Stem cell regulation by the Hippo pathway

Biochimica et Biophysica Acta - General Subjects

Volumn 1830, Issue 2, 2013, Pages 2323-2334

  Hiemer, Samantha E ^a   Varelas, Xaralabos ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Hippo pathway; Regeneration; Stem cell; TAZ; YAP

Indexed keywords

ADAPTOR PROTEIN; BETA CATENIN; EPHRIN; EPHRIN RECEPTOR; NOTCH RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN KINASE; PROTEIN MST1; PROTEIN MST2; PROTEIN SALVADOR 1; PROTEIN TAZ; PROTEIN YAP; REGULATOR PROTEIN; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR TEAD; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; WNT PROTEIN;

ADIPOGENESIS; ADULT STEM CELL; BONE DEVELOPMENT; CANCER GROWTH; CANCER STEM CELL; CARCINOGENESIS; CELL DIFFERENTIATION; CELL FATE; CELL PROLIFERATION; CELL RENEWAL; CELLULAR DISTRIBUTION; EMBRYONIC STEM CELL; EPIDERMAL STEM CELL; EPITHELIAL MESENCHYMAL TRANSITION; HIPPO PATHWAY; HUMAN; INTESTINAL STEM CELL; LIVER STEM CELL; MESENCHYMAL STEM CELL; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MUSCLE DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; STEM CELL REGULATION; TISSUE REGENERATION;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PROTEIN-SERINE-THREONINE KINASES; STEM CELLS;

MAMMALIA;

EID: 84872497913     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2012.07.005     Document Type: Review

References (150)

1. 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
2. J. Jia, W. Zhang, B. Wang, R. Trinko, and J. Jiang The Drosophila Ste20 family kinase dMST functions as a tumor suppressor by restricting cell proliferation and promoting apoptosis Genes Dev. 17 2003 2514 2519
3. R.W. Justice, O. Zilian, D.F. Woods, M. Noll, and P.J. Bryant 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
4. S. Pantalacci, N. Tapon, and P. Leopold The Salvador partner Hippo promotes apoptosis and cell-cycle exit in Drosophila Nat. Cell Biol. 5 2003 921 927
5. N. Tapon, K.F. Harvey, D.W. Bell, D.C. Wahrer, T.A. Schiripo, D.A. Haber, and I.K. Hariharan salvador Promotes both cell cycle exit and apoptosis in Drosophila and is mutated in human cancer cell lines Cell 110 2002 467 478
6. R.S. Udan, M. Kango-Singh, R. Nolo, C. Tao, and G. Halder Hippo promotes proliferation arrest and apoptosis in the Salvador/Warts pathway Nat. Cell Biol. 5 2003 914 920
7. 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
8. D. Pan The hippo signaling pathway in development and cancer Dev. Cell 19 2010 491 505
9. B. Zhao, K. Tumaneng, and K.L. Guan The Hippo pathway in organ size control, tissue regeneration and stem cell self-renewal Nat. Cell Biol. 13 2011 877 883
10. F. Kanai, P.A. Marignani, D. Sarbassova, R. Yagi, R.A. Hall, M. Donowitz, A. Hisaminato, T. Fujiwara, Y. Ito, L.C. Cantley, and M.B. Yaffe TAZ: a novel transcriptional co-activator regulated by interactions with 14-3-3 and PDZ domain proteins EMBO J. 19 2000 6778 6791
11. S. Basu, N.F. Totty, M.S. Irwin, M. Sudol, and J. Downward Akt phosphorylates the Yes-associated protein, YAP, to induce interaction with 14-3-3 and attenuation of p73-mediated apoptosis Mol. Cell 11 2003 11 23
12. Q.Y. Lei, H. Zhang, B. Zhao, Z.Y. Zha, F. Bai, X.H. Pei, S. Zhao, Y. Xiong, and K.L. Guan TAZ promotes cell proliferation and epithelial-mesenchymal transition and is inhibited by the hippo pathway Mol. Cell. Biol. 28 2008 2426 2436
13. B. Zhao, X. Wei, W. Li, R.S. Udan, Q. Yang, J. Kim, J. Xie, T. Ikenoue, J. Yu, L. Li, P. Zheng, K. Ye, A. Chinnaiyan, G. Halder, Z.C. Lai, and K.L. Guan Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control Genes Dev. 21 2007 2747 2761
14. A. Mauviel, F. Nallet-Staub, and X. Varelas Integrating developmental signals: a Hippo in the (path)way Oncogene 31 14 2012 1743 1756
15. M. Sudol, and K.F. Harvey Modularity in the Hippo signaling pathway Trends Biochem. Sci. 35 2010 627 633
16. P. Bork, and M. Sudol The WW domain: a signalling site in dystrophin? Trends Biochem. Sci. 19 1994 531 533
17. M. Sudol, P. Bork, A. Einbond, K. Kastury, T. Druck, M. Negrini, K. Huebner, and D. Lehman Characterization of the mammalian YAP (Yes-associated protein) gene and its role in defining a novel protein module, the WW domain J. Biol. Chem. 270 1995 14733 14741
18. S.W. Chan, C.J. Lim, L.S. Loo, Y.F. Chong, C. Huang, and W. Hong TEADs mediate nuclear retention of TAZ to promote oncogenic transformation J. Biol. Chem. 284 2009 14347 14358
19. B. Zhao, X. Ye, J. Yu, L. Li, W. Li, S. Li, J.D. Lin, C.Y. Wang, A.M. Chinnaiyan, Z.C. Lai, and K.L. Guan TEAD mediates YAP-dependent gene induction and growth control Genes Dev. 22 2008 1962 1971
20. S. Dupont, L. Morsut, M. Aragona, E. Enzo, S. Giulitti, M. Cordenonsi, F. Zanconato, J. Le Digabel, M. Forcato, S. Bicciato, N. Elvassore, and S. Piccolo Role of YAP/TAZ in mechanotransduction Nature 474 2011 179 183
21. K. Wada, K. Itoga, T. Okano, S. Yonemura, and H. Sasaki Hippo pathway regulation by cell morphology and stress fibers Development 138 2011 3907 3914
22. B. Zhao, L. Li, L. Wang, C.Y. Wang, J. Yu, and K.L. Guan Cell detachment activates the Hippo pathway via cytoskeleton reorganization to induce anoikis Genes Dev. 26 2012 54 68
23. V. Vogel, and M.P. Sheetz Cell fate regulation by coupling mechanical cycles to biochemical signaling pathways Curr. Opin. Cell Biol. 21 2009 38 46
24. L. Sansores-Garcia, W. Bossuyt, K. Wada, S. Yonemura, C. Tao, H. Sasaki, and G. Halder Modulating F-actin organization induces organ growth by affecting the Hippo pathway EMBO J. 30 2011 2325 2335
25. R. Sopko, and H. McNeill The skinny on Fat: an enormous cadherin that regulates cell adhesion, tissue growth, and planar cell polarity Curr. Opin. Cell Biol. 21 2009 717 723
26. F.A. Grusche, H.E. Richardson, and K.F. Harvey Upstream regulation of the hippo size control pathway Curr. Biol. 20 2010 R574 R582
27. T. Yue, A. Tian, and J. Jiang The cell adhesion molecule echinoid functions as a tumor suppressor and upstream regulator of the Hippo signaling pathway Dev. Cell 22 2012 255 267
28. 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
29. F. Hamaratoglu, K. Gajewski, L. Sansores-Garcia, C. Morrison, C. Tao, and G. Halder The Hippo tumor-suppressor pathway regulates apical-domain size in parallel to tissue growth J. Cell Sci. 122 2009 2351 2359
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. U. S. A. 107 2010 10532 10537
31. 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. U. S. A. 107 2010 15810 15815
32. 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
33. L. Angus, S. Moleirinho, L. Herron, A. Sinha, X. Zhang, M. Niestrata, K. Dholakia, M.B. Prystowsky, K.F. Harvey, P.A. Reynolds, and F.J. Gunn-Moore Willin/FRMD6 expression activates the Hippo signaling pathway kinases in mammals and antagonizes oncogenic YAP Oncogene 31 2012 238 250
34. 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
35. K. Schlegelmilch, M. Mohseni, O. Kirak, J. Pruszak, J.R. Rodriguez, D. Zhou, B.T. Kreger, V. Vasioukhin, J. Avruch, T.R. Brummelkamp, and F.D. Camargo Yap1 acts downstream of alpha-catenin to control epidermal proliferation Cell 144 2011 782 795
36. E. Remue, K. Meerschaert, T. Oka, C. Boucherie, J. Vandekerckhove, M. Sudol, and J. Gettemans TAZ interacts with zonula occludens-1 and - 2 proteins in a PDZ-1 dependent manner FEBS Lett. 584 2010 4175 4180
37. T. Oka, A.P. Schmitt, and M. Sudol Opposing roles of angiomotin-like-1 and zona occludens-2 on pro-apoptotic function of YAP Oncogene 31 2012 128 134
38. M. Cordenonsi, F. Zanconato, L. Azzolin, M. Forcato, A. Rosato, C. Frasson, M. Inui, M. Montagner, A.R. Parenti, A. Poletti, M.G. Daidone, S. Dupont, G. Basso, S. Bicciato, and S. Piccolo The Hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells Cell 147 2011 759 772
39. K. Skouloudaki, M. Puetz, M. Simons, J.R. Courbard, C. Boehlke, B. Hartleben, C. Engel, M.J. Moeller, C. Englert, F. Bollig, T. Schafer, H. Ramachandran, M. Mlodzik, T.B. Huber, E.W. Kuehn, E. Kim, A. Kramer-Zucker, and G. Walz Scribble participates in Hippo signaling and is required for normal zebrafish pronephros development Proc. Natl. Acad. Sci. U. S. A. 106 2009 8579 8584
40. 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-beta-SMAD pathway Dev. Cell 19 2010 831 844
41. S.W. Chan, C.J. Lim, Y.F. Chong, A.V. Pobbati, C. Huang, and W. Hong Hippo pathway-independent restriction of TAZ and YAP by angiomotin J. Biol. Chem. 286 2011 7018 7026
42. B. Zhao, L. Li, Q. Lu, L.H. Wang, C.Y. Liu, Q. Lei, and K.L. Guan Angiomotin is a novel Hippo pathway component that inhibits YAP oncoprotein Genes Dev. 25 2011 51 63
43. K. Takahashi, and S. Yamanaka Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors Cell 126 2006 663 676
44. C. Alarcon, A.I. Zaromytidou, Q. Xi, S. Gao, J. Yu, S. Fujisawa, A. Barlas, A.N. Miller, K. Manova-Todorova, M.J. Macias, G. Sapkota, D. Pan, and J. Massague Nuclear CDKs drive Smad transcriptional activation and turnover in BMP and TGF-beta pathways Cell 139 2009 757 769
45. I. Lian, J. Kim, H. Okazawa, J. Zhao, B. Zhao, J. Yu, A. Chinnaiyan, M.A. Israel, L.S. Goldstein, R. Abujarour, S. Ding, and K.L. Guan The role of YAP transcription coactivator in regulating stem cell self-renewal and differentiation Genes Dev. 24 2010 1106 1118
46. H. Qin, K. Blaschke, G. Wei, Y. Ohi, L. Blouin, Z. Qi, J. Yu, R.F. Yeh, M. Hebrok, and M. Ramalho-Santos Transcriptional analysis of pluripotency reveals the Hippo pathway as a barrier to reprogramming Hum. Mol. Genet. 21 9 2012 2054 2067
47. X. Varelas, R. Sakuma, P. Samavarchi-Tehrani, R. Peerani, B.M. Rao, J. Dembowy, M.B. Yaffe, P.W. Zandstra, and J.L. Wrana TAZ controls Smad nucleocytoplasmic shuttling and regulates human embryonic stem-cell self-renewal Nat. Cell Biol. 10 2008 837 848
48. C. Tamm, N. Bower, and C. Anneren Regulation of mouse embryonic stem cell self-renewal by a Yes-YAP-TEAD2 signaling pathway downstream of LIF J. Cell Sci. 124 2011 1136 1144
49. D. James, A.J. Levine, D. Besser, and A. Hemmati-Brivanlou TGFbeta/activin/nodal signaling is necessary for the maintenance of pluripotency in human embryonic stem cells Development 132 2005 1273 1282
50. L. Vallier, M. Alexander, and R.A. Pedersen Activin/Nodal and FGF pathways cooperate to maintain pluripotency of human embryonic stem cells J. Cell Sci. 118 2005 4495 4509
51. Q.L. Ying, J. Nichols, I. Chambers, and A. Smith BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3 Cell 115 2003 281 292
52. L. Attisano, and J.L. Wrana Signal transduction by the TGF-beta superfamily Science 296 2002 1646 1647
53. A.C. Mullen, D.A. Orlando, J.J. Newman, J. Loven, R.M. Kumar, S. Bilodeau, J. Reddy, M.G. Guenther, R.P. DeKoter, and R.A. Young Master transcription factors determine cell-type-specific responses to TGF-beta signaling Cell 147 2011 565 576
54. R.H. Xu, T.L. Sampsell-Barron, F. Gu, S. Root, R.M. Peck, G. Pan, J. Yu, J. Antosiewicz-Bourget, S. Tian, R. Stewart, and J.A. Thomson NANOG is a direct target of TGFbeta/activin-mediated SMAD signaling in human ESCs Cell Stem Cell 3 2008 196 206
55. K. Cockburn, and J. Rossant Making the blastocyst: lessons from the mouse J. Clin. Invest. 120 2010 995 1003
56. N. Nishioka, K. Inoue, K. Adachi, H. Kiyonari, M. Ota, A. Ralston, N. Yabuta, S. Hirahara, R.O. Stephenson, N. Ogonuki, R. Makita, H. Kurihara, E.M. Morin-Kensicki, H. Nojima, J. Rossant, K. Nakao, H. Niwa, and H. Sasaki The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass Dev. Cell 16 2009 398 410
57. S.J. Arnold, and E.J. Robertson Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo Nat. Rev. Mol. Cell Biol. 10 2009 91 103
58. X. Varelas, and J.L. Wrana Coordinating developmental signaling: novel roles for the Hippo pathway Trends Cell Biol. 22 2012 88 96
59. N.R. Dunn, S.D. Vincent, L. Oxburgh, E.J. Robertson, and E.K. Bikoff Combinatorial activities of Smad2 and Smad3 regulate mesoderm formation and patterning in the mouse embryo Development 131 2004 1717 1728
60. H. Xie, S. Tranguch, X. Jia, H. Zhang, S.K. Das, S.K. Dey, C.J. Kuo, and H. Wang Inactivation of nuclear Wnt-beta-catenin signaling limits blastocyst competency for implantation Development 135 2008 717 727
61. C. Kemp, E. Willems, S. Abdo, L. Lambiv, and L. Leyns Expression of all Wnt genes and their secreted antagonists during mouse blastocyst and postimplantation development Dev. Dyn. 233 2005 1064 1075
62. T. Heallen, M. Zhang, J. Wang, M. Bonilla-Claudio, E. Klysik, R.L. Johnson, and J.F. Martin Hippo pathway inhibits Wnt signaling to restrain cardiomyocyte proliferation and heart size Science 332 2011 458 461
63. M. Imajo, K. Miyatake, A. Iimura, A. Miyamoto, and E. Nishida A molecular mechanism that links Hippo signalling to the inhibition of Wnt/beta-catenin signalling EMBO J. 31 2012 1109 1122
64. X. Varelas, B.W. Miller, R. Sopko, S. Song, A. Gregorieff, F.A. Fellouse, R. Sakuma, T. Pawson, W. Hunziker, H. McNeill, J.L. Wrana, and L. Attisano The Hippo pathway regulates Wnt/beta-catenin signaling Dev. Cell 18 2010 579 591
65. M. Owen, and A.J. Friedenstein Stromal stem cells: marrow-derived osteogenic precursors Ciba Found. Symp. 136 1988 42 60
66. A.I. Caplan, and S.P. Bruder Mesenchymal stem cells: building blocks for molecular medicine in the 21st century Trends Mol. Med. 7 2001 259 264
67. C.B. Cui, L.F. Cooper, X. Yang, G. Karsenty, and I. Aukhil Transcriptional coactivation of bone-specific transcription factor Cbfa1 by TAZ Mol. Cell. Biol. 23 2003 1004 1013
68. J.H. Hong, E.S. Hwang, M.T. McManus, A. Amsterdam, Y. Tian, R. Kalmukova, E. Mueller, T. Benjamin, B.M. Spiegelman, P.A. Sharp, N. Hopkins, and M.B. Yaffe TAZ, a transcriptional modulator of mesenchymal stem cell differentiation Science 309 2005 1074 1078
69. R. Yagi, L.F. Chen, K. Shigesada, Y. Murakami, and Y. Ito A WW domain-containing yes-associated protein (YAP) is a novel transcriptional co-activator EMBO J. 18 1999 2551 2562
70. M. Al-Hajj, M.S. Wicha, A. Benito-Hernandez, S.J. Morrison, and M.F. Clarke Prospective identification of tumorigenic breast cancer cells Proc. Natl. Acad. Sci. U. S. A. 100 2003 3983 3988
71. S.K. Zaidi, A.J. Sullivan, R. Medina, Y. Ito, A.J. van Wijnen, J.L. Stein, J.B. Lian, and G.S. Stein Tyrosine phosphorylation controls Runx2-mediated subnuclear targeting of YAP to repress transcription EMBO J. 23 2004 790 799
72. H. Id Boufker, L. Lagneaux, M. Najar, M. Piccart, G. Ghanem, J.J. Body, and F. Journe The Src inhibitor dasatinib accelerates the differentiation of human bone marrow-derived mesenchymal stromal cells into osteoblasts BMC Cancer 10 2010 298
73. M. Sudol Yes-associated protein (YAP65) is a proline-rich phosphoprotein that binds to the SH3 domain of the Yes proto-oncogene product Oncogene 9 1994 2145 2152
74. B.H. Park, D.S. Kim, G.W. Won, H.J. Jeon, B.C. Oh, Y. Lee, E.G. Kim, and Y.H. Lee Mammalian ste20-like kinase and SAV1 promote 3T3-L1 adipocyte differentiation by activation of PPARgamma PLoS One 7 2012 e30983
75. D. Genini, and C.V. Catapano Control of peroxisome proliferator-activated receptor fate by the ubiquitinproteasome system J. Recept. Signal Transduct. Res. 26 2006 679 692
76. G.M. Boland, G. Perkins, D.J. Hall, and R.S. Tuan Wnt 3a promotes proliferation and suppresses osteogenic differentiation of adult human mesenchymal stem cells J. Cell. Biochem. 93 2004 1210 1230
77. H.H. Cho, Y.J. Kim, S.J. Kim, J.H. Kim, Y.C. Bae, B. Ba, and J.S. Jung Endogenous Wnt signaling promotes proliferation and suppresses osteogenic differentiation in human adipose derived stromal cells Tissue Eng. 12 2006 111 121
78. D. Baksh, G.M. Boland, and R.S. Tuan Cross-talk between Wnt signaling pathways in human mesenchymal stem cells leads to functional antagonism during osteogenic differentiation J. Cell. Biochem. 101 2007 1109 1124
79. Y. Gong, R.B. Slee, N. Fukai, G. Rawadi, S. Roman-Roman, A.M. Reginato, H. Wang, T. Cundy, F.H. Glorieux, D. Lev, M. Zacharin, K. Oexle, J. Marcelino, W. Suwairi, S. Heeger, G. Sabatakos, S. Apte, W.N. Adkins, J. Allgrove, M. Arslan-Kirchner, J.A. Batch, P. Beighton, G.C. Black, R.G. Boles, L.M. Boon, C. Borrone, H.G. Brunner, G.F. Carle, B. Dallapiccola, A. De Paepe, B. Floege, M.L. Halfhide, B. Hall, R.C. Hennekam, T. Hirose, A. Jans, H. Juppner, C.A. Kim, K. Keppler-Noreuil, A. Kohlschuetter, D. LaCombe, M. Lambert, E. Lemyre, T. Letteboer, L. Peltonen, R.S. Ramesar, M. Romanengo, H. Somer, E. Steichen-Gersdorf, B. Steinmann, B. Sullivan, A. Superti-Furga, W. Swoboda, M.J. van den Boogaard, W. Van Hul, M. Vikkula, M. Votruba, B. Zabel, T. Garcia, R. Baron, B.R. Olsen, and M.L. Warman LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development Cell 107 2001 513 523
80. J. De Boer, H.J. Wang, and C. Van Blitterswijk Effects of Wnt signaling on proliferation and differentiation of human mesenchymal stem cells Tissue Eng. 10 2004 393 401
81. W. Qiu, T.E. Andersen, J. Bollerslev, S. Mandrup, B.M. Abdallah, and M. Kassem Patients with high bone mass phenotype exhibit enhanced osteoblast differentiation and inhibition of adipogenesis of human mesenchymal stem cells J. Bone Miner. Res. 22 2007 1720 1731
82. M. Moldes, Y. Zuo, R.F. Morrison, D. Silva, B.H. Park, J. Liu, and S.R. Farmer Peroxisome-proliferator-activated receptor gamma suppresses Wnt/beta-catenin signalling during adipogenesis Biochem. J. 376 2003 607 613
83. C. Hartmann, and C.J. Tabin Dual roles of Wnt signaling during chondrogenesis in the chicken limb Development 127 2000 3141 3159
84. L. Zhao, S. Jiang, and B.M. Hantash Transforming growth factor beta1 induces osteogenic differentiation of murine bone marrow stromal cells Tissue Eng. Part A 16 2010 725 733
85. G. Zimmermann, P. Henle, M. Kusswetter, A. Moghaddam, A. Wentzensen, W. Richter, and S. Weiss TGF-beta1 as a marker of delayed fracture healing Bone 36 2005 779 785
86. H.H. Cho, K.K. Shin, Y.J. Kim, J.S. Song, J.M. Kim, Y.C. Bae, C.D. Kim, and J.S. Jung NF-kappaB activation stimulates osteogenic differentiation of mesenchymal stem cells derived from human adipose tissue by increasing TAZ expression J. Cell. Physiol. 223 2010 168 177
87. L. Gilbert, X. He, P. Farmer, S. Boden, M. Kozlowski, J. Rubin, and M.S. Nanes Inhibition of osteoblast differentiation by tumor necrosis factor-alpha Endocrinology 141 2000 3956 3964
88. L. Gilbert, X. He, P. Farmer, J. Rubin, H. Drissi, A.J. van Wijnen, J.B. Lian, G.S. Stein, and M.S. Nanes Expression of the osteoblast differentiation factor RUNX2 (Cbfa1/AML3/Pebp2alpha A) is inhibited by tumor necrosis factor-alpha J. Biol. Chem. 277 2002 2695 2701
89. B. Li, M. Shi, J. Li, H. Zhang, B. Chen, L. Chen, W. Gao, N. Giuliani, and R.C. Zhao Elevated tumor necrosis factor-alpha suppresses TAZ expression and impairs osteogenic potential of Flk-1 + mesenchymal stem cells in patients with multiple myeloma Stem Cells Dev. 16 2007 921 930
90. W. Xing, J. Kim, J. Wergedal, S.T. Chen, and S. Mohan Ephrin B1 regulates bone marrow stromal cell differentiation and bone formation by influencing TAZ transactivation via complex formation with NHERF1 Mol. Cell. Biol. 30 2010 711 721
91. E. Jang, H. Jeong, J. Kang, N. Kim, M. Kim, S. Choi, S. Yoo, J. Hong, M. Bae, and E. Hwang TM-25659 enhances osteogenic differentiation and suppresses adipogenic differentiation by modulating the transcriptional co-activator TAZ Br. J. Pharmacol. 165 2012 1584 1594
92. H. Jung, M.S. Lee, E.J. Jang, J.H. Ahn, N.S. Kang, S.E. Yoo, M.A. Bae, J.H. Hong, and E.S. Hwang Augmentation of PPARgamma-TAZ interaction contributes to the anti-adipogenic activity of KR62980 Biochem. Pharmacol. 78 2009 1323 1329
93. R. McBeath, D.M. Pirone, C.M. Nelson, K. Bhadriraju, and C.S. Chen Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment Dev. Cell 6 2004 483 495
94. F.S. Tedesco, A. Dellavalle, J. Diaz-Manera, G. Messina, and G. Cossu Repairing skeletal muscle: regenerative potential of skeletal muscle stem cells J. Clin. Invest. 120 2010 11 19
95. K.I. Watt, R. Judson, P. Medlow, K. Reid, T.B. Kurth, J.G. Burniston, A. Ratkevicius, C. De Bari, and H. Wackerhage Yap is a novel regulator of C2C12 myogenesis Biochem. Biophys. Res. Commun. 393 2010 619 624
96. H. Jeong, S. Bae, S.Y. An, M.R. Byun, J.H. Hwang, M.B. Yaffe, J.H. Hong, and E.S. Hwang TAZ as a novel enhancer of MyoD-mediated myogenic differentiation FASEB J. 24 2010 3310 3320
97. T. Yoshida MCAT elements and the TEF-1 family of transcription factors in muscle development and disease Arterioscler. Thromb. Vasc. Biol. 28 2008 8 17
98. Y. Matsui, N. Nakano, D. Shao, S. Gao, W. Luo, C. Hong, P. Zhai, E. Holle, X. Yu, N. Yabuta, W. Tao, T. Wagner, H. Nojima, and J. Sadoshima Lats2 is a negative regulator of myocyte size in the heart Circ. Res. 103 2008 1309 1318
99. A. von Gise, Z. Lin, K. Schlegelmilch, L.B. Honor, G.M. Pan, J.N. Buck, Q. Ma, T. Ishiwata, B. Zhou, F.D. Camargo, and W.T. Pu YAP1, the nuclear target of Hippo signaling, stimulates heart growth through cardiomyocyte proliferation but not hypertrophy Proc. Natl. Acad. Sci. U. S. A. 109 2012 2394 2399
100. M. Xin, Y. Kim, L.B. Sutherland, X. Qi, J. McAnally, R.J. Schwartz, J.A. Richardson, R. Bassel-Duby, and E.N. Olson Regulation of insulin-like growth factor signaling by Yap governs cardiomyocyte proliferation and embryonic heart size Sci. Signal. 4 2011 ra70
101. Z. Chen, G.A. Friedrich, and P. Soriano Transcriptional enhancer factor 1 disruption by a retroviral gene trap leads to heart defects and embryonic lethality in mice Genes Dev. 8 1994 2293 2301
102. 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
103. 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
104. D. Zhou, Y. Zhang, H. Wu, E. Barry, Y. Yin, E. Lawrence, D. Dawson, J.E. Willis, S.D. Markowitz, F.D. Camargo, and J. Avruch Mst1 and Mst2 protein kinases restrain intestinal stem cell proliferation and colonic tumorigenesis by inhibition of Yes-associated protein (Yap) overabundance Proc. Natl. Acad. Sci. U. S. A. 108 2011 E1312 E1320
105. C.A. Micchelli, and N. Perrimon Evidence that stem cells reside in the adult Drosophila midgut epithelium Nature 439 2006 475 479
106. B. Ohlstein, and A. Spradling The adult Drosophila posterior midgut is maintained by pluripotent stem cells Nature 439 2006 470 474
107. B. Ohlstein, and A. Spradling Multipotent Drosophila intestinal stem cells specify daughter cell fates by differential notch signaling Science 315 2007 988 992
108. P. Karpowicz, J. Perez, and N. Perrimon The Hippo tumor suppressor pathway regulates intestinal stem cell regeneration Development 137 2010 4135 4145
109. R.L. Shaw, A. Kohlmaier, C. Polesello, C. Veelken, B.A. Edgar, and N. Tapon The Hippo pathway regulates intestinal stem cell proliferation during Drosophila adult midgut regeneration Development 137 2010 4147 4158
110. B.K. Staley, and K.D. Irvine Warts and Yorkie mediate intestinal regeneration by influencing stem cell proliferation Curr. Biol. 20 2010 1580 1587
111. F. Ren, B. Wang, T. Yue, E.Y. Yun, Y.T. Ip, and J. Jiang Hippo signaling regulates Drosophila intestine stem cell proliferation through multiple pathways Proc. Natl. Acad. Sci. U. S. A. 107 2010 21064 21069
112. 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. U. S. A. 108 2011 2270 2275
113. I. D'Addario, C. Abbruzzese, M. Lo Iacono, M. Teson, O. Golisano, and V. Barone Overexpression of YAP1 induces immortalization of normal human keratinocytes by blocking clonal evolution Histochem. Cell Biol. 134 2010 265 276
114. J.H. Lee, T.S. Kim, T.H. Yang, B.K. Koo, S.P. Oh, K.P. Lee, H.J. Oh, S.H. Lee, Y.Y. Kong, J.M. Kim, and D.S. Lim A crucial role of WW45 in developing epithelial tissues in the mouse EMBO J. 27 2008 1231 1242
115. M.R. Silvis, B.T. Kreger, W.H. Lien, O. Klezovitch, G.M. Rudakova, F.D. Camargo, D.M. Lantz, J.T. Seykora, and V. Vasioukhin alpha-catenin is a tumor suppressor that controls cell accumulation by regulating the localization and activity of the transcriptional coactivator Yap1 Sci. Signal. 4 2011 ra33
116. K. Doggett, F.A. Grusche, H.E. Richardson, and A.M. Brumby Loss of the Drosophila cell polarity regulator Scribbled promotes epithelial tissue overgrowth and cooperation with oncogenic Ras-Raf through impaired Hippo pathway signaling BMC Dev. Biol. 11 2011 57
117. N.G. Kim, E. Koh, X. Chen, and B.M. Gumbiner E-cadherin mediates contact inhibition of proliferation through Hippo signaling-pathway components Proc. Natl. Acad. Sci. U. S. A. 108 2011 11930 11935
118. D.M. Bryant, and K.E. Mostov From cells to organs: building polarized tissue Nat. Rev. Mol. Cell Biol. 9 2008 887 901
119. F.T. Merkle, and A. Alvarez-Buylla Neural stem cells in mammalian development Curr. Opin. Cell Biol. 18 2006 704 709
120. X. Cao, S.L. Pfaff, and F.H. Gage YAP regulates neural progenitor cell number via the TEA domain transcription factor Genes Dev. 22 2008 3320 3334
121. S.T. Gee, S.L. Milgram, K.L. Kramer, F.L. Conlon, and S.A. Moody Yes-associated protein 65 (YAP) expands neural progenitors and regulates Pax3 expression in the neural plate border zone PLoS One 6 2011 e20309
122. N.J. Van Hateren, R.M. Das, G.M. Hautbergue, A.G. Borycki, M. Placzek, and S.A. Wilson FatJ acts via the Hippo mediator Yap1 to restrict the size of neural progenitor cell pools Development 138 2011 1893 1902
123. B.V. Reddy, C. Rauskolb, and K.D. Irvine Influence of fat-hippo and notch signaling on the proliferation and differentiation of Drosophila optic neuroepithelia Development 137 2010 2397 2408
124. Y. Li, M.A. Hibbs, A.L. Gard, N.A. Shylo, and K. Yun Genome-Wide Analysis of N1ICD/RBPJ Targets in vivo Reveals Direct Transcriptional Regulation of Wnt, SHH, and Hippo Pathway Effectors by Notch1 Stem Cells 30 4 2012 741 752
125. R.C. Milewski, N.C. Chi, J. Li, C. Brown, M.M. Lu, and J.A. Epstein Identification of minimal enhancer elements sufficient for Pax3 expression in neural crest and implication of Tead2 as a regulator of Pax3 Development 131 2004 829 837
126. M. Murakami, J. Tominaga, R. Makita, Y. Uchijima, Y. Kurihara, O. Nakagawa, T. Asano, and H. Kurihara Transcriptional activity of Pax3 is co-activated by TAZ Biochem. Biophys. Res. Commun. 339 2006 533 539
127. Q. Jiang, D. Liu, Y. Gong, Y. Wang, S. Sun, Y. Gui, and H. Song yap is required for the development of brain, eyes, and neural crest in zebrafish Biochem. Biophys. Res. Commun. 384 2009 114 119
128. H. Zhang, M. Deo, R.C. Thompson, M.D. Uhler, and D.L. Turner Negative regulation of Yap during neuronal differentiation Dev. Biol. 361 2012 103 115
129. B.N. Nicolay, B. Bayarmagnai, N.S. Moon, E.V. Benevolenskaya, and M.V. Frolov Combined inactivation of pRB and hippo pathways induces dedifferentiation in the Drosophila retina PLoS Genet. 6 2010 e1000918
130. D. Jukam, and C. Desplan Binary regulation of Hippo pathway by Merlin/NF2, Kibra, Lgl, and Melted specifies and maintains postmitotic neuronal fate Dev. Cell 21 2011 874 887
131. T. Mikeladze-Dvali, M.F. Wernet, D. Pistillo, E.O. Mazzoni, A.A. Teleman, Y.W. Chen, S. Cohen, and C. Desplan 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
132. M. Tanaka, T. Itoh, N. Tanimizu, and A. Miyajima Liver stem/progenitor cells: their characteristics and regulatory mechanisms J. Biochem. 149 2011 231 239
133. 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
134. Y. Liu-Chittenden, B. Huang, J.S. Shim, Q. Chen, S.J. Lee, R.A. Anders, J.O. Liu, and D. Pan Genetic and pharmacological disruption of the TEAD-YAP complex suppresses the oncogenic activity of YAP Genes Dev. 26 2012 1300 1305
135. 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
136. K.P. Lee, J.H. Lee, T.S. Kim, T.H. Kim, H.D. Park, J.S. Byun, M.C. Kim, W.I. Jeong, D.F. Calvisi, J.M. Kim, and D.S. Lim The Hippo-Salvador pathway restrains hepatic oval cell proliferation, liver size, and liver tumorigenesis Proc. Natl. Acad. Sci. U. S. A. 107 2010 8248 8253
137. 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. U. S. A. 107 2010 1437 1442
138. H. Song, K.K. Mak, L. Topol, K. Yun, J. Hu, L. Garrett, Y. Chen, O. Park, J. Chang, R.M. Simpson, C.Y. Wang, B. Gao, J. Jiang, and Y. Yang Mammalian Mst1 and Mst2 kinases play essential roles in organ size control and tumor suppression Proc. Natl. Acad. Sci. U. S. A. 107 2010 1431 1436
139. 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
140. S. Benhamouche, M. Curto, I. Saotome, A.B. Gladden, C.H. Liu, M. Giovannini, and A.I. McClatchey Nf2/Merlin controls progenitor homeostasis and tumorigenesis in the liver Genes Dev. 24 2010 1718 1730
141. M.R. Alison Liver stem cells: implications for hepatocarcinogenesis Stem Cell Rev. 1 2005 253 260
142. C. Wang, L. Zhang, Q. He, X. Feng, J. Zhu, Z. Xu, X. Wang, F. Chen, X. Li, and J. Dong Differences in Yes-associated protein and mRNA levels in regenerating liver and hepatocellular carcinoma Mol. Med. Rep. 5 2012 410 414
143. D. Hanahan, and R.A. Weinberg Hallmarks of cancer: the next generation Cell 144 2011 646 674
144. K.P. Bhat, K.L. Salazar, V. Balasubramaniyan, K. Wani, L. Heathcock, F. Hollingsworth, J.D. James, J. Gumin, K.L. Diefes, S.H. Kim, A. Turski, Y. Azodi, Y. Yang, T. Doucette, H. Colman, E.P. Sulman, F.F. Lang, G. Rao, S. Copray, B.D. Vaillant, and K.D. Aldape The transcriptional coactivator TAZ regulates mesenchymal differentiation in malignant glioma Genes Dev. 25 2011 2594 2609
145. S.W. Chan, C.J. Lim, K. Guo, C.P. Ng, I. Lee, W. Hunziker, Q. Zeng, and W. Hong A role for TAZ in migration, invasion, and tumorigenesis of breast cancer cells Cancer Res. 68 2008 2592 2598
146. M. Overholtzer, J. Zhang, G.A. Smolen, B. Muir, W. Li, D.C. Sgroi, C.X. Deng, J.S. Brugge, and D.A. Haber Transforming properties of YAP, a candidate oncogene on the chromosome 11q22 amplicon Proc. Natl. Acad. Sci. U. S. A. 103 2006 12405 12410
147. S.A. Mani, W. Guo, M.J. Liao, E.N. Eaton, A. Ayyanan, A.Y. Zhou, M. Brooks, F. Reinhard, C.C. Zhang, M. Shipitsin, L.L. Campbell, K. Polyak, C. Brisken, J. Yang, and R.A. Weinberg The epithelial-mesenchymal transition generates cells with properties of stem cells Cell 133 2008 704 715
148. C. Scheel, E.N. Eaton, S.H. Li, C.L. Chaffer, F. Reinhardt, K.J. Kah, G. Bell, W. Guo, J. Rubin, A.L. Richardson, and R.A. Weinberg Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast Cell 145 2011 926 940
149. J.P. Thiery, H. Acloque, R.Y. Huang, and M.A. Nieto Epithelial- mesenchymal transitions in development and disease Cell 139 2009 871 890
150. L. Jansson, and J. Larsson Normal hematopoietic stem cell function in mice with enforced expression of the Hippo signaling effector YAP1 PLoS One 7 2012 e32013