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Horm Metab Res 2014; 46(03): 171-180
DOI: 10.1055/s-0033-1363264
Endocrine Research
© Georg Thieme Verlag KG Stuttgart · New York

miRNAs with the Potential to Distinguish Follicular Thyroid Carcinomas from Benign Follicular Thyroid Tumors: Results of a Meta-analysis

T. Stokowy
1   Institute of Automatic Control, Silesian University of Technology, Gliwice, Poland
2   Department of Nuclear Medicine and Endocrine Oncology, M. Sklodowska-Curie Memorial Cancer Center and Institute of Oncology, Gliwice, Poland
,
B. Wojtaś
2   Department of Nuclear Medicine and Endocrine Oncology, M. Sklodowska-Curie Memorial Cancer Center and Institute of Oncology, Gliwice, Poland
,
K. Fujarewicz
1   Institute of Automatic Control, Silesian University of Technology, Gliwice, Poland
,
B. Jarząb
2   Department of Nuclear Medicine and Endocrine Oncology, M. Sklodowska-Curie Memorial Cancer Center and Institute of Oncology, Gliwice, Poland
,
M. Eszlinger
3   Division of Endocrinology and Nephrology, University of Leipzig, Leipzig, Germany
,
R. Paschke
3   Division of Endocrinology and Nephrology, University of Leipzig, Leipzig, Germany
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Publikationsverlauf

received 02. Juli 2013

accepted after second revision 28. November 2013

Publikationsdatum:
20. Januar 2014 (online)

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Abstract

The detection of somatic mutations in indeterminate or follicular proliferation fine-needle aspiration cytologies (FNACs) is able to clarify only a subgroup of those FNACs. Therefore, further markers to differentiate this problematic FNAC category by the identification of mutation negative thyroid cancers and benign nodules are urgently needed. Our objective was to evaluate previously published miRNA markers and discover novel ones from all publicly available miRNA expression profiling data sets. By literature review and data repository search we gathered 3 data sets describing human miRNA expression profiles of follicular thyroid cancer (FTC) and follicular adenoma (FA) samples. Literature review summarized 27 previously published miRNAs, which were validated in the 3 available data sets. By means of uniform statistical analysis 6 further miRNAs were identified and tested in an independent, previously published microarray data set. Meta-analysis confirmed 7 out of 27 previously published, and 4 out of 6 de novo identified miRNAs. The low confirmation rate of previously published miRNA markers was induced by low numbers of samples in the analyzed studies and high false discovery rates that were higher than 0.2. Finally, miR-637, miR-181c-3p, miR-206, and miR-7-5p were discovered as de novo potential FTC markers and validated in at least one independent, previously published data set. Two out of these new identified miRNAs (miR-7-5p and miR-206) were validated by qPCR in an independent sample set of 32 FTC and 46 FA samples. Especially miR-7-5p was able to differentiate benign and malignant thyroid tumors in several datasets.

Key words

miRNA - follicular thyroid tumors - microarray - integrated statistical analysis
 

  • References

  • 1 Gharib H, Papini E, Paschke R, Duick DS, Valcavi R, Hegedüs L, Vitti P. American Association of Clinical Endocrinologists, Associazione Medici Endocrinologi, and European Thyroid Association Medical guidelines for clinical practice for the diagnosis and management of thyroid nodules: executive summary of recommendations. Endocr Pract 2010; 16: 468-475
    CrossrefPubMedSuche in Google Scholar
  • 2 Paschke R, Hegedüs L, Alexander E, Valcavi R, Papini E, Gharib H. Thyroid nodule guidelines: agreement, disagreement and need for future research. Nat Rev Endocrinol 2011; 7: 354-361
    CrossrefPubMedSuche in Google Scholar
  • 3 Cooper DS, Doherty GM, Haugen BR, Hauger BR, Kloos RT, Lee SL, Mandel SJ, Mazzaferri EL, McIver B, Pacini F, Schlumberger M, Sherman SI, Steward DL, Tuttle RM. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2009; 19: 1167-1214
    Suche in Google Scholar
  • 4 Baloch ZW, LiVolsi VA, Asa SL, Rosai J, Merino MJ, Randolph G, Vielh P, DeMay RM, Sidawy MK, Frable WJ. 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
    CrossrefPubMedSuche in Google Scholar
  • 5 Eszlinger M, Paschke R. Molecular fine-needle aspiration biopsy diagnosis of thyroid nodules by tumor specific mutations and gene expression patterns. Mol Cell Endocrinol 2010; 322: 29-37
    CrossrefPubMedSuche in Google Scholar
  • 6 Ferraz C, Eszlinger M, Paschke R. Current state and future perspective of molecular diagnosis of fine-needle aspiration biopsy of thyroid nodules. J Clin Endocrinol Metab 2011; 96: 2016-2026
    CrossrefPubMedSuche in Google Scholar
  • 7 Lodewijk L, Prins AM, Kist JW, Valk GD, Kranenburg O, IHMB Rinkes, Vriens MR. The value of miRNA in diagnosing thyroid cancer: A systematic review. Cancer Biomark 2012; 11: 229-238
    PubMedSuche in Google Scholar
  • 8 Rossing M. Classification of Follicular Cell-derived Thyroid Cancer by Global RNA Profiling. J Mol Endocrinol 2013; 50: R39-R51
    CrossrefPubMedSuche in Google Scholar
  • 9 Dettmer M, Vogetseder A, Durso MB, Moch H, Komminoth P, Perren A, Nikiforov YE, Nikiforova MN. MicroRNA expression array identifies novel diagnostic markers for conventional and oncocytic follicular thyroid carcinomas. J Clin Endocrinol Metab 2013; 98: E1-E7
    CrossrefPubMedSuche in Google Scholar
  • 10 Thomas L. Retrospective Power Analysis. Conservation Biology 1997; 11: 276-280
    CrossrefPubMedSuche in Google Scholar
  • 11 Eszlinger M, Krohn K, Hauptmann S, Dralle H, Giordano TJ, Paschke R. Perspectives for improved and more accurate classification of thyroid epithelial tumors. J Clin Endocrinol Metab 2008; 93: 3286-3294
    CrossrefPubMedSuche in Google Scholar
  • 12 Eszlinger M, Krohn K, Kukulska A, Jarzab B, Paschke R. Perspectives and limitations of microarray-based gene expression profiling of thyroid tumors. Endocr Rev 2007; 28: 322-338
    CrossrefPubMedSuche in Google Scholar
  • 13 Rossing M, Borup R, Henao R, Winther O, Vikesaa J, Niazi O, Godballe C, Krogdahl A, Glud M, Hjort-Sørensen C, Kiss K, Bennedbæk FN, Nielsen FC. Down-regulation of microRNAs controlling tumourigenic factors in follicular thyroid carcinoma. J Mol Endocrinol 2012; 48: 11-23
    CrossrefPubMedSuche in Google Scholar
  • 14 Reddi HV, Madde P, Milosevic D, Hackbarth JS, Algeciras-Schimnich A, McIver B, Grebe SKG, Eberhardt NL. The Putative PAX8/PPARg Fusion Oncoprotein Exhibits Partial Tumor Suppressor Activity through Up-Regulation of Micro-RNA-122 and Dominant-Negative PPARg Activity. Genes Cancer 2011; 2: 46-55
    CrossrefPubMedSuche in Google Scholar
  • 15 Lassalle S, Hofman V, Ilie M, Bonnetaud C, Puisségur M-P, Brest P, Loubatier C, Guevara N, Bordone O, Cardinaud B, Lebrigand K, Rios G, Santini J, Franc B, Mari B, Al Ghuzlan A, Vielh P, Barbry P, Hofman P. Can the microRNA signature distinguish between thyroid tumors of uncertain malignant potential and other well-differentiated tumors of the thyroid gland?. Endocr Relat Cancer 2011; 18: 579-594
    CrossrefPubMedSuche in Google Scholar
  • 16 Nikiforova MN, Tseng GC, Steward D, Diorio D, Nikiforov YE. MicroRNA expression profiling of thyroid tumors: biological significance and diagnostic utility. J Clin Endocrinol Metab 2008; 93: 1600-1608
    CrossrefPubMedSuche in Google Scholar
  • 17 Sheu S-Y, Grabellus F, Schwertheim S, Worm K, Broecker-Preuss M, Schmid KW. Differential miRNA expression profiles in variants of papillary thyroid carcinoma and encapsulated follicular thyroid tumours. Br J Cancer 2010; 102: 376-382
    CrossrefPubMedSuche in Google Scholar
  • 18 Weber F, Teresi RE, Broelsch CE, Frilling A, Eng C. A limited set of human MicroRNA is deregulated in follicular thyroid carcinoma. J Clin Endocrinol Metab 2006; 91: 3584-3591
    CrossrefPubMedSuche in Google Scholar
  • 19 Vriens MR, Weng J, Suh I, Huynh N, Guerrero MA, Shen WT, Duh Q-Y, Clark OH, Kebebew E. MicroRNA expression profiling is a potential diagnostic tool for thyroid cancer. Cancer 2012; 118: 3426-3432
    CrossrefPubMedSuche in Google Scholar
  • 20 Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JYH, Zhang J. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004; 5: R80
    CrossrefPubMedSuche in Google Scholar
  • 21 Kozomara A, Griffiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 2011; 39: D152-D157
    CrossrefPubMedSuche in Google Scholar
  • 22 Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ. miRBase: tools for microRNA genomics. Nucleic Acids Res 2008; 36: D154-D158
    CrossrefPubMedSuche in Google Scholar
  • 23 Stadler PF, Chen JJ-L, Hackermüller J, Hoffmann S, Horn F, Khaitovich P, Kretzschmar AK, Mosig A, Prohaska SJ, Qi X, Schutt K, Ullmann K. Evolution of vault RNAs. Mol Biol Evol 2009; 26: 1975-1991
    CrossrefPubMedSuche in Google Scholar
  • 24 Jazdzewski K, Liyanarachchi S, Swierniak M, Pachucki J, Ringel MD, Jarzab B, de la Chapelle A. Polymorphic mature microRNAs from passenger strand of pre-miR-146a contribute to thyroid cancer. Proc Natl Acad Sci USA 2009; 106: 1502-1505
    CrossrefPubMedSuche in Google Scholar
  • 25 De la Chapelle A, Jazdzewski K. MicroRNAs in thyroid cancer. J Clin Endocrinol Metab 2011; 96: 3326-3336
    CrossrefPubMedSuche in Google Scholar
  • 26 Visser WE, Heemstra KA, Swagemakers SMA, Ozgür Z, Corssmit EP, Burggraaf J, van Ijcken WFJ, van der Spek PJ, Smit JWA, Visser TJ. Physiological thyroid hormone levels regulate numerous skeletal muscle transcripts. J Clin Endocrinol Metab 2009; 94: 3487-3496
    CrossrefPubMedSuche in Google Scholar
  • 27 Di Leva G, Gasparini P, Piovan C, Ngankeu A, Garofalo M, Taccioli C, Iorio MV, Li M, Volinia S, Alder H, Nakamura T, Nuovo G, Liu Y, Nephew KP, Croce CM. MicroRNA cluster 221-222 and estrogen receptor alpha interactions in breast cancer. J Natl Cancer Inst 2010; 102: 706-721
    CrossrefPubMedSuche in Google Scholar
  • 28 Kitano M, Rahbari R, Patterson EE, Xiong Y, Prasad NB, Wang Y, Zeiger MA, Kebebew E. Expression profiling of difficult-to-diagnose thyroid histologic subtypes shows distinct expression profiles and identify candidate diagnostic microRNAs. Ann Surg Oncol 2011; 18: 3443-3452
    CrossrefPubMedSuche in Google Scholar
  • 29 Zhao X, Dou W, He L, Liang S, Tie J, Liu C, Li T, Lu Y, Mo P, Shi Y, Wu K, Nie Y, Fan D. MicroRNA-7 functions as an anti-metastatic microRNA in gastric cancer by targeting insulin-like growth factor-1 receptor. Oncogene 2013; 32: 1363-1372
    CrossrefPubMedSuche in Google Scholar
  • 30 Renwick N, Cekan P, Masry PA, McGeary SE, Miller JB, Hafner M, Li Z, Mihailovic A, Morozov P, Brown M, Gogakos T, Mobin MB, Snorrason EL, Feilotter HE, Zhang X, Perlis CS, Wu H, Suárez-Fariñas M, Feng H, Shuda M, Moore PS, Tron VA, Chang Y, Tuschl T. Multicolor microRNA FISH effectively differentiates tumor types. J Clin Invest 2013; 123: 2694-2702
    CrossrefPubMedSuche in Google Scholar
  • 31 Santarpia L, Calin GA, Adam L, Ye L, Fusco A, Giunti S, Thaller C, Paladini L, Zhang X, Jimenez C, Trimarchi F, El-Naggar AK, Gagel RF. A miRNA signature associated with human metastatic medullary thyroid carcinoma. Endocr Relat Cancer 2013; 20: 809-823
    CrossrefPubMedSuche in Google Scholar