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MicroRNAs and Lymph Node Metastasis in Papillary Thyroid Cancers

  • Mutalib, Nurul-Syakima Ab (UKM Medical Molecular Biology Institute (UMBI)) ;
  • Yusof, Azliana Mohamad (UKM Medical Molecular Biology Institute (UMBI)) ;
  • Mokhtar, Norfilza Mohd (Department of Physiology, Faculty of Medicine, Universiti Kebangsaan Malaysia) ;
  • Harun, Roslan (KPJ Ampang Puteri Specialist Hospital) ;
  • Muhammad, Rohaizak (Department of Surgery, Faculty of Medicine, Universiti Kebangsaan Malaysia) ;
  • Jamal, Rahman (UKM Medical Molecular Biology Institute (UMBI))
  • Published : 2016.02.05

Abstract

Lymph node metastasis (LNM) in papillary thyroid cancer (PTC) has been shown to be associated with increased risk of locoregional recurrence, poor prognosis and decreased survival, especially in older patients. Hence, there is a need for a reliable biomarker for the prediction of LNM in this cancer. MicroRNAs (miRNAs) are small noncoding RNAs that regulate gene translation or degradation and play key roles in numerous cellular functions including cell-cycle regulation, differentiation, apoptosis, invasion and migration. Various studies have demonstrated deregulation of miRNA levels in many diseases including cancers. While a large number of miRNAs have been identified from PTCs using various means, association of miRNAs with LNM in such cases is still controversial. Furthermore, studies linking most of the identified miRNAs to the mechanism of LNM have not been well documented. The aim of this review is to update readers on the current knowledge of miRNAs in relation to LNM in PTC.

Keywords

microRNAs;papillary thyroid cancer;lymph node;metastasis;biomarker

Acknowledgement

Supported by : Fundamental Research Grant Scheme (FRGS)

References

  1. Acibucu F, Dokmetas HS, Tutar Y, et al (2014). Correlations between the expression levels of micro-RNA146b, 221, 222 and p27Kip1 protein mRNA and the clinicopathologic parameters in papillary thyroid cancers. Exp Clin Endocrinol Diabetes, 122, 137-43. https://doi.org/10.1055/s-0034-1367025
  2. Akao Y, Nakagawa Y, Naoe T (2006). Let-7 microRNA functions as a potential growth suppressor in human colon cancer cells. Biol Pharm Bull, 29, 903-6. https://doi.org/10.1248/bpb.29.903
  3. Altuvia Y, Landgraf P, Lithwick G, et al (2005). Clustering and conservation patterns of human microRNAs. Nucleic Acids Res, 33, 2697-706. https://doi.org/10.1093/nar/gki567
  4. Bandres E, Bitarte N, Arias F, et al (2009). MicroRNA-451 regulates macrophage migration inhibitory factor production and proliferation of gastrointestinal cancer cells. Clin Cancer Res, 15, 2281-90. https://doi.org/10.1158/1078-0432.CCR-08-1818
  5. Bartel DP (2009). MicroRNAs: target recognition and regulatory functions. Cell, 136, 215-233. https://doi.org/10.1016/j.cell.2009.01.002
  6. Bergamaschi A, Katzenellenbogen BS (2012). Tamoxifen downregulation of miR-451 increases 14-3-3zeta and promotes breast cancer cell survival and endocrine resistance. Oncogene, 31, 39-47. https://doi.org/10.1038/onc.2011.223
  7. Bonci D, Coppola V, Musumeci M, et al (2008). The miR-15a-miR-16-1 cluster controls prostate cancer by targeting multiple oncogenic activities. Nat Med, 14, 1271-7. https://doi.org/10.1038/nm.1880
  8. Boyerinas B, Park SM, Hau A, et al (2010). The role of let-7 in cell differentiation and cancer. Endocr Relat Cancer, 17, 19-36.
  9. Braun J, Huttelmaier S (2011). Pathogenic mechanisms of deregulated microRNA expression in thyroid carcinomas of follicular origin. Thyroid Res, 4, 1. https://doi.org/10.1186/1756-6614-4-1
  10. Cahill S, Smyth P, Finn SP, et al (2006). Effect of ret/PTC 1 rearrangement on transcription and post-transcriptional regulation in a papillary thyroid carcinoma model. Mol Cancer, 11, 70.
  11. Calin GA, Sevignani C, Dumitru CD, et al (2004). Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci U S A, 101, 2999-3004. https://doi.org/10.1073/pnas.0307323101
  12. Cancer Genome Atlas Research Network (2014). Integrated genomic characterization of papillary thyroid carcinoma. Cell, 159, 676-90. https://doi.org/10.1016/j.cell.2014.09.050
  13. Cantile M, Scognamiglio G, La Sala L, et al (2013). Aberrant expression of posterior HOX genes in well differentiated histotypes of thyroid cancers. Int J Mol Sci, 14, 21727-40. https://doi.org/10.3390/ijms141121727
  14. Chang TC, Wentzel EA, Kent OA, et al (2007). Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell, 26, 745-52. https://doi.org/10.1016/j.molcel.2007.05.010
  15. Chen D, Huang J, Zhang K, et al (2014). MicroRNA-451 induces epithelial-mesenchymal transition in docetaxel-resistant lung adenocarcinoma cells by targeting proto-oncogene c-Myc. Eur J Cancer, 50, 3050-67. https://doi.org/10.1016/j.ejca.2014.09.008
  16. Chen X, Zhao G, Wang F, et al (2014). Upregulation of miR-513b inhibits cell proliferation, migration, and promotes apoptosis by targeting high mobility group-box 3 protein in gastric cancer. Tumour Biol, 35, 11081-9. https://doi.org/10.1007/s13277-014-2405-z
  17. Chen YT, Kitabayashi N, Zhou XK, et al (2008). MicroRNA analysis as a potential diagnostic tool for papillary thyroid carcinoma. Mod Pathol, 21, 1139-46. https://doi.org/10.1038/modpathol.2008.105
  18. Chou CK, Chen RF, Chou FF, et al (2010). miR-146b is highly expressed in adult papillary thyroid carcinomas with high risk features including extrathyroidal invasion and the BRAF(V600E) mutation. Thyroid, 20, 489-94. https://doi.org/10.1089/thy.2009.0027
  19. Chou CK, Yang KD, Chou FF, et al (2013). Prognostic implications of miR-146b expression and its functional role in papillary thyroid carcinoma. J Clin Endocrinol Metab, 98, 196-205. https://doi.org/10.1210/jc.2012-2666
  20. Cognetti OM, Pribitkin EA, Keane WB (2008). Management of the neck in differentiated thyroid cancer. Surg Oneal Clin N Am, 17, 157-73. https://doi.org/10.1016/j.soc.2007.10.002
  21. Corney DC, Flesken-Nikitin A, Godwin AK, et al (2007). MicroRNA-34b and MicroRNA-34c are targets of p53 and cooperate in control of cell proliferation and adhesionindependent growth. Cancer Res, 67, 8433-8. https://doi.org/10.1158/0008-5472.CAN-07-1585
  22. de la Chapelle A, Jazdzewski K (2011). MicroRNAs in thyroid cancer. J Clin Endocrinol Metab, 96, 3326-36. https://doi.org/10.1210/jc.2011-1004
  23. Deng X, Wu B, Xiao K, et al (2015). MiR-146b-5p promotes metastasis and induces epithelial-mesenchymal transition in thyroid cancer by targeting ZNRF3. Cell Physiol Biochem, 35, 71-82. https://doi.org/10.1159/000369676
  24. Dettmer M, Vogetseder A, Durso MB, et al (2013). MicroRNA expression array identifies novel diagnostic markers for conventional and oncocytic follicular thyroid carcinomas. J Clin Endocrinol Metab, 98, 1-7. https://doi.org/10.1210/jc.2011-2306
  25. Ding J, Huang S, Wu S, et al (2010). Gain of miR-151 on chromosome 8q24.3 facilitates tumour cell migration and spreading through downregulating RhoGDIA. Nat Cell Biol, 12, 390-9. https://doi.org/10.1038/ncb2039
  26. Fassina A, Cappellesso R, Simonato F, et al (2014). A 4-MicroRNA signature can discriminate primary lymphomas from anaplastic carcinomas in thyroid cytology smears. Cancer Cytopathol, 122, 274-81. https://doi.org/10.1002/cncy.21383
  27. Felekkis K, Touvana E, Stefanou Ch, et al (2010). microRNAs: a newly described class of encoded molecules that play a role in health and disease. Hippokratia, 14, 236-40.
  28. Flamant S, Ritchie W, Guilhot J, et al (2010). Micro-RNA response to imatinib mesylate in patients with chronic myeloid leukemia. Haematologica, 95, 1325-33. https://doi.org/10.3324/haematol.2009.020636
  29. Gal H, Pandi G, Kanner AA, et al (2008). miR-451 and Imatinib mesylate inhibit tumor growth of Glioblastoma stem cells. Biochem Biophys Res Commun, 376, 86-90. https://doi.org/10.1016/j.bbrc.2008.08.107
  30. Gao J, Liu QG (2012). The role of miR-26 in tumors and normal tissues (Review). Oncol Lett, 6, 1019-23.
  31. Gao Y, Wang C, Shan Z, et al (2010). miRNA expression in a human papillary thyroid carcinoma cell line varies with invasiveness. Endocr J, 57, 81-6. https://doi.org/10.1507/endocrj.K09E-220
  32. Gehring WJ, Hiromi Y (1986). Homeotic genes and the homeobox. Annu Rev Genet, 20, 147-73. https://doi.org/10.1146/annurev.ge.20.120186.001051
  33. Geraldo MV, Yamashita AS, Kimura ET (2012). MicroRNA miR-146b-5p regulates signal transduction of TGF-${\beta}$ by repressing SMAD4 in thyroid cancer. Oncogene, 31, 1910-22. https://doi.org/10.1038/onc.2011.381
  34. Guerrero MA, Clark OH (2011). Controversies in the Management of Papillary Thyroid Cancer Revisited. ISRN Oncol, 2011, 303128,
  35. Hao HX, Xie Y, Zhang Y, et al (2012). ZNRF3 promotes Wnt receptor turnover in an R-spondin-sensitive manner. Nature, 485, 195-200. https://doi.org/10.1038/nature11019
  36. He H, Jazdzewski K, Li W, et al (2005). The role of microRNA genes in papillary thyroid carcinoma. Proc Natl Acad Sci U S A, 102, 19075-80. https://doi.org/10.1073/pnas.0509603102
  37. He L, He X, Lim LP, et al (2007). A microRNA component of the p53 tumour suppressor network. Nature, 447, 1130-4. https://doi.org/10.1038/nature05939
  38. Hotomi M, Sugitani I, Toda K, et al (2012). A novel definition of extrathyroidal invasion for patients with papillary thyroid carcinoma for predicting prognosis. World J Surg, 36, 1231-40. https://doi.org/10.1007/s00268-012-1518-z
  39. Hsieh SH, Chen ST, Hsueh C, et al (2012). Gender-specific variation in the prognosis of papillary thyroid cancer TNM stages II to IV. Int J Endocrinol, 2012, 379097.
  40. Huang KH, Lan YT, Fang WL, et al (2015). The correlation between miRNA and lymph node metastasis in gastric cancer. Biomed Res Int, 2015, 543163.
  41. Iorio MV, Croce CM (2012). MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review. EMBO Mol Med, 4, 143-59. https://doi.org/10.1002/emmm.201100209
  42. Ito Y, Kudo T, Kobayashi K, et al (2012). Prognostic factors for recurrence of papillary thyroid carcinoma in the lymph nodes, lung, and bone: analysis of 5,768 patients with average 10-year follow-up. World J Surg, 36, 1274-8. https://doi.org/10.1007/s00268-012-1423-5
  43. Jonklaas J, Nogueras-Gonzalez G, Munsell M, et al (2012). The impact of age and gender on papillary thyroid cancer survival. J Clin Endocrinol Metab, 97, 878-87. https://doi.org/10.1210/jc.2011-2864
  44. Ju X, Li D, Shi Q, et al (2009). Differential microRNA expression in childhood B-cell precursor acute lymphoblastic leukemia. Pediatr Hematol Oncol, 26, 1-10. https://doi.org/10.1080/08880010802378338
  45. Kim HJ, Kim YH, Lee DS, et al (2008). In vivo imaging of functional targeting of miR-221 in papillary thyroid carcinoma. J Nucl Med, 49, 1686-93. https://doi.org/10.2967/jnumed.108.052894
  46. Kozomara A, Griffiths-Jones S (2014). miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res, 42, 68-73.
  47. Kramer JA, Schmid KW, Dralle H, et al (2010). Primary tumour size is a prognostic parameter in patients suffering from differentiated thyroid carcinoma with extrathyroidal growth: results of the MSDS trial. Eur J Endocrinol, 163, 637-44. https://doi.org/10.1530/EJE-10-0116
  48. Krell J, Frampton AE, Jacob J, et al (2012). The clinicopathologic role of microRNAs miR-9 and miR-151-5p in breast cancer metastasis. Mol Diagn Ther, 16, 167-72. https://doi.org/10.1007/BF03262205
  49. Kriegel AJ, Liu Y, Fang Y, et al (2012). The miR-29 family: genomics, cell biology, and relevance to renal and cardiovascular injury. Physiol Genomics, 44, 237-44. https://doi.org/10.1152/physiolgenomics.00141.2011
  50. Lagos-Quintana M, Rauhut R, Lendeckel W, et al (2001). Identification of novel genes coding for small expressed RNAs. Science, 294, 853-58. https://doi.org/10.1126/science.1064921
  51. Lee DY, Jeyapalan Z, Fang L, et al (2010). Expression of versican 3'-untranslated region modulates endogenous microRNA functions. PLoS One, 5, 13599. https://doi.org/10.1371/journal.pone.0013599
  52. Lee J, Song Y, Soh EY (2014). Central lymph node metastasis is an important prognostic factor in patients with papillary thyroid microcarcinoma. J Korean Med Sci, 29, 48-52. https://doi.org/10.3346/jkms.2014.29.1.48
  53. Lee JC, Zhao JT, Clifton-Bligh RJ, et al (2013). MicroRNA-222 and microRNA-146b are tissue and circulating biomarkers of recurrent papillary thyroid cancer. Cancer, 119, 4358-65. https://doi.org/10.1002/cncr.28254
  54. Leonardi GC, Candido S, Carbone M, et al (2012). microRNAs and thyroid cancer: biological and clinical significance (Review). Int J Mol Med, 30, 991-9. https://doi.org/10.3892/ijmm.2012.1089
  55. Li H, Xie H, Liu W, et al (2009). A novel microRNA targeting HDAC5 regulates osteoblast differentiation in mice and contributes to primary osteoporosis in humans. J Clin Invest, 119, 3666-77. https://doi.org/10.1172/JCI39832
  56. Li X, Abdel-Mageed AB, Mondal D, et al (2013). MicroRNA expression profiles in differentiated thyroid cancer, a review. Int J Clin Exp Med, 6, 74-80.
  57. Liu X, Sempere LF, Ouyang H, et al (2010). MicroRNA-31 functions as an oncogenic microRNA in mouse and human lung cancer cells by repressing specific tumor suppressors. J Clin Invest, 120, 1298-309. https://doi.org/10.1172/JCI39566
  58. Lodewijk L, Prins AM, Kist JW, et al (2012). The value of miRNA in diagnosing thyroid cancer: a systematic review. Cancer Biomark, 11, 229-38. https://doi.org/10.3233/CBM-2012-0273
  59. Lundgren CI, Hall P, Dickman PW, et al (2006). Clinically significant prognostic factors for differentiated thyroid carcinoma: a population-based, nested case-control study. Cancer, 106, 524-31. https://doi.org/10.1002/cncr.21653
  60. Lv M, Zhang X, Li M, et al (2013). miR-26a and its target CKS2 modulate cell growth and tumorigenesis of papillary thyroid carcinoma. PLoS One, 8, 67591. https://doi.org/10.1371/journal.pone.0067591
  61. Ma Y, Qin H, Cui Y (2013). MiR-34a targets GAS1 to promote cell proliferation and inhibit apoptosis in papillary thyroid carcinoma via PI3K/Akt/Bad pathway. Biochem Biophys Res Commun, 441, 958-63. https://doi.org/10.1016/j.bbrc.2013.11.010
  62. Machens A, Hinze R, Thomusch O, et al (2002). Pattern of nodal metastasis for primary and reoperative thyroid cancer. World J Surg, 26, 22-8. https://doi.org/10.1007/s00268-001-0176-3
  63. Mackiewicz M, Huppi K, Pitt JJ, et al (2011). Identification of the receptor tyrosine kinase AXL in breast cancer as a target for the human miR-34a microRNA. Breast Cancer Res Treat, 130, 663-79. https://doi.org/10.1007/s10549-011-1690-0
  64. Mardente S, Mari E, Consorti F, et al (2012). HMGB1 induces the overexpression of miR-222 and miR-221 and increases growth and motility in papillary thyroid cancer cells. Oncol Rep, 28, 2285-9. https://doi.org/10.3892/or.2012.2058
  65. Mardente S, Zicari A, Consorti F, et al (2010). Cross-talk between NO and HMGB1 in lymphocytic thyroiditis and papillary thyroid cancer. Oncol Rep, 24, 1455-61.
  66. Marini F, Luzi E, Brandi ML (2011). MicroRNA Role in Thyroid Cancer Development. J Thyroid Res, 2011, 407123.
  67. Mattick JS (2001). Non-coding RNAs: the architects of eukaryotic complexity. EMBO Rep, 2, 986-91. https://doi.org/10.1093/embo-reports/kve230
  68. McConahey WM, Hay ID, Woolner LB, et al (1986). Papillary thyroid cancer treated at the mayo clinic, 1946 through 1970: initial manifestations, pathologic findings, therapy, and outcome. Mayo Clin Proc, 61, 978-96. https://doi.org/10.1016/S0025-6196(12)62641-X
  69. Migliore C, Petrelli A, Ghiso E, et al (2008). MicroRNAs impair MET-mediated invasive growth. Cancer Res, 68, 10128-36. https://doi.org/10.1158/0008-5472.CAN-08-2148
  70. Misso G, Di Martino MT, De Rosa G, et al (2014). miR-34: a new weapon against cancer? Mol Ther Nucleic Acids, 3, 194. https://doi.org/10.1038/mtna.2014.46
  71. Mitomo S, Maesawa C, Ogasawara S, et al (2008). Downregulation of miR-138 is associated with overexpression of human telomerase reverse transcriptase protein in human anaplastic thyroid carcinoma cell lines. Cancer Sci, 99, 280-6. https://doi.org/10.1111/j.1349-7006.2007.00666.x
  72. Moo TA, Fahey TJ 3rd (2011). Lymph node dissection in papillary thyroid carcinoma. Semin Nucl Med, 41, 84-8. https://doi.org/10.1053/j.semnuclmed.2010.10.003
  73. Nam S, Li M, Choi K, et al (2009). MicroRNA and mRNA integrated analysis (MMIA): a web tool for examining biological functions of microRNA expression. Nucleic Acids Res, 37, 356-62. https://doi.org/10.1093/nar/gkp294
  74. Nikiforov YE (2011). Molecular analysis of thyroid tumors. Mod Pathol, 24, 34-43. https://doi.org/10.1038/modpathol.2010.167
  75. Nikiforov YE, Nikiforova MN (2011). Molecular genetics and diagnosis of thyroid cancer. Nat Rev Endocrinol, 7, 569-80. https://doi.org/10.1038/nrendo.2011.142
  76. Nikiforova MN, Tseng GC, Steward D, et al (2008). MicroRNA expression profiling of thyroid tumors: biological significance and diagnostic utility. J Clin Endocrinol Metab, 93, 1600-8. https://doi.org/10.1210/jc.2007-2696
  77. Nymark P, Guled M, Borze I, et al (2011). Integrative analysis of microRNA, mRNA and aCGH data reveals asbestosand histology-related changes in lung cancer. Genes Chromosomes Cancer, 50, 585-97. https://doi.org/10.1002/gcc.20880
  78. Ozata DM, Caramuta S, Velazquez-Fernandez D, et al (2011). The role of microRNA deregulation in the pathogenesis of adrenocortical carcinoma. Endocr Relat Cancer, 27, 643-55.
  79. Pallante P, Battista S, Pierantoni GM, et al (2014). Deregulation of microRNA expression in thyroid neoplasias. Nat Rev Endocrinol, 10, 88-101. https://doi.org/10.1038/nrendo.2013.223
  80. Pallante P, Visone R, Croce CM, et al (2010). Deregulation of microRNA expression in follicular-cell-derived human thyroid carcinomas. Endocr Relat Cancer, 17, 91-104.
  81. Pallante P, Visone R, Ferracin M, et al (2006). MicroRNA deregulation in human thyroid papillary carcinomas. Endocr Relat Cancer, 13, 497-508. https://doi.org/10.1677/erc.1.01209
  82. Pasquinelli AE, Reinhart BJ, Slack F, et al (2000). Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature, 408, 86-9. https://doi.org/10.1038/35040556
  83. Peng Y, Li C, Luo DC, et al (2014). Expression profile and clinical significance of microRNAs in papillary thyroid carcinoma. Molecules, 19, 11586-99. https://doi.org/10.3390/molecules190811586
  84. Pikarsky E, Porat RM, Stein I, et al (2004). NF-${\kappa}B$ funtions as a tumor promoter in inflammation-associated cancer. Nature, 431, 261-66. https://doi.org/10.1038/431261a
  85. Qu N, Zhang L, Ji QH, et al (2014). Number of tumor foci predicts prognosis in papillary thyroid cancer. BMC Cancer, 4, 914.
  86. Ricarte-Filho JC, Fuziwara CS, Yamashita AS, et al (2009). Effects of let-7 microRNA on cell growth and differentiation of papillary thyroid cancer. Transl Oncol, 2, 236-41. https://doi.org/10.1593/tlo.09151
  87. Rokah OH, Granot G, Ovcharenko A, et al (2012). Downregulation of miR-31, miR-155, and miR-564 in chronic myeloid leukemia cells. PLoS One, 7, 35501. https://doi.org/10.1371/journal.pone.0035501
  88. Rossing M, Borup R, Henao R, et al (2012). Down-regulation of microRNAs controlling tumourigenic factors in follicular thyroid carcinoma. J Mol Endocrinol, 48, 11-23. https://doi.org/10.1530/JME-11-0039
  89. Samimi H, Zaki Dizaji M, Ghadami M, et al (2013). MicroRNAs networks in thyroid cancers: focus on miRNAs related to the fascin. J Diabetes Metab Disord, 12, 31. https://doi.org/10.1186/2251-6581-12-31
  90. Scheumann GF, Gimm O, Wegener G, et al (1994). Prognostic significance and surgical management of locoregional lymph node metastases in papillary thyroid cancer. World J Surg, 18, 559-67. https://doi.org/10.1007/BF00353765
  91. Shaha AR, Shah JP, Loree TR (1996). Patterns of nodal and distant metastasis based on histologic varieties in differentiated carcinoma of the thyroid. Am J Surg, 172, 692-4. https://doi.org/10.1016/S0002-9610(96)00310-8
  92. Wada N, Duh QY, Sugino K, et al (2003). Lymph node metastasis from 259 papillary thyroid microcarcinomas: frequency, pattern of occurrence and recurrence, and optimal strategy for neck dissection. Ann Surg, 237, 399-407.
  93. Shen S, Yue H, Li Y, et al (2014). Upregulation of miR-136 in human non-small cell lung cancer cells promotes Erk1/2 activation by targeting PPP2R2A. Tumour Biol, 35, 631-40. https://doi.org/10.1007/s13277-013-1087-2
  94. Sheu SY, Grabellus F, Schwertheim S, et al (2010). Differential miRNA expression profiles in variants of papillary thyroid carcinoma and encapsulated follicular thyroid tumours. Br J Cancer, 102, 376-82. https://doi.org/10.1038/sj.bjc.6605493
  95. Slaby O, Svoboda M, Fabian P, et al (2007). Altered expression of miR-21, miR-31, miR-143 and miR-145 is related to clinicopathologic features of colorectal cancer. Oncol, 72, 397-402. https://doi.org/10.1159/000113489
  96. Stein S, Fritsch R, Lemaire L, et al (1996). Checklist: vertebrate homeobox genes. Mech Dev, 55, 91-108. https://doi.org/10.1016/0925-4773(95)00494-7
  97. Sun Y, Yu S, Liu Y, et al (2013). Expression of miRNAs in papillary thyroid carcinomas is associated with BRAF mutation and clinicopathological features in Chinese patients. Int J Endocrinol, 2013, 128735.
  98. Sun Z, Zhang Y, Zhang R, et al (2013). Functional divergence of the rapidly evolving miR-513 subfamily in primates. BMC Evol Biol, 13, 255. https://doi.org/10.1186/1471-2148-13-255
  99. Takahashi Y, Hamada J, Murakawa K, et al (2004). Expression profiles of 39 HOX genes in normal human adult organs and anaplastic thyroid cancer cell lines by quantitative real-time RT-PCR system. Exp Cell Res, 293, 144-53. https://doi.org/10.1016/j.yexcr.2003.09.024
  100. Tetzlaff MT, Liu A, Xu X, et al (2007). Differential expression of miRNAs in papillary thyroid carcinoma compared to multinodular goiter using formalin fixed paraffin embedded tissues. Endocr Pathol, 18, 163-73. https://doi.org/10.1007/s12022-007-0023-7
  101. Vigneri R, Malandrino P, Vigneri P (2015). The changing epidemiology of thyroid cancer: why is incidence increasing? Curr Opin Oncol, 27, 1-7. https://doi.org/10.1097/CCO.0000000000000148
  102. Visone R, Pallante P, Vecchione A, et al (2007). Specific microRNAs are downregulated in human thyroid anaplastic carcinomas. Oncogene, 26, 7590-5. https://doi.org/10.1038/sj.onc.1210564
  103. Visone R, Russo L, Pallante P, et al (2007). MicroRNAs (miR)-221 and miR-222, both overexpressed in human thyroid papillary carcinomas, regulate p27Kip1 protein levels and cell cycle. Endocr Relat Cancer, 14, 791-8. https://doi.org/10.1677/ERC-07-0129
  104. Vriens MR, Weng J, Suh I, et al (2012). Microrna expression profiling is a potential diagnostic tool for thyroid cancer. Cancer, 118, 3426-32. https://doi.org/10.1002/cncr.26587
  105. Wang C, Song B, Song W, et al (2011). Underexpressed microRNA-199b-5p targets Hypoxia-Inducible Factor-$1{\alpha}$ in hepatocellular carcinoma and predicts prognosis of hepatocellular carcinoma patients. J Gastroenterol Hepatol, 26, 1630-7. https://doi.org/10.1111/j.1440-1746.2011.06758.x
  106. Wang R, Wang ZX, Yang JS, et al (2011). MicroRNA-451 functions as a tumor suppressor in human non-small cell lung cancer by targeting ras-related protein 14 (RAB14). Oncogene, 30, 2644-58. https://doi.org/10.1038/onc.2010.642
  107. Wang W, Li T, Han G, et al (2013). Expression and Role of miR-34a in bladder cancer. Indian J Biochem Biophys, 50, 87-92.
  108. Wang Z, Zhang H, He L, et al (2013). Association between the expression of four upregulated miRNAs and extrathyroidal invasion in papillary thyroid carcinoma. Onco Targets Ther, 6, 281-7.
  109. Wang Z, Zhang H, Zhang P, et al (2013). Upregulation of miR-2861 and miR-451 expression in papillary thyroid carcinoma with lymph node metastasis. Med Oncol, 30, 577. https://doi.org/10.1007/s12032-013-0577-9
  110. Wojtas B, Ferraz C, Stokowy T, et al (2014). Differential miRNA expression defines migration and reduced apoptosis in follicular thyroid carcinomas. Mol Cell Endocrinol, 388, 1-9. https://doi.org/10.1016/j.mce.2014.02.011
  111. Xing M (2013). Molecular pathogenesis and mechanisms of thyroid cancer. Nat Rev Cancer, 13, 184-99. https://doi.org/10.1038/nrc3431
  112. Xing M, Alzahrani AS, Carson KA, et al (2013). Association between BRAF V600E mutation and mortality in patients with papillary thyroid cancer. JAMA, 309, 1493-501. https://doi.org/10.1001/jama.2013.3190
  113. Yan LX, Huang XF, Shao Q, et al (2008). MicroRNA miR-21 overexpression in human breast cancer is associated with advanced clinical stage, lymph node metastasis and patient poor prognosis. RNA, 14, 2348-60. https://doi.org/10.1261/rna.1034808
  114. Yang JS, Maurin T, Robine N, et al (2010). Conserved vertebrate miR-451 provides a platform for Dicer-independent, Ago2-mediated microRNA biogenesis. Proc Natl Acad Sci U S A, 107, 15163-8. https://doi.org/10.1073/pnas.1006432107
  115. Yang Z, Yuan Z, Fan Y, et al (2013). Integrated analyses of microRNA and mRNA expression profiles in aggressive papillary thyroid carcinoma. Mol Med Rep, 8, 1353-8. https://doi.org/10.3892/mmr.2013.1699
  116. Yip L, Kelly L, Shuai Y, et al (2011). MicroRNA signature distinguishes the degree of aggressiveness of papillary thyroid carcinoma. Ann Surg Oncol, 18, 2035-41. https://doi.org/10.1245/s10434-011-1733-0
  117. Yu F, Yao H, Zhu P, et al (2007). let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell, 131, 1109-23. https://doi.org/10.1016/j.cell.2007.10.054
  118. Yu J, Wang F, Yang GH, et al (2006). Human microRNA clusters: genomic organization and expression profile in leukemia cell lines. Biochem Biophys Res Commun, 349, 59-68. https://doi.org/10.1016/j.bbrc.2006.07.207
  119. Yu S, Liu Y, Wang J, et al (2012). Circulating microRNA profiles as potential biomarkers for diagnosis of papillary thyroid carcinoma. J Clin Endocrinol Metab, 97, 2084-92. https://doi.org/10.1210/jc.2011-3059
  120. Yuan ZM, Yang ZL, Zheng Q (2014). Deregulation of microRNA expression in thyroid tumors. J Zhejiang Univ Sci B, 15, 212-24. https://doi.org/10.1631/jzus.B1300192
  121. Zaydfudim V, Feurer ID, Griffin MR, et al (2008). The impact of lymph node involvement on survival in patients with papillary and follicular thyroid carcinoma. Surgery, 144, 1070-8. https://doi.org/10.1016/j.surg.2008.08.034
  122. Zhao H, Ma B, Wang Y, et al (2013). miR-34a inhibits the metastasis of osteosarcoma cells by repressing the expression of CD44. PLoS One, 9, 78644.

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