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Single-cell transcriptomics reveals cellular evolution underlying pleomorphic adenoma recurrence and malignant

Yike Li1, Zhixuan Li1, Guile Zhao1

  • 1State Key Laboratory of Oral Diseases & National Center for Stomatology & National Clinical Research Center for Oral Diseases, Department of Head and Neck Oncology, West China Hospital of Stomatology, Sichuan University, Chengdu, Sichuan, China.

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Pleomorphic adenoma (PA) can recur or transform into carcinoma ex pleomorphic adenoma (CXPA). This study identifies specific myoepithelial cells as malignant progenitors and reveals tumor microenvironment adaptations driving PA progression.

Keywords:
Malignant transformationMyoepithelial cellsPleomorphic adenomaRecurrenceSingle-cell RNA sequencingTumor microenvironment

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Area of Science:

  • Oncology
  • Molecular Biology
  • Translational Research

Background:

  • Pleomorphic adenoma (PA) is the most common benign salivary gland tumor.
  • PA recurrence and malignant transformation to carcinoma ex pleomorphic adenoma (CXPA) present clinical challenges.
  • Understanding the molecular mechanisms of PA transformation is crucial for improved patient outcomes.

Purpose of the Study:

  • To delineate the molecular trajectory of PA recurrence and malignant transformation.
  • To identify key cellular players and microenvironmental factors involved in PA progression.
  • To establish a molecular atlas of PA to CXPA transformation.

Main Methods:

  • Single-cell RNA sequencing of normal salivary gland, primary PA, recurrent PA (rPA), and CXPA.
  • Cell trajectory reconstruction and differential gene expression analysis.
  • Immunohistochemistry for validation of key molecular findings.

Main Results:

  • GALNT13+ myoepithelial cells identified as specific malignant progenitors in CXPA.
  • MIF+ myoepithelial cells showed enhanced tissue-destructive potential.
  • Fibroblasts shifted from fibrotic restraint in PA to extracellular matrix degradation in CXPA.
  • CXPA exhibited pro-inflammatory MIF-CD74/CD44 signaling, while rPA showed immunosuppressive traits.

Conclusions:

  • This study provides the first molecular atlas of PA to CXPA transformation.
  • Malignant specialization of myoepithelial cells, fibroblast reprogramming, and immune editing drive tumor progression.
  • Findings support precision stratification of PA malignant potential and highlight microenvironmental interventions.