Role of reduced expression of SMAD4 in papillary thyroid carcinoma

Journal of Molecular Endocrinology

Volumn 45, Issue 4, 2010, Pages 229-244

  D'Inzeo, Sonia ^a   Nicolussi, Arianna ^a   Ricci, Antonella ^a   Mancini, Patrizia ^a   Porcellini, Antonio ^b   Nardi, Francesco ^a   Coppa, Anna ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF MOLISE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; SMAD2 PROTEIN; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CARCINOGENESIS; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVITY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RELATIVE BIOLOGIC EFFECTIVENESS; SIGNAL TRANSDUCTION; THYROID CARCINOMA; TREATMENT OUTCOME;

CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; HUMANS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SMAD4 PROTEIN; SUBCELLULAR FRACTIONS; THYROID NEOPLASMS; TRANSFORMING GROWTH FACTOR BETA;

EID: 77957850602     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1677/JME-10-0044     Document Type: Article

References (75)

1. Ambesi-Impiombato FS, Parks L & Coon HG 1980 Culture of hormone dependent functional epithelial cells from rat thyroids. PNAS 77 3455-3459. (doi:10.1073/pnas.77.6.3455)
2. Attisano L & Wrana JL 2000 Smads as transcriptional co-modulators. Current Opinion in Cell Biology 12 235-243. (doi:10.1016/S0955- 0674(99)00081-2)
3. Baldini E, Toller M, Graziano FM, Russo FP, Pepe M, Biordi L, Marchioni E, Curcio F, Ulisse S, Ambesi-Impiombato FS et al. 2004 Expression of matrix metalloproteinases and their specific inhibitors in normal and different human thyroid tumor cell lines. Thyroid 14 881-888. (doi:10.1089/thy.2004.14.881) (Pubitemid 39612905)
4. Bidey SP, Hill DJ & Eggo MC 1999 Growth factors and goitrogenesis. Journal of Endocrinology 160 321-332. (doi:10.1677/joe.0.1600321)
5. de Caestecker MP, Hemmati P, Larisch-Bloch S, Ajmera R, Roberts AB & Lechleider RJ 1997 Characterization of functional domains within Smad4/DPC4. Journal of Biological Chemistry 272 13690-13696. (doi:10.1074/jbc.272.21.13690) (Pubitemid 27224803)
6. Carcamo J, Weis FM, Ventura F, Wieser R, Wrana JL, Attisano L & Massagué J 1994 Type I receptors specify growth-inhibitory and transcriptional responses to TGF-β and activin. Molecular and Cellular Biology 14 3810-3821. (Pubitemid 24160788)
7. Carneiro C, Alvarez CV, Zalvide J, Vidal A & Domínguez F 1998 TGF-β1 actions on FRTL-5 cells provide a model for the physiological regulation of thyroid growth. Oncogene 16 1455-1465. (doi:10.1038/ sj.onc.1201662) (Pubitemid 28151852)
8. Cerutti JM, Ebina KN, Matsuo SE, Martins L, Maciel RM & Kimura ET 2003 Expression of Smad4 and Smad7 in human thyroid follicular carcinoma cell lines. Journal of Endocrinological Investigation 26 516-521. (Pubitemid 36998699)
9. Chiang AC & Massagué J 2008 Molecular basis of metastasis. New England Journal of Medicine 359 2814-2823. (doi:10.1056/ NEJMra0805239)
10. Christofori G 2006 New signals from the invasive front. Nature 441 444-450. (doi:10.1038/nature04872)
11. Colletta G, Cirafici AM & Di Carlo A 1989 Dual effect of transforming growth factor β on rat thyroid cells: inhibition of thyrotropin-induced proliferation and reduction of thyroid-specific differentiation markers. Cancer Research 49 3457-3462. (Pubitemid 19178158)
12. Coppa A, Mincione G, Mammarella S, Ranieri A & Colletta G 1995 Epithelial rat thyroid cell clones, escaping from transforming growth factor β negative growth control, are still inhibited by this factor in the ability to trap iodide. Cell Growth and Differentiation 6 281-290.
13. Costamagna E, Garcia B & Santisteban P 2004 The functional interaction between the paired domain transcription factor Pax8 and Smad3 is involved in transforming growth factor-β repression of the sodium/iodide symporter gene. Journal of Biological Chemistry 279 3439-3446. (doi:10.1074/jbc.M307138200) (Pubitemid 38140582)
14. Depoortere F, Pirson I, Bartek J, Dumont JE & Roger PP 2000 Transforming growth factor β(1) selectively inhibits the cyclic AMP-dependent proliferation of primary thyroid epithelial cells by preventing the association of cyclin D3-cdk4 with nuclear p27(kip1). Molecular Biology of the Cell 11 1061-1076.
15. ten Dijke P & Hill CS 2004 New insights into TGF-β-Smad signalling. Trends in Biochemical Sciences 29 265-273. (doi:10.1016/j.tibs.2004. 03.008)
16. Dupont S, Zacchigna L, Cordenonsi M, Soligo S, Adorno M, Rugge M & Piccolo S 2005 Germ-layer specification and control of cell growth by Ectodermin, a Smad4 ubiquitin ligase. Cell 121 87-99. (doi:10. 1016/j.cell.2005.01.033)
17. Erson AE & Petty EM 2008 MicroRNAs in development and disease. Clinical Genetics 74 296-306. (doi:10.1111/j.1399-0004.2008.01076.x)
18. Franzén Å, Piek E, Westermark B, ten Dijke P & Heldin NE 1999 Expression of transforming growth factor-β1, activin A, and their receptors in thyroid follicle cells: negative regulation of thyrocyte growth and function. Endocrinology 140 4300-4310. (doi:10.1210/ en.140.9.4300)
19. Goretzki PE, Frilling A, Simon D & Roeher HD 1990 Growth regulation of normal thyroids and thyroid tumors in man. Recent Results in Cancer Research 118 48-63.
20. de Groot RP & Kruijer W 1990 Transcriptional activation by TGF β1 mediated by the dyad symmetry element (DSE) and the TPA responsive element (TRE). Biochemical and Biophysical Research Communications 168 1074-1081. (doi:10.1016/0006- 291X(90)91139-J) (Pubitemid 20175990)
21. Grubeck-Loebenstein B, Buchan G, Sadeghi R, Kissonerghis M, Londei M, Turner M, Pirich K, Roka R, Niederle B, Kassal H et al. 1989 Transforming growth factor β regulates thyroid growth. Role in the pathogenesis of nontoxic goiter. Journal of Clinical Investigation 83 764-770. (doi:10.1172/JCI113955)
22. Gurdon JB & Bourillot PY 2001 Morphogen gradient interpretation. Nature 413 797-803. (doi:10.1038/35101500)
23. Heldin NE, Bergström D, Hermansson A, Bergenstråhle A, Nakao A, Westermark B & ten Dijke P 1999 Lack of responsiveness to TGF-β1 in a thyroid carcinoma cell line with functional type I and type II TGF-β receptors and Smad proteins, suggests a novel mechanism for TGF-β insensitivity in carcinoma cells. Molecular and Cellular Endocrinology 153 79-90. (doi:10.1016/S0303-7207(99)00086-6)
24. Hill CS 2001 TGF-β signalling pathways in early Xenopus development. Current Opinion in Genetics and Development 11 533-540. (doi:10.1016/ S0959-437X(00)00229-X)
25. Hill CS 2009 Nucleocytoplasmic shuttling of Smad proteins. Cell Research 19 36-46. (doi:10.1038/cr.2008.325)
26. Hogan C, Serpente N, Cogram P, Hosking CR, Bialucha CU, Feller SM, Braga VM, Birchmeier W & Fujita Y 2004 Rap1 regulates the formation of E-cadherin-based cell-cell contacts. Molecular and Cellular Biology 24 6690-6700. (doi:10.1128/MCB.24.15. 6690-6700.2004)
27. Hoodless PA, Tsukazaki T, Nishimatsu S, Attisano L, Wrana JL & Thomsen GH 1999 Dominant-negative Smad2 mutants inhibit activin/Vg1 signaling and disrupt axis formation in Xenopus. Developmental Biology 207 364-379. (doi:10.1006/dbio.1998.9168) (Pubitemid 29136350)
28. Imamura T, Takase M, Nishihara A, Oeda E, Hanai J, Kawabata M & Miyazono K 1997 Smad6 inhibits signalling by the TGF-β superfamily. Nature 389 622-626. (doi:10.1038/39355) (Pubitemid 27446182)
29. Iuliano R, Trapasso F, Le Pera I, Schepis F, Sama I, Clodomiro A, Dumon KR, Santoro M, Chiariotti L, Viglietto G et al. 2003 An adenovirus carrying the rat protein tyrosine phosphatase eta suppresses the growth of human thyroid carcinoma cell lines in vitro and in vivo. Cancer Research 63 882-886. (Pubitemid 36231992)
30. Keeton MR, Curriden SA, van Zonneveld AJ & Loskutoff DJ 1991 Identification of regulatory sequences in the type 1 plasminogen activator inhibitor gene responsive to transforming growth factor β. Journal of Biological Chemistry 266 23048-23052.
31. Kimura ET, Kopp P, Zbaeren J, Asmis LM, Ruchti C, Maciel RM & Studer H 1999 Expression of transforming growth factor β1, β2, and β3 in multinodular goiters and differentiated thyroid carcinomas: a comparative study. Thyroid 9 119-125. (doi:10.1089/ thy.1999.9.119)
32. Kogai T, Sajid-Crockett S, Newmarch LS, Liu YY & Brent GA 2008 Phosphoinositide-3-kinase inhibition induces sodium/iodide symporter expression in rat thyroid cells and human papillary thyroid cancer cells. Journal of Endocrinology 199 243-252. (doi:10.1677/JOE- 08-0333)
33. Lagna G, Hata A, Hemmati-Brivanlou A & Massagué J 1996 Partnership between DPC4 and SMAD proteins in TGF-β signalling pathways. Nature 383 832-836. (doi:10.1038/383832a0) (Pubitemid 26372668)
34. Lazzereschi D, Ranieri A, Mincione G, Taccogna S, Nardi F & Colletta G 1997 Human malignant thyroid tumors displayed reduced levels of transforming growth factor β receptor type II messenger RNA and protein. Cancer Research 57 2071-2076. (Pubitemid 27209743)
35. Lazzereschi D, Nardi F, Turco A, Ottini L, D'Amico C, Mariani- Costantini R, Gulino A & Coppa A 2005 A complex pattern of mutations and abnormal splicing of Smad4 is present in thyroid tumours. Oncogene 24 5344-5354. (doi:10.1038/sj.onc.1208603) (Pubitemid 43080104)
36. Liu F, Pouponnot C & Massagué J 1997 Dual role of the Smad4/DPC4 tumor suppressor in TGFβ-inducible transcriptional complexes. Genes and Development 11 3157-3167. (doi:10.1101/gad.11.23.3157) (Pubitemid 27528056)
37. Lönn P, Morén A, Raja E, Dahl M & Moustakas A 2009 Regulating the stability of TGFβ receptors and Smads. Cell Research 19 21-35. (doi:10.1038/cr.2008.308)
38. Matsuo SE, Leoni SG, Colquhoun A & Kimura ET 2006 Transforming growth factor-b1 and activin A generate antiproliferative signaling in thyroid cancer cells. Journal of Endocrinology 190 141-150. (doi:10. 1677/joe.1.06713) (Pubitemid 44161069)
39. Meireles AM, Preto A, Rocha AS, Rebocho AP, Máximo V, Pereira- Castro I, Moreira S, Feijão T, Botelho T, Marques R et al. 2007 Molecular and genotypic characterization of human thyroid follicular cell carcinoma-derived cell lines. Thyroid 17 707-715. (doi:10.1089/thy.2007.0097)
40. Morén A, Itoh S, Moustakas A, ten Dijke P & Heldin CH 2000 Functional consequences of tumorigenic missense mutations in the amino-terminal domain of Smad4. Oncogene 19 4396-4404. (doi:10. 1038/sj.onc.1203798)
41. Morosini P, Taccaliti A, Di Loreto C, Arnaldi G, Faloia E, Giacchetti G & Mantero F 1994 Transforming growth factor-β 1 is more expressed in thyroid follicular adenoma than in normal tissue. Journal of Endocrinological Investigation 17 335-340.
42. Morris JC III, Ranganathan G, Hay ID, Nelson RE & Jiang NS 1988 The effects of transforming growth factor-β on growth and differentiation of the continuous rat thyroid follicular cell line, FRTL-5. Endocrinology 123 1385-1394. (doi:10.1210/endo- 123-3-1385)
43. Motti ML, Califano D, Baldassarre G, Celetti A, Merolla F, Forzati F, Napolitano M, Tavernise B, Fusco A & Viglietto G 2005 Reduced E-cadherin expression contributes to the loss of p27kip1-mediated mechanism of contact inhibition in thyroid anaplastic carcinomas. Carcinogenesis 26 1021-1034. (doi:10.1093/carcin/bgi050) (Pubitemid 41214295)
44. Müller N, Reinacher-Schick A, Baldus S, van Hengel J, Berx G, Baar A, van Roy F, Schmiegel W & Schwarte-Waldhoff I 2002 Smad4 induces the tumor suppressor E-cadherin and P-cadherin in colon carcinoma cells. Oncogene 21 6049-6058. (doi:10.1038/sj.onc. 1205766)
45. Nakao A, Afrakhte M, Morén A, Nakayama T, Christian JL, Heuchel R, Itoh S, Kawabata M, Heldin NE, Heldin CH et al. 1997 Identification of Smad7, a TGFβ-inducible antagonist of TGF-β signaling. Nature 389 631-635. (doi:10.1038/39369)
46. Nicolussi A, D'Inzeo S, Santulli M, Colletta G & Coppa A 2003 TGF-β control of rat thyroid follicular cells differentiation. Molecular and Cellular Endocrinology 207 1-11. (doi:10.1016/S0303- 7207(03)00238-7) (Pubitemid 37102948)
47. Nicolussi A, D'Inzeo S, Gismondi A & Coppa A 2006 Reduction of invasive potential in K-ras-transformed thyroid cells by restoring of TGF-β pathway. Clinical and Experimental Metastasis 23 237-248. (doi:10.1007/s10585- 006-9023-0)
48. Padua D & Massagué J 2009 Roles of TGFb in metastasis. Cell Research 19 89-102. (doi:10.1038/cr.2008.316)
49. Pang XP, Hershman JM, Chung M & Pekary AE 1989 Characterization of tumor necrosis factor-α receptors in human and rat thyroid cells and regulation of the receptors by thyrotropin. Endocrinology 125 1783-1788. (doi:10.1210/endo-125-4-1783) (Pubitemid 19258610)
50. Patterson GI & Padgett RW 2000 TGF β-related pathways. Roles in Caenorhabditis elegans development. Trends in Genetics 16 27-33. (doi:10.1016/S0168-9525(99)01916-2)
51. - symporter messenger ribonucleic acid levels in FRTL-5 cells. Endocrinology 139 703-712. (doi:10.1210/en.139.2.703)
52. Pierreux CE, Nicolás FJ & Hill CS 2000 Transforming growth factor β-independent shuttling of Smad4 between the cytoplasm and nucleus. Molecular and Cellular Biology 20 9041-9054. (doi:10.1128/ MCB.20.23.9041-9054. 2000)
53. Pomérance M, Quillard J, Chantoux F, Young J & Blondeau JP 2006 High-level expression, activation, and subcellular localization of p38-MAP kinase in thyroid neoplasms. Journal of Pathology 209 298-306. (doi:10.1002/path.1975) (Pubitemid 43997738)
54. Riesco-Eizaguirre G, Rodríguez I, De la Vieja A, Costamagna E, Carrasco N, Nistal M & Santisteban P 2009 The BRAFV600E oncogene induces transforming growth factor β secretion leading to sodium iodide symporter repression and increased malignancy in thyroid cancer. Cancer Research 69 8317-8325. (doi:10.1158/0008- 5472.CAN-09-1248)
55. Rosenwald IB 2004 The role of translation in neoplastic transformation from a pathologist's point of view. Oncogene 23 3230-3247. (doi:10.1038/sj.onc. 1207552)
56. Salerno P, De Falco V, Tamburrino A, Nappi TC, Vecchio G, Schweppe RE, Bollag G, Santoro M & Salvatore G 2010 Cytostatic activity of adenosine triphosphate-competitive kinase inhibitors in BRAF mutant thyroid carcinoma cells. Journal of Clinical Endocrinology and Metabolism 95 450-455. (doi:10.1210/jc.2009-0373)
57. Sancho M, Vieira JM, Casalou C, Mesquita M, Pereira T, Cavaco BM, Dias S & Leite V 2006 Expression and function of the chemokine receptor CCR7 in thyroid carcinomas. Journal of Endocrinology 191 229-238. (doi:10.1677/joe.1. 06688)
58. Scarpino S, Di Napoli A, Melotti F, Talerico C, Cancrini A & Ruco L 2007 Papillary carcinoma of the thyroid: low expression of NCAM (CD56) is associated with downregulation of VEGF-D production by tumour cells. Journal of Pathology 212 411-419. (doi:10.1002/path.2183) (Pubitemid 47099018)
59. Schutte M, Hruban RH, Hedrick L, Cho KR, Nadasdy GM, Weinstein CL, Bova GS, Isaacs WB, Cairns P, NawrozHet al. 1996 DPC4 gene in various tumor types. Cancer Research 56 2527-2530.
60. Schweppe RE, Klopper JP, Korch C, Pugazhenthi U, Benezra M, Knauf JA, Fagin JA, Marlow LA, Copland JA, Smallridge RC et al. 2008 Deoxyribonucleic acid profiling analysis of 40 human thyroid cancer cell lines reveals cross-contamination resulting in cell line redundancy and misidentification. Journal of Clinical Endocrinology and Metabolism 93 4331-4341. (doi:10.1210/ jc.2008-1102)
61. Shi Y & Massagué J 2003 Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 113 685-700. (doi:10.1016/S0092- 8674(03)00432-X) (Pubitemid 36724933)
62. Shimura H, Suzuki H, Miyazaki A, Furuya F, Ohta K, Haraguchi K, Endo T & Onaya T 2001 Transcriptional activation of the thyroglobulin promoter directing suicide gene expression by thyroid transcription factor-1 in thyroid cancer cells. Cancer Research 61 3640-3646. (Pubitemid 32694974)
63. Shiou S, Singh AB, Moorthy K, Datta PK, Washington MK, Beauchamp RD & Dhawan P 2007 Smad4 regulates claudin-1 expression in a transforming growth factor-b-independent manner in colon cancer cells. Cancer Research 67 1571-1579. (doi:10.1158/0008-5472.CAN- 06-1680)
64. Suzuki C, Murakami G, Fukuchi M, Shimanuki T, Shikauchi Y, Imamura T & Miyazono K 2002 Smurf1 regulates the inhibitory activity of Smad7 by targeting Smad7 to the plasma membrane. Journal of Biological Chemistry 277 39919-39925. (doi:10.1074/jbc. M201901200)
65. Takaku K, Oshima M, Miyoshi H, Matsui M, Seldin MF & Taketo MM 1998 Intestinal tumorigenesis in compound mutant mice of both Dpc4 (Smad4) and Apc genes. Cell 92 645-656. (doi:10.1016/ S0092-8674(00)81132-0) (Pubitemid 28141513)
66. Taton M, Lamy F, Roger PP & Dumont JE 1993 General inhibition by transforming growth factor β 1 of thyrotropin and cAMP responses in human thyroid cells in primary culture. Molecular and Cellular Endocrinology 95 13-21. (doi:10.1016/0303-7207(93)90024-E) (Pubitemid 23267191)
67. Tian X, Du H, Fu X, Li K, Li A & Zhang Y 2009 Smad4 restoration leads to a suppression of Wnt/β-catenin signaling activity and migration capacity in human colon carcinoma cells. Biochemical and Biophysical Research Communications 380 478-483. (doi:10. 1016/j.bbrc.2009.01.124)
68. Turco A, Coppa A, Aloe S, Baccheschi G, Morrone S, Zupi G & Colletta G 1999 Overexpression of transforming growth factor b-type II receptor reduces tumorigenicity and metastastic potential of K-ras-transformed thyroid cells. International Journal of Cancer 80 85-91. (doi:10.1002/(SICI)1097-0215 (19990105)80:1〈85::AID-IJC17〉3.0.CO;2-P)
69. Vasko V, Espinosa AV, Scouten W, He H, Auer H, Liyanarachchi S, Larin A, Savchenko V, Francis GL, de la Chapelle A et al. 2007 Gene expression and functional evidence of epithelial to mesenchymal transition in papillary thyroid carcinoma invasion. PNAS 104 2803-2808. (doi:10.1073/pnas.0610733104)
70. Visconti R, Federico A, Coppola V, Pentimalli F, Berlingieri MT, Pallante P, Kruhoffer M, Orntoft TF & Fusco A 2007 Transcriptional profile of Ki-Ras-induced transformation of thyroid cells. Cancer Investigation 25 256-266. (doi:10.1080/07357900701206406) (Pubitemid 47026943)
71. Visone R, Russo L, Pallante P, De Martino I, Ferraro A, Leone V, Borbone E, Petrocca F, Alder H, Croce CM et al. 2007 MicroRNAs (miR)-221 and miR-222, both overexpressed in human thyroid papillary carcinomas, regulate p27Kip1 protein levels and cell cycle. Endocrine-Related Cancer 14 791-798. (doi:10. 1677/ERC-07-0129)
72. Watanabe M, Masuyama N, Fukuda M & Nishida E 2000 Regulation of intracellular dynamics of Smad4 by its leucine-rich nuclear export signal. EMBO Reports 1 176-182. (doi:10.1093/embo-reports/ kvd029)
73. Wrana JL, Attisano L, Carcamo J, Zentella A, Doody J, Laiho M, Wang XF & Massagué J 1992 TGF β signals through a heteromeric protein kinase receptor complex. Cell 71 1003-1014. (doi:10. 1016/0092-8674(92)90395-S)
74. Wyllie FS, Dawson T, Bond JA, Goretzki P, Game S, Prime S &Wynford- Thomas D 1991 Correlated abnormalities of transforming growth factor-b1 response and p53 expression in thyroid epithelial cell transformation. Molecular and Cellular Endocrinology 76 13-21. (doi:10.1016/0303-7207(91)90255-Q)
75. Yingling JM, Wang XF & Bassing CH 1995 Signaling by the transforming growth factor-β receptors. Biochimica et Biophysica Acta 1242 115-136.