Genetic markers differentiating follicular thyroid carcinoma from benign lesions

Molecular and Cellular Endocrinology

Volumn 321, Issue 1, 2010, Pages 77-85

  Freitas, Beatriz C G ^a   Cerutti, Janete M ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

FNA; Follicular thyroid adenoma; Follicular thyroid carcinoma; Indeterminate nodule; Molecular markers

Indexed keywords

ARGINASE 2; BIOLOGICAL MARKER; GALECTIN 3; GENE PRODUCT; INTESTINAL TREFOIL FACTOR; MICRORNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN ARG2; PROTEIN TFF3; TELOMERASE REVERSE TRANSCRIPTASE; TRANSCRIPTION FACTOR PAX8; UNCLASSIFIED DRUG;

ASPIRATION BIOPSY; CELL DIFFERENTIATION; CHROMOSOME REARRANGEMENT; CHROMOSOME TRANSLOCATION; COST EFFECTIVENESS ANALYSIS; DIAGNOSTIC ACCURACY; DOWN REGULATION; GENE EXPRESSION PROFILING; GENE MUTATION; GENETIC MARKER; GENETIC TRANSCRIPTION; HUMAN; IMMUNOHISTOCHEMISTRY; NONHUMAN; PREOPERATIVE PERIOD; PRIORITY JOURNAL; REVIEW; SERIAL ANALYSIS OF GENE EXPRESSION; THYROID FOLLICULAR CARCINOMA;

ADENOCARCINOMA, FOLLICULAR; DIAGNOSIS, DIFFERENTIAL; GENE EXPRESSION PROFILING; GENETIC MARKERS; HUMANS; THYROID NEOPLASMS; THYROID NODULE;

EID: 77950920868     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2009.11.008     Document Type: Review

References (103)

1. Baloch Z.W., Gupta P.K., Yu G.H., Sack M.J., LiVolsi V.A. Follicular variant of papillary carcinoma. Cytologic and histologic correlation. Am. J. Clin. Pathol. 1999, 111:216-222.
2. Baloch Z.W., Fleisher S., LiVolsi V.A., Gupta P.K. Diagnosis of " follicular neoplasm": a gray zone in thyroid fine-needle aspiration cytology. Diagn. Cytopathol. 2002, 26:41-44.
3. Baloch Z.W., LiVolsi V.A., Asa S.L., Rosai J., Merino M.J., Randolph G., Vielh P., DeMay R.M., Sidawy M.K., Frable W.J. Diagnostic terminology and morphologic criteria for cytologic diagnosis of thyroid lesions: a synopsis of the National Cancer Institute Thyroid Fine-Needle Aspiration State of the Science Conference. Diagn. Cytopathol. 2008, 36:425-437.
4. Barden C.B., Shister K.W., Zhu B., Guiter G., Greenblatt D.Y., Zeiger M.A., Fahey T.J. Classification of follicular thyroid tumors by molecular signature: results of gene profiling. Clin. Cancer Res. 2003, 9:1792-1800.
5. Baris O., Savagner F., Nasser V., Loriod B., Granjeaud S., Guyetant S., Franc B., Rodien P., Rohmer V., Bertucci F., Birnbaum D., Malthiery Y., Reynier P., Houlgatte R. Transcriptional profiling reveals coordinated up-regulation of oxidative metabolism genes in thyroid oncocytic tumors. J. Clin. Endocrinol. Metab. 2004, 89:994-1005.
6. Barroeta J.E., Baloch Z.W., Lal P., Pasha T.L., Zhang P.J., LiVolsi V.A. Diagnostic value of differential expression of CK19, Galectin-3, HBME-1, ERK, RET, and p16 in benign and malignant follicular-derived lesions of the thyroid: an immunohistochemical tissue microarray analysis. Endocr. Pathol. 2006, 17:225-234.
7. Bartolazzi A., Gasbarri A., Papotti M., Bussolati G., Lucante T., Khan A., Inohara H., Marandino F., Orlandi F., Nardi F., Vecchione A., Tecce R., Larsson O. Application of an immunodiagnostic method for improving preoperative diagnosis of nodular thyroid lesions. Lancet 2001, 357:1644-1650.
8. Bartolazzi A., Papotti M., Orlandi F. Methodological considerations regarding the use of galectin-3 expression analysis in preoperative evaluation of thyroid nodules. J. Clin. Endocrinol. Metab. 2003, 88(950):950. (author reply 950-1).
9. Bartolazzi A., Orlandi F., Saggiorato E., Volante M., Arecco F., Rossetto R., Palestini N., Ghigo E., Papotti M., Bussolati G., Martegani M.P., Pantellini F., Carpi A., Giovagnoli M.R., Monti S., Toscano V., Sciacchitano S., Pennelli G.M., Mian C., Pelizzo M.R., Rugge M., Troncone G., Palombini L., Chiappetta G., Botti G., Vecchione A., Bellocco R. Galectin-3-expression analysis in the surgical selection of follicular thyroid nodules with indeterminate fine-needle aspiration cytology: a prospective multicentre study. Lancet Oncol. 2008, 9:543-549.
10. Boon K., Osorio E.C., Greenhut S.F., Schaefer C.F., Shoemaker J., Polyak K., Morin P.J., Buetow K.H., Strausberg R.L., De Souza S.J., Riggins G.J. An anatomy of normal and malignant gene expression. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:11287-11292.
11. Bryson P.C., Shores C.G., Hart C., Thorne L., Patel M.R., Richey L., Farag A., Zanation A.M. Immunohistochemical distinction of follicular thyroid adenomas and follicular carcinomas. Arch. Otolaryngol. Head Neck Surg. 2008, 134:581-586.
12. Camacho C.P., Latini F.R., Oler G., Hojaij F.C., Maciel R.M., Riggins G.J., Cerutti J.M. Down-regulation of NR4A1 in follicular thyroid carcinomas is restored following lithium treatment. Clin. Endocrinol. (Oxf.) 2009, 70:475-483.
13. Castro P., Roque L., Magalhaes J., Sobrinho-Simoes M. A subset of the follicular variant of papillary thyroid carcinoma harbors the PAX8-PPARgamma translocation. Int. J. Surg. Pathol. 2005, 13:235-238.
14. Castro P., Rebocho A.P., Soares R.J., Magalhaes J., Roque L., Trovisco V., Vieira de Castro I., Cardoso-de-Oliveira M., Fonseca E., Soares P., Sobrinho-Simoes M. PAX8-PPARgamma rearrangement is frequently detected in the follicular variant of papillary thyroid carcinoma. J. Clin. Endocrinol. Metab. 2006, 91:213-220.
15. Cerutti J.M., Riggins G.J., de Souza S.J. What can digital transcript profiling reveal about human cancers?. Braz. J. Med. Biol. Res. 2003, 36:975-985.
16. Cerutti J.M., Delcelo R., Amadei M.J., Nakabashi C., Maciel R.M., Peterson B., Shoemaker J., Riggins G.J. A preoperative diagnostic test that distinguishes benign from malignant thyroid carcinoma based on gene expression. J. Clin. Invest. 2004, 113:1234-1242.
17. Cerutti J.M., Latini F.R., Nakabashi C., Delcelo R., Andrade V.P., Amadei M.J., Maciel R.M., Hojaij F.C., Hollis D., Shoemaker J., Riggins G.J. Diagnosis of suspicious thyroid nodules using four protein biomarkers. Clin. Cancer Res. 2006, 12:3311-3318.
18. Cerutti J.M. Nodule diagnosed as follicular patterned lesion: are biomarkers the promise?. Arq. Bras. Endocrinol. Metabol. 2007, 51:832-842.
19. Cerutti J.M., Oler G., Michaluart P., Delcelo R., Beaty R.M., Shoemaker J., Riggins G.J. Molecular profiling of matched samples identifies biomarkers of papillary thyroid carcinoma lymph node metastasis. Cancer Res. 2007, 67:7885-7892.
20. Cheng S.Y. Thyroid hormone receptor mutations in cancer. Mol. Cell. Endocrinol. 2003, 213:23-30.
21. Cheung L., Messina M., Gill A., Clarkson A., Learoyd D., Delbridge L., Wentworth J., Philips J., Clifton-Bligh R., Robinson B.G. Detection of the PAX8-PPAR gamma fusion oncogene in both follicular thyroid carcinomas and adenomas. J. Clin. Endocrinol. Metab. 2003, 88:354-357.
22. Chevillard S., Ugolin N., Vielh P., Ory K., Levalois C., Elliott D., Clayman G.L., El-Naggar A.K. Gene expression profiling of differentiated thyroid neoplasms: diagnostic and clinical implications. Clin. Cancer Res. 2004, 10:6586-6597.
23. Collet J.F., Hurbain I., Prengel C., Utzmann O., Scetbon F., Bernaudin J.F., Fajac A. Galectin-3 immunodetection in follicular thyroid neoplasms: a prospective study on fine-needle aspiration samples. Br. J. Cancer 2005, 93:1175-1181.
24. Cvejic D., Savin S., Paunovic I., Tatic S., Havelka M., Sinadinovic J. Immunohistochemical localization of galectin-3 in malignant and benign human thyroid tissue. Anticancer Res. 1998, 18:2637-2641.
25. Dahia P.L., Marsh D.J., Zheng Z., Zedenius J., Komminoth P., Frisk T., Wallin G., Parsons R., Longy M., Larsson C., Eng C. Somatic deletions and mutations in the Cowden disease gene. PTEN, in sporadic thyroid tumors. Cancer Res. 1997, 57:4710-4713.
26. de Matos P.S., Ferreira A.P., de Oliveira Facuri F., Assumpcao L.V., Metze K., Ward L.S. Usefulness of HBME-1, cytokeratin 19 and galectin-3 immunostaining in the diagnosis of thyroid malignancy. Histopathology 2005, 47:391-401.
27. Di Cristofaro J., Silvy M., Lanteaume A., Marcy M., Carayon P., De Micco C. Expression of tpo mRNA in thyroid tumors: quantitative PCR analysis and correlation with alterations of ret, Braf, ras and pax8 genes. Endocr. Relat. Cancer 2006, 13:485-495.
28. Durand S., Ferraro-Peyret C., Selmi-Ruby S., Paulin C., El Atifi M., Berger F., Berger-Dutrieux N., Decaussin M., Peix J.L., Bournaud C., Orgiazzi J., Borson-Chazot F., Rousset B. Evaluation of gene expression profiles in thyroid nodule biopsy material to diagnose thyroid cancer. J. Clin. Endocrinol. Metab. 2008, 93:1195-1202.
29. Dwight T., Thoppe S.R., Foukakis T., Lui W.O., Wallin G., Hoog A., Frisk T., Larsson C., Zedenius J. Involvement of the PAX8/peroxisome proliferator-activated receptor gamma rearrangement in follicular thyroid tumors. J. Clin. Endocrinol. Metab. 2003, 88:4440-4445.
30. Ezzat S., Sarti D.A., Cain D.R., Braunstein G.D. Thyroid incidentalomas. Prevalence by palpation and ultrasonography. Arch. Intern. Med. 1994, 154:1838-1840.
31. Fernandez P.L., Merino M.J., Gomez M., Campo E., Medina T., Castronovo V., Sanjuan X., Cardesa A., Liu F.T., Sobel M.E. Galectin-3 and laminin expression in neoplastic and non-neoplastic thyroid tissue. J. Pathol. 1997, 181:80-86.
32. Finley D.J., Zhu B., Barden C.B., Fahey T.J. Discrimination of benign and malignant thyroid nodules by molecular profiling. Ann. Surg. 2004, 240:425-436.
33. Foukakis T., Gusnanto A., Au A.Y., Hoog A., Lui W.O., Larsson C., Wallin G., Zedenius J. A PCR-based expression signature of malignancy in follicular thyroid tumors. Endocr. Relat. Cancer 2007, 14:381-391.
34. Franc B., de la Salmoniere P., Lange F., Hoang C., Louvel A., de Roquancourt A., Vilde F., Hejblum G., Chevret S., Chastang C. Interobserver and intraobserver reproducibility in the histopathology of follicular thyroid carcinoma. Hum. Pathol. 2003, 34:1092-1100.
35. French C.A., Alexander E.K., Cibas E.S., Nose V., Laguette J., Faquin W., Garber J., Moore F., Fletcher J.A., Larsen P.R., Kroll T.G. Genetic and biological subgroups of low-stage follicular thyroid cancer. Am. J. Pathol. 2003, 162:1053-1060.
36. Garcia-Rostan G., Costa A.M., Pereira-Castro I., Salvatore G., Hernandez R., Hermsem M.J., Herrero A., Fusco A., Cameselle-Teijeiro J., Santoro M. Mutation of the PIK3CA gene in anaplastic thyroid cancer. Cancer Res. 2005, 65:10199-10207.
37. Giordano T.J., Au A.Y., Kuick R., Thomas D.G., Rhodes D.R., Wilhelm K.G., Vinco M., Misek D.E., Sanders D., Zhu Z., Ciampi R., Hanash S., Chinnaiyan A., Clifton-Bligh R.J., Robinson B.G., Nikiforov Y.E., Koenig R.J. Delineation, functional validation, and bioinformatic evaluation of gene expression in thyroid follicular carcinomas with the PAX8-PPARG translocation. Clin. Cancer Res. 2006, 12:1983-1993.
38. Grebe S.K., McIver B., Hay I.D., Wu P.S., Maciel L.M., Drabkin H.A., Goellner J.R., Grant C.S., Jenkins R.B., Eberhardt N.L. Frequent loss of heterozygosity on chromosomes 3p and 17p without VHL or p53 mutations suggests involvement of unidentified tumor suppressor genes in follicular thyroid carcinoma. J. Clin. Endocrinol. Metab. 1997, 82:3684-3691.
39. Griffith O.L., Melck A., Jones S.J., Wiseman S.M. Meta-analysis and meta-review of thyroid cancer gene expression profiling studies identifies important diagnostic biomarkers. J. Clin. Oncol. 2006, 24:5043-5051.
40. Haugen B.R., Nawaz S., Markham N., Hashizumi T., Shroyer A.L., Werness B., Shroyer K.R. Telomerase activity in benign and malignant thyroid tumors. Thyroid 1997, 7:337-342.
41. He H., Jazdzewski K., Li W., Liyanarachchi S., Nagy R., Volinia S., Calin G.A., Liu C.G., Franssila K., Suster S., Kloos R.T., Croce C.M., de la Chapelle A. The role of microRNA genes in papillary thyroid carcinoma. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:19075-19080.
42. Herrmann M.A., Hay I.D., Bartelt D.H., Ritland S.R., Dahl R.J., Grant C.S., Jenkins R.B. Cytogenetic and molecular genetic studies of follicular and papillary thyroid cancers. J. Clin. Invest. 1991, 88:1596-1604.
43. Herrmann M.E., LiVolsi V.A., Pasha T.L., Roberts S.A., Wojcik E.M., Baloch Z.W. Immunohistochemical expression of galectin-3 in benign and malignant thyroid lesions. Arch. Pathol. Lab. Med. 2002, 126:710-713.
44. Hibi Y., Nagaya T., Kambe F., Imai T., Funahashi H., Nakao A., Seo H. Is thyroid follicular cancer in Japanese caused by a specific t(2; 3)(q13; p25) translocation generating Pax8-PPAR gamma fusion mRNA?. Endocr. J. 2004, 51:361-366.
45. Joseph B., Ji M., Liu D., Hou P., Xing M. Lack of mutations in the thyroid hormone receptor (TR) alpha and beta genes but frequent hypermethylation of the TRbeta gene in differentiated thyroid tumors. J. Clin. Endocrinol. Metab. 2007, 92:4766-4770.
46. Kato Y., Ying H., Willingham M.C., Cheng S.Y. A tumor suppressor role for thyroid hormone beta receptor in a mouse model of thyroid carcinogenesis. Endocrinology 2004, 145:4430-4438.
47. Krause K., Eszlinger M., Gimm O., Karger S., Engelhardt C., Dralle H., Fuhrer D. TFF3-based candidate gene discrimination of benign and malignant thyroid tumors in a region with borderline iodine deficiency. J. Clin. Endocrinol. Metab. 2008, 93:1390-1393.
48. Kroll T.G., Sarraf P., Pecciarini L., Chen C.J., Mueller E., Spiegelman B.M., Fletcher J.A. PAX8-PPARgamma1 fusion oncogene in human thyroid carcinoma [corrected]. Science 2000, 289:1357-1360.
49. Lacroix L., Lazar V., Michiels S., Ripoche H., Dessen P., Talbot M., Caillou B., Levillain J.P., Schlumberger M., Bidart J.M. Follicular thyroid tumors with the PAX8-PPARgamma1 rearrangement display characteristic genetic alterations. Am. J. Pathol. 2005, 167:223-231.
50. Layfield L.J., Cibas E.S., Gharib H., Mandel S.J. Thyroid aspiration cytology: current status. CA Cancer J. Clin. 2009, 59:99-110.
51. Liou M.J., Chan E.C., Lin J.D., Liu F.H., Chao T.C. Human telomerase reverse transcriptase (hTERT) gene expression in FNA samples from thyroid neoplasms. Cancer Lett. 2003, 191:223-227.
52. Liu Z., Hou P., Ji M., Guan H., Studeman K., Jensen K., Vasko V., El-Naggar A.K., Xing M. Highly prevalent genetic alterations in receptor tyrosine kinases and phosphatidylinositol 3-kinase/akt and mitogen-activated protein kinase pathways in anaplastic and follicular thyroid cancers. J. Clin. Endocrinol. Metab. 2008, 93:3106-3116.
53. Lloyd R.V., Erickson L.A., Casey M.B., Lam K.Y., Lohse C.M., Asa S.L., Chan J.K., DeLellis R.A., Harach H.R., Kakudo K., LiVolsi V.A., Rosai J., Sebo T.J., Sobrinho-Simoes M., Wenig B.M., Lae M.E. Observer variation in the diagnosis of follicular variant of papillary thyroid carcinoma. Am. J. Surg. Pathol. 2004, 28:1336-1340.
54. Logani S., Gupta P.K., LiVolsi V.A., Mandel S., Baloch Z.W. Thyroid nodules with FNA cytology suspicious for follicular variant of papillary thyroid carcinoma: follow-up and management. Diagn. Cytopathol. 2000, 23:380-385.
55. Marques A.R., Espadinha C., Catarino A.L., Moniz S., Pereira T., Sobrinho L.G., Leite V. Expression of PAX8-PPAR gamma 1 rearrangements in both follicular thyroid carcinomas and adenomas. J. Clin. Endocrinol. Metab. 2002, 87:3947-3952.
56. Martelli M.L., Iuliano R., Le Pera I., Sama I., Monaco C., Cammarota S., Kroll T., Chiariotti L., Santoro M., Fusco A. Inhibitory effects of peroxisome poliferator-activated receptor gamma on thyroid carcinoma cell growth. J. Clin. Endocrinol. Metab. 2002, 87:4728-4735.
57. Martins L., Matsuo S.E., Ebina K.N., Kulcsar M.A., Friguglietti C.U., Kimura E.T. Galectin-3 messenger ribonucleic acid and protein are expressed in benign thyroid tumors. J. Clin. Endocrinol. Metab. 2002, 87:4806-4810.
58. Matsumoto F., Fujii H., Abe M., Kajino K., Kobayashi T., Matsumoto T., Ikeda K., Hino O. A novel tumor marker Niban, is expressed in subsets of thyroid tumors and Hashimoto's thyroiditis. Hum. Pathol. 2006, 37:1592-1600.
59. Mazzaferri E.L. Management of a solitary thyroid nodule. N. Engl. J. Med. 1993, 328:553-559.
60. Nakabashi C.C., Guimaraes G.S., Michaluart P., Ward L.S., Cerutti J.M., Maciel R.M. The expression of PAX8-PPARgamma rearrangements is not specific to follicular thyroid carcinoma. Clin. Endocrinol. (Oxf.) 2004, 61:280-282.
61. Nascimento M.C., Bisi H., Alves V.A., Longatto-Filho A., Kanamura C.T., Medeiros-Neto G. Differential reactivity for galectin-3 in Hurthle cell adenomas and carcinomas. Endocr. Pathol. 2001, 12:275-279.
62. Nayar R., Ivanovic M. The indeterminate thyroid fine-needle aspiration: experience from an academic center using terminology similar to that proposed in the 2007 National Cancer Institute Thyroid Fine Needle Aspiration State of the Science Conference. Cancer Cytopathol. 2009, 117:195-202.
63. Nikiforov Y.E., Steward D.L., Robinson-Smith T.M., Haugen B.R., Klopper J.P., Zhu Z., Fagin J.A., Falciglia M., Weber K., Nikiforova M.N. Molecular testing for mutations in improving the fine-needle aspiration diagnosis of thyroid nodules. J. Clin. Endocrinol. Metab. 2009, 94:2092-2098.
64. Nikiforova M.N., Biddinger P.W., Caudill C.M., Kroll T.G., Nikiforov Y.E. PAX8-PPARgamma rearrangement in thyroid tumors: RT-PCR and immunohistochemical analyses. Am. J. Surg. Pathol. 2002, 26:1016-1023.
65. Nikiforova M.N., Lynch R.A., Biddinger P.W., Alexander E.K., Dorn G.W., Tallini G., Kroll T.G., Nikiforov Y.E. RAS point mutations and PAX8-PPARgamma rearrangement in thyroid tumors: evidence for distinct molecular pathways in thyroid follicular carcinoma. J. Clin. Endocrinol. Metab. 2003, 88:2318-2326.
66. Nikiforova M.N., Tseng G.C., Steward D., Diorio D., Nikiforov Y.E. MicroRNA expression profiling of thyroid tumors: biological significance and diagnostic utility. J. Clin. Endocrinol. Metab. 2008, 93:1600-1608.
67. Oler G., Camacho C.P., Hojaij F.C., Michaluart P., Riggins G.J., Cerutti J.M. Gene expression profiling of papillary thyroid carcinoma identifies transcripts correlated with BRAF mutational status and lymph node metastasis. Clin. Cancer Res. 2008, 14:4735-4742.
68. Oler G., Cerutti J.M. High prevalence of BRAF mutation in a Brazilian cohort of patients with sporadic papillary thyroid carcinomas: correlation with more aggressive phenotype and decreased expression of iodide-metabolizing genes. Cancer 2009, 115:972-980.
69. Orlandi F., Saggiorato E., Pivano G., Puligheddu B., Termine A., Cappia S., De Giuli P., Angeli A. Galectin-3 is a presurgical marker of human thyroid carcinoma. Cancer Res. 1998, 58:3015-3020.
70. Pallante P., Visone R., Ferracin M., Ferraro A., Berlingieri M.T., Troncone G., Chiappetta G., Liu C.G., Santoro M., Negrini M., Croce C.M., Fusco A. MicroRNA deregulation in human thyroid papillary carcinomas. Endocr. Relat. Cancer 2006, 13:497-508.
71. Patel M.R., Bryson P.C., Shores C.G., Hart C.F., Thorne L.B., Deal A.M., Zanation A.M. Trefoil factor 3 immunohistochemical characterization of follicular thyroid lesions from tissue microarray. Arch. Otolaryngol. Head Neck Surg. 2009, 135:590-596.
72. Prasad M.L., Pellegata N.S., Huang Y., Nagaraja H.N., de la Chapelle A., Kloos R.T. Galectin-3, fibronectin-1, CITED-1, HBME1 and cytokeratin-19 immunohistochemistry is useful for the differential diagnosis of thyroid tumors. Mod. Pathol. 2005, 18:48-57.
73. Ricarte-Filho J.C., Ryder M., Chitale D.A., Rivera M., Heguy A., Ladanyi M., Janakiraman M., Solit D., Knauf J.A., Tuttle R.M., Ghossein R.A., Fagin J.A. Mutational profile of advanced primary and metastatic radioactive iodine-refractory thyroid cancers reveals distinct pathogenetic roles for BRAF, PIK3CA, and AKT1. Cancer Res. 2009, 69:4885-4893.
74. Rocha A.S., Marques R., Bento I., Soares R., Magalhaes J., de Castro I.V., Soares P. Thyroid hormone receptor beta mutations in the 'hot-spot region' are rare events in thyroid carcinomas. J. Endocrinol. 2007, 192:83-86.
75. Rowe L.R., Bentz B.G., Bentz J.S. Detection of BRAF V600E activating mutation in papillary thyroid carcinoma using PCR with allele-specific fluorescent probe melting curve analysis. J. Clin. Pathol. 2007, 60:1211-1215.
76. Saggiorato E., Cappia S., De Giuli P., Mussa A., Pancani G., Caraci P., Angeli A., Orlandi F. Galectin-3 as a presurgical immunocytodiagnostic marker of minimally invasive follicular thyroid carcinoma. J. Clin. Endocrinol. Metab. 2001, 86:5152-5158.
77. Saggiorato E., De Pompa R., Volante M., Cappia S., Arecco F., Dei Tos A.P., Orlandi F., Papotti M. Characterization of thyroid 'follicular neoplasms' in fine-needle aspiration cytological specimens using a panel of immunohistochemical markers: a proposal for clinical application. Endocr. Relat. Cancer 2005, 12:305-317.
78. Sahin M., Allard B.L., Yates M., Powell J.G., Wang X.L., Hay I.D., Zhao Y., Goellner J.R., Sebo T.J., Grebe S.K., Eberhardt N.L., McIver B. PPARgamma staining as a surrogate for PAX8/PPARgamma fusion oncogene expression in follicular neoplasms: clinicopathological correlation and histopathological diagnostic value. J. Clin. Endocrinol. Metab. 2005, 90:463-468.
79. Sanabria A., Carvalho A.L., Piana de Andrade V., Pablo Rodrigo J., Vartanian J.G., Rinaldo A., Ikeda M.K., Devaney K.O., Magrin J., Augusto Soares F., Ferlito A., Kowalski L.P. Is galectin-3 a good method for the detection of malignancy in patients with thyroid nodules and a cytologic diagnosis of " follicular neoplasm" ? A critical appraisal of the evidence. Head Neck 2007, 29:1046-1054.
80. Sapio M.R., Posca D., Raggioli A., Guerra A., Marotta V., Deandrea M., Motta M., Limone P.P., Troncone G., Caleo A., Rossi G., Fenzi G., Vitale M. Detection of RET/PTC, TRK and BRAF mutations in preoperative diagnosis of thyroid nodules with indeterminate cytological findings. Clin. Endocrinol. (Oxf.) 2007, 66:678-683.
81. Sebesta J., Brown T., Williard W., Dehart M.J., Aldous W., Kavolius J., Azarow K. Does telomerase activity add to the value of fine needle aspirations in evaluating thyroid nodules?. Am. J. Surg. 2001, 181:420-422.
82. Suzuki H., Willingham M.C., Cheng S.Y. Mice with a mutation in the thyroid hormone receptor beta gene spontaneously develop thyroid carcinoma: a mouse model of thyroid carcinogenesis. Thyroid 2002, 12:963-969.
83. Takano T., Amino N. Molecular-based diagnosis of thyroid carcinomas by detecting cancer-specific mRNAs. Rinsho Byori 2000, 48:149-154.
84. Takano T., Hasegawa Y., Matsuzuka F., Miyauchi A., Yoshida H., Higashiyama T., Kuma K., Amino N. Gene expression profiles in thyroid carcinomas. Br. J. Cancer 2000, 83:1495-1502.
85. Takano T., Miyauchi A., Matsuzuka F., Yoshida H., Kuma K., Amino N. Ubiquitous expression of galectin-3 mRNA in benign and malignant thyroid tumors. Cancer Lett. 2003, 199:69-73.
86. Takano T., Miyauchi A., Yoshida H., Kuma K., Amino N. High-throughput differential screening of mRNAs by serial analysis of gene expression: decreased expression of trefoil factor 3 mRNA in thyroid follicular carcinomas. Br. J. Cancer 2004, 90:1600-1605.
87. Takano T., Miyauchi A., Yoshida H., Kuma K., Amino N. Decreased relative expression level of trefoil factor 3 mRNA to galectin-3 mRNA distinguishes thyroid follicular carcinoma from adenoma. Cancer Lett. 2005, 219:91-96.
88. Takano T., Yamada H. Trefoil factor 3 (TFF3): a promising indicator for diagnosing thyroid follicular carcinoma. Endocr. J. 2009, 56:9-16.
89. Tan G.H., Gharib H. Thyroid incidentalomas: management approaches to nonpalpable nodules discovered incidentally on thyroid imaging. Ann. Intern. Med. 1997, 126:226-231.
90. Tetzlaff M.T., Liu A., Xu X., Master S.R., Baldwin D.A., Tobias J.W., Livolsi V.A., Baloch Z.W. Differential expression of miRNAs in papillary thyroid carcinoma compared to multinodular goiter using formalin fixed paraffin embedded tissues. Endocr. Pathol. 2007, 18:163-173.
91. Umbricht C.B., Conrad G.T., Clark D.P., Westra W.H., Smith D.C., Zahurak M., Saji M., Smallridge R.C., Goodman S., Zeiger M.A. Human telomerase reverse transcriptase gene expression and the surgical management of suspicious thyroid tumors. Clin. Cancer Res. 2004, 10:5762-5768.
92. Vasko V., Ferrand M., Di Cristofaro J., Carayon P., Henry J.F., de Micco C. Specific pattern of RAS oncogene mutations in follicular thyroid tumors. J. Clin. Endocrinol Metab. 2003, 88:2745-2752.
93. Velculescu V.E., Zhang L., Vogelstein B., Kinzler K.W. Serial analysis of gene expression. Science 1995, 270:484-487.
94. Visone R., Russo L., Pallante P., De Martino I., Ferraro A., Leone V., Borbone E., Petrocca F., Alder H., Croce C.M., Fusco A. MicroRNAs (miR)-221 and miR-222, both overexpressed in human thyroid papillary carcinomas, regulate p27Kip1 protein levels and cell cycle. Endocr. Relat. Cancer 2007, 14:791-798.
95. Weber F., Shen L., Aldred M.A., Morrison C.D., Frilling A., Saji M., Schuppert F., Broelsch C.E., Ringel M.D., Eng C. Genetic classification of benign and malignant thyroid follicular neoplasia based on a 3-gene combination. J. Clin. Endocrinol. Metab. 2005, 90:2512-2521.
96. Weber F., Teresi R.E., Broelsch C.E., Frilling A., Eng C. A limited set of human MicroRNA is deregulated in follicular thyroid carcinoma. J. Clin. Endocrinol. Metab. 2006, 91:3584-3591.
97. Wu G., Mambo E., Guo Z., Hu S., Huang X., Gollin S.M., Trink B., Ladenson P.W., Sidransky D., Xing M. Uncommon mutation, but common amplifications, of the PIK3CA gene in thyroid tumors. J. Clin. Endocrinol. Metab. 2005, 90:4688-4693.
98. Xing M., Clark D., Guan H., Ji M., Dackiw A., Carson K.A., Kim M., Tufaro A., Ladenson P., Zeiger M., Tufano R. BRAF mutation testing of thyroid fine-needle aspiration biopsy specimens for preoperative risk stratification in papillary thyroid cancer. J. Clin. Oncol. 2009, 27:2977-2982.
99. Xu X.C., el-Naggar A.K., Lotan R. Differential expression of galectin-1 and galectin-3 in thyroid tumors. Potential diagnostic implications. Am. J. Pathol. 1995, 147:815-822.
100. Yashima K., Vuitch F., Gazdar A.F., Fahey T.J. Telomerase activity in benign and malignant thyroid diseases. Surgery 1997, 122:1141-1145. [discussion 1145-6].
101. Yeh M.W., Demircan O., Ituarte P., Clark O.H. False-negative fine-needle aspiration cytology results delay treatment and adversely affect outcome in patients with thyroid carcinoma. Thyroid 2004, 14:207-215.
102. Ying H., Suzuki H., Furumoto H., Walker R., Meltzer P., Willingham M.C., Cheng S.Y. Alterations in genomic profiles during tumor progression in a mouse model of follicular thyroid carcinoma. Carcinogenesis 2003, 24:1467-1479.
103. Zhu Z., Gandhi M., Nikiforova M.N., Fischer A.H., Nikiforov Y.E. Molecular profile and clinical-pathologic features of the follicular variant of papillary thyroid carcinoma. An unusually high prevalence of ras mutations. Am. J. Clin. Pathol. 2003, 120:71-77.