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Open AccessArticle

Patient-Derived Papillary Thyroid Cancer Organoids for Radioactive Iodine Refractory Screening

1
Department of Surgical Oncology, University of Groningen, University Medical Center Groningen, 9713 GZ Groningen, The Netherlands
2
Department of Biomedical Sciences of Cell & Systems–Section Molecular Cell Biology, University of Groningen, University Medical Center Groningen, 9700 RB Groningen, The Netherlands
3
Department of Radiation Oncology, University of Groningen, University Medical Center Groningen, 9700 RB Groningen, The Netherlands
4
Department of Surgery, Martini Hospital, 9728 NT Groningen, The Netherlands
5
Department of Surgery, Treant Hospital, 7909 AA Hoogeveen, The Netherlands
6
Department of Endocrinology, University of Groningen, University Medical Center Groningen, 9700 RB Groningen, The Netherlands
*
Authors to whom correspondence should be addressed.
These authors contributed equally to this work.
These authors contributed equally to this work.
Cancers 2020, 12(11), 3212; https://doi.org/10.3390/cancers12113212
Received: 29 September 2020 / Revised: 22 October 2020 / Accepted: 29 October 2020 / Published: 31 October 2020
(This article belongs to the Special Issue Cancer Organoids in Basic Science and Translational Medicine)
Over the past three decades, the incidence of thyroid cancer has been rising, with 90% being the well-differentiated thyroid cancer subtype. After diagnosis and surgical removal of the thyroid gland, radioactive iodine is administered to induce a localized post-operative radiation treatment. However, in 15-33% of papillary thyroid cancer cases, the cells are unable to take up radioactive iodine, resulting in an ineffective treatment which sometimes has severe side effects. Pre-treatment diagnosis of non-responding patients would prevent ineffective and toxic iodine treatment. Therefore, in this study, we developed a patient-derived papillary thyroid cancer organoid model. Patient-derived organoids responding or not responding to radioactive iodine clearly resembled the tumor of origin, but showed clear differences in sodium/iodide symporter expression. Our results indicate that thyroid cancer organoids might be a suitable tool for the early diagnosis of non-responding patients, in order to eventually reduce radioactive iodine overtreatment and its many side effects for thyroid cancer patients.
Patients with well-differentiated thyroid cancer, especially papillary thyroid cancer (PTC), are treated with surgical resection of the thyroid gland. This is followed by post-operative radioactive iodine (I131), resulting in total thyroid ablation. Unfortunately, about 15-33% of PTC patients are unable to take up I131, limiting further treatment options. The aim of our study was to develop a cancer organoid model with the potential for pre-treatment diagnosis of these I131-resistant patients. PTC tissue from thirteen patients was used to establish a long-term organoid model. These organoids showed a self-renewal potential for at least five passages, suggesting the presence of cancer stem cells. We demonstrated that thyroid specific markers, a PTC marker, and transporters/receptors necessary for iodine uptake and thyroid hormone production were expressed on a gene and protein level. Additionally, we cultured organoids from I131-resistant PTC material from three patients. When comparing PTC organoids to radioactive iodine (RAI)-refractory disease (RAIRD) organoids, a substantial discordance on both a protein and gene expression level was observed, indicating a treatment prediction potential. We showed that patient-derived PTC organoids recapitulate PTC tissue and a RAIRD phenotype. Patient-specific PTC organoids may enable the early identification of I131-resistant patients, in order to reduce RAI overtreatment and its many side effects for thyroid cancer patients. View Full-Text
Keywords: patient-derived tumor organoids; three-dimensional culture; tumor organoids; papillary thyroid carcinoma; cancer stem cells; treatment prediction; RAI therapy patient-derived tumor organoids; three-dimensional culture; tumor organoids; papillary thyroid carcinoma; cancer stem cells; treatment prediction; RAI therapy
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MDPI and ACS Style

Sondorp, L.H.J.; Ogundipe, V.M.L.; Groen, A.H.; Kelder, W.; Kemper, A.; Links, T.P.; Coppes, R.P.; Kruijff, S. Patient-Derived Papillary Thyroid Cancer Organoids for Radioactive Iodine Refractory Screening. Cancers 2020, 12, 3212. https://doi.org/10.3390/cancers12113212

AMA Style

Sondorp LHJ, Ogundipe VML, Groen AH, Kelder W, Kemper A, Links TP, Coppes RP, Kruijff S. Patient-Derived Papillary Thyroid Cancer Organoids for Radioactive Iodine Refractory Screening. Cancers. 2020; 12(11):3212. https://doi.org/10.3390/cancers12113212

Chicago/Turabian Style

Sondorp, Luc H.J.; Ogundipe, Vivian M.L.; Groen, Andries H.; Kelder, Wendy; Kemper, Annelies; Links, Thera P.; Coppes, Robert P.; Kruijff, Schelto. 2020. "Patient-Derived Papillary Thyroid Cancer Organoids for Radioactive Iodine Refractory Screening" Cancers 12, no. 11: 3212. https://doi.org/10.3390/cancers12113212

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