YAP promotes breast cell proliferation and survival partially through stabilizing the KLF5 transcription factor

American Journal of Pathology

Volumn 180, Issue 6, 2012, Pages 2452-2461

  Zhi, Xu ^a,b   Zhao, Dong ^a,b   Zhou, Zhongmei ^a   Liu, Rong ^a   Chen, Ceshi ^a  

^a KUNMING INSTITUTE OF ZOOLOGY   (China)

^b ALBANY MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN RECEPTOR ALPHA; KRUPPEL LIKE FACTOR 5; LENTIVIRUS VECTOR; ONCOPROTEIN; RETROVIRUS VECTOR; TUMOR SUPPRESSOR PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; YES ASSOCIATED PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BREAST CANCER; BREAST CELL; CANCER CELL CULTURE; CANCER THERAPY; CARCINOGENESIS; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME INDUCTION; FEMALE; GENE OVEREXPRESSION; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR VOLUME; TUMOR XENOGRAFT; UBIQUITINATION;

ANIMALS; BREAST; BREAST NEOPLASMS; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION, NEOPLASTIC; FEMALE; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICE, SCID; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, ESTROGEN; RNA, SMALL INTERFERING; TRANSCRIPTION FACTORS; TRANSPLANTATION, HETEROLOGOUS; TUMOR CELLS, CULTURED;

EID: 84861650780     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.02.025     Document Type: Article

References (54)

1. K. Wang, C. Degerny, M. Xu, X.J. Yang YAP, TAZ, and Yorkie: a conserved family of signal-responsive transcriptional coregulators in animal development and human disease Biochem Cell Biol 87 2009 77 91
2. B. Zhao, L. Li, Q. Lei, K.L. Guan The Hippo-YAP pathway in organ size control and tumorigenesis: an updated version Genes Dev 24 2010 862 874
3. L. Zender, M.S. Spector, W. Xue, P. Flemming, C. Cordon-Cardo, J. Silke, S.T. Fan, J.M. Luk, M. Wigler, G.J. Hannon, D. Mu, R. Lucito, S. Powers, S.W. Lowe Identification and validation of oncogenes in liver cancer using an integrative oncogenomic approach Cell 125 2006 1253 1267
4. J. Dong, G. Feldmann, J. Huang, S. Wu, N. Zhang, S.A. Comerford, M.F. Gayyed, R.A. Anders, A. Maitra, D. Pan Elucidation of a universal size-control mechanism in Drosophila and mammals Cell 130 2007 1120 1133
5. M. Overholtzer, J. Zhang, G.A. Smolen, B. Muir, W. Li, D.C. Sgroi, C.X. Deng, J.S. Brugge, D.A. Haber Transforming properties of YAP, a candidate oncogene on the chromosome 11q22 amplicon Proc Natl Acad Sci USA 103 2006 12405 12410
6. X. Zhang, J. George, S. Deb, J.L. Degoutin, E.A. Takano, S.B. Fox, D.D. Bowtell, K.F. Harvey AOCS Study group The Hippo pathway transcriptional co-activator YAP, is an ovarian cancer oncogene Oncogene 30 2011 2810 2822
7. M.Z. Xu, T.J. Yao, N.P. Lee, I.O. Ng, Y.T. Chan, L. Zender, S.W. Lowe, R.T. Poon, J.M. Luk Yes-associated protein is an independent prognostic marker in hepatocellular carcinoma Cancer 115 2009 4576 4585
8. M.Z. Xu, S.W. Chan, A.M. Liu, K.F. Wong, S.T. Fan, J. Chen, R.T. Poon, L. Zender, S.W. Lowe, W. Hong, J.M. Luk AXL receptor kinase is a mediator of YAP-dependent oncogenic functions in hepatocellular carcinoma Oncogene 30 2011 1229 1240
9. T. Muramatsu, I. Imoto, T. Matsui, K. Kozaki, S. Haruki, M. Sudol, Y. Shimada, H. Tsuda, T. Kawano, J. Inazawa YAP is a candidate oncogene for esophageal squamous cell carcinoma Carcinogenesis 32 2011 389 398
10. J.H. Hsu, E.R. Lawlor BMI-1 suppresses contact inhibition and stabilizes YAP in Ewing sarcoma Oncogene 30 2011 2077 2085
11. B. Zhao, Q.Y. Lei, K.L. Guan The Hippo-YAP pathway: new connections between regulation of organ size and cancer Curr Opin Cell Biol 20 2008 638 646
12. J. Zhang, G.A. Smolen, D.A. Haber Negative regulation of YAP by LATS1 underscores evolutionary conservation of the Drosophila Hippo pathway Cancer Res 68 2008 2789 2794
13. B. Zhao, J. Kim, X. Ye, Z.C. Lai, K.L. Guan Both TEAD-binding and WW domains are required for the growth stimulation and oncogenic transformation activity of yes-associated protein Cancer Res 69 2009 1089 1098
14. F.D. Camargo, S. Gokhale, J.B. Johnnidis, D. Fu, G.W. Bell, R. Jaenisch, T.R. Brummelkamp YAP1 increases organ size and expands undifferentiated progenitor cells [Erratum appeared in Curr Biol 2007, 17:2094] Curr Biol 17 2007 2054 2060
15. B. Zhao, X. Ye, J. Yu, L. Li, W. Li, S. Li, J. Yu, J.D. Lin, C.Y. Wang, A.M. Chinnaiyan, Z.C. Lai, K.L. Guan TEAD mediates YAP-dependent gene induction and growth control Genes Dev 22 2008 1962 1971
16. H. Zhang, C.Y. Liu, Z.Y. Zha, B. Zhao, J. Yao, S. Zhao, Y. Xiong, Q.Y. Lei, K.L. Guan TEAD transcription factors mediate the function of TAZ in cell growth and epithelial-mesenchymal transition J Biol Chem 284 2009 13355 13362
17. S. Basu, N.F. Totty, M.S. Irwin, M. Sudol, 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
18. D. Levy, Y. Adamovich, N. Reuven, Y. Shaul The Yes-associated protein 1 stabilizes p73 by preventing Itch-mediated ubiquitination of p73 Cell Death Differ 14 2007 743 751
19. M. Zagurovskaya, M.M. Shareef, A. Das, A. Reeves, S. Gupta, M. Sudol, M.T. Bedford, J. Prichard, M. Mohiuddin, M.M. Ahmed EGR-1 forms a complex with YAP-1 and upregulates Bax expression in irradiated prostate carcinoma cells Oncogene 28 2009 1121 1131
20. J. Omerovic, E.M. Puggioni, S. Napoletano, V. Visco, R. Fraioli, L. Frati, A. Gulino, M. Alimandi Ligand-regulated association of ErbB-4 to the transcriptional co-activator YAP65 controls transcription at the nuclear level Exp Cell Res 294 2004 469 479
21. R.I. Aqeilan, V. Donati, A. Palamarchuk, F. Trapasso, M. Kaou, Y. Pekarsky, M. Sudol, C.M. Croce WW domain-containing proteins, WWOX and YAP, compete for interaction with ErbB-4 and modulate its transcriptional function Cancer Res 65 2005 6764 6772
22. R.S. Muraoka-Cook, M. Sandahl, D. Hunter, L. Miraglia, H.S. Earp 3rd Prolactin and ErbB4/HER4 signaling interact via Janus kinase 2 to induce mammary epithelial cell gene expression differentiation Mol Endocrinol 22 2008 2307 2321
23. M.I. Vitolo, I.E. Anglin, W.M. Mahoney Jr, K.J. Renoud, R.B. Gartenhaus, K.E. Bachman, A. Passaniti The RUNX2 transcription factor cooperates with the YES-associated protein, YAP65, to promote cell transformation Cancer Biol Ther 6 2007 856 863
24. X. Zhang, C.C. Milton, P.O. Humbert, K.F. Harvey Transcriptional output of the Salvador/Warts/Hippo pathway is controlled in distinct fashions in Drosophila melanogaster and mammalian cell lines Cancer Res 69 2009 6033 6041
25. I. Ben-Porath, M.W. Thomson, V.J. Carey, R. Ge, G.W. Bell, A. Regev, R.A. Weinberg An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors Nat Genet 40 2008 499 507
26. D. Tong, K. Czerwenka, G. Heinze, M. Ryffel, E. Schuster, A. Witt, S. Leodolter, R. Zeillinger Expression of KLF5 is a prognostic factor for disease-free survival and overall survival in patients with breast cancer Clin Cancer Res 12 2006 2442 2448
27. C. Chen, M.S. Benjamin, X. Sun, K.B. Otto, P. Guo, X.Y. Dong, Y. Bao, Z. Zhou, X. Cheng, J.W. Simons, J.T. Dong KLF5 promotes cell proliferation and tumorigenesis through gene regulation in the TSU-Pr1 human bladder cancer cell line Int J Cancer 118 2006 1346 1355
28. H.Q. Zheng, Z. Zhou, J. Huang, L. Chaudhury, J.T. Dong, C. Chen Krüppel-like factor 5 promotes breast cell proliferation partially through upregulating the transcription of fibroblast growth factor binding protein 1 Oncogene 28 2009 3702 3713
29. R. Liu, H.Q. Zheng, Z. Zhou, J.T. Dong, C. Chen KLF5 promotes breast cell survival partially through fibroblast growth factor-binding protein 1-pERK-mediated dual specificity MKP-1 protein phosphorylation and stabilization J Biol Chem 284 2009 16791 16798
30. C. Chen, X. Sun, Q. Ran, K.D. Wilkinson, T.J. Murphy, J.W. Simons, J.T. Dong Ubiquitin-proteasome degradation of KLF5 transcription factor in cancer and untransformed epithelial cells Oncogene 24 2005 3319 3327
31. C. Chen, X. Sun, P. Guo, X.Y. Dong, P. Sethi, X. Cheng, J. Zhou, J. Ling, J.W. Simons, J.B. Lingrel, J.T. Dong Human Krüppel-like factor 5 is a target of the E3 ubiquitin ligase WWP1 for proteolysis in epithelial cells J Biol Chem 280 2005 41553 41561
32. D. Zhao, H.Q. Zheng, Z. Zhou, C. Chen The Fbw7 tumor suppressor targets KLF5 for ubiquitin-mediated degradation and suppresses breast cell proliferation Cancer Res 70 2010 4728 4738
33. S. Parisi, F. Passaro, L. Aloia, I. Manabe, R. Nagai, L. Pastore, T. Russo Klf5 is involved in self-renewal of mouse embryonic stem cells J Cell Sci 121 2008 2629 2634
34. I. Lian, J. Kim, H. Okazawa, J. Zhao, B. Zhao, J. Yu, A. Chinnaiyan, M.A. Israel, L.S. Goldstein, R. Abujarour, S. Ding, K.L. Guan The role of YAP transcription coactivator in regulating stem cell self-renewal and differentiation Genes Dev 24 2010 1106 1118
35. C. Chen, Z. Zhou, J.S. Ross, W. Zhou, J.T. Dong The amplified WWP1 gene is a potential molecular target in breast cancer Int J Cancer 121 2007 80 87
36. C. Chen, Y. Zhou, Z. Zhou, X. Sun, K.B. Otto, R.M. Uht, J.T. Dong Regulation of KLF5 involves the Sp1 transcription factor in human epithelial cells Gene 330 2004 133 142
37. B.L. Chang, S.D. Cramer, F. Wiklund, S.D. Isaacs, V.L. Stevens, J. Sun, S. Smith, K. Pruett, L.M. Romero, K.E. Wiley, S.T. Kim, Y. Zhu, Z. Zhang, F.C. Hsu, A.R. Turner, J. Adolfsson, W. Liu, J.W. Kim, D. Duggan, J. Carpten, S.L. Zheng, C. Rodriguez, W.B. Isaacs, H. Grönberg, J. Xu Fine mapping association study and functional analysis implicate a SNP in MSMB at 10q11 as a causal variant for prostate cancer risk Hum Mol Genet 18 2009 1368 1375
38. Y. Hao, A. Chun, K. Cheung, B. Rashidi, X. Yang Tumor suppressor LATS1 is a negative regulator of oncogene YAP J Biol Chem 283 2008 5496 5509
39. C. Chen, Z. Zhou, C.E. Sheehan, E. Slodkowska, C.B. Sheehan, A. Boguniewicz, J.S. Ross Overexpression of WWP1 is associated with the estrogen receptor and insulin-like growth factor receptor 1 in breast carcinoma Int J Cancer 124 2009 2829 2836
40. M. Yuan, V. Tomlinson, R. Lara, D. Holliday, C. Chelala, T. Harada, R. Gangeswaran, C. Manson-Bishop, P. Smith, S.A. Danovi, O. Pardo, T. Crook, C.A. Mein, N.R. Lemoine, L.J. Jones, S. Basu Yes-associated protein (YAP) functions as a tumor suppressor in breast Cell Death Differ 15 2008 1752 1759
41. M.O. Nandan, B.B. McConnell, A.M. Ghaleb, A.B. Bialkowska, H. Sheng, J. Shao, B.A. Babbin, S. Robine, V.W. Yang Krüppel-like factor 5 mediates cellular transformation during oncogenic KRAS-induced intestinal tumorigenesis Gastroenterology 134 2008 120 130
42. B.B. McConnell, A.B. Bialkowska, M.O. Nandan, A.M. Ghaleb, F.J. Gordon, V.W. Yang Haploinsufficiency of Krüppel-like factor 5 rescues the tumor-initiating effect of the Apc(Min) mutation in the intestine Cancer Res 69 2009 4125 4133
43. P. Guo, X.Y. Dong, K. Zhao, X. Sun, Q. Li, J.T. Dong Opposing effects of KLF5 on the transcription of MYC in epithelial proliferation in the context of transforming growth factor beta J Biol Chem 284 2009 28243 28252
44. J. Zhang, J.Y. Ji, M. Yu, M. Overholtzer, G.A. Smolen, R. Wang, J.S. Brugge, N.J. Dyson, D.A. Haber YAP-dependent induction of amphiregulin identifies a non-cell-autonomous component of the Hippo pathway Nat Cell Biol 11 2009 1444 1450
45. J.T. Dong, C. Chen Essential role of KLF5 transcription factor in cell proliferation and differentiation and its implications for human diseases Cell Mol Life Sci 66 2009 2691 2706
46. E. Tassi, R.T. Henke, E.T. Bowden, M.R. Swift, D.P. Kodack, A.H. Kuo, A. Maitra, A. Wellstein Expression of a fibroblast growth factor-binding protein during the development of adenocarcinoma of the pancreas and colon Cancer Res 66 2006 1191 1198
47. B.B. McConnell, J.M. Klapproth, M. Sasaki, M.O. Nandan, V.W. Yang Krüppel-like factor 5 mediates transmissible murine colonic hyperplasia caused by Citrobacter rodentium infection Gastroenterology 134 2008 1007 1016
48. J. Cai, N. Zhang, Y. Zheng, R.F. de Wilde, A. Maitra, D. Pan The Hippo signaling pathway restricts the oncogenic potential of an intestinal regeneration program Genes Dev 24 2010 2383 2388
49. C.A. Hall, R. Wang, J. Miao, E. Oliva, X. Shen, T. Wheeler, S.G. Hilsenbeck, S. Orsulic, S. Goode Hippo pathway effector Yap is an ovarian cancer oncogene Cancer Res 70 2010 8517 8525
50. Y. Wang, Q. Dong, Q. Zhang, Z. Li, E. Wang, X. Qiu Overexpression of yes-associated protein contributes to progression and poor prognosis of non-small-cell lung cancer Cancer Sci 101 2010 1279 1285
51. R. Ehsanian, M. Brown, H. Lu, X.P. Yang, A. Pattatheyil, B. Yan, P. Duggal, R. Chuang, J. Doondeea, S. Feller, M. Sudol, Z. Chen, C. Van Waes YAP dysregulation by phosphorylation or DeltaNp63-mediated gene repression promotes proliferation, survival and migration in head and neck cancer subsets Oncogene 29 2010 6160 6171
52. E. Lapi, S. Di Agostino, S. Donzelli, H. Gal, E. Domany, G. Rechavi, P.P. Pandolfi, D. Givol, S. Strano, X. Lu, G. Blandino PML, YAP, and p73 are components of a proapoptotic autoregulatory feedback loop Mol Cell 32 2008 803 814
53. T. Oka, M. Sudol Nuclear localization and pro-apoptotic signaling of YAP2 require intact PDZ-binding motif Genes Cells 14 2009 607 615
54. N. Zhang, H. Bai, K.K. David, J. Dong, Y. Zheng, J. Cai, M. Giovannini, P. Liu, R.A. Anders, D. Pan The Merlin/NF2 tumor suppressor functions through the YAP oncoprotein to regulate tissue homeostasis in mammals Dev Cell 19 2010 27 38