SIX6 is a TAL1-regulated transcription factor in T-ALL and associated with inferior outcome

References

• Pui C, Relling MV, Downing JR. Acute lymphoblastic leukemia. N Engl J Med. 2004;350(15):1535–1548.
   PubMed Web of Science ®Google Scholar
• Quist-Paulsen P, Toft N, Heyman M, et al. T-cell acute lymphoblastic leukemia in patients 1–45 years treated with the pediatric NOPHO ALL2008 protocol. Leukemia. 2020;34(2):347–357.
   PubMed Web of Science ®Google Scholar
• Liu Y, Easton J, Shao Y, et al. The genomic landscape of pediatric and young adult T-lineage acute lymphoblastic leukemia. Nat Genet. 2017;49(8):1211–1218.
   PubMed Web of Science ®Google Scholar
• Rothenberg EV. The chromatin landscape and transcription factors in T cell programming. Trends Immunol. 2014;35(5):195–204.
   PubMed Web of Science ®Google Scholar
• Girardi T, Vicente C, Cools J, et al. The genetics and molecular biology of T-ALL, Blood. 2017;129:1113–1123.
   PubMed Web of Science ®Google Scholar
• Haider Z, Larsson P, Landfors M, et al. An integrated transcriptome analysis in T-cell acute lymphoblastic leukemia links DNA methylation subgroups to dysregulated TAL1 and ANTP homeobox gene expression. Cancer Med. 2019;8(1):311–324.
   PubMed Web of Science ®Google Scholar
• Heinäniemi M, Vuorenmaa T, Teppo S, et al. Transcription-coupled genetic instability marks acute lymphoblastic leukemia structural variation hotspots. eLife. 2016;5:e13087.
   PubMed Web of Science ®Google Scholar
• Teppo S, Laukkanen S, Liuksiala T, et al. Genome-wide repression of eRNA and target gene loci by the ETV6-RUNX1 fusion in acute leukemia. Genome Res. 2016;26(11):1468–1477.
   PubMed Web of Science ®Google Scholar
• Wang D, Garcia-Bassets I, Benner C, et al. Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA. Nature. 2011;474(7351):390–394.
   PubMed Web of Science ®Google Scholar
• Kaikkonen M, Spann N, Heinz S, et al. Remodeling of the enhancer landscape during macrophage activation is coupled to enhancer transcription. Mol Cell. 2013;51(3):310–325.
   PubMed Web of Science ®Google Scholar
• Hnisz D, Weintraub AS, Day DS, et al. Activation of proto-oncogenes by disruption of chromosome neighborhoods. Science. 2016;351(6280):1454–1458.
   PubMed Web of Science ®Google Scholar
• Abraham BJ, Hnisz D, Weintraub AS, et al. Small genomic insertions form enhancers that misregulate oncogenes. Nat Commun. 2017;8:14385.
   PubMed Web of Science ®Google Scholar
• Leong WZ, Tan SH, Ngoc PCT, et al. ARID5B as a critical downstream target of the TAL1 complex that activates the oncogenic transcriptional program and promotes T-cell leukemogenesis. Genes Dev. 2017;31(23–24):2343–2360.
   PubMed Web of Science ®Google Scholar
• Orlando D, Chen M, Brown V, et al. Quantitative ChIP-Seq normalization reveals global modulation of the epigenome. Cell Rep. 2014;9(3):1163–1170.
   PubMed Web of Science ®Google Scholar
• Sanda T, Lawton LN, Barrasa MI, et al. Core transcriptional regulatory circuit controlled by the TAL1 complex in human T cell acute lymphoblastic leukemia. Cancer Cell. 2012;22(2):209–221.
   PubMed Web of Science ®Google Scholar
• Lucic B, Chen H, Kuzman M, et al. Spatially clustered loci with multiple enhancers are frequent targets of HIV-1 integration. Nat Commun. 2019;10(1):4059.
   PubMedGoogle Scholar
• Park J, Botting RA, Domínguez Conde C, et al. A cell atlas of human thymic development defines T cell repertoire formation. Science. 2020;367(6480):eaay3224.
   PubMed Web of Science ®Google Scholar
• Mehtonen J, Pölönen P, Häyrynen S, et al. Data-driven characterization of molecular phenotypes across heterogeneous sample collections. Nucleic Acids Res. 2019;47(13):e76.
   PubMed Web of Science ®Google Scholar
• Pölönen P, Mehtonen J, Lin J, et al. Hemap: an interactive online resource for characterizing molecular phenotypes across hematologic malignancies. Cancer Res. 2019;79(10):2466–2479.
   PubMed Web of Science ®Google Scholar
• Laukkanen S, Grönroos T, Pölönen P, et al. In silico and preclinical drug screening identifies dasatinib as a targeted therapy for T-ALL. Blood Cancer J. 2017;7(9):e604.
   PubMedGoogle Scholar
• Seki M, Kimura S, Isobe T, et al. Recurrent SPI1 (PU.1) fusions in high-risk pediatric T cell acute lymphoblastic leukemia. Nat Genet. 2017;49(8):1274–1281.
   PubMed Web of Science ®Google Scholar
• Roberts KG, Li Y, Payne-Turner D, et al. Targetable kinase-activating lesions in Ph-like acute lymphoblastic leukemia. N Engl J Med. 2014;371(11):1005–1015.
   PubMed Web of Science ®Google Scholar
• Blackburn JS, Liu S, Raiser DM, et al. Notch signaling expands a pre-malignant pool of T-cell acute lymphoblastic leukemia clones without affecting leukemia-propagating cell frequency. Leukemia. 2012;26(9):2069–2078.
   PubMed Web of Science ®Google Scholar
• Grönroos T, Mäkinen A, Laukkanen S, et al. Clinicopathological features and prognostic value of SOX11 in childhood acute lymphoblastic leukemia. Sci Rep. 2020;10(1):2043.
   PubMed Web of Science ®Google Scholar
• Li X, Oghi KA, Zhang J, et al. Eya protein phosphatase activity regulates Six1-Dach-Eya transcriptional effects in mammalian organogenesis. Nature. 2003;426(6964):247–254.
   PubMed Web of Science ®Google Scholar
• López-Rı́os J, Gallardo ME, Rodrı́guez de Córdoba S, et al. Six9 (Optx2), a new member of the six gene family of transcription factors, is expressed at early stages of vertebrate ocular and pituitary development. Mech.Dev. 1999;83(1–2):155–159.
   PubMed Web of Science ®Google Scholar
• Jean D, Bernier G, Gruss P. Six6 (Optx2) is a novel murine Six3-related homeobox gene that demarcates the presumptive pituitary/hypothalamic axis and the ventral optic stalk. Mech Dev. 1999;84(1–2):31–40.
   PubMed Web of Science ®Google Scholar
• Toy J, Sundin OH. Expression of the Optx2 homeobox gene during mouse development. Mech Dev. 1999;83(1–2):183–186.
   PubMed Web of Science ®Google Scholar
• Kuo CT, Leiden JM. Transcriptional regulation of T lymphocyte development and function. Annu Rev Immunol. 1999;17:149–187.
   PubMed Web of Science ®Google Scholar
• Seo W, Taniuchi I. Transcriptional regulation of early T-cell development in the thymus. Eur J Immunol. 2016;46(3):531–538.
   PubMed Web of Science ®Google Scholar
• Naito T, Tanaka H, Naoe Y, et al. Transcriptional control of T-cell development. Int Immunol. 2011;23(11):661–668.
   PubMed Web of Science ®Google Scholar
• Douglas NC, Jacobs H, Bothwell ALM, et al. Defining the specific physiological requirements for C-Myc in T cell development. Nat Immunol. 2001;2(4):307–315.
   PubMed Web of Science ®Google Scholar
• Mingueneau M, Kreslavsky T, Gray D, et al. The transcriptional landscape of Αβ T cell differentiation. Nat Immunol. 2013;14(6):619–632.
   PubMed Web of Science ®Google Scholar
• Lécuyer E, Herblot S, Saint-Denis M, et al. The SCL complex regulates C-kit expression in hematopoietic cells through functional interaction with Sp1. Blood. 2002;100(7):2430–2440.
   PubMed Web of Science ®Google Scholar
• Mansour MR, Abraham BJ, Anders L, et al. Oncogene regulation. An oncogenic super-enhancer formed through somatic mutation of a noncoding intergenic element. Science. 2014;346(6215):1373–1377.
   PubMed Web of Science ®Google Scholar
• Gardini A. Global Run-on Sequencing (GRO-Seq). In: Ørom UA, editor. Enhancer RNAs: methods and protocols. New York (NY): Springer; 2017. p. 111–120.
   Google Scholar
• Calo E, Wysocka J. Modification of enhancer chromatin: what, how, and why? Mol Cell. 2013;49:825–837.
   PubMed Web of Science ®Google Scholar
• Oliveira ML, Akkapeddi P, Ribeiro D, et al. IL-7R-mediated signaling in T-cell acute lymphoblastic leukemia: an update. Adv Biol Regul. 2019;71:88–96.
   PubMedGoogle Scholar
• Ferrando AA. The role of NOTCH1 signaling in T-ALL. Hematology Am Soc Hematol Educ Program. 2009;2009(1):353–361.
   Google Scholar
• Xie H, Hoffmann HM, Meadows JD, et al. Homeodomain proteins SIX3 and SIX6 regulate gonadotrope-specific genes during pituitary development. Mol Endocrinol. 2015;29(6):842–855.
   PubMedGoogle Scholar
• Langenau DM, Traver D, Ferrando AA, et al. Myc-induced T cell leukemia in transgenic zebrafish. Science. 2003;299(5608):887–890.
   PubMed Web of Science ®Google Scholar
• Evangelisti C, Evangelisti C, Chiarini Francesca Lonetti A, et al. Therapeutic potential of targeting mTOR in T-cell acute lymphoblastic leukemia (review). Int J Oncol. 2014;45(3):909–918.
   PubMed Web of Science ®Google Scholar
• Wullschleger S, Loewith R, Hall MN. TOR signaling in growth and metabolism. Cell. 2006;124(3):471–484.
   PubMed Web of Science ®Google Scholar
• Prior IA, Lewis PD, Mattos C. A comprehensive survey of Ras mutations in cancer. Cancer Res. 2012;72(10):2457–2467.
   PubMed Web of Science ®Google Scholar
• Zhou X, Li Z, Zhou J. Tumor necrosis factor Α in the onset and progression of leukemia. Exp Hematol. 2017;45:17–26.
   PubMed Web of Science ®Google Scholar
• Kumar JP. The Sine Oculis Homeobox (SIX) family of transcription factors as regulators of development and disease. Cell Mol Life Sci. 2009;66(4):565–583.
   PubMed Web of Science ®Google Scholar
• Kobayashi M, Nishikawa K, Suzuki T, et al. The Homeobox Protein Six3 interacts with the groucho corepressor and acts as a transcriptional repressor in eye and forebrain formation. Dev Biol. 2001;232(2):315–326.
   PubMed Web of Science ®Google Scholar
• Kenyon KL, Li DJ, Clouser C, et al. Fly six-type homeodomain proteins sine oculis and optix partner with different cofactors during eye development. Dev Dyn. 2005;234(3):497–504.
   PubMed Web of Science ®Google Scholar
• Zhu CC, Dyer MA, Uchikawa M, et al. Six3-mediated auto repression and eye development requires its interaction with members of the groucho-related family of co-repressors. Development. 2002;129(12):2835–2849.
   PubMed Web of Science ®Google Scholar
• Silver SJ, Davies EL, Doyon L, et al. Functional dissection of eyes absent reveals new modes of regulation within the retinal determination gene network. Mol Cell Biol. 2003;23(17):5989–5999.
   PubMed Web of Science ®Google Scholar
• López-Ríos J, Tessmar K, Loosli F, et al. Six3 and Six6 activity is modulated by members of the groucho family. Development. 2003;130(1):185–195.
   PubMed Web of Science ®Google Scholar
• Li X, Perissi V, Liu F, et al. Tissue-specific regulation of retinal and pituitary precursor cell proliferation. Science. 2002;297(5584):1180–1183.
   PubMed Web of Science ®Google Scholar
• Kawakami K, Sato S, Ozaki H, et al. Six family genes—structure and function as transcription factors and their roles in development. Bioessays. 2000;22(7):616–626.
   PubMed Web of Science ®Google Scholar
• Larder R, Clark DD, Miller NLG, et al. Hypothalamic dysregulation and infertility in mice lacking the homeodomain protein Six6. J Neurosci. 2011;31(2):426–438.
   PubMed Web of Science ®Google Scholar
• Liu Q, Li A, Tian Y, et al. The expression profile and clinic significance of the SIX family in non-small cell lung cancer. J Hematol Oncol. 2016;9(1):119.
   PubMedGoogle Scholar
• Chen B, Jiang L, Zhong M, et al. Identification of fusion genes and characterization of transcriptome features in T-cell acute lymphoblastic leukemia. Proc Natl Acad Sci USA. 2018;115(2):373–378.
   PubMed Web of Science ®Google Scholar
• Nagel S, Ehrentraut S, Tomasch J, et al. Transcriptional activation of prostate specific homeobox gene NKX3-1 in subsets of T-cell lymphoblastic leukemia (T-ALL). PLoS One. 2012;7(7):e40747.
   PubMed Web of Science ®Google Scholar
• Nagel S, Meyer C, Kaufmann M, et al. Aberrant activity of NKL homeobox gene NKX3-2 in a T-ALL subset. PLoS One. 2018;13(5):e0197194.
   PubMed Web of Science ®Google Scholar
• Soulier J, Clappier E, Cayuela J, et al. HOXA genes are included in genetic and biologic networks defining human acute T-cell leukemia (T-ALL). Blood. 2005;106(1):274–286.
   PubMed Web of Science ®Google Scholar
• Xu H, Wu K, Tian Y, et al. Expression profile of SIX family members correlates with clinic-pathological features and prognosis of breast cancer: a systematic review and meta-analysis. Medicine. 2016;95(27):e4085.
   PubMed Web of Science ®Google Scholar
• Borssén M, Palmqvist L, Karrman K, et al. Promoter DNA methylation pattern identifies prognostic subgroups in childhood T-cell acute lymphoblastic leukemia. Plos One. 2013;8(6):e65373.
   PubMed Web of Science ®Google Scholar
• De Smedt R, Morscio J, Goossens S, et al. Targeting steroid resistance in T-cell acute lymphoblastic leukemia. Blood Rev. 2019;38:100591.
   PubMed Web of Science ®Google Scholar