Skip to main content
Top
Published in: World Journal of Surgical Oncology 1/2017

Open Access 01-12-2017 | Research

MiR-221, a potential prognostic biomarker for recurrence in papillary thyroid cancer

Authors: Lei Dai, Yaozong Wang, Liangliang Chen, Jueru Zheng, Jianjun Li, Xianjiang Wu

Published in: World Journal of Surgical Oncology | Issue 1/2017

Login to get access

Abstract

Background

Many studies have reported several transcriptionally deregulated microRNAs (miRNAs) in papillary thyroid cancer (PTC) tissue in comparison with benign thyroid nodules and normal thyroid tissues. However, the correlation between miRNA expressions and PTC recurrence still remains unclear.

Methods

The PTC patients who scheduled to undergo total thyroidectomy by the same surgical team in Ningbo NO.2 Hospital from March 1998 to March 2008 were enrolled in this study. The clinical and pathological characteristics of each patient were recorded in detail. The selected miRNA expressions were detected using quantitative reverse transcriptase-polymerase chain reaction (qRT-PCR). Potential predictive factors for cancer recurrence were evaluated by univariate and multivariate Cox proportional hazard analysis.

Results

A total of 78 patients were enrolled with 49 females at a mean age of 45.8 years. Enrolled patients were divided into two groups: nonrecurrent group (n = 54) and recurrent group (n = 24). The results from the univariate Cox proportional hazard analysis revealed that primary tumor size, TNM stage, extrathyroid extension, miR-221, and miR-222 expressions were significantly associated with PTC recurrence (P < 0.05). The tissue expression of miR-221 was the only independent risk factor for PTC recurrence (HR 1.41; 95%CI 1.14–1.95, P = 0.007) by multiple Cox proportional hazard analysis.

Conclusions

This study identified the potential role of miR-221 as a prognostic biomarker for the recurrence in PTC.
Literature
1.
go back to reference Sondermann A, Andreghetto FM, Moulatlet AC, da Silva VE, de Castro MG, Nunes FD, Brandao LG, Severino P. MiR-9 and miR-21 as prognostic biomarkers for recurrence in papillary thyroid cancer. Clin Exp Metastasis. 2015;32:521–30.CrossRefPubMed Sondermann A, Andreghetto FM, Moulatlet AC, da Silva VE, de Castro MG, Nunes FD, Brandao LG, Severino P. MiR-9 and miR-21 as prognostic biomarkers for recurrence in papillary thyroid cancer. Clin Exp Metastasis. 2015;32:521–30.CrossRefPubMed
2.
go back to reference Hundahl SA, Fleming ID, Fremgen AM, Menck HR. A National Cancer Data Base report on 53,856 cases of thyroid carcinoma treated in the U.S., 1985-1995. Cancer. 1998;83:2638–48.CrossRefPubMed Hundahl SA, Fleming ID, Fremgen AM, Menck HR. A National Cancer Data Base report on 53,856 cases of thyroid carcinoma treated in the U.S., 1985-1995. Cancer. 1998;83:2638–48.CrossRefPubMed
3.
go back to reference Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ, Mazzaferri EL, McIver B, Sherman SI, Tuttle RM, American Thyroid Association Guidelines T. Management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid. 2006;16:109–42.CrossRefPubMed Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ, Mazzaferri EL, McIver B, Sherman SI, Tuttle RM, American Thyroid Association Guidelines T. Management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid. 2006;16:109–42.CrossRefPubMed
4.
go back to reference Pellegriti G, Scollo C, Lumera G, Regalbuto C, Vigneri R, Belfiore A. Clinical behavior and outcome of papillary thyroid cancers smaller than 1.5 cm in diameter: study of 299 cases. J Clin Endocrinol Metab. 2004;89:3713–20.CrossRefPubMed Pellegriti G, Scollo C, Lumera G, Regalbuto C, Vigneri R, Belfiore A. Clinical behavior and outcome of papillary thyroid cancers smaller than 1.5 cm in diameter: study of 299 cases. J Clin Endocrinol Metab. 2004;89:3713–20.CrossRefPubMed
6.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
7.
go back to reference American Thyroid Association Guidelines Taskforce on Thyroid N, Differentiated Thyroid C, Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ, Mazzaferri EL, McIver B, et al. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid. 2009;19:1167–214.CrossRef American Thyroid Association Guidelines Taskforce on Thyroid N, Differentiated Thyroid C, Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ, Mazzaferri EL, McIver B, et al. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid. 2009;19:1167–214.CrossRef
8.
go back to reference Cady B, Rossi R. An expanded view of risk-group definition in differentiated thyroid carcinoma. Surgery. 1988;104:947–53.PubMed Cady B, Rossi R. An expanded view of risk-group definition in differentiated thyroid carcinoma. Surgery. 1988;104:947–53.PubMed
9.
go back to reference Prasad NB, Somervell H, Tufano RP, Dackiw AP, Marohn MR, Califano JA, Wang Y, Westra WH, Clark DP, Umbricht CB, et al. Identification of genes differentially expressed in benign versus malignant thyroid tumors. Clin Cancer Res. 2008;14:3327–37.CrossRefPubMedPubMedCentral Prasad NB, Somervell H, Tufano RP, Dackiw AP, Marohn MR, Califano JA, Wang Y, Westra WH, Clark DP, Umbricht CB, et al. Identification of genes differentially expressed in benign versus malignant thyroid tumors. Clin Cancer Res. 2008;14:3327–37.CrossRefPubMedPubMedCentral
10.
go back to reference Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E, Aldler H, Rattan S, Keating M, Rai K, et al. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci U S A. 2002;99:15524–9.CrossRefPubMedPubMedCentral Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E, Aldler H, Rattan S, Keating M, Rai K, et al. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci U S A. 2002;99:15524–9.CrossRefPubMedPubMedCentral
11.
go back to reference Ma L, Teruya-Feldstein J, Weinberg RA. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature. 2007;449:682–8.CrossRefPubMed Ma L, Teruya-Feldstein J, Weinberg RA. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature. 2007;449:682–8.CrossRefPubMed
12.
go back to reference Bryant RJ, Pawlowski T, Catto JW, Marsden G, Vessella RL, Rhees B, Kuslich C, Visakorpi T, Hamdy FC. Changes in circulating microRNA levels associated with prostate cancer. Br J Cancer. 2012;106:768–74.CrossRefPubMedPubMedCentral Bryant RJ, Pawlowski T, Catto JW, Marsden G, Vessella RL, Rhees B, Kuslich C, Visakorpi T, Hamdy FC. Changes in circulating microRNA levels associated with prostate cancer. Br J Cancer. 2012;106:768–74.CrossRefPubMedPubMedCentral
14.
go back to reference Pallante P, Visone R, Ferracin M, Ferraro A, Berlingieri MT, Troncone G, Chiappetta G, Liu CG, Santoro M, Negrini M, et al. MicroRNA deregulation in human thyroid papillary carcinomas. Endocr Relat Cancer. 2006;13:497–508.CrossRefPubMed Pallante P, Visone R, Ferracin M, Ferraro A, Berlingieri MT, Troncone G, Chiappetta G, Liu CG, Santoro M, Negrini M, et al. MicroRNA deregulation in human thyroid papillary carcinomas. Endocr Relat Cancer. 2006;13:497–508.CrossRefPubMed
15.
go back to reference 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;93:1600–8.CrossRefPubMedPubMedCentral 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;93:1600–8.CrossRefPubMedPubMedCentral
16.
go back to reference Chen YT, Kitabayashi N, Zhou XK, Fahey 3rd TJ, Scognamiglio T. MicroRNA analysis as a potential diagnostic tool for papillary thyroid carcinoma. Mod Pathol. 2008;21:1139–46.CrossRefPubMed Chen YT, Kitabayashi N, Zhou XK, Fahey 3rd TJ, Scognamiglio T. MicroRNA analysis as a potential diagnostic tool for papillary thyroid carcinoma. Mod Pathol. 2008;21:1139–46.CrossRefPubMed
17.
go back to reference Tetzlaff MT, Liu A, Xu X, Master SR, Baldwin DA, Tobias JW, Livolsi VA, Baloch ZW. Differential expression of miRNAs in papillary thyroid carcinoma compared to multinodular goiter using formalin fixed paraffin embedded tissues. Endocr Pathol. 2007;18:163–73.CrossRefPubMed Tetzlaff MT, Liu A, Xu X, Master SR, Baldwin DA, Tobias JW, Livolsi VA, Baloch ZW. Differential expression of miRNAs in papillary thyroid carcinoma compared to multinodular goiter using formalin fixed paraffin embedded tissues. Endocr Pathol. 2007;18:163–73.CrossRefPubMed
18.
go back to reference He H, Jazdzewski K, Li W, Liyanarachchi S, Nagy R, Volinia S, Calin GA, Liu CG, Franssila K, Suster S, et al. The role of microRNA genes in papillary thyroid carcinoma. Proc Natl Acad Sci U S A. 2005;102:19075–80.CrossRefPubMedPubMedCentral He H, Jazdzewski K, Li W, Liyanarachchi S, Nagy R, Volinia S, Calin GA, Liu CG, Franssila K, Suster S, et al. The role of microRNA genes in papillary thyroid carcinoma. Proc Natl Acad Sci U S A. 2005;102:19075–80.CrossRefPubMedPubMedCentral
19.
go back to reference Lee JC, Zhao JT, Clifton-Bligh RJ, Gill A, Gundara JS, Ip JC, Glover A, Sywak MS, Delbridge LW, Robinson BG, Sidhu SB. MicroRNA-222 and microRNA-146b are tissue and circulating biomarkers of recurrent papillary thyroid cancer. Cancer. 2013;119:4358–65.CrossRefPubMed Lee JC, Zhao JT, Clifton-Bligh RJ, Gill A, Gundara JS, Ip JC, Glover A, Sywak MS, Delbridge LW, Robinson BG, Sidhu SB. MicroRNA-222 and microRNA-146b are tissue and circulating biomarkers of recurrent papillary thyroid cancer. Cancer. 2013;119:4358–65.CrossRefPubMed
20.
go back to reference Shaha AR, Shah JP, Loree TR. Patterns of failure in differentiated carcinoma of the thyroid based on risk groups. Head Neck. 1998;20:26–30.CrossRefPubMed Shaha AR, Shah JP, Loree TR. Patterns of failure in differentiated carcinoma of the thyroid based on risk groups. Head Neck. 1998;20:26–30.CrossRefPubMed
21.
go back to reference Wittekind C. Lymph nodes, tumour deposits, and TNM: are we getting better? 7th edition of UICC 2010 TNM classification of malignant tumors. Strahlenther Onkol. 2012;188:191–2.CrossRefPubMed Wittekind C. Lymph nodes, tumour deposits, and TNM: are we getting better? 7th edition of UICC 2010 TNM classification of malignant tumors. Strahlenther Onkol. 2012;188:191–2.CrossRefPubMed
22.
go back to reference Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods. 2001;25:402–8.CrossRefPubMed Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods. 2001;25:402–8.CrossRefPubMed
23.
go back to reference Wang Q, Chu B, Zhu J, Zhang S, Liu Y, Zhuang M, Yang Y. Clinical analysis of prophylactic central neck dissection for papillary thyroid carcinoma. Clin Transl Oncol. 2014;16:44–8.CrossRefPubMed Wang Q, Chu B, Zhu J, Zhang S, Liu Y, Zhuang M, Yang Y. Clinical analysis of prophylactic central neck dissection for papillary thyroid carcinoma. Clin Transl Oncol. 2014;16:44–8.CrossRefPubMed
24.
go back to reference Lee YS, Kim SW, Kim SW, Kim SK, Kang HS, Lee ES, Chung KW. Extent of routine central lymph node dissection with small papillary thyroid carcinoma. World J Surg. 2007;31:1954–9.CrossRefPubMed Lee YS, Kim SW, Kim SW, Kim SK, Kang HS, Lee ES, Chung KW. Extent of routine central lymph node dissection with small papillary thyroid carcinoma. World J Surg. 2007;31:1954–9.CrossRefPubMed
25.
go back to reference Machens A, Holzhausen HJ, Dralle H. The prognostic value of primary tumor size in papillary and follicular thyroid carcinoma. Cancer. 2005;103:2269–73.CrossRefPubMed Machens A, Holzhausen HJ, Dralle H. The prognostic value of primary tumor size in papillary and follicular thyroid carcinoma. Cancer. 2005;103:2269–73.CrossRefPubMed
26.
go back to reference Suh YJ, Kwon H, Kim SJ, Choi JY, Lee KE, Park YJ, Park do J, Youn YK. Factors affecting the locoregional recurrence of conventional papillary thyroid carcinoma after surgery: a retrospective analysis of 3381 patients. Ann Surg Oncol. 2015;22:3543–9.CrossRefPubMed Suh YJ, Kwon H, Kim SJ, Choi JY, Lee KE, Park YJ, Park do J, Youn YK. Factors affecting the locoregional recurrence of conventional papillary thyroid carcinoma after surgery: a retrospective analysis of 3381 patients. Ann Surg Oncol. 2015;22:3543–9.CrossRefPubMed
27.
go back to reference Roh JL, Kim JM, Park CI. Central lymph node metastasis of unilateral papillary thyroid carcinoma: patterns and factors predictive of nodal metastasis, morbidity, and recurrence. Ann Surg Oncol. 2011;18:2245–50.CrossRefPubMed Roh JL, Kim JM, Park CI. Central lymph node metastasis of unilateral papillary thyroid carcinoma: patterns and factors predictive of nodal metastasis, morbidity, and recurrence. Ann Surg Oncol. 2011;18:2245–50.CrossRefPubMed
28.
go back to reference Chou CK, Chen RF, Chou FF, Chang HW, Chen YJ, Lee YF, Yang KD, Cheng JT, Huang CC, Liu RT. miR-146b is highly expressed in adult papillary thyroid carcinomas with high risk features including extrathyroidal invasion and the BRAF(V600E) mutation. Thyroid. 2010;20:489–94.CrossRefPubMed Chou CK, Chen RF, Chou FF, Chang HW, Chen YJ, Lee YF, Yang KD, Cheng JT, Huang CC, Liu RT. miR-146b is highly expressed in adult papillary thyroid carcinomas with high risk features including extrathyroidal invasion and the BRAF(V600E) mutation. Thyroid. 2010;20:489–94.CrossRefPubMed
29.
go back to reference Visone R, Russo L, Pallante P, De Martino I, Ferraro A, Leone V, Borbone E, Petrocca F, Alder H, Croce CM, 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;14:791–8.CrossRefPubMed Visone R, Russo L, Pallante P, De Martino I, Ferraro A, Leone V, Borbone E, Petrocca F, Alder H, Croce CM, 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;14:791–8.CrossRefPubMed
30.
go back to reference Sheu SY, 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;102:376–82.CrossRefPubMed Sheu SY, 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;102:376–82.CrossRefPubMed
31.
go back to reference Yang Z, Zhang Y, Zhang X, Zhang M, Liu H, Zhang S, Qi B, Sun X. Serum microRNA-221 functions as a potential diagnostic and prognostic marker for patients with osteosarcoma. Biomed Pharmacother. 2015;75:153–8.CrossRefPubMed Yang Z, Zhang Y, Zhang X, Zhang M, Liu H, Zhang S, Qi B, Sun X. Serum microRNA-221 functions as a potential diagnostic and prognostic marker for patients with osteosarcoma. Biomed Pharmacother. 2015;75:153–8.CrossRefPubMed
32.
go back to reference Vergho DC, Kneitz S, Kalogirou C, Burger M, Krebs M, Rosenwald A, Spahn M, Loser A, Kocot A, Riedmiller H, Kneitz B. Impact of miR-21, miR-126 and miR-221 as prognostic factors of clear cell renal cell carcinoma with tumor thrombus of the inferior vena cava. PLoS One. 2014;9:e109877.CrossRefPubMedPubMedCentral Vergho DC, Kneitz S, Kalogirou C, Burger M, Krebs M, Rosenwald A, Spahn M, Loser A, Kocot A, Riedmiller H, Kneitz B. Impact of miR-21, miR-126 and miR-221 as prognostic factors of clear cell renal cell carcinoma with tumor thrombus of the inferior vena cava. PLoS One. 2014;9:e109877.CrossRefPubMedPubMedCentral
33.
go back to reference Mazeh H, Mizrahi I, Halle D, Ilyayev N, Stojadinovic A, Trink B, Mitrani-Rosenbaum S, Roistacher M, Ariel I, Eid A, et al. Development of a microRNA-based molecular assay for the detection of papillary thyroid carcinoma in aspiration biopsy samples. Thyroid. 2011;21:111–8.CrossRefPubMed Mazeh H, Mizrahi I, Halle D, Ilyayev N, Stojadinovic A, Trink B, Mitrani-Rosenbaum S, Roistacher M, Ariel I, Eid A, et al. Development of a microRNA-based molecular assay for the detection of papillary thyroid carcinoma in aspiration biopsy samples. Thyroid. 2011;21:111–8.CrossRefPubMed
34.
go back to reference Mattia G, Errico MC, Felicetti F, Petrini M, Bottero L, Tomasello L, Romania P, Boe A, Segnalini P, Di Virgilio A, et al. Constitutive activation of the ETS-1-miR-222 circuitry in metastatic melanoma. Pigment Cell Melanoma Res. 2011;24:953–65.CrossRefPubMedPubMedCentral Mattia G, Errico MC, Felicetti F, Petrini M, Bottero L, Tomasello L, Romania P, Boe A, Segnalini P, Di Virgilio A, et al. Constitutive activation of the ETS-1-miR-222 circuitry in metastatic melanoma. Pigment Cell Melanoma Res. 2011;24:953–65.CrossRefPubMedPubMedCentral
35.
go back to reference Pan Y, Li J, Zhang Y, Wang N, Liang H, Liu Y, Zhang CY, Zen K, Gu H. Slug-upregulated miR-221 promotes breast cancer progression through suppressing E-cadherin expression. Sci Rep. 2016;6:25798.CrossRefPubMedPubMedCentral Pan Y, Li J, Zhang Y, Wang N, Liang H, Liu Y, Zhang CY, Zen K, Gu H. Slug-upregulated miR-221 promotes breast cancer progression through suppressing E-cadherin expression. Sci Rep. 2016;6:25798.CrossRefPubMedPubMedCentral
36.
go back to reference Coarfa C, Fiskus W, Eedunuri VK, Rajapakshe K, Foley C, Chew SA, Shah SS, Geng C, Shou J, Mohamed JS, et al. Comprehensive proteomic profiling identifies the androgen receptor axis and other signaling pathways as targets of microRNAs suppressed in metastatic prostate cancer. Oncogene. 2016;35:2345–56.CrossRefPubMed Coarfa C, Fiskus W, Eedunuri VK, Rajapakshe K, Foley C, Chew SA, Shah SS, Geng C, Shou J, Mohamed JS, et al. Comprehensive proteomic profiling identifies the androgen receptor axis and other signaling pathways as targets of microRNAs suppressed in metastatic prostate cancer. Oncogene. 2016;35:2345–56.CrossRefPubMed
Metadata
Title
MiR-221, a potential prognostic biomarker for recurrence in papillary thyroid cancer
Authors
Lei Dai
Yaozong Wang
Liangliang Chen
Jueru Zheng
Jianjun Li
Xianjiang Wu
Publication date
01-12-2017
Publisher
BioMed Central
Published in
World Journal of Surgical Oncology / Issue 1/2017
Electronic ISSN: 1477-7819
DOI
https://doi.org/10.1186/s12957-016-1086-z

Other articles of this Issue 1/2017

World Journal of Surgical Oncology 1/2017 Go to the issue