The miR-221/222 cluster, miR-10b and miR-92a are highly upregulated in metastatic minimally invasive follicular thyroid carcinoma

Jikuzono,Tomoo; Kawamoto,Masashi; Yoshitake,Hiroshi; Kikuchi,Kunio; Akasu,Haruki; Ishikawa,Hitoshi; Hirokawa,Mitsuyoshi; Miyauchi,Akira; Tsuchiya,Shinichi; Shimizu,Kazuo; Takizawa,Toshihiro

doi:10.3892/ijo.2013.1879

The miR-221/222 cluster, miR-10b and miR-92a are highly upregulated in metastatic minimally invasive follicular thyroid carcinoma

Authors:
- Tomoo Jikuzono
- Masashi Kawamoto
- Hiroshi Yoshitake
- Kunio Kikuchi
- Haruki Akasu
- Hitoshi Ishikawa
- Mitsuyoshi Hirokawa
- Akira Miyauchi
- Shinichi Tsuchiya
- Kazuo Shimizu
- Toshihiro Takizawa
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Affiliations: Department of Molecular Medicine and Anatomy, Nippon Medical School, Tokyo, Japan, Division of Diagnostic Pathology, Nippon Medical School Hospital, Tokyo, Japan, Division of Endocrine Surgery, Nippon Medical School Musashi-kosugi Hospital, Kanagawa, Japan, Yamagata Saisei Hospital, Yamagata, Japan, Kuma Hospital, Hyogo, Japan, Department of Surgery, Division of Endocrine Surgery, Nippon Medical School, Tokyo, Japan
Published online on: April 2, 2013 https://doi.org/10.3892/ijo.2013.1879
Pages: 1858-1868
Copyright: © Jikuzono et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY_NC 3.0].

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Abstract

Minimally invasive follicular thyroid carcinoma (MI-FTC) is characterized by limited capsular and/or vascular invasion with good long-term outcomes. However, some cases of MI-FTC show a poor prognosis because of severe distant metastasis (i.e., metastatic MI-FTC). Nonetheless, no method has been established for predicting the prognosis of MI-FTC. This study was conducted to identify novel prognostic factors for metastatic MI-FTC by the use of microRNA (miRNA). Thirty-four patients with MI-FTC were categorized into two groups: the metastatic group, M(+) (n=12) and the non-metastatic group, M(-) (n=22). In the M(+) group, distant metastasis was recognized after the initial operation established the diagnosis of MI-FTC. In the M(-) group, no distant metastasis was recognized postoperatively for ≥10 years. Using laser microdissection followed by quantitative real-time PCR and PCR arrays, we performed a comprehensive expression profiling of 667 miRNAs in formalin-fixed, paraffin-embedded samples from the initial MI-FTC operation. Furthermore, we assessed the potential use of miRNAs as novel biomarkers for the metastatic potential of MI-FTC by logistic regression analysis. Comprehensive quantitative analysis of miRNA expression in MI-FTC samples revealed that the miR-221/222 cluster (i.e., miR-221, miR-222 and miR-222*), miR-10b and miR-92a were significantly upregulated in the M(+) group compared with the M(-) group. Interestingly, the expression levels of these miRNAs were also shown to be upregulated in widely invasive FTC (WI-FTC; n=13) that has distant metastasis and worse prognosis, indicating a close similarity in the miRNA expression between metastatic MI-FTC and WI-FTC. Logistic regression analysis revealed that miR-10b made a significant contribution to prognosis (OR 19.759, 95% CI 1.433-272.355, p=0.026). Our findings suggest that miR-10b is a potential prognostic factor for evaluating the metastatic potential of MI-FTC at an initial operation stage.

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1	Vinay K, Abul KA, Nelson F and Richard M: Robbins: Basic Pathology. 8th edition. Saunders; Philadelphia, PA: 2007
2	LiVolsi VA: Pathology of thyroid disease. Thyroid Disease: Endocrinology, Surgery, Nuclear Medicine and Radiotherapy. Falk SA: Lippincott-Raven; Philadelphia, PA: pp. 127–175. 1997
3	DeLellis RA and Williams ED: Thyroid and parathyroid tumours. World Health Organization Classification of Tumours. Pathology and Genetics. Tumours of Endocrine Organs. DeLellis RA, Lloyd RV, Heitz PU and Eng C: IARC Press; Lyon: pp. 51–56. 2004
4	Sobrinho-Simoes M, Albores-Saavedra J and Tallini G: Poorly dirrerentiated carcinoma. World Health Organization Classification of Tumours. Pathology and Genetics. Tumours of Endocrine Organs. DeLellis RA, Lloyd RV, Heitz PU and Eng C: IARC Press; Lyon: pp. 73–76. 2004
5	Ito Y, Hirokawa M, Higashiyama T, Takamura Y, Miya A, Kobayashi K, Matsuzuka F, Kuma K and Miyauchi A: Prognosis and prognostic factors of follicular carcinoma in Japan: importance of postoperative pathological examination. World J Surg. 31:1417–1424. 2007. View Article : Google Scholar : PubMed/NCBI
6	Bartel DP: MicroRNAs: genomics, biogenesis, mechanism and function. Cell. 116:281–297. 2004. View Article : Google Scholar : PubMed/NCBI
7	Chen CZ: MicroRNAs as oncogenes and tumor suppressors. N Engl J Med. 353:1768–1771. 2005. View Article : Google Scholar : PubMed/NCBI
8	Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S, Magri E, Pedriali M, Fabbri M, Campiglio M, Menard S, Palazzo JP, Rosenberg A, Musiani P, Volinia S, Nenci I, Calin GA, Querzoli P, Neqrini M and Croce CM: MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 65:7065–7070. 2005. View Article : Google Scholar : PubMed/NCBI
9	Murakami Y, Yasuda T, Saigo K, Urashima T, Toyoda H, Okanoue T and Shimotohno K: Comprehensive analysis of microRNA expression patterns in hepatocellular carcinoma and non-tumorous tissues. Oncogene. 25:2537–2545. 2005. View Article : Google Scholar : PubMed/NCBI
10	Calin GA, Ferracin M, Cimmino A, Di Leva G, Shimizu M, Wojcik SE, Iorio MV, Visone R, Sever NI, Fabbri M, Iuliano R, Palumbo T, Pichiorri F, Roldo C, Garzon R, Sevignani C, Rassenti L, Alder H, Volnia S, Liu CG, Kipps TJ, Negrini M and Croce CM: A microRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med. 353:1793–1801. 2005. View Article : Google Scholar : PubMed/NCBI
11	Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, Yi M, Stephens RM, Okamoto A, Yokota J, Tanaka T, Calin GA, Liu CG, Croce CM and Harris CC: Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell. 9:189–198. 2006. View Article : Google Scholar : PubMed/NCBI
12	Visone R, Russo L, Pallante P, De Martino I, Ferraro A, Leone V, Borbone E, Petrocca F, Alder H, Croce CM and Fusco A: MicroRNAs(miR)-221 and miR-222, both overexpressed in human thyroid papillary carcinomas, regulate p27^Kip1 protein levels and cell cycle. Endocr Relat Cancer. 14:791–798. 2007. View Article : Google Scholar : PubMed/NCBI
13	Pallante P, Visone R, Croce CM and Fusco A: Deregulation of microRNA expression in follicular cell-derived human thyroid carcinomas. Endocr Relat Cancer. 17:F91–F104. 2010. View Article : Google Scholar : PubMed/NCBI
14	Mazeh H, Mizrahi I, Halle D, Ilyayev N, Stojadinovic A, Trink B, Mitrani-Rosenbaum S, Roistacher M, Ariel I, Eid A, Freund HR and Nissan A: Development of a microRNA-based molecular assay for the detection of papillary thyroid carcinoma in aspiration biopsy samples. Thyroid. 21:111–118. 2011. View Article : Google Scholar : PubMed/NCBI
15	Hair JF Jr, Anderson RE, Tatham RL and Black WC: Multivariate Data Analysis with Readings. 4th edition. Prentice-Hall; Englewood Cliffs: 1995
16	Cohen J, Cohen P, West SG and Aiken LS: Applied Multiple Regression/Correlation Analysis for the Behavioral Sciences. 3rd edition. Lawrence Erlbaum Associates; Mahwah, NJ: 2003
17	Guthrie JL, Seah C, Brown S, Tang P, Jamieson F and Drews SJ: Use of Bordetella pertussis BP3385 to establish a cutoff value for an IS481-targeted real-time PCR assay. J Clin Microbiol. 46:3798–3799. 2008. View Article : Google Scholar : PubMed/NCBI
18	Xi Y, Nakajima G, Gavin E, Morris CG, Kudo K, Hayashi K and Ju J: Systematic analysis of microRNA expression of RNA extracted from fresh frozen and formalin-fixed paraffin-embedded samples. RNA. 13:1668–1674. 2007. View Article : Google Scholar : PubMed/NCBI
19	Cronin M, Pho M, Dutta D, Stephans JC, Shak S, Kiefer MC, Esteban JM and Baker JB: Measurement of gene expression in archival paraffin-embedded tissues: development and performance of a 92-gene reverse transcriptase-polymerase chain reaction assay. Am J Pathol. 164:35–42. 2004. View Article : Google Scholar
20	Masuda N, Ohnishi T, Kawamoto S, Monden M and Okubo K: Analysis of chemical modification of RNA from formalin-fixed samples and optimization of molecular biology applications for such samples. Nucleic Acids Res. 27:4436–4443. 1999. View Article : Google Scholar : PubMed/NCBI
21	Srinivasan M, Sedmak D and Jewell S: Effect of fixatives and tissue processing on the content and integrity of nucleic acids. Am J Pathol. 161:1961–1971. 2002. View Article : Google Scholar : PubMed/NCBI
22	Nikiforova MN, Tseng GC, Steward D, Diorio D and Nikiforov YE: MicroRNA expression profiling of thyroid tumors: biological significance and diagnostic utility. J Clin Endocrinol Metab. 93:1600–1608. 2008. View Article : Google Scholar : PubMed/NCBI
23	Takano T, Miyauchi A, Yoshida H, Kuma k and 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. 90:1600–1605. 2004. View Article : Google Scholar
24	Foukakis T, Gusnanto A, Au AY, Höög A, Lui WO, Larsson C, Wallin G and Zedenius J: A PCR-based expression signature of malignancy in follicular thyroid tumors. Endocr Relat Cancer. 14:381–391. 2007. View Article : Google Scholar : PubMed/NCBI
25	Lu J, Getz G, Miska EA, Alvarz-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, Downing JR, Jacks T, Horvitz HR and Golub TR: MicroRNA expression profiles classify human cancers. Nature. 435:834–838. 2005. View Article : Google Scholar : PubMed/NCBI
26	Galardi S, Mercatelli N, Giorda E, Massalini S, Frajese GV, Ciafere SA and Farace MG: miR-221 and miR-222 expression affects the proliferation potential of human prostate carcinoma cell lines by targeting p27^Kip1. J Biol Chem. 282:23716–23724. 2007. View Article : Google Scholar : PubMed/NCBI
27	Miller TE, Ghoshal K, Ramaswamy B, Roy S, Datta J, Shapiro CL, Jacob S and Majumder S: MicroRNA-221/222 confers tamoxifen resistance in breast cancer by targeting p27^Kip1. J Biol Chem. 283:29897–29903. 2008. View Article : Google Scholar : PubMed/NCBI
28	Zhang C, Han L, Zhag A, Yang W, Zhou X, Pu P, Du Y, Zeng H and Kang C: Global changes of mRNA expression reveals an increased activity of the interferon-induced signal transducer and activator of transcription (STAT) pathway by repression of miR-221/222 in glioblastoma U251 cells. Int J Oncol. 36:1503–1512. 2010.
29	Le Sage C, Nagel R, Egan DA, Schrier M, Mesman E, Mangiola A, Anile C, Maira G, Mercatelli N, Ciafre SA, Farace MG and Agami R: Regulation of the p27(Kip1) tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation. EMBO J. 26:3699–3708. 2007.PubMed/NCBI
30	Fornari F, Gramantieri L, Ferracin M, Veronese A, Sabbiori S, Calin GA, Grazi GL, Giovannini C, Croce CM, Bolondi L and Negrini M: MiR-221 controls CDKN1C/p57 and CDKN1B/p27 expression in human hepatocellular carcinoma. Oncogene. 27:5651–5661. 2008. View Article : Google Scholar : PubMed/NCBI
31	He H, Jazdzewski K, Li W, Liyanarachchi S, Nagy R, Volinia S, Calin GA, Liu CG, Franssila K, Suster S, Kloos RT, Croce CM and de la Chapelle A: The role of microRNA genes in papillary thyroid carcinoma. Proc Natl Acad Sci USA. 102:19075–19080. 2005. View Article : Google Scholar : PubMed/NCBI
32	Ma L, Teruya-Feldstein J and Weinberg RA: Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature. 449:682–688. 2007. View Article : Google Scholar : PubMed/NCBI
33	Tan HX, Wang Q, Chen LZ, Huang XH, Chen JS, Fu XH, Cao LQ, Chen XL, Li W and Zhang LJ: MicroRNA-9 reduces cell invasion and E-cadherin secretion in SK-Hep-1 cell. Med Oncol. 27:654–660. 2010. View Article : Google Scholar : PubMed/NCBI
34	Bloomston M, Frankel WL, Petrocca F, Volinia S, Alder H, Hagan JP, Liu CG, Bhatt D, Taccioli C and Croce CM: MicroRNA expression patterns to differentiate pancreatic adenocarcinoma from normal pancreas and chronic pancreatitis. JAMA. 297:1901–1908. 2007. View Article : Google Scholar : PubMed/NCBI
35	Ciafre SA, Galardi S, Mangiola A, Ferracin M, Liu CG, Sabatino G, Negrini M, Maira G, Croce CM and Farace MG: Extensive modulation of a set of microRNAs in primary glioblastoma. Biochem Biophys Res Commun. 334:1351–1358. 2005. View Article : Google Scholar : PubMed/NCBI
36	Huse JT, Brennan C, Hambardzumyan D, Wee B, Pena J, Rouhanifard SH, Sohn-Lee C, le Sage C, Agami R, Tuschl T and Holland EC: The PTEN-regulating microRNA miR-26a is amplified in high-grade glioma and facilitates gliomagenesis in vivo. Genes Dev. 23:1327–1337. 2009. View Article : Google Scholar : PubMed/NCBI
37	Sun L, Yan W, Wang Y, Sun G, Luo H, Zhang J, Wang X, You Y, Yang Z and Liu N: MicroRNA-10b induces glioma cell invasion by modulating MMP-14 and uPAR expression via HOXD10. Brain Res. 1389:9–18. 2011. View Article : Google Scholar : PubMed/NCBI
38	Ma L and Weinberg RA: Micromanagers of malignancy: role of microRNAs in regulating metastasis. Trends Genet. 24:448–456. 2008. View Article : Google Scholar : PubMed/NCBI
39	Ota A, Tagawa H, Karnan S, Tsuzuki S, Karpas A, Kira S, Yoshida Y and Seto M: Identification and characterization of a novel gene, C13orf25, as a target for 13q31-q32 amplification in malignant lymphoma. Cancer Res. 64:3087–3095. 2004. View Article : Google Scholar : PubMed/NCBI
40	Hayashita Y, Osada H, Tatematsu Y, Yamada H, Yanagisawa K, Tomida S, Yatabe Y, Kawahara K, Sekido Y and Takahashi T: A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res. 65:9628–9632. 2005. View Article : Google Scholar : PubMed/NCBI
41	Monzo M, Navarro A, Bandres E, Artells R, Moreno I, Gel B, Ibeas R, Moreno J, Martinez F, Diaz T, Martinez A, Balagué O and Garcia-Foncillas J: Overlapping expression of microRNAs in human embryonic colon and colorectal cancer. Cell Res. 18:823–833. 2008. View Article : Google Scholar : PubMed/NCBI
42	Diosdado B, van de Wiel MA, Terhaar Sive Droste JS, Mongera S, Postma C, Meijerink W J, Carvalho B and Meijer GA: MiR-17-92 cluster is associated with 13q gain and c-myc expression during colorectal adenoma to adenocarcinoma progression. Br J Cancer. 101:707–714. 2009. View Article : Google Scholar : PubMed/NCBI
43	Connolly E, Melegari M, Landgraf P, Tchaikovskaya T, Tennant BC, Slagle BL, Rogler LE, Zavolan M, Tuschl T and Rogler CE: Elevated expression of the miR-17-92 polycistron and miR-21 in hepadnavirus-associated hepatocellular carcinoma contributes to the malignant phenotype. Am J Pathol. 173:856–864. 2008. View Article : Google Scholar
44	Chen HC, Chen GH, Chen Y H, Liao WL, Liu CY, Chang KP, Chang YS and Chen SJ: MicroRNA deregulation and pathway alterations in nasopharyngeal carcinoma. Br J Cancer. 100:1002–1011. 2009. View Article : Google Scholar : PubMed/NCBI
45	Takakura S, Mitsutake N, Nakashima M, Namba H, Saenko VA, Rogounovitch TI, Nakazawa Y, Hayashi T, Ohtsuru A and Yamashita S: Oncogenic role of miR-17-92 cluster in anaplastic thyroid cancer cells. Cancer Sci. 99:147–154. 2008. View Article : Google Scholar : PubMed/NCBI
46	Chen ZL, Zhao XH, Wang JW, Li BZ, Wang Z, Sun J, Tan FW, Ding DP, Xu XH, Zhou F, Tan XG, Hang J, Shi SS, Feng XL and He J: microRNA-92a promotes lymph node metastasis of human esophageal squamous cell carcinoma via E-cadherin. J Biol Chem. 25:10725–10734. 2011. View Article : Google Scholar : PubMed/NCBI
47	Mete O and Asa SL: Pathological definition and clinical significance of vascular invasion in thyroid carcinomas of follicular epithelial derivation. Mod Pathol. 24:1545–1552. 2011. View Article : Google Scholar : PubMed/NCBI
48	Asari R, Koperek O, Scheuba C, Riss P, Kaserer K, Hoffmann M and Niederle B: Follicular thyroid carcinoma in an iodine-replete endemic goiter region: a prospectively collected, retrospectively analyzed clinical trial. Ann Surg. 249:1023–1031. 2009. View Article : Google Scholar
49	Sugino K and Ito K, Nagahama M, Kitagawa W, Shibuya H, Ohkuwa K, Yano Y, Uruno T, Akaishi J, Kameyama K and Ito K: Prognosis and prognostic factors for distant metastases and tumor mortality in follicular thyroid carcinoma. Thyroid. 21:751–757. 2011. View Article : Google Scholar : PubMed/NCBI
50	Mazzaferri EL and Jhiang SM: Long-term impact of initial surgical and medical therapy on papillary and follicular thyroid cancer. Am J Med. 97:418–428. 1994. View Article : Google Scholar : PubMed/NCBI
51	van Heerden JA, Hay ID, Goellner JR, Salomao D, Ebersold JR, Bergstralh EJ and Grant CS: Follicular thyroid carcinoma with capsular invasion alone: a nonthreatening malignancy. Surgery. 112:1130–1138. 1992.PubMed/NCBI
52	Thompson LD, Wieneke JA, Paal E, Frommelt RA, Adair CF and Heffess CS: A clinicopathologic study of minimally invasive follicular carcinoma of the thyroid gland with a review of the English literature. Cancer. 91:505–524. 2001. View Article : Google Scholar : PubMed/NCBI
53	Mazafferi EL and Kloos RT: Carcinoma of follicular epithelium: radioiodine and other treatments and outcomes. The Thyroid. Braverman LE and Utiger RD: Lippincott Williams & Wilkins; Philadelphia, PA: pp. 934–966. 2005