Molecular functions of the TLE tetramerization domain in Wnt target gene repression

EMBO Journal

Volumn 33, Issue 7, 2014, Pages 719-731

  Chodaparambil, Jayanth V ^a   Pate, Kira T ^b   Hepler, Margretta R D ^c   Tsai, Becky P ^b   Muthurajan, Uma M ^c   Luger, Karolin ^c   Waterman, Marian L ^b   Weis, William I ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

chromatin; TCF LEF; TLE groucho; Wnt signaling

Indexed keywords

BETA CATENIN; FLUORESCENT DYE; HISTONE H4; TETRAMER; TRANSDUCIN; TRANSDUCIN LIKE ENHANCER OF SPLIT; UNCLASSIFIED DRUG; WNT PROTEIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CHROMATIN; HISTONE; PROTEIN BINDING; REPRESSOR PROTEIN; T CELL FACTOR PROTEIN; TCF3 PROTEIN, HUMAN; TLE1 PROTEIN, HUMAN;

ANISOTROPY; ARTICLE; BINDING AFFINITY; CHROMATIN; GENE REPRESSION; GENE TARGETING; IN VIVO STUDY; MOLECULAR DYNAMICS; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; WNT SIGNALING PATHWAY; ANIMAL; AUDIOVISUAL EQUIPMENT; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; CRYSTALLOGRAPHY; GENE EXPRESSION REGULATION; HUMAN; METABOLISM; METHYLATION; MOUSE; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BETA CATENIN; CELL LINE; CERCOPITHECUS AETHIOPS; CHROMATIN; COS CELLS; CRYSTALLOGRAPHY; GENE EXPRESSION REGULATION; HISTONES; HUMANS; METHYLATION; MICE; MODELS, MOLECULAR; MODELS, STRUCTURAL; MUTATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TCF TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; WNT PROTEINS;

EID: 84898606032     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1002/embj.201387188     Document Type: Article

References (69)

1. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH, (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221
2. Arce L, Pate KT, Waterman ML, (2009) Groucho binds two conserved regions of LEF-1 for HDAC-dependent repression. BMC Cancer 9: 159
3. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA, (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci USA 98: 10037-10041 (Pubitemid 32802969)
4. Barbera AJ, Chodaparambil JV, Kelley-Clarke B, Joukov V, Walter JC, Luger K, Kaye KM, (2006) The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA. Science 311: 856-861 (Pubitemid 43228851)
5. Beagle B, Johnson GV, (2010) AES/GRG5: more than just a dominant-negative TLE/GRG family member. Dev Dyn 239: 2795-2805
6. Berger SL, (2007) The complex language of chromatin regulation during transcription. Nature 447: 407-412 (Pubitemid 46816746)
7. Billin AN, Thirlwell H, Ayer DE, (2000) β-Catenin-histone deacetylase interactions regulate the transition of LEF1 from a transcriptional repressor to an activator. Mol Cell Biol 20: 6882-6890
8. Brantjes H, Roose J, van de Wetering M, Clevers H, (2001) All Tcf HMG box transcription factors interact with Groucho-related co-repressors. Nucleic Acids Res 29: 1410-1419 (Pubitemid 32288486)
9. Buscarlet M, Stifani S, (2007) The 'Marx' of Groucho on development and disease. Trends Cell Biol 17: 353-361 (Pubitemid 47102197)
10. Cadigan KM, Waterman ML, (2012) TCF/LEFs and Wnt signaling in the nucleus. Cold Spring Harb Perspect Biol, 4: a007906.
11. Chen G, Fernandez J, Mische S, Courey AJ, (1999) A functional interaction between the histone deacetylase Rpd3 and the corepressor groucho in Drosophila development. Genes Dev 13: 2218-2230 (Pubitemid 29426727)
12. Chen G, Nguyen PH, Courey AJ, (1998) A role for Groucho tetramerization in transcriptional repression. Mol Cell Biol 18: 7259-7268 (Pubitemid 28533045)
13. Chen VB, Arendall WB, Headd JJ, Keed DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC, (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D66: 12-21
14. Chodaparambil JV, Barbera AJ, Lu X, Kaye KM, Hansen JC, Luger K, (2007) A charged and contoured surface on the nucleosome regulates chromatin compaction. Nat Struct Mol Biol 14: 1105-1107 (Pubitemid 350060342)
15. Choi CY, Kim YH, Kim YO, Park SJ, Kim EA, Riemenschneider W, Gajewski K, Schulz RA, Kim Y, (2005) Phosphorylation by the DHIPK2 protein kinase modulates the corepressor activity of Groucho. J Biol Chem 280: 21427-21436 (Pubitemid 40805707)
16. Cowtan K, (2006) The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr D Biol Crystallogr 62: 1002-1011 (Pubitemid 44337374)
17. Daniels DL, Weis WI, (2005) β-catenin directly displaces Groucho/TLE repressors from Tcf/Lef in Wnt-mediated transcription activation. Nat Struct Mol Biol 12: 364-371 (Pubitemid 43093092)
18. Dorigo B, Schalch T, Bystricky K, Richmond TJ, (2003) Chromatin fiber folding: requirement for the histone H4 N-terminal tail. J Mol Biol 327: 85-96 (Pubitemid 36293304)
19. Fasolini M, Wu X, Flocco M, Trosset JY, Oppermann U, Knapp S, (2003) Hot spots in Tcf4 for the interaction with β-catenin. J Biol Chem 278: 21092-21098 (Pubitemid 36806421)
20. Fiedler M, Sanchez-Barrena MJ, Nekrasov M, Mieszczanek J, Rybin V, Muller J, Evans P, Bienz M, (2008) Decoding of methylated histone H3 tail by the Pygo-BCL9 Wnt signaling complex. Mol Cell 30: 507-518 (Pubitemid 351672372)
21. Fisher AL, Ohsako S, Caudy M, (1996) The WRPW motif of the hairy-related basic helix-loop-helix repressor proteins acts as a 4-amino-acid transcription repression and protein-protein interaction domain. Mol Cell Biol 16: 2670-2677 (Pubitemid 26161270)
22. Flores-Saaib RD, Courey AJ, (2000) Analysis of Groucho-histone interactions suggests mechanistic similarities between Groucho- and Tup1-mediated repression. Nucleic Acids Res 28: 4189-4196
23. Gu B, Sun P, Yuan Y, Moraes RC, Li A, Teng A, Agrawal A, Rheaume C, Bilanchone V, Veltmaat JM, Takemaru K, Millar S, Lee EY, Lewis MT, Li B, Dai X, (2009) Pygo2 expands mammary progenitor cells by facilitating histone H3 K4 methylation. J Cell Biol 185: 811-826
24. Hanson AJ, Wallace HA, Freeman TJ, Beauchamp RD, Lee LA, Lee E, (2012) XIAP monoubiquitylates Groucho/TLE to promote canonical Wnt signaling. Mol Cell 45: 619-628
25. Hasson P, Egoz N, Winkler C, Volohonsky G, Jia S, Dinur T, Volk T, Courey AJ, Paroush Z, (2005) EGFR signaling attenuates Groucho-dependent repression to antagonize Notch transcriptional output. Nat Genet 37: 101-105 (Pubitemid 40070947)
26. Hasson P, Paroush Z, (2007) Crosstalk between the EGFR and other signalling pathways at the level of the global transcriptional corepressor Groucho/TLE. Br J Cancer 96 (Suppl): R21-R25
27. Hecht A, Vleminckx K, Stemmler MP, van Roy F, Kemler R, (2000) The p300/CBP acetyltransferases function as transcriptional coactivators of β-catenin in vertebrates. EMBO J 19: 1839-1850 (Pubitemid 30204395)
28. Hieb AR, D'Arcy S, Kramer MA, White AE, Luger K, (2012) Fluorescence strategies for high-throughput quantification of protein interactions. Nucleic Acids Res 40: e33
29. Hikasa H, Ezan J, Itoh K, Li X, Klymkowsky MW, Sokol SY, (2010) Regulation of TCF3 by Wnt-dependent phosphorylation during vertebrate axis specification. Dev Cell 19: 521-532
30. Hikasa H, Sokol SY, (2011) Phosphorylation of TCF proteins by homeodomain-interacting protein kinase 2. J Biol Chem 286: 12093-12100
31. Jessen S, Gu B, Dai X, (2008) Pygopus and the Wnt signaling pathway: a diverse set of connections. BioEssays 30: 448-456 (Pubitemid 351588926)
32. Jimenez G, Paroush Z, Ish-Horowicz D, (1997) Groucho acts as a corepressor for a subset of negative regulators, including Hairy and Engrailed. Genes Dev 11: 3072-3082 (Pubitemid 27508516)
33. Kabsch W, (2010) Integration, scaling, space-group assignment and post-refinement. Acta Crystallogr D Biol Crystallogr 66: 133-144
34. Kim CH, Oda T, Itoh M, Jiang D, Artinger KB, Chandrasekharappa SC, Driever W, Chitnis AB, (2000) Repressor activity of Headless/Tcf3 is essential for vertebrate head formation. Nature 407: 913-916
35. Knapp S, Zamai M, Volpi D, Nardese V, Avanzi N, Breton J, Plyte S, Flocco M, Marconi M, Isacchi A, Caiolfa VR, (2001) Thermodynamics of the high-affinity interaction of TCF4 with β-catenin. J Mol Biol 306: 1179-1189 (Pubitemid 33030013)
36. Konarev PV, Volkov VV, Sokolova AV, Koch MHJ, Svergun DI, (2003) PRIMUS: a windows PC-based system for small-angel scattering data analysis. J Appl Crystallogr 36: 1277-1282
37. Korinek V, Barker N, Willert K, Molenaar M, Roose J, Wagenaar G, Markman M, Lamers W, Destree O, Clevers H, (1998) Two members of the Tcf family implicated in Wnt/beta-catenin signaling during embryogenesis in the mouse. Mol Cell Biol 18: 1248-1256 (Pubitemid 28100888)
38. Kuo D, Nie M, De Hoff P, Chambers M, Phillips M, Hirsch AM, Courey AJ, (2011) A SUMO-Groucho Q domain fusion protein: characterization and in vivo Ulp1-mediated cleavage. Protein Expr Purif 76: 65-71
39. Laskowski RA, MacArthur MW, Moss DS, Thornton JM, (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26: 283-291
40. Lee W, Swarup S, Chen J, Ishitani T, Verheyen EM, (2009) Homeodomain-interacting protein kinases (Hipks) promote Wnt/Wg signaling through stabilization of beta-catenin/Arm and stimulation of target gene expression. Development 136: 241-251
41. Liu F, van den Broek O, Destree O, Hoppler S, (2005) Distinct roles for Xenopus Tcf/Lef genes in mediating specific responses to Wnt/β-catenin signalling in mesoderm development. Development 132: 5375-5385 (Pubitemid 43125866)
42. Logan CY, Nusse R, (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20: 781-810 (Pubitemid 39488658)
43. Merrill BJ, Pasolli HA, Polak L, Rendl M, Garcia-Garcia MJ, Anderson KV, Fuchs E, (2004) Tcf3: a transcriptional regulator of axis induction in the early embryo. Development 131: 263-274 (Pubitemid 38181367)
44. Nguyen H, Merrill BJ, Polak L, Nikolova M, Rendl M, Shaver TM, Pasolli HA, Fuchs E, (2009) Tcf3 and Tcf4 are essential for long-term homeostasis of skin epithelia. Nat Genet 41: 1068-1075
45. Nuthall HN, Joachim K, Palaparti A, Stifani S, (2002) A role for cell cycle-regulated phosphorylation in Groucho-mediated transcriptional repression. J Biol Chem 277: 51049-51057 (Pubitemid 36042277)
46. Palaparti A, Baratz A, Stifani S, (1997) The Groucho/transducin-like enhancer of split transcriptional repressors interact with the genetically defined amino-terminal silencing domain of histone H3. J Biol Chem 272: 26604-26610 (Pubitemid 27458883)
47. Patel SR, Bhumbra SS, Paknikar RS, Dressler GR, (2012) Epigenetic mechanisms of Groucho/Grg/TLE mediated transcriptional repression. Mol Cell 45: 185-195
48. Pereira L, Yi F, Merrill BJ, (2006) Repression of Nanog Gene Transcription by Tcf3 Limits Embryonic Stem Cell Self-Renewal. Mol Cell Biol, 26: 7479-7491 (Pubitemid 44547699)
49. Polakis P, (2007) The many ways of Wnt in cancer. Curr Opin Genet Dev 17: 45-51 (Pubitemid 46109296)
50. Roose J, Huls G, van Beest M, Moerer P, van der Horn K, Goldschmeding R, Logtenberg T, Clevers H, (1999) Synergy between tumor suppressor APC and the beta-catenin-Tcf4 target Tcf1. Science 285: 1923-1926
51. Schiltz M, Bricogne G, (2007) Modelling and refining site-specific radiation damage in SAD/MAD phasing. J Synchrotron Radiat 14: 34-42 (Pubitemid 46058904)
52. Sekiya T, Zaret KS, (2007) Repression by Groucho/TLE/Grg proteins: genomic site recruitment generates compacted chromatin in vitro and impairs activator binding in vivo. Mol Cell 28: 291-303 (Pubitemid 47600002)
53. Semenyuk AV, Svergun DI, (1991) GNOM-a program package for small-angle scattering data processing. J Appl Crystallogr 24: 537-540
54. Sierra J, Yoshida T, Joazeiro CA, Jones KA, (2006) The APC tumor suppressor counteracts β-catenin activation and H3K4 methylation at Wnt target genes. Genes Dev 20: 586-600 (Pubitemid 43345324)
55. Song H, Hasson P, Paroush Z, Courey AJ, (2004) Groucho oligomerization is required for repression in vivo. Mol Cell Biol 24: 4341-4350 (Pubitemid 41071004)
56. Standley HJ, Destree O, Kofron M, Wylie C, Heasman J, (2006) Maternal XTcf1 and XTcf4 have distinct roles in regulating Wnt target genes. Dev Biol 289: 318-328 (Pubitemid 43049935)
57. Suganuma T, Workman JL, (2011) Signals and combinatorial functions of histone modifications. Annu Rev Biochem 80: 473-499
58. Sun J, Weis WI, (2011) Biochemical and structural characterization of beta-catenin interactions with nonphosphorylated and CK2-phosphorylated Lef-1. J Mol Biol 405: 519-530
59. Svergun D, Barberato C, Koch MHJ, (1995) CRYSOL: a program to evaluate x-ray solution scattering of biological macromolecules from atomic coordinates. J Appl Crystallogr 28: 768-773 (Pubitemid 3014671)
60. Takemaru K, Moon RT, (2000) The transcriptional coactivator CBP interacts with β-catenin to activate gene expression. J Cell Biol 149: 249-254 (Pubitemid 30227143)
61. Tam WL, Lim CY, Han J, Zhang J, Ang YS, Ng HH, Yang H, Lim B, (2008) T-cell factor 3 regulates embryonic stem cell pluripotency and self-renewal by the transcriptional control of multiple lineage pathways. Stem Cells 26: 2019-2031
62. Tang W, Dodge M, Gundapaneni D, Michnoff C, Roth M, Lum L, (2008) A genome-wide RNAi screen for Wnt/beta-catenin pathway components identifies unexpected roles for TCF transcription factors in cancer. Proc Natl Acad Sci USA 105: 9697-9702 (Pubitemid 352031363)
63. Turki-Judeh W, Courey AJ, (2012) Groucho: a corepressor with instructive roles in development. Curr Top Dev Biol 98: 65-96
64. van de Wetering M, Cavallo R, Booijes D, van Beest M, van Es J, Loureiro J, Ypma A, Hursh D, Jones T, Bejsovec A, Peifer M, Mortin M, Clevers H, (1997) Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88: 789-799 (Pubitemid 27164267)
65. Winkler DD, Muthurajan UM, Hieb AR, Luger K, (2011) Histone chaperone FACT coordinates nucleosome interaction through multiple synergistic binding events. J Biol Chem 286: 41883-41892
66. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS, (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67: 235-242
67. Wu B, Piloto S, Zeng W, Hoverter NP, Schilling TF, Waterman ML, (2013) Ring Finger Protein 14 is a new regulator of TCF/beta-catenin-mediated transcription and colon cancer cell survival. EMBO Rep 14: 347-355
68. Yi F, Pereira L, Hoffman JA, Shy BR, Yuen CM, Liu DR, Merrill BJ, (2011) Opposing effects of Tcf3 and Tcf1 control Wnt stimulation of embryonic stem cell self-renewal. Nat Cell Biol 13: 762-770
69. Zhou J, Fan JY, Rangasamy D, Tremethick DJ, (2007) The nucleosome surface regulates chromatin compaction and couples it with transcriptional repression. Nat Struct Mol Biol 14: 1070-1076 (Pubitemid 350060339)