Kibra Functions as a Tumor Suppressor Protein that Regulates Hippo Signaling in Conjunction with Merlin and Expanded

Developmental Cell

Volumn 18, Issue 2, 2010, Pages 288-299

  Yu, Jianzhong ^a,b   Zheng, Yonggang ^b   Dong, Jixin ^b   Klusza, Stephen ^a   Deng, Wu Min ^a   Pan, Duojia ^b  

^a FLORIDA STATE UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CELLCYCLE; DEVBIO; SIGNALING

Indexed keywords

EXPANDED PROTEIN; HIPPO KINASE; KIBRA PROTEIN; MEMBRANE PROTEIN; MERLIN; SALVADOR PROTEIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL STRAIN HEK293; COMPLEX FORMATION; CONTROLLED STUDY; DROSOPHILA; EPITHELIUM CELL; HUMAN; HUMAN CELL; INSECT CELL; NEUROFIBROMATOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL LINE; CELL POLARITY; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; GENES, INSECT; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MULTIPROTEIN COMPLEXES; NEUROFIBROMIN 2; NUCLEAR PROTEINS; OOCYTES; PROTEIN-SERINE-THREONINE KINASES; PROTEINS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TUMOR SUPPRESSOR PROTEINS;

MAMMALIA;

EID: 76249109900     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2009.12.012     Document Type: Article

References (65)

1. Badouel C., Gardano L., Amin N., Garg A., Rosenfeld R., Le B.T., and McNeill H. The FERM-domain protein expanded regulates Hippo pathway activity via direct interactions with the transcriptional activator Yorkie. Dev. Cell 16 (2009) 411-420
2. Bennett F.C., and Harvey K.F. Fat cadherin modulates organ size in Drosophila via the Salvador/Warts/Hippo signaling pathway. Curr. Biol. 16 (2006) 2101-2110
3. Boedigheimer M., and Laughon A. Expanded: a gene involved in the control of cell proliferation in imaginal discs. Development 118 (1993) 1291-1301
4. Camargo F.D., Gokhale S., Johnnidis J.B., Fu D., Bell G.W., Jaenisch R., and Brummelkamp T.R. YAP1 increases organ size and expands undifferentiated progenitor cells. Curr. Biol. 17 (2007) 2054-2060
5. Casal J., Lawrence P.A., and Struhl G. Two separate molecular systems, Dachsous/Fat and Starry night/Frizzled, act independently to confer planar cell polarity. Development 133 (2006) 4561-4572
6. Chan E.H., Nousiainen M., Chalamalasetty R.B., Schafer A., Nigg E.A., and Sillje H.H. The Ste20-like kinase Mst2 activates the human large tumor suppressor kinase Lats1. Oncogene 24 (2005) 2076-2086
7. Cho E., Feng Y., Rauskolb C., Maitra S., Fehon R., and Irvine K.D. Delineation of a Fat tumor suppressor pathway. Nat. Genet. 38 (2006) 1142-1150
8. Colombani J., Polesello C., Josue F., and Tapon N. Dmp53 activates the Hippo pathway to promote cell death in response to DNA damage. Curr. Biol. 16 (2006) 1453-1458
9. de Celis J.F., Tyler D.M., de Celis J., and Bray S.J. Notch signalling mediates segmentation of the Drosophila leg. Development 125 (1998) 4617-4626
10. Dong J., Feldmann G., Huang J., Wu S., Zhang N., Comerford S.A., Gayyed M.F., Anders R.A., Maitra A., and Pan D. Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 130 (2007) 1120-1133
11. Duning K., Schurek E.M., Schluter M., Bayer M., Reinhardt H.C., Schwab A., Schaefer L., Benzing T., Schermer B., Saleem M.A., et al. KIBRA modulates directional migration of podocytes. J. Am. Soc. Nephrol. 19 (2008) 1891-1903
12. Emoto K., Parrish J.Z., Jan L.Y., and Jan Y.N. The tumour suppressor Hippo acts with the NDR kinases in dendritic tiling and maintenance. Nature 443 (2006) 210-213
13. Formstecher E., Aresta S., Collura V., Hamburger A., Meil A., Trehin A., Reverdy C., Betin V., Maire S., Brun C., et al. Protein interaction mapping: a Drosophila case study. Genome Res. 15 (2005) 376-384
14. Gao X., and Pan D. TSC1 and TSC2 tumor suppressors antagonize insulin signaling in cell growth. Genes Dev. 15 (2001) 1383-1392
15. Gosens I., Sessa A., den Hollander A.I., Letteboer S.J., Belloni V., Arends M.L., Le B.A., Cremers F.P., Broccoli V., and Roepman R. FERM protein EPB41L5 is a novel member of the mammalian CRB-MPP5 polarity complex. Exp. Cell Res. 313 (2007) 3959-3970
16. Goulev Y., Fauny J.D., Gonzalez-Marti B., Flagiello D., Silber J., and Zider A. SCALLOPED interacts with YORKIE, the nuclear effector of the hippo tumor-suppressor pathway in Drosophila. Curr. Biol. 18 (2008) 435-441
17. Hamaratoglu F., Willecke M., Kango-Singh M., Nolo R., Hyun E., Tao C., Jafar-Nejad H., and Halder G. The tumour-suppressor genes NF2/Merlin and Expanded act through Hippo signalling to regulate cell proliferation and apoptosis. Nat. Cell Biol. 8 (2006) 27-36
18. Harvey K.F., Pfleger C.M., and Hariharan I.K. The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 114 (2003) 457-467
19. Hay B.A., Wolff T., and Rubin G.M. Expression of baculovirus P35 prevents cell death in Drosophila. Development 120 (1994) 2121-2129
20. Hergovich A., Bichsel S.J., and Hemmings B.A. Human NDR kinases are rapidly activated by MOB proteins through recruitment to the plasma membrane and phosphorylation. Mol. Cell. Biol. 25 (2005) 8259-8272
21. Hilton H.N., Stanford P.M., Harris J., Oakes S.R., Kaplan W., Daly R.J., and Ormandy C.J. KIBRA interacts with discoidin domain receptor 1 to modulate collagen-induced signalling. Biochim. Biophys. Acta 1783 (2008) 383-393
22. Huang J., Wu S., Barrera J., Matthews K., and Pan D. The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila Homolog of YAP. Cell 122 (2005) 421-434
23. Jia J., Zhang W., Wang B., Trinko R., and Jiang J. The Drosophila Ste20 family kinase dMST functions as a tumor suppressor by restricting cell proliferation and promoting apoptosis. Genes Dev. 17 (2003) 2514-2519
24. Justice R.W., Zilian O., Woods D.F., Noll M., and Bryant P.J. The Drosophila tumor suppressor gene warts encodes a homolog of human myotonic dystrophy kinase and is required for the control of cell shape and proliferation. Genes Dev. 9 (1995) 534-546
25. Kango-Singh M., Nolo R., Tao C., Verstreken P., Hiesinger P.R., Bellen H.J., and Halder G. Shar-pei mediates cell proliferation arrest during imaginal disc growth in Drosophila. Development 129 (2002) 5719-5730
26. Kremerskothen J., Plaas C., Buther K., Finger I., Veltel S., Matanis T., Liedtke T., and Barnekow A. Characterization of KIBRA, a novel WW domain-containing protein. Biochem. Biophys. Res. Commun. 300 (2003) 862-867
27. Lai Z.C., Wei X., Shimizu T., Ramos E., Rohrbaugh M., Nikolaidis N., Ho L.L., and Li Y. Control of cell proliferation and apoptosis by Mob as tumor suppressor, Mats. Cell 120 (2005) 675-685
28. Maitra S., Kulikauskas R.M., Gavilan H., and Fehon R.G. The tumor suppressors Merlin and Expanded function cooperatively to modulate receptor endocytosis and signaling. Curr. Biol. 16 (2006) 702-709
29. Matakatsu H., and Blair S.S. Separating the adhesive and signaling functions of the Fat and Dachsous protocadherins. Development 133 (2006) 2315-2324
30. McCartney B.M., Kulikauskas R.M., LaJeunesse D.R., and Fehon R.G. The neurofibromatosis-2 homologue, Merlin, and the tumor suppressor expanded function together in Drosophila to regulate cell proliferation and differentiation. Development 127 (2000) 1315-1324
31. McClatchey A.I., and Giovannini M. Membrane organization and tumorigenesis-the NF2 tumor suppressor, Merlin. Genes Dev. 19 (2005) 2265-2277
32. Meignin C., Alvarez-Garcia I., Davis I., and Palacios I.M. The salvador-warts-hippo pathway is required for epithelial proliferation and axis specification in Drosophila. Curr. Biol. 17 (2007) 1871-1878
33. Mikeladze-Dvali T., Wernet M.F., Pistillo D., Mazzoni E.O., Teleman A.A., Chen Y.W., Cohen S., and Desplan C. The growth regulators warts/lats and melted interact in a bistable loop to specify opposite fates in Drosophila R8 photoreceptors. Cell 122 (2005) 775-787
34. Nolo R., Morrison C.M., Tao C., Zhang X., and Halder G. The bantam microRNA is a target of the hippo tumor-suppressor pathway. Curr. Biol. 16 (2006) 1895-1904
35. Oh H., and Irvine K.D. In vivo regulation of Yorkie phosphorylation and localization. Development 135 (2008) 1081-1088
36. Ohnishi S., Guntert P., Koshiba S., Tomizawa T., Akasaka R., Tochio N., Sato M., Inoue M., Harada T., Watanabe S., et al. Solution structure of an atypical WW domain in a novel beta-clam-like dimeric form. FEBS Lett. 581 (2007) 462-468
37. Okada T., You L., and Giancotti F.G. Shedding light on Merlin's wizardry. Trends Cell Biol. 17 (2007) 222-229
38. Pantalacci S., Tapon N., and Leopold P. The Salvador partner Hippo promotes apoptosis and cell-cycle exit in Drosophila. Nat. Cell Biol. 5 (2003) 921-927
39. Papassotiropoulos A., Stephan D.A., Huentelman M.J., Hoerndli F.J., Craig D.W., Pearson J.V., Huynh K.D., Brunner F., Corneveaux J., Osborne D., et al. Common Kibra alleles are associated with human memory performance. Science 314 (2006) 475-478
40. Parks A.L., Cook K.R., Belvin M., Dompe N.A., Fawcett R., Huppert K., Tan L.R., Winter C.G., Bogart K.P., Deal J.E., et al. Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat. Genet. 36 (2004) 288-292
41. Pellock B.J., Buff E., White K., and Hariharan I.K. The Drosophila tumor suppressors Expanded and Merlin differentially regulate cell cycle exit, apoptosis, and Wingless signaling. Dev. Biol. 304 (2006) 102-115
42. Polesello C., and Tapon N. Salvador-warts-hippo signaling promotes Drosophila posterior follicle cell maturation downstream of notch. Curr. Biol. 17 (2007) 1864-1870
43. Praskova M., Xia F., and Avruch J. MOBKL1A/MOBKL1B phosphorylation by MST1 and MST2 inhibits cell proliferation. Curr. Biol. 18 (2008) 311-321
44. Rayala S.K., den Hollander P., Manavathi B., Talukder A.H., Song C., Peng S., Barnekow A., Kremerskothen J., and Kumar R. Essential role of KIBRA in co-activator function of dynein light chain 1 in mammalian cells. J. Biol. Chem. 281 (2006) 19092-19099
45. Rogulja D., Rauskolb C., and Irvine K.D. Morphogen control of wing growth through the Fat signaling pathway. Dev. Cell 15 (2008) 309-321
46. Scheel H., and Hofmann K. A novel interaction motif, SARAH, connects three classes of tumor suppressor. Curr. Biol. 13 (2003) R899-R900
47. Silva E., Tsatskis Y., Gardano L., Tapon N., and McNeill H. The tumor-suppressor gene fat controls tissue growth upstream of expanded in the hippo signaling pathway. Curr. Biol. 16 (2006) 2081-2089
48. Sun J., and Deng W.M. Notch-dependent downregulation of the homeodomain gene cut is required for the mitotic cycle/endocycle switch and cell differentiation in Drosophila follicle cells. Development 132 (2005) 4299-4308
49. Sun J., and Deng W.M. Hindsight mediates the role of notch in suppressing hedgehog signaling and cell proliferation. Dev. Cell 12 (2007) 431-442
50. Tapon N., Harvey K.F., Bell D.W., Wahrer D.C., Schiripo T.A., Haber D.A., and Hariharan I.K. salvador promotes both cell cycle exit and apoptosis in Drosophila and is mutated in human cancer cell lines. Cell 110 (2002) 467-478
51. Thompson B.J., and Cohen S.M. The Hippo pathway regulates the bantam microRNA to control cell proliferation and apoptosis in Drosophila. Cell 126 (2006) 767-774
52. Tyler D.M., and Baker N.E. Expanded and fat regulate growth and differentiation in the Drosophila eye through multiple signaling pathways. Dev. Biol. 305 (2007) 187-201
53. Udan R.S., Kango-Singh M., Nolo R., Tao C., and Halder G. Hippo promotes proliferation arrest and apoptosis in the Salvador/Warts pathway. Nat. Cell Biol. 5 (2003) 914-920
54. Verdu J., Buratovich M.A., Wilder E.L., and Birnbaum M.J. Cell-autonomous regulation of cell and organ growth in Drosophila by Akt/PKB. Nat. Cell Biol. 1 (1999) 500-506
55. Wei X., Shimizu T., and Lai Z.C. Mob as tumor suppressor is activated by Hippo kinase for growth inhibition in Drosophila. EMBO J. 26 (2007) 1772-1781
56. Willecke M., Hamaratoglu F., Kango-Singh M., Udan R., Chen C.L., Tao C., Zhang X., and Halder G. The fat cadherin acts through the hippo tumor-suppressor pathway to regulate tissue size. Curr. Biol. 16 (2006) 2090-2100
57. Willecke M., Hamaratoglu F., Sansores-Garcia L., Tao C., and Halder G. Boundaries of Dachsous Cadherin activity modulate the Hippo signaling pathway to induce cell proliferation. Proc. Natl. Acad. Sci. USA 105 (2008) 14897-14902
58. Wu S., Huang J., Dong J., and Pan D. hippo encodes a Ste-20 family protein kinase that restricts cell proliferation and promotes apoptosis in conjunction with salvador and warts. Cell 114 (2003) 445-456
59. Wu S., Liu Y., Zheng Y., Dong J., and Pan D. The TEAD/TEF family protein Scalloped mediates transcriptional output of the Hippo growth-regulatory pathway. Dev. Cell 14 (2008) 388-398
60. Xu T., Wang W., Zhang S., Stewart R.A., and Yu W. Identifying tumor suppressors in genetic mosaics: the Drosophila lats gene encodes a putative protein kinase. Development 121 (1995) 1053-1063
61. Yang C.H., Axelrod J.D., and Simon M.A. Regulation of Frizzled by fat-like cadherins during planar polarity signaling in the Drosophila compound eye. Cell 108 (2002) 675-688
62. Yu J., Poulton J., Huang Y.C., and Deng W.M. The hippo pathway promotes Notch signaling in regulation of cell differentiation, proliferation, and oocyte polarity. PLoS ONE 3 (2008) e1761
63. Zhang L., Ren F., Zhang Q., Chen Y., Wang B., and Jiang J. The TEAD/TEF family of transcription factor Scalloped mediates Hippo signaling in organ size control. Dev. Cell 14 (2008) 377-387
64. Zhao B., Wei X., Li W., Udan R.S., Yang Q., Kim J., Xie J., Ikenoue T., Yu J., Li L., et al. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev. 21 (2007) 2747-2761
65. Zhou D., Conrad C., Xia F., Park J.S., Payer B., Yin Y., Lauwers G.Y., Thasler W., Lee J.T., Avruch J., and Bardeesy N. Mst1 and Mst2 maintain hepatocyte quiescence and suppress hepatocellular carcinoma development through inactivation of the Yap1 oncogene. Cancer Cell 16 (2009) 425-438