Skip to main content

Advertisement

Log in

MiR-9 and miR-21 as prognostic biomarkers for recurrence in papillary thyroid cancer

  • Research Paper
  • Published:
Clinical & Experimental Metastasis Aims and scope Submit manuscript

Abstract

Despite low mortality rates, nodal recurrence in papillary thyroid carcinoma occurs in up to 20 % of patients. Emerging evidences indicate that dysregulated microRNAs are implicated in the process of metastasis. In the present study, we investigated whether miR-9, miR-10b, miR-21 and miR-146b levels are predictive of papillary thyroid carcinoma recurrence. Using macro-dissection followed by quantitative real-time PCR, we measured miR-9, miR-10b, miR-21 and miR-146b expression levels in formalin-fixed, paraffin-embedded samples of 66 patients with papillary thyroid carcinoma categorized into two groups: the recurrent group (n = 19) and the non-recurrent group (n = 47). All patients underwent total thyroidectomy and were followed for at least 120 months after surgery to be considered recurrence-free. Univariate and multivariate analysis were performed using the Cox proportional hazard model in order to identify associations between multiple clinical variables and microRNA expression levels and papillary thyroid carcinoma recurrence. MiR-9 and miR-21 expression levels were found to be significant prognostic factors for recurrence in patients with papillary thyroid carcinoma (HR = 1.48; 95 % CI 1.24–1.77, p < 0.001; and HR = 1.52; 95 % CI 1.18–1.94, p = 0.001; respectively). Multivariate analysis involving the expression level of miR-9 and miR-21 and various clinical parameters identified the expression of these microRNAs as independent prognostic factors for papillary thyroid cancer patients. In conclusion, our results support the potential clinical value of miR-9 and miR-21 as prognostic biomarkers for recurrence in papillary thyroid carcinoma.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Abbreviations

PTC:

Papillary thyroid carcinoma

miR:

microRNA

PCR:

Polymerase chain reaction

qRT-PCR:

Quantitative real time polymerase chain reaction

RNA:

Ribonucleic acid

IBCC:

Instituto Brasileiro de Controle do Câncer

UICC:

Union for International Cancer Control

TNM:

Tumor, nodes, metastasis

ATA:

American Thyroid Association

MSKCC–NY:

Memorial Sloan Kettering Cancer Center–New York

FFPE:

Formalin-fixed paraffin-embedded

cDNA:

Complementary deoxyribonucleic acid

HR:

Hazard ratio

CI:

Confidence interval

cm:

Centimeter

EGFR:

Epidermal growth factor receptor

MMP16:

Matrix metalloproteinase 16

ICAM1:

Intercellular adhesion molecule 1

STMN1:

Stathmin 1

References

  1. Ferlay J, Soerjomataram I, Ervik M, et al (2013) GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11 [Internet]. Lyon, France: International Agency for Research on Cance. http://globocan.iarc.fr. Accessed 04 Dec 2014

  2. Hundahl SA, Fleming ID, Fremgen AM, Menck HR (1998) A National Cancer Data Base report on 53,856 cases of thyroid carcinoma treated in the U.S., 1985–1995. Cancer 83:2638–2648

    Article  CAS  PubMed  Google Scholar 

  3. Mazzaferri EL, Jhiang S (1994) Long term impact of initial surgical and medical therapy on papillary and follicular thyroid cancer. Am J Med 97:418–428

    Article  CAS  PubMed  Google Scholar 

  4. Gilliand FD, Hunt WC, Morris DM, Key CR (1997) Prognostic factors for thyroid carcinoma. A population-based study of 151,698 cases from surveillance, epidemiology and end results (SEER) program 1973–1991. Cancer 79:564–573

    Article  Google Scholar 

  5. Cooper DS, Doherty GM, Haugen BR et al (2006) American Thyroid Association Guidelines Taskforce. Management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 16:109–142

    Article  PubMed  Google Scholar 

  6. Scheumann GF, Gimm O, Wegener G, Hundeshagen H, Dralle H (1994) Prognostic significance and surgical management of locoregional lymph node metastases in papillary thyroid cancer. World J Surg 18:559–567

    Article  CAS  PubMed  Google Scholar 

  7. Mazzaferri EL, Kloos RT (2001) Clinical review 128: current approaches to primary therapy for papillary and follicular thyroid cancer. J Clin Endocrinol Metab 86:1447–1463

    Article  CAS  PubMed  Google Scholar 

  8. Hay ID, Thompson GB, Grant CS et al (2002) Papillary thyroid carcinoma managed at the Mayo Clinic during six decades (1940–1999): temporal trends in initial therapy and long-term outcome in 2444 consecutively treated patients. World J Surg 26:879–885

    Article  PubMed  Google Scholar 

  9. Pellegriti G, Scollo C, Lumera G, Regalbuto C, Vigneri R, Belfiore A (2004) Clinical behaviour and outcome of papillary thyroid cancers smaller than 1,5 cm in diameter: study of 299 cases. J Clin Endocr Metabol 89:3713–3720

    Article  CAS  Google Scholar 

  10. Grant CS (2015) Recurrence of papillary thyroid cancer after optimized surgery. Gland Surg 4(1):52–56

    PubMed Central  PubMed  Google Scholar 

  11. Sobin LH, Wittekind C (2009) UICC: TNM classification of malignant tumors, 7th edn. Wiley-Liss, New York

    Google Scholar 

  12. Cady B, Rossi R (1998) An expanded view of risk group definition in differentiated thyroid carcinoma. Surgery 104:947–953

    Article  Google Scholar 

  13. Hay ID, Grant CS, Taylor WF, MaConahey WM (1987) Ipsilateral lobectomy versus bilateral lobar resection in papillary thyroid carcinoma: a retrospective analysis of survival outcome using a novel prognostic scoring system. Surgery 102:1088–1095

    CAS  PubMed  Google Scholar 

  14. Hay ID, Bergstrahl EJ, Goellner JR, Ebersold JR, Grant CS (1993) Predicting outcome in papillary thyroid carcinoma: development of a reliable prognostic scoring system in a cohort of 1779 patients surgically treated at one institution during 1940 through 1989. Surgery 114:1050–1058

    CAS  PubMed  Google Scholar 

  15. Revised American Thyroid Association Management Guidelines For Patients With Thyroid Nodules And Differentiated Thyroid Cancer (2009) The American Thyroid Association (ATA) guidelines taskforce on thyroid nodules and differentiated thyroid cancer. Thyroid 19(11):1167–1214

    Article  Google Scholar 

  16. Shaha AR, Shah JP, Loree TR (1998) Patterns of failure in differentiated carcinoma of the thyroid based on risk groups. Head Neck 20:26–30

    Article  CAS  PubMed  Google Scholar 

  17. Byar DP, Green SB, Dor P et al (1979) A prognostic index for thyroid carcinoma. A study of the E.O.R.T.C. Thyroid Cancer Cooperative Group. Eur J Cancer 15:1033–1041

    Article  CAS  PubMed  Google Scholar 

  18. Calin GA, Dumitru CD, Shimizu M et al (2002) Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 99:15524–15529

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Ma L, Teruya-Feldstein J, Weinberg RA (2007) Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449:682–688

    Article  CAS  PubMed  Google Scholar 

  20. He H, Jazdzewski K, Li W et al (2005) The role of microRNA genes in papillary thyroid carcinoma. Proc Natl Acad Sci USA 102:19075–19080

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Pallante P, Visone R, Ferracin M et al (2006) MicroRNA deregulation in human thyroid papillary carcinomas. Endocr Relat Cancer 13(2):497–508

    Article  CAS  PubMed  Google Scholar 

  22. 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(3):163–173

    Article  CAS  PubMed  Google Scholar 

  23. Nikiforova MN, Tseng GC, Steward D et al (2008) MicroRNA expression profiling of thyroid tumors: biological significance and diagnostic utility. J Clin Endocrinol Metab 93:1600–1608

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. 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 mutation. Thyroid 20(5):489–494

    Article  CAS  PubMed  Google Scholar 

  25. 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 119:4358–4365

    Article  CAS  PubMed  Google Scholar 

  26. Yip L, Kelly L, Shuai Y et al (2011) MicroRNA signature distinguishes the degree of aggressiveness of papillary thyroid carcinoma. Ann Surg Oncol 18:2035–2041

    Article  PubMed  Google Scholar 

  27. Chou CK, Yang KD, Chou FF et al (2013) Prognostic implications of miR-146b expression and its functional role in papillary thyroid carcinoma. JCEM 98(2):E196–E205

    CAS  PubMed  Google Scholar 

  28. Sun XJ, Liu H, Zhang P, Zhang ZD, Jiang ZW, Jiang CC (2013) miR-10b promotes migration and invasion in nasopharyngeal carcinoma cells. Asian Pac J Cancer Prev 14(9):5533–5537

    Article  PubMed  Google Scholar 

  29. Ouyang H, Gore J, Deitz S, Korc M (2013) microRNA-10b enhances pancreatic cancer cell invasion by suppressing TIP30 expression and promoting EGF and TGF-b actions. Oncogene 1–11

  30. Li Z, Gu X, Fang Y, Xiang J, Chen Z (2012) microRNA expression profiles in human colorectal cancers with brain metastases. Oncol Lett 3(2):346–350

    CAS  PubMed Central  PubMed  Google Scholar 

  31. Yang Z, Miao R, Li G et al (2013) Identification of recurrence related microRNAs in hepatocellular carcinoma after surgical resection. Int J Mol Sci 14:1105–1118

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Huang Y-H, Lin K-H, Chen H-C et al (2012) Identification of postoperative prognostic MicroRNA predictors in hepatocellular carcinoma. PLoS One 7(5):e37188

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Han Z, Chen HY, Fan JW, Wu JY, Tang HM, Peng ZH (2012) Up-regulation of microRNA-155 promotes cancer cell invasion and predicts poor survival of hepatocellular carcinoma following liver transplantation. J Cancer Res Clin Oncol 138:153–161

    Article  CAS  PubMed  Google Scholar 

  34. Han Z, Zhonga L, Tengb M-J et al (2012) Identification of recurrence-related microRNAs in hepatocellular carcinoma following liver transplantation. Mol Oncol 6:445–447

    Article  CAS  PubMed  Google Scholar 

  35. Jikuzono T, Kawamoto M, Yoshitake H et al (2013) The miR-221/222 cluster, miR-10b and miR-92a are highly up-regulated in metastatic minimally invasive follicular thyroid carcinoma. Int J Oncol 42:1858–1868

    CAS  PubMed Central  PubMed  Google Scholar 

  36. Xu T, Liu X, Han L, Shen H, Liu L, Shu Y (2013) Up-regulation of mir-9 expression as a poor prognostic biomarker in patients with non-small cell lung cancer. Clin Transl Oncol. doi:10.1007/s12094-013-1106-1

    Google Scholar 

  37. Sun Z, Han Q, Zhou N et al (2013) MicroRNA-9 enhances migration and invasion through KLF17 in hepatocellular carcinoma. Mol Oncol 7:884–894

    Article  CAS  PubMed  Google Scholar 

  38. Ma L, Young J, Prabhala H et al (2010) Mir-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol 12(3):247–256

    CAS  PubMed Central  PubMed  Google Scholar 

  39. Wang J, Zhao H, Tang D et al (2013) Overexpressions of microRNA-9 and microRNA-200c in human breast cancers are associated with lymph node metastasis. Cancer Biother Radiopharma 28(4):283–288

    Article  CAS  Google Scholar 

  40. Zhu L, Chen H, Zhou D et al (2012) MicroRNA-9 up-regulation is involved in colorectal cancer metastasis via promoting cell motility. Med Oncol 29:1037–1043

    Article  CAS  PubMed  Google Scholar 

  41. Hildebrandt MAT, Gu J, Lin J et al (2010) Hsa-miR-9 methylation status is associated with cancer development and metastatic recurrence in patients with clear cell renal cell carcinoma. Oncogene 29:5724–5728

    Article  CAS  PubMed  Google Scholar 

  42. Zheng L, Qi T, Yang D et al (2013) microRNA-9 suppresses the proliferation, invasion and metastasis of gastric cancer cells through targeting cyclin D1 and Ets1. PLoS One 8(1):e55719

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  43. Laios A, O’Toole S, Flavin R et al (2008) Potential role of miR-9 and miR-223 in recurrent ovarian cancer. Mol Cancer 28(7):35

    Article  Google Scholar 

  44. Kjaer-Frifeldt S, Hansen TF, Nielsen BS, Joergensen S, Lindebjerg J, Soerensen FB (2012) The prognostic importance of mir-21 in stage II colon cancer: a population-based study. Br J Cancer 107:1169–1174

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  45. Oue N, Anami K, Schetter AJ et al (2014) High mir-21 expression from FFPE tissues is associated with poor survival and response to adjuvant chemotherapy in colon cancer. Int J Cancer 134:1926–1934

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  46. Weissmann-Brenner A, Kushnir M, Yanai GL et al (2012) Tumor microRNA-29a expression and the risk of recurrence in stage II colon cancer. Int J Oncol 40(6):2097–2103

    CAS  PubMed  Google Scholar 

  47. Zaravinos A, Radojicic J, Lambrou GI et al (2012) Expression of MiRNAs involved in angiogenesis, tumor cell proliferation, tumor suppressor inhibition, epithelial-mesenchymal transition and activation of metastasis in bladder cancer. J Urol 188:615–623

    Article  CAS  PubMed  Google Scholar 

  48. Yang M, Shen H, Qiu C et al (2013) High expression of mir-21 and mir-155 predicts recurrence and unfavorable survival in non-small cell lung cancer. Eur J Cancer 49:604–615

    Article  CAS  PubMed  Google Scholar 

  49. Ota D, Mimori K, Yokobori T et al (2011) Identification of recurrence-related microRNAs in the bone marrow of breast cancer patients. Int J Oncol 38:955–962

    CAS  PubMed  Google Scholar 

  50. Wang G, Wang L, Sun S et al (2015) Quantitative measurement of serum microRNA-21 expression in relation to breast cancer metastasis in Chinese female. Ann Lab Med 35(2):226–232

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  51. Li T, Li RS, Li YH et al (2012) miR-21 as an independent biochemical recurrence predictor and potential therapeutic target for prostate cancer. J Urol 187:1466–1472

    Article  CAS  PubMed  Google Scholar 

  52. Hummel R, Hussey DJ, Michael MZ et al (2011) MiRNAs and their association with locoregional staging and survival following surgery for esophageal carcinoma. Ann Surg Oncol 18:253–260

    Article  PubMed  Google Scholar 

  53. Akagi I, Miyashita M, Ishibashi O et al (2011) Relationship between altered expression levels of MIR21, MIR143, MIR145, and MIR205 and clinicopathologic features of esophageal squamous cell carcinoma. Dis Esophagus 24:523–530

    Article  CAS  PubMed  Google Scholar 

  54. Li P, Mao WM, Zheng ZG et al (2013) Down-regulation of PTEN expression modulated by dysregulated miR-21 contributes to the progression of esophageal cancer. Dig Dis Sci 58(12):3483–3493

    Article  CAS  PubMed  Google Scholar 

  55. Ren Q, Liang J, Wei J et al (2014) Epithelial and stromal expression of miRNAs during prostate cancer progression. Am J Transl Res 6(4):329–339

    PubMed Central  PubMed  Google Scholar 

  56. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  57. Costa S, Giugliano G, Santoro L et al (2009) Role of prophylactic central neck dissection in cN0 papillary thyroid cancer. Acta Otorhinolaryngol Ital 29:61–69

    CAS  PubMed Central  PubMed  Google Scholar 

  58. Wada N, Duh QY, Sugino K et al (2003) Lymph node metastasis from 259 papillary thyroid microcarcinomas. Ann Surg 237(3):399–407

    PubMed Central  PubMed  Google Scholar 

  59. Wang Q, Chu B, Zhu J et al (2014) Clinical analysis of prophylactic central neck dissection for papillary thyroid carcinoma. Clin Transl Oncol 16:44–48

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  60. Lee YS, Kim SW, Kim SK, Kang HS, Lee ES, Chung KW (2007) Extent of routine central lymph node dissection with small papillary thyroid carcinoma. World J Surg 31:1954–1959

    Article  PubMed  Google Scholar 

  61. Shaha AR, Loree TR, Shah JP (1994) Intermediate risk group for differentiated carcinoma of the Thyroid. Surgery 116:1036–1042

    CAS  PubMed  Google Scholar 

  62. Ito Y, Tomoda C, Uruno T et al (2006) Clinical significance of metastasis to the central compartment from papillary microcarcinoma of the thyroid. World J Surg 30:91–99

    Article  PubMed  Google Scholar 

  63. Machens A, Holzhausen HJ, Dralle H (2005) The prognostic value of primary tumor size in papillary and follicular thyroid carcinoma. Cancer 103:2269–2273

    Article  PubMed  Google Scholar 

  64. Suh YJ, Kwon H, Kim SJ et al (2015) Factors affecting the locoregional recurrence of conventional papillary thyroid carcinoma after surgery: a retrospective analysis of 3381 patients. Ann Surg Oncol [Epub ahead of print]

  65. Ito Y, Jikuzono T, Higashiyama T et al (2006) Clinical significance of lymph node metastasis of thyroid papillary carcinoma located in one lobe. World J Surg 30:1821–1828

    Article  PubMed  Google Scholar 

  66. Roh JL, Kim JM, Park CI (2011) Central lymph node metastasis of unilateral papillary thyroid carcinoma: patterns and factors predictive of nodal metastasis, mor- bidity, and recurrence. Ann Surg Oncol 18:2245–2250

    Article  PubMed  Google Scholar 

  67. Koo BS, Choi EC, Yoon YH, Kim DH, Kim EH, Lim YC (2009) Predictive factors for ipsilateral or contralateral central lymph node metastasis in unilateral papillary thyroid carcinoma. Ann Surg 249:840–844

    Article  PubMed  Google Scholar 

  68. Sato N, Oyamatsu M, Koyama Y, Emura I, Tamiya Y, Hatakeyama K (1998) Do the level of nodal disease according to the TNM classification and the number of involved cervical nodes reflect prognosis in patients with differentiated carcinoma of the thyroid gland? J Surg Oncol 69:151–155

    Article  CAS  PubMed  Google Scholar 

  69. Grebe SK, Hay ID (1996) Thyroid cancer nodal metastases: biological significance and therapeutic considerations. Surg Oncol Clin N Am 5:43–63

    CAS  PubMed  Google Scholar 

  70. Wada N, Suganuma N, Nakayama H et al (2007) Microscopic regional lymph node status in papillary thyroid carcinoma with and without lymphadenopathy and its relation to outcomes. Langenbecks Arch Surg 392:417–422

    Article  PubMed  Google Scholar 

  71. Hughes CJ, Shaha AR, Shah JP, Loree TR (1996) Impact of lymph node metastasis in differentiated carcinoma of the thyroid: a matched-pair analysis. Head Neck 18:127–132

    Article  CAS  PubMed  Google Scholar 

  72. Lundgren CI, Hall P, Dickman PW, Zedenius J (2006) Clinically significant prognostic factors for differentiated thyroid carcinoma: a population-based, nested case-control study. Cancer 106:524–531

    Article  PubMed  Google Scholar 

  73. Beasley NJP, Lee J, Eski S, Walfish P, Witterick I, Freeman JL (2002) Impact of nodal metastases on prognosis in patients with well-differentiated thyroid cancer. Arch Otolaryngol Head Neck Surg 128:825–828

    Article  PubMed  Google Scholar 

  74. Bardet S, Malville E, Rame JP et al (2008) Macroscopic lymph-node involvement and neck dissection predict lymph-node recurrence in papillary thyroid carcinoma. Eur J Endocr 158:551–560

    Article  CAS  Google Scholar 

  75. Edmonds MD, Hurst DR, Vaidya KS, Stafford LJ, Chen D, Welch DR (2009) Breast cancer metastasis suppressor 1 coordinately regulates metastasis-associated microRNA expression. Int J Cancer 125(8):1778–1785

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  76. Liu Y, Zhao J, Zhang PY et al (2012) MicroRNA-10b targets E-cadherin and modulates breast cancer metastasis. Med Sci Monit 18(8):BR299–BR308

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  77. Katakowski M, Zheng X, Jiang F, Rogers T, Szalad A, Chopp M (2010) MiR-146b-5p suppresses EGFR expression and reduces in vitro migration and invasion of glioma. Cancer Invest 28(10):1024–1030

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  78. Hurst DR, Edmonds MD, Scott GK, Benz CC, Vaidya KS, Welch DR (2009) Breast cancer metastasis suppressor 1 up-regulates miR-146, which suppresses breast cancer metastasis. Cancer Res 69(4):1279–1283

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  79. Li Y, Wang Y, Yu L et al (2013) MiR-146b-5p inhibits glioma migration and invasion by targeting MMP16. Cancer Lett 339:260–269

    Article  CAS  PubMed  Google Scholar 

  80. Wang Z, Zhang H, He L et al (2013) Association between the expression of four up-regulated miRNAs and extrathyroidal invasion in papillary thyroid carcinoma. Oncotargets Ther 6:281–287

    Article  CAS  Google Scholar 

  81. Terao M, Fratelli M, Kurosaki M et al (2011) Induction of miR-21 by retinoic acid in estrogen receptor-positive breast carcinoma cells: biological correlates and molecular targets. J Biol Chem. 286(5):4027–4042

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  82. Buitrago D, Keutgen XM, Crowley M et al (2012) Intercellular adhesion molecule-1 (ICAM-1) is upregulated in aggressive papillary thyroid carcinoma. Ann Surg Oncol 19(3):973–980

    Article  CAS  PubMed  Google Scholar 

  83. Tan W, Gu J, Huang M, Wu X, Hildebrandt MAT (2014) Epigenetic analysis of microRNA genes in tumors from surgically resected lung cancer patients and association with survival. Carcinog, Mol. doi:10.1002/mc.22149

    Google Scholar 

  84. Lujambio A, Calin GA, Villanueva A et al (2008) A microRNA DNA methylation signature for human cancer metastasis. Proc Natl Acad Sci 105:13556–13561

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  85. Khoo MLC, Beasley NJP, Ezzat S et al (2002) Overexpression of cyclin D1 and underexpression of p27 predict lymph node metastases in papillary thyroid carcinoma. J Clin Endocrinol Metab 87(4):1814–1818

    Article  CAS  PubMed  Google Scholar 

  86. Song Y, Mu L, Han X et al (2013) MicroRNA-9 inhibits vasculogenic mimicry of glioma cell lines by suppressing Stathmin expression. J Neurooncol 115(3):381–390

    Article  CAS  PubMed  Google Scholar 

  87. Gustavo Baldassarre G, Belletti B, Nicoloso MS et al (2005) p27Kip1-stathmin interaction influences sarcoma cell migration and invasion. Cancer Cell 7(1):51–63

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Patricia Severino.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 92 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sondermann, A., Andreghetto, F.M., Moulatlet, A.C.B. et al. MiR-9 and miR-21 as prognostic biomarkers for recurrence in papillary thyroid cancer. Clin Exp Metastasis 32, 521–530 (2015). https://doi.org/10.1007/s10585-015-9724-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10585-015-9724-3

Keywords

Navigation