarization","volume":"21","author":"Lee Y","year":"2011","unstructured":"Y Lee, , ATXN1 protein family and CIC regulate extracellular matrix remodeling and lung alveolarization. Dev Cell 21, 746\u2013757 (2011).","journal-title":"Dev Cell"},{"key":"e_1_3_4_4_2","doi-asserted-by":"crossref","first-page":"1383","DOI":"10.1242\/jcs.092965","article-title":"The Capicua repressor: A general sensor of RTK signaling in development and disease","volume":"125","author":"Jim\u00e9nez G","year":"2012","unstructured":"G Jim\u00e9nez, SY Shvartsman, Z Paroush, The Capicua repressor: A general sensor of RTK signaling in development and disease. J Cell Sci 125, 1383\u20131391 (2012).","journal-title":"J Cell Sci"},{"key":"e_1_3_4_5_2","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1038\/ng.3808","article-title":"Disruption of the ATXN1-CIC complex causes a spectrum of neurobehavioral phenotypes in mice and humans","volume":"49","author":"Lu HC","year":"2017","unstructured":"HC Lu, , Disruption of the ATXN1-CIC complex causes a spectrum of neurobehavioral phenotypes in mice and humans. Nat Genet 49, 527\u2013536 (2017).","journal-title":"Nat Genet"},{"key":"e_1_3_4_6_2","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1101\/gad.14.2.224","article-title":"Relief of gene repression by torso RTK signaling: Role of capicua in Drosophila terminal and dorsoventral patterning","volume":"14","author":"Jim\u00e9nez G","year":"2000","unstructured":"G Jim\u00e9nez, A Guichet, A Ephrussi, J Casanova, Relief of gene repression by torso RTK signaling: Role of capicua in Drosophila terminal and dorsoventral patterning. 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Development 138, 915\u2013924 (2011).","journal-title":"Development"},{"key":"e_1_3_4_9_2","doi-asserted-by":"crossref","first-page":"234","DOI":"10.4161\/fly.21160","article-title":"EGFR-dependent downregulation of Capicua and the establishment of Drosophila dorsoventral polarity","volume":"6","author":"Andreu MJ","year":"2012","unstructured":"MJ Andreu, , EGFR-dependent downregulation of Capicua and the establishment of Drosophila dorsoventral polarity. Fly (Austin) 6, 234\u2013239 (2012).","journal-title":"Fly (Austin)"},{"key":"e_1_3_4_10_2","doi-asserted-by":"crossref","first-page":"e1005634","DOI":"10.1371\/journal.pgen.1005634","article-title":"EGFR\/Ras signaling controls Drosophila intestinal stem cell proliferation via capicua-regulated genes","volume":"11","author":"Jin Y","year":"2015","unstructured":"Y Jin, , EGFR\/Ras signaling controls Drosophila intestinal stem cell proliferation via capicua-regulated genes. 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Science 334, 690\u2013693 (2011).","journal-title":"Science"},{"key":"e_1_3_4_13_2","first-page":"1","article-title":"A native interactor scaffolds and stabilizes toxic ATAXIN-1 oligomers in SCA1","volume":"4","author":"Lasagna-Reeves CA","year":"2015","unstructured":"CA Lasagna-Reeves, , A native interactor scaffolds and stabilizes toxic ATAXIN-1 oligomers in SCA1. eLife 4, 1\u201346 (2015).","journal-title":"eLife"},{"key":"e_1_3_4_14_2","doi-asserted-by":"crossref","first-page":"1456","DOI":"10.1101\/gad.300244.117","article-title":"Inactivation of Capicua in adult mice causes T-cell lymphoblastic lymphoma","volume":"31","author":"Sim\u00f3n-Carrasco L","year":"2017","unstructured":"L Sim\u00f3n-Carrasco, , Inactivation of Capicua in adult mice causes T-cell lymphoblastic lymphoma. Genes Dev 31, 1456\u20131468 (2017).","journal-title":"Genes Dev"},{"key":"e_1_3_4_15_2","doi-asserted-by":"crossref","first-page":"2125","DOI":"10.1093\/hmg\/ddl136","article-title":"Fusion between CIC and DUX4 up-regulates PEA3 family genes in Ewing-like sarcomas with t(4;19)(q35;q13) translocation","volume":"15","author":"Kawamura-Saito M","year":"2006","unstructured":"M Kawamura-Saito, , Fusion between CIC and DUX4 up-regulates PEA3 family genes in Ewing-like sarcomas with t(4;19)(q35;q13) translocation. Hum Mol Genet 15, 2125\u20132137 (2006).","journal-title":"Hum Mol Genet"},{"key":"e_1_3_4_16_2","doi-asserted-by":"crossref","first-page":"1324","DOI":"10.1038\/modpathol.2016.140","article-title":"Evaluation of ETV4 and WT1 expression in CIC-rearranged sarcomas and histologic mimics","volume":"29","author":"Hung YP","year":"2016","unstructured":"YP Hung, CDM Fletcher, JL Hornick, Evaluation of ETV4 and WT1 expression in CIC-rearranged sarcomas and histologic mimics. 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Nature 548, 297\u2013303 (2017).","journal-title":"Nature"},{"key":"e_1_3_4_19_2","doi-asserted-by":"crossref","first-page":"1453","DOI":"10.1126\/science.1210557","article-title":"Mutations in CIC and FUBP1 contribute to human oligodendroglioma","volume":"333","author":"Bettegowda C","year":"2011","unstructured":"C Bettegowda, , Mutations in CIC and FUBP1 contribute to human oligodendroglioma. Science 333, 1453\u20131455 (2011).","journal-title":"Science"},{"key":"e_1_3_4_20_2","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1002\/ana.24443","article-title":"CIC inactivating mutations identify aggressive subset of 1p19q codeleted gliomas","volume":"78","author":"Gleize V","year":"2015","unstructured":"V Gleize, , CIC inactivating mutations identify aggressive subset of 1p19q codeleted gliomas. Ann Neurol; POLA network 78, 355\u2013374 (2015).","journal-title":"Ann Neurol"},{"key":"e_1_3_4_21_2","doi-asserted-by":"crossref","first-page":"6097","DOI":"10.1158\/0008-5472.CAN-17-1018","article-title":"Cic loss promotes gliomagenesis via aberrant neural stem cell proliferation and differentiation","volume":"77","author":"Yang R","year":"2017","unstructured":"R Yang, , Cic loss promotes gliomagenesis via aberrant neural stem cell proliferation and differentiation. Cancer Res 77, 6097\u20136108 (2017).","journal-title":"Cancer Res"},{"key":"e_1_3_4_22_2","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1038\/sj.emboj.7601532","article-title":"A MAPK docking site is critical for downregulation of Capicua by Torso and EGFR RTK signaling","volume":"26","author":"Astigarraga S","year":"2007","unstructured":"S Astigarraga, , A MAPK docking site is critical for downregulation of Capicua by Torso and EGFR RTK signaling. 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