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Single-cell RNA Sequencing Reveals Tumor Subtypes Within Salivary Gland Pleomorphic Adenoma

ABSTRACT: Single-cell RNA Sequencing Reveals Tumor Subtypes Within Salivary Gland Pleomorphic Adenoma

PROVIDER: PRJNA804107 | ENA |

REPOSITORIES: ENA

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			Action	DRS
	SRR17914840_1.fastq.gz	Fastqsanger.gz
	SRR17914840_2.fastq.gz	Fastqsanger.gz
	SRR17914841_1.fastq.gz	Fastqsanger.gz
	SRR17914841_2.fastq.gz	Fastqsanger.gz

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Single-cell RNA Sequencing Reveals Tumor Subtypes Within Salivary Gland Pleomorphic Adenoma

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Project description:Pleomorphic adenoma (PA), the most common benign salivary gland tumor, presents unpredictable risks of recurrence and malignant transformation into carcinoma ex pleomorphic adenoma (CXPA), posing significant clinical challenges. To better delineate the tumor progression trajectory, we performed single-cell RNA sequencing on normal salivary glands, primary PA, recurrent PA (rPA), and CXPA, integrating cell trajectory reconstruction, differential gene expression analysis, and key gene network exploration to uncover molecular transitions and intercellular crosstalk underlying PA recurrence and malignant transformation. Our findings revealed GALNT13⁺ myoepithelial cells as CXPA-specific malignant progenitors, marking early malignant conversion, while MIF⁺ myoepithelial cells exhibited enhanced tissue-destructive capabilities. Fibroblasts played dual roles, enforcing fibrotic restraint in primary PA and promoting extracellular matrix degradation in CXPA. The tumor microenvironment demonstrated stage-specific adaptations, with CXPA favoring pro-inflammatory MIF–CD74/CD44 signaling, whereas rPA adopted immunosuppressive characteristics. Together, stromal reprogramming and immune-editing dynamics orchestrated microenvironmental adaptation, linking cellular heterogeneity to clinical aggressiveness. This study presents the first comprehensive molecular atlas of PA progression, highlighting the malignant specialization of myoepithelial subpopulations, fibroblast-mediated stromal remodeling, and immune-driven microenvironmental evolution, offering a valuable framework for precision stratification of malignant potential and future microenvironment-targeted therapeutic strategies.

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Project description:Supposed risk of malignant transformation of salivary gland pleomorphic adenoma (SGPA) is an important reason for aggressive retreatment in recurrent pleomorphic adenoma (RPA). However, although the diagnostic category 'carcinoma ex-pleomorphic adenoma' suggests that malignant transformation of a pleomorphic adenoma is a regular event, this has to date not been shown to occur in sequential lesions of one patient. Here, we show the molecular events in transformation to malignancy of a pleomorphic adenoma of the parotid gland. Detailed molecular analysis revealed an LIFR/PLAG1 translocation characteristic for pleomorphic adenoma and, next to this, a PIK3R1 frameshift mutation and several allelic imbalances. In subsequent malignant recurrences, the same LIFR/PLAG1 translocation, PIK3R1 frameshift mutation, and allelic imbalances were present in addition to TP53 mutations. Thus, this case not only shows malignant transformation of SGPA, but also demonstrates that molecular analysis can be of help in recognising malignancy in the rare instance of RPA.

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Project description:Salivary gland tumors (SGTs) are a rare and heterogeneous group of lesions with diverse microscopic appearances and variable clinical behavior. The most common SGT subtype, pleomorphic adenoma (PA), can undergo malignant transformation into carcinoma ex pleomorphic adenoma (CXPA). Carcinomatous transformation from PA to CXPA is a highly progressive and multi-step process. Distinguishing a PA with some atypia from a low-grade intracapsular or minimally invasive CXPA is primarily subjective as no mitotic count thresholds exist to help pathologists distinguish between them in difficult cases. In this prospective study, we collected 140 cases encompassing both PA and CXPA to study their molecular signatures. The primary objective was to investigate the use of DNA methylation profiling as a potential molecular tool for differentiating between these two entities. Methylation analysis was performed on 33 PA cases and 33 CXPA cases. We were able to demonstrate that based on their methylation profiles, PA and CXPA could be classified into three distinct clusters that we called benign, intermediate, and malignant. We also revealed that the presence of TP53, HRAS, PTEN and/or TERT pathogenic mutations were exclusively present in CXPA cases; and that chromosomal alteration on chromosomes 5 and 8 are potentially associated with malignant transformation. In conclusion, our study provides a comprehensive molecular framework for PA and CXPA. The presence of a pathogenic mutation in TP53, HRAS, PTEN, or pTERT or HER2 amplification could be integrated into a molecular diagnosis of CXPA for tumors within the PA CXPA spectrum. In the future, we aim to improve our methylomic classification to make it a precision medicine diagnostic tool for the treatment management of tumors within the PA-CXPA spectrum.

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