Revisiting the molecular landscape of Rosai-Dorfman disease: insights from whole exome sequencing of Saudi patients

Rosai-Dorfman disease (RDD) has traditionally been viewed as a reactive histiocytic disorder, defined by its unique clinical features and immunophenotype. However, recent genetic studies suggest a more complex molecular landscape, challenging the notion of RDD as solely reactive and hinting at a pos...

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Main Authors: Sarah Binhassan, Manar Samman, Yazeed Al-Sheikh, Wafaa Alshakweer, Tahani Alhalouli, Najd Alshamlan, Manal Abudawood
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-05-01
Series:Frontiers in Oncology
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Online Access:https://www.frontiersin.org/articles/10.3389/fonc.2025.1556830/full
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author Sarah Binhassan
Sarah Binhassan
Manar Samman
Yazeed Al-Sheikh
Wafaa Alshakweer
Tahani Alhalouli
Najd Alshamlan
Manal Abudawood
Manal Abudawood
author_facet Sarah Binhassan
Sarah Binhassan
Manar Samman
Yazeed Al-Sheikh
Wafaa Alshakweer
Tahani Alhalouli
Najd Alshamlan
Manal Abudawood
Manal Abudawood
author_sort Sarah Binhassan
collection DOAJ
description Rosai-Dorfman disease (RDD) has traditionally been viewed as a reactive histiocytic disorder, defined by its unique clinical features and immunophenotype. However, recent genetic studies suggest a more complex molecular landscape, challenging the notion of RDD as solely reactive and hinting at a possible neoplastic component. Mutations in MAPK/ERK pathway genes, such as KRAS and MAP2K1, have been observed in up to 33% of cases. Additional genetic alterations in cell cycle regulation, DNA repair, and other processes, along with low-frequency BRAF mutations, further emphasize this complexity. To better understand the molecular basis of RDD and enhance diagnostic precision, we conducted whole exome sequencing (WES) on seven Saudi patients with RDD, comparing their genetic profiles with existing literature. While no kinase driver mutations were detected, our analysis revealed thirteen distinct mutations. Recurrent mutations were observed in CD207 and TDG, each found in six patients. CD207 is linked to antigen processing, while TDG is associated with DNA repair. MUC4 and PDS5A mutations, related to cell cycle regulation, were each identified in three patients. DNMT3A mutation, affecting DNA methylation, was found in two patients. Single mutations were observed in BRCA1, LATS2, ATM, USP35, and CIC, associated with DNA repair, the ubiquitin proteasome pathway, and transcriptional regulation respectively. These findings offer insights into the genetic makeup of RDD, revealing candidate genes and expanding our understanding of the disease’s molecular complexities. By uncovering these genetic markers, this study contributes to the ongoing efforts to develop more accurate diagnostic tools and refine the classification of RDD, paving the way for improved patient care and disease management.
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spelling doaj-art-dff1041c0d024d72b214564b971a04602025-08-20T03:52:43ZengFrontiers Media S.A.Frontiers in Oncology2234-943X2025-05-011510.3389/fonc.2025.15568301556830Revisiting the molecular landscape of Rosai-Dorfman disease: insights from whole exome sequencing of Saudi patientsSarah Binhassan0Sarah Binhassan1Manar Samman2Yazeed Al-Sheikh3Wafaa Alshakweer4Tahani Alhalouli5Najd Alshamlan6Manal Abudawood7Manal Abudawood8Department of Clinical Laboratory Sciences, College of Applied Medical Sciences, King Saud University, Riyadh, Saudi ArabiaCentral Research Laboratory, King Saud University, Riyadh, Saudi ArabiaMolecular Pathology (Genetics) Section, Pathology and Clinical Laboratory Medicine Administration, King Fahad Medical City, Riyadh, Saudi ArabiaDepartment of Clinical Laboratory Sciences, College of Applied Medical Sciences, King Saud University, Riyadh, Saudi ArabiaDepartment of Pathology and Laboratory Medicine, King Fahad Medical City, Riyadh, Saudi ArabiaDepartment of Pathology and Laboratory Medicine, King Fahad Medical City, Riyadh, Saudi ArabiaDepartment of Pathology and Laboratory Medicine, King Abdullah bin Abdulaziz University Hospital, Riyadh, Saudi ArabiaDepartment of Clinical Laboratory Sciences, College of Applied Medical Sciences, King Saud University, Riyadh, Saudi ArabiaCentral Research Laboratory, King Saud University, Riyadh, Saudi ArabiaRosai-Dorfman disease (RDD) has traditionally been viewed as a reactive histiocytic disorder, defined by its unique clinical features and immunophenotype. However, recent genetic studies suggest a more complex molecular landscape, challenging the notion of RDD as solely reactive and hinting at a possible neoplastic component. Mutations in MAPK/ERK pathway genes, such as KRAS and MAP2K1, have been observed in up to 33% of cases. Additional genetic alterations in cell cycle regulation, DNA repair, and other processes, along with low-frequency BRAF mutations, further emphasize this complexity. To better understand the molecular basis of RDD and enhance diagnostic precision, we conducted whole exome sequencing (WES) on seven Saudi patients with RDD, comparing their genetic profiles with existing literature. While no kinase driver mutations were detected, our analysis revealed thirteen distinct mutations. Recurrent mutations were observed in CD207 and TDG, each found in six patients. CD207 is linked to antigen processing, while TDG is associated with DNA repair. MUC4 and PDS5A mutations, related to cell cycle regulation, were each identified in three patients. DNMT3A mutation, affecting DNA methylation, was found in two patients. Single mutations were observed in BRCA1, LATS2, ATM, USP35, and CIC, associated with DNA repair, the ubiquitin proteasome pathway, and transcriptional regulation respectively. These findings offer insights into the genetic makeup of RDD, revealing candidate genes and expanding our understanding of the disease’s molecular complexities. By uncovering these genetic markers, this study contributes to the ongoing efforts to develop more accurate diagnostic tools and refine the classification of RDD, paving the way for improved patient care and disease management.https://www.frontiersin.org/articles/10.3389/fonc.2025.1556830/fullRosai-Dorfman diseasewhole exome sequencingmolecular markersBRCA1 mutationgenetic landscape
spellingShingle Sarah Binhassan
Sarah Binhassan
Manar Samman
Yazeed Al-Sheikh
Wafaa Alshakweer
Tahani Alhalouli
Najd Alshamlan
Manal Abudawood
Manal Abudawood
Revisiting the molecular landscape of Rosai-Dorfman disease: insights from whole exome sequencing of Saudi patients
Frontiers in Oncology
Rosai-Dorfman disease
whole exome sequencing
molecular markers
BRCA1 mutation
genetic landscape
title Revisiting the molecular landscape of Rosai-Dorfman disease: insights from whole exome sequencing of Saudi patients
title_full Revisiting the molecular landscape of Rosai-Dorfman disease: insights from whole exome sequencing of Saudi patients
title_fullStr Revisiting the molecular landscape of Rosai-Dorfman disease: insights from whole exome sequencing of Saudi patients
title_full_unstemmed Revisiting the molecular landscape of Rosai-Dorfman disease: insights from whole exome sequencing of Saudi patients
title_short Revisiting the molecular landscape of Rosai-Dorfman disease: insights from whole exome sequencing of Saudi patients
title_sort revisiting the molecular landscape of rosai dorfman disease insights from whole exome sequencing of saudi patients
topic Rosai-Dorfman disease
whole exome sequencing
molecular markers
BRCA1 mutation
genetic landscape
url https://www.frontiersin.org/articles/10.3389/fonc.2025.1556830/full
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