Identification of Happyhour/MAP4K as Alternative Hpo/Mst-like Kinases in the Hippo Kinase Cascade

Developmental Cell

Volumn 34, Issue 6, 2015, Pages 642-655

  Zheng, Yonggang ^a   Wang, Wei ^a   Liu, Bo ^a   Deng, Hua ^a   Uster, Eliza ^a   Pan, Duojia ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

HAPPYHOUR PROTEIN; HIPPO KINASE; MAP4K PROTEIN; MAP4K1 PROTEIN; MAP4K2 PROTEIN; MAP4K3 PROTEIN; MAP4K5 PROTEIN; PHOSPHOTRANSFERASE; TAZ PROTEIN; UNCLASSIFIED DRUG; WTS PROTEIN; YAP PROTEIN; YKI PROTEIN; CELL CYCLE PROTEIN; CYTOSKELETON PROTEIN; DROSOPHILA PROTEIN; HAPPYHOUR PROTEIN, DROSOPHILA; HPO PROTEIN, DROSOPHILA; MAP4K3 PROTEIN, DROSOPHILA; MESSENGER RNA; MST PROTEIN, DROSOPHILA; PROTEIN SERINE THREONINE KINASE; SIGNAL PEPTIDE;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTACT INHIBITION; CONTROLLED STUDY; CYTOPLASM; DROSOPHILA; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HYDROPHOBICITY; IMAGINAL DISC; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; REGULATORY MECHANISM; ANIMAL; CELL CULTURE; DROSOPHILA MELANOGASTER; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANIMALS; CELL CYCLE PROTEINS; CELLS, CULTURED; CYTOSKELETAL PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; IMAGINAL DISCS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84942550443     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.08.014     Document Type: Article

References (64)

1. Aragona M., Panciera T., Manfrin A., Giulitti S., Michielin F., Elvassore N., Dupont S., Piccolo S. A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 2013, 154:1047-1059.
2. Barry E.R., Camargo F.D. The Hippo superhighway: signaling crossroads converging on the Hippo/Yap pathway in stem cells and development. Curr. Opin. Cell Biol. 2013, 25:247-253.
3. Boggiano J.C., Fehon R.G. Growth control by committee: intercellular junctions, cell polarity, and the cytoskeleton regulate Hippo signaling. Dev. Cell 2012, 22:695-702.
4. Boggiano J.C., Vanderzalm P.J., Fehon R.G. Tao-1 phosphorylates Hippo/MST kinases to regulate the Hippo-Salvador-Warts tumor suppressor pathway. Dev. Cell 2011, 21:888-895.
5. Bryk B., Hahn K., Cohen S.M., Teleman A.A. MAP4K3 regulates body size and metabolism in Drosophila. Dev. Biol. 2010, 344:150-157.
6. Chan E.H., Nousiainen M., Chalamalasetty R.B., Schäfer A., Nigg E.A., Silljé H.H. The Ste20-like kinase Mst2 activates the human large tumor suppressor kinase Lats1. Oncogene 2005, 24:2076-2086.
7. Cho E., Feng Y., Rauskolb C., Maitra S., Fehon R., Irvine K.D. Delineation of a Fat tumor suppressor pathway. Nat. Genet. 2006, 38:1142-1150.
8. Corl A.B., Berger K.H., Ophir-Shohat G., Gesch J., Simms J.A., Bartlett S.E., Heberlein U. Happyhour, a Ste20 family kinase, implicates EGFR signaling in ethanol-induced behaviors. Cell 2009, 137:949-960.
9. Dong J., Feldmann G., Huang J., Wu S., Zhang N., Comerford S.A., Gayyed M.F., Anders R.A., Maitra A., Pan D. Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 2007, 130:1120-1133.
10. Duan R., Jin P., Luo F., Zhang G., Anderson N., Chen E.H. Group I PAKs function downstream of Rac to promote podosome invasion during myoblast fusion in vivo. J. Cell Biol. 2012, 199:169-185.
11. Dupont S., Morsut L., Aragona M., Enzo E., Giulitti S., Cordenonsi M., Zanconato F., Le Digabel J., Forcato M., Bicciato S., et al. Role of YAP/TAZ in mechanotransduction. Nature 2011, 474:179-183.
12. Enderle L., McNeill H. Hippo gains weight: added insights and complexity to pathway control. Sci. Signal. 2013, 6:re7.
13. Findlay G.M., Yan L., Procter J., Mieulet V., Lamb R.F. A MAP4 kinase related to Ste20 is a nutrient-sensitive regulator of mTOR signalling. Biochem. J. 2007, 403:13-20.
14. Gaspar P., Tapon N. Sensing the local environment: actin architecture and Hippo signalling. Curr. Opin. Cell Biol. 2014, 31:74-83.
15. Gratz S.J., Ukken F.P., Rubinstein C.D., Thiede G., Donohue L.K., Cummings A.M., O'Connor-Giles K.M. Highly specific and efficient CRISPR/Cas9-catalyzed homology-directed repair in Drosophila. Genetics 2014, 196:961-971.
16. Halder G., Johnson R.L. Hippo signaling: growth control and beyond. Development 2011, 138:9-22.
17. Halder G., Dupont S., Piccolo S. Transduction of mechanical and cytoskeletal cues by YAP and TAZ. Nat. Rev. Mol. Cell Biol. 2012, 13:591-600.
18. Harvey K., Tapon N. The Salvador-Warts-Hippo pathway-an emerging tumour-suppressor network. Nat. Rev. Cancer 2007, 7:182-191.
19. Harvey K.F., Pfleger C.M., Hariharan I.K. The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 2003, 114:457-467.
20. Harvey K.F., Zhang X., Thomas D.M. The Hippo pathway and human cancer. Nat. Rev. Cancer 2013, 13:246-257.
21. Hergovich A., Stegert M.R., Schmitz D., Hemmings B.A. NDR kinases regulate essential cell processes from yeast to humans. Nat. Rev. Mol. Cell Biol. 2006, 7:253-264.
22. Hergovich A., Kohler R.S., Schmitz D., Vichalkovski A., Cornils H., Hemmings B.A. The MST1 and hMOB1 tumor suppressors control human centrosome duplication by regulating NDR kinase phosphorylation. Curr. Biol. 2009, 19:1692-1702.
23. Hu L., Huang H., Li J., Yin M.X., Lu Y., Wu W., Zeng R., Jiang J., Zhao Y., Zhang L. Drosophila casein kinase 2 (CK2) promotes warts protein to suppress Yorkie protein activity for growth control. J. Biol. Chem. 2014, 289:33598-33607.
24. Huang J., Wu S., Barrera J., Matthews K., Pan D. The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila Homolog of YAP. Cell 2005, 122:421-434.
25. Johnson R., Halder G. The two faces of Hippo: targeting the Hippo pathway for regenerative medicine and cancer treatment. Nat. Rev. Drug Discov. 2014, 13:63-79.
26. Justice R.W., Zilian O., Woods D.F., Noll M., 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. 1995, 9:534-546.
27. Kango-Singh M., Nolo R., Tao C., Verstreken P., Hiesinger P.R., Bellen H.J., Halder G. Shar-pei mediates cell proliferation arrest during imaginal disc growth in Drosophila. Development 2002, 129:5719-5730.
28. Kim M., Kim M., Lee S., Kuninaka S., Saya H., Lee H., Lee S., Lim D.S. cAMP/PKA signalling reinforces the LATS-YAP pathway to fully suppress YAP in response to actin cytoskeletal changes. EMBO J. 2013, 32:1543-1555.
29. Koontz L.M., Liu-Chittenden Y., Yin F., Zheng Y., Yu J., Huang B., Chen Q., Wu S., Pan D. The Hippo effector Yorkie controls normal tissue growth by antagonizing scalloped-mediated default repression. Dev. Cell 2013, 25:388-401.
30. Lai Z.C., Wei X., Shimizu T., Ramos E., Rohrbaugh M., Nikolaidis N., Ho L.L., Li Y. Control of cell proliferation and apoptosis by mob as tumor suppressor, mats. Cell 2005, 120:675-685.
31. Lam D., Shah S., de Castro I.P., Loh S.H., Martins L.M. Drosophila happyhour modulates JNK-dependent apoptosis. Cell Death Dis. 2010, 1:e66.
32. Li Q., Li S., Mana-Capelli S., Roth Flach R.J., Danai L.V., Amcheslavsky A., Nie Y., Kaneko S., Yao X., Chen X., et al. The conserved misshapen-warts-Yorkie pathway acts in enteroblasts to regulate intestinal stem cells in Drosophila. Dev. Cell 2014, 31:291-304.
33. Li W., Cooper J., Zhou L., Yang C., Erdjument-Bromage H., Zagzag D., Snuderl M., Ladanyi M., Hanemann C.O., Zhou P., et al. Merlin/NF2 loss-driven tumorigenesis linked to CRL4(DCAF1)-mediated inhibition of the hippo pathway kinases Lats1 and 2 in the nucleus. Cancer Cell 2014, 26:48-60.
34. Low B.C., Pan C.Q., Shivashankar G.V., Bershadsky A., Sudol M., Sheetz M. YAP/TAZ as mechanosensors and mechanotransducers in regulating organ size and tumor growth. FEBS Lett. 2014, 588:2663-2670.
35. Manning G., Whyte D.B., Martinez R., Hunter T., Sudarsanam S. The protein kinase complement of the human genome. Science 2002, 298:1912-1934.
36. Miralles F., Visa N. Actin in transcription and transcription regulation. Curr. Opin. Cell Biol. 2006, 18:261-266.
37. Miyamoto K., Gurdon J.B. Transcriptional regulation and nuclear reprogramming: roles of nuclear actin and actin-binding proteins. Cell. Mol. Life Sci. 2013, 70:3289-3302.
38. Olson E.N., Nordheim A. Linking actin dynamics and gene transcription to drive cellular motile functions. Nat. Rev. Mol. Cell Biol. 2010, 11:353-365.
39. Pan D. Hippo signaling in organ size control. Genes Dev. 2007, 21:886-897.
40. Pan D. The hippo signaling pathway in development and cancer. Dev. Cell 2010, 19:491-505.
41. Pantalacci S., Tapon N., Léopold P. The Salvador partner Hippo promotes apoptosis and cell-cycle exit in Drosophila. Nat. Cell Biol. 2003, 5:921-927.
42. Poon C.L., Lin J.I., Zhang X., Harvey K.F. The sterile 20-like kinase Tao-1 controls tissue growth by regulating the Salvador-Warts-Hippo pathway. Dev. Cell 2011, 21:896-906.
43. Port F., Chen H.M., Lee T., Bullock S.L. Optimized CRISPR/Cas tools for efficient germline and somatic genome engineering in Drosophila. Proc. Natl. Acad. Sci. USA 2014, 111:E2967-E2976.
44. Praskova M., Xia F., Avruch J. MOBKL1A/MOBKL1B phosphorylation by MST1 and MST2 inhibits cell proliferation. Curr. Biol. 2008, 18:311-321.
45. Rauskolb C., Sun S., Sun G., Pan Y., Irvine K.D. Cytoskeletal tension inhibits Hippo signaling through an Ajuba-Warts complex. Cell 2014, 158:143-156.
46. Resnik-Docampo M., de Celis J.F. MAP4K3 is a component of the TORC1 signalling complex that modulates cell growth and viability in Drosophila melanogaster. PLoS ONE 2011, 6:e14528.
47. Stegert M.R., Hergovich A., Tamaskovic R., Bichsel S.J., Hemmings B.A. Regulation of NDR protein kinase by hydrophobic motif phosphorylation mediated by the mammalian Ste20-like kinase MST3. Mol. Cell. Biol. 2005, 25:11019-11029.
48. Suzuki K., Bose P., Leong-Quong R.Y., Fujita D.J., Riabowol K. REAP: A two minute cell fractionation method. BMC Res. Notes 2010, 3:294.
49. Tapon N., Harvey K.F., Bell D.W., Wahrer D.C., Schiripo T.A., Haber D., Hariharan I.K. salvador Promotes both cell cycle exit and apoptosis in Drosophila and is mutated in human cancer cell lines. Cell 2002, 110:467-478.
50. Udan R.S., 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.
51. Varelas X., Samavarchi-Tehrani P., Narimatsu M., Weiss A., Cockburn K., Larsen B.G., Rossant J., Wrana J.L. The Crumbs complex couples cell density sensing to Hippo-dependent control of the TGF-β-SMAD pathway. Dev. Cell 2010, 19:831-844.
52. Wada K., Itoga K., Okano T., Yonemura S., Sasaki H. Hippo pathway regulation by cell morphology and stress fibers. Development 2011, 138:3907-3914.
53. Wei X., Shimizu T., Lai Z.C. Mob as tumor suppressor is activated by Hippo kinase for growth inhibition in Drosophila. EMBO J. 2007, 26:1772-1781.
54. 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.
55. Xu T., Wang W., Zhang S., Stewart R.A., Yu W. Identifying tumor suppressors in genetic mosaics: the Drosophila lats gene encodes a putative protein kinase. Development 1995, 121:1053-1063.
56. Yin F., Yu J., Zheng Y., Chen Q., Zhang N., Pan D. Spatial organization of Hippo signaling at the plasma membrane mediated by the tumor suppressor Merlin/NF2. Cell 2013, 154:1342-1355.
57. Yu F.X., Guan K.L. The Hippo pathway: regulators and regulations. Genes Dev. 2013, 27:355-371.
58. Yu J., Zheng Y., Dong J., Klusza S., Deng W.M., 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.
59. Yu F.X., Zhao B., Panupinthu N., Jewell J.L., Lian I., Wang L.H., Zhao J., Yuan H., Tumaneng K., Li H., et al. Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell 2012, 150:780-791.
60. Zhang L., Tang F., Terracciano L., Hynx D., Kohler R., Bichet S., Hess D., Cron P., Hemmings B.A., Hergovich A., Schmitz-Rohmer D. NDR functions as a physiological YAP1 kinase in the intestinal epithelium. Curr. Biol. 2015, 25:296-305.
61. 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. 2007, 21:2747-2761.
62. Zhao B., Lei Q.Y., Guan K.L. The Hippo-YAP pathway: new connections between regulation of organ size and cancer. Curr. Opin. Cell Biol. 2008, 20:638-646.
63. Zhao B., Li L., Wang L., Wang C.Y., Yu J., Guan K.L. Cell detachment activates the Hippo pathway via cytoskeleton reorganization to induce anoikis. Genes Dev. 2012, 26:54-68.
64. Zhou D., Conrad C., Xia F., Park J.S., Payer B., Yin Y., Lauwers G.Y., Thasler W., Lee J.T., Avruch J., Bardeesy N. Mst1 and Mst2 maintain hepatocyte quiescence and suppress hepatocellular carcinoma development through inactivation of the Yap1 oncogene. Cancer Cell 2009, 16:425-438.