Allosteric Remodelling of the Histone H3 Binding Pocket in the Pygo2 PHD Finger Triggered by Its Binding to the B9L/BCL9 Co-Factor

Journal of Molecular Biology

Volumn 401, Issue 5, 2010, Pages 969-984

  Miller, Thomas C R ^a   Rutherford, Trevor J ^a   Johnson, Christopher M ^a   Fiedler, Marc ^a   Bienz, Mariann ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Allosteric modulation; B9L BCL9; Methylated histone H3 tail; PHD signature residue; Pygo

Indexed keywords

BETA CATENIN; HISTONE H3; LEUCINE; LIOTHYRONINE; PROTEIN; PYGOPUS PROTEIN; THREONINE; TRYPTOPHAN; UNCLASSIFIED DRUG;

ALLOSTERISM; ARTICLE; BINDING AFFINITY; CRYSTAL STRUCTURE; HUMAN; METHYLATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PARALOGY; PRIORITY JOURNAL; SURFACE PROPERTY;

PYGOPUS;

EID: 77955557074     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.07.007     Document Type: Article

References (49)

1. Clevers H. Wnt/β-catenin signaling in development and disease. Cell 2006, 127:469-480.
2. Klaus A., Birchmeier W. Wnt signalling and its impact on development and cancer. Nat. Rev. Cancer 2008, 8:387-398.
3. Bienz M., Clevers H. Linking colorectal cancer to Wnt signaling. Cell 2000, 103:311-320.
4. Polakis P. The many ways of Wnt in cancer. Curr. Opin. Genet. Dev. 2007, 17:45-51.
5. Mosimann C., Hausmann G., Basler K. β-Catenin hits chromatin: regulation of Wnt target gene activation. Nat. Rev. Mol. Cell Biol. 2009, 10:276-286.
6. Belenkaya T.Y., Han C., Standley H.J., Lin X., Houston D.W., Heasman J. Pygopus encodes a nuclear protein essential for wingless/Wnt signaling. Development 2002, 129:4089-4101.
7. Kramps T., Peter O., Brunner E., Nellen D., Froesch B., Chatterjee S., et al. Wnt/wingless signaling requires BCL9/Legless-mediated recruitment of pygopus to the nuclear β-catenin-TCF complex. Cell 2002, 109:47-60.
8. Parker D.S., Jemison J., Cadigan K.M. Pygopus, a nuclear PHD-finger protein required for Wingless signaling in Drosophila. Development 2002, 129:2565-2576.
9. Thompson B., Townsley F., Rosin-Arbesfeld R., Musisi H., Bienz M. A new nuclear component of the Wnt signalling pathway. Nat. Cell Biol. 2002, 4:367-373.
10. Stadeli R., Basler K. Dissecting nuclear Wingless signalling: recruitment of the transcriptional co-activator Pygopus by a chain of adaptor proteins. Mech. Dev. 2005, 122:1171-1182.
11. de la Roche M., Bienz M. Wingless-independent association of Pygopus with dTCF target genes. Curr. Biol. 2007, 17:556-561.
12. Townsley F.M., Cliffe A., Bienz M. Pygopus and Legless target Armadillo/β-catenin to the nucleus to enable its transcriptional co-activator function. Nat. Cell Biol. 2004, 6:626-633.
13. Fiedler M., Sanchez-Barrena M.J., Nekrasov M., Mieszczanek J., Rybin V., Muller J., et al. Decoding of methylated histone H3 tail by the Pygo-BCL9 Wnt signaling complex. Mol. Cell 2008, 30:507-518.
14. Gu B., Sun P., Yuan Y., Moraes R.C., Li A., Teng A., et al. Pygo2 expands mammary progenitor cells by facilitating histone H3 K4 methylation. J. Cell Biol. 2009, 185:811-826.
15. Pena P.V., Davrazou F., Shi X., Walter K.L., Verkhusha V.V., Gozani O., et al. Molecular mechanism of histone H3K4me3 recognition by plant homeodomain of ING2. Nature 2006, 442:100-103.
16. Shi X., Hong T., Walter K.L., Ewalt M., Michishita E., Hung T., et al. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 2006, 442:96-99.
17. Taverna S.D., Li H., Ruthenburg A.J., Allis C.D., Patel D.J. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat. Struct. Mol. Biol. 2007, 14:1025-1040.
18. Adachi S., Jigami T., Yasui T., Nakano T., Ohwada S., Omori Y., et al. Role of a BCL9-related β-catenin-binding protein, B9L, in tumorigenesis induced by aberrant activation of Wnt signaling. Cancer Res. 2004, 64:8496-8501.
19. Brembeck F.H., Schwarz-Romond T., Bakkers J., Wilhelm S., Hammerschmidt M., Birchmeier W. Essential role of BCL9-2 in the switch between β-catenin's adhesive and transcriptional functions. Genes Dev. 2004, 18:2225-2230.
20. de la Roche M., Worm J., Bienz M. The function of BCL9 in Wnt/β-catenin signaling and colorectal cancer cells. BMC Cancer 2008, 8:199.
21. Andrews P.G., Lake B.B., Popadiuk C., Kao K.R. Requirement of Pygopus 2 in breast cancer. Int. J. Oncol. 2007, 30:357-363.
22. Popadiuk C.M., Xiong J., Wells M.G., Andrews P.G., Dankwa K., Hirasawa K., et al. Antisense suppression of pygopus 2 results in growth arrest of epithelial ovarian cancer. Clin. Cancer Res. 2006, 12:2216-2223.
23. Wang, Z. X., Chen, Y. Y., Li, B. A., Tan, G. W., Liu, X. Y., Shen, S. H., et al. Decreased pygopus 2 expression suppresses glioblastoma U251 cell growth. J. Neuro-Oncol. in press [E-publication ahead of print].
24. Mani M., Carrasco D.E., Zhang Y., Takada K., Gatt M.E., Dutta-Simmons J., et al. BCL9 promotes tumor progression by conferring enhanced proliferative, metastatic, and angiogenic properties to cancer cells. Cancer Res. 2009, 69:7577-7586.
25. Li B., Rheaume C., Teng A., Bilanchone V., Munguia J.E., Hu M., et al. Developmental phenotypes and reduced Wnt signaling in mice deficient for pygopus 2. Genesis 2007, 45:318-325.
26. Schwab K.R., Patterson L.T., Hartman H.A., Song N., Lang R.A., Lin X., Potter S.S. Pygo1 and Pygo2 roles in Wnt signaling in mammalian kidney development. BMC Biol. 2007, 5:15.
27. Brack A.S., Murphy-Seiler F., Hanifi J., Deka J., Eyckerman S., Keller C., et al. BCL9 is an essential component of canonical Wnt signaling that mediates the differentiation of myogenic progenitors during muscle regeneration. Dev. Biol. 2009, 335:93-105.
28. Nair M., Nagamori I., Sun P., Mishra D.P., Rheaume C., Li B., et al. Nuclear regulator Pygo2 controls spermiogenesis and histone H3 acetylation. Dev. Biol. 2008, 320:446-455.
29. Song N., Schwab K.R., Patterson L.T., Yamaguchi T., Lin X., Potter S.S., Lang R.A. Pygopus 2 has a crucial, Wnt pathway-independent function in lens induction. Development 2007, 134:1873-1885.
30. Sustmann C., Flach H., Ebert H., Eastman Q., Grosschedl R. Cell-type-specific function of BCL9 involves a transcriptional activation domain that synergizes with β-catenin. Mol. Cell. Biol. 2008, 28:3526-3537.
31. Li H., Fischle W., Wang W., Duncan E.M., Liang L., Murakami-Ishibe S., et al. Structural basis for lower lysine methylation state-specific readout by MBT repeats of L3MBTL1 and an engineered PHD finger. Mol. Cell 2007, 28:677-691.
32. Wysocka J., Swigut T., Xiao H., Milne T.A., Kwon S.Y., Landry J., et al. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 2006, 442:86-90.
33. Aasland R., Gibson T.J., Stewart A.F. The PHD finger: implications for chromatin-mediated transcriptional regulation. Trends Biochem. Sci. 1995, 20:56-59.
34. Bienz M. The PHD finger, a nuclear protein-interaction domain. Trends Biochem. Sci. 2006, 31:35-40.
35. Pascual J., Martinez-Yamout M., Dyson H.J., Wright P.E. Structure of the PHD zinc finger from human Williams-Beuren syndrome transcription factor. J. Mol. Biol. 2000, 304:723-729.
36. Capili A.D., Schultz D.C., Rauscher I.F., Borden K.L. Solution structure of the PHD domain from the KAP-1 corepressor: structural determinants for PHD, RING and LIM zinc-binding domains. EMBO J. 2001, 20:165-177.
37. Townsley F.M., Thompson B., Bienz M. Pygopus residues required for its binding to Legless are critical for transcription and development. J. Biol. Chem. 2004, 279:5177-5183.
38. Hajduk P.J., Dinges J., Miknis G.F., Merlock M., Middleton T., Kempf D.J., et al. NMR-based discovery of lead inhibitors that block DNA binding of the human papillomavirus E2 protein. J. Med. Chem. 1997, 40:3144-3150.
39. Lee E., Salic A., Kruger R., Heinrich R., Kirschner M.W. The roles of APC and Axin derived from experimental and theoretical analysis of the Wnt pathway. PLoS Biol. 2003, 1:E10.
40. Meyer B.J. Targeting X chromosomes for repression. Curr. Opin. Genet. Dev. 2010, 20:179-189.
41. Stock D., Perisic O., Löwe J. Robotic nanolitre protein crystallisation at the MRC Laboratory of Molecular Biology. Prog. Biophys. Mol. Biol. 2005, 88:311-327.
42. McCoy A.J., Grosse-Kunstleve R.W., Storoni L.C., Read R.J. Likelihood-enhanced fast translation functions. Acta Crystallogr. Sect. D 2005, 61:458-464.
43. Leslie A.G. The integration of macromolecular diffraction data. Acta Crystallogr. Sect. D 2006, 62:48-57.
44. Evans P. Scaling and assessment of data quality. Acta Crystallogr. Sect. D 2006, 62:72-82.
45. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. Sect. D 1997, 53:240-255.
46. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. Sect. D 2004, 60:2126-2132.
47. Potterton E., Briggs P., Turkenburg M., Dodson E. A graphical user interface to the CCP4 program suite. Acta Crystallogr. Sect. D 2003, 59:1131-1137.
48. Davis I.W., Leaver-Fay A., Chen V.B., Block J.N., Kapral G.J., Wang X., et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 2007, 35:W375-W383.
49. Mori S., Abeygunawardana C., Johnson M.O., van Zijl P.C. Improved sensitivity of HSQC spectra of exchanging protons at short interscan delays using a new fast HSQC (FHSQC) detection scheme that avoids water saturation. J. Magn. Reson. Ser. B 1995, 108:94-98.