Yap1 acts downstream of α-catenin to control epidermal proliferation

Cell

Volumn 144, Issue 5, 2011, Pages 782-795

  Schlegelmilch, Karin ^a,b,c,d   Mohseni, Morvarid ^a,b,c   Kirak, Oktay ^e   Pruszak, Jan ^c,e   Rodriguez, J Renato ^e   Zhou, Dawang ^f   Kreger, Bridget T ^g   Vasioukhin, Valera ^g   Avruch, Joseph ^f   Brummelkamp, Thijn R ^e   Camargo, Fernando D ^a,b,c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b Harvard University   (United States)

^c HARVARD STEM CELL INSTITUTE   (United States)

^d FREIE UNIVERSITÄT BERLIN   (Germany)

^e WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^f MASSACHUSETTS GENERAL HOSPITAL   (United States)

^g Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CATENIN; CELL PROTEIN; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN 14 3 3; PROTEIN HIPPO; TRANSCRIPTION FACTOR YAP1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CELL DENSITY; CELL PROLIFERATION; CELL REGENERATION; EPIDERMIS; EPIDERMIS CELL; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SKIN EXPANSION; SQUAMOUS CELL CARCINOMA; STEM CELL; STEM CELL EXPANSION; TISSUE EXPANSION;

MAMMALIA;

EID: 79952298459     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2011.02.031     Document Type: Article

References (58)

1. R. Baumgartner, I. Poernbacher, N. Buser, E. Hafen, and H. Stocker The WW domain protein Kibra acts upstream of Hippo in Drosophila Dev. Cell 18 2010 309 316
2. G. Belteki, J. Haigh, N. Kabacs, K. Haigh, K. Sison, F. Costantini, J. Whitsett, S.E. Quaggin, and A. Nagy Conditional and inducible transgene expression in mice through the combinatorial use of Cre-mediated recombination and tetracycline induction Nucleic Acids Res. 33 2005 e51
3. J.M. Benjamin, and W.J. Nelson Bench to bedside and back again: molecular mechanisms of alpha-catenin function and roles in tumorigenesis Semin. Cancer Biol. 18 2008 53 64 (Pubitemid 350266369)
4. J. Cai, N. Zhang, Y. Zheng, R.F. de Wilde, A. Maitra, and D. Pan The Hippo signaling pathway restricts the oncogenic potential of an intestinal regeneration program Genes Dev. 24 2010 2383 2388
5. F.D. Camargo, S. Gokhale, J.B. Johnnidis, D. Fu, G.W. Bell, R. Jaenisch, and T.R. Brummelkamp YAP1 increases organ size and expands undifferentiated progenitor cells Curr. Biol. 17 2007 2054 2060 (Pubitemid 350180465)
6. C.L. Chen, K.M. Gajewski, F. Hamaratoglu, W. Bossuyt, L. Sansores-Garcia, C. Tao, and G. Halder The apical-basal cell polarity determinant Crumbs regulates Hippo signaling in Drosophila Proc. Natl. Acad. Sci. USA 107 2010 15810 15815
7. C.W. Chiang, C. Kanies, K.W. Kim, W.B. Fang, C. Parkhurst, M. Xie, T. Henry, and E. Yang Protein phosphatase 2A dephosphorylation of phosphoserine 112 plays the gatekeeper role for BAD-mediated apoptosis Mol. Cell. Biol. 23 2003 6350 6362 (Pubitemid 37075749)
8. M. Das Thakur, Y. Feng, R. Jagannathan, M.J. Seppa, J.B. Skeath, and G.D. Longmore Ajuba LIM proteins are negative regulators of the Hippo signaling pathway Curr. Biol. 20 2010 657 662
9. H.R. Dassule, P. Lewis, M. Bei, R. Maas, and A.P. McMahon Sonic hedgehog regulates growth and morphogenesis of the tooth Development 127 2000 4775 4785
10. E. Dellambra, O. Golisano, S. Bondanza, E. Siviero, P. Lacal, M. Molinari, S. D'Atri, and M. De Luca Downregulation of 14-3-3sigma prevents clonal evolution and leads to immortalization of primary human keratinocytes J. Cell Biol. 149 2000 1117 1130
11. V. Depaepe, N. Suarez-Gonzalez, A. Dufour, L. Passante, J.A. Gorski, K.R. Jones, C. Ledent, and P. Vanderhaeghen Ephrin signalling controls brain size by regulating apoptosis of neural progenitors Nature 435 2005 1244 1250 (Pubitemid 40943090)
12. J. Dong, G. Feldmann, J. Huang, S. Wu, N. Zhang, S.A. Comerford, M.F. Gayyed, R.A. Anders, A. Maitra, and D. Pan Elucidation of a universal size-control mechanism in Drosophila and mammals Cell 130 2007 1120 1133 (Pubitemid 47410268)
13. E. Fuchs Scratching the surface of skin development Nature 445 2007 834 842
14. A. Genevet, M.C. Wehr, R. Brain, B.J. Thompson, and N. Tapon Kibra is a regulator of the Salvador/Warts/Hippo signaling network Dev. Cell 18 2010 300 308
15. A.B. Gladden, A.M. Hebert, E.E. Schneeberger, and A.I. McClatchey The NF2 tumor suppressor, Merlin, regulates epidermal development through the establishment of a junctional polarity complex Dev. Cell 19 2010 727 739
16. N.A. Grzeschik, L.M. Parsons, M.L. Allott, K.F. Harvey, and H.E. Richardson Lgl, aPKC, and Crumbs regulate the Salvador/Warts/Hippo pathway through two distinct mechanisms Curr. Biol. 20 2010 573 581
17. F. Hamaratoglu, M. Willecke, M. Kango-Singh, R. Nolo, E. Hyun, C. Tao, H. Jafar-Nejad, and G. Halder 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 (Pubitemid 43064794)
18. I.K. Hariharan Growth regulation: a beginning for the hippo pathway Curr. Biol. 16 2006 R1037 R1039
19. K. Harvey, and N. Tapon The Salvador-Warts-Hippo pathway - an emerging tumour-suppressor network Nat. Rev. Cancer 7 2007 182 191
20. K.F. Harvey, C.M. Pfleger, and I.K. Hariharan The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis Cell 114 2003 457 467 (Pubitemid 37100994)
21. B.J. Herron, R.A. Liddell, A. Parker, S. Grant, J. Kinne, J.K. Fisher, and L.D. Siracusa A mutation in stratifin is responsible for the repeated epilation (Er) phenotype in mice Nat. Genet. 37 2005 1210 1212 (Pubitemid 41568702)
22. J. Huang, S. Wu, J. Barrera, K. Matthews, and D. Pan The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila Homolog of YAP Cell 122 2005 421 434 (Pubitemid 41127143)
23. K.A. Kim, M. Kakitani, J. Zhao, T. Oshima, T. Tang, M. Binnerts, Y. Liu, B. Boyle, E. Park, and P. Emtage Mitogenic influence of human R-spondin1 on the intestinal epithelium Science 309 2005 1256 1259 (Pubitemid 41170922)
24. A. Kobielak, and E. Fuchs Links between alpha-catenin, NF-kappaB, and squamous cell carcinoma in skin Proc. Natl. Acad. Sci. USA 103 2006 2322 2327 (Pubitemid 43271668)
25. Z.C. Lai, X. Wei, T. Shimizu, E. Ramos, M. Rohrbaugh, N. Nikolaidis, L.L. Ho, and Y. Li Control of cell proliferation and apoptosis by mob as tumor suppressor, mats Cell 120 2005 675 685 (Pubitemid 40343079)
26. Q. Li, Q. Lu, G. Estepa, and I.M. Verma Identification of 14-3-3sigma mutation causing cutaneous abnormality in repeated-epilation mutant mouse Proc. Natl. Acad. Sci. USA 102 2005 15977 15982 (Pubitemid 41552853)
27. I. Lian, J. Kim, H. Okazawa, J. Zhao, B. Zhao, J. Yu, A. Chinnaiyan, M.A. Israel, L.S. Goldstein, and R. Abujarour The role of YAP transcription coactivator in regulating stem cell self-renewal and differentiation Genes Dev. 24 2010 1106 1118
28. W.H. Lien, O. Klezovitch, T.E. Fernandez, J. Delrow, and V. Vasioukhin alphaE-catenin controls cerebral cortical size by regulating the hedgehog signaling pathway Science 311 2006 1609 1612
29. W.H. Lien, O. Klezovitch, and V. Vasioukhin Cadherin-catenin proteins in vertebrate development Curr. Opin. Cell Biol. 18 2006 499 506 (Pubitemid 44349063)
30. C. Ling, Y. Zheng, F. Yin, J. Yu, J. Huang, Y. Hong, S. Wu, and D. Pan The apical transmembrane protein Crumbs functions as a tumor suppressor that regulates Hippo signaling by binding to Expanded Proc. Natl. Acad. Sci. USA 107 2010 10532 10537
31. L. Lu, Y. Li, S.M. Kim, W. Bossuyt, P. Liu, Q. Qiu, Y. Wang, G. Halder, M.J. Finegold, J.S. Lee, and R.L. Johnson Hippo signaling is a potent in vivo growth and tumor suppressor pathway in the mammalian liver Proc. Natl. Acad. Sci. USA 107 2010 1437 1442
32. M. Martin, M. Potente, V. Janssens, D. Vertommen, J.C. Twizere, M.H. Rider, J. Goris, S. Dimmeler, R. Kettmann, and F. Dequiedt Protein phosphatase 2A controls the activity of histone deacetylase 7 during T cell apoptosis and angiogenesis Proc. Natl. Acad. Sci. USA 105 2008 4727 4732 (Pubitemid 351753814)
33. G.K. Menon, and P.M. Elias Ultrastructural localization of calcium in psoriatic and normal human epidermis Arch. Dermatol. 127 1991 57 63
34. H. Nguyen, B.J. Merrill, L. Polak, M. Nikolova, M. Rendl, T.M. Shaver, H.A. Pasolli, and E. Fuchs Tcf3 and Tcf4 are essential for long-term homeostasis of skin epithelia Nat. Genet. 41 2009 1068 1075
35. H. Oh, and K.D. Irvine In vivo regulation of Yorkie phosphorylation and localization Development 135 2008 1081 1088 (Pubitemid 351578136)
36. T. Oka, V. Mazack, and M. Sudol Mst2 and Lats kinases regulate apoptotic function of Yes kinase-associated protein (YAP) J. Biol. Chem. 283 2008 27534 27546
37. S. Pantalacci, N. Tapon, and P. Léopold The Salvador partner Hippo promotes apoptosis and cell-cycle exit in Drosophila Nat. Cell Biol. 5 2003 921 927 (Pubitemid 37220699)
38. G. Pellegrini, E. Dellambra, O. Golisano, E. Martinelli, I. Fantozzi, S. Bondanza, D. Ponzin, F. McKeon, and M. De Luca p63 identifies keratinocyte stem cells Proc. Natl. Acad. Sci. USA 98 2001 3156 3161 (Pubitemid 32220815)
39. M. Perez-Moreno, M.A. Davis, E. Wong, H.A. Pasolli, A.B. Reynolds, and E. Fuchs p120-catenin mediates inflammatory responses in the skin Cell 124 2006 631 644 (Pubitemid 43199446)
40. P.S. Ribeiro, F. Josué, A. Wepf, M.C. Wehr, O. Rinner, G. Kelly, N. Tapon, and M. Gstaiger Combined functional genomic and proteomic approaches identify a PP2A complex as a negative regulator of Hippo signaling Mol. Cell 39 2010 521 534
41. B.S. Robinson, J. Huang, Y. Hong, and K.H. Moberg Crumbs regulates Salvador/Warts/Hippo signaling in Drosophila via the FERM-domain protein Expanded Curr. Biol. 20 2010 582 590
42. M. Senoo, F. Pinto, C.P. Crum, and F. McKeon p63 Is essential for the proliferative potential of stem cells in stratified epithelia Cell 129 2007 523 536 (Pubitemid 46660965)
43. H. Song, K.K. Mak, L. Topol, K. Yun, J. Hu, L. Garrett, Y. Chen, O. Park, J. Chang, and R.M. Simpson Mammalian Mst1 and Mst2 kinases play essential roles in organ size control and tumor suppression Proc. Natl. Acad. Sci. USA 107 2010 1431 1436
44. B.Z. Stanger, A.J. Tanaka, and D.A. Melton Organ size is limited by the number of embryonic progenitor cells in the pancreas but not the liver Nature 445 2007 886 891
45. E. Stepniak, G.L. Radice, and V. Vasioukhin Adhesive and signaling functions of cadherins and catenins in vertebrate development Cold Spring Harb. Perspect. Biol. 1 2009 a002949
46. C.L. Tinkle, H.A. Pasolli, N. Stokes, and E. Fuchs New insights into cadherin function in epidermal sheet formation and maintenance of tissue integrity Proc. Natl. Acad. Sci. USA 105 2008 15405 15410
47. X. Varelas, P. Samavarchi-Tehrani, M. Narimatsu, A. Weiss, K. Cockburn, B.G. Larsen, J. Rossant, and J.L. Wrana The Crumbs complex couples cell density sensing to Hippo-dependent control of the TGF-β-SMAD pathway Dev. Cell 19 2010 831 844
48. V. Vasioukhin, C. Bauer, L. Degenstein, B. Wise, and E. Fuchs Hyperproliferation and defects in epithelial polarity upon conditional ablation of alpha-catenin in skin Cell 104 2001 605 617 (Pubitemid 32201954)
49. A. Vassilev, K.J. Kaneko, H. Shu, Y. Zhao, and M.L. DePamphilis TEAD/TEF transcription factors utilize the activation domain of YAP65, a Src/Yes-associated protein localized in the cytoplasm Genes Dev. 15 2001 1229 1241 (Pubitemid 32472752)
50. S. Wu, J. Huang, J. Dong, and D. Pan 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 (Pubitemid 37100993)
51. S. Wu, Y. Liu, Y. Zheng, J. Dong, and D. Pan The TEAD/TEF family protein Scalloped mediates transcriptional output of the Hippo growth-regulatory pathway Dev. Cell 14 2008 388 398
52. T. Xu, W. Wang, S. Zhang, R.A. Stewart, and W. Yu Identifying tumor suppressors in genetic mosaics: the Drosophila lats gene encodes a putative protein kinase Development 121 1995 1053 1063
53. H. Zhang, H.A. Pasolli, and E. Fuchs Yes-associated protein (YAP) transcriptional coactivator functions in balancing growth and differentiation in skin Proc. Natl. Acad. Sci. USA 108 2011 2270 2275
54. L. Zhang, F. Ren, Q. Zhang, Y. Chen, B. Wang, and J. Jiang The TEAD/TEF family of transcription factor Scalloped mediates Hippo signaling in organ size control Dev. Cell 14 2008 377 387
55. N. Zhang, H. Bai, K.K. David, J. Dong, Y. Zheng, J. Cai, M. Giovannini, P. Liu, R.A. Anders, and D. Pan The Merlin/NF2 tumor suppressor functions through the YAP oncoprotein to regulate tissue homeostasis in mammals Dev. Cell 19 2010 27 38
56. B. Zhao, X. Wei, W. Li, R.S. Udan, Q. Yang, J. Kim, J. Xie, T. Ikenoue, J. Yu, and L. Li Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control Genes Dev. 21 2007 2747 2761 (Pubitemid 350070721)
57. B. Zhao, X. Ye, J. Yu, L. Li, W. Li, S. Li, J. Yu, J.D. Lin, C.Y. Wang, and A.M. Chinnaiyan TEAD mediates YAP-dependent gene induction and growth control Genes Dev. 22 2008 1962 1971 (Pubitemid 352008643)
58. D. Zhou, C. Conrad, F. Xia, J.S. Park, B. Payer, Y. Yin, G.Y. Lauwers, W. Thasler, J.T. Lee, J. Avruch, and N. Bardeesy Mst1 and Mst2 maintain hepatocyte quiescence and suppress hepatocellular carcinoma development through inactivation of the Yap1 oncogene Cancer Cell 16 2009 425 438