SCFSlmb E3 ligase-mediated degradation of expanded is inhibited by the hippo pathway in Drosophila

Cell Research

Volumn 25, Issue 1, 2015, Pages 93-109

  Zhang, Hongtao ^a,b   Li, Changqing ^a   Chen, Hanqing ^a,b   Wei, Chuanxian ^a,b   Dai, Fei ^a,b   Wu, Honggang ^a,b   Dui, Wen ^a,b   Deng, Wu Min ^c   Jiao, Renjie ^a,d  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c FLORIDA STATE UNIVERSITY   (United States)

^d GUANGZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Drosophila; Expanded; Hippo pathway; SCFSlmb

Indexed keywords

ANIMALIA;

DROSOPHILA PROTEIN; EXPANDED PROTEIN, DROSOPHILA; HPO PROTEIN, DROSOPHILA; MEMBRANE PROTEIN; PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE; SIGNAL PEPTIDE; UBIQUITIN PROTEIN LIGASE; WARTS PROTEIN, DROSOPHILA;

ANIMAL; CELL LINE; DROSOPHILA; METABOLISM; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UBIQUITINATION;

ANIMALS; CELL LINE; DROSOPHILA; DROSOPHILA PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; PROTEIN INTERACTION MAPS; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; PROTEOLYSIS; SIGNAL TRANSDUCTION; SKP CULLIN F-BOX PROTEIN LIGASES; UBIQUITINATION;

EID: 84920273954     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2014.166     Document Type: Article

References (56)

1. Harvey KF, Pfleger CM, Hariharan IK. The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 2003; 114:457-467.
2. Udan RS, Kango-Singh M, Nolo R, Tao C, Halder G. Hippo promotes proliferation arrest and apoptosis in the Salvador/Warts pathway. Nat Cell Biol 2003; 5:914-920.
3. Wu S, Huang J, Dong J, Pan D. hippo encodes a Ste-20 family protein kinase that restricts cell proliferation and promotes apoptosis in conjunction with salvador and warts. Cell 2003; 114:445-456.
4. Lai ZC, Wei X, Shimizu T, et al. Control of cell proliferation and apoptosis by mob as tumor suppressor, mats. Cell 2005; 120:675-685.
5. Staley BK, Irvine KD. Hippo signaling in Drosophila: recent advances and insights. Dev Dyn 2012; 241:3-15.
6. Jia J, Zhang W, Wang B, Trinko R, Jiang J. The Drosophila Ste20 family kinase dMST functions as a tumor suppressor by restricting cell proliferation and promoting apoptosis. Genes Dev 2003; 17:2514-2519.
7. Pan D. The hippo signaling pathway in development and cancer. Dev Cell 2010; 19:491-505.
8. Harvey KF, Zhang X, Thomas DM. The Hippo pathway and human cancer. Nat Rev Cancer 2013; 13:246-257.
9. Yu FX, Guan KL. The Hippo pathway: regulators and regulations. Genes Dev 2013; 27:355-371.
10. Thompson BJ, Cohen SM. The Hippo pathway regulates the bantam microRNA to control cell proliferation and apoptosis in Drosophila. Cell 2006; 126:767-774.
11. Hamaratoglu F, Willecke M, Kango-Singh M, et al. The tumour-suppressor genes NF2/Merlin and Expanded act through Hippo signalling to regulate cell proliferation and apoptosis. Nat Cell Biol 2006; 8:27-36.
12. 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.
13. 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.
14. Yu J, Zheng Y, Dong J, et al. Kibra functions as a tumor suppressor protein that regulates Hippo signaling in conjunction with Merlin and Expanded. Dev Cell 2010; 18:288-299.
15. Boggiano JC, Fehon RG. Growth control by committee: intercellular junctions, cell polarity, and the cytoskeleton regulate Hippo signaling. Dev Cell 2012; 22:695-702.
16. Cho E, Feng Y, Rauskolb C, et al. Delineation of a Fat tumor suppressor pathway. Nat Genet 2006; 38:1142-1150.
17. Rauskolb C, Pan G, Reddy BV, Oh H, Irvine KD. Zyxin links fat signaling to the hippo pathway. PLoS Biol 2011; 9:e1000624.
18. Bennett FC, Harvey KF. Fat cadherin modulates organ size in Drosophila via the Salvador/Warts/Hippo signaling pathway. Curr Biol 2006; 16:2101-2110.
19. Silva E, Tsatskis Y, Gardano L, Tapon N, McNeill H. The tumor-suppressor gene fat controls tissue growth upstream of expanded in the hippo signaling pathway. Curr Biol 2006; 16:2081-2089.
20. Willecke M, Hamaratoglu F, Kango-Singh M, et al. The fat cadherin acts through the hippo tumor-suppressor pathway to regulate tissue size. Curr Biol 2006; 16:2090-2100.
21. Feng Y, Irvine KD. Fat and expanded act in parallel to regulate growth through warts. Proc Natl Acad Sci USA 2007; 104:20362-20367.
22. Chen CL, Gajewski KM, Hamaratoglu F, et al. The apical-basal cell polarity determinant Crumbs regulates Hippo signaling in Drosophila. Proc Natl Acad Sci USA 2010; 107:15810-15815.
23. Grzeschik NA, Parsons LM, Allott ML, Harvey KF, Richardson HE. Lgl, aPKC, and Crumbs regulate the Salvador/Warts/ Hippo pathway through two distinct mechanisms. Curr Biol 2010; 20:573-581.
24. Ling C, Zheng Y, Yin F, 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.
25. Robinson BS, Huang J, Hong Y, Moberg KH. Crumbs regulates Salvador/Warts/Hippo signaling in Drosophila via the FERM-domain protein Expanded. Curr Biol 2010; 20:582-590.
26. Yue T, Tian A, Jiang J. The cell adhesion molecule echinoid functions as a tumor suppressor and upstream regulator of the Hippo signaling pathway. Dev Cell 2012; 22:255-267.
27. Dui W, Lu W, Ma J, Jiao R. A systematic phenotypic screen of F-box genes through a tissue-specific RNAi-based approach in Drosophila. J Genet Genomics 2012; 39:397-413.
28. Rogers GC, Rusan NM, Roberts DM, Peifer M, Rogers SL. The SCF Slimb ubiquitin ligase regulates Plk4/Sak levels to block centriole reduplication. J Cell Biol 2009; 184:225-239.
29. Ho MS, Ou C, Chan YR, Chien CT, Pi H. The utility F-box for protein destruction. Cell Mol Life Sci 2008; 65:1977-2000.
30. Wu S, Liu Y, Zheng Y, Dong J, Pan D. The TEAD/TEF family protein Scalloped mediates transcriptional output of the Hippo growth-regulatory pathway. Dev Cell 2008; 14:388-398.
31. Miletich I, Limbourg-Bouchon B. Drosophila null slimb clones transiently deregulate Hedgehog-independent transcription of wingless in all limb discs, and induce decapentaplegic transcription linked to imaginal disc regeneration. Mech Dev 2000; 93:15-26.
32. Herranz H, Hong X, Cohen SM. Mutual repression by bantam miRNA and Capicua links the EGFR/MAPK and Hippo pathways in growth control. Curr Biol 2012; 22:651-657.
33. Oh H, Irvine KD. In vivo regulation of Yorkie phosphorylation and localization. Development 2008; 135:1081-1088.
34. Jiang J, Struhl G. Regulation of the Hedgehog and Wingless signalling pathways by the F-box/WD40-repeat protein Slimb. Nature 1998; 391:493-496.
35. McCartney BM, Kulikauskas RM, LaJeunesse DR, Fehon RG. The neurofibromatosis-2 homologue, Merlin, and the tumor suppressor expanded function together in Drosophila to regulate cell proliferation and differentiation. Development 2000; 127:1315-1324.
36. Clark HF, Brentrup D, Schneitz K, et al. Dachsous encodes a member of the cadherin superfamily that controls imaginal disc morphogenesis in Drosophila. Genes Dev 1995; 9:1530-1542.
37. Villano JL, Katz FN. four-jointed is required for intermediate growth in the proximal-distal axis in Drosophila. Development 1995; 121:2767-2777.
38. Brodsky MH, Steller H. Positional information along the dorsal-ventral axis of the Drosophila eye: graded expression of the four-jointed gene. Dev Biol 1996; 173:428-446.
39. Rogulja D, Rauskolb C, Irvine KD. Morphogen control of wing growth through the Fat signaling pathway. Dev Cell 2008; 15:309-321.
40. Zecca M, Struhl G. A feed-forward circuit linking wingless, fat-dachsous signaling, and the warts-hippo pathway to Drosophila wing growth. PLoS Biol 2010; 8:e1000386.
41. Schwank G, Tauriello G, Yagi R, et al. Antagonistic growth regulation by Dpp and Fat drives uniform cell proliferation. Dev Cell 2011; 20:123-130.
42. Simon MA, Xu A, Ishikawa HO, Irvine KD. Modulation of fat:dachsous binding by the cadherin domain kinase four-jointed. Curr Biol 2010; 20:811-817.
43. Ribeiro P, Holder M, Frith D, Snijders AP, Tapon N. Crumbs promotes expanded recognition and degradation by the SCFSlimb/beta-TrCP ubiquitin ligase. Proc Natl Acad Sci USA 2014; 111:E1980-E1989.
44. Liu CY, Zha ZY, Zhou X, et al. The hippo tumor pathway promotes TAZ degradation by phosphorylating a phosphodegron and recruiting the SCF{beta}-TrCP E3 ligase. J Biol Chem 2010; 285:37159-37169.
45. Zhao B, Li L, Tumaneng K, Wang CY, Guan KL. A coordinated phosphorylation by Lats and CK1 regulates YAP stability through SCF(beta-TRCP). Genes Dev 2010; 24:72-85.
46. Frescas D, Pagano M. Deregulated proteolysis by the F-box proteins SKP2 and beta-TrCP: tipping the scales of cancer. Nat Rev Cancer 2008; 8:438-449.
47. Fuchs SY, Spiegelman VS, Kumar KG. The many faces of beta-TrCP E3 ubiquitin ligases: reflections in the magic mirror of cancer. Oncogene 2004; 23:2028-2036.
48. Aza-Blanc P, Ramirez-Weber FA, Laget MP, Schwartz C, Kornberg TB. Proteolysis that is inhibited by hedgehog targets Cubitus interruptus protein to the nucleus and converts it to a repressor. Cell 1997; 89:1043-1053.
49. Valenta T, Hausmann G, Basler K. The many faces and functions of beta-catenin. EMBO J 2012; 31:2714-2736.
50. Genevet A, Polesello C, Blight K, et al. The Hippo pathway regulates apical-domain size independently of its growth-control function. J Cell Sci 2009; 122(Part 14):2360-2370.
51. Swarup S, Verheyen EM. Drosophila homeodomain-interacting protein kinase inhibits the Skp1-Cul1-F-box E3 ligase complex to dually promote Wingless and Hedgehog signaling. Proc Natl Acad Sci USA 2011; 108:9887-9892.
52. Xie G, Zhang H, Du G, et al. Uif, a large transmembrane protein with EGF-like repeats, can antagonize Notch signaling in Drosophila. PLoS One 2012; 7:e36362.
53. Boggiano JC, Vanderzalm PJ, Fehon RG. Tao-1 phosphorylates Hippo/MST kinases to regulate the Hippo-Salvador-Warts tumor suppressor pathway. Dev Cell 2011; 21:888-895.
54. Simcox A, Mitra S, Truesdell S, et al. Efficient genetic method for establishing Drosophila cell lines unlocks the potential to create lines of specific genotypes. PLoS Genet 2008; 4:e1000142.
55. Dui W, Wei B, He F, et al. The Drosophila F-box protein dSkp2 regulates cell proliferation by targeting Dacapo for degradation. Mol Biol Cell 2013; 24:1676-1687, S1-S7.
56. Li C, Andrake M, Dunbrack R, Enders GH. A bifunctional regulatory element in human somatic Wee1 mediates cyclin A/Cdk2 binding and Crm1-dependent nuclear export. Mol Cell Biol 2010; 30:116-130.