Molecular profiles of cancer stem-like cell populations in aggressive thyroid cancers

Endocrine

Volumn 53, Issue 1, 2016, Pages 145-156

  Dima, Mariavittoria ^a   Pecce, Valeria ^a   Biffoni, Mauro ^b   Di Gioia, Cira Rosaria Tiziana ^a   Tallini, Giovanni ^c   Biffoni, Marco ^a   Rosignolo, Francesca ^a   Verrienti, Antonella ^a   Sponziello, Marialuisa ^a   Damante, Giuseppe ^d   Russo, Diego ^e   Durante, Cosimo ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^c UNIVERSITY OF BOLOGNA   (Italy)

^d UNIVERSITY OF UDINE   (Italy)

^e UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

Author keywords

Cancer stem cells; Drug resistance; Epithelial mesenchymal transition; Metastatic thyroid cancer

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALPHA FETOPROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CHORIONIC GONADOTROPIN; CRIZOTINIB; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; HEPATOCYTE NUCLEAR FACTOR 3BETA; IODINE 131; OCTAMER TRANSCRIPTION FACTOR 4; PLATELET DERIVED GROWTH FACTOR B; PROTEIN TYROSINE KINASE A; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR OTX2; TRANSCRIPTION FACTOR PAX8; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR SOX17; TRANSCRIPTION FACTOR SOX2; TYROSINE KINASE RECEPTOR; UVOMORULIN; VASCULOTROPIN RECEPTOR 2; PYRAZOLE DERIVATIVE; PYRIDINE DERIVATIVE; TUMOR MARKER;

ACTB GENE; ADVANCED CANCER; ARTICLE; B2 M GENE; CANCER GROWTH; CANCER STEM CELL; CELL DENSITY; CELL POPULATION; CELL PROLIFERATION; CELL RENEWAL; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EPITHELIAL MESENCHYMAL TRANSITION; EXON; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GADPH GENE; GENE EXPRESSION; HOUSEKEEPING GENE; HRPT1 GENE; HUMAN; HUMAN TISSUE; LYMPH NODE METASTASIS; METASTASIS POTENTIAL; ONCOGENE BRAF; ONCOGENE H RAS; ONCOGENE K RAS; ONCOGENE N RAS; ONCOGENE PTEN; ONCOGENE TP53; POORLY DIFFERENTIATED THYROID CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; PROTO ONCOGENE; RADIOISOTOPE THERAPY; THYROID CANCER; THYROID CARCINOMA; THYROID CELL; THYROID PAPILLARY CARCINOMA; THYROSPHERE; DRUG EFFECTS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; THYROID GLAND; THYROID TUMOR; TUMOR CELL LINE;

ALDEHYDE DEHYDROGENASE; BIOMARKERS, TUMOR; CELL LINE, TUMOR; CELL PROLIFERATION; HUMANS; NEOPLASTIC STEM CELLS; PHOSPHORYLATION; PYRAZOLES; PYRIDINES; THYROID GLAND; THYROID NEOPLASMS;

EID: 84941662549     PISSN: 1355008X     EISSN: 15590100     Source Type: Journal    
DOI: 10.1007/s12020-015-0739-y     Document Type: Article

References (49)

1. C. Durante, N. Haddy, E. Baudin, S. Leboulleux, D. Hartl, J.P. Travagli, B. Caillou, M. Ricard, J.D. Lumbroso, F. De Vathaire et al., Long-term outcome of 444 patients with distant metastases from papillary and follicular thyroid carcinoma: benefits and limits of radioiodine therapy. J. Clin. Endocrinol. Metab. 91, 2892–2899 (2006)
2. M. Schlumberger, L. Lacroix, D. Russo, S. Filetti, J.M. Bidart, Defects in iodide metabolism in thyroid cancer and implications for the follow-up and treatment of patients. Nat. Clin. Pract. Endocrinol. Metab. 3, 260–269 (2007)
3. F. Arturi, D. Russo, D. Giuffrida, M. Schlumberger, S. Filetti, Sodium–iodide symporter (NIS) gene expression in lymph-node metastases of papillary thyroid carcinomas. Eur. J. Endocrinol. 143, 623–627 (2000)
4. F. Arturi, D. Russo, J.M. Bidart, D. Scarpelli, M. Schlumberger, S. Filetti, Expression pattern of the pendrin and sodium/iodide symporter (NIS) gene in human thyroid carcinoma cell lines and human thyroid tumors. Eur. J. Endocrinol. 145, 129–135 (2001)
5. T. Kogai, G.A. Brent, The sodium iodide symporter (NIS): regulation and approaches to targeting for cancer therapeutics. Pharmacol. Ther. 135, 355–370 (2013)
6. D. Russo, G. Damante, E. Puxeddu, C. Durante, S. Filetti, Epigenetics of thyroid cancer and novel therapeutic targets. J. Mol. Endocrinol. 46, R73–R81 (2011)
7. M. Xing, Molecular pathogenesis and mechanisms of thyroid cancer. Nat. Rev. Cancer 13, 184–199 (2013)
8. J.P. Thiery, Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer 2, 442–454 (2002)
9. T. Reya, S.J. Morrison, M.F. Clarke, I.L. Weissman, Stem cells, cancer, and cancer stem cells. Nature 414, 105–111 (2001)
10. T. Brabletz, A. Jung, S. Spaderna, F. Hlubek, T. Kirchner, Migrating cancer stem cells—an integrated concept of malignant tumour progression. Nat. Rev. Cancer 5, 744–749 (2005)
11. Z. Guo, H. Hardin, R.V. Lloyd, Cancer stem-like cells and thyroid cancer. Endocr. Relat. Cancer 21, T285–T300 (2014)
12. H. Hardin, C. Montemayor-Garcia, R.V. Lloyd, Thyroid cancer stem-like cells and epithelial-mesenchymal transition in thyroid cancers. Hum. Pathol. 44, 1707–1713 (2013)
13. M. Todaro, F. Iovino, V. Eterno, P. Cammareri, G. Gambara, V. Espina, G. Gulotta, F. Dieli, S. Giordano, R. De Maria, G. Stassi, Tumorigenic and metastatic activity of human thyroid cancer stem cells. Cancer Res. 70, 8874–8885 (2010)
14. Y. Qin, C. Capaldo, B.M. Gumbiner, I.G. Macara, The mammalian Scribble polarity protein regulates epithelial cell adhesion and migration through E-cadherin. J. Cell Biol. 171, 1061–1071 (2005)
15. S.A. Mani, W. Guo, M. Liao, E.N. Eaton, A.Y. Zhou, M. Brooks, F. Reinhard, C.C. Zhang, L.L. Campbell, K. Polyak, C. Brisken, J. Yang, R.A. Weinberg, The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133, 704–715 (2008)
16. Thyroid American Joint Committee on Cancer 2002: AJCC Cancer Staging Man. pp. 77–87 (2010)
17. M.D. Castellone, A. Verrienti, D. Magendra Rao, M. Sponziello, D. Fabbro, M. Muthu, C. Durante, M. Maranghi, G. Damante, S. Pizzolitto, G. Costante, D. Russo, M. Santoro, S. Filetti, A novel de novo germ-line V292M mutation in the extracellular region of RET in a patient with phaeochromocytoma and medullary thyroid carcinoma: functional characterization. Clin. Endocrinol. 73, 529–534 (2010)
18. F. Rosignolo, V. Maggisano, M. Sponziello, M. Celano, C.R. Di Gioia, M. D’Agostino, L. Giacomelli, A. Verrienti, M. Dima, V. Pecce, C. Durante, Reduced expression of THRβ in papillary thyroid carcinomas: relationship with BRAF mutation, aggressiveness and miR expression. J. Endocrinol. Invest. (2015). doi:10.1007/s40618-015-0309-4
19. L. Khandrika, F.J. Kim, A. Campagna, S. Koul, R.B. Meacham, H.K. Koul, Primary culture and characterization of human renal inner medullary collecting duct epithelial cells. J. Urol. 179, 2057–2063 (2008)
20. A. Hague, C. Paraskeva, The intestinal epithelial cell, in Epithelial Cell Culture, ed. by A. Harris (Cambridge University Press, New York, 1996), pp. 25–41
21. L. Ricci-Vitiani, D.G. Lombardi, E. Pilozzi, M. Biffoni, M. Todaro, C. Peschle, R. De Maria, Identification and expansion of human colon-cancer-initiating cells. Nature 445, 111–115 (2007)
22. M. Todaro, M.P. Alea, A.B. Di Stefano, P. Cammareri, L. Vermeulen, F. Iovino, C. Tripodo, A. Russo, G. Gulotta, J.P. Medema, G. Stassi, Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell 1, 389–402 (2007)
23. M. Sponziello, E. Lavarone, E. Pegolo, C. Di Loreto, C. Puppin, M. Russo, R. Bruno, S. Filetti, C. Durante, D. Russo, A. Di Cristofano, G. Damante, Molecular differences between human thyroid follicular adenoma and carcinoma revealed by analysis of a murine model of thyroid cancer. Endocrinology. 154, 3043–3053 (2013)
24. Y. Zhou, C. Zhao, S. Gery, G.D. Braunstein, R. Okamoto, R. Alvarez, S.A. Miles, N.B. Doan, J.W. Said, J. Gu, H. Phillip Koeffler, Off-target effects of c-MET inhibitors on thyroid cancer cells. Mol. Cancer Ther. 13, 134–143 (2014)
25. M.M. Nociari, A. Shalev, P. Benias, C. Russo, A novel one-step, highly sensitive fluorometric assay to evaluate cell-mediated cytotoxicity. J. Immunol. Methods 213, 157–167 (1998)
26. E.H. Huang, M.J. Hynes, T. Zhang, C. Ginestier, G. Dontu, H. Appelman, J.Z. Fields, M.S. Wicha, B.M. Boman, Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res. 69, 3382–3389 (2009)
27. J.L. Dembinski, S. Krauss, Characterization and functional analysis of a slow cycling stem cell-like subpopulation in pancreas adenocarcinoma. Clin. Exp. Metastasis 26, 611–623 (2009)
28. C. van den Hoogen, G. van der Horst, H. Cheung, J.T. Buijs, J.M. Lippitt, N. Guzmán-Ramírez, F.C. Hamdy, C.L. Eaton, G.N. Thalmann, M.G. Cecchini, R.C.M. Pelger, G. van der Pluijm, High aldehyde dehydrogenase activity identifies tumor-initiating and metastasis-initiating cells in human prostate cancer. Cancer Res. 70, 5163–5173 (2010)
29. L.P. Fernández, A. López-Márquez, P. Santisteban, Thyroid transcription factors in development, differentiation and disease. Nat. Rev. Endocrinol. 11, 29–42 (2015)
30. H.R. Kim, W.S. Kim, Y.J. Choi, C.M. Choi, J.K. Rho, J.C. Lee, Epithelial-mesenchymal transition leads to crizotinib resistance in H2228 lung cancer cells with EML4-ALK translocation. Mol. Oncol. 7, 1093–1102 (2013)
31. S. Thomson, F. Petti, I. Sujka-Kwok, P. Mercado, J. Bean, M. Monaghan, S.L. Seymour, G.M. Argast, D.M. Epstein, J.D. Haley, A systems view of epithelial–mesenchymal transition signaling states. Clin. Exp. Metastasis 28, 137–155 (2010)
32. C. Holz, F. Niehr, M. Boyko, T. Hristozova, L. Distel, V. Budach, I. Tinhofer, Epithelial-mesenchymal-transition induced by EGFR activation interferes with cell migration and response to irradiation and cetuximab in head and neck cancer cells. Radiother. Oncol. 101, 158–164 (2011)
33. I. Cañadas, F. Rojo, Á. Taus, O. Arpí, M. Arumí-Uría, L. Pijuan, S. Menéndez, S. Zazo, M. Dómine, M. Salido, S. Mojal, A. García de Herreros, A. Rovira, J. Albanell, E. Arriola, Targeting epithelial-to-mesenchymal transition with Met inhibitors reverts chemoresistance in small cell lung cancer. Clin. Cancer Res. 20, 938–950 (2014)
34. H.Y. Zou, Q. Li, J.H. Lee, M.E. Arango, S.R. McDonnell, S. Yamazaki, T.B. Koudriakova, G. Alton, J.J. Cui, P.P. Kung, M.D. Nambu, G. Los, S.L. Bender, B. Mroczkowski, J.G. Christensen, An orally available small-molecule inhibitor of c-Met, PF-2341066, exhibits cytoreductive antitumor efficacy through antiproliferative and antiangiogenic mechanisms. Cancer Res. 67, 4408–4417 (2007)
35. Drug Evaluation: Center for Drug Evaluation and Pharmacology Review (S). http://www.accessdata.fda.gov/drugsatfda_docs/nda/2011/202570Orig1s000PharmR.pdf (2011)
36. U. Hinterseher, A. Wunderlich, S. Roth, A. Ramaswamy, D.K. Bartsch, S. Hauptmann, B.H. Greene, V. Fendrich, S. Hoffmann, Expression of hedgehog signalling pathway in anaplastic thyroid cancer. Endocrine 45, 439–447 (2014)
37. S.M. Rodriguez-Pinilla, D. Sarrio, G. Moreno-Bueno, Y. Rodriguez-Gil, M. Martinez, L. Hernandez, D. Hardisson, J.S. Reis-Filho, J. Palacios, Sox2: a possible driver of the basal-like phenotype in sporadic breast cancer. Mod. Pathol. 20, 474–481 (2007)
38. R.M.R. Gangemi, F. Griffero, D. Marubbi, M. Perera, M.C. Capra, P. Malatesta, G.L. Ravetti, G.L. Zona, A. Daga, G. Corte, SOX2 silencing in glioblastoma tumor-initiating cells causes stop of proliferation and loss of tumorigenicity. Stem Cells 27, 40–48 (2009)
39. H. Ikushima, T. Todo, Y. Ino, M. Takahashi, K. Miyazawa, K. Miyazono, Autocrine TGF-beta signaling maintains tumorigenicity of glioma-initiating cells through Sry-related HMG-box factors. Cell Stem Cell 5, 504–514 (2009)
40. A.C. Laga, C.-Y. Lai, Q. Zhan, S.J. Huang, E.F. Velazquez, Q. Yang, M.-Y. Hsu, G.F. Murphy, Expression of The Embryonic Stem Cell Transcription Factor SOX2 in Human Skin. Am. J. Pathol. 176, 903–913 (2010)
41. V. Carina, G. Zito, G. Pizzolanti, P. Richiusa, A. Criscimanna, V. Rodolico, L. Tomasello, M. Pitrone, W. Arancio, C. Giordano, Multiple pluripotent stem cell markers in human anaplastic thyroid cancer: the putative upstream role of SOX2. Thyroid 23, 829–837 (2013)
42. R. Jauch, I. Aksoy, A.P. Hutchins, C.K.L. Ng, X.F. Tian, J. Chen, P. Palasingam, P. Robson, L.W. Stanton, P.R. Kolatkar, Conversion of Sox17 into a pluripotency reprogramming factor by reengineering its association with Oct4 on DNA. Stem Cells 29, 940–951 (2011)
43. I. Aksoy, R. Jauch, J. Chen, M. Dyla, U. Divakar, G.K. Bogu, R. Teo, C. Keow, L. Ng, W. Herath, S. Lili, P. Hutchins, P. Robson, P.R. Kolatkar, L.W. Stanton, Oct4 switches partnering from Sox2 to Sox17 to reinterpret the enhancer code and specify endoderm. EMBO J. 32, 938–953 (2013)
44. Y. Chao, Q. Wu, C. Shepard, A. Wells, Hepatocyte induced re-expression of E-cadherin in breast and prostate cancer cells increases chemoresistance. Clin. Exp. Metastasis 29, 39–50 (2012)
45. Y. Chao, Q. Wu, M. Acquafondata, R. Dhir, A. Wells, Partial mesenchymal to epithelial reverting transition in breast and prostate cancer metastases. Cancer Microenviron. 5, 19–28 (2012)
46. T. Sasaki, J. Koivunen, A. Ogino, M. Yanagita, S. Nikiforow, W. Zheng, C. Lathan, J.P. Marcoux, J. Du, K. Okuda, M. Capelletti, T. Shimamura, D. Ercan, M. Stumpfova, Y. Xiao, S. Weremowicz, M. Butaney, S. Heon, K. Wilner, J.G. Christensen, M.J. Eck, K.-K. Wong, N. Lindeman, N.S. Gray, S.J. Rodig, P. aJänne, A novel ALK secondary mutation and EGFR signaling cause resistance to ALK kinase inhibitors. Cancer Res. 71, 6051–6060 (2011)
47. R. Katayama, A.T. Shaw, T.M. Khan, M. Mino-kenudson, B.J. Solomon, B. Halmos, N.A. Jessop, J.C. Wain, A. Tien, C. Benes, L. Drew, J.C. Saeh, K. Crosby, V. Lecia, A.J. Iafrate, J.A. Engelman, Mechanisms of acquired crizotinib resistance in ALK- rearranged lung cancers. Sci. Transl. Med. 4, 1–25 (2012)
48. J. Tanizaki, I. Okamoto, T. Okabe, K. Sakai, K. Tanaka, H. Hayashi, H. Kaneda, K. Takezawa, K. Kuwata, H. Yamaguchi, E. Hatashita, K. Nishio, K. Nakagawa, Activation of HER family signaling as a mechanism of acquired resistance to ALK inhibitors in EML4-ALK-positive non-small cell lung cancer. Clin. Cancer Res. 18, 6219–6226 (2012)
49. A. Wunderlich, S. Roth, A. Ramaswamy, B.H. Greene, I.C. Brende, U. Hinterseher, D.K. Bartsch, S. Hoffmann, Combined inhibition of cellular pathways as a future therapeutic option in fatal anaplastic thyroid cancer. Endocrine 42, 637–646 (2012)