Structure and function of WD40 domain proteins

Protein and Cell

Volumn 2, Issue 3, 2011, Pages 202-214

  Xu, Chao ^a   Min, Jinrong ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Beta propeller; Post translational modification; Protein protein interaction; Scaffold; WD40

Indexed keywords

BINDING PROTEIN; CLATHRIN; F BOX PROTEIN; PROTEIN CUL1; PROTEIN RBX1; PROTEIN WD40; S PHASE KINASE ASSOCIATED PROTEIN; S PHASE KINASE ASSOCIATED PROTEIN 1; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; BETA SHEET; BINDING SITE; CELL CYCLE PROGRESSION; COMPLEX FORMATION; DNA MODIFICATION; DNA REPAIR; MOLECULAR DYNAMICS; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TARGETING; REVIEW; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; UBIQUITINATION;

EUKARYOTA;

EID: 79960068470     PISSN: 1674800X     EISSN: 16748018     Source Type: Journal    
DOI: 10.1007/s13238-011-1018-1     Document Type: Review

References (82)

1. Adams-Cioaba, M.A., Guo, Y., Bian, C., Amaya, M.F., Lam, R., Wasney, G.A., Vedadi, M., Xu, C., and Min, J. (2010). Structural studies of the tandem Tudor domains of fragile X mental retardation related proteins FXR1 and FXR2. PLoS One 5, e13559.
2. Adams-Cioaba, M.A., and Min, J. (2009). Structure and function of histone methylation binding proteins. Biochemistry and cell biology = Biochimie et biologie cellulaire 87, 93-105.
3. Andrade, M.A., Perez-Iratxeta, C., and Ponting, C.P. (2001). Protein repeats: structures, functions, and evolution. J Struct Biol 134, 117-131.
4. Ang, X.L., and Wade Harper, J. (2005). SCF-mediated protein degradation and cell cycle control. Oncogene 24, 2860-2870.
5. Angers, S., Li, T., Yi, X., MacCoss, M.J., Moon, R.T., and Zheng, N. (2006). Molecular architecture and assembly of the DDB1-CUL4A ubiquitin ligase machinery. Nature 443, 590-593.
6. Bergametti, F., Bianchi, J., and Transy, C. (2002). Interaction of hepatitis B virus X protein with damaged DNA-binding protein p127: structural analysis and identification of antagonists. J Biomed Sci 9, 706-715.
7. Brohawn, S.G., Partridge, J.R., Whittle, J.R., and Schwartz, T.U. (2009). The nuclear pore complex has entered the atomic age. Structure 17, 1156-1168.
8. Cao, R., Wang, L., Wang, H., Xia, L., Erdjument-Bromage, H., Tempst, P., Jones, R.S., and Zhang, Y. (2002). Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298, 1039-1043.
9. Cao, R., and Zhang, Y. (2004). The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr Opin Genet Dev 14, 155-164.
10. Cardozo, T., and Pagano, M. (2004). The SCF ubiquitin ligase: insights into a molecular machine. Nat Rev Mol Cell Biol 5, 739-751.
11. Chan, D.W., Wang, Y., Wu, M., Wong, J., Qin, J., and Zhao, Y. (2009). Unbiased proteomic screen for binding proteins to modified lysines on histone H3. Proteomics 9, 2343-2354.
12. Chen, X., Zhang, Y., Douglas, L., and Zhou, P. (2001). UV-damaged DNA-binding proteins are targets of CUL-4A-mediated ubiquitination and degradation. J Biol Chem 276, 48175-48182.
13. Couture, J.F., Collazo, E., and Trievel, R.C. (2006). Molecular recognition of histone H3 by the WD40 protein WDR5. Nat Struct Mol Biol 13, 698-703.
14. Czermin, B., Melfi, R., McCabe, D., Seitz, V., Imhof, A., and Pirrotta, V. (2002). Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111, 185-196.
15. English, C.M., Adkins, M.W., Carson, J.J., Churchill, M.E., and Tyler, J.K. (2006). Structural basis for the histone chaperone activity of Asf1. Cell 127, 495-508.
16. Eryilmaz, J., Pan, P., Amaya, M.F., Allali-Hassani, A., Dong, A., Adams-Cioaba, M.A., Mackenzie, F., Vedadi, M., and Min, J. (2009). Structural studies of a four-MBT repeat protein MBTD1. PLoS One 4, e7274.
17. Feng, Q., and Zhang, Y. (2003). The NuRD complex: linking histone modification to nucleosome remodeling. Curr Top Microbiol Immunol 274, 269-290.
18. Fong, H.K., Hurley, J.B., Hopkins, R.S., Miake-Lye, R., Johnson, M. S., Doolittle, R.F., and Simon, M.I. (1986). Repetitive segmental structure of the transducin beta subunit: homology with the CDC4 gene and identification of related mRNAs. Proc Natl Acad Sci U S A 83, 2162-2166.
19. Gao, Z., Huang, Z., Olivey, H.E., Gurbuxani, S., Crispino, J.D., and Svensson, E.C. (2010). FOG-1-mediated recruitment of NuRD is required for cell lineage re-enforcement during haematopoiesis. EMBO J 29, 457-468.
20. Gaudet, R., Bohm, A., and Sigler, P.B. (1996). Crystal structure at 2.4 angstroms resolution of the complex of transducin betagamma and its regulator, phosducin. Cell 87, 577-588.
21. Groisman, R., Polanowska, J., Kuraoka, I., Sawada, J., Saijo, M., Drapkin, R., Kisselev, A.F., Tanaka, K., and Nakatani, Y. (2003). The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell 113, 357-367.
22. Guerrero-Santoro, J., Kapetanaki, M.G., Hsieh, C.L., Gorbachinsky, I., Levine, A.S., and Rapić-Otrin, V. (2008). The cullin 4B-based UV-damaged DNA-binding protein ligase binds to UV-damaged chromatin and ubiquitinates histone H2A. Cancer Res 68, 5014-5022.
23. Guo, Y., Nady, N., Qi, C., Allali-Hassani, A., Zhu, H., Pan, P., Adams-Cioaba, M.A., Amaya, M.F., Dong, A., Vedadi, M., et al. (2009). Methylation-state-specific recognition of histones by the MBT repeat protein L3MBTL2. Nucleic Acids Res 37, 2204-2210.
24. Han, Z., Guo, L., Wang, H., Shen, Y., Deng, X.W., and Chai, J. (2006). Structural basis for the specific recognition of methylated histone H3 lysine 4 by the WD-40 protein WDR5. Mol Cell 22, 137-144.
25. Hansen, K.H., Bracken, A.P., Pasini, D., Dietrich, N., Gehani, S.S., Monrad, A., Rappsilber, J., Lerdrup, M., and Helin, K. (2008). A model for transmission of the H3K27me3 epigenetic mark. Nat Cell Biol 10, 1291-1300.
26. Hao, B., Oehlmann, S., Sowa, M.E., Harper, J.W., and Pavletich, N.P. (2007). Structure of a Fbw7-Skp1-cyclin E complex: multisitephosphorylated substrate recognition by SCF ubiquitin ligases. Mol Cell 26, 131-143.
27. Hardwick, K.G., Johnston, R.C., Smith, D.L., and Murray, A.W. (2000). MAD3 encodes a novel component of the spindle checkpoint which interacts with Bub3p, Cdc20p, and Mad2p. J Cell Biol 148, 871-882.
28. Hattendorf, D.A., Andreeva, A., Gangar, A., Brennwald, P.J., and Weis, W.I. (2007). Structure of the yeast polarity protein Sro7 reveals a SNARE regulatory mechanism. Nature 446, 567-571.
29. He, Y.J., McCall, C.M., Hu, J., Zeng, Y., and Xiong, Y. (2006). DDB1 functions as a linker to recruit receptor WD40 proteins to CUL4-ROC1 ubiquitin ligases. Genes Dev 20, 2949-2954.
30. Higa, L.A., Wu, M., Ye, T., Kobayashi, R., Sun, H., and Zhang, H. (2006). CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation. Nat Cell Biol 8, 1277-1283.
31. Hu, J., McCall, C.M., Ohta, T., and Xiong, Y. (2004). Targeted ubiquitination of CDT1 by the DDB1-CUL4A-ROC1 ligase in response to DNA damage. Nat Cell Biol 6, 1003-1009.
32. Jennings, B.H., Pickles, L.M., Wainwright, S.M., Roe, S.M., Pearl, L. H., and Ish-Horowicz, D. (2006). Molecular recognition of transcriptional repressor motifs by the WD domain of the Groucho/TLE corepressor. Mol Cell 22, 645-655.
33. Jin, J., Cardozo, T., Lovering, R.C., Elledge, S.J., Pagano, M., and Harper, J.W. (2004). Systematic analysis and nomenclature of mammalian F-box proteins. Genes Dev 18, 2573-2580.
34. Johnston, C.A., Kimple, A.J., Giguère, P.M., and Siderovski, D.P. (2008). Structure of the parathyroid hormone receptor C terminus bound to the G-protein dimer Gbeta1gamma2. Structure 16, 1086-1094.
35. Kirchhausen, T., and Harrison, S.C. (1981). Protein organization in clathrin trimers. Cell 23, 755-761.
36. Lambright, D.G., Sondek, J., Bohm, A., Skiba, N.P., Hamm, H.E., and Sigler, P.B. (1996). The 2.0 A crystal structure of a heterotrimeric G protein. Nature 379, 311-319.
37. Larsen, N.A., Al-Bassam, J., Wei, R.R., and Harrison, S.C. (2007). Structural analysis of Bub3 interactions in the mitotic spindle checkpoint. Proc Natl Acad Sci U S A 104, 1201-1206.
38. Lejon, S., Thong, S.Y., Murthy, A., AlQarni, S., Murzina, N.V., Blobel, G.A., Laue, E.D., and Mackay, J.P. (2011). Insights into association of the NuRD complex with FOG-1 from the crystal structure of an RbAp48$FOG-1 complex. J Biol Chem 286, 1196-1203.
39. Lens, S.M., Wolthuis, R.M., Klompmaker, R., Kauw, J., Agami, R., Brummelkamp, T., Kops, G., and Medema, R.H. (2003). Survivin is required for a sustained spindle checkpoint arrest in response to lack of tension. EMBO J 22, 2934-2947.
40. Letunic, I., Doerks, T., and Bork, P. (2009). SMART 6: recent updates and new developments. Nucleic Acids Res 37, D229-D232.
41. Li, D., and Roberts, R. (2001). WD-repeat proteins: structure characteristics, biological function, and their involvement in human diseases. Cell Mol Life Sci 58, 2085-2097.
42. Li, T., Chen, X., Garbutt, K.C., Zhou, P., and Zheng, N. (2006). Structure of DDB1 in complex with a paramyxovirus V protein: viral hijack of a propeller cluster in ubiquitin ligase. Cell 124, 105-117.
43. Li, T., Robert, E.I., van Breugel, P.C., Strubin, M., and Zheng, N. (2010). A promiscuous α-helical motif anchors viral hijackers and substrate receptors to the CUL4-DDB1 ubiquitin ligase machinery. Nat Struct Mol Biol 17, 105-111.
44. Liu, H., Wang, J.Y., Huang, Y., Li, Z., Gong, W., Lehmann, R., and Xu, R.M. (2010a). Structural basis for methylarginine-dependent recognition of Aubergine by Tudor. Genes & Dev 24: 1876-1881
45. Liu, K., Chen, C., Guo, Y., Lam, R., Bian, C., Xu, C., Zhao, D.Y., Jin, J., MacKenzie, F., Pawson, T., et al. (2010b). Structural basis for recognition of arginine methylated Piwi proteins by the extended Tudor domain. Proc Natl Acad Sci U S A 107, 18398-18403.
46. Margueron, R., Justin, N., Ohno, K., Sharpe, M.L., Son, J., Drury, W.J. 3rd, Voigt, P., Martin, S.R., Taylor, W.R., De Marco, V., et al. (2009). Role of the polycomb protein EED in the propagation of repressive histone marks. Nature 461, 762-767.
47. Michel, J.J., and Xiong, Y. (1998). Human CUL-1, but not other cullin family members, selectively interacts with SKP1 to form a complex with SKP2 and cyclin A. Cell Growth Differ 9, 435-449.
48. Min, J., Allali-Hassani, A., Nady, N., Qi, C., Ouyang, H., Liu, Y., MacKenzie, F., Vedadi, M., and Arrowsmith, C.H. (2007). L3MBTL1 recognition of mono-and dimethylated histones. Nat Struct Mol Biol 14, 1229-1230.
49. Min, J., Zhang, Y., and Xu, R.M. (2003). Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Genes Dev 17, 1823-1828.
50. Mohri, K., Vorobiev, S., Fedorov, A.A., Almo, S.C., and Ono, S. (2004). Identification of functional residues on Caenorhabditis elegans actin-interacting protein 1 (UNC-78) for disassembly of actin depolymerizing factor/cofilin-bound actin filaments. J Biol Chem 279, 31697-31707.
51. Müller, J., Hart, C.M., Francis, N.J., Vargas, M.L., Sengupta, A., Wild, B., Miller, E.L., O'Connor, M.B., Kingston, R.E., and Simon, J.A. (2002). Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111, 197-208.
52. Murzin, A.G. (1992). Structural principles for the propeller assembly of beta-sheets: the preference for seven-fold symmetry. Proteins 14, 191-201.
53. Murzina, N.V., Pei, X.Y., Zhang, W., Sparkes, M., Vicente-Garcia, J., Pratap, J.V., McLaughlin, S.H., Ben-Shahar, T.R., Verreault, A., Luisi, B.F., et al. (2008). Structural basis for the recognition of histone H4 by the histone-chaperone RbAp46. Structure 16, 1077-1085.
54. Nash, P., Tang, X., Orlicky, S., Chen, Q., Gertler, F.B., Mendenhall, M. D., Sicheri, F., Pawson, T., and Tyers, M. (2001). Multisite phosphorylation of a CDK inhibitor sets a threshold for the onset of DNA replication. Nature 414, 514-521.
55. Neer, E.J., Schmidt, C.J., Nambudripad, R., and Smith, T.F. (1994). The ancient regulatory-protein family of WD-repeat proteins. Nature 371, 297-300.
56. Oliver, A.W., Swift, S., Lord, C.J., Ashworth, A., and Pearl, L.H. (2009). Structural basis for recruitment of BRCA2 by PALB2. EMBO Rep 10, 990-996.
57. Orlicky, S., Tang, X., Willems, A., Tyers, M., and Sicheri, F. (2003). Structural basis for phosphodependent substrate selection and orientation by the SCFCdc4 ubiquitin ligase. Cell 112, 243-256.
58. Paoli, M. (2001). Protein folds propelled by diversity. Prog Biophys Mol Biol 76, 103-130.
59. Patel, A., Dharmarajan, V., and Cosgrove, M.S. (2008). Structure of WDR5 bound to mixed lineage leukemia protein-1 peptide. J Biol Chem 283, 32158-32161.
60. Ruthenburg, A.J., Wang, W., Graybosch, D.M., Li, H., Allis, C.D., Patel, D.J., and Verdine, G.L. (2006). Histone H3 recognition and presentation by the WDR5 module of the MLL1 complex. Nat Struct Mol Biol 13, 704-712.
61. Schuetz, A., Allali-Hassani, A., Martín, F., Loppnau, P., Vedadi, M., Bochkarev, A., Plotnikov, A.N., Arrowsmith, C.H., and Min, J. (2006). Structural basis for molecular recognition and presentation of histone H3 by WDR5. EMBO J 25, 4245-4252.
62. Schuster-Böckler, B., Schultz, J., and Rahmann, S. (2004). HMM Logos for visualization of protein families. BMC Bioinformatics 5, 7.
63. Shaw, N., Zhao, M., Cheng, C., Xu, H., Saarikettu, J., Li, Y., Da, Y., Yao, Z., Silvennoinen, O., Yang, J., et al. (2007). The multifunctional human p100 protein 'hooks' methylated ligands. Nat Struct Mol Biol 14, 779-784.
64. Smith, T.F., Gaitatzes, C., Saxena, K., and Neer, E.J. (1999). The WD repeat: a common architecture for diverse functions. Trends Biochem Sci 24, 181-185.
65. Song, J.J., Garlick, J.D., and Kingston, R.E. (2008). Structural basis of histone H4 recognition by p55. Genes Dev 22, 1313-1318.
66. Song, J.J., and Kingston, R.E. (2008). WDR5 interacts with mixed lineage leukemia (MLL) protein via the histone H3-binding pocket. J Biol Chem 283, 35258-35264.
67. Stirnimann, C.U., Petsalaki, E., Russell, R.B., and Müller, C.W. (2010). WD40 proteins propel cellular networks. Trends Biochem Sci 35, 565-574.
68. Sy, S.M., Huen, M.S., and Chen, J. (2009). PALB2 is an integral component of the BRCA complex required for homologous recombination repair. Proc Natl Acad Sci U S A 106, 7155-7160.
69. ter Haar, E., Harrison, S.C., and Kirchhausen, T. (2000). Peptide-ingroove interactions link target proteins to the beta-propeller of clathrin. Proc Natl Acad Sci U S A 97, 1096-1100.
70. Ungewickell, E., and Branton, D. (1981). Assembly units of clathrin coats. Nature 289, 420-422.
71. Verreault, A., Kaufman, P.D., Kobayashi, R., and Stillman, B. (1996). Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4. Cell 87, 95-104.
72. Verreault, A., Kaufman, P.D., Kobayashi, R., and Stillman, B. (1998). Nucleosomal DNA regulates the core-histone-binding subunit of the human Hat1 acetyltransferase. Curr Biol 8, 96-108.
73. Voegtli, W.C., Madrona, A.Y., and Wilson, D.K. (2003). The structure of Aip1p, a WD repeat protein that regulates Cofilin-mediated actin depolymerization. J Biol Chem 278, 34373-34379.
74. Wall, M.A., Coleman, D.E., Lee, E., Iñiguez-Lluhi, J.A., Posner, B.A., Gilman, A.G., and Sprang, S.R. (1995). The structure of the G protein heterotrimer Gi alpha 1 beta 1 gamma 2. Cell 83, 1047-1058.
75. Wang, H., Zhai, L., Xu, J., Joo, H.Y., Jackson, S., Erdjument-Bromage, H., Tempst, P., Xiong, Y., and Zhang, Y. (2006). Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Mol Cell 22, 383-394.
76. Wang, L., Brown, J.L., Cao, R., Zhang, Y., Kassis, J.A., and Jones, R. S. (2004). Hierarchical recruitment of polycomb group silencing complexes. Mol Cell 14, 637-646.
77. Whittle, J.R., and Schwartz, T.U. (2010). Structure of the Sec13-Sec16 edge element, a template for assembly of the COPII vesicle coat. J Cell Biol 190, 347-361.
78. Wittschieben, B.O., Iwai, S., and Wood, R.D. (2005). DDB1-DDB2 (xeroderma pigmentosum group E) protein complex recognizes a cyclobutane pyrimidine dimer, mismatches, apurinic/apyrimidinic sites, and compound lesions in DNA. J Biol Chem 280, 39982-39989.
79. Wu, G., Xu, G., Schulman, B.A., Jeffrey, P.D., Harper, J.W., and Pavletich, N.P. (2003). Structure of a beta-TrCP1-Skp1-betacatenin complex: destruction motif binding and lysine specificity of the SCF(beta-TrCP1) ubiquitin ligase. Mol Cell 11, 1445-1456.
80. Wu, X.H., Chen, R.C., Gao, Y., and Wu, Y.D. (2010). The effect of Asp-His-Ser/Thr-Trp tetrad on the thermostability of WD40-repeat proteins. Biochemistry 49, 10237-10245.
81. Wysocka, J., Swigut, T., Milne, T.A., Dou, Y., Zhang, X., Burlingame, A.L., Roeder, R.G., Brivanlou, A.H., and Allis, C.D. (2005). WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell 121, 859-872.
82. Xu, C., Bian, C., Yang, W., Galka, M., Ouyang, H., Chen, C., Qiu, W., Liu, H., Jones, A.E., MacKenzie, F., et al. (2010). Binding of different histone marks differentially regulates the activity and specificity of polycomb repressive complex 2 (PRC2). Proc Natl Acad Sci U S A 107, 19266-19271.