Wnt-independent role of β-catenin in thyroid cell proliferation and differentiation

Molecular Endocrinology

Volumn 28, Issue 5, 2014, Pages 681-695

  Sastre Perona, Ana ^a   Santisteban, Pilar ^a  

^a INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIN D1; PROTEIN KINASE B; SODIUM IODIDE SYMPORTER; SOMATOMEDIN C; T CELL FACTOR 4; T CELL FACTOR PROTEIN; THYROTROPIN; TRANSCRIPTION FACTOR PAX8; UNCLASSIFIED DRUG; UVOMORULIN; WNT PROTEIN; CCND1 PROTEIN, RAT; CTNNB1 PROTEIN, RAT; PAIRED BOX TRANSCRIPTION FACTOR; PAX8 PROTEIN, RAT;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL JUNCTION; CELL NUCLEUS; CELL PROLIFERATION; CONTROLLED STUDY; DNA SYNTHESIS; GENE; NIS GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; REGULATORY MECHANISM; THYROID CELL; THYROID FUNCTION; ACTIVE TRANSPORT; ANIMAL; CELL LINE; CYTOLOGY; FISCHER 344 RAT; METABOLISM; PHYSIOLOGY; THYROID GLAND; TRANSCRIPTION INITIATION; WNT SIGNALING PATHWAY;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; BETA CATENIN; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; CYCLIN D1; INSULIN-LIKE GROWTH FACTOR I; PAIRED BOX TRANSCRIPTION FACTORS; RATS, INBRED F344; THYROID GLAND; THYROTROPIN; TRANSCRIPTIONAL ACTIVATION; WNT SIGNALING PATHWAY;

EID: 84899755132     PISSN: 08888809     EISSN: 19449917     Source Type: Journal    
DOI: 10.1210/me.2013-1377     Document Type: Article

References (57)

1. Kimura T, Van Keymeulen A, Golstein J, Fusco A, Dumont JE, Roger PP. Regulation of thyroid cell proliferation by TSH and other factors: a critical evaluation of in vitro models. Endocr Rev. 2001; 22: 631-656.
2. Postiglione MP, Parlato R, Rodriguez-Mallon A, et al. Role of the thyroid-stimulating hormone receptor signaling in development and differentiation of the thyroid gland. Proc Natl Acad Sci USA. 2002; 99: 15462-15467.
3. Marians RC, Ng L, Blair HC, Unger P, Graves PN, Davies TF. Defining thyrotropin-dependent and-independent steps of thyroid hormone synthesis by using thyrotropin receptor-null mice. Proc Natl Acad Sci USA. 2002; 99: 15776-15781.
4. Zaballos MA, Garcia B, Santisteban P. Gβγ dimers released in response to thyrotropin activate phosphoinositide 3-kinase and regulate gene expression in thyroid cells. Mol Endocrinol. 2008; 22: 1183-1199.
5. Blancquaert S, Wang L, Paternot S, et al. cAMP-dependent activation of mammalian target of rapamycin (mTOR) in thyroid cells. Implication in mitogenesis and activation of CDK4. Mol Endocrinol. 2010; 24: 1453-1468.
6. De Felice M, Di Lauro R. Minireview: Intrinsic and extrinsic factors in thyroid gland development: an update. Endocrinology. 2011; 152: 2948-2956.
7. Riesco-Eizaguirre G, Santisteban P. A perspective view of sodium iodide symporter research and its clinical implications. Eur J Endocrinol. 2006; 155: 495-512.
8. Helmbrecht K, Kispert A, von Wasielewski R, Brabant G. Identification of a Wnt/β-catenin signaling pathway in human thyroid cells. Endocrinology. 2001; 142: 5261-5266.
9. Tasevski V, Benn D, King M, Luttrell B, Simpson A. Mitogenic effect of lithium in FRTL-5 cells can be reversed by blocking de novo cholesterol synthesis and subsequent signal transduction. Thyroid. 2000; 10: 305-311.
10. Chen G, Jiang Q, You Z, et al. Regulation of GSK-3β in the proliferation and apoptosis of human thyrocytes investigated using a GSK-3β-targeting RNAi adenovirus expression vector: involvement the Wnt/β-catenin pathway. Mol Biol Rep. 2010; 37: 2773-2779.
11. Rubinfeld B, Albert I, Porfiri E, Fiol C, Munemitsu S, Polakis P. Binding of GSK3β to the APC-β-catenin complex and regulation of complex assembly. Science. 1996; 272: 1023-1026.
12. Kim WB, Lewis CJ, McCall KD, et al. Overexpression of Wnt-1 in thyrocytes enhances cellular growth but suppresses transcription of the thyroperoxidase gene via different signaling mechanisms. J Endocrinol. 2007; 193: 93-106.
13. Fang X, Yu SX, Lu Y, Bast RC Jr, Woodgett JR, Mills GB. Phosphorylation and inactivation of glycogen synthase kinase 3 by protein kinase A. Proc Natl Acad Sci USA. 2000; 97: 11960-11965.
14. Valenta T, Hausmann G, Basler K. The many faces and functions of β-catenin. EMBO J. 2012; 31: 2714-2736.
15. Fang D, Hawke D, Zheng Y, et al. Phosphorylation of β-catenin by AKT promotes β-catenin transcriptional activity. J Biol Chem. 2007; 282: 11221-11229.
16. Tian Q, Feetham MC, Tao WA, et al. Proteomic analysis identifies that 14-3-3β interacts with β-catenin and facilitates its activation by Akt. Proc Natl Acad Sci USA. 2004; 101: 15370-15375.
17. Taurin S, Sandbo N, Qin Y, Browning D, Dulin NO. Phosphorylation of β-catenin by cyclic AMP-dependent protein kinase. J Biol Chem. 2006; 281: 9971-9976.
18. Fusco A, Berlingieri MT, Di Fiore PP, Portella G, Grieco M, Vecchio G. One-and two-step transformations of rat thyroid epithelial cells by retroviral oncogenes. Mol Cell Biol. 1987; 7: 3365-3370.
19. Ambesi-Impiombato FS, Parks LA, Coon HG. Culture of hormonedependent functional epithelial cells from rat thyroids. Proc Natl Acad Sci USA. 1980; 77: 3455-3459.
20. Zaballos MA, Santisteban P. FOXO1 controls thyroid cell proliferation in response to TSH and IGF-I and is involved in thyroid tumorigenesis. Mol Endocrinol. 2013; 27: 50-62.
21. García B, Santisteban P. PI3K is involved in the IGF-I inhibition of TSH-induced sodium/iodide symporter gene expression. Mol Endocrinol. 2002; 16: 342-352.
22. Pohlenz J, Dumitrescu A, Zundel D, et al. Partial deficiency of thyroid transcription factor 1 produces predominantly neurological defects in humans and mice. J Clin Invest. 2002; 109: 469-473.
23. Baratta MG, Porreca I, Di Lauro R. Oncogenic ras blocks the cAMP pathway and dedifferentiates thyroid cells via an impairment of pax8 transcriptional activity. Mol Endocrinol. 2009; 23: 838-848.
24. Veeman MT, Axelrod JD, Moon RT. A second canon. Functions and mechanisms of β-catenin-independent Wnt signaling. Dev Cell. 2003; 5: 367-377.
25. Vilain C, Rydlewski C, Duprez L, et al. Autosomal dominant transmission of congenital thyroid hypoplasia due to loss-of-function mutation of PAX8. J Clin Endocrinol Metab. 2001; 86: 234-238.
26. Guazzi S, Price M, De Felice M, Damante G, Mattei MG, Di Lauro R. Thyroid nuclear factor 1 (TTF-1) contains a homeodomain and displays a novel DNA binding specificity. EMBO J. 1990; 9: 3631-3639.
27. Méndez-Pertuz M, Sánchez-Pacheco A, Aranda A. The thyroid hormone receptor antagonizes CREB-mediated transcription. EMBO J. 2003; 22: 3102-3112.
28. Morin PJ, Sparks AB, Korinek V, et al. Activation of β-catenin-Tcf signaling in colon cancer by mutations inβ-catenin or APC. Science. 1997; 275: 1787-1790.
29. Chen CA, Okayama H. Calcium phosphate-mediated gene transfer: a highly efficient transfection system for stably transforming cells with plasmid DNA. Biotechniques. 1988; 6: 632-638.
30. Perona R, Montaner S, Saniger L, Sánchez-Pérez I, Bravo R, Lacal JC. Activation of the nuclear factor-kappaB by Rho, CDC42, and Rac-1 proteins. Genes Dev. 1997; 11: 463-475.
31. De La Vieja A, Ginter CS, Carrasco N. The Q267E mutation in the sodium/iodide symporter (NIS) causes congenital iodide transport defect (ITD) by decreasing the NIS turnover number. J Cell Sci. 2004; 117: 677-687.
32. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding. Anal Biochem. 1976; 72: 248-254.
33. De la Vieja A, Ginter CS, Carrasco N. Molecular analysis of a congenital iodide transport defect: G543E impairs maturation and trafficking of the Na+/I- symporter. Mol Endocrinol. 2005; 19: 2847-2858.
34. Ruiz-Llorente S, Carrillo Santa de Pau E, Sastre-Perona A, et al. Genome-wide analysis of Pax8 binding provides new insights into thyroid functions. BMC Genomics. 2012; 13: 147.
35. Fuerer C, Nusse R. Lentiviral vectors to probe and manipulate the Wnt signaling pathway. PLoS One. 2010; 5: e9370.
36. Dull T, Zufferey R, Kelly M, et al. A third-generation lentivirus vector with a conditional packaging system. J Virol. 1998; 72: 8463-8471.
37. Zhang XY, La Russa VF, Reiser J. Transduction of bone-marrowderived mesenchymal stem cells by using lentivirus vectors pseudotyped with modified RD114 envelope glycoproteins. J Virol. 2004; 78: 1219-1229.
38. Sastre-Perona A, Santisteban P. Role of the wnt pathway in thyroid cancer. Front Endocrinol (Lausanne). 2012; 3: 31.
39. Stambolic V, Ruel L, Woodgett JR. Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr Biol. 1996; 6: 1664-1668.
40. Shibamoto S, Higano K, Takada R, Ito F, Takeichi M, Takada S. Cytoskeletal reorganization by soluble Wnt-3a protein signalling. Genes Cells. 1998; 3: 659-670.
41. Brewer C, Yeager N, Di Cristofano A. Thyroid-stimulating hormone initiated proliferative signals converge in vivo on the mTOR kinase without activating AKT. Cancer Res. 2007; 67: 8002-8006.
42. Tetsu O, McCormick F. β-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature. 1999; 398: 422-426.
43. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B, Kinzler KW. Identification of c-MYC as a target of the APC pathway. Science. 1998; 281: 1509-1512.
44. Schmidt-Ott KM, Masckauchan TN, Chen X, et al. β-Catenin/TCF/Lef controls a differentiation-associated transcriptional program in renal epithelial progenitors. Development. 2007; 134: 3177-3190.
45. Wingender E, Chen X, Hehl R, et al. TRANSFAC: an integrated system for gene expression regulation. Nucleic Acids Res. 2000; 28: 316-319.
46. Kobielak K, Stokes N, de la Cruz J, Polak L, Fuchs E. Loss of a quiescent niche but not follicle stem cells in the absence of bone morphogenetic protein signaling. Proc Natl Acad Sci USA. 2007; 104: 10063-10068.
47. Guturi KK, Mandal T, Chatterjee A, et al. Mechanism of β-cateninmediated transcriptional regulation of epidermal growth factor receptor expression in glycogen synthase kinase 3β-inactivated prostate cancer cells. J Biol Chem. 2012; 287: 18287-18296.
48. Lee G, Goretsky T, Managlia E, et al. Phosphoinositide 3-kinase signaling mediates β-catenin activation in intestinal epithelial stem and progenitor cells in colitis. Gastroenterology. 2010; 139: 869-881, 881. e1-9.
49. Hino S, Tanji C, Nakayama KI, Kikuchi A. Phosphorylation of β-catenin by cyclic AMP-dependent protein kinase stabilizes β-catenin through inhibition of its ubiquitination. Mol Cell Biol. 2005; 25: 9063-9072.
50. Ng SS, Mahmoudi T, Danenberg E, Bejaoui I, et al. Phosphatidylinositol 3-kinase signaling does not activate the wnt cascade. J Biol Chem. 2009; 284: 35308-35313.
51. Kang DE, Soriano S, Xia X, et al. Presenilin couples the paired phosphorylation of β-catenin independent of axin: implications for β-catenin activation in tumorigenesis. Cell. 2002; 110: 751-762.
52. Pasca di Magliano M, Di Lauro R, Zannini M. Pax8 has a key role in thyroid cell differentiation. Proc Natl Acad Sci USA. 2000; 97: 13144-13149.
53. Rossi DL, Acebrón A, Santisteban P. Function of the homeo and paired domain proteins TTF-1 and Pax-8 in thyroid cell proliferation. J Biol Chem. 1995; 270: 23139-23142.
54. Park JS, Valerius MT, McMahon AP. Wnt/β-catenin signaling regulates nephron induction during mouse kidney development. Development. 2007; 134: 2533-2539.
55. Garcia-Rostan G, Camp RL, Herrero A, Carcangiu ML, Rimm DL, Tallini G. β-Catenin dysregulation in thyroid neoplasms: downregulation, aberrant nuclear expression, and CTNNB1 exon 3 mutations are markers for aggressive tumor phenotypes and poor prognosis. Am J Pathol. 2001; 158: 987-996.
56. Pons F, Carrió I, Estorch M, Ginjaume M, Pons J, Milian R. Lithium as an adjuvant of iodine-131 uptake when treating patients with well-differentiated thyroid carcinoma. Clin Nucl Med. 1987; 12: 644-647.
57. di Gennaro A, Spadaro O, Baratta MG, De Felice M, Di Lauro R. Functional analysis of the Pax8 promoter reveals autoregulation and the presence of a novel thyroid-specific DNA binding activity. Thyroid. 2013; 23: 488-496.