The transcriptional coactivator TAZ regulates mesenchymal differentiation in malignant glioma

Genes and Development

Volumn 25, Issue 24, 2011, Pages 2594-2609

  Bhat, Krishna P L ^a,c   Salazar, Katrina L ^a,c   Balasubramaniyan, Veerakumar ^a,b,c   Wani, Khalida ^a   Heathcock, Lindsey ^a   Hollingsworth, Faith ^a   James, Johanna D ^a   Gumin, Joy ^a   Diefes, Kristin L ^a   Kim, Se Hoon ^a,d   Turski, Alice ^a   Azodi, Yasaman ^a   Yang, Yuhui ^a   Doucette, Tiffany ^a   Colman, Howard ^a,e,f   Sulman, Erik P ^a   Lang, Frederick F ^a   Rao, Ganesh ^a   Copray, Sjef ^b   Vaillant, Brian D ^a   Aldape, Kenneth D ^a   more..

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c Yonsei University College of Medicine   (South Korea)

^d UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF UTAH   (United States)

^f HOUSTON METHODIST HOSPITAL   (United States)

Author keywords

Glioma; HIPPO; Mesenchymal; TAZ; TEAD

Indexed keywords

PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TAZ; TRANSCRIPTION FACTOR TEAD2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CLASSIFICATION; CANCER GRADING; CARCINOGENESIS; CARTILAGE CELL; CELL DIFFERENTIATION; CELL INVASION; CELL PROLIFERATION; CELL RENEWAL; CELL SURVIVAL; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EPIGENETICS; GENE EXPRESSION; GENE SILENCING; GENETIC ASSOCIATION; GLIOBLASTOMA; MESENCHYMAL STEM CELL; MOUSE; NEUROIMAGING; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

ANIMALS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELLS, CULTURED; DNA-BINDING PROTEINS; EPIGENOMICS; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOMA; HUMANS; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED C57BL; MICE, SCID; NEOPLASTIC STEM CELLS; TRANSCRIPTION FACTORS; TUMOR CELLS, CULTURED;

EID: 84255160601     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.176800.111     Document Type: Article

References (93)

1. Alcantara Llaguno S, Chen J, Kwon CH, Jackson EL, Li Y, Burns DK, Alvarez-Buylla A, Parada LF. 2009. Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell 15: 45-56.
2. Anido J, Saez-Borderias A, Gonzalez-Junca A, Rodon L, Folch G, Carmona MA, Prieto-Sanchez RM, Barba I, Martinez-Saez E, Prudkin L, et al. 2010. TGF-b receptor inhibitors target the CD44(high)/Id1(high) glioma-initiating cell population in human glioblastoma. Cancer Cell 18: 655-668.
3. Bachoo RM, Maher EA, Ligon KL, Sharpless NE, Chan SS, You MJ, Tang Y, De Frances J, Stover E, Weissleder R, et al. 2002. Epidermal growth factor receptor and Ink4a/Arf: Convergent mechanisms governing terminal differentiation and transformation along the neural stem cell to astrocyte axis. Cancer Cell 1: 269-277.
4. Basu S, Totty NF, Irwin MS, Sudol M, Downward J. 2003. Akt phosphorylates the Yes-associated protein, YAP, to induce interaction with 14-3-3 and attenuation of p73-mediated apoptosis. Mol Cell 11: 11-23.
5. Begemann M, Fuller GN, Holland EC. 2002. Genetic modeling of glioma formation in mice. Brain Pathol 12: 117-132.
6. Burns WC, Twigg SM, Forbes JM, Pete J, Tikellis C, Thallas-Bonke V, Thomas MC, Cooper ME, Kantharidis P. 2006. Connective tissue growth factor plays an important role in advanced glycation end product-induced tubular epithelialto-mesenchymal transition: Implications for diabetic renal disease. J Am Soc Nephrol 17: 2484-2494.
7. Burton EC, Lamborn KR, Feuerstein BG, Prados M, Scott J, Forsyth P, Passe S, Jenkins RB, Aldape KD. 2002. Genetic aberrations defined by comparative genomic hybridization distinguish long-term from typical survivors of glioblastoma. Cancer Res 62: 6205-6210.
8. Cao X, Pfaff SL, Gage FH. 2008. YAP regulates neural progenitor cell number via the TEA domain transcription factor. Genes Dev 22: 3320-3334.
9. Carro MS, Lim WK, Alvarez MJ, Bollo RJ, Zhao X, Snyder EY, Sulman EP, Anne SL, Doetsch F, Colman H, et al. 2010. The transcriptional network for mesenchymal transformation of brain tumours. Nature 463: 318-325.
10. Chan SW, Lim CJ, Chong YF, Pobbati AV, Huang C, Hong W. 2011. Hippo pathway-independent restriction of TAZ and YAP by angiomotin. J Biol Chem 286: 7018-7026.
11. Colman H, Zhang L, Sulman EP, McDonald JM, Shooshtari NL, Rivera A, Popoff S, Nutt CL, Louis DN, Cairncross JG, et al. 2010. A multigene predictor of outcome in glioblastoma. Neuro Ooncol 12: 49-57.
12. Cooper LA, Gutman DA, Long Q, Johnson BA, Cholleti SR, Kurc T, Saltz JH, Brat DJ, Moreno CS. 2010. The proneural molecular signature is enriched in oligodendrogliomas and predicts improved survival among diffuse gliomas. PLoS ONE 5: e12548. doi: 10.1371/journal.pone.002548.
13. Dai C, Celestino JC, Okada Y, Louis DN, Fuller GN, Holland EC. 2001. PDGF autocrine stimulation dedifferentiates cultured astrocytes and induces oligodendrogliomas and oligoastrocytomas from neural progenitors and astrocytes in vivo. Genes Dev 15: 1913-1925.
14. Deaton AM, Bird A. 2011. CpG islands and the regulation of transcription. Genes Dev 25: 1010-1022.
15. de Bruin A, Maiti B, Jakoi L, Timmers C, Buerki R, Leone G. 2003. Identification and characterization of E2F7, a novel mammalian E2F family member capable of blocking cellular proliferation. J Biol Chem 278: 42041-42049.
16. de Groot JF, Gilbert MR, Aldape K, Hess KR, Hanna TA, Ictech S, Groves MD, Conrad C, Colman H, Puduvalli VK, et al. 2008. Phase II study of carboplatin and erlotinib (Tarceva, OSI-774) in patients with recurrent glioblastoma. J Neurooncol 90: 89-97.
17. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. 2003. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: 3. doi: 10.1186/gb-2003-4-5-p3.
18. Di Palma T, D'Andrea B, Liguori GL, Liguoro A, de Cristofaro T, Del Prete D, Pappalardo A, Mascia A, Zannini M. 2009. TAZ is a coactivator for Pax8 and TTF-1, two transcription factors involved in thyroid differentiation. Exp Cell Res 315: 162-175.
19. Duning K, Rosenbusch D, Schluter MA, Tian Y, Kunzelmann K, Meyer N, Schulze U, Markoff A, Pavenstadt H, Weide T. 2010. Polycystin-2 activity is controlled by transcriptional coactivator with PDZ binding motif and PALS1-associated tight junction protein. J Biol Chem 285: 33584-33588.
20. Freije WA, Castro-Vargas FE, Fang Z, Horvath S, Cloughesy T, Liau LM, Mischel PS, Nelson SF. 2004. Gene expression profiling of gliomas strongly predicts survival. Cancer Res 64: 6503-6510.
21. Furnari FB, Fenton T, Bachoo RM, Mukasa A, Stommel JM, Stegh A, Hahn WC, Ligon KL, Louis DN, Brennan C, et al. 2007. Malignant astrocytic glioma: Genetics, biology, and paths to treatment. Genes Dev 21: 2683-2710.
22. Gage FH, Ray J, Fisher LJ. 1995. Isolation, characterization, and use of stem cells from the CNS. Annu Rev Neurosci 18: 159-192.
23. Gore-Hyer E, Shegogue D, Markiewicz M, Lo S, Hazen-Martin D, Greene EL, Grotendorst G, Trojanowska M. 2002. TGF-b and CTGF have overlapping and distinct fibrogenic effects on human renal cells. Am J Physiol Renal Physiol 283: F707-F716. doi: 10.1152/ajprenal.00007.2002.
24. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, Vadas MA, Khew-Goodall Y, Goodall GJ. 2008. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 10: 593-601.
25. Gupta PB, Chaffer CL, Weinberg RA. 2009. Cancer stem cells: Mirage or reality? Nat Med 15: 1010-1012.
26. Halder G, Johnson RL. 2011. Hippo signaling: Growth control and beyond. Development 138: 9-22.
27. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, et al. 2005. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352: 997-1003.
28. Hiratsuka S, Nakamura K, Iwai S, Murakami M, Itoh T, Kijima H, Shipley JM, Senior RM, Shibuya M. 2002.MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer Cell 2: 289-300.
29. Hong JH, Yaffe MB. 2006. TAZ: A b-catenin-like molecule that regulates mesenchymal stem cell differentiation. Cell Cycle 5: 176-179.
30. Hong JH, Hwang ES, McManus MT, Amsterdam A, Tian Y, Kalmukova R, Mueller E, Benjamin T, Spiegelman BM, Sharp PA, et al. 2005. TAZ, a transcriptional modulator of mesenchymal stem cell differentiation. Science 309: 1074-1078.
31. Hossain Z, Ali SM, Ko HL, Xu J, Ng CP, Guo K, Qi Z, Ponniah S, Hong W, Hunziker W. 2007. Glomerulocystic kidney disease in mice with a targeted inactivation of Wwtr1. Proc Natl Acad Sci 104: 1631-1636.
32. Huang J, Wu S, Barrera J, Matthews K, Pan D. 2005. The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila Homolog of YAP. Cell 122: 421-434.
33. Huang DW, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
34. Huse JT, Holland EC. 2010. Targeting brain cancer: Advances in the molecular pathology of malignant glioma and medulloblastoma. Nat Rev Cancer 10: 319-331.
35. Huse JT, Phillips HS, Brennan CW. 2011. Molecular subclassification of diffuse gliomas: Seeing order in the chaos. Glia 59: 1190-1199.
36. Kalluri R, Weinberg RA. 2009. The basics of epithelial- mesenchymal transition. J Clin Invest 119: 1420-1428.
37. Komuro A, Nagai M, Navin NE, Sudol M. 2003. WW domaincontaining protein YAP associates with ErbB-4 and acts as a co-transcriptional activator for the carboxyl-terminal fragment of ErbB-4 that translocates to the nucleus. J Biol Chem 278: 33334-33341.
38. Kudo-Saito C, Shirako H, Takeuchi T, Kawakami Y. 2009. Cancer metastasis is accelerated through immunosuppression during Snail-induced EMT of cancer cells. Cancer Cell 15: 195-206.
39. Lal S, Lacroix M, Tofilon P, Fuller GN, Sawaya R, Lang FF. 2000. An implantable guide-screw system for brain tumor studies in small animals. J Neurosurg 92: 326-333.
40. Lei QY, Zhang H, Zhao B, Zha ZY, Bai F, Pei XH, Zhao S, Xiong Y, Guan KL. 2008. TAZ promotes cell proliferation and epithelial-mesenchymal transition and is inhibited by the hippo pathway. Mol Cell Biol 28: 2426-2436.
41. Lei L, Sonabend AM, Guarnieri P, Soderquist C, Ludwig T, Rosenfeld S, Bruce JN, Canoll P. 2011. Glioblastoma models reveal the connection between adult glial progenitors and the proneural phenotype. PLoS ONE 6: e20041. doi: 10.1371/journal.pone.0020041.
42. Li A, Walling J, Ahn S, Kotliarov Y, Su Q, Quezado M, Oberholtzer JC, Park J, Zenklusen JC, Fine HA. 2009. Unsupervised analysis of transcriptomic profiles reveals six glioma subtypes. Cancer Res 69: 2091-2099.
43. Lian I, Kim J, Okazawa H, Zhao J, Zhao B, Yu J, Chinnaiyan A, Israel MA, Goldstein LS, Abujarour R, et al. 2010. The role of YAP transcription coactivator in regulating stem cell selfrenewal and differentiation. Genes Dev 24: 1106-1118.
44. Lindberg N, Kastemar M, Olofsson T, Smits A, Uhrbom L. 2009. Oligodendrocyte progenitor cells can act as cell of origin for experimental glioma. Oncogene 28: 2266-2275.
45. Liu CY, Zha ZY, Zhou X, Zhang H, Huang W, Zhao D, Li T, Chan SW, Lim CJ, Hong W, et al. 2010. The hippo tumor pathway promotes TAZ degradation by phosphorylating a phosphodegron and recruiting the SCFb-TrCP E3 ligase. J Biol Chem 285: 37159-37169.
46. Liu C, Sage JC, Miller MR, Verhaak RG, Hippenmeyer S, Vogel H, Foreman O, Bronson RT, Nishiyama A, Luo L, et al. 2011. Mosaic analysis with double markers reveals tumor cell of origin in glioma. Cell 146: 209-221.
47. Makita R, Uchijima Y, Nishiyama K, Amano T, Chen Q, Takeuchi T, Mitani A, Nagase T, Yatomi Y, Aburatani H, et al. 2008. Multiple renal cysts, urinary concentration defects, and pulmonary emphysematous changes in mice lacking TAZ. Am J Physiol Renal Physiol 294: F542-F553. doi: 10.1152/ajprenal.00201.2007.
48. Mani SA, Yang J, Brooks M, Schwaninger G, Zhou A, Miura N, Kutok JL, Hartwell K, Richardson AL, Weinberg RA. 2007. Mesenchyme Forkhead 1 (FOXC2) plays a key role in metastasis and is associated with aggressive basal-like breast cancers. Proc Natl Acad Sci 104: 10069-10074.
49. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, et al. 2008. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715.
50. Margolin AA, Wang K, Lim WK, Kustagi M, Nemenman I, Califano A. 2006. Reverse engineering cellular networks. Nat Protoc 1: 662-671.
51. Martinez J, Chalupowicz DG, Roush RK, Sheth A, Barsigian C. 1994. Transglutaminase-mediated processing of fibronectin by endothelial cell monolayers. Biochemistry 33: 2538-2545.
52. Meloan SN, Puchtler H, Valentine LS. 1972. Alkaline and acid alizarin red S stains for alkali-soluble and alkali-insoluble calcium deposits. Arch Pathol 93: 190-197.
53. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstrale M, Laurila E, et al. 2003. PGC-1a-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34: 267-273.
54. Morin-Kensicki EM, Boone BN, Howell M, Stonebraker JR, Teed J, Alb JG, Magnuson TR, O'Neal W, Milgram SL. 2006. Defects in yolk sac vasculogenesis, chorioallantoic fusion, and embryonic axis elongation in mice with targeted disruption of Yap65. Mol Cell Biol 26: 77-87.
55. Murakami M, Nakagawa M, Olson EN, Nakagawa O. 2005. AWWdomain protein TAZ is a critical coactivator for TBX5, a transcription factor implicated in Holt-Oram syndrome. Proc Natl Acad Sci 102: 18034-18039.
56. Murakami M, Tominaga J, Makita R, Uchijima Y, Kurihara Y, Nakagawa O, Asano T, Kurihara H. 2006. Transcriptional activity of Pax3 is co-activated by TAZ. Biochem Biophys Res Commun 339: 533-539.
57. Nakajima Y, Mironov V, Yamagishi T, Nakamura H, Markwald RR. 1997. Expression of smooth muscle a-actin in mesenchymal cells during formation of avian endocardial cushion tissue: A role for transforming growth factor b3. Dev Dyn 209: 296-309.
58. Nigro JM, Misra A, Zhang L, Smirnov I, Colman H, Griffin C, Ozburn N, Chen M, Pan E, Koul D, et al. 2005. Integrated array-comparative genomic hybridization and expression array profiles identify clinically relevant molecular subtypes of glioblastoma. Cancer Res 65: 1678-1686.
59. Noushmehr H, Weisenberger DJ, Diefes K, Phillips HS, Pujara K, Berman BP, Pan F, Pelloski CE, Sulman EP, Bhat KP, et al. 2010. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 17: 510-522.
60. Palii SS, Robertson KD. 2007. Epigenetic control of tumor suppression. Crit Rev Eukaryot Gene Expr 17: 295-316.
61. Pan D. 2010. The hippo signaling pathway in development and cancer. Dev Cell 19: 491-505.
62. Park SM, Gaur AB, Lengyel E, Peter ME. 2008. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 22: 894-907.
63. Pelloski CE, Mahajan A, Maor M, Chang EL, Woo S, Gilbert M, Colman H, Yang H, Ledoux A, Blair H, et al. 2005. YKL-40 expression is associated with poorer response to radiation and shorter overall survival in glioblastoma. Clin Cancer Res 11: 3326-3334.
64. Penuelas S, Anido J, Prieto-Sanchez RM, Folch G, Barba I, Cuartas I, Garcia-Dorado D, Poca MA, Sahuquillo J, Baselga J, et al. 2009. TGF-b increases glioma-initiating cell self-renewal through the induction of LIF in human glioblastoma. Cancer Cell 15: 315-327.
65. Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH, Wu TD, Misra A, Nigro JM, Colman H, Soroceanu L, et al. 2006. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 9: 157-173.
66. Remue E, Meerschaert K, Oka T, Boucherie C, Vandekerckhove J, Sudol M, Gettemans J. 2010. TAZ interacts with zonula occludens-1 and -2 proteins in a PDZ-1 dependent manner. FEBS Lett 584: 4175-4180.
67. Ridet JL, Malhotra SK, Privat A, Gage FH. 1997. Reactive astrocytes: Cellular and molecular cues to biological function. Trends Neurosci 20: 570-577.
68. Rosenberg L. 1971. Chemical basis for the histological use of safranin O in the study of articular cartilage. J Bone Joint Surg Am 53: 69-82.
69. Sawada A, Kiyonari H, Ukita K, Nishioka N, Imuta Y, Sasaki H. 2008. Redundant roles of Tead1 and Tead2 in notochord development and the regulation of cell proliferation and survival. Mol Cell Biol 28: 3177-3189.
70. Schieker M, Pautke C, Reitz K, Hemraj I, Neth P, Mutschler W, Milz S. 2004. The use of four-colour immunofluorescence techniques to identify mesenchymal stem cells. J Anat 204: 133-139.
71. Schieker M, Pautke C, Haasters F, Schieker J, Docheva D, Bocker W, Guelkan H, Neth P, Jochum M, Mutschler W. 2007. Human mesenchymal stem cells at the single-cell level: Simultaneous seven-colour immunofluorescence. J Anat 210: 592-599.
72. Schlegelmilch K, Mohseni M, Kirak O, Pruszak J, Rodriguez JR, Zhou D, Kreger BT, Vasioukhin V, Avruch J, Brummelkamp TR, et al. 2011. Yap1 acts downstream of a-catenin to control epidermal proliferation. Cell 144: 782-795.
73. Sher F, Rossler R, Brouwer N, Balasubramaniyan V, Boddeke E, Copray S. 2008. Differentiation of neural stem cells into oligodendrocytes: Involvement of the polycomb group protein Ezh2. Stem Cells 26: 2875-2883.
74. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, et al. 2005. Gene set enrichment analysis: A knowledgebased approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci 102: 15545-15550.
75. Sugiarto S, Persson AI, Munoz EG, Waldhuber M, Lamagna C, Andor N, Hanecker P, Ayers-Ringler J, Phillips J, Siu J, et al. 2011. Asymmetry-defective oligodendrocyte progenitors are glioma precursors. Cancer Cell 20: 328-340.
76. Takizawa T, Nakashima K, Namihira M, Ochiai W, Uemura A, Yanagisawa M, Fujita N, Nakao M, Taga T. 2001. DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev Cell 1: 749-758.
77. Thiery JP, Acloque H, Huang RY, Nieto MA. 2009. Epithelial-mesenchymal transitions in development and disease. Cell 139: 871-890.
78. Uhrbom L, Holland EC. 2001. Modeling gliomagenesis with somatic cell gene transfer using retroviral vectors. J Neurooncol 53: 297-305.
79. Varelas X, Sakuma R, Samavarchi-Tehrani P, Peerani R, Rao BM, Dembowy J, Yaffe MB, Zandstra PW, Wrana JL. 2008. TAZ controls Smad nucleocytoplasmic shuttling and regulates human embryonic stem-cell self-renewal. Nat Cell Biol 10: 837-848.
80. Varelas X, Miller BW, Sopko R, Song S, Gregorieff A, Fellouse FA, Sakuma R, Pawson T, Hunziker W, McNeill H, et al. 2010a. The Hippo pathway regulates Wnt/b-catenin signaling. Dev Cell 18: 579-591.
81. Varelas X, Samavarchi-Tehrani P, Narimatsu M, Weiss A, Cockburn K, Larsen BG, Rossant J, Wrana JL. 2010b. The Crumbs complex couples cell density sensing to Hippodependent control of the TGF-b-SMAD pathway. Dev Cell 19: 831-844.
82. Vassilev A, Kaneko KJ, Shu H, Zhao Y, DePamphilis ML. 2001. TEAD/TEF transcription factors utilize the activation domain of YAP65, a Src/Yes-associated protein localized in the cytoplasm. Genes Dev 15: 1229-1241.
83. Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, Miller CR, Ding L, Golub T, Mesirov JP, et al. 2010. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17: 98-110.
84. Ward RJ, Lee L, Graham K, Satkunendran T, Yoshikawa K, Ling E, Harper L, Austin R, Nieuwenhuis E, Clarke ID, et al. 2009. Multipotent CD15+ cancer stem cells in patched-1-deficient mouse medulloblastoma. Cancer Res 69: 4682-4690.
85. Wicki A, Lehembre F, Wick N, Hantusch B, Kerjaschki D, Christofori G. 2006. Tumor invasion in the absence of epithelial-mesenchymal transition: Podoplanin-mediated remodeling of the actin cytoskeleton. Cancer Cell 9: 261-272.
86. Yagi R, Chen LF, Shigesada K, Murakami Y, Ito Y. 1999. AWW domain-containing yes-associated protein (YAP) is a novel transcriptional co-activator. EMBO J 18: 2551-2562.
87. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA. 2004. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117: 927-939.
88. Zhang H, Liu CY, Zha ZY, Zhao B, Yao J, Zhao S, Xiong Y, Lei QY, Guan KL. 2009. TEAD transcription factors mediate the function of TAZ in cell growth and epithelial-mesenchymal transition. J Biol Chem 284: 13355-13362.
89. Zhao B, Lei QY, Guan KL. 2008a. The Hippo-YAP pathway: New connections between regulation of organ size and cancer. Curr Opin Cell Biol 20: 638-646.
90. Zhao B, Ye X, Yu J, Li L, Li W, Li S, Lin JD, Wang CY, Chinnaiyan AM, Lai ZC, et al. 2008b. TEAD mediates YAP-dependent gene induction and growth control. Genes Dev 22: 1962-1971.
91. Zhao Q, Guo X, Nash GB, Stone PC, Hilkens J, Rhodes JM, Yu LG. 2009. Circulating galectin-3 promotes metastasis by modifying MUC1 localization on cancer cell surface. Cancer Res 69: 6799-6806.
92. Zhao B, Li L, Lei Q, Guan KL. 2010. The Hippo-YAP pathway in organ size control and tumorigenesis: An updated version. Genes Dev 24: 862-874.
93. Zhao B, Li L, Lu Q, Wang LH, Liu CY, Lei Q, Guan KL. 2011. Angiomotin is a novel Hippo pathway component that inhibits YAP oncoprotein. Genes Dev 25: 51-63.