A novel human Smad4 mutation is involved in papillary thyroid carcinoma progression

Endocrine-Related Cancer

Volumn 19, Issue 1, 2012, Pages 39-55

  D'Inzeo, Sonia ^a   Nicolussi, Arianna ^a   Donini, Caterina Francesca ^a   Zani, Massimo ^b   Mancini, Patrizia ^a   Nardi, Francesco ^a   Coppa, Anna ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRONECTIN; LAMININ; RECOMBINANT TRANSFORMING GROWTH FACTOR BETA1; SMAD4 PROTEIN; UVOMORULIN; SMAD4 PROTEIN, HUMAN; TRANSFORMING GROWTH FACTOR BETA1;

ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER GROWTH; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENE MUTATION; HUMAN; HUMAN CELL; LYMPH NODE METASTASIS; OLIGOMERIZATION; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; THYROID PAPILLARY CARCINOMA; CANCER INVASION; CARCINOMA; CELL ADHESION; CELL MOTION; DISEASE COURSE; GENETICS; METABOLISM; MUTATION; PATHOLOGY; THYROID CANCER; THYROID TUMOR; TUMOR CELL LINE;

CARCINOMA; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DISEASE PROGRESSION; HUMANS; MUTATION; NEOPLASM INVASIVENESS; SMAD4 PROTEIN; THYROID NEOPLASMS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84860431089     PISSN: 13510088     EISSN: 14796821     Source Type: Journal    
DOI: 10.1530/ERC-11-0233     Document Type: Article

References (60)

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 & Lee-Hoeflich ST 2001 The Smads. Genome Biology 2 reviews30101-reviews30108. (doi:10.1186/gb-2001-2-8-reviews3010)
3. Blobe GC, Schiemann WP & Lodish HF 2000 Role of transforming growth factor beta in human disease. New England Journal of Medicine 342 1350-1358. (doi:10.1056/NEJM200005043421807)
4. Bornstein S, White R, Malkoski S, Oka M, Han G, Cleaver T, Reh D, Andersen P, Gross N, Olson S et al. 2009 Smad4 loss in mice causes spontaneous head and neck cancer with increased genomic instability and inflammation. Journal of Clinical Investigation 119 3408-3419. (doi:10.1172/JCI38854)
5. Chacko BM, Qin BY, Tiwari A, Shi G, Lam S, Hayward LJ, De Caestecker M & Lin K 2004 Structural basis of heteromeric smad protein assembly in TGF-beta signaling. Molecular Cell 15 813-823. (doi:10.1016/j.molcel.2004.07. 016)
6. Chen Y, Yee D & Magnuson T 2006 A novel mouse Smad4 mutation reduces protein stability and wild-type protein levels. Mammalian Genome 17 211-219. (doi:10.1007/s00335-005-0074-3)
7. Derynck R & Akhurst RJ 2007 Differentiation plasticity regulated by TGF-beta family proteins in development and disease. Nature Cell Biology 9 1000-1004. (doi:10.1038/ncb434)
8. ten Dijke P & Hill CS 2004 New insights into TGF-beta-Smad signalling. Trends in Biochemical Sciences 29 265-273. (doi:10.1016/j.tibs.2004. 03.008)
9. D'Inzeo S, Nicolussi A, Ricci A, Mancini P, Porcellini A, Nardi F & Coppa A 2010 Role of reduced expression of SMAD4 in papillary thyroid carcinoma. Journal of Molecular Endocrinology 45 229-244. (doi:10.1677/JME-10-0044)
10. Gassmann P, Enns A & Haier J 2004 Role of tumor cell adhesion and migration in organ-specific metastasis formation. Onkologie 27 577-582. (doi:10.1159/000081343)
11. de Groot RP & Kruijer W 1990 Transcriptional activation by TGF beta 1 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)
12. Gurdon JB & Bourillot PY 2001 Morphogen gradient interpretation. Nature 413 797-803. (doi:10.1038/35101500)
13. Hahn SA, Schutte M, Hoque AT, Moskaluk CA, da Costa LT, Rozenblum E, Weinstein CL, Fischer A, Yeo CJ, Hruban RH et al. 1996 DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science 271 350-353. (doi:10.1126/science.271.5247.350)
14. Hata A, Lo RS, Wotton D, Lagna G & Massagué J 1997 Mutations increasing autoinhibition inactivate tumour suppressors Smad2 and Smad4. Nature 388 82-87. (doi:10.1038/40424)
15. Heldin CH, Miyazono K & ten Dijke P 1997 TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 390 465-471. (doi:10.1038/37284)
16. Hill CS 2001 TGF-beta signalling pathways in early Xenopus development. Current Opinion in Genetics &Development 11 533-540. (doi:10.1016/S0959- 437X(00)00229-X)
17. Hill CS 2009 Nucleocytoplasmic shuttling of Smad proteins. Cell Research 19 36-46. (doi:10.1038/cr.2008.325)
18. 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)
19. 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)
20. Iacobuzio-Donahue CA, Song J, Parmiagiani G, Yeo CJ, Hruban RH & Kern SE 2004 Missense mutations of MADH4: characterization of the mutational hot spot and functional consequences in human tumors. Clinical Cancer Research 10 1597-1604. (doi:10.1158/1078-0432.CCR-1121-3)
21. Ikushima H & Miyazono K 2010 TGFbeta signalling: a complex web in cancer progression. Nature Reviews. Cancer 10 415-424. (doi:10.1038/nrc2853)
22. Jayaraman L & Massague J 2000 Distinct oligomeric states of SMAD proteins in the transforming growth factor-beta pathway. Journal of Biological Chemistry 275 40710-40717. (doi:10.1074/jbc.M005799200)
23. 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 beta. Journal of Biological Chemistry 266 23048-23052. (Pubitemid 21908758)
24. Knauf JA, Sartor MA, Medvedovic M, Lundsmith E, Ryder M, Salzano M, Nikiforov YE, Giordano TJ, Ghossein RA &Fagin JA 2011 Progression of BRAF-induced thyroid cancer is associated with epithelial-mesenchymal transition requiring concomitant MAP kinase and TGFβ signaling. Oncogene 30 3153-3162. (doi:10.1038/onc.2011.44)
25. 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)
26. 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)
27. Liu F, Pouponnot C & Massagué J 1997 Dual role of the Smad4/DPC4 tumor suppressor in TGFbeta-inducible transcriptional complexes. Genes and Development 11 3157-3167. (doi:10.1101/gad.11.23.3157)
28. Massagué J 1998 TGF-beta signal transduction. Annual Review of Biochemistry 67 753-791. (doi:10.1146/annurev.biochem.67.1.753)
29. Massagué J & Gomis RR 2006 The logic of TGFbeta signaling. FEBS Letters 580 2811-2820. (doi:10.1016/j.febslet.2006.04.033)
30. Massagué J, Seoane J & Wotton D 2005 Smad transcription factors. Genes and Development 19 2783-2810. (doi:10.1101/gad.1350705)
31. Miettinen PJ, Ebner R, Lopez AR & Derynck R 1994 TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. Journal of Cell Biology 127 2021-2036. (doi:10.1083/jcb.127.6.2021)
32. Miyaki M, Iijima T, Konishi M, Sakai K, Ishii A, Yasuno M, Hishima T, Koike M, Shitara N, Iwama T et al. 1999 Higher frequency of Smad4 gene mutation in human colorectal cancer with distant metastasis. Oncogene 18 3098-3103. (doi:10.1038/sj.onc.1202642)
33. Morén A, Itoh S, Moustakas A, 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)
34. Nicolussi A, D'Inzeo S, Santulli M, Colletta G & Coppa A 2003 TGF-beta control of rat thyroid follicular cells differentiation. Molecular and Cellular Endocrinology 207 1-11. (doi:10.1016/S0303-7207(03)00238-7)
35. Nicolussi A, D'Inzeo S, Gismondi A & Coppa A 2006 Reduction of invasive potential in K-ras-transformed thyroid cells by restoring of TGF-beta pathway. Clinical and Experimental Metastasis 23 237-248. (doi:10.1007/s10585- 006-9023-0)
36. Padua D & Massagué J 2009 Roles of TGFbeta in metastasis. Cell Research 19 89-102. (doi:10.1038/cr.2008.316)
37. Pang XP, Hershman JM, Chung M & Pekary AE 1989 Characterization of tumor necrosis factor-alpha 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)
38. Pardali K & Moustakas A 2007 Actions of TGF-beta as tumor suppressor and pro-metastatic factor in human cancer. Biochimica et Biophysica Acta 1775 21-62. (Pubitemid 44881193)
39. Pierreux CE, Nicolás FJ & Hill CS 2000 Transforming growth factor beta-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)
40. 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)
41. Prokova V, Mavridou S, Papakosta P, Petratos K &Kardassis D 2007 Novel mutations in Smad proteins that inhibit signaling by the transforming growth factor beta in mammalian cells. Biochemistry 46 13775-13786. (doi:10.1021/bi701540u)
42. 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 beta 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)
43. Schmierer B, Tournier AL, Bates PA & Hill CS 2008 Mathematical modeling identifies Smad nucleocytoplasmic shuttling as a dynamic signal-interpreting system. PNAS 105 6608-6613. (doi:10.1073/pnas.0710134105)
44. Schutte M, Hruban RH, Hedrick L, Cho KR, Nadasdy GM, Weinstein CL, Bova GS, Isaacs WB, Cairns P, Nawroz H et al. 1996 DPC4 gene in various tumor types. Cancer Research 56 2527-2530. (Pubitemid 26170688)
45. Shi Y 2001 Structural insights on Smad function in TGFbeta signaling. BioEssays 23 223-232. (doi:10.1002/1521-1878(200103)23:3<223::AID- BIES1032>3.0.CO;2-U)
46. Shi Y, Hata A, Lo RS, Massagué J & Pavletich NP 1997 A structural basis for mutational inactivation of the tumour suppressor Smad4. Nature 388 87-93. (doi:10.1038/40431)
47. 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)
48. Thiagalingam S, Lengauer C, Leach FS, Schutte M, Hahn SA, Overhauser J, Willson JK, Markowitz S, Hamilton SR, Kern SE et al. 1996 Evaluation of candidate tumour suppressor genes on chromosome 18 in colorectal cancers. Nature Genetics 13 343-346. (doi:10.1038/ng0796-343)
49. Thiery JP 2003 Epithelial-mesenchymal transitions in development and pathologies. Current Opinion in Cell Biology 15 740-746. (doi:10.1016/j.ceb. 2003.10.006)
50. Varelas X, Sakuma R, Samavarchi-Tehrani P, Peerani R, Rao BM, Dembowy J, Yaffe MB, Zandstra PW &Wrana JL 2008 TAZ controls Smad nucleocytoplasmic shuttling and regulates human embryonic stem-cell self-renewal. Nature Cell Biology 10 837-848. (doi:10.1038/ncb1748)
51. Vincent T, Neve EP, Johnson JR, Kukalev A, Rojo F, Albanell J, Pietras K, Virtanen I, Philipson L, Leopold PL et al. 2009 A SNAIL1-SMAD3/4 transcriptional repressor complex promotes TGF-beta mediated epithelial-mesenchymal transition. Nature Cell Biology 11 943-950. (doi:10.1038/ncb1905)
52. 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)
53. 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)
54. Wikström P, Stattin P, Franck-Lissbrant I, Damber JE &Bergh A 1998 Transforming growth factor beta1 is associated with angiogenesis, metastasis, and poor clinical outcome in prostate cancer. Prostate 37 19-29. (doi:10.1002/(SICI)1097-0045(19980915)37:1<19::AID-PROS4>3.0.CO;2-3)
55. de Winter JP, Roelen BA, ten Dijke P, van der Burg B & van den Eijnden-van Raaij AJ 1997 DPC4 (SMAD4) mediates transforming growth factor-beta1 (TGF-beta1) induced growth inhibition and transcriptional response in breast tumour cells. Oncogene 14 1891-1899. (doi:10.1038/sj.onc.1201017)
56. Wotton D, Lo RS, Lee S & Massagué J 1999 A Smad transcriptional corepressor. Cell 97 29-39. (doi:10.1016/S0092-8674(00)80712-6)
57. Wrana JL, Attisano L, Carcamo J, Zentella A, Doody J, Laiho M, Wang XF & Massagué J 1992 TGFbeta signals through a heteromeric protein kinase receptor complex. Cell 71 1003-1014. (doi:10.1016/0092-8674(92)90395-S)
58. Wu JW, Fairman R, Penry J & Shi Y 2001 Formation of a stable heterodimer between Smad2 and Smad4. Journal of Biological Chemistry 276 20688-20694. (doi:10.1074/jbc.M100174200)
59. Xu L, Kang Y, Cöl S & Massagué J 2002 Smad2 nucleocytoplasmic shuttling by nucleoporins CAN/Nup214 and Nup153 feeds TGFbeta signaling complexes in the cytoplasm and nucleus. Molecular Cell 10 271-282. (doi:10.1016/S1097-2765(02)00586-5)
60. Yamaguchi H, Wyckoff J & Condeelis J 2005 Cell migration in tumors. Current Opinion in Cell Biology 17 559-564. (doi:10.1016/j.ceb.2005.08.002)