The orphan nuclear receptor Ear-2 (Nr2f6) is a novel negative regulator of T cell development

Experimental Hematology

Volumn 42, Issue 1, 2014, Pages 46-58

  Ichim, Christine V ^a,b,c   Dervović, Džana D ^b,d   Zúñiga Pflücker, Juan Carlos ^b,d   Wells, Richard A ^a,b,e  

^a UNIVERSITY OF TORONTO   (Canada)

^b Canada   (Canada)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

^e DEPARTMENT OF RADIATION ONCOLOGY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 1; INHIBITOR OF DIFFERENTIATION 2; NOTCH3 RECEPTOR; ORPHAN NUCLEAR RECEPTOR; ORPHAN NUCLEAR RECEPTOR V ERB A RELATED 2; PEPTIDES AND PROTEINS; PROTEIN BAD; PROTEIN BCL XL; PROTEIN BCL11B; PROTEIN P21; PROTEIN P27; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR 7; TRANSCRIPTION FACTOR GFI 1; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR HOXA9; TRANSCRIPTION FACTOR PU 1; TRANSCRIPTION FACTOR TAL1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE MARROW TRANSPLANTATION; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; HEMATOPOIETIC STEM CELL; IN VITRO STUDY; LYMPHOPOIESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETROVIRUS; T LYMPHOCYTE; THYMOCYTE; THYMUS;

ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; COUP TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HEMATOPOIETIC STEM CELLS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; T-LYMPHOCYTES;

EID: 84890025531     PISSN: 0301472X     EISSN: 18732399     Source Type: Journal    
DOI: 10.1016/j.exphem.2013.09.010     Document Type: Article

References (52)

1. Ichim C.V., Atkins H.L., Iscove N.N., Wells R.A. Identification of a role for the nuclear receptor EAR-2 in the maintenance of clonogenic status within the leukemia cell hierarchy. Leukemia 2011, 25:1687-1696.
2. Mettler U., Vogler G., Urban J. Timing of identity: spatiotemporal regulation of hunchback in neuroblast lineages of Drosophila by Seven-up and Prospero. Development 2006, 133:429-437.
3. Qiu Y., Pereira F.A., DeMayo F.J., Lydon J.P., Tsai S.Y., Tsai M.J. Null mutation of mCOUP-TFI results in defects in morphogenesis of the glossopharyngeal ganglion, axonal projection, and arborization. Genes Dev 1997, 11:1925-1937.
4. Zhou C., Qiu Y., Pereira F.A., Crair M.C., Tsai S.Y., Tsai M.J. The nuclear orphan receptor COUP-TFI is required for differentiation of subplate neurons and guidance of thalamocortical axons. Neuron 1999, 24:847-859.
5. Zhou C., Tsai S.Y., Tsai M.J. COUP-TFI: an intrinsic factor for early regionalization of the neocortex. Genes Dev 2001, 15:2054-2059.
6. You L.R., Lin F.J., Lee C.T., DeMayo F.J., Tsai M.J., Tsai S.Y. Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity. Nature 2005, 435:98-104.
7. Ciszek B., Skubiszewska D., Ratajska A. The anatomy of the cardiac veins in mice. J Anat 2007, 211:53-63.
8. Lee S., Kang J., Yoo J., et al. Prox1 physically and functionally interacts with COUP-TFII to specify lymphatic endothelial cell fate. Blood 2009, 113:1856-1859.
9. Lin F.J., Chen X., Qin J., Hong Y.K., Tsai M.J., Tsai S.Y. Direct transcriptional regulation of neuropilin-2 by COUP-TFII modulates multiple steps in murine lymphatic vessel development. J Clin Invest 2010, 120:1694-1707.
10. Yamazaki T., Yoshimatsu Y., Morishita Y., Miyazono K., Watabe T. COUP-TFII regulates the functions of Prox1 in lymphatic endothelial cells through direct interaction. Genes Cells 2009, 14:425-434.
11. Qin J., Tsai M.J., Tsai S.Y. Essential roles of COUP-TFII in Leydig cell differentiation and male fertility. PLoS One 2008, 3:e3285.
12. Petit F.G., Jamin S.P., Kurihara I., et al. Deletion of the orphan nuclear receptor COUP-TFII in uterus leads to placental deficiency. Proc Natl Acad Sci U S A 2007, 104:6293-6298.
13. Li L., Xie X., Qin J., et al. The nuclear orphan receptor COUP-TFII plays an essential role in adipogenesis, glucose homeostasis, and energy metabolism. Cell Metab 2009, 9:77-87.
14. Okamura M., Kudo H., Wakabayashi K., et al. COUP-TFII acts downstream of Wnt/beta-catenin signal to silence PPARgamma gene expression and repress adipogenesis. Proc Natl Acad Sci U S A 2009, 106:5819-5824.
15. Xu Z., Yu S., Hsu C.H., Eguchi J., Rosen E.D. The orphan nuclear receptor chicken ovalbumin upstream promoter-transcription factor II is a critical regulator of adipogenesis. Proc Natl Acad Sci U S A 2008, 105:2421-2426.
16. Kim B.J., Takamoto N., Yan J., Tsai S.Y., Tsai M.J. Chicken Ovalbumin Upstream Promoter-Transcription Factor II (COUP-TFII) regulates growth and patterning of the postnatal mouse cerebellum. Dev Biol 2009, 326:378-391.
17. Satoh S., Tang K., Iida A., et al. The spatial patterning of mouse cone opsin expression is regulated by bone morphogenetic protein signaling through downstream effector COUP-TF nuclear receptors. J Neurosci 2009, 29:12401-12411.
18. Tang K., Xie X., Park J.I., Jamrich M., Tsai S., Tsai M.J. COUP-TFs regulate eye development by controlling factors essential for optic vesicle morphogenesis. Development 2010, 137:725-734.
19. Warnecke M., Oster H., Revelli J.P., Alvarez-Bolado G., Eichele G. Abnormal development of the locus coeruleus in Ear2(Nr2f6)-deficient mice impairs the functionality of the forebrain clock and affects nociception. Genes Dev 2005, 19:614-625.
20. Hermann-Kleiter N., Gruber T., Lutz-Nicoladoni C., et al. The nuclear orphan receptor NR2F6 suppresses lymphocyte activation and T helper 17-dependent autoimmunity. Immunity 2008, 29:205-216.
21. Zhu X.G., Park K.S., Kaneshige M., et al. The orphan nuclear receptor Ear-2 is a negative coregulator for thyroid hormone nuclear receptor function. Mol Cell Biol 2000, 20:2604-2618.
22. Ivanov I.I., Zhou L., Littman D.R. Transcriptional regulation of Th17 cell differentiation. Semin Immunol 2007, 19:409-417.
23. Ichim C.V., Wells R.A. Generation of high-titer viral preparations by concentration using successive rounds of ultracentrifugation. J Transl Med 2011, 9:137.
24. Schmitt T.M., Zúñiga-Pflücker J.C. Induction of T cell development from hematopoietic progenitor cells by delta-like-1 invitro. Immunity 2002, 17:749-756.
25. Holmes R., Zuniga-Pflucker J.C. The OP9-DL1 system: generation of T-lymphocytes from embryonic or hematopoietic stem cells invitro. Cold Spring Harb Protoc 2009, 2009. pdb prot5156.
26. Yun T.J., Bevan M.J. Notch-regulated ankyrin-repeat protein inhibits Notch1 signaling: multiple Notch1 signaling pathways involved in T cell development. J Immunol 2003, 170:5834-5841.
27. Lamar E., Deblandre G., Wettstein D., et al. Nrarp is a novel intracellular component of the Notch signaling pathway. Genes Dev 2001, 15:1885-1899.
28. Germar K., Dose M., Konstantinou T., et al. T-cell factor 1 is a gatekeeper for T-cell specification in response to Notch signaling. Proc Natl Acad Sci U S A 2011, 108:20060-20065.
29. Schilham M.W., Wilson A., Moerer P., Benaissa-Trouw B.J., Cumano A., Clevers H.C. Critical involvement of Tcf-1 in expansion of thymocytes. J Immunol 1998, 161:3984-3991.
30. Chu Q., Liu L., Wang W. Overexpression of hCLP46 enhances Notch activation and regulates cell proliferation in a cell type-dependent manner. Cell proliferation 2013, 46:254-262.
31. Xiao X., Ning L., Chen H. Notch1 mediates growth suppression of papillary and follicular thyroid cancer cells by histone deacetylase inhibitors. Mol Cancer Ther 2009, 8:350-356.
32. Talora C., Sgroi D.C., Crum C.P., Dotto G.P. Specific down-modulation of Notch1 signaling in cervical cancer cells is required for sustained HPV-E6/E7 expression and late steps of malignant transformation. Genes Dev 2002, 16:2252-2263.
33. Qi R., An H., Yu Y., et al. Notch1 signaling inhibits growth of human hepatocellular carcinoma through induction of cell cycle arrest and apoptosis. Cancer Res 2003, 63:8323-8329.
34. Yucel R., Karsunky H., Klein-Hitpass L., Moroy T. The transcriptional repressor Gfi1 affects development of early, uncommitted c-Kit+ T cell progenitors and CD4/CD8 lineage decision in the thymus. J Exp Med 2003, 197:831-844.
35. Izon D.J., Rozenfeld S., Fong S.T., Komuves L., Largman C., Lawrence H.J. Loss of function of the homeobox gene Hoxa-9 perturbs early T-cell development and induces apoptosis in primitive thymocytes. Blood 1998, 92:383-393.
36. Lawrence H.J., Helgason C.D., Sauvageau G., et al. Mice bearing a targeted interruption of the homeobox gene HOXA9 have defects in myeloid, erythroid, and lymphoid hematopoiesis. Blood 1997, 89:1922-1930.
37. Nagel S., Venturini L., Marquez V.E., et al. Polycomb repressor complex 2 regulates HOXA9 and HOXA10, activating ID2 in NK/T-cell lines. Molecular cancer 2010, 9:151.
38. Min I.M., Pietramaggiori G., Kim F.S., Passegue E., Stevenson K.E., Wagers A.J. The transcription factor EGR1 controls both the proliferation and localization of hematopoietic stem cells. Cell Stem Cell 2008, 2:380-391.
39. Sun Z., Unutmaz D., Zou Y.R., et al. Requirement for RORgamma in thymocyte survival and lymphoid organ development. Science 2000, 288:2369-2373.
40. Guo J., Hawwari A., Li H., et al. Regulation of the TCRalpha repertoire by the survival window of CD4(+)CD8(+) thymocytes. Nat Immunol 2002, 3:469-476.
41. Albu D.I., Feng D., Bhattacharya D., et al. BCL11B is required for positive selection and survival of double-positive thymocytes. J Exp Med 2007, 204:3003-3015.
42. Ladias J.A. Convergence of multiple nuclear receptor signaling pathways onto the long terminal repeat of human immunodeficiency virus-1. J Biol Chem 1994, 269:5944-5951.
43. Ahn M.Y., Huang G., Bae S.C., Wee H.J., Kim W.Y., Ito Y. Negative regulation of granulocytic differentiation in the myeloid precursor cell line 32Dcl3 by ear-2, a mammalian homolog of Drosophila seven-up, and a chimeric leukemogenic gene, AML1/ETO. Proc Natl Acad Sci U S A 1998, 95:1812-1817.
44. Kurebayashi S., Ueda E., Sakaue M., et al. Retinoid-related orphan receptor gamma (RORgamma) is essential for lymphoid organogenesis and controls apoptosis during thymopoiesis. Proc Natl Acad Sci U S A 2000, 97:10132-10137.
45. Dzhagalov I., Giguere V., He Y.W. Lymphocyte development and function in the absence of retinoic acid-related orphan receptor alpha. J Immunol 2004, 173:2952-2959.
46. Trenkner E., Hoffmann M.K. Defective development of the thymus and immunological abnormalities in the neurological mouse mutation "staggerer". J Neurosci 1986, 6:1733-1737.
47. Ivanov I.I., McKenzie B.S., Zhou L., et al. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006, 126:1121-1133.
48. Klemsz M.J., McKercher S.R., Celada A., Van Beveren C., Maki R.A. The macrophage and B cell-specific transcription factor PU.1 is related to the ets oncogene. Cell 1990, 61:113-124.
49. Anderson M.K., Weiss A.H., Hernandez-Hoyos G., Dionne C.J., Rothenberg E.V. Constitutive expression of PU.1 in fetal hematopoietic progenitors blocks T cell development at the pro-T cell stage. Immunity 2002, 16:285-296.
50. Spain L.M., Guerriero A., Kunjibettu S., Scott E.W. T cell development in PU.1-deficient mice. J Immunol 1999, 163:2681-2687.
51. Scott E.W., Simon M.C., Anastasi J., Singh H. Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science 1994, 265:1573-1577.
52. Morrow M.A., Mayer E.W., Perez C.A., Adlam M., Siu G. Overexpression of the Helix-Loop-Helix protein Id2 blocks T cell development at multiple stages. Mol Immunol 1999, 36:491-503.