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Published in: Tumor Biology 1/2016

01-01-2016 | Original Article

Antisense-miR-21 enhances differentiation/apoptosis and reduces cancer stemness state on anaplastic thyroid cancer

Authors: Vahid Haghpanah, Parviz Fallah, Rezvan Tavakoli, Mahmood Naderi, Hilda Samimi, Masoud Soleimani, Bagher Larijani

Published in: Tumor Biology | Issue 1/2016

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Abstract

Anaplastic thyroid carcinoma (ATC) is the most aggressive malignancy in thyroid cancers. Resistance to current therapies is still a challenge. MicroRNAs are a class of small non-coding RNAs, regulating gene expression. MiR-21 is an oncomiR that is overexpressed in nearly all cancers including ATC. Accumulating evidence suggested that miR-21 has a role in cancer stemness state, apoptosis, cell cycle progression, and differentiation. Therefore, we evaluated the application of Off-miR-21 to sequester the microRNA for therapeutic purposes on ATC cell lines. In this study, C643 and SW1736 were transducted by hsa-miR-21 antagomir (Off-miR-21). PTEN gene expression was performed as a known target of miR-21. Stemness state in cancer stem cells (CSCs) was evaluated by the changes of CSC biomarkers including Oct-4 and ABCG2. Apoptosis was assessed by PDCD4 and Mcl-1 gene expression and flow cytometry. Sodium/iodide symporter (NIS) and thyroglobulin (TG) were measured as ATC differentiation markers. In addition, cell cycle progression was investigated via the alterations of p21 gene expression and flow cytometry. Specific downregulation of miR-21 induced the differentiation and apoptosis in C643 and SW1736. Inversely, the treatment inhibited stemness state and cell cycle progression. Knockdown of miR-21 significantly increased the expression of PDCD4, p21, NIS, and TG while leading to decreased expression of Oct-4, ABCG2, and Mcl-1.Taken together, the results suggest that miR-21, as an oncomiR, has a role not only in stemness state but also in tumor growth, differentiation, and apoptosis. Hence, suppression of miR-21 could pave the way for ATC therapy.
Literature
1.
go back to reference Sipos J, Mazzaferri E. Thyroid cancer epidemiology and prognostic variables. Clin Oncol. 2010;22:395–404.CrossRef Sipos J, Mazzaferri E. Thyroid cancer epidemiology and prognostic variables. Clin Oncol. 2010;22:395–404.CrossRef
2.
go back to reference Davies L, Welch HG. Increasing incidence of thyroid cancer in the United States, 1973–2002. JAMA. 2006;295:2164–7.CrossRefPubMed Davies L, Welch HG. Increasing incidence of thyroid cancer in the United States, 1973–2002. JAMA. 2006;295:2164–7.CrossRefPubMed
3.
go back to reference Pierie J-PE, Muzikansky A, Gaz RD, Faquin WC, Ott MJ. The effect of surgery and radiotherapy on outcome of anaplastic thyroid carcinoma. Ann Surg Oncol. 2002;9:57–64.CrossRefPubMed Pierie J-PE, Muzikansky A, Gaz RD, Faquin WC, Ott MJ. The effect of surgery and radiotherapy on outcome of anaplastic thyroid carcinoma. Ann Surg Oncol. 2002;9:57–64.CrossRefPubMed
4.
go back to reference Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001;414:105–11.CrossRefPubMed Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001;414:105–11.CrossRefPubMed
5.
go back to reference Guo Z, Hardin H, Lloyd RV. Cancer stem-like cells and thyroid cancer. Endocr Relat Cancer. 2014;21:T285–300.CrossRefPubMed Guo Z, Hardin H, Lloyd RV. Cancer stem-like cells and thyroid cancer. Endocr Relat Cancer. 2014;21:T285–300.CrossRefPubMed
6.
go back to reference Ma R, Minsky N, Morshed SA, Davies TF. Stemness in human thyroid cancers and derived cell lines: the role of asymmetrically dividing cancer stem cells resistant to chemotherapy. J Clin Endocrinol Metab. 2014;99:E400–E9. Ma R, Minsky N, Morshed SA, Davies TF. Stemness in human thyroid cancers and derived cell lines: the role of asymmetrically dividing cancer stem cells resistant to chemotherapy. J Clin Endocrinol Metab. 2014;99:E400–E9.
8.
go back to reference Gao Y-J, Li B, Wu X-Y, Cui J, Han J-K. Thyroid tumor-initiating cells: increasing evidence and opportunities for anticancer therapy (review). Oncol Rep. 2014;31:1035–42.PubMedPubMedCentral Gao Y-J, Li B, Wu X-Y, Cui J, Han J-K. Thyroid tumor-initiating cells: increasing evidence and opportunities for anticancer therapy (review). Oncol Rep. 2014;31:1035–42.PubMedPubMedCentral
11.
go back to reference Riesco-Eizaguirre G, Santisteban P. A perspective view of sodium iodide symporter research and its clinical implications. Eur J Endocrinol. 2006;155:495–512.CrossRefPubMed Riesco-Eizaguirre G, Santisteban P. A perspective view of sodium iodide symporter research and its clinical implications. Eur J Endocrinol. 2006;155:495–512.CrossRefPubMed
12.
13.
go back to reference Song MS, Salmena L, Pandolfi PP. The functions and regulation of the PTEN tumour suppressor. Nat Rev Mol Cell Biol. 2012;13:283–96.PubMed Song MS, Salmena L, Pandolfi PP. The functions and regulation of the PTEN tumour suppressor. Nat Rev Mol Cell Biol. 2012;13:283–96.PubMed
14.
go back to reference Samimi H, Zaki dizaji M, Ghadami M, Shahzadeh fazeli A, Khashayar P, Soleimani M, et al. MicroRNAs networks in thyroid cancers: focus on miRNAs related to the fascin. J Diabetes MetabDisord. 2013;12:31. Samimi H, Zaki dizaji M, Ghadami M, Shahzadeh fazeli A, Khashayar P, Soleimani M, et al. MicroRNAs networks in thyroid cancers: focus on miRNAs related to the fascin. J Diabetes MetabDisord. 2013;12:31.
15.
go back to reference Selcuklu SD, Donoghue MA. Spillane C: miR-21 as a key regulator of oncogenic processes. Biochem Soc Trans. 2009;37:918–25.CrossRefPubMed Selcuklu SD, Donoghue MA. Spillane C: miR-21 as a key regulator of oncogenic processes. Biochem Soc Trans. 2009;37:918–25.CrossRefPubMed
16.
go back to reference Galderisi U, Cascino A, Giordano A. Antisense oligonucleotides as therapeutic agents. J Cell Physiol. 1999;181:251–7.CrossRefPubMed Galderisi U, Cascino A, Giordano A. Antisense oligonucleotides as therapeutic agents. J Cell Physiol. 1999;181:251–7.CrossRefPubMed
17.
go back to reference Naldini L, Blömer U, Gallay P, Ory D, Mulligan R, Gage FH, et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science. 1996;272:263–7.CrossRefPubMed Naldini L, Blömer U, Gallay P, Ory D, Mulligan R, Gage FH, et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science. 1996;272:263–7.CrossRefPubMed
18.
go back to reference Naderi M, Abdul TH, Soleimani M, Shabani I, Hashemi SM: A home-brew real-time PCR assay for reliable detection and quantification of mature miR-122. Appl Immunohistochem Mol Morphol 2014. Naderi M, Abdul TH, Soleimani M, Shabani I, Hashemi SM: A home-brew real-time PCR assay for reliable detection and quantification of mature miR-122. Appl Immunohistochem Mol Morphol 2014.
19.
go back to reference Samimi H, Zaki dizaji M, Ghadami M, Shahzadeh fazeli A, Khashayar P, Soleimani M, et al. Essential genes in thyroid cancers: focus on fascin. J Diabetes MetabDisord. 2013;12:32. Samimi H, Zaki dizaji M, Ghadami M, Shahzadeh fazeli A, Khashayar P, Soleimani M, et al. Essential genes in thyroid cancers: focus on fascin. J Diabetes MetabDisord. 2013;12:32.
21.
go back to reference Schweppe RE, Klopper JP, Korch C, Pugazhenthi U, Benezra M, Knauf JA, et al. 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. 2008;93:4331–41.CrossRefPubMedPubMedCentral Schweppe RE, Klopper JP, Korch C, Pugazhenthi U, Benezra M, Knauf JA, et al. 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. 2008;93:4331–41.CrossRefPubMedPubMedCentral
22.
go back to reference Meireles AM, Preto A, Rocha AS, Rebocho AP, Máximo V, Pereira-Castro I, et al. Molecular and genotypic characterization of human thyroid follicular cell carcinoma-derived cell lines. Thyroid. 2007;17:707–15.CrossRefPubMed Meireles AM, Preto A, Rocha AS, Rebocho AP, Máximo V, Pereira-Castro I, et al. Molecular and genotypic characterization of human thyroid follicular cell carcinoma-derived cell lines. Thyroid. 2007;17:707–15.CrossRefPubMed
23.
go back to reference Pilli T, Prasad KV, Jayarama S, Pacini F, Prabhakar BS. Potential utility and limitations of thyroid cancer cell lines as models for studying thyroid cancer. Thyroid. 2009;19:1333–42.CrossRefPubMedPubMedCentral Pilli T, Prasad KV, Jayarama S, Pacini F, Prabhakar BS. Potential utility and limitations of thyroid cancer cell lines as models for studying thyroid cancer. Thyroid. 2009;19:1333–42.CrossRefPubMedPubMedCentral
24.
go back to reference Altmann A, Markert A, Askoxylakis V, Schöning T, Jesenofsky R, Eisenhut M, et al. Antitumor effects of proteasome inhibition in anaplastic thyroid carcinoma. J Nucl Med. 2012;53:1764–71.CrossRefPubMed Altmann A, Markert A, Askoxylakis V, Schöning T, Jesenofsky R, Eisenhut M, et al. Antitumor effects of proteasome inhibition in anaplastic thyroid carcinoma. J Nucl Med. 2012;53:1764–71.CrossRefPubMed
25.
go back to reference Thomas T, Nowka K, Lan L, Derwahl M. Expression of endoderm stem cell markers: evidence for the presence of adult stem cells in human thyroid glands. Thyroid. 2006;16:537–44.CrossRefPubMed Thomas T, Nowka K, Lan L, Derwahl M. Expression of endoderm stem cell markers: evidence for the presence of adult stem cells in human thyroid glands. Thyroid. 2006;16:537–44.CrossRefPubMed
26.
go back to reference Niwa H, Miyazaki J-I, Smith AG. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet. 2000;24:372–6.CrossRefPubMed Niwa H, Miyazaki J-I, Smith AG. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet. 2000;24:372–6.CrossRefPubMed
27.
go back to reference Zheng X, Cui D, Xu S, Brabant G, Derwahl M. Doxorubicin fails to eradicate cancer stem cells derived from anaplastic thyroid carcinoma cells: characterization of resistant cells. Int J Oncol. 2010;37:307–15.CrossRefPubMed Zheng X, Cui D, Xu S, Brabant G, Derwahl M. Doxorubicin fails to eradicate cancer stem cells derived from anaplastic thyroid carcinoma cells: characterization of resistant cells. Int J Oncol. 2010;37:307–15.CrossRefPubMed
28.
go back to reference Fierabracci A. Identifying thyroid stem/progenitor cells: advances and limitations. J Endocrinol. 2012;213:1–13.CrossRefPubMed Fierabracci A. Identifying thyroid stem/progenitor cells: advances and limitations. J Endocrinol. 2012;213:1–13.CrossRefPubMed
29.
go back to reference Kogai T, Taki K, Brent G. Enhancement of sodium/iodide symporter expression in thyroid and breast cancer. Endocr Relat Cancer. 2006;13:797–826.CrossRefPubMed Kogai T, Taki K, Brent G. Enhancement of sodium/iodide symporter expression in thyroid and breast cancer. Endocr Relat Cancer. 2006;13:797–826.CrossRefPubMed
30.
go back to reference Lan L, Cui D, Nowka K, Derwahl M. Stem cells derived from goiters in adults form spheres in response to intense growth stimulation and require thyrotropin for differentiation into thyrocytes. J Clin Endocrinol Metab. 2007;92:3681–8.CrossRefPubMed Lan L, Cui D, Nowka K, Derwahl M. Stem cells derived from goiters in adults form spheres in response to intense growth stimulation and require thyrotropin for differentiation into thyrocytes. J Clin Endocrinol Metab. 2007;92:3681–8.CrossRefPubMed
31.
go back to reference Lankat-Buttgereit B, Göke R. Programmed cell death protein 4 (pdcd4): a novel target for antineoplastic therapy? Biol Cell. 2003;95:515–9.CrossRefPubMed Lankat-Buttgereit B, Göke R. Programmed cell death protein 4 (pdcd4): a novel target for antineoplastic therapy? Biol Cell. 2003;95:515–9.CrossRefPubMed
32.
go back to reference Asangani I, Rasheed S, Nikolova D, Leupold J, Colburn N, Post S, et al. MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene. 2008;27:2128–36.CrossRefPubMed Asangani I, Rasheed S, Nikolova D, Leupold J, Colburn N, Post S, et al. MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene. 2008;27:2128–36.CrossRefPubMed
33.
go back to reference Nijhawan D, Fang M, Traer E, Zhong Q, Gao W, Du F, et al. Elimination of Mcl-1 is required for the initiation of apoptosis following ultraviolet irradiation. Genes Dev. 2003;17:1475–86.CrossRefPubMedPubMedCentral Nijhawan D, Fang M, Traer E, Zhong Q, Gao W, Du F, et al. Elimination of Mcl-1 is required for the initiation of apoptosis following ultraviolet irradiation. Genes Dev. 2003;17:1475–86.CrossRefPubMedPubMedCentral
35.
39.
go back to reference Smallridge RC, Marlow LA, Copland JA. Anaplastic thyroid cancer: molecular pathogenesis and emerging therapies. Endocr Relat Cancer. 2009;16:17–44.CrossRefPubMed Smallridge RC, Marlow LA, Copland JA. Anaplastic thyroid cancer: molecular pathogenesis and emerging therapies. Endocr Relat Cancer. 2009;16:17–44.CrossRefPubMed
40.
go back to reference Nijhawan D, Fang M, Traer E, Zhong Q, Gao W, Du F, et al. Sorafenib inhibits intracellular signaling pathways and induces cell cycle arrest and cell death in thyroid carcinoma cells irrespective of histological origin or BRAF mutational status. BMC Cancer. 2015;15:184.CrossRef Nijhawan D, Fang M, Traer E, Zhong Q, Gao W, Du F, et al. Sorafenib inhibits intracellular signaling pathways and induces cell cycle arrest and cell death in thyroid carcinoma cells irrespective of histological origin or BRAF mutational status. BMC Cancer. 2015;15:184.CrossRef
Metadata
Title
Antisense-miR-21 enhances differentiation/apoptosis and reduces cancer stemness state on anaplastic thyroid cancer
Authors
Vahid Haghpanah
Parviz Fallah
Rezvan Tavakoli
Mahmood Naderi
Hilda Samimi
Masoud Soleimani
Bagher Larijani
Publication date
01-01-2016
Publisher
Springer Netherlands
Published in
Tumor Biology / Issue 1/2016
Print ISSN: 1010-4283
Electronic ISSN: 1423-0380
DOI
https://doi.org/10.1007/s13277-015-3923-z

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