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Metformin Inhibits Growth of Thyroid Carcinoma Cells, Suppresses Self-Renewal of Derived Cancer Stem Cells, and Potentiates the Effect of Chemotherapeutic Agents
Abstract
CONTEXT: Hyperinsulinemia and insulin resistance are the major reasons for a higher prevalence of several cancer entities in type 2 diabetes mellitus and obesity. Metformin exerts a growth-inhibitory effect by reducing hyperinsulinemia and by a direct cellular action. OBJECTIVE: We investigated the effect of metformin on growth of differentiated human thyroid cells, anaplastic thyroid carcinoma cells, a doxorubicin-resistant thyroid carcinoma cell line, and thyroid cancer stem cells. DESIGN: The antimitogenic effect of metformin was studied in thyroid cells derived from goiters and in thyroid carcinoma cell lines by analysis of cell growth, cell cycle progression, and apoptosis. Furthermore, the influence of pretreatment with insulin or with chemotherapeutic agents on metformin-induced growth inhibition was investigated in thyroid carcinoma cells, in a doxorubicin-resistant thyroid carcinoma cell line, and in derived carcinoma stem cells. RESULTS: Metformin showed an antimitogenic effect by inhibition of cell cycle progression and induction of apoptosis. In addition, metformin antagonized the growth-stimulatory effect of insulin, inhibited clonal cell growth, reduced thyroid cancer sphere formation, and potentiated the antimitogenic effect of chemotherapeutic agents such as doxorubicin and cisplatin on undifferentiated thyroid carcinoma cells. Remarkably, the antiproliferative effect of metformin was even found in a doxorubicin-resistant thyroid carcinoma cell line. The growth-inhibitory effect of metformin was, however, not restricted to differentiated thyroid cells and undifferentiated thyroid carcinoma cells but was also demonstrated in thyroid carcinoma cancer stem cells. CONCLUSIONS: Metformin markedly diminished growth stimulation by insulin and showed an additive antimitogenic effect to chemotherapeutics agents. Therefore, our results suggest this drug as adjuvant treatment for thyroid cancer in type 2 diabetic patients.
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“Recent studies have indicated that metformin might exert direct anticancer effects on a range of tumor cells, including the elusive CSCs,197,198”
From Drug repurposing for cancer therapy (2024) · cites this paper as [198]
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Cites
Metformin and reduced risk of cancer in diabetic patients
Evans, J. M. M., Donnelly, L. A., Emslie-Smith, A. M., Alessi, D. R., & Morris, A. D. (2005) · BMJ · doi:10.1136/bmj.38415.708634.f7 · Cited by 2,388
The Kinase LKB1 Mediates Glucose Homeostasis in Liver and Therapeutic Effects of Metformin
Shaw, R. J., Lamia, K. A., Vasquez, D., Koo, S.-H., Bardeesy, N., DePinho, R. A., Montminy, M., & Cantley, L. C. (2005) · Science · doi:10.1126/science.1120781 · Cited by 1,950
Hirsch, H. A., Iliopoulos, D., Tsichlis, P. N., & Struhl, K. (2009) · Cancer Research · doi:10.1158/0008-5472.can-09-2994 · Cited by 1,115
Metformin is an AMP kinase-dependent growth inhibitor for breast cancer cells
Zakikhani, M., Dowling, R., Fantus, I. G., Sonenberg, N., & Pollak, M. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-1500 · Cited by 1,048
Vigneri, P., Frasca, F., Sciacca, L., Pandini, G., & Vigneri, R. (2009) · Endocrine Related Cancer · doi:10.1677/erc-09-0087 · Cited by 1,009
Bowker, S. L., Majumdar, S. R., Veugelers, P., & Johnson, J. A. (2006) · Diabetes Care · doi:10.2337/diacare.29.02.06.dc05-1558 · Cited by 933
Dowling, R. J. O., Zakikhani, M., Fantus, I. G., Pollak, M., & Sonenberg, N. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-2310 · Cited by 933
Jiralerspong, S., Palla, S. L., Giordano, S. H., Meric-Bernstam, F., Liedtke, C., Barnett, C. M., Hsu, L., Hung, M.-C., Hortobagyi, G. N., & Gonzalez-Angulo, A. M. (2009) · Journal of Clinical Oncology · doi:10.1200/jco.2009.19.6410 · Cited by 880 · cited 3×
“Furthermore, retrospective analysis of data from neoadjuvant breast cancer therapy indicated that metformin may potentiate the effect of chemotherapy (7).”
BackgroundSahra, I. B., Laurent, K., Loubat, A., Giorgetti-Peraldi, S., Colosetti, P., Auberger, P., Tanti, J. F., Le Marchand-Brustel, Y., & Bost, F. (2008) · Oncogene · doi:10.1038/sj.onc.1211024 · Cited by 861
Metformin Associated With Lower Cancer Mortality in Type 2 Diabetes
Landman, G. W. D., Kleefstra, N., van Hateren, K. J. J., Groenier, K. H., Gans, R. O. B., & Bilo, H. J. G. (2010) · Diabetes Care · doi:10.2337/dc09-1380 · Cited by 502
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Pernicova, I., & Korbonits, M. (2014) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2013.256 · Cited by 1,393
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Biondi, B., Kahaly, G. J., & Robertson, R. P. (2019) · Endocrine Reviews · doi:10.1210/er.2018-00163 · Cited by 598
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“190,191 196 Recent studies have indicated that metformin might exert direct anticancer effects on a range of tumor cells, including the elusive CSCs, 197,198 thereby highlighting the multifaceted impact of metformin on cancer cells, as well as its potential to reduce phenotypic plasticity.”
BackgroundThe relationship between type 2 diabetes mellitus and related thyroid diseases
Wang, C. (2013) · Journal of Diabetes Research · doi:10.1155/2013/390534 · Cited by 273
Li, L., Han, R., Xiao, H., Lin, C., Wang, Y., Liu, H., Li, K., Chen, H., Sun, F., Yang, Z., et al. (2014) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-13-2613 · Cited by 240
Bahmad, H. F., Cheaito, K. A., Chalhoub, R., Hadadeh, O., Monzer, A., Ballout, F., Hajj, A. E., Mukherji, D., Liu, Y., Daoud, G., et al. (2018) · Frontiers in Oncology · doi:10.3389/fonc.2018.00347 · Cited by 209
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Hua, Y., Zheng, Y., Yao, Y., Jia, R., Ge, S., & Zhuang, A. (2023) · Journal of Translational Medicine · doi:10.1186/s12967-023-04263-8 · Cited by 220
Stevens, R. J., Ali, R., Bankhead, C. R., Bethel, M. A., Cairns, B. J., Camisasca, R. P., Crowe, F. L., Farmer, A. J., Harrison, S., Hirst, J. A., et al. (2012) · Diabetologia · doi:10.1007/s00125-012-2653-7 · Cited by 161
Metformin selectively affects human glioblastoma tumor-initiating cell viability
Würth, R., Pattarozzi, A., Gatti, M., Bajetto, A., Corsaro, A., Parodi, A., Sirito, R., Massollo, M., Marini, C., Zona, G., et al. (2012) · Cell Cycle · doi:10.4161/cc.23050 · Cited by 176
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Saini, N., & Yang, X. (2017) · Acta Biochimica et Biophysica Sinica · doi:10.1093/abbs/gmx106 · Cited by 180
Mao‐Ying, Q., Kavelaars, A., Krukowski, K., Huo, X., Zhou, W., Price, T. J., Cleeland, C. S., & Heijnen, C. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0100701 · Cited by 174
The Links Between Insulin Resistance, Diabetes, and Cancer
Orgel, E., & Mittelman, S. D. (2012) · Current Diabetes Reports · doi:10.1007/s11892-012-0356-6 · Cited by 168
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Eom, Y. S., Wilson, J. R., & Bernet, V. J. (2022) · Diabetes & Metabolism Journal · doi:10.4093/dmj.2022.0013 · Cited by 182
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Ma, J., Kavelaars, A., Dougherty, P. M., & Heijnen, C. J. (2018) · Cancer · doi:10.1002/cncr.31248 · Cited by 154
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Menéndez, J. A., Oliveras‐Ferraros, C., Cufí, S., Corominas-Faja, B., Joven, J., Martı́n-Castillo, B., & Vázquez‐Martín, A. (2012) · Cell Cycle · doi:10.4161/cc.20948 · Cited by 134
Gritti, M., Würth, R., Angelini, M., Barbieri, F., Peretti, M., Pizzi, E., Pattarozzi, A., Carra, E., Sirito, R., Daga, A., et al. (2014) · Oncotarget · doi:10.18632/oncotarget.2617 · Cited by 126
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Peng, M., Darko, K. O., Tao, T., Huang, Y., Su, Q., He, C., Yin, T., Liu, Z., & Yang, X. (2017) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2017.01.005 · Cited by 111
Yin, D., He, H., Yu, K., Xie, J., Lei, M., Ma, R., Li, H., Wang, Y., & Liu, Z. (2018) · International Journal of Surgery · doi:10.1016/j.ijsu.2018.07.013 · Cited by 110
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Korsse, S. E., Peppelenbosch, M. P., & van Veelen, W. (2012) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2012.12.006 · Cited by 107
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Kłubo-Gwieździńska, J., Costello, J. M., Patel, A. D., Bauer, A. J., Jensen, K. E., Mete, M., Burman, K. D., Wartofsky, L., & Vasko, V. V. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-3799 · Cited by 106
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Yang, J., Wei, J., Wu, Y., Wang, Z., Guo, Y., Lee, P. J., & Li, X. (2015) · Oncogenesis · doi:10.1038/oncsis.2015.18 · Cited by 101
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Han, B., Cui, H., Kang, L., Zhang, X., Jin, Z., Lu, L., & Fan, Z. (2015) · Tumor Biology · doi:10.1007/s13277-015-3315-4 · Cited by 100
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Kłubo-Gwieździńska, J., Jensen, K. E., Costello, J. M., Patel, A. D., Hoperia, V., Bauer, A. J., Burman, K. D., Wartofsky, L., & Vasko, V. V. (2012) · Endocrine Related Cancer · doi:10.1530/erc-12-0046 · Cited by 92
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Rotondi, M., Coperchini, F., Latrofa, F., & Chiovato, L. (2018) · Frontiers in Endocrinology · doi:10.3389/fendo.2018.00314 · Cited by 77
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Yang, Y., Mauldin, P. D., Ebeling, M. D., Hulsey, T. C., Liu, B., Thomas, M. B., Camp, E. R., & Esnaola, N. F. (2012) · Cancer · doi:10.1002/cncr.27923 · Cited by 79
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Nishi, M. (2018) · Diabetology International · doi:10.1007/s13340-018-0352-4 · Cited by 73
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Harada, K., Ferdous, T., Harada, T., & Ueyama, Y. (2016) · International Journal of Oncology · doi:10.3892/ijo.2016.3523 · Cited by 66
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Mimeault, M., & Batra, S. K. (2013) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2013.08.001 · Cited by 65
Ling, S., Feng, T., Ke, Q., FAN, N., Li, L., Li, Z., Dong, C., WANG, C., Xu, F., Li, Y., et al. (2014) · Oncology Reports · doi:10.3892/or.2014.3151 · Cited by 62
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Thakur, S., Daley, B., & Kłubo-Gwieździńska, J. (2019) · Journal of Molecular Endocrinology · doi:10.1530/jme-19-0083 · Cited by 66
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Plews, R. L., Yusof, A. M., Wang, C., Saji, M., Zhang, X., Chen, C., Ringel, M. D., & Phay, J. E. (2015) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-1777 · Cited by 62
Blanc, E., Ponce, C., Brodschi, D., Nepote, A., Barreto, A., Schnitman, M., Fossati, P., Salgado, P., Cejas, C. P., Faingold, C., et al. (2015) · Metabolic Syndrome and Related Disorders · doi:10.1089/met.2014.0158 · Cited by 59
Glucose-deprivation increases thyroid cancer cells sensitivity to metformin
Bikas, A., Jensen, K. E., Patel, A. D., Costello, J. M., McDaniel, D. P., Kłubo-Gwieździńska, J., Ларін, О. С., Hoperia, V., Burman, K. D., Boyle, L., et al. (2015) · Endocrine Related Cancer · doi:10.1530/erc-15-0402 · Cited by 63
Barbieri, F., Thellung, S., Ratto, A., Carra, E., Marini, V., Fucile, C., Bajetto, A., Pattarozzi, A., Würth, R., Gatti, M., et al. (2015) · BMC Cancer · doi:10.1186/s12885-015-1235-8 · Cited by 61
Liu, M., Zhang, Z., Wang, H., Chen, X., & Jin, C. (2019) · International Journal of Biological Sciences · doi:10.7150/ijbs.29689 · Cited by 57
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Xiao, Z., Sperl, B., Ullrich, A., & Knyazev, P. G. (2014) · Oncotarget · doi:10.18632/oncotarget.2657 · Cited by 55
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Cho, S. W., Yi, K. H., Han, S. K., Sun, H. J., Kim, Y. A., Oh, B., Park, Y. J., & Park, D. J. (2014) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2014.05.021 · Cited by 46
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Abdulrahman, R. M., Boon, M. R., Sips, H. C. M., Guigas, B., Rensen, P. C. N., Smit, J. W. A., & Hovens, G. C. (2013) · Thyroid · doi:10.1089/thy.2013.0041 · Cited by 33
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He, X., Wu, D., Hu, C., Xu, T., Liu, Y., Liu, C., Xu, B., & Tang, W. (2018) · Thyroid · doi:10.1089/thy.2017.0707 · Cited by 35
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Becker, C., Jick, S. S., Meier, C. R., & Bodmer, M. (2015) · BMC Cancer · doi:10.1186/s12885-015-1719-6 · Cited by 32
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Metadata
- Authors
- Chen, G., Xu, S., Renko, K., & Derwahl, M.
- Affiliations
- St. Hedwig-Krankenhaus (DE)
- Charité – Universitätsmedizin Berlin (DE)
- Corresponding author
- Derwahl, Michael
- Venue
- The Journal of Clinical Endocrinology & Metabolism
- Publisher
- The Endocrine Society
- Published
- 2012-04
- Volume
- 97
- Issue
- 4
- Pages
- E510-E520
- ISSN
- 0021-972X (ISSN-L)
- 1945-7197
- OpenAlex
- W2124231104
- Cited by
- 196
- References
- 32
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 11 · 2023: 15 · 2022: 14 · 2021: 6 · 2020: 11 · 2019: 13 · 2018: 18 · 2017: 15 · 2016: 12 · 2015: 19 · 2014: 19 · 2013: 15 · 2012: 17
- FWCI
- 8.98
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Clinical Endocrinology & Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Government of Jiangsu Province
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Thyroid Cancer Diagnosis and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Keywords
- metformin, thyroid cancer, cancer stem cells, self-renewal, doxorubicin resistance, cisplatin, chemosensitization, insulin resistance, hyperinsulinemia, type 2 diabetes, apoptosis, cell cycle arrest, cell growth inhibition, adjuvant therapy
- MeSH terms
- Animals, Antineoplastic Agents, Carcinoma, Cell Cycle, Cell Differentiation, Cell Line, Goiter, Nodular, Humans, Hypoglycemic Agents, Insulin, Insulin Antagonists, Metformin, Thyroid Neoplasms, Tumor Cells, Cultured, Neoplastic Stem Cells, Apoptosis, Adenocarcinoma, Follicular, Drug Resistance, Neoplasm, Cell Line, Tumor, Cell Proliferation, Rats, Thyroid Carcinoma, Anaplastic
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