Expression of miR-31-5p affects growth, migration and invasiveness of papillary thyroid cancer cells.
EMT
Hippo pathway
PTC
miR-31-5-p
β-catenin.
Journal
Endocrine
ISSN: 1559-0100
Titre abrégé: Endocrine
Pays: United States
ID NLM: 9434444
Informations de publication
Date de publication:
03 2023
03 2023
Historique:
received:
02
11
2022
accepted:
17
11
2022
pubmed:
7
12
2022
medline:
9
3
2023
entrez:
6
12
2022
Statut:
ppublish
Résumé
In this study, we evaluated the biological role of miRNA-31-5p in papillary thyroid cancer (PTC). By using the real-time PCR, we measured miRNA-31-5p expression levels in 25 PTC tissues and in two human PTC cell lines (K1 and TPC-1). Then, K1 cells were transiently transfected with mirVana inhibitor or mirVana mimic to miRNA-31-5-p. Cell proliferation was determined by MTT and colony formation assays. The in vitro metastatic ability of thyroid cancer cells was evaluated by adhesion, migration and invasion assays. Epithelial mesenchymal transition (EMT) and Hippo pathway related gene and protein levels were evaluated by using the TaqMan™ Gene Expression Assays and western blot analysis, respectively. We found a significant increase of miR-31-5-p expression in tumor tissue and in K1 cells harboring the BRAF p.V600E mutation. Knockdown of miR-31-5p determined a reduction of cell proliferation, associated with a significant decrease in cell adhesion, migration and invasion properties. A downregulation of EMT markers and YAP/β-catenin axis was also observed. Our findings suggest that miRNA-31-5p acts as oncogenic miRNA in human thyrocytes and its overexpression may be involved in the BRAF-related tumorigenesis in PTCs, providing new understanding into its pathological role in PTC progression and invasiveness.
Identifiants
pubmed: 36474133
doi: 10.1007/s12020-022-03267-6
pii: 10.1007/s12020-022-03267-6
doi:
Substances chimiques
Proto-Oncogene Proteins B-raf
EC 2.7.11.1
MicroRNAs
0
MIRN31 microRNA, human
0
Types de publication
Journal Article
Comment
Langues
eng
Sous-ensembles de citation
IM
Pagination
517-526Commentaires et corrections
Type : CommentOn
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
S. Bulotta, M. Celano, G. Costante, D. Russo, Novel therapeutic options for radioiodine-refractory thyroid cancer: redifferentiation and beyond. Curr. Opin. Oncol. 32(1), 13–19 (2020). https://doi.org/10.1097/CCO.0000000000000593
doi: 10.1097/CCO.0000000000000593
pubmed: 31599772
R. Niciporuka, J. Nazarovs, A. Ozolins, Z. Narbuts, E. Miklasevics, J. Gardovskis. Can we predict differentiated thyroid cancer behavior? role of genetic and molecular markers. Medicina (Kaunas, Lithuania) 57(10), 1131 (2021). https://doi.org/10.3390/medicina57101131 .
M. Rogucki, A. Buczynska, A.J. Kretowski, A. Poplawska-Kita, The Importance of miRNA in the Diagnosis and Prognosis of Papillary Thyroid Cancer. J. Clin. Med. 10(20), 4738 (2021). https://doi.org/10.3390/jcm10204738
doi: 10.3390/jcm10204738
pubmed: 34682861
pmcid: 8537372
M. Hussain, Micro-RNAs (miRNAs): Genomic Organisation, Biogenesis and Mode of Action. Cell. Tissue Res. 349, 405–413 (2012). https://doi.org/10.1007/s00441-012-1438-0
doi: 10.1007/s00441-012-1438-0
C.R. Lima, C.C. Gomes, M.F. Santos, Role of microRNAs in endocrine cancer metastasis. Mol. Cell. Endocrinol. 456, 62–75 (2017). https://doi.org/10.1016/j.mce.2017.03.015
doi: 10.1016/j.mce.2017.03.015
pubmed: 28322989
H. Shakib, S. Rajabi, M.H. Dehghan, F.J. Mashayekhi, N. Safari-Alighiarloo, M. Hedayati, Epithelial-to-mesenchymal transition in thyroid cancer: a comprehensive review. Endocrine 66, 435–455 (2019). https://doi.org/10.1007/s12020-019-02030-8
doi: 10.1007/s12020-019-02030-8
pubmed: 31378850
Y. Sun, S. Yu, Y. Liu, F. Wang, Y. Liu, H. Xiao, Expression of miRNAs in Papillary Thyroid Carcinomas Is Associated with BRAF Mutation and Clinicopathological Features in Chinese Patients. Int. J. Endocrinol. 2013, 128735 (2013). https://doi.org/10.1155/2013/128735
doi: 10.1155/2013/128735
pubmed: 23690767
pmcid: 3639632
M. Papaioannou, A.G. Chorti, A. Chatzikyriakidou, K. Giannoulis, S. Bakkar, T.S. Papavramidis, MicroRNAs in Papillary Thyroid Cancer: What Is New in Diagnosis and Treatment. Front. Oncol. 11, 755097 (2022). https://doi.org/10.3389/fonc.2021.755097
doi: 10.3389/fonc.2021.755097
pubmed: 35186709
pmcid: 8851242
M. Celano, F. Rosignolo, V. Maggisano, V. Pecce, M. Iannone, D. Russo, S. Bulotta, MicroRNAs as Biomarkers in Thyroid Carcinoma. Int. J. Genomics. 2017, 6496570 (2017). https://doi.org/10.1155/2017/6496570
doi: 10.1155/2017/6496570
pubmed: 29038786
pmcid: 5606057
V. Maggisano, F. Capriglione, A. Verrienti, M. Celano, A. Gagliardi, S. Bulotta, M. Sponziello, C. Mio, V. Pecce, C. Durante, G. Damante, D. Russo, Identification of Exosomal microRNAs and Their Targets in Papillary Thyroid Cancer Cells. Biomedicines 10(5), 961 (2022). https://doi.org/10.3390/biomedicines10050961
doi: 10.3390/biomedicines10050961
pubmed: 35625697
pmcid: 9138952
Y. Wang, B.G. Liu, C.X. Zhou, MicroRNA-31 inhibits papillary thyroid carcinoma cell biological progression by directly targeting SOX11 and regulating epithelial-to-mesenchymal transition, ERK and Akt signaling pathways. Eur. Rev. Med. Pharmacol. Sci. 23, 5863–5873 (2019). https://doi.org/10.26355/eurrev_201907_18329
doi: 10.26355/eurrev_201907_18329
pubmed: 31298337
D. Yi, D. Zhang, J. He, Long non-coding RNA LIFR-AS1 suppressed the proliferation, angiogenesis, migration and invasion of papillary thyroid cancer cells via the miR-31-5p/SIDT2 axis. Cell. Cycle 20, 2619–2637 (2021). https://doi.org/10.1080/15384101.2021.1995129
doi: 10.1080/15384101.2021.1995129
pubmed: 34781815
pmcid: 8726651
R.M. Tuttle, B. Haugen, N.D. Perrier, Updated American Joint Committee on Cancer/Tumor-Node-Metastasis Staging System for Differentiated and Anaplastic Thyroid Cancer (Eighth Edition): What Changed and Why? Thyroid 27(6), 751–756 (2017). https://doi.org/10.1089/thy.2017.0102
doi: 10.1089/thy.2017.0102
pubmed: 28463585
pmcid: 5467103
B.R. Haugen, E.K. Alexander, K.C. Bible, G.M. Doherty, S.J. Mandel, Y.E. Nikiforov, F. Pacini, G.W. Randolph, A.M. Sawka, M. Schlumberger, K.G. Schuff, S.I. Sherman, J.A. Sosa, D.L. Steward, R.M. Tuttle, L. Wartofsky, 2015 American Thyroid Association Management Guidelines for Adult Patients with Thyroid Nodules and Differentiated Thyroid Cancer: The American Thyroid Association Guidelines Task Force on Thyroid Nodules and Differentiated Thyroid Cancer. Thyroid 26, 1–133 (2016). https://doi.org/10.1089/thy.2015.0020
doi: 10.1089/thy.2015.0020
pubmed: 26462967
pmcid: 4739132
N. Passon, E. Bregant, M. Sponziello, M. Dima, F. Rosignolo, C. Durante, M. Celano, D. Russo, S. Filetti, G. Damante, Somatic amplifications and deletions in genome of papillary thyroid carcinomas. Endocrine 50, 453–464 (2015). https://doi.org/10.1007/s12020-015-0592-z
doi: 10.1007/s12020-015-0592-z
pubmed: 25863487
R.E. Schweppe, J.P. Klopper, C. Korch, U. Pugazhenthi, M. Benezra, J.A. Knauf, J.A. Fagin, L.A. Marlow, J.A. Copland, R.C. Smallridge, B.R. Haugen, Deoxyribonucleic acid profiling analysis of 40 human thyroid cancer cell lines reveals cross-contamination resulting in cell line redundancy and misidentification. J. Clin. Endocrinol. Metab. 93, 4331–4341 (2008). https://doi.org/10.1210/jc.2008-1102
doi: 10.1210/jc.2008-1102
pubmed: 18713817
pmcid: 2582569
A. Bairoch, The Cellosaurus, a Cell-Line Knowledge Resource. J. Biomol. Tech. 29(2), 25–38 (2018). https://doi.org/10.7171/jbt.18-2902-002
doi: 10.7171/jbt.18-2902-002
pubmed: 29805321
pmcid: 5945021
V. Maggisano, M. Celano, S.M. Lepore, M. Sponziello, F. Rosignolo, V. Pecce, A. Verrienti, F. Baldan, C. Mio, L. Allegri, M. Maranghi, R. Falcone, G. Damante, D. Russo, S. Bulotta, Human telomerase reverse transcriptase in papillary thyroid cancer: gene expression, effects of silencing and regulation by BET inhibitors in thyroid cancer cells. Endocrine 63, 545–553 (2019). https://doi.org/10.1007/s12020-018-01836-2
doi: 10.1007/s12020-018-01836-2
pubmed: 30661164
K.J. Livak, S.J. Flood, J. Marmaro, W. Giusti, K. Deetz, Oligonucleotides with fluorescent dyes at opposite ends provide a quenched probe system useful for detecting PCR product and nucleic acid hybridization. PCR Methods Appl. 4, 357–362 (1995). https://doi.org/10.1101/gr.4.6.357
doi: 10.1101/gr.4.6.357
pubmed: 7580930
M. Celano, V. Maggisano, S. Bulotta, L. Allegri, V. Pecce, L. Abballe, G. Damante, D. Russo, Quercetin improves the effects of sorafenib on growth and migration of thyroid cancer cells. Endocrine 67, 496–498 (2020). https://doi.org/10.1007/s12020-019-02140-3
doi: 10.1007/s12020-019-02140-3
pubmed: 31776977
S. Borowicz, M. Van Scoyk, S. Avasarala, M.K.K. Rathinam, J. Tauler, R.K. Bikkavilli, R.A. Winn, The soft agar colony formation assay. J. Vis. Exp. 92, e51998 (2014). https://doi.org/10.3791/51998
doi: 10.3791/51998
S. Bulotta, M.V. Ierardi, J. Maiuolo, M.G. Cattaneo, A. Cerullo, L.M. Vicentini, N. Borgese, Basal nitric oxide release attenuates cell migration of HeLa and endothelial cells. Biochem. Biophys. Res. Commun. 386, 744e749 (2009). https://doi.org/10.1016/j.bbrc.2009.06.118
doi: 10.1016/j.bbrc.2009.06.118
M. D’Agostino, P. Voce, M. Celano, M. Sponziello, S. Moretti, V. Maggisano, A. Verrienti, C. Durante, S. Filetti, E. Puxeddu, D. Russo, Sunitinib exerts only limited effects on the proliferation and differentiation of anaplastic thyroid cancer cells. Thyroid 22, 138–144 (2012). https://doi.org/10.1089/thy.2011.0060
doi: 10.1089/thy.2011.0060
pubmed: 22191389
S. Bulotta, A. Cerullo, R. Barsacchi, C. De Palma, D. Rotiroti, E. Clementi, N. Borgese, Endothelial nitric oxide synthase is segregated from caveolin-1 and localizes to the leading edge of migrating cells. Exp. Cell Res. 312(6), 877–889 (2006). https://doi.org/10.1016/j.yexcr.2005.12.014
doi: 10.1016/j.yexcr.2005.12.014
pubmed: 16427620
N. Mastronikolis, E. Tsiambas, D. Roukas, P. Fotiades, A. Chrysovergis, V. Papanikolaou, E. Kyrodimos, S. Mastronikoli, A. Niotis, V. Ragos, Micro-RNAs signatures in papillary thyroid carcinoma. J. Buon. 25(5), 2144–2146 (2020)
pubmed: 33277828
X. Chen, L. Zhong, X. Li, W. Liu, Y. Zhao, J. Li, Down-regulation of microRNA-31-5p inhibits proliferation and invasion of osteosarcoma cells through Wnt/β-catenin signaling pathway by enhancing AXIN1. Exp. Mol. Pathol. 108, 32–41 (2019). https://doi.org/10.1016/j.yexmp.2019.03.001
doi: 10.1016/j.yexmp.2019.03.001
pubmed: 30844369
Z. Lu, Q. He, J. Liang, W. Li, Q. Su, Z. Chen, Q. Wan, X. Zhou, L. Cao, J. Sun, Y. Wu, L. Liu, X. Wu, J. Hou, K. Lian, A. Wang, miR-31-5p Is a Potential Circulating Biomarker and Therapeutic Target for Oral Cancer. Mol. Ther. Nucleic Acids 16, 471–480 (2019). https://doi.org/10.1016/j.omtn.2019.03.012
doi: 10.1016/j.omtn.2019.03.012
pubmed: 31051332
pmcid: 6495075
Y.L. Du, Y. Liang, G.Q. Shi, Y. Cao, J. Qiu, L. Yuan, Z. Yong, L. Liu, J. Li, LINC00689 participates in proliferation, chemoresistance and metastasis via miR-31-5p/YAP/beta-catenin axis in colorectal cancer. Exp. Cell. Res. 395, 112176 (2020). https://doi.org/10.1016/j.yexcr.2020.112176
doi: 10.1016/j.yexcr.2020.112176
pubmed: 32682784
F. Song, Z. Xuan, X. Yang, X. Ye, Z. Pan, Q. Fang, Identification of key microRNAs and hub genes in non-small-cell lung cancer using integrative bioinformatics and functional analyses. J. Cell. Biochem. 121, 2690–2703 (2020). https://doi.org/10.1002/jcb.29489
doi: 10.1002/jcb.29489
pubmed: 31692035
H.G. Vuong, A.M.A. Altibi, U.N.P. Duong, L. Hassell, Prognostic implication of BRAF and TERT promoter mutation combination in papillary thyroid carcinoma-A meta-analysis. Clin. Endocrinol. (Oxf.). 87, 411–417 (2017). https://doi.org/10.1111/cen.13413
doi: 10.1111/cen.13413
pubmed: 28666074
V. Vasko, A.V. Espinosa, W. Scouten, H. He, H. Auer, S. Liyanarachchi, A. Larin, V. Savchenko, G.L. Francis, A. de la Chapelle, M. Saji, M.D. Ringel, Gene expression and functional evidence of epithelial-to-mesenchymal transition in papillary thyroid carcinoma invasion. Proc. Natl Acad. Sci. USA. 104, 2803–2808 (2007). https://doi.org/10.1073/pnas.0610733104
doi: 10.1073/pnas.0610733104
pubmed: 17296934
pmcid: 1815262
P. Baquero, E. Jimenez-Mora, A. Santos, M. Lasa, A. Chiloeches, TGF beta induces epithelial-mesenchymal transition of thyroid cancer cells by both the BRAF/MEK/ERK and Src/FAK pathways. Mol. Carcinog. 55, 1639–1654 (2016). https://doi.org/10.1002/mc.22415
doi: 10.1002/mc.22415
pubmed: 26392228
M. Sponziello, F. Rosignolo, M. Celano, V. Maggisano, V. Pecce, R.F. De Rose, G.E. Lombardo, C. Durante, S. Filetti, G. Damante, D. Russo, S. Bulotta, Fibronectin-1 expression is increased in aggressive thyroid cancer and favors the migration and invasion of cancer cells. Mol. Cell. Endocrinol. 431, 123–132 (2016). https://doi.org/10.1016/j.mce.2016.05.007
doi: 10.1016/j.mce.2016.05.007
pubmed: 27173027
S. Xia, C. Wang, E.L. Postma, Y. Yang, X. Ni, W. Zhan, Fibronectin 1 promotes migration and invasion of papillary thyroid cancer and predicts papillary thyroid cancer lymph node metastasis. Onco Targets Ther. 10, 1743–1755 (2017). https://doi.org/10.2147/OTT.S122009
doi: 10.2147/OTT.S122009
pubmed: 28367057
pmcid: 5370387
Y. Lei, L. Chen, G. Zhang, A. Shan, C. Ye, B. Liang, J. Sun, X. Liao, C. Zhu, Y. Chen, J. Wang, E. Zhang, L. Deng, MicroRNAs target the Wnt/betacatenin signaling pathway to regulate epithelial mesenchymal transition in cancer (Review). Oncol. Rep. 44, 1299–1313 (2020). https://doi.org/10.3892/or.2020.7703
doi: 10.3892/or.2020.7703
pubmed: 32700744
pmcid: 7448411
B. Mi, Q. Li, T. Li, G. Liu, J. Sai, High miR-31-5p expression promotes colon adenocarcinoma progression by targeting TNS1. Aging (Albany NY) 12, 7480–7490 (2020). https://doi.org/10.18632/aging.103096
doi: 10.18632/aging.103096
pubmed: 32315285
I. Akrida, V. Bravou, H. Papadaki, The deadly cross-talk between Hippo pathway and epithelial-mesenchymal transition (EMT) in cancer. Mol. Biol. Rep. 49(10), 10065–10076 (2022). https://doi.org/10.1007/s11033-022-07590-z
doi: 10.1007/s11033-022-07590-z
pubmed: 35604626
T. Pei, Y. Li, J. Wang, H. Wang, Y. Liang, H. Shi, B. Sun, D. Yin, J. Sun, R. Song, S. Pan, Y. Sun, H. Jiang, T. Zheng, L. Liu, YAP is a critical oncogene in human cholangiocarcinoma. Oncotarget 6, 17206–17220 (2015). https://doi.org/10.18632/oncotarget.4043
doi: 10.18632/oncotarget.4043
pubmed: 26015398
pmcid: 4627302
S.E. Hiemer, L. Zhang, V.K. Kartha, T.S. Packer, M. Almershed, V. Noonan, M. Kukuruzinska, M.V. Bais, S. Monti, X. Varelas, A YAP/TAZ-Regulated Molecular Signature Is Associated with Oral Squamous Cell Carcinoma. Mol. Cancer Res. 13, 957–968 (2015). https://doi.org/10.1158/1541-7786.MCR-14-0580
doi: 10.1158/1541-7786.MCR-14-0580
pubmed: 25794680
pmcid: 4470857
W. Zhang, Y. Gao, F. Li, X. Tong, Y. Ren, X. Han, S. Yao, F. Long, Z. Yang, H. Fan, L. Zhang, H. Ji, YAP promotes malignant progression of Lkb1-deficient lung adenocarcinoma through downstream regulation of survivin. Cancer Res. 75, 4450–4457 (2015). https://doi.org/10.1158/0008-5472.CAN-14-3396
doi: 10.1158/0008-5472.CAN-14-3396
pubmed: 26363011
M. Celano, C. Mignogna, F. Rosignolo, M. Sponziello, M. Iannone, S.M. Lepore, G.E. Lombardo, V. Maggisano, A. Verrienti, S. Bulotta, C. Durante, C. Di Loreto, G. Damante, D. Russo, Expression of YAP1 in aggressive thyroid cancer. Endocrine 59(1), 209–212 (2018). https://doi.org/10.1007/s12020-017-1240-6
doi: 10.1007/s12020-017-1240-6
pubmed: 28120182
Z. Liu, W. Zeng, Y. Maimaiti, J. Ming, Y. Guo, Y. Liu, C. Liu, T. Huang, High Expression of Yes-activated Protein-1 in Papillary Thyroid Carcinoma Correlates With Poor Prognosis. Appl. Immunohistochem. Mol. Morphol. 27(1), 59–64 (2019). https://doi.org/10.1097/PAI.0000000000000544.
doi: 10.1097/PAI.0000000000000544.
pubmed: 28682834
M. Wang, M. Dai, D. Wang, W. Xiong, Z. Zeng, C. Guo, The regulatory networks of the Hippo signaling pathway in cancer development. J. Cancer 12, 6216–6230 (2021). https://doi.org/10.7150/jca.62402
doi: 10.7150/jca.62402
pubmed: 34539895
pmcid: 8425214
P. Ma, J. Han, Overexpression of miR-100-5p inhibits papillary thyroid cancer progression via targeting FZD8. Open Med. (Wars.) 17(1), 1172–1182 (2022). https://doi.org/10.1515/med-2022-0490
doi: 10.1515/med-2022-0490
pubmed: 35859793
B. Basu, M.K. Ghosh, Ubiquitination and deubiquitination in the regulation of epithelial-mesenchymal transition in cancer: Shifting gears at the molecular level. Biochim. Biophys. Acta Mol. Cell. Res. 1869, 119261 (2022). https://doi.org/10.1016/j.bbamcr.2022.119261
doi: 10.1016/j.bbamcr.2022.119261
pubmed: 35307468