WW domain interactions regulate the Hippo tumor suppressor pathway

Cell Death and Disease

Volumn 2, Issue 6, 2011, Pages

  Salah, Z ^a   Aqeilan, R I ^a  

^a HEBREW UNIVERSITY   (Israel)

Author keywords

Hippo pathway; ITCH; LATS1; Protein protein interaction; WW domain

Indexed keywords

HIPPO TUMOR SUPPRESSOR PROTEIN; PROTEIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; WW DOMAIN PROTEIN; PROTEIN SERINE THREONINE KINASE;

CARCINOGENESIS; DIMERIZATION; HUMAN; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN STABILITY; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; TUMOR CELL; TUMOR GROWTH; ANIMAL; CHEMISTRY; METABOLISM;

MAMMALIA;

ANIMALS; HUMANS; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

EID: 79960027086     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2011.53     Document Type: Review

References (76)

1. Dong J, Feldmann G, Huang J, Wu S, Zhang N, Comerford SA et al. Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 2007; 130: 1120-1133. (Pubitemid 47410268)
2. McNeill H, Woodgett JR. When pathways collide: collaboration and connivance among signalling proteins in development. Nat Rev Mol Cell Biol 2010; 11: 404-413.
3. Zhao B, Li L, Lei Q, Guan KL. The Hippo-YAP pathway in organ size control and tumorigenesis: an updated version. Genes Dev 2010; 24: 862-874.
4. Sudol M, Harvey KF. Modularity in the Hippo signaling pathway. Trends Biochem Sci 2010; 35: 627-633.
5. Sudol M. Newcomers to the WWdomain-mediated network of the Hippo tumor suppressor pathway. Genes Cancer 2011; 1: 1115-1118.
6. Bork P, Sudol M. The WW domain: a signalling site in dystrophin? Trends Biochem Sci 1994; 19: 531-533. (Pubitemid 24360488)
7. Sudol M, Bork P, Einbond A, Kastury K, Druck T, Negrini M et al. Characterization of the mammalian YAP (Yes-associated protein) gene and its role in defining a novel protein module, the WW domain. J Biol Chem 1995; 270: 14733-14741.
8. Sudol M. WW domain in "modular protein domains" In: Cesareni G, Gimona M, Sudol M, and Yaffe M (eds). Modular Protein Domains. Wiley-VCH Verlag GmBH & Co, KGaA: Weinheim, FRG, 2004, pp 59-72.
9. Chen HI, Sudol M. The WW domain of Yes-associated protein binds a proline-rich ligand that differs from the consensus established for Src homology 3-binding modules. Proc Natl Acad Sci USA 1995; 92: 7819-7823.
10. Sudol M. Structure and function of the WW domain. Prog Biophys Mol Biol 1996; 65: 113-132. (Pubitemid 27161010)
11. Chen HI, Einbond A, Kwak SJ, Linn H, Koepf E, Peterson S et al. Characterization of the WW domain of human yes-associated protein and its polyproline-containing ligands. J Biol Chem 1997; 272: 17070-17077. (Pubitemid 27289814)
12. Macias MJ, Wiesner S, Sudol M. WW and SH3 domains, two different scaffolds to recognize proline-rich ligands. FEBS Lett 2002; 513: 30-37. (Pubitemid 34242975)
13. Otte L, Wiedemann U, Schlegel B, Pires JR, Beyermann M, Schmieder P et al.WWdomain sequence activity relationships identified using ligand recognition propensities of 42 WW domains. Protein Sci 2003; 12: 491-500. (Pubitemid 36241107)
14. Sudol M, Hunter T. NeW wrinkles for an old domain. Cell 2000; 103: 1001-1004. (Pubitemid 32037388)
15. Fotia AB, Dinudom A, Shearwin KE, Koch JP, Korbmacher C, Cook DI et al. The role of individual Nedd4-2 (KIAA0439) WW domains in binding and regulating epithelial sodium channels. FASEB J 2003; 17: 70-72.
16. Ingham RJ, Colwill K, Howard C, Dettwiler S, Lim CS, Yu J et al. WW domains provide a platform for the assembly of multiprotein networks. Mol Cell Biol 2005; 25: 7092-7106. (Pubitemid 41105907)
17. Salah Z, Alian A, Aqeilan RI. Domain-containing proteins: retrospectives and the future. Front Biosci 2011.
18. Hansson JH, Schild L, Lu Y, Wilson TA, Gautschi I, Shimkets R et al. A de novo missense mutation of the beta subunit of the epithelial sodium channel causes hypertension and Liddle syndrome, identifying a proline-rich segment critical for regulation of channel activity. Proc Natl Acad Sci USA 1995; 92: 11495-11499.
19. Inoue J, Iwaoka T, Tokunaga H, Takamune K, Naomi S, Araki M et al. A family with Liddle's syndrome caused by a new missense mutation in the beta subunit of the epithelial sodium channel. J Clin Endocrinol Metab 1998; 83: 2210-2213. (Pubitemid 28496361)
20. Chung W, Campanelli JT.WW and EF hand domains of dystrophin-family proteins mediate dystroglycan binding. Mol Cell Biol Res Commun 1999; 2: 162-171. (Pubitemid 129533213)
21. Huang X, Poy F, Zhang R, Joachimiak A, Sudol M, Eck MJ. Structure of a WW domain containing fragment of dystrophin in complex with beta-dystroglycan. Nat Struct Biol 2000; 7: 634-638. (Pubitemid 30636672)
22. Liu F, Li B, Tung EJ, Grundke-Iqbal I, Iqbal K, Gong CX. Site-specific effects of tau phosphorylation on its microtubule assembly activity and self-aggregation. Eur J Neurosci 2007; 26: 3429-3436. (Pubitemid 350243526)
23. Mandelkow EM, Mandelkow E. Tau in Alzheimer's disease. Trends Cell Biol 1998; 8: 425-427. (Pubitemid 28529713)
24. Morishima-Kawashima M, Hasegawa M, Takio K, Suzuki M, Yoshida H, Watanabe A et al. Hyperphosphorylation of tau in PHF. Neurobiol Aging 1995; 16: 365-371; discussion 371-380.
25. Faber PW, Barnes GT, Srinidhi J, Chen J, Gusella JF, MacDonald ME. Huntingtin interacts with a family of WW domain proteins. Hum Mol Genet 1998; 7: 1463-1474. (Pubitemid 28429928)
26. Passani LA, Bedford MT, Faber PW, McGinnis KM, Sharp AH, Gusella JF et al. Huntingtin's WW domain partners in Huntington's disease post-mortem brain fulfill genetic criteria for direct involvement in Huntington's disease pathogenesis. Hum Mol Genet 2000; 9: 2175-2182.
27. Tapia VE, Nicolaescu E, McDonald CB, Musi V, Oka T, Inayoshi Y et al. Y65C missense mutation in the WW domain of the Golabi-Ito-Hall syndrome protein PQBP1 affects its binding activity and deregulates pre-mRNA splicing. J Biol Chem 2010; 285: 19391-19401.
28. Del Mare S, Salah Z, Aqeilan RI. WWOX: its genomics, partners, and functions. J Cell Biochem 2009; 108: 737-745.
29. Pan D. The hippo signaling pathway in development and cancer. Dev Cell 2010; 19: 491-505.
30. Salah Z, Aqeilan R, Huebner K. WWOX gene and gene product: tumor suppression through specific protein interactions. Future Oncol 2010; 6: 249-259.
31. Harvey K, Tapon N. The Salvador-Warts-Hippo pathway - an emerging tumour-suppressor network. Nat Rev Cancer 2007; 7: 182-191.
32. Grusche FA, Richardson HE, Harvey KF. Upstream regulation of the hippo size control pathway. Curr Biol 2010; 20: R574-R582.
33. Hao Y, Chun A, Cheung K, Rashidi B, Yang X. Tumor suppressor LATS1 is a negative regulator of oncogene YAP. J Biol Chem 2008; 283: 5496-5509.
34. Zhang J, Smolen GA, Haber DA. Negative regulation of YAP by LATS1 underscores evolutionary conservation of the Drosophila Hippo pathway. Cancer Res 2008; 68: 2789-2794. (Pubitemid 351556277)
35. Zhao B, Wei X, Li W, Udan RS, Yang Q, Kim J et al. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev 2007; 21: 2747-2761. (Pubitemid 350070721)
36. Lei QY, Zhang H, Zhao B, Zha ZY, Bai F, Pei XH et al. TAZ promotes cell proliferation and epithelial-mesenchymal transition and is inhibited by the hippo pathway. Mol Cell Biol 2008; 28: 2426-2436. (Pubitemid 351429986)
37. Zhao B, Kim J, Ye X, Lai ZC, Guan KL. Both TEAD-binding and WW domains are required for the growth stimulation and oncogenic transformation activity of yes-associated protein. Cancer Res 2009; 69: 1089-1098.
38. Genevet A, Wehr MC, Brain R, Thompson BJ, Tapon N. Kibra is a regulator of the Salvador/Warts/Hippo signaling network. Dev Cell 2010; 18: 300-308.
39. Yu J, Zheng Y, Dong J, Klusza S, Deng WM, Pan D. Kibra functions as a tumor suppressor protein that regulates Hippo signaling in conjunction with Merlin and Expanded. Dev Cell 2010; 18: 288-299.
40. Baumgartner R, Poernbacher I, Buser N, Hafen E, Stocker H. The WW domain protein Kibra acts upstream of Hippo in Drosophila. Dev Cell 2010; 18: 309-316.
41. Xiao L, Chen Y, Ji M, Dong J. KIBRA regulates Hippo signaling activity via interactions with large tumor suppressor kinases. J Biol Chem 2011; 286: 7788-7796.
42. Salah Z, Melino G, Aqeilan RI. Negative regulation of the Hippo pathway by E3 ubiquitin ligase Itch is sufficient to promote tumorigenicity. Cancer Res 2011; 71: 2010-2020.
43. Ho KC, Zhou Z, She YM, Chun A, Cyr TD, Yang X. Itch E3 ubiquitin ligase regulates large tumor suppressor 1 tumor-suppressor stability. Proc Natl Acad Sci USA 2011; 108: 4870-4875.
44. Rossi M, De Laurenzi V, Munarriz E, Green DR, Liu YC, Vousden KH et al. The ubiquitinprotein ligase Itch regulates p73 stability. EMBO J 2005; 24: 836-848. (Pubitemid 40396112)
45. Strano S, Munarriz E, Rossi M, Castagnoli L, Shaul Y, Sacchi A et al. Physical interaction with Yes-associated protein enhances p73 transcriptional activity. J Biol Chem 2001; 276: 15164-15173.
46. Oka T, Mazack V, Sudol M. Mst2 and Lats kinases regulate apoptotic function of Yes kinase-associated protein (YAP). J Biol Chem 2008; 283: 27534-27546.
47. Zhang X, Milton CC, Poon CL, Hong W, Harvey KF. Wbp2 cooperates with Yorkie to drive tissue growth downstream of the Salvador-Warts-Hippo pathway. Cell Death Differ 2011.
48. Chan SW, Lim CJ, Huang C, Chong YF, Gunaratne HJ, Hogue KA et al. WW domain-mediated interaction with Wbp2 is important for the oncogenic property of TAZ. Oncogene 2011; 30: 600-610.
49. Chan SW, Lim CJ, Chong YF, Pobbati AV, Huang C, Hong W. Hippo pathway-independent restriction of TAZ and YAP by angiomotin. J Biol Chem 2011; 286: 7018-7026.
50. Wang W, Huang J, Chen J. Angiomotin-like proteins associate with and negatively regulate YAP1. J Biol Chem 2011; 286: 4364-4370.
51. Zhao B, Li L, Lu Q, Wang LH, Liu CY, Lei Q et al. Angiomotin is a novel Hippo pathway component that inhibits YAP oncoprotein. Genes Dev 2011; 25: 51-63.
52. Liu CY, Lv X, Li T, Xu Y, Zhou X, Zhao S et al. PP1 cooperates with ASPP2 to dephosphorylate and activate TAZ. J Biol Chem 2011; 286: 5558-5566.
53. Vigneron AM, Ludwig RL, Vousden KH. Cytoplasmic ASPP1 inhibits apoptosis through the control of YAP. Genes Dev 2010; 24: 2430-2439.
54. Hoffman RM. The multiple uses of fluorescent proteins to visualize cancer in vivo. Nat Rev Cancer 2005; 5: 796-806. (Pubitemid 41400779)
55. Hoffman RM, Yang M. Subcellular imaging in the live mouse. Nat Protoc 2006; 1: 775-782.
56. Hoffman RM, Yang M. Color-coded fluorescence imaging of tumor-host interactions. Nat Protoc 2006; 1: 928-935.
57. Hoffman RM, Yang M. Whole-body imaging with fluorescent proteins. Nat Protoc 2006; 1: 1429-1438.
58. Macias MJ, Hyvonen M, Baraldi E, Schultz J, Sudol M, Saraste M et al. Structure of theWW domain of a kinase-associated protein complexed with a proline-rich peptide. Nature 1996; 382: 646-649. (Pubitemid 26268960)
59. Hong JH, Hwang ES, McManus MT, Amsterdam A, Tian Y, Kalmukova R et al. TAZ, a transcriptional modulator of mesenchymal stem cell differentiation. Science 2005; 309: 1074-1078. (Pubitemid 41134465)
60. Harvey KF, Pfleger CM, Hariharan IK. The Drosophila Mst ortholog, Hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 2003; 114: 457-467. (Pubitemid 37100994)
61. Tapon N, Harvey KF, Bell DW, Wahrer DC, Schiripo TA, Haber DA et al. Salvador promotes both cell cycle exit and apoptosis in Drosophila and is mutated in human cancer cell lines. Cell 2002; 110: 467-478. (Pubitemid 35232290)
62. Brittle AL, Repiso A, Casal J, Lawrence PA, Strutt D. Four-jointed modulates growth and planar polarity by reducing the affinity of dachsous for fat. Curr Biol 2010; 20: 803-810.
63. Cho E, Feng Y, Rauskolb C, Maitra S, Fehon R, Irvine KD. Delineation of a fat tumor suppressor pathway. Nat Genet 2006; 38: 1142-1150. (Pubitemid 44470359)
64. Feng Y, Irvine KD. Processing and phosphorylation of the Fat receptor. Proc Natl Acad Sci USA 2009; 106: 11989-11994.
65. Sopko R, Silva E, Clayton L, Gardano L, Barrios-Rodiles M, Wrana J et al. Phosphorylation of the tumor suppressor fat is regulated by its ligand Dachsous and the kinase discs overgrown. Curr Biol 2009; 19: 1112-1117.
66. Chen CL, Gajewski KM, Hamaratoglu F, Bossuyt W, Sansores-Garcia L, Tao C et al. The apical-basal cell polarity determinant Crumbs regulates Hippo signaling in Drosophila. Proc Natl Acad Sci USA 2010; 107: 15810-15815.
67. Ling C, Zheng Y, Yin F, Yu J, Huang J, Hong Y et al. The apical transmembrane protein Crumbs functions as a tumor suppressor that regulates Hippo signaling by binding to Expanded. Proc Natl Acad Sci USA 2010; 107: 10532-10537.
68. Song H, Mak KK, Topol L, Yun K, Hu J, Garrett L et al. Mammalian Mst1 and Mst2 kinases play essential roles in organ size control and tumor suppression. Proc Natl Acad Sci USA 2010; 107: 1431-1436.
69. Zhou D, Conrad C, Xia F, Park JS, Payer B, Yin Y et al. Mst1 and Mst2 maintain hepatocyte quiescence and suppress hepatocellular carcinoma development through inactivation of the Yap1 oncogene. Cancer Cell 2009; 16: 425-438.
70. Patel S, George R, Autore F, Fraternali F, Ladbury JE, Nikolova PV. Molecular interactions of ASPP1 and ASPP2 with the p53 protein family and the apoptotic promoters PUMA and Bax. Nucleic Acids Res 2008; 36: 5139-5151.
71. Komuro A, Nagai M, Navin NE, Sudol M. WW domain-containing protein YAP associates with ErbB-4 and acts as a co-transcriptional activator for the carboxyl-terminal fragment of ErbB-4 that translocates to the nucleus. J Biol Chem 2003; 278: 33334-33341. (Pubitemid 37055785)
72. Webb C, Upadhyay A, Giuntini F, Eggleston I, Furutani-Seiki M, Ishima R et al. Structural features and ligand binding properties of tandem WW domains from YAP and TAZ, nuclear effectors of the Hippo pathway. Biochemistry 2011; 50: 3300-3309.
73. Aqeilan RI, Donati V, Palamarchuk A, Trapasso F, Kaou M, Pekarsky Y et al. WW domaincontaining proteins, WWOX and YAP, compete for interaction with ErbB-4 and modulate its transcriptional function. Cancer Res 2005; 65: 6764-6772. (Pubitemid 41060714)
74. Alarcon C, Zaromytidou AI, Xi Q, Gao S, Yu J, Fujisawa S et al. Nuclear CDKs drive Smad transcriptional activation and turnover in BMP and TGF-beta pathways. Cell 2009; 139: 757-769.
75. Zaidi SK, Sullivan AJ, Medina R, Ito Y, van Wijnen AJ, Stein JL et al. Tyrosine phosphorylation controls Runx2-mediated subnuclear targeting of YAP to repress transcription. EMBO J 2004; 23: 790-799. (Pubitemid 38418746)
76. Varelas X, Miller BW, Sopko R, Song S, Gregorieff A, Fellouse FA et al. The Hippo pathway regulates Wnt/beta-catenin signaling. Dev Cell 2010; 18: 579-591.