Repressed BMP signaling reactivates NKL homeobox gene MSX1 in a T-ALL subset

References

• Aifantis I, Raetz E, Buonamici S. Molecular pathogenesis of T-cell leukaemia and lymphoma. Nat Rev Immunol 2008;8:380–390.
   PubMed Web of Science ®Google Scholar
• Ferrando AA, Neuberg DS, Staunton J, et al. Gene expression signatures define novel oncogenic pathways in T cell acute lymphoblastic leukemia. Cancer Cell 2002;1:75–87.
   PubMed Web of Science ®Google Scholar
• Graux C, Cools J, Michaux L, et al. Cytogenetics and molecular genetics of T-cell acute lymphoblastic leukemia: from thymocyte to lymphoblast. Leukemia 2006;20:1496–1510.
   PubMed Web of Science ®Google Scholar
• Duboule D. Guidebook to the homeobox genes. Oxford: Oxford University Press; 1994.
   Google Scholar
• Argiropoulos B, Humphries RK. Hox genes in hematopoiesis and leukemogenesis. Oncogene 2007;26:6766–6776.
   PubMed Web of Science ®Google Scholar
• Holland PW, Booth HA, Bruford EA. Classification and nomenclature of all human homeobox genes. BMC Biol 2007;5:47.
   PubMed Web of Science ®Google Scholar
• Alappat S, Zhang ZY, Chen YP. Msx homeobox gene family and craniofacial development. Cell Res 2003;13:429–442.
   PubMed Web of Science ®Google Scholar
• Ramos C, Robert B. msh/Msx gene family in neural development. Trends Genet 2005;21:624–632.
   PubMed Web of Science ®Google Scholar
• Chen YH, Ishii M, Sun J, et al. Msx1 and Msx2 regulate survival of secondary heart field precursors and post-migratory proliferation of cardiac neural crest in the outflow tract. Dev Biol 2007;308:421–437.
   PubMedGoogle Scholar
• Satokata I, Maas R. Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nat Genet 1994;6:348–356.
   PubMed Web of Science ®Google Scholar
• Nieminen P, Kotilainen J, Aalto Y, et al. MSX1 gene is deleted in Wolf-Hirschhorn syndrome patients with oligodontia. J Dent Res 2003;82:1013–1017.
   PubMed Web of Science ®Google Scholar
• Nagel S, Venturini L, Przybylski GK, et al. NK-like homeodomain proteins activate NOTCH3-signaling in leukemic T-cells. BMC Cancer 2009;9:371.
   PubMed Web of Science ®Google Scholar
• Nagel S, Schneider B, Meyer C, et al. Transcriptional deregulation of homeobox gene ZHX2 in Hodgkin lymphoma. Leuk Res 2012;36: 646–655.
   PubMed Web of Science ®Google Scholar
• Nagel S, Ehrentraut S, Meyer C, et al. Oncogenic deregulation of NKL homeobox gene MSX1 in mantle cell lymphoma. Leuk Lymphoma 2014 Feb 17. [Epub ahead of print]
   Web of Science ®Google Scholar
• Borges L, Iacovino M, Mayerhofer T, et al. A critical role for endoglin in the emergence of blood during embryonic development. Blood 2012;119:5417–5428.
   PubMed Web of Science ®Google Scholar
• Laurenti E, Doulatov S, Zandi S, et al. The transcriptional architecture of early human hematopoiesis identifies multilevel control of lymphoid commitment. Nat Immunol 2013;14:756–763.
   PubMed Web of Science ®Google Scholar
• Jojic V, Shay T, Sylvia K, et al. Identification of transcriptional regulators in the mouse immune system. Nat Immunol 2013;14:633–643.
   PubMed Web of Science ®Google Scholar
• Lee H, Habas R, Abate-Shen C. MSX1 cooperates with histone H1b for inhibition of transcription and myogenesis. Science 2004; 304:1675–1678.
   PubMed Web of Science ®Google Scholar
• Rave-Harel N, Miller NL, Givens ML, et al. The Groucho-related gene family regulates the gonadotropin-releasing hormone gene through interaction with the homeodomain proteins MSX1 and OCT1. J Biol Chem 2005;280:30975–30983.
   PubMed Web of Science ®Google Scholar
• Wang J, Kumar RM, Biggs VJ, et al. The Msx1 homeoprotein recruits Polycomb to the nuclear periphery during development. Dev Cell 2011;21:575–588.
   PubMedGoogle Scholar
• Wang J, Abate-Shen C. The MSX1 homeoprotein recruits G9a methyltransferase to repressed target genes in myoblast cells. PLoS One 2012;7:e37647.
   PubMed Web of Science ®Google Scholar
• Alvarez Martinez CE, Binato R, Gonzalez S, et al. Characterization of a Smad motif similar to Drosophila mad in the mouse Msx 1 promoter. Biochem Biophys Res Commun 2002;291:655–662.
   PubMed Web of Science ®Google Scholar
• Tribulo C, Aybar MJ, Nguyen VH, et al. Regulation of Msx genes by a Bmp gradient is essential for neural crest specification. Development 2003;130:6441–6452.
   PubMed Web of Science ®Google Scholar
• Nie X, Deng CX, Wang Q, et al. Disruption of Smad4 in neural crest cells leads to mid-gestation death with pharyngeal arch, craniofacial and cardiac defects. Dev Biol 2008;316:417–430.
   PubMed Web of Science ®Google Scholar
• Weiss A, Attisano L. The TGFbeta superfamily signaling pathway. Wiley Interdiscip Rev Dev Biol 2013;2:47–63.
   PubMed Web of Science ®Google Scholar
• Yu PB, Hong CC, Sachidanandan C, et al. Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat Chem Biol 2008;4:33–41.
   PubMed Web of Science ®Google Scholar
• Harvey RP. NK-2 homeobox genes and heart development. Dev Biol 1996;178:203–216.
   PubMed Web of Science ®Google Scholar
• Nagel S, Ehrentraut S, Tomasch J, et al. Ectopic expression of homeobox gene NKX2-1 in diffuse large B-cell lymphoma is mediated by aberrant chromatin modifications. PLoS One 2013;8:e61447.
   PubMed Web of Science ®Google Scholar
• Drexler HG. Guide to leukemia-lymphoma cell lines. 2nd ed. Braunschweig: DSMZ; 2010.
   Google Scholar
• Kees UR, Ford J, Price PJ, et al. PER-117: a new human ALL cell line with an immature thymic phenotype. Leuk Res 1987;11: 489–498.
   PubMed Web of Science ®Google Scholar
• Homminga I, Pieters R, Langerak AW, et al. Integrated transcript and genome analyses reveal NKX2-1 and MEF2C as potential oncogenes in T cell acute lymphoblastic leukemia. Cancer Cell 2011;19:484–497.
   PubMed Web of Science ®Google Scholar
• Novershtern N, Subramanian A, Lawton LN, et al. Densely interconnected transcriptional circuits control cell states in human hematopoiesis. Cell 2011;144:296–309.
   PubMed Web of Science ®Google Scholar
• Macleod RA, Kaufmann M, Drexler HG. Cytogenetic analysis of cancer cell lines. Methods Mol Biol 2011;731:57–78.
   PubMedGoogle Scholar
• MacLeod RA, Kaufmann M, Drexler HG. Cytogenetic harvesting of commonly used tumor cell lines. Nat Protoc 2007;2:372–382.
   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: e40747.
   PubMed Web of Science ®Google Scholar
• Hatano M, Roberts CW, Minden M, et al. Deregulation of a homeobox gene, HOX11, by the t(10;14) in T cell leukemia. Science 1991;253:79–82.
   PubMed Web of Science ®Google Scholar
• Bernard OA, Busson-LeConiat M, Ballerini P, et al. A new recurrent and specific cryptic translocation, t(5;14)(q35;q32), is associated with expression of the Hox11L2 gene in T acute lymphoblastic leukemia. Leukemia 2001;15:1495–1504.
   PubMed Web of Science ®Google Scholar
• Nagel S, Kaufmann M, Drexler HG, et al. The cardiac homeobox gene NKX2-5 is deregulated by juxtaposition with BCL11B in pediatric T-ALL cell lines via a novel t(5;14)(q35.1;q32.2). Cancer Res 2003;63:5329–5334.
   PubMed Web of Science ®Google Scholar
• Nagel S, Venturini L, Przybylski GK, et al. Activation of paired-homeobox gene PITX1 by del(5)(q31) in T-cell acute lymphoblastic leukemia. Leuk Lymphoma 2011;52:1348–1359.
   PubMed Web of Science ®Google Scholar
• Grégoire JM, Roméo PH. T-cell expression of the human GATA-3 gene is regulated by a non-lineage-specific silencer. J Biol Chem 1999;274:6567–6578.
   PubMed Web of Science ®Google Scholar
• Yu S, Zhou X, Steinke FC, et al. The TCF-1 and LEF-1 transcription factors have cooperative and opposing roles in T cell development and malignancy. Immunity 2012;37:813–826.
   PubMed Web of Science ®Google Scholar
• Held W, Clevers H, Grosschedl R. Redundant functions of TCF-1 and LEF-1 during T and NK cell development, but unique role of TCF-1 for Ly49 NK cell receptor acquisition. Eur J Immunol 2003;33:1393–1398.
   PubMed Web of Science ®Google Scholar
• Oosterwegel M, van de Wetering M, Timmerman J, et al. Differential expression of the HMG box factors TCF-1 and LEF-1 during murine embryogenesis. Development 1993;118:439–448.
   PubMed Web of Science ®Google Scholar
• Meulemans D, Bronner-Fraser M. Central role of gene cooption in neural crest evolution. J Exp Zool B Mol Dev Evol 2005;304:298–303.
   PubMed Web of Science ®Google Scholar
• Sauka-Spengler T, Meulemans D, Jones M, et al. Ancient evolutionary origin of the neural crest gene regulatory network. Dev Cell 2007;13:405–420.
   PubMed Web of Science ®Google Scholar
• Gouti M, Briscoe J, Gavalas A. Anterior Hox genes interact with components of the neural crest specification network to induce neural crest fates. Stem Cells 2011;29:858–870.
   PubMed Web of Science ®Google Scholar
• Ishii M, Arias AC, Liu L, et al. A stable cranial neural crest cell line from mouse. Stem Cells Dev 2012;21:3069–3080.
   PubMed Web of Science ®Google Scholar
• Coles EG, Gammill LS, Miner JH, et al. Abnormalities in neural crest cell migration in laminin alpha5 mutant mice. Dev Biol 2006;289:218–228.
   PubMed Web of Science ®Google Scholar
• Soulier J, Clappier E, Cayuela JM, et al. HOXA genes are included in genetic and biologic networks defining human acute T-cell leukemia (T-ALL). Blood 2005;106:274–286.
   PubMed Web of Science ®Google Scholar
• Kusy S, Gerby B, Goardon N, et al. NKX3.1 is a direct TAL1 target gene that mediates proliferation of TAL1-expressing human T cell acute lymphoblastic leukemia. J Exp Med 2010;207:2141–2156.
   PubMedGoogle Scholar
• Franceschini A, Szklarczyk D, Frankild S, et al. STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res 2013;41(Database issue):D808–D815.
   PubMedGoogle Scholar
• Passa O, Tsalavos S, Belyaev NN, et al. Compartmentalization of bone morphogenetic proteins and their antagonists in lymphoid progenitors and supporting microenvironments and functional implications. Immunology 2011;134:349–359.
   PubMed Web of Science ®Google Scholar
• Hager-Theodorides AL, Outram SV, Shah DK, et al. Bone morphogenetic protein 2/4 signaling regulates early thymocyte differentiation. J Immunol 2002;169:5496–5504.
   PubMed Web of Science ®Google Scholar
• Graf D, Nethisinghe S, Palmer DB, et al. The developmentally regulated expression of twisted gastrulation reveals a role for bone morphogenetic proteins in the control of T cell development. J Exp Med 2002;196:163–171.
   PubMed Web of Science ®Google Scholar
• Hidalgo L, Martínez VG, Valencia J, et al. Expression of BMPRIA on human thymic NK cell precursors: role of BMP signaling in intrathymic NK cell development. Blood 2012;119:1861–1871.
   PubMed Web of Science ®Google Scholar
• Garcia-Fernàndez J. The genesis and evolution of homeobox gene clusters. Nat Rev Genet 2005;6:881–892.
   PubMed Web of Science ®Google Scholar
• Bernassola F, Karin M, Ciechanover A, et al. The HECT family of E3 ubiquitin ligases: multiple players in cancer development. Cancer Cell 2008;14:10–21.
   PubMed Web of Science ®Google Scholar
• Weng Q, Chen Y, Wang H, et al. Dual-mode modulation of Smad signaling by Smad-interacting protein Sip1 is required for myelination in the central nervous system. Neuron 2012;73:713–728.
   PubMed Web of Science ®Google Scholar
• Goossens S, Janzen V, Bartunkova S, et al. The EMT regulator Zeb2/Sip1 is essential for murine embryonic hematopoietic stem/progenitor cell differentiation and mobilization. Blood 2011;117:5620–5630.
   PubMedGoogle Scholar
• Van de Putte T, Maruhashi M, Francis A, et al. Mice lacking ZFHX1B, the gene that codes for Smad-interacting protein-1, reveal a role for multiple neural crest cell defects in the etiology of Hirschsprung disease-mental retardation syndrome. Am J Hum Genet 2003;72:465–470.
   PubMed Web of Science ®Google Scholar
• Kalkan T, Iwasaki Y, Park CY, et al. Tumor necrosis factor-receptor-associated factor-4 is a positive regulator of transforming growth factor-beta signaling that affects neural crest formation. Mol Biol Cell 2009;20:3436–3450.
   PubMed Web of Science ®Google Scholar
• Coffinier C, Tran U, Larraín J, et al. Neuralin-1 is a novel Chordin-related molecule expressed in the mouse neural plate. Mech Dev 2001;100:119–122.
   PubMed Web of Science ®Google Scholar
• Nakayama N, Han CE, Scully S, et al. A novel chordin-like protein inhibitor for bone morphogenetic proteins expressed preferentially in mesenchymal cell lineages. Dev Biol 2001;232:372–387.
   PubMed Web of Science ®Google Scholar
• Odelberg SJ, Kollhoff A, Keating MT. Dedifferentiation of mammalian myotubes induced by msx1. Cell 2000;103:1099–1109.
   PubMed Web of Science ®Google Scholar
• Hu G, Lee H, Price SM, et al. Msx homeobox genes inhibit differentiation through upregulation of cyclin D1. Development 2001;128:2373–2384.
   PubMed Web of Science ®Google Scholar
• Catron KM, Zhang H, Marshall SC, et al. Transcriptional repression by Msx-1 does not require homeodomain DNA-binding sites. Mol Cell Biol 1995;15:861–871.
   PubMed Web of Science ®Google Scholar
• Wang J, Abate-Shen C. Transcriptional repression by the Msx1 homeoprotein is associated with global redistribution of the H3K27me3 repressive mark to the nuclear periphery. Nucleus 2012;3:155–161.
   PubMed Web of Science ®Google Scholar
• Dadi S, Le Noir S, Payet-Bornet D, et al. TLX homeodomain oncogenes mediate T cell maturation arrest in T-ALL via interaction with ETS1 and suppression of TCRα gene expression. Cancer Cell 2012;21:563–576.
   PubMed Web of Science ®Google Scholar
• Harvey RP. NK-2 homeobox genes and heart development. Dev Biol 1996;178:203–216.
   PubMed Web of Science ®Google Scholar
• Nagel S, Venturini L, Marquez VE, et al. Polycomb repressor complex 2 regulates HOXA9 and HOXA10, activating ID2 in NK/T-cell lines. Mol Cancer 2010;9:151.
   PubMed Web of Science ®Google Scholar
• Gascoyne DM, Long E, Veiga-Fernandes H, et al. The basic leucine zipper transcription factor E4BP4 is essential for natural killer cell development. Nat Immunol 2009;10:1118–1124.
   PubMedGoogle Scholar
• Martinsen BJ, Bronner-Fraser M. Neural crest specification regulated by the helix-loop-helix repressor Id2. Science 1998;281:988–991.
   PubMed Web of Science ®Google Scholar
• Rothenberg EV, Dionne CJ. Lineage plasticity and commitment in T-cell development. Immunol Rev 2002;187:96–115.
   PubMed Web of Science ®Google Scholar