Endocrinology and Metabolism

Original Articles

Thyroid
BRAF^V600E Mutation Enhances Estrogen-Induced Metastatic Potential of Thyroid Cancer by Regulating the Expression of Estrogen Receptors: Minjun Kim, Su-jin Kim, Seong Yun Ha, Zhen Xu, Youngjin Han, Hyeon-Gun Jee, Sun Wook Cho, Young Joo Park, Kyu Eun Lee; Endocrinol Metab. 2022;37(6):879-890. Published online December 26, 2022; DOI: https://doi.org/10.3803/EnM.2022.1563

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Background
Cross-talk between mitogen-activated protein kinase and estrogen has been reported; however, the role of BRAF^V600E in the estrogen responsiveness of thyroid cancer is unknown. We elucidated the effect of BRAF^V600E on the estrogen-induced increase in metastatic potential in thyroid cancer.
Methods
Using a pair of cell lines, human thyroid cell lines which harbor wild type BRAF gene (Nthy/WT) and Nthy/BRAF^V600E (Nthy/V600E), the expression of estrogen receptors (ERs) and estrogen-induced metastatic phenotypes were evaluated. Susceptibility to ERα- and ERβ-selective agents was evaluated to confirm differential ER expression. ESR expression was analyzed according to BRAF^V600E status and age (≤50 years vs. >50 years) using The Cancer Genome Atlas (TCGA) data.
Results
Estradiol increased the ERα/ERβ expression ratio in Nthy/V600E, whereas the decreased ERα/ERβ expression ratio was found in Nthy/WT. BRAF^V600E-mutated cell lines showed a higher E2-induced increase in metastatic potential, including migration, invasion, and anchorage-independent growth compared with Nthy/WT. An ERα antagonist significantly inhibited migration in Nthy/V600E cells, whereas an ERβ agonist was more effective in Nthy/WT. In the BRAF^V600E group, ESR1/ESR2 ratio was significantly higher in younger age group (≤50 years) compared with older age group (>50 years) by TCGA data analysis.
Conclusion
Our data show that BRAF^V600E mutation plays a crucial role in the estrogen responsiveness of thyroid cancer by regulating ER expression. Therefore, BRAF^V600E might be used as a biomarker when deciding future hormone therapies based on estrogen signaling in thyroid cancer patients.

Citations

Citations to this article as recorded by

The importance of protein domain mutations in cancer therapy
Kiran Kumar Chitluri, Isaac Arnold Emerson
Heliyon.2024; 10(6): e27655. CrossRef
Three cases of thyroid cancer in transgender female veterans receiving gender-affirming estrogen treatment
John D. Christensen, Hiba T. Basheer
Endocrine and Metabolic Science.2024; 15: 100177. CrossRef
Thyroid Cancer Prevalence, Risk Exposure, and Clinical Features Among Transgender Female Veterans
John David Christensen, Hiba T Basheer, Jose Joaquin Lado Abeal
Journal of the Endocrine Society.2024;[Epub] CrossRef
Association of DNA Promoter Methylation and BRAF Mutation in Thyroid Cancer
Farzana Jasmine, Briseis Aschebrook-Kilfoy, Mohammad M. Rahman, Garrett Zaagman, Raymon H. Grogan, Mohammed Kamal, Habibul Ahsan, Muhammad G. Kibriya
Current Oncology.2023; 30(3): 2978. CrossRef
Editorial: Recent advances in papillary thyroid carcinoma: Progression, treatment and survival predictors
Erivelto Martinho Volpi, Margarita Carmen Ramirez-Ortega, Jose Federico Carrillo
Frontiers in Endocrinology.2023;[Epub] CrossRef

Clinical Study
Molecular Correlates and Nuclear Features of Encapsulated Follicular-Patterned Thyroid Neoplasms: Chan Kwon Jung, Andrey Bychkov, Dong Eun Song, Jang-Hee Kim, Yun Zhu, Zhiyan Liu, Somboon Keelawat, Chiung-Ru Lai, Mitsuyoshi Hirokawa, Kaori Kameyama, Kennichi Kakudo; Endocrinol Metab. 2021;36(1):123-133. Published online February 24, 2021; DOI: https://doi.org/10.3803/EnM.2020.860

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Background
Assessing nuclear features is diagnostically challenging in the aspect of thyroid pathology. The aim of this study was to determine whether pathologists could distinguish BRAF-like and RAS-like nuclear features morphologically and identify morphological features to differentiate thyroid tumors with RAS-like mutations from encapsulated papillary thyroid carcinoma (PTC) with predominant follicular growth and BRAFV^600E mutation.
Methods
Representative whole slide images of 16 encapsulated thyroid tumors with predominant follicular growth were reviewed by 12 thyroid pathologists using a web browser-based image viewer. Total nuclear score was calculated from semi-quantitatively scored eight nuclear features. The molecular profile of RAS and BRAF genes was determined by Sanger sequencing.
Results
Total nuclear score ranging 0 to 24 could differentiate BRAF-like tumors from RAS-like tumors with a cut-off value of score 14. The interobserver agreement was the highest for the assessment of nuclear pseudoinclusions (NPIs) but the lowest for nuclear elongation and sickle-shaped nuclei. NPIs were found in tumors with BRAFV^600E mutation, but not in tumors with RAS-like mutations. Total nuclear scores were significantly higher for tumors with BRAFV^600E than for those with RAS-like mutations (P<0.001).
Conclusion
Our results suggest that NPIs and high nuclear scores have diagnostic utility as rule-in markers for differentiating PTC with BRAFV^600E mutation from benign or borderline follicular tumors with RAS-like mutations. Relaxation of rigid criteria for nuclear features resulted in an overdiagnosis of PTC. Immunostaining or molecular testing for BRAFV^600E mutation is a useful adjunct for cases with high nuclear scores to identify true PTC.

Citations

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Differentiating BRAF V600E- and RAS-like alterations in encapsulated follicular patterned tumors through histologic features: a validation study
Chankyung Kim, Shipra Agarwal, Andrey Bychkov, Jen-Fan Hang, Agnes Stephanie Harahap, Mitsuyoshi Hirokawa, Kennichi Kakudo, Somboon Keelawat, Chih-Yi Liu, Zhiyan Liu, Truong Phan-Xuan Nguyen, Chanchal Rana, Huy Gia Vuong, Yun Zhu, Chan Kwon Jung
Virchows Archiv.2024;[Epub] CrossRef
The Presence of Typical “BRAFV600E-Like” Atypia in Papillary Thyroid Carcinoma is Highly Specific for the Presence of the BRAFV600E Mutation
John Turchini, Loretta Sioson, Adele Clarkson, Amy Sheen, Leigh Delbridge, Anthony Glover, Mark Sywak, Stan Sidhu, Anthony J. Gill
Endocrine Pathology.2023; 34(1): 112. CrossRef
Could Oxidative Stress Play a Role in the Development and Clinical Management of Differentiated Thyroid Cancer?
Maria Kościuszko, Angelika Buczyńska, Adam Jacek Krętowski, Anna Popławska-Kita
Cancers.2023; 15(12): 3182. CrossRef
Pitfalls in thyroid pathology and the medicolegal aspects of error
David N Poller
Diagnostic Histopathology.2023; 29(11): 495. CrossRef
Developing Models to Predict BRAFV600E and RAS Mutational Status in Papillary Thyroid Carcinoma Using Clinicopathological Features and pERK1/2 Immunohistochemistry Expression
Agnes Stephanie Harahap, Imam Subekti, Sonar Soni Panigoro, Asmarinah, Lisnawati, Retno Asti Werdhani, Hasrayati Agustina, Dina Khoirunnisa, Mutiah Mutmainnah, Fajar Lamhot Gultom, Abdillah Hasbi Assadyk, Maria Francisca Ham
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The Asian Thyroid Working Group, from 2017 to 2023
Kennichi Kakudo, Chan Kwon Jung, Zhiyan Liu, Mitsuyoshi Hirokawa, Andrey Bychkov, Huy Gia Vuong, Somboon Keelawat, Radhika Srinivasan, Jen-Fan Hang, Chiung-Ru Lai
Journal of Pathology and Translational Medicine.2023; 57(6): 289. CrossRef
Noninvasive Follicular Thyroid Neoplasm with Papillary-like Nuclear Features (NIFTP): Tumour Entity with a Short History. A Review on Challenges in Our Microscopes, Molecular and Ultrasonographic Profile
Ivana Kholová, Elina Haaga, Jaroslav Ludvik, David Kalfert, Marie Ludvikova
Diagnostics.2022; 12(2): 250. CrossRef
Update from the 2022 World Health Organization Classification of Thyroid Tumors: A Standardized Diagnostic Approach
Chan Kwon Jung, Andrey Bychkov, Kennichi Kakudo
Endocrinology and Metabolism.2022; 37(5): 703. CrossRef
Different Threshold of Malignancy for RAS-like Thyroid Tumors Causes Significant Differences in Thyroid Nodule Practice
Kennichi Kakudo
Cancers.2022; 14(3): 812. CrossRef
The Incidence of Noninvasive Follicular Thyroid Neoplasm with Papillary-Like Nuclear Features: A Meta-Analysis Assessing Worldwide Impact of the Reclassification
Chanchal Rana, Huy Gia Vuong, Thu Quynh Nguyen, Hoang Cong Nguyen, Chan Kwon Jung, Kennichi Kakudo, Andrey Bychkov
Thyroid.2021;[Epub] CrossRef

Review Articles

Thyroid
Mouse Models as a Tool for Understanding Progression in Braf^V600E-Driven Thyroid Cancers: Iñigo Landa, Jeffrey A. Knauf; Endocrinol Metab. 2019;34(1):11-22. Published online February 15, 2019; DOI: https://doi.org/10.3803/EnM.2019.34.1.11

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The development of next generation sequencing (NGS) has led to marked advancement of our understanding of genetic events mediating the initiation and progression of thyroid cancers. The NGS studies have confirmed the previously reported high frequency of mutually-exclusive oncogenic alterations affecting BRAF and RAS proto-oncogenes in all stages of thyroid cancer. Initially identified by traditional sequencing approaches, the NGS studies also confirmed the acquisition of alterations that inactivate tumor protein p53 (TP53) and activate phosphatidylinositol-4,5-bisphosphate 3-kinase catalytic subunit alpha (PIK3CA) in advanced thyroid cancers. Novel alterations, such as those in telomerase reverse transcriptase (TERT) promoter and mating-type switching/sucrose non-fermenting (SWI/SNF) complex, are also likely to promote progression of the BRAF^V600E-driven thyroid cancers. A number of genetically engineered mouse models (GEMM) of BRAF^V600E-driven thyroid cancer have been developed to investigate thyroid tumorigenesis mediated by oncogenic BRAF and to explore the role of genetic alterations identified in the genomic analyses of advanced thyroid cancer to promote tumor progression. This review will discuss the various GEMMs that have been developed to investigate oncogenic BRAF^V600E-driven thyroid cancers.

Citations

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Daniel M. Chopyk, Priya H. Dedhia
Current Opinion in Endocrine and Metabolic Research.2024; 34: 100502. CrossRef
Comparative efficiency of differential diagnostic methods for the identification of BRAF V600E gene mutation in papillary thyroid cancer (Review)
Qian Liu, Xue Jiang, Wenling Tu, Lina Liu, Ying Huang, Yuxiao Xia, Xuliang Xia, Yuhong Shi
Experimental and Therapeutic Medicine.2024;[Epub] CrossRef
Mouse Models to Examine Differentiated Thyroid Cancer Pathogenesis: Recent Updates
Hye Choi, Kwangsoon Kim
International Journal of Molecular Sciences.2023; 24(13): 11138. CrossRef
Mechanistic Insights of Thyroid Cancer Progression
Luis Javier Leandro-García, Iñigo Landa
Endocrinology.2023;[Epub] CrossRef
Anaplastic thyroid cancer: Pathogenesis, prognostic factors and genetic landscape (Review)
Abdul-Mohsen Alhejaily, Omar Alhuzim, Yazeed Alwelaie
Molecular and Clinical Oncology.2023;[Epub] CrossRef
Tissue architecture delineates field cancerization in BRAFV600E-induced tumor development
Elin Schoultz, Ellen Johansson, Carmen Moccia, Iva Jakubikova, Naveen Ravi, Shawn Liang, Therese Carlsson, Mikael Montelius, Konrad Patyra, Jukka Kero, Kajsa Paulsson, Henrik Fagman, Martin O. Bergo, Mikael Nilsson
Disease Models & Mechanisms.2022;[Epub] CrossRef
BRAFV600E Expression in Thyrocytes Causes Recruitment of Immunosuppressive STABILIN-1 Macrophages
Catherine Spourquet, Ophélie Delcorte, Pascale Lemoine, Nicolas Dauguet, Axelle Loriot, Younes Achouri, Maija Hollmén, Sirpa Jalkanen, François Huaux, Sophie Lucas, Pierre Van Meerkeeck, Jeffrey A. Knauf, James A. Fagin, Chantal Dessy, Michel Mourad, Patr
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Positive BRAFV600E mutation of primary tumor influences radioiodine avidity but not prognosis of papillary thyroid cancer with lung metastases
Shuhui Huang, Mengfang Qi, Tian Tian, Hongyuan Dai, Yuan Tang, Rui Huang
Frontiers in Endocrinology.2022;[Epub] CrossRef
Preclinical Models of Follicular Cell-Derived Thyroid Cancer: An Overview from Cancer Cell Lines to Mouse Models
Min Ji Jeon, Bryan R. Haugen
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An Animal Model Further Uncovers the Role of Mutant Braf during Papillary Thyroid Cancer Development
Bernd Koelsch, Sarah Theurer, Magdalena Staniszewska, Jacqueline Heupel, Amelie Koch, Svenja Mergener, Franziska Walk, Christine Fischer, Andrea Kutritz, Kurt W. Schmid, Andrea Kindler-Röhrborn
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Intratumoral Genetic Heterogeneity in Papillary Thyroid Cancer: Occurrence and Clinical Significance
Laura Fugazzola, Marina Muzza, Gabriele Pogliaghi, Mario Vitale
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The Aryl Hydrocarbon Receptor Is Expressed in Thyroid Carcinoma and Appears to Mediate Epithelial-Mesenchymal-Transition
Sonia Moretti, Nicole Nucci, Elisa Menicali, Silvia Morelli, Vittorio Bini, Renato Colella, Martina Mandarano, Angelo Sidoni, Efisio Puxeddu
Cancers.2020; 12(1): 145. CrossRef

Thyroid
Mutation Profile of Well-Differentiated Thyroid Cancer in Asians: Young Shin Song, Jung Ah Lim, Young Joo Park; Endocrinol Metab. 2015;30(3):252-262. Published online September 22, 2015; DOI: https://doi.org/10.3803/EnM.2015.30.3.252

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Recent advances in molecular diagnostics have led to significant insights into the genetic basis of thyroid tumorigenesis. Among the mutations commonly seen in thyroid cancers, the vast majority are associated with the mitogen-activated protein kinase pathway. B-Raf proto-oncogene (BRAF) mutations are the most common mutations observed in papillary thyroid cancers (PTCs), followed by RET/PTC rearrangements and RAS mutations, while follicular thyroid cancers are more likely to harbor RAS mutations or PAX8/peroxisome proliferator-activated receptor γ (PPARγ) rearrangements. Beyond these more common mutations, alterations in the telomerase reverse transcriptase (TERT) promoter have recently been associated with clinicopathologic features, disease prognosis, and tumorigenesis in thyroid cancer. While the mutations underlying thyroid tumorigenesis are well known, the frequency of these mutations is strongly associated with geography, with clear differences reported between Asian and Western countries. Of particular interest is the prevalence of BRAF mutations, with Korean patients exhibiting the highest rate of BRAF-associated thyroid cancers in the world. Here, we review the prevalence of each of the most common mutations in Asian and Western countries, and identify the characteristics of well-differentiated thyroid cancer in Asians.

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Thyroid.2017; 27(2): 207. CrossRef
Low Rate of Noninvasive Follicular Thyroid Neoplasm with Papillary-Like Nuclear Features in Asian Practice
Andrey Bychkov, Mitsuyoshi Hirokawa, Chan Kwon Jung, Zhiyan Liu, Yun Zhu, Soon Won Hong, Shinya Satoh, Chiung-Ru Lai, Lien Huynh, Kennichi Kakudo
Thyroid.2017; 27(7): 983. CrossRef
Changes in the clinicopathological characteristics and genetic alterations of follicular thyroid cancer
Young Shin Song, Jung Ah Lim, Hye Sook Min, Min Joo Kim, Hoon Sung Choi, Sun Wook Cho, Jae Hoon Moon, Ka Hee Yi, Do Joon Park, Bo Youn Cho, Young Joo Park
European Journal of Endocrinology.2017; 177(6): 465. CrossRef
Effects of CoexistentBRAFV600EandTERTPromoter Mutations on Poor Clinical Outcomes in Papillary Thyroid Cancer: A Meta-Analysis
Shinje Moon, Young Shin Song, Ye An Kim, Jung Ah Lim, Sun Wook Cho, Jae Hoon Moon, Seokyung Hahn, Do Joon Park, Young Joo Park
Thyroid.2017; 27(5): 651. CrossRef
TERT Promoter Mutation in an Aggressive Cribriform Morular Variant of Papillary Thyroid Carcinoma
Eun Ji Oh, Sohee Lee, Ja Seong Bae, Yourha Kim, Sora Jeon, Chan Kwon Jung
Endocrine Pathology.2017; 28(1): 49. CrossRef
TERT Promoter Mutation Predicts Radioiodine-Refractory Character in Distant Metastatic Differentiated Thyroid Cancer
Xue Yang, Jiao Li, Xiaoyi Li, Zhiyong Liang, Wen Gao, Jun Liang, Shujun Cheng, Yansong Lin
Journal of Nuclear Medicine.2017; 58(2): 258. CrossRef
Molecular Diagnosis Using Residual Liquid-Based Cytology Materials for Patients with Nondiagnostic or Indeterminate Thyroid Nodules
Hyemi Kwon, Won Gu Kim, Markus Eszlinger, Ralf Paschke, Dong Eun Song, Mijin Kim, Suyeon Park, Min Ji Jeon, Tae Yong Kim, Young Kee Shong, Won Bae Kim
Endocrinology and Metabolism.2016; 31(4): 586. CrossRef
TERT promoter mutations and long-term survival in patients with thyroid cancer
Tae Hyuk Kim, Young-Eun Kim, Soomin Ahn, Ji-Youn Kim, Chang-Seok Ki, Young Lyun Oh, Kyunga Kim, Jae Won Yun, Woong-Yang Park, Jun-Ho Choe, Jung-Han Kim, Jee Soo Kim, Sun Wook Kim, Jae Hoon Chung
Endocrine-Related Cancer.2016; 23(10): 813. CrossRef
Reply:
Y. Che
American Journal of Neuroradiology.2016; 37(1): E9. CrossRef
Prognostic effects of TERT promoter mutations are enhanced by coexistence with BRAF or RAS mutations and strengthen the risk prediction by the ATA or TNM staging system in differentiated thyroid cancer patients
Young Shin Song, Jung Ah Lim, Hoonsung Choi, Jae‐Kyung Won, Jae Hoon Moon, Sun Wook Cho, Kyu Eun Lee, Young Joo Park, Ka Hee Yi, Do Joon Park, Jeong‐Sun Seo
Cancer.2016; 122(9): 1370. CrossRef

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