Structural basis for corepressor assembly by the orphan nuclear receptor TLX

Genes and Development

Volumn 29, Issue 4, 2015, Pages 440-450

  Zhi, Xiaoyong ^a,b   Zhou, X Edward ^a   He, Yuanzheng ^a   Searose Xu, Kelvin ^a   Zhang, Chun Li ^b   Tsai, Chih Cheng ^c   Melcher, Karsten ^a   Xu, H Eric ^a,d  

^a VAN ANDEL RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

Author keywords

COUP; PNR; SHP; TLX

Indexed keywords

ATRO BOX PEPTIDE; ATROPHIN; ORPHAN NUCLEAR RECEPTOR; ORPHAN NUCLEAR RECEPTOR TLX; PEPTIDE; PROTEIN; UNCLASSIFIED DRUG; CELL RECEPTOR; DROSOPHILA PROTEIN; NR2E1 PROTEIN, HUMAN;

ARTICLE; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME ACTIVITY; HUMAN; LIGAND BINDING; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REPRESSOR GENE; TRIBOLIUM CASTANEUM; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; DROSOPHILA MELANOGASTER; HEK293 CELL LINE; METABOLISM;

HEXAPODA;

ANIMALS; CRYSTALLIZATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HEK293 CELLS; HUMANS; MODELS, MOLECULAR; ORPHAN NUCLEAR RECEPTORS; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 84922985285     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.254904.114     Document Type: Article

References (61)

1. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, et al. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221.
2. Bailey S. 1994. The Ccp4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763
3. Bavner A, Johansson L, Toresson G, Gustafsson JA, Treuter E. 2002. A transcriptional inhibitor targeted by the atypical orphan nuclear receptor SHP. EMBO Rep 3: 478-484.
4. Benod C, Villagomez R, Filgueira CS, Hwang PK, Leonard PG, Poncet-Montange G, Rajagopalan S, Fletterick RJ, Gustafsson JA, Webb P. 2014. The human orphan nuclear receptor tailless (TLX, NR2E1) is druggable. PLoS ONE 9: e99440.
5. Boulias K, Talianidis I. 2004. Functional role of G9a-induced histone methylation in small heterodimer partner-mediated transcriptional repression. Nucleic Acids Res 32: 6096-6103
6. Brelivet Y, Rochel N, Moras D. 2012. Structural analysis of nuclear receptors: from isolated domains to integral proteins. Mol Cell Endocrinol 348: 466-473.
7. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, et al. 1998. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54: 905-921.
8. Davis SM, Thomas AL, Nomie KJ, Huang L, Dierick HA. 2014. Tailless and Atrophin control Drosophila aggression by regulating neuropeptide signalling in the pars intercerebralis. Nat Commun 5: 3177.
9. Di Maio F, Echols N, Headd JJ, Terwilliger TC, Adams PD, Baker A 2013. Improved low-resolution crystallographic refinement with Phenix and Rosetta. Nat Methods 10: 1102-1104.
10. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
11. Escher P, Gouras P, Roduit R, Tiab L, Bolay S, Delarive T, Chen SM, Tsai CC, Hayashi M, Zernant J, et al. 2009. Mutations in NR2E3 can cause dominant or recessive retinal degenerations in the same family. Hum Mutat 30: 342-351.
12. Evans RM, Mangelsdorf DJ. 2014. Nuclear receptors, RXR, and the big bang. Cell 157: 255-266.
13. Flaig R, Greschik H, Peluso-Iltis C, Moras D. 2005. Structural basis for the cell-specific activities of the NGFI-B and the Nurr1 ligand-binding domain. J Biol Chem 280: 19250-19258.
14. Gallastegui N, Mackinnon JA, Fletterick RJ, Estebanez-Perpina A 2015. Advances in our structural understanding of orphan nuclear receptors. Trends Biochem Sci 40: 25-35.
15. Gampe RT Jr, Montana VG, Lambert MH, Miller AB, Bledsoe RK, Milburn MV, Kliewer SA, Willson TM, Xu HE. 2000. Asymmetry in the PPARg/RXRa crystal structure reveals the molecular basis of heterodimerization among nuclear receptors. Mol Cell 5: 545-555.
16. Gui H, Li ML, Tsai CC. 2011. A tale of tailless. Dev Neurosci 33: 1-13.
17. Haecker A, Qi D, Lilja T, Moussian B, Andrioli LP, Luschnig S, Mannervik M. 2007. Drosophila brakeless interacts with atrophin and is required for tailless-mediated transcriptional repression in early embryos. PLoS Biol 5: e145.
18. Islam MM, Zhang CL. 2014. TLX: a master regulator for neural stem cell maintenance and neurogenesis. Biochim Biophys Acta 1849: 210-216.
19. Jones TA, Zou JY, Cowan SW, Kjeldgaard M. 1991. Improved methods for building protein models in electron-density maps and the location of errors in these models. Acta Crystallogr A 47: 110-119.
20. Kabsch W. 2010. XDS. Acta Crystallogr D Biol Crystallogr 66: 125-132.
21. Kruse SW, Suino-Powell K, Zhou XE, Kretschman JE, Reynolds R, Vonrhein C, Xu Y, Wang L, Tsai SY, Tsai MJ, et al. 2008. Identification of COUP-TFII orphan nuclear receptor as a retinoic acid-activated receptor. PLoS Biol 6: e227.
22. Lalli E, Bardoni B, Zazopoulos E, Wurtz JM, Strom TM, Moras D, Sassone-Corsi P. 1997. A transcriptional silencing domain in DAX-1 whose mutation causes adrenal hypoplasia congenita. Mol Endocrinol 11: 1950-1960.
23. Li Y, Choi M, Suino K, Kovach A, Daugherty J, Kliewer SA, Xu HE. 2005. Structural and biochemical basis for selective repression of the orphan nuclear receptor liver receptor homolog 1 by small heterodimer partner. Proc Natl Acad Sci 102: 9505-9510.
24. Liu HK, Belz T, Bock D, Takacs A, Wu H, Lichter P, Chai M, Schutz G. 2008. The nuclear receptor tailless is required for neurogenesis in the adult subventricular zone. Genes Dev 22: 2473-2478.
25. Liu HK, Wang Y, Belz T, Bock D, Takacs A, Radlwimmer B, Barbus S, Reifenberger G, Lichter P, Schutz G. 2010. The nuclear receptor tailless induces long-term neural stem cell expansion and brain tumor initiation. Genes Dev 24: 683-695.
26. Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schutz G, Umesono K, Blumberg B, Kastner P, Mark M, Chambon P, et al. 1995. The nuclear receptor superfamily: the second decade. Cell 83: 835-839.
27. Mullican SE, DiSpirito JR, Lazar MA. 2013. The orphan nuclear receptors at their 25-year reunion. J Mol Endocrinol 51: T115-T140.
28. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Macromol Crystallogr Pt A 276: 307-326.
29. Pankratz MJ, Hoch M, Seifert E, Jackle H. 1989. Kruppel requirement for knirps enhancement reflects overlapping gap gene activities in the Drosophila embryo. Nature 341:337-340.
30. Park HJ, Kim JK, Jeon HM, Oh SY, Kim SH, Park MJ, Soeda A, Nam DH, Kim H. 2010. The neural stem cell fate determinant TLX promotes tumorigenesis and genesis of cells resembling glioma stem cells. Mol Cells 30: 403-408.
31. Phelan CA, Gampe RT Jr, Lambert MH, Parks DJ, Montana V, Bynum J, Broderick TM, Hu X, Williams SP, Nolte RT, et al. 2010. Structure of Rev-erba bound to N-CoR reveals a unique mechanism of nuclear receptor-co-repressor interaction. Nat Struct Mol Biol 17: 808-814.
32. Pignoni F, Baldarelli RM, Steingrimsson E, Diaz RJ, Patapoutian A, Merriam JR, Lengyel JA. 1990. The Drosophila gene tailless is expressed at the embryonic termini and is a member of the steroid receptor superfamily. Cell 62: 151-163.
33. Sablin EP, Woods A, Krylova IN, Hwang P, Ingraham HA, Fletterick RJ. 2008. The structure of corepressor Dax-1 bound to its target nuclear receptor LRH-1. Proc Natl Acad Sci 105: 18390-18395.
34. Sanyal S, Bavner A, Haroniti A, Nilsson LM, Lundasen T, Rehnmark S, Witt MR, Einarsson C, Talianidis I, Gustafsson JA, et al. 2007. Involvement of corepressor complex subunit GPS2 in transcriptional pathways governing human bile acid biosynthesis. Proc Natl Acad Sci 104: 15665-15670.
35. Schroder GF, Levitt M, Brunger AT. 2010. Super-resolution biomolecular crystallography with low-resolution data. Nature 464: 1218-1222.
36. Shi Y, Chichung Lie D, Taupin P, Nakashima K, Ray J, Yu RT, Gage FH, Evans RM. 2004. Expression and function of orphan nuclear receptor TLX in adult neural stem cells. Nature 427: 78-83.
37. Steingrimsson E, Pignoni F, Liaw GJ, Lengyel JA. 1991. Dual role of the Drosophila pattern gene tailless in embryonic termini. Science 254: 418-421.
38. Sun G, Yu RT, Evans RM, Shi Y. 2007. Orphan nuclear receptor TLX recruits histone deacetylases to repress transcription and regulate neural stem cell proliferation. Proc Natl Acad Sci 104: 15282-15287.
39. Sun G, Alzayady K, Stewart R, Ye P, Yang S, Li W, Shi Y. 2010. Histone demethylase LSD1 regulates neural stem cell proliferation. Mol Cell Biol 30: 1997-2005.
40. Takezawa S, Yokoyama A, Okada M, Fujiki R, Iriyama A, Yasuo Y, Ito H, Takada I, Kishimoto M, Miyajima A, et al. 2007. A cell cycle-dependent co-repressor mediates photoreceptor cell-specific nuclear receptor function. EMBO J 26: 764-774.
41. Tan MH, Zhou XE, Soon FF, Li X, Li J, Yong EL, Melcher K, Xu HE. 2013. The crystal structure of the orphan nuclear receptor NR2E3/PNR ligand binding domain reveals a dimeric auto-repressed conformation. PLoS ONE 8: e74359.
42. Vilhais-Neto GC, Maruhashi M, Smith KT, Vasseur-Cognet M, Peterson AS, Workman JL, Pourquie O. 2010. Rere controls retinoic acid signalling and somite bilateral symmetry. Nature 463: 953-957.
43. Wang L, Tsai CC. 2008. Atrophin proteins: an overview of a new class of nuclear receptor corepressors. Nucl Recept Signal 6: e009.
44. Wang ZL, Benoit G, Liu JS, Prasad S, Aarnisalo P, Liu XH, Xu HD, Walker NPC, Perlmann T. 2003. Structure and function of Nurr1 identifies a class of ligand-independent nuclear receptors. Nature 423: 555-560.
45. Wang L, Rajan H, Pitman JL, McKeown M, Tsai CC. 2006. Histone deacetylase-associating Atrophin proteins are nuclear receptor corepressors. Genes Dev 20: 525-530.
46. Wang L, Charroux B, Kerridge S, Tsai CC. 2008. Atrophin recruits HDAC1/2 and G9a to modify histone H3K9 and to determine cell fates. EMBO Rep 9: 555-562.
47. Xie Q, Flavahan WA, Bao SD, Rich J. 2014. The tailless root of glioma: cancer stem cells. Cell Stem Cell 15: 114-116.
48. Xu HE, Lambert MH, Montana VG, Parks DJ, Blanchard SG, Brown PJ, Sternbach DD, Lehmann JM, Wisely GB, Willson TM, et al. 1999a. Molecular recognition of fatty acids by peroxisome proliferator-activated receptors. Mol Cell 3: 397-403.
49. Xu L, Glass CK, Rosenfeld MG. 1999b. Coactivator and corepressor complexes in nuclear receptor function. Curr Opin Genet Dev 9: 140-147.
50. Xu HE, Lambert MH, Montana VG, Plunket KD, Moore LB, Collins JB, Oplinger JA, Kliewer SA, Gampe RT, McKee DD, et al. 2001. Structural determinants of ligand binding selectivity between the peroxisome proliferator-activated receptors. Proc Natl Acad Sci 98: 13919-13924.
51. Xu HE, Stanley TB, Montana VG, Lambert MH, Shearer BG, Cobb JE, McKee DD, Galardi CM, Plunket KD, Nolte RT, et al. 2002. Structural basis for antagonist-mediated recruitment of nuclear co-repressors by PPARa. Nature 415: 813817.
52. Yokoyama A, Takezawa S, Schule R, Kitagawa H, Kato S. 2008. Transrepressive function of TLX requires the histone de-methylase LSD1. Mol Cell Biol 28: 3995-4003.
53. Younossi-Hartenstein A, Green P, Liaw GJ, Rudolph K, Lengyel J, Hartenstein V. 1997. Control of early neurogenesis of the Drosophila brain by the head gap genes tll, otd, ems, and btd. Dev Biol 182: 270-283.
54. Yu RT, Mckeown M, Evans RM, Umesono K. 1994. Relationship between Drosophila gap gene tailless and a vertebrate nuclear receptor Tlx. Nature 370: 375-379.
55. Zhang Y, Dufau ML. 2004. Gene silencing by nuclear orphan receptors. Vitam Horm 68: 1-48.
56. Zhang CL, Zou Y, Yu RT, Gage FH, Evans RM. 2006. Nuclear receptor TLX prevents retinal dystrophy and recruits the corepressor atrophin1. Genes Dev 20: 1308-1320.
57. Zhang CL, Zou Y, He W, Gage FH, Evans RM. 2008. A role for adult TLX-positive neural stem cells in learning and behaviour. Nature 451: 1004-1007.
58. Zhi X, Zhou XE, Melcher K, Motola DL, Gelmedin V, Hawdon J, Kliewer SA, Mangelsdorf DJ, Xu HE. 2012. Structural conservation of ligand binding reveals a bile acid-like signaling pathway in nematodes. J Biol Chem 287: 4894-4903.
59. Zhi X, Zhou XE, He Y, Zechner C, Suino-Powell KM, Kliewer SA, Melcher K, Mangelsdorf DJ, Xu HE. 2014. Structural insights into gene repression by the orphan nuclear receptor SHP. Proc Natl Acad Sci 111: 839-844.
60. Zhou XE, Suino-Powell KM, Xu Y, Chan CW, Tanabe O, Kruse SW, Reynolds R, Engel JD, Xu HE. 2011. The orphan nuclear receptor TR4 is a vitamin A-activated nuclear receptor. J Biol Chem 286: 2877-2885.
61. Zou Y, Niu W, Qin S, Downes M, Burns DK, Zhang CL. 2012. The nuclear receptor TLX is required for gliomagenesis within the adult neurogenic niche. Mol Cell Biol 32: 4811-4820