C-PTCs: classical form of papillary thyroid carcinomas; F-PTCs: follicular variant of papillary thyroid carcinomas; ATCs: anaplastic thyroid carcinomas.
Declarations
Acknowledgments
This work is based in part on the doctoral dissertation of the first author, ‘Role of NADPH oxidase NOX4 in regulating the expression and the activity of CHD4 in BRAFV600E mutated thyroid cancer cells’, submitted to Paris-Saclay University, accessible at https://theses.hal.science/tel-04992343v1. The thesis is publicly available and not under exclusive copyright with any publisher. The first author retains copyright and publication rights for dissemination in peer-reviewed journals.
Author contributions
RAEH and CD: Conceptualization, Writing—original draft, Writing—review & editing, Supervision, Funding acquisition. SF: Writing—original draft, Formal analysis, Visualization, Writing—review & editing. YB: Formal analysis, Supervision, Writing—review & editing. MO, YO, and ND: Formal analysis, Writing—review & editing. MRE, AM, and AA: Formal analysis. AL: Writing—review & editing. All authors read and approved the submitted version.
Conflicts of interest
The authors declare no conflict of interest.
Ethical approval
This research was approved by the Ethics Committee for Biomedical Research (CERB) of the Faculty of Medicine and Pharmacy in Rabat under approval number 52/20 and complies with the Declaration of Helsinki.
Consent to participate
This study was conducted in 2022–2023, as a retrospective analysis of existing medical records and archived FFPE blocks (2015–2021). In this case, the consent to participate is waived.
Consent to publication
Not applicable.
Availability of data and materials
Data sharing is not applicable due to ethical restrictions and due to the possible future exploration of this cohort.
Funding
Research funded by (1) Cancer Research Institute (IRC). www.irc.ma; Project: 767/AAmP2019; (2) PHC TOUBKAL N_ TBK/20/113 N_CAMPUS: 43586FYA (Maroc/France) (2020–2022); and (3) doctoral scholarship to S. FENNICHE from CNRST, Maroc (Bourse d’excellence). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Open Exploration maintains a neutral stance on jurisdictional claims in published institutional affiliations and maps. All opinions expressed in this article are the personal views of the author(s) and do not represent the stance of the editorial team or the publisher.
References
Nikiforov YE, Nikiforova MN. Molecular genetics and diagnosis of thyroid cancer.Nat Rev Endocrinol. 2011;7:569–80. [DOI] [PubMed]
Newfield RS, Jiang W, Sugganth DX, Hantash FM, Lee E, Newbury RO. Mutational analysis using next generation sequencing in pediatric thyroid cancer reveals BRAF and fusion oncogenes are common.Int J Pediatr Otorhinolaryngol. 2022;157:111121. [DOI] [PubMed]
Kebebew E, Weng J, Bauer J, Ranvier G, Clark OH, Duh QY, et al. The prevalence and prognostic value of BRAF mutation in thyroid cancer.Ann Surg. 2007;246:466–70. [DOI] [PubMed] [PMC]
Kimura ET, Nikiforova MN, Zhu Z, Knauf JA, Nikiforov YE, Fagin JA. High prevalence of BRAF mutations in thyroid cancer: genetic evidence for constitutive activation of the RET/PTC-RAS-BRAF signaling pathway in papillary thyroid carcinoma.Cancer Res. 2003;63:1454–7. [PubMed]
Xing M, Alzahrani AS, Carson KA, Viola D, Elisei R, Bendlova B, et al. Association between BRAF V600E mutation and mortality in patients with papillary thyroid cancer.JAMA. 2013;309:1493–501. [DOI] [PubMed] [PMC]
Galrão AL, Camargo RY, Friguglietti CU, Moraes L, Cerutti JM, Serrano-Nascimento C, et al. Hypermethylation of a New Distal Sodium/Iodide Symporter (NIS) enhancer (NDE) is associated with reduced NIS expression in thyroid tumors.J Clin Endocrinol Metab. 2014;99:E944–52. [DOI] [PubMed]
Yi JW, Ha SY, Jee HG, Kim K, Kim SJ, Chai YJ, et al. Induction of the BRAFV600E Mutation in Thyroid Cells Leads to Frequent Hypermethylation.Clin Exp Otorhinolaryngol. 2022;15:273–82. [DOI] [PubMed] [PMC]
Azouzi N, Cailloux J, Cazarin JM, Knauf JA, Cracchiolo J, Ghuzlan AA, et al. NADPH Oxidase NOX4 Is a Critical Mediator of BRAFV600E-Induced Downregulation of the Sodium/Iodide Symporter in Papillary Thyroid Carcinomas.Antioxid Redox Signal. 2017;26:864–77. [DOI] [PubMed] [PMC]
Riesco-Eizaguirre G, Santisteban P, De la Vieja A. The complex regulation of NIS expression and activity in thyroid and extrathyroidal tissues.Endocr Relat Cancer. 2021;28:T141–65. [DOI] [PubMed]
Fenniche S, Oukabli M, Oubaddou Y, Chahdi H, Damiri A, Alghuzlan A, et al. A Comparative Analysis of NOX4 Protein Expression in Malignant and Non-Malignant Thyroid Tumors.Curr Issues Mol Biol. 2023;45:5811–23. [DOI] [PubMed] [PMC]
Xue Y, Wong J, Moreno GT, Young MK, Côté J, Wang W. NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities.Mol Cell. 1998;2:851–61. [DOI] [PubMed]
McKenzie LD, LeClair JW, Miller KN, Strong AD, Chan HL, Oates EL, et al. CHD4 regulates the DNA damage response and RAD51 expression in glioblastoma.Sci Rep. 2019;9:4444. [DOI] [PubMed] [PMC]
Wang Y, Chen Y, Bao L, Zhang B, Wang JE, Kumar A, et al. CHD4 Promotes Breast Cancer Progression as a Coactivator of Hypoxia-Inducible Factors.Cancer Res. 2020;80:3880–91. [DOI] [PubMed] [PMC]
Novillo A, Fernández-Santander A, Gaibar M, Galán M, Romero-Lorca A, Abdellaoui-Soussi FE, et al. Role of Chromodomain-Helicase-DNA-Binding Protein 4 (CHD4) in Breast Cancer.Front Oncol. 2021;11:633233. [DOI] [PubMed] [PMC]
D’Alesio C, Bellese G, Gagliani MC, Lechiara A, Dameri M, Grasselli E, et al. The chromodomain helicase CHD4 regulates ERBB2 signaling pathway and autophagy in ERBB2+ breast cancer cells.Biol Open. 2019;8:bio038323. [DOI] [PubMed] [PMC]
Xia L, Huang W, Bellani M, Seidman MM, Wu K, Fan D, et al. CHD4 Has Oncogenic Functions in Initiating and Maintaining Epigenetic Suppression of Multiple Tumor Suppressor Genes.Cancer Cell. 2017;31:653–68.e7. [DOI] [PubMed] [PMC]
Xu N, Liu F, Wu S, Ye M, Ge H, Zhang M, et al. CHD4 mediates proliferation and migration of non-small cell lung cancer via the RhoA/ROCK pathway by regulating PHF5A.BMC Cancer. 2020;20:262. [DOI] [PubMed] [PMC]
Wang HC, Chou CL, Yang CC, Huang WL, Hsu YC, Luo CW, et al. Over-Expression of CHD4 Is an Independent Biomarker of Poor Prognosis in Patients with Rectal Cancers Receiving Concurrent Chemoradiotherapy.Int J Mol Sci. 2019;20:4087. [DOI] [PubMed] [PMC]
Pratheeshkumar P, Siraj AK, Divya SP, Parvathareddy SK, Alobaisi K, Al-Sobhi SS, et al. CHD4 Predicts Aggressiveness in PTC Patients and Promotes Cancer Stemness and EMT in PTC Cells.Int J Mol Sci. 2021;22:504. [DOI] [PubMed] [PMC]
Polo SE, Kaidi A, Baskcomb L, Galanty Y, Jackson SP. Regulation of DNA-damage responses and cell-cycle progression by the chromatin remodelling factor CHD4.EMBO J. 2010;29:3130–9. [DOI] [PubMed] [PMC]
Zhang J, Shih DJH, Lin SY. The Tale of CHD4 in DNA Damage Response and Chemotherapeutic Response.J Cancer Res Cell Ther. 2019;3:052. [PubMed] [PMC]
Lloyd RV, Osamura RY, Klöppel G, Rosai J, editors. WHO classification of tumours of endocrine organs. 4th ed. Lyon: International Agency for Research on Cancer; 2017.
Li P, Ding Y, Liu M, Wang W, Li X. Sex disparities in thyroid cancer: a SEER population study.Gland Surg. 2021;10:3200–10. [DOI] [PubMed] [PMC]
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.CA Cancer J Clin. 2018;68:394–424. [DOI] [PubMed]
Kaabouch M, Chahdi H, Azouzi N, Oukabli M, Rharrassi I, Boudhas A, et al. BRAFV600E hot spot mutation in thyroid carcinomas: first Moroccan experience from a single-institution retrospective study.Afr Health Sci. 2020;20:1849–56. [DOI] [PubMed] [PMC]
Shi X, Liu R, Basolo F, Giannini R, Shen X, Teng D, et al. Differential Clinicopathological Risk and Prognosis of Major Papillary Thyroid Cancer Variants.J Clin Endocrinol Metab. 2016;101:264–74. [DOI] [PubMed] [PMC]
Shafique K, Baloch Z. Risk stratification of papillary thyroid carcinoma and its variants; from clinicopathologic features to molecular profiling.Diagn Histopathol. 2019;25:143–53. [DOI]
Hu J, Yuan IJ, Mirshahidi S, Simental A, Lee SC, Yuan X. Thyroid Carcinoma: Phenotypic Features, Underlying Biology and Potential Relevance for Targeting Therapy.Int J Mol Sci. 2021;22:1950. [DOI] [PubMed] [PMC]
Kim S, Lee KE, Myong JP, Park JH, Jeon YK, Min HS, et al. BRAF V600E mutation is associated with tumor aggressiveness in papillary thyroid cancer.World J Surg. 2012;36:310–7. [DOI] [PubMed]
Choi YW, Kim HJ, Kim YH, Park SH, Chwae YJ, Lee J, et al. B-RafV600E inhibits sodium iodide symporter expression via regulation of DNA methyltransferase 1.Exp Mol Med. 2014;46:e120. [DOI] [PubMed] [PMC]
Masoodi T, Siraj AK, Siraj S, Azam S, Qadri Z, Albalawy WN, et al. Whole-Exome Sequencing of Matched Primary and Metastatic Papillary Thyroid Cancer.Thyroid. 2020;30:42–56. [DOI] [PubMed] [PMC]
Li S, Hu G, Chen Y, Sang Y, Tang Q, Liu R. TERT upstream promoter methylation regulates TERT expression and acts as a therapeutic target in TERT promoter mutation-negative thyroid cancer.Cancer Cell Int. 2024;24:271. [DOI] [PubMed] [PMC]
Oskouie AA, Ahmadi MS, Taherkhani A. Identification of Prognostic Biomarkers in Papillary Thyroid Cancer and Developing Non-Invasive Diagnostic Models Through Integrated Bioinformatics Analysis.Microrna. 2022;11:73–87. [DOI] [PubMed]
Larsen DH, Poinsignon C, Gudjonsson T, Dinant C, Payne MR, Hari FJ, et al. The chromatin-remodeling factor CHD4 coordinates signaling and repair after DNA damage.J Cell Biol. 2010;190:731–40. [DOI] [PubMed] [PMC]