Thyroid hormone receptors are tumor suppressors in a mouse model of metastatic follicular thyroid carcinoma

Oncogene

Volumn 29, Issue 13, 2010, Pages 1909-1919

  Zhu, X G ^a   Zhao, L ^a   Willingham, M C ^b   Cheng, S Y ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Mouse model; Mutations of thyroid hormone receptors; Thyroid cancer

Indexed keywords

PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN MDM2; PROTEIN P53; THYROID HORMONE RECEPTOR;

ADENOMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INVASION; CARCINOGENESIS; CELL INVASION; CONTROLLED STUDY; FOLLICULAR CARCINOMA; GENE EXPRESSION; HISTOPATHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; THYROID CARCINOMA; TUMOR GROWTH; TUMOR SUPPRESSOR GENE;

ADENOCARCINOMA, FOLLICULAR; ANIMALS; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; MICE, TRANSGENIC; MUTATION; RECEPTORS, THYROID HORMONE; SIGNAL TRANSDUCTION; THYROID NEOPLASMS;

MUS;

EID: 77950519366     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2009.476     Document Type: Article

References (63)

1. Ando S, Sarlis NJ, Krishnan J, Feng X, Refetoff S, Zhang MQ et al. (2001a). Aberrant alternative splicing of thyroid hormone receptor in a TSH-secreting pituitary tumor is a mechanism for hormone resistance. Mol Endocrinol 15: 1529-1538. (Pubitemid 32826405)
2. Ando S, Sarlis NJ, Oldfield EH, Yen PM. (2001b). Somatic mutation of TRbeta can cause a defect in negative regulation of TSH in a TSH-secreting pituitary tumor. J Clin Endocrinol Metab 86: 5572-5576. (Pubitemid 33070290)
3. Brinckerhoff CE, Matrisian LM. (2002). Matrix metalloproteinases: a tail of a frog that became a prince. Nat Rev Mol Cell Biol 3: 207-214. (Pubitemid 37237143)
4. Chen HW, Privalsky ML. (1993). The erbA oncogene represses the actions of both retinoid X and retinoid A receptors but does so by distinct mechanisms. Mol Cell Biol 13: 5970-5980.
5. Davis PJ, Leonard JL, Davis FB. (2008). Mechanisms of non-genomic actions of thyroid hormone. Front Neuroendocrinol 29: 211-218.
6. Fagin JA. (2002). Minireview: branded from the start-distinct oncogenic initiating events may determine tumor fate in the thyroid. Mol Endocrinol 16: 903-911.
7. Forrest D, Erway LC, Ng L, Altschuler R, Curran T. (1996a). Thyroid hormone receptor beta is essential for development of auditory function. Nat Genet 13: 354-357. (Pubitemid 26230504)
8. Forrest D, Hanebuth E, Smeyne RJ, Everds N, Stewart CL, Wehner JM et al. (1996b). Recessive resistance to thyroid hormone in mice lacking thyroid hormone receptor beta: evidence for tissue-specific modulation of receptor function. EMBO J 15: 3006-3015. (Pubitemid 26187749)
9. Forrest D, Vennstrom B. (2000). Functions of thyroid hormone receptors in mice. Thyroid 10: 41-52. (Pubitemid 30090364)
10. Furumoto H, Ying H, Chandramouli GV, Zhao L, Walker RL, Meltzer PS et al. (2005). An unliganded thyroid hormone beta receptor activates the cyclin D1/cyclin-dependent kinase/retinoblas-toma/E2F pathway and induces pituitary tumorigenesis. Mol Cell Biol 25: 124-135. (Pubitemid 40039805)
11. Furuya F, Lu C, Guigon CJ, Cheng SY. (2009). Nongenomic activation of phosphatidylinositol 3-kinase signaling by thyroid hormone receptors. Steroids 74: 628-634. (Pubitemid 43228770)
12. Garcia-Silva S, Aranda A. (2004). The thyroid hormone receptor is a suppressor of ras-mediated transcription, proliferation, and transformation. Mol Cell Biol 24: 7514-7523. (Pubitemid 39121479)
13. Gothe S, Wang Z, Ng L, Kindblom JM, Barros AC, Ohlsson C et al. (1999). Mice devoid of all known thyroid hormone receptors are viable but exhibit disorders of the pituitary-thyroid axis, growth, and bone maturation. Genes Dev 13: 1329-1341. (Pubitemid 29250200)
14. Guigon CJ, Zhao L, Lu C, Willingham MC, Cheng SY. (2008). Regulation of beta-catenin by a novel nongenomic action of thyroid hormone beta receptor. Mol Cell Biol 28: 4598-4608. (Pubitemid 351977757)
15. Heaney AP, Nelson V, Fernando M, Horwitz G. (2001). Transforming events in thyroid tumorigenesis and their association with follicular lesions. J Clin Endocrinol Metab 86: 5025-5032. (Pubitemid 33020559)
16. Herwig S, Strauss M. (1997). The retinoblastoma protein: a master regulator of cell cycle, differentiation and apoptosis. Eur J Biochem 246: 581-601. (Pubitemid 27252898)
17. Kamiya Y, Puzianowska-Kuznicka M, McPhie P, Nauman J, Cheng SY, Nauman A. (2002). Expression of mutant thyroid hormone nuclear receptors is associated with human renal clear cell carcinoma. Carcinogenesis 23: 25-33. (Pubitemid 34213548)
18. Kaneshige M, Kaneshige K, Zhu X, Dace A, Garrett L, Carter TA et al. (2000). Mice with a targeted mutation in the thyroid hormone beta receptor gene exhibit impaired growth and resistance to thyroid hormone. Proc Natl Acad Sci USA 97: 13209-13214.
19. Kato Y, Ying H, Willingham MC, Cheng SY. (2004). A tumor suppressor role for thyroid hormone beta receptor in a mouse model of thyroid carcinogenesis. Endocrinology 145: 4430-4438. (Pubitemid 39281432)
20. Kato Y, Ying H, Zhao L, Furuya F, Araki O, Willingham MC et al. (2006). PPARgamma insufficiency promotes follicular thyroid carcinogenesis via activation of the nuclear factor-kappaB signaling pathway. Oncogene 25: 2736-2747.
21. Kim CS, Ying H, Willingham MC, Cheng SY. (2007). The pituitary tumor-transforming gene promotes angiogenesis in a mouse model of follicular thyroid cancer. Carcinogenesis 28: 932-939. (Pubitemid 47072175)
22. Kim DS, Franklyn JA, Boelaert K, Eggo MC, Watkinson JC, McCabe CJ. (2006). Pituitary tumor transforming gene (PTTG) stimulates thyroid cell proliferation via a vascular endothelial growth factor/ kinase insert domain receptor/inhibitor of DNA binding-3 autocrine pathway. J Clin Endocrinol Metab 91: 4603-4611. (Pubitemid 44833445)
23. Kim DS, McCabe CJ, Buchanan MA, Watkinson JC. (2003). Oncogenes in thyroid cancer. Clin Otolaryngol Allied Sci 28: 386-395.
24. Lawal O, Agbakwuru A, Olayinka OS, Adelusola K. (2001). Thyroid malignancy in endemic nodular goitres: prevalence, pattern and treatment. Eur J Surg Oncol 27: 157-161. (Pubitemid 32621727)
25. Ledent C, Dumont JE, Vassart G, Parmentier M. (1992). Thyroid expression of an A2 adenosine receptor transgene induces thyroid hyperplasia and hyperthyroidism. EMBO J 11: 537-542.
26. Li Z, Meng ZH, Chandrasekaran R, Kuo WL, Collins CC, Gray JW et al. (2002). Biallelic inactivation of the thyroid hormone receptor beta1 gene in early stage breast cancer. Cancer Res 62: 1939-1943. (Pubitemid 34408433)
27. Lin KH, Shieh HY, Chen SL, Hsu HC. (1999). Expression of mutant thyroid hormone nuclear receptors in human hepatocellular carcinoma cells. Mol Carcinog 26: 53-61.
28. Maeda K, Chung YS, Takatsuka S, Ogawa Y, Sawada T, Yamashita Y et al. (1995). Tumor angiogenesis as a predictor of recurrence in gastric carcinoma. J Clin Oncol 13: 477-481.
29. Martinez-Iglesias O, Garcia-Silva S, Tenbaum SP, Regadera J, Larcher F, Paramio JM et al. (2009). Thyroid hormone receptor beta1 acts as a potent suppressor of tumor invasiveness and metastasis. Cancer Res 69: 501-509.
30. McCabe CJ, Boelaert K, Tannahill LA, Heaney AP, Stratford AL, Khaira JS et al. (2002). Vascular endothelial growth factor, its receptor KDR/Flk-1, and pituitary tumor transforming gene in pituitary tumors. J Clin Endocrinol Metab 87: 4238-4244.
31. Meier CA, Dickstein BM, Ashizawa K, McClaskey JH, Muchmore P, Ransom SC et al. (1992). Variable transcriptional activity and ligand binding of mutant beta 1 3,5,3-triiodothyronine receptors from four families with generalized resistance to thyroid hormone. Mol Endocrinol 6: 248-258.
32. Michiels FM, Caillou B, Talbot M, Dessarps-Freichey F, Maunoury MT, Schlumberger M et al. (1994). Oncogenic potential of guanine nucleotide stimulatory factor alpha subunit in thyroid glands of transgenic mice. Proc Natl Acad Sci USA 91: 10488-10492. (Pubitemid 24329023)
33. Miyakawa M, Tsushima T, Murakami H, Wakai K, Isozaki O, Takano K. (2003). Increased expression of phosphorylated p70S6 kinase and Akt in papillary thyroid cancer tissues. Endocr J 50: 77-83. (Pubitemid 36305850)
34. Pei L, Melmed S. (1997). Isolation and characterization of a pituitary tumor-transforming gene (PTTG). Mol Endocrinol 11: 433-441. (Pubitemid 27147011)
35. Persad S, Dedhar S. (2003). The role of integrin-linked kinase (ILK) in cancer progression. Cancer Metastasis Rev 22: 375-384. (Pubitemid 36791893)
36. Puzianowska-Kuznicka M, Krystyniak A, Madej A, Cheng SY, Nauman J. (2002). Functionally impaired TR mutants are present in thyroid papillary cancer. J Clin Endocrinol Metab 87: 1120-1128. (Pubitemid 36121076)
37. Puzianowska-Kuznicka M, Nauman A, Madej A, Tanski Z, Cheng S, Nauman J. (2000). Expression of thyroid hormone receptors is disturbed in human renal clear cell carcinoma. Cancer Lett 155: 145-152. (Pubitemid 30259128)
38. Puzianowska-Kuznicka M, Pietrzak M, Turowska O, Nauman A. (2006). Thyroid hormones and their receptors in the regulation of cell proliferation. Acta Biochim Pol 53: 641-650. (Pubitemid 46090114)
39. Ringel MD, Hayre N, Saito J, Saunier B, Schuppert F, Burch H et al. (2001). Overexpression and overactivation of Akt in thyroid carcinoma. Cancer Res 61: 6105-6111. (Pubitemid 32762546)
40. Safer JD, Colan SD, Fraser LM, Wondisford FE. (2001). A pituitary tumor in a patient with thyroid hormone resistance: a diagnostic dilemma. Thyroid 11: 281-291. (Pubitemid 32298427)
41. Sap J, Munoz A, Damm K, Goldberg Y, Ghysdael J, Leutz A et al. (1986). The c-erb-A protein is a high-affinity receptor for thyroid hormone. Nature 324: 635-640. (Pubitemid 17206350)
42. Sharpless NE, DePinho RA. (2002). p53: good cop/bad cop. Cell 110: 9-12.
43. Shen WT, Chung WY. (2005). Treatment of thyroid cancer with histone deacetylase inhibitors and peroxisome proliferator-activated receptor-gamma agonists. Thyroid 15: 594-599.
44. Suzuki H, Willingham MC, Cheng SY. (2002). Mice with a mutation in the thyroid hormone receptor beta gene spontaneously develop thyroid carcinoma: a mouse model of thyroid carcinogenesis. Thyroid 12: 963-969. (Pubitemid 35404130)
45. Suzuki H, Zhang XY, Forrest D, Willingham MC, Cheng SY. (2003). Marked potentiation of the dominant negative action of a mutant thyroid hormone receptor beta in mice by the ablation of one wild-type beta allele. Mol Endocrinol 17: 895-907. (Pubitemid 36539579)
46. Takano T, Miyauchi A, Yoshida H, Nakata Y, Kuma K, Amino N. (2003). Expression of TRbeta1 mRNAs with functionally impaired mutations is rare in thyroid papillary carcinoma. J Clin Endocrinol Metab 88: 3447-3449. (Pubitemid 36877528)
47. Teresi RE, Waite KA. (2008). PPARgamma, PTEN, and the fight against cancer. PPAR Res 2008: 932632.
48. Thormeyer D, Baniahmad A. (1999). The v-erbA oncogene (review). Int J Mol Med 4: 351-358.
49. Troussard AA, Costello P, Yoganathan TN, Kumagai S, Roskelley CD, Dedhar S. (2000). The integrin linked kinase (ILK) induces an invasive phenotype via AP-1 transcription factor-dependent upre-gulation of matrix metalloproteinase 9 (MMP-9). Oncogene 19: 5444-5452.
50. Troussard AA, Mawji NM, Ong C, Mui A, St-Arnaud R, Dedhar S. (2003). Conditional knock-out of integrin-linked kinase demonstrates an essential role in protein kinase B/Akt activation. J Biol Chem 278: 22374-22378. (Pubitemid 36830287)
51. Turpeenniemi-Hujanen T. (2005). Gelatinases (MMP-2 and-9) and their natural inhibitors as prognostic indicators in solid cancers. Biochimie 87: 287-297. (Pubitemid 40387607)
52. Ward JM, Ohshima M. (1986). The role of iodine in carcinogenesis. Adv Exp Med Biol 206: 529-542.
53. Weidner N, Semple JP, Welch WR, Folkman J. (1991). Tumor angiogenesis and metastasis-correlation in invasive breast carcinoma. N Engl J Med 324: 1-8. (Pubitemid 24058195)
54. Weinberger C, Thompson CC, Ong ES, Lebo R, Gruol DJ, Evans RM. (1986). The c-erb-A gene encodes a thyroid hormone receptor. Nature 324: 641-646. (Pubitemid 17206351)
55. Weiss RE, Refetoff S. (2000). Resistance to thyroid hormone. Rev Endocr Metab Disord 1: 97-108.
56. Wikstrom L, Johansson C, Salto C, Barlow C, Campos Barros A, Baas F et al. (1998). Abnormal heart rate and body temperature in mice lacking thyroid hormone receptor alpha 1. EMBO J 17: 455-461. (Pubitemid 28045486)
57. Yen PM, Ikeda M, Brubaker JH, Forgione M, Sugawara A, Chin WW. (1994). Roles of v-erbA homodimers and heterodimers in mediating dominant negative activity by v-erbA. J Biol Chem 269: 903-909. (Pubitemid 24032462)
58. Ying H, Furuya F, Zhao L, Araki O, West BL, Hanover JA et al. (2006). Aberrant accumulation of PTTG1 induced by a mutated thyroid hormone beta receptor inhibits mitotic progression. J Clin Invest 116: 2972-2984. (Pubitemid 44684482)
59. Ying H, Suzuki H, Furumoto H, Walker R, Meltzer P, Willingham MC et al. (2003a). Alterations in genomic profiles during tumor progression in a mouse model of follicular thyroid carcinoma. Carcinogenesis 24: 1467-1479. (Pubitemid 37160837)
60. Ying H, Suzuki H, Zhao L, Willingham MC, Meltzer P, Cheng SY. (2003b). Mutant thyroid hormone receptor beta represses the expression and transcriptional activity of peroxisome proliferator-activated receptor gamma during thyroid carcinogenesis. Cancer Res 63: 5274-5280. (Pubitemid 37139841)
61. Zeiger MA, Saji M, Gusev Y, Westra WH, Takiyama Y, Dooley WC et al. (1997). Thyroid-specific expression of cholera toxin A1 subunit causes thyroid hyperplasia and hyperthyroidism in transgenic mice. Endocrinology 138: 3133-3140. (Pubitemid 27345661)
62. Zhang XY, Kaneshige M, Kamiya Y, Kaneshige K, McPhie P, Cheng SY. (2002). Differential expression of thyroid hormone receptor isoforms dictates the dominant negative activity of mutant Beta receptor. Mol Endocrinol 16: 2077-2092. (Pubitemid 35013456)
63. Zimonjic DB, Kato Y, Ying H, Popescu NC, Cheng SY. (2005). Chromosomal aberrations in cell lines derived from thyroid tumors spontaneously developed in TRbetaPV/PV mice. Cancer Genet Cytogenet 161: 104-109. (Pubitemid 41133475)