RAF kinase inhibitor-independent constitutive activation of Yes-associated protein 1 promotes tumor progression in thyroid cancer

Oncogenesis

Volumn 2, Issue , 2013, Pages

  Lee, S E ^a   Lee, J U ^b   Lee, M H ^a   Ryu, M J ^a   Kim, S J ^a   Kim, Y K ^a   Choi, M J ^a   Kim, K S ^a   Kim, J M ^c   Kim, J W ^d   Koh, Y W ^e   Lim, D S ^f   Jo, Y S ^a   Shong, M ^a  

^a Chungnam National University   (South Korea)

^b Daejeon St Mary's Hospital   (South Korea)

^c Chungnam National University College of Medicine   (South Korea)

^d Soonchunhyang University College of Medicine   (South Korea)

^e Yonsei University College of Medicine   (South Korea)

^f Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

Author keywords

drug resistance; molecular targeted therapy; orthotopic model; proto oncogene proteins B Raf; thyroid neoplasm; Yes associated protein 1

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; N [3 (5 CHLORO 1H PYRROLO[2,3 B]PYRIDINE 3 CARBONYL) 2,4 DIFLUOROPHENYL]PROPANESULFONAMIDE; SORAFENIB; TRANSCRIPTION FACTOR YAP1;

ANAPLASTIC THYROID CANCER; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL CULTURE; CELL DENSITY; CONTROLLED STUDY; DISTANT METASTASIS; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MOUSE; MUTATION; NONHUMAN; PAPILLARY THYROID CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; THYROID CANCER; TUMOR GROWTH; TUMOR VOLUME; TUMOR XENOGRAFT;

EID: 84880549551     PISSN: None     EISSN: 21579024     Source Type: Journal    
DOI: 10.1038/oncsis.2013.12     Document Type: Article

References (60)

1. Cohen Y, Xing M, Mambo E, Guo Z, Wu G, Trink B et al. BRAF mutation in papillary thyroid carcinoma. J Natl Cancer Inst 2003; 95: 625-627. (Pubitemid 36553510)
2. Kondo T, Ezzat S, Asa SL. Pathogenetic mechanisms in thyroid follicular-cell neoplasia. Nat Rev Cancer 2006; 6: 292-306.
3. Pratilas CA, Taylor BS, Ye Q, Viale A, Sander C, Solit DB et al. (V600E)BRAF is associated with disabled feedback inhibition of RAF-MEK signaling and elevated transcriptional output of the pathway. Proc Natl Acad Sci USA 2009; 106: 4519-4524.
4. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S et al. Mutations of the BRAF gene in human cancer. Nature 2002; 417: 949-954. (Pubitemid 34716871)
5. Kimura ET, Nikiforova MN, Zhu Z, Knauf JA, Nikiforov YE, Fagin JA. High prevalence of BRAF mutations in thyroid cancer: genetic evidence for constitutive activation of the RET/PTC-RAS-BRAF signaling pathway in papillary thyroid carcinoma. Cancer Res 2003; 63: 1454-1457. (Pubitemid 36373628)
6. Puxeddu E, Durante C, Avenia N, Filetti S, Russo D. Clinical implications of BRAF mutation in thyroid carcinoma. Trends Endocrinol Metab 2008; 19: 138-145. (Pubitemid 351621952)
7. Soares P, Trovisco V, Rocha AS, Lima J, Castro P, Preto A et al. BRAF mutations and RET/PTC rearrangements are alternative events in the etiopathogenesis of PTC. Oncogene 2003; 22: 4578-4580. (Pubitemid 36920701)
8. Nikiforova MN, Kimura ET, Gandhi M, Biddinger PW, Knauf JA, Basolo F et al. BRAF mutations in thyroid tumors are restricted to papillary carcinomas and anaplastic or poorly differentiated carcinomas arising from papillary carcinomas. J Clin Endocrinol Metab 2003; 88: 5399-5404. (Pubitemid 37452745)
9. Hong DS, Cabanillas ME, Wheler J, Naing A, Tsimberidou AM, Ye L et al. Inhibition of the Ras/Raf/MEK/ERK and RET kinase pathways with the combination of the multikinase inhibitor sorafenib and the farnesyltransferase inhibitor tipifarnib in medullary and differentiated thyroid malignancies. J Clin Endocrinol Metab 2011; 96: 997-1005.
10. Nikiforov YE, Nikiforova MN. Molecular genetics and diagnosis of thyroid cancer. Nat Rev Endocrinol 2011; 7: 569-580.
11. Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ et al. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2009; 19: 1167-1214.
12. Ota M, Sasaki H. Mammalian Tead proteins regulate cell proliferation and contact inhibition as transcriptional mediators of Hippo signaling. Development 2008; 135: 4059-4069.
13. Saucedo LJ, Edgar BA. Filling out the Hippo pathway. Nat Rev Mol Cell Biol 2007; 8: 613-621. (Pubitemid 47106618)
14. Edgar BA. From cell structure to transcription: Hippo forges a new path. Cell 2006; 124: 267-273. (Pubitemid 43121976)
15. Zhao B, Li L, Lei Q, Guan KL. The Hippo-YAP pathway in organ size control and tumorigenesis: an updated version. Genes Dev 2010; 24: 862-874.
16. Dong J, Feldmann G, Huang J, Wu S, Zhang N, Comerford SA et al. Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 2007; 130: 1120-1133. (Pubitemid 47410268)
17. Oh H, Irvine KD. In vivo regulation of Yorkie phosphorylation and localization. Development 2008; 135: 1081-1088. (Pubitemid 351578136)
18. Zhao B, Wei X, Li W, Udan RS, Yang Q, Kim J 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. (Pubitemid 350070721)
19. Steinhardt AA, Gayyed MF, Klein AP, Dong J, Maitra A, Pan D et al. Expression of Yes-associated protein in common solid tumors. Hum Pathol 2008; 39: 1582-1589.
20. Wang K, Degerny C, Xu M, Yang XJ. YAP, TAZ, and Yorkie: a conserved family of signal-responsive transcriptional coregulators in animal development and human disease. Biochem Cell Biol 2009; 87: 77-91.
21. Zheng T, Wang J, Jiang H, Liu L. Hippo signaling in oval cells and hepatocarcinogenesis. Cancer Lett 2011; 302: 91-99.
22. Xu MZ, Yao TJ, Lee NP, Ng IO, Chan YT, Zender L et al. Yes-associated protein is an independent prognostic marker in hepatocellular carcinoma. Cancer 2009; 115: 4576-4585.
23. O'Neill E, Rushworth L, Baccarini M, Kolch W. Role of the kinase MST2 in suppression of apoptosis by the proto-oncogene product Raf-1. Science 2004; 306: 2267-2270. (Pubitemid 40024466)
24. O'Neill E, Kolch W. Taming the Hippo: Raf-1 controls apoptosis by suppressing MST2/Hippo. Cell Cycle 2005; 4: 365-367. (Pubitemid 41359716)
25. Romano D, Matallanas D, Weitsman G, Preisinger C, Ng T, Kolch W. Proapoptotic kinase MST2 coordinates signaling crosstalk between RASSF1A, Raf-1, and Akt. Cancer Res 2010; 70: 1195-1203.
26. Doggett K, Grusche FA, Richardson HE, Brumby AM. 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 2011; 11: 57.
27. Lee SJ, Lee MH, Kim DW, Lee S, Huang S, Ryu MJ et al. Cross-regulation between oncogenic BRAF(V600E) kinase and the MST1 pathway in papillary thyroid carcinoma. PLoS One 2011; 6: e16180.
28. Kim NG, Koh E, Chen X, Gumbiner BM. E-cadherin mediates contact inhibition of proliferation through Hippo signaling-pathway components. Proc Natl Acad Sci USA 2011; 108: 11930-11935.
29. Zhao B, Ye X, Yu J, Li L, Li W, Li S et al. TEAD mediates YAP-dependent gene induction and growth control. Genes Dev 2008; 22: 1962-1971. (Pubitemid 352008643)
30. Ito T, Seyama T, Hayashi Y, Hayashi T, Dohi K, Mizuno T et al. Establishment of 2 human thyroid-carcinoma cell-lines (8305c, 8505c) bearing p53 gene-mutations. Int J Oncol 1994; 4: 583-586. (Pubitemid 24091390)
31. Ceraline J, Deplanque G, Noel F, Natarajan-Ame S, Bergerat JP, Klein-Soyer C. Sensitivity to cisplatin treatment of human K1 thyroid carcinoma cell lines with altered p53 function. Cancer Chemother Pharmacol 2003; 51: 91-95. (Pubitemid 36057029)
32. Wan PT, Garnett MJ, Roe SM, Lee S, Niculescu-Duvaz D, Good VM et al. Mechanism of activation of the RAF-ERK signaling pathway by oncogenic mutations of B-RAF. Cell 2004; 116: 855-867. (Pubitemid 38410730)
33. Gild ML, Bullock M, Robinson BG, Clifton-Bligh R. Multikinase inhibitors: a new option for the treatment of thyroid cancer. Nat Rev Endocrinol 2011; 7: 617-624.
34. Downward J. Targeting RAF: trials and tribulations. Nat Med 2011; 17: 286-288.
35. Nucera C, Nehs MA, Mekel M, Zhang X, Hodin R, Lawler J et al. A novel orthotopic mouse model of human anaplastic thyroid carcinoma. Thyroid 2009; 19: 1077-1084.
36. Raveh S, Gavert N, Ben-Ze'ev A. L1 cell adhesion molecule (L1CAM) in invasive tumors. Cancer Lett 2009; 282: 137-145.
37. Gavert N, Conacci-Sorrell M, Gast D, Schneider A, Altevogt P, Brabletz T et al. L1, a novel target of beta-catenin signaling, transforms cells and is expressed at the invasive front of colon cancers. J Cell Biol 2005; 168: 633-642. (Pubitemid 40271028)
38. Konsavage Jr WM, Kyler SL, Rennoll SA, Jin G, Yochum GS. Wnt/beta-catenin signaling regulates Yes-associated protein (YAP) gene expression in colorectal carcinoma cells. J Biol Chem 2012; 287: 11730-11739.
39. Kim KS, Min JK, Liang ZL, Lee K, Lee JU, Bae KH et al. Aberrant l1 cell adhesion molecule affects tumor behavior and chemosensitivity in anaplastic thyroid carcinoma. Clin Cancer Res. 2012; 18: 3071-3078.
40. Lee JH, Kim TS, Yang TH, Koo BK, Oh SP, Lee KP et al. A crucial role of WW45 in developing epithelial tissues in the mouse. EMBO J 2008; 27: 1231-1242.
41. Liu AM, Xu MZ, Chen J, Poon RT, Luk JM. Targeting YAP and Hippo signaling pathway in liver cancer. Expert Opin Ther Targets 2010; 14: 855-868.
42. Heallen T, Zhang M, Wang J, Bonilla-Claudio M, Klysik E, Johnson RL et al. Hippo pathway inhibits Wnt signaling to restrain cardiomyocyte proliferation and heart size. Science 2011; 332: 458-461.
43. Zhao B, Tumaneng K, Guan KL. The Hippo pathway in organ size control, tissue regeneration and stem cell self-renewal. Nat Cell Biol 2011; 13: 877-883.
44. Genevet A, Tapon N. The Hippo pathway and apico-basal cell polarity. Biochem J 2011; 436: 213-224.
45. Genevet A, Wehr MC, Brain R, Thompson BJ, Tapon N. Kibra is a regulator of the Salvador/Warts/Hippo signaling network. Dev Cell 2010; 18: 300-308.
46. Willecke M, Hamaratoglu F, Kango-Singh M, Udan R, Chen CL, Tao C et al. The fat cadherin acts through the hippo tumor-suppressor pathway to regulate tissue size. Curr Biol 2006; 16: 2090-2100. (Pubitemid 44692095)
47. Yokoyama T, Osada H, Murakami H, Tatematsu Y, Taniguchi T, Kondo Y et al. YAP1 is involved in mesothelioma development and negatively regulated by Merlin through phosphorylation. Carcinogenesis 2008; 29: 2139-2146.
48. Oh HJ, Lee KK, Song SJ, Jin MS, Song MS, Lee JH et al. Role of the tumor suppressor RASSF1A in Mst1-mediated apoptosis. Cancer Res 2006; 66: 2562-2569.
49. Zhang H, Liu CY, Zha ZY, Zhao B, Yao J, Zhao S et al. TEAD transcription factors mediate the function of TAZ in cell growth and epithelial-mesenchymal transition. J Biol Chem 2009; 284: 13355-13362.
50. Chan SW, Lim CJ, Huang C, Chong YF, Gunaratne HJ, Hogue KA et al. WW domainmediated interaction with Wbp2 is important for the oncogenic property of TAZ. Oncogene 2011; 30: 600-610.
51. Zhao B, Li L, Lu Q, Wang LH, Liu CY, Lei Q et al. Angiomotin is a novel Hippo pathway component that inhibits YAP oncoprotein. Genes Dev 2011; 25: 51-63.
52. Chan SW, Lim CJ, Chong YF, Pobbati AV, Huang C, Hong W. Hippo pathwayindependent restriction of TAZ and YAP by angiomotin. J Biol Chem 2011; 286: 7018-7026.
53. Wrighton KH. Mechanotransduction: YAP and TAZ feel the force. Nat Rev Mol Cell Biol 2011; 12: 404.
54. Pritchard CA, Hayes L, Wojnowski L, Zimmer A, Marais RM, Norman JC. B-Raf acts via the ROCKII/LIMK/cofilin pathway to maintain actin stress fibers in fibroblasts. Mol Cell Biol 2004; 24: 5937-5952. (Pubitemid 38787977)
55. Kirui JK, Xie Y, Wolff DW, Jiang H, Abel PW, Tu Y. Gbetagamma signaling promotes breast cancer cell migration and invasion. J Pharmacol Exp Ther 2010; 333: 393-403.
56. Lehtinen L, Vainio P, Wikman H, Reemts J, Hilvo M, Issa R et al. 15-Hydroxyprostaglandin dehydrogenase associates with poor prognosis in breast cancer, induces epithelial-mesenchymal transition, and promotes cell migration in cultured breast cancer cells. J Pathol 2012; 226: 674-686.
57. Lee KP, Lee JH, Kim TS, Kim TH, Park HD, Byun JS et al. The Hippo-Salvador pathway restrains hepatic oval cell proliferation, liver size, and liver tumorigenesis. Proc Natl Acad Sci USA 2010; 107: 8248-8253.
58. Nikiforov YE. Genetic alterations involved in the transition from well-differentiated to poorly differentiated and anaplastic thyroid carcinomas. Endocr Pathol 2004, Winter 15: 319-327.
59. Jo YS, Huang S, Kim YJ, Lee IS, Kim SS, Kim JR et al. Diagnostic value of pyrosequencing for the BRAF V600E mutation in ultrasound-guided fine-needle aspiration biopsy samples of thyroid incidentalomas. Clin Endocrinol (Oxf) 2009; 70: 139-144.
60. Stoeltzing O, Liu W, Reinmuth N, Fan F, Parikh AA, Bucana CD et al. Regulation of hypoxia-inducible factor-1alpha, vascular endothelial growth factor, and angiogenesis by an insulin-like growth factor-I receptor autocrine loop in human pancreatic cancer. Am J Pathol 2003; 163: 1001-1011. (Pubitemid 37040136)