A coordinated phosphorylation by Lats and CK1 regulates YAP stability through SCFβ-TRCP

Genes and Development

Volumn 24, Issue 1, 2010, Pages 72-85

  Zhao, Bin ^a   Li, Li ^a,b   Tumaneng, Karen ^a   Wang, Cun Yu ^c   Guan, Kun Liang ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UCLA SCHOOL OF DENTISTRY   (United States)

Author keywords

CK1; Hippo pathway; Lats; Phosphodegron; SCF; YAP

Indexed keywords

CASEIN KINASE IDELTA; CASEIN KINASE IEPSILON; PROTEIN KINASE; PROTEIN LATS; REGULATOR PROTEIN; SERINE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; YES ASSOCIATED PROTEIN;

ARTICLE; CATALYSIS; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; UBIQUITINATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID MOTIFS; CASEIN KINASE I; CELL LINE; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MUTATION; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN-SERINE-THREONINE KINASES; SERINE; SKP CULLIN F-BOX PROTEIN LIGASES; UBIQUITINATION;

EID: 73549095761     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1843810     Document Type: Article

References (48)

1. Camargo FD, Gokhale S, Johnnidis JB, Fu D, Bell GW, Jaenisch R, Brummelkamp TR. 2007. YAP1 increases organ size and expands undifferentiated progenitor cells. Curr Biol 17: 2054-2060.
2. Cho E, Feng Y, Rauskolb C, Maitra S, Fehon R, Irvine KD. 2006. Delineation of a Fat tumor suppressor pathway. Nat Genet 38: 1142-1150.
3. Clevers H. 2006. Wnt/β-catenin signaling in development and disease. Cell 127: 469-480.
4. Dephoure N, Zhou C, Villen J, Beausoleil SA, Bakalarski CE, Elledge SJ, Gygi SP. 2008. A quantitative atlas of mitotic phosphorylation. Proc Natl Acad Sci 105: 10762-10767.
5. Deshaies RJ. 1999. SCF and Cullin/Ring H2-based ubiquitin ligases. Annu Rev Cell Dev Biol 15: 435-467.
6. Dong J, Feldmann G, Huang J, Wu S, Zhang N, Comerford SA, Gayyed MF, Anders RA, Maitra A, Pan D. 2007. Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 130: 1120-1133.
7. Frescas D, Pagano M. 2008. Deregulated proteolysis by the F-box proteins SKP2 and β-TrCP: Tipping the scales of cancer. Nat Rev Cancer 8: 438-449.
8. Fuchs SY, Spiegelman VS, Kumar KG. 2004. The many faces of β-TrCP E3 ubiquitin ligases: Reflections in the magic mirror of cancer. Oncogene 23: 2028-2036.
9. Hao Y, Chun A, Cheung K, Rashidi B, Yang X. 2008. Tumor suppressor LATS1 is a negative regulator of oncogene YAP. J Biol Chem 283: 5496-5509.
10. Hart M, Concordet JP, Lassot I, Albert I, del los Santos R, Durand H, Perret C, Rubinfeld B, Margottin F, Benarous R, et al. 1999. The F-box protein β-TrCP associates with phosphorylated β-catenin and regulates its activity in the cell. Curr Biol 9: 207-210.
11. Harvey KF, Pfleger CM, Hariharan IK. 2003. The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 114: 457-467.
12. Hershko A, Ciechanover A. 1998. The ubiquitin system. Annu Rev Biochem 67: 425-479.
13. Huang J, Wu S, Barrera J, Matthews K, Pan D. 2005. The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila homo-log of YAP. Cell 122: 421-434.
14. Jia J, Zhang W, Wang B, Trinko R, Jiang J. 2003. The Drosophila Ste20 family kinase dMST functions as a tumor suppressor by restricting cell proliferation and promoting apoptosis. Genes & Dev 17: 2514-2519.
15. Jin J, Shirogane T, Xu L, Nalepa G, Qin J, Elledge SJ, Harper JW. 2003. SCFβ-TRCP links Chk1 signaling to degradation of the Cdc25A protein phosphatase. Genes & Dev 17: 3062-3074.
16. Kango-Singh M, Nolo R, Tao C, Verstreken P, Hiesinger PR, Bellen HJ, Halder G. 2002. Shar-pei mediates cell proliferation arrest during imaginal disc growth in Drosophila. Development 129: 5719-5730.
17. Knippschild U, Gocht A, Wolff S, Huber N, Lohler J, Stoter M. 2005. The casein kinase 1 family: Participation in multiple cellular processes in eukaryotes. Cell Signal 17: 675-689.
18. Lai ZC,Wei X, Shimizu T, Ramos E, Rohrbaugh M, Nikolaidis N, Ho LL, Li Y. 2005. Control of cell proliferation and apoptosis by mob as tumor suppressor, mats. Cell 120: 675-685.
19. Lapi E, Di Agostino S, Donzelli S, Gal H, Domany E, Rechavi G, Pandolfi PP, Givol D, Strano S, Lu X, et al. 2008. PML, YAP, and p73 are components of a proapoptotic autoregulatory feedback loop. Mol Cell 32: 803-814.
20. Latres E, Chiaur DS, Pagano M. 1999. The human F box protein β-Trcp associates with the Cul1/Skp1 complex and regulates the stability of β-catenin. Oncogene 18: 849-854.
21. Levy D, Adamovich Y, Reuven N, Shaul Y. 2008. Yap1 phosphorylation by c-Abl is a critical step in selective activation of proapoptotic genes in response to DNA damage. Mol Cell 29: 350-361.
22. Li Q, Verma IM. 2002. NF-κB regulation in the immune system. Nat Rev Immunol 2: 725-734.
23. Liu W, Dong X, Mai M, Seelan RS, Taniguchi K, Krishnadath KK, Halling KC, Cunningham JM, Boardman LA, Qian C, et al. 2000. Mutations in AXIN2 cause colorectal cancer with defective mismatch repair by activating β-catenin/TCF signalling. Nat Genet 26: 146-147.
24. Liu C, Li Y, Semenov M, Han C, Baeg GH, Tan Y, Zhang Z, Lin X, He X. 2002. Control of β-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108: 837-847.
25. McClatchey AI, Giovannini M. 2005. Membrane organization and tumorigenesis - the NF2 tumor suppressor, Merlin. Genes & Dev 19: 2265-2277.
26. Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, Vogelstein B, Kinzler KW. 1997. Activation of β-catenin-Tcf signaling in colon cancer by mutations in β-catenin or APC. Science 275: 1787-1790.
27. Oh H, Irvine KD. 2009. In vivo analysis of Yorkie phosphorylation sites. Oncogene 28: 1916-1927.
28. Oka T, Mazack V, Sudol M. 2008. Mst2 and Lats kinases regulate apoptotic function of Yes kinase-associated protein (YAP). J Biol Chem 283: 27534-27546.
29. Overholtzer M, Zhang J, Smolen GA, Muir B, Li W, Sgroi DC, Deng CX, Brugge JS, Haber DA. 2006. Transforming properties of YAP, a candidate oncogene on the chromosome 11q22 amplicon. Proc Natl Acad Sci 103: 12405-12410.
30. Pan D. 2007. Hippo signaling in organ size control. Genes & Dev 21: 886-897.
31. Pantalacci S, Tapon N, Leopold P. 2003. The Salvador partner Hippo promotes apoptosis and cell-cycle exit in Drosophila. Nat Cell Biol 5: 921-927.
32. Pickart CM. 2001. Mechanisms underlying ubiquitination. Annu Rev Biochem 70: 503-533.
33. Provost E, McCabe A, Stern J, Lizardi I, D'Aquila TG, Rimm DL. 2005. Functional correlates of mutation of the Asp32 and Gly34 residues of β-catenin. Oncogene 24: 2667-2676.
34. Rubinfeld B, Albert I, Porfiri E, Fiol C, Munemitsu S, Polakis P. 1996. Binding of GSK3β to the APC-β-catenin complex and regulation of complex assembly. Science 272: 1023-1026.
35. Sopko R, Silva E, Clayton L, Gardano L, Barrios-Rodiles M, Wrana J, Varelas X, Arbouzova NI, Shaw S, Saburi S, et al. 2009. Phosphorylation of the tumor suppressor fat is regulated by its ligand Dachsous and the kinase discs overgrown. Curr Biol 19: 1112-1117.
36. Steinhardt AA, Gayyed MF, Klein AP, Dong J, Maitra A, Pan D, Montgomery EA, Anders RA. 2008. Expression of Yes-associated protein in common solid tumors. Hum Pathol 39: 1582-1589.
37. Tapon N, Harvey KF, Bell DW, Wahrer DC, Schiripo TA, Haber DA, Hariharan IK. 2002. salvador Promotes both cell cycle exit and apoptosis in Drosophila and is mutated in human cancer cell lines. Cell 110: 467-478.
38. Udan RS, Kango-Singh M, Nolo R, Tao C, Halder G. 2003. Hippo promotes proliferation arrest and apoptosis in the Salvador/ Warts pathway. Nat Cell Biol 5: 914-920.
39. Westbrook TF, Hu G, Ang XL, Mulligan P, Pavlova NN, Liang A, Leng Y, Maehr R, Shi Y, Harper JW, et al. 2008. SCFβ-TRCP controls oncogenic transformation and neural differentiation through REST degradation. Nature 452: 370-374.
40. Wu G, He X. 2006. Threonine 41 in β-catenin serves as a key phosphorylation relay residue in β-catenin degradation. Biochemistry 45: 5319-5323.
41. Wu G, Xu G, Schulman BA, Jeffrey PD, Harper JW, Pavletich NP. 2003. Structure of a β-TrCP1-Skp1-β-catenin complex: Destruction motif binding and lysine specificity of the SCF(β-TrCP1) ubiquitin ligase. Mol Cell 11: 1445-1456.
42. Wu S, Huang J, Dong J, Pan D. 2003. hippo encodes a Ste-20 family protein kinase that restricts cell proliferation and promotes apoptosis in conjunction with salvador and warts. Cell 114: 445-456.
43. Zender L, Spector MS, Xue W, Flemming P, Cordon-Cardo C, Silke J, Fan ST, Luk JM, Wigler M, Hannon GJ, et al. 2006. Identification and validation of oncogenes in liver cancer using an integrative oncogenomic approach. Cell 125: 1253-1267.
44. Zeng Q, Hong W. 2008. The emerging role of the hippo pathway in cell contact inhibition, organ size control, and cancer development in mammals. Cancer Cell 13: 188-192.
45. Zhang J, Smolen GA, Haber DA. 2008. Negative regulation of YAP by LATS1 underscores evolutionary conservation of the Drosophila Hippo pathway. Cancer Res 68: 2789-2794.
46. Zhao B, Wei X, Li W, Udan RS, Yang Q, Kim J, Xie J, Ikenoue T, Yu J, Li L, et al. 2007. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes & Dev 21: 2747-2761.
47. Zhao B, Ye X, Yu J, Li L, Li W, Li S, Lin JD, Wang CY, Chinnaiyan AM, Lai ZC, et al. 2008. TEAD mediates YAP-dependent gene induction and growth control. Genes & Dev 22: 1962-1971.
48. Zhao B, Kim J, Ye X, Lai ZC, Guan KL. 2009. Both TEAD-binding and WW domains are required for the growth stimulation and oncogenic transformation activity of yes-associated protein. Cancer Res 69: 1089-1098.