Role of the Wnt pathway in thyroid cancer

Frontiers in Endocrinology

Volumn 3, Issue FEB, 2012, Pages

  Sastre Perona, Ana ^a   Santisteban, Pilar ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Differentiation; Proliferation; Signaling network; Thyroid cancer; Wnt pathway

Indexed keywords

EID: 84868647819     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2012.00031     Document Type: Review

References (71)

1. Abbosh, P. H., Li, X., Li, L., Gardner, T. A., Kao, C., and Nephew, K. P. (2007). A conditionally replicative, Wnt/beta-catenin pathway-based adenovirus therapy for anaplastic thyroid cancer. Cancer Gene Ther. 14, 399-408.
2. Aguilera, O., Fraga, M. F., Ballestar, E., Paz, M. F., Herranz, M., Espada, J., Garcia, J. M., Munoz, A., Esteller, M., and Gonzalez-Sancho, J. M. (2006). Epigenetic inactivation of the Wnt antagonist DICKKOPF-1 (DKK-1) gene in human colorectal cancer. Oncogene 25, 4116-4121.
3. Arufe, M. C., Lu, M., Kubo,A., Keller, G., Davies, T. F., and Lin, R. Y. (2006). Directed differentiation of mouse embryonic stem cells into thyroid follicular cells. Endocrinology 147, 3007-3015.
4. Berx,G.,and van Roy,F. (2009). Involve ment of members of the cadherin superfamily in cancer. Cold Spring Harb. Perspect. Biol. 1, a003129.
5. Brabant, G., Hoang-Vu, C., Cetin, Y., Dralle, H., Scheumann, G., Molne, J., Hansson, G., Jansson, S., Eric son, L. E., and Nilsson, M. (1993). E-cadherin: a differentiation marker in thyroid malignancies. Cancer Res. 53, 4987-4993.
6. Cali, G., Gentile, F., Mogavero, S., Pal lante, P., Nitsch, R., Ciancia, G., Ferraro, A., Fusco, A., and Nitsch, L. (2012). CDH16/Ksp-cadherin is expressed in the developing thy roid gland and is strongly down regulated in thyroid carcinomas. Endocrinology 153, 522-534.
7. Cassinelli, G., Favini,E.,Degl'Innocenti, D., Salvi, A., De Petro, G., Pierotti, M. A., Zunino, F., Borrello, M. G., and Lanzi, C. (2009). RET/PTC1 driven neoplastic transformation and proinvasive phenotype of human thyrocytes involve Met induction and beta-catenin nuclear translocation. Neoplasia 11, 10-21.
8. Castellone, M. D., De Falco, V., Rao, D. M., Bellelli, R., Muthu, M., Basolo, F., Fusco, A., Gutkind, J. S., and San toro, M. (2009). The beta-catenin axis integrates multiple signals downstream from RET/papillary thyroid carcinoma leading to cell proliferation. Cancer Res. 69, 1867-1876.
9. Cerrato, A., Fulciniti, F., Avallone, A., Benincasa, G., Palombini, L., and Grieco, M. (1998). Beta and gamma-catenin expression in thy roid carcinomas. J. Pathol. 185, 267-272.
10. Cetta, F., Chiappetta, G., Melillo, R. M., Petracci, M., Montalto, G., San toro, M., and Fusco, A. (1998). Theret/ptc1oncogeneisactivated in familial adenomatous polyposis associated thyroid papillary carcino mas. J. Clin. Endocrinol. Metab. 83, 1003-1006.
11. Cetta, F., Montalto, G., Gori, M., Curia, M. C., Cama, A., and Olschwang, S. (2000). Germline mutations of the APC gene in patients with familial adenomatous polyposis-associated thyroid carcinoma: results from a European cooperative study. J. Clin. Endocrinol. Metab. 85, 286-292.
12. Chen, G., Jiang, Q., You, Z., Yao, J., Mou, L., Lin, X., Shen, X., You, T., Lin, Q., Wen, J., and Lin, L. (2010). Regulation of GSK-3 beta in the proliferation and apoptosis of human thyrocytes investigated using a GSK-3 beta-targeting RNAi ade novirus expression vector: involve ment the Wnt/beta-catenin pathway. Mol. Biol. Rep. 37, 2773-2779.
13. Cho, N. L., Lin, C. I., Whang, E. E., Carothers, A. M., Moore, F. D. Jr., and Ruan, D. T. (2010). Sulin dac reverses aberrant expression and localization of beta-catenin in pap illary thyroid cancer cells with the BRAFV600E mutation. Thyroid 20, 615-622.
14. de Cristofaro, T., Di Palma, T., Fichera, I., Lucci,V., Parrillo, L., De Felice, M., and Zannini, M. (2012). An essential role for pax8 in the transcriptional regulation of cadherin-16 in thyroid cells. Mol. Endocrinol. 26, 67-78.
15. De Felice, M., and Di Lauro, R. (2004). Thyroid development and its disor ders: genetics and molecular mecha nisms. Endocr. Rev. 25, 722-746.
16. Derwahl, M. (2011). Linking stem cells to thyroid cancer. J. Clin. Endocrinol. Metab. 96, 610-613.
17. Dick, J. E. (2008). Stem cell concepts renew cancer research. Blood 112, 4793-4807.
18. Dick,J. E. (2009). Looking ahead in can cer stem cell research. Nat. Biotech nol. 27, 44-46.
19. Dumaz, N., and Marais, R. (2005). Inte grating signals between cAMP and the RAS/RAF/MEK/ERK signalling pathways. Based on the anniversary prize of the Gesellschaft fur Bio chemie und Molekularbiologie lec ture delivered on 5 July 2003 at the Special FEBS Meeting in Brussels. FEBS J. 272, 3491-504.
20. Fagin, J. A., Matsuo, K., Karmakar, A., Chen, D. L., Tang, S. H., and Koef fler, H. P. (1993). High prevalence of mutations of the p53 gene in poorly differentiated human thy roid carcinomas. J. Clin. Invest. 91, 179-184.
21. Filipovich, A., Gehrke, I., Poll-Wolbeck, S. J., and Kreuzer, K. A. (2011). Phys iological inhibitors of Wnt signaling. Eur. J. Haematol. 86, 453-465.
22. Garcia-Rostan,G.,Camp,R. L.,Herrero, A., Carcangiu, M. L., Rimm, D. L., and Tallini, G. (2001). Beta-catenin dysregulation in thyroid neoplasms: down-regulation, aberrant nuclear expression, and CTNNB1 exon 3 mutations are markers for aggres sive tumor phenotypes and poor prognosis. Am. J. Pathol. 158, 987-996.
23. Garcia-Rostan,G.,Costa,A. M.,Pereira Castro, I., Salvatore, G., Hernan dez, R., Hermsem, M. J., Herrero, A., Fusco, A., Cameselle-Teijeiro, J., and Santoro, M. (2005). Mutation of the PIK3CA gene in anaplas tic thyroid cancer. Cancer Res. 65, 10199-10207.
24. Garcia-Rostan, G., Tallini, G., Herrero, A., D'Aquila, T. G., Carcangiu, M. L., and Rimm, D. L. (1999). Fre quent mutation and nuclear local ization of beta-catenin in anaplastic thyroid carcinoma. Cancer Res. 59, 1811-1815.
25. Graff, J. R., Greenberg, V. E., Herman, J. G., Westra, W. H., Boghaert, E. R., Ain, K. B., Saji, M., Zeiger, M. A., Zimmer, S. G., and Baylin, S. B. (1998). Distinct patterns of E cadherin CpG island methylation in papillary, follicular, Hurthle's cell, and poorly differentiated human thyroid carcinoma. Cancer Res. 58, 2063-2066.
26. Guigon, C. J., Zhao, L., Lu, C., Will ingham, M. C., and Cheng, S. Y. (2008). Regulation of beta-catenin by a novel nongenomic action of thyroid hormone beta receptor. Mol. Cell. Biol. 28, 4598-4608.
27. He, T. C., Sparks, A. B., Rago, C., Her meking, H., Zawel, L., da Costa, L. T., Morin, P. J., Vogelstein, B., and Kinzler, K. W. (1998). Identification of c-MYC as a target of the APC pathway. Science 281, 1509-1512.
28. Helmbrecht, K., Kispert, A., von Wasielewski, R., and Brabant, G. (2001). Identification of a Wnt/beta catenin signaling pathway in human thyroid cells. Endocrinology 142, 5261-5266.
29. Huang, S. M., Mishina, Y. M., Liu, S., Cheung, A., Stegmeier, F., Michaud, G. A., Charlat, O., Wiellette, E., Zhang,Y., Wiessner, S., Hild, M., Shi, X., Wilson, C. J., Mickanin, C., Myer, V., Fazal, A., Tomlinson, R., Ser luca, F., Shao, W., Cheng, H., Shultz, M., Rau, C., Schirle, M., Schlegl, J., Ghidelli, S., Fawell, S., Lu, C., Cur tis, D., Kirschner, M. W., Lengauer, C., Finan, P. M., Tallarico, J. A., Bouwmeester, T., Porter, J. A., Bauer, A., and Cong, F. (2009). Tankyrase inhibition stabilizes axin and antag onizes Wnt signalling. Nature 461, 614-620.
30. Hulsken, J., Birchmeier, W., and Behrens, J. (1994). E-cadherin and APC compete for the inter action with beta-catenin and the cytoskeleton. J. Cell Biol. 127(Pt 2), 2061-2069.
31. Ishigaki, K., Namba, H., Nakashima, M., Nakayama, T., Mitsutake, N., Hayashi, T., Maeda, S., Ichinose, M., Kanematsu, T., and Yamashita, S. (2002). Aberrant localization of beta-catenin correlates with overex pression of its target gene in human papillary thyroid cancer. J. Clin. Endocrinol. Metab. 87, 3433-3440.
32. Kikuchi, A., and Yamamoto, H. (2008). Tumor formation due to abnormali ties in the beta-catenin-independent pathway of Wnt signaling. Cancer Sci. 99, 202-208.
33. Kim, W. B., Lewis, C. J., McCall, K. D., Malgor, R., Kohn, A. D., Moon, R. T., and Kohn, L. D. (2007). Over expression of Wnt-1 in thyrocytes enhances cellular growth but sup presses transcription of the thy roperoxidase gene via different sig naling mechanisms. J. Endocrinol. 193, 93-106.
34. Kimura, T., Van Keymeulen, A., Gol stein, J., Fusco, A., Dumont, J. E., and Roger, P. P. (2001). Regulation of thyroid cell proliferation by TSH and other factors: a critical evalua tion of in vitro models. Endocr. Rev. 22, 631-656.
35. Kremenevskaja, N., von Wasielewski, R., Rao, A. S., Schofl, C., Andersson, T., and Brabant, G. (2005). Wnt 5a has tumor suppressor activity in thyroid carcinoma. Oncogene 24, 2144-2154.
36. Kroll, T. G., Sarraf, P., Pecciarini, L., Chen, C. J., Mueller, E., Spiegelman, B. M., and Fletcher, J. A. (2000). PAX8-PPARgamma1 fusion onco gene in human thyroid carcinoma [corrected]. Science 289, 1357-1360.
37. Kurihara, T., Ikeda, S., Ishizaki, Y., Fuji mori, M., Tokumoto, N., Hirata, Y., Ozaki, S., Okajima, M., Sugino, K., and Asahara, T. (2004). Immunohis tochemical and sequencing analyses of the Wnt signaling components in Japanese anaplastic thyroid cancers. Thyroid 14, 1020-1029.
38. Lepourcelet, M., Chen, Y. N., France, D. S., Wang, H., Crews, P., Petersen, F., Bruseo, C., Wood, A. W., and Shivdasani, R. A. (2004). Small molecule antagonists of the onco genic Tcf/beta-catenin protein com plex. Cancer Cell 5, 91-102.
39. Lin, R. Y. (2011). Thyroid cancer stem cells. Nat. Rev. Endocrinol. 7, 609-616.
40. Lu, C., Zhu, X., Willingham, M. C., and Cheng, S. Y. (2011). Activation of tumor cell proliferation by thyroid hormone in a mouse model of fol licular thyroid carcinoma. Oncogene. doi: 10.1038/onc.2011.390. [Epub ahead of print].
41. MacDonald, B. T., Tamai, K., and He, X. (2009). Wnt/beta-catenin signal ing: components, mechanisms, and diseases. Dev. Cell 17, 9-26.
42. Malanchi, I., Santamaria-Martinez, A., Susanto, E., Peng, H., Lehr, H. A., Delaloye, J. F., and Huelsken, J. (2011). Interactions between cancer stem cells and their niche govern metastatic colonization. Nature 481, 85-89.
43. McDonald, S. L., and Silver, A. (2009). The opposing roles of Wnt-5a in cancer. Br. J. Cancer 101, 209-214.
44. Medina, D. L., and Santisteban, P. (2000). Thyrotropin-dependent proliferation of in vitro rat thyroid cell systems. Eur. J. Endocrinol. 143, 161-178.
45. Meirmanov, S., Nakashima, M., Kondo, H., Matsufuji, R., Takamura, N., Ishigaki, K., Ito, M., Prouglo, Y., Yamashita, S., and Sekine, I. (2003). Correlation of cytoplasmic beta catenin and cyclin D1 overexpres sion during thyroid carcinogenesis around Semipalatinsk nuclear test site. Thyroid 13, 537-545.
46. Nikiforov, Y. E., and Nikiforova, M. N. (2011). Molecular genetics and diag nosis of thyroid cancer. Nat. Rev. Endocrinol. 7, 569-580.
47. Nishita, M., Enomoto, M.,Yamagata, K., and Minami, Y. (2010). Cell/tissue tropic functions of Wnt5a signaling in normal and cancer cells. Trends Cell Biol. 20, 346-354.
48. O'Sullivan, C., Barton, C. M., Staddon, S. L., Brown, C. L., and Lemoine, N. R. (1991). Activating point muta tions of the gsp oncogene in human thyroid adenomas. Mol. Carcinog. 4, 345-349.
49. Parma, J., Duprez, L., Van Sande, J., Cochaux, P., Gervy, C., Mockel, J., Dumont, J., and Vassart, G. (1993). Somatic mutations in the thyrotropin receptor gene cause hyperfunctioning thyroid adeno mas. Nature 365, 649-651.
50. Polakis, P. (2007). The many ways of Wnt in cancer. Curr. Opin. Genet. Dev. 17, 45-51.
51. Rao, A. S., Kremenevskaja, N., von Wasielewski, R., Jakubcakova, V., Kant, S., Resch, J., and Brabant, G. (2006). Wnt/beta-catenin signal ing mediates antineoplastic effects of imatinib mesylate (gleevec) in anaplastic thyroid cancer. J. Clin. Endocrinol. Metab. 91, 159-168.
52. Reya, T., and Clevers, H. (2005). Wnt signalling in stem cells and cancer. Nature 434, 843-850.
53. Rezk, S., Brynes, R. K., Nelson, V., Thein, M., Patwardhan, N., Fis cher, A., and Khan, A. (2004). Beta catenin expression in thyroid follic ular lesions: potential role in nuclear envelope changes in papillary carci nomas. Endocr. Pathol. 15, 329-337.
54. Rice, P. L., Kelloff, J., Sullivan, H., Drig gers, L. J., Beard, K. S., Kuwada, S., Piazza, G., and Ahnen, D. J. (2003). Sulindac metabolites induce caspase and proteasome-dependent degradation of beta-catenin protein in human colon cancer cells. Mol. Cancer Ther. 2, 885-892.
55. Riesco-Eizaguirre, G., Rodriguez, I., De la Vieja, A., Costamagna, E., Car rasco,N.,Nistal,M.,and Santisteban, P. (2009). The BRAFV600E onco gene induces transforming growth factor beta secretion leading to sodium iodide symporter repression and increased malignancy in thyroid cancer. Cancer Res. 69, 8317-8325.
56. Riesco-Eizaguirre, G., and Santisteban, P. (2007). Molecular biology of thy roid cancer initiation. Clin. Transl. Oncol. 9, 686-693.
57. Rubinfeld, B., Albert, I., Porfiri, E., Fiol, C., Munemitsu, S., and Polakis, P. (1996). Binding of GSK3beta to the APC-beta-catenin complex and reg ulation of complex assembly. Science 272, 1023-1026.
58. Santisteban, P., and Bernal, J. (2005). Thyroid development and effect on the nervous system. Rev. Endocr. Metab. Disord. 6, 217-228.
59. Soravia, C., Sugg, S. L., Berk, T., Mitri, A., Cheng, H., Gallinger, S., Cohen, Z., Asa, S. L., and Bapat, B. V. (1999). Familial adenomatous polyposis-associated thyroid cancer: a clinical, pathological, and molecu lar genetics study. Am. J. Pathol. 154, 127-135.
60. Strumane, K., Berx, G., and Van Roy, F. (2004). Cadherins in cancer. Handb. Exp. Pharmacol. 69-103.
61. Tartari, C. J., Donadoni, C., Manieri, E., Mologni, L., Mina, P. D., Villa, A., and Gambacorti-Passerini, C. (2011). Dissection of the RET/beta catenin interaction in the TPC1 thy roid cancer cell line. Am. J. Cancer Res. 1, 716-725.
62. Tetsu, O., and McCormick, F. (1999). Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398, 422-426.
63. Thomas, D., Friedman, S., and Lin, R. Y. (2008). Thyroid stem cells: lessons from normal development and thy roid cancer. Endocr. Relat. Cancer 15, 51-58.
64. Todaro, M., Iovino, F., Eterno, V., Cam mareri, P., Gambara, G., Espina, V., Gulotta, G., Dieli, F., Giordano, S., De Maria, R., and Stassi, G. (2010). Tumorigenic and metastatic activity of human thyroid cancer stem cells. Cancer Res. 70, 8874-8885.
65. Tzelepi, V. N., Tsamandas, A. C., Vloti nou, H. D., Vagianos, C. E., and Scopa, C. D. (2008). Tight junctions in thyroid carcinogenesis: diverse expression of claudin-1, claudin 4, claudin-7 and occludin in thy roid neoplasms. Mod. Pathol. 21, 22-30.
66. Vassart, G., and Dumont, J. E. (1992). The thyrotropin receptor and the regulation of thyrocyte function and growth. Endocr. Rev. 13, 596-611.
67. Vermeulen, L., De Sousa, E. M. F., van der Heijden, M., Cameron, K., de Jong, J. H., Borovski, T., Tuyn man, J. B., Todaro, M., Merz, C., Rodermond, H., Sprick, M. R., Kem per, K., Richel, D. J., Stassi, G., and Medema, J. P. (2010). Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat. Cell Biol. 12, 468-476.
68. Wada, H., and Okamoto, H. (2009). Roles of planar cell polarity pathway genes for neural migration and dif ferentiation. Dev. Growth Differ. 51, 233-240.
69. Xu, B., Yoshimoto, K., Miyauchi, A., Kuma, S., Mizusawa, N., Hirokawa, M., and Sano, T. (2003). Cribriform morular variant of papillary thyroid carcinoma: a pathological and mole cular genetic study with evidence of frequent somatic mutations in exon 3 of the beta-catenin gene. J. Pathol. 199, 58-67.
70. Zaballos, M. A., Garcia, B., and San tisteban, P. (2008). Gbetagamma dimers released in response to thy rotropin activate phosphoinositide 3-kinase and regulate gene expres sion in thyroid cells. Mol. Endocrinol. 22, 1183-1199.
71. Zhang, J., Gill, A. J., Issacs, J. D., Atmore, B., Johns, A., Delbridge, L. W., Lai, R., and Mcmullen, T. P. (2011). The Wnt/beta-catenin path way drives increased cyclin D1 levels in lymph node metastasis in pap illary thyroid cancer. Hum. Pathol. PMID: 22204713. [Epub ahead of print]