MAML3-fusions modulate vascular and immune tumour microenvironment and confer high metastatic risk in pheochromocytoma and paraganglioma

Best Pract Res Clin Endocrinol Metab. 2024 Dec;38(6):101931. doi: 10.1016/j.beem.2024.101931. Epub 2024 Aug 29.

Abstract

Pheochromocytomas and paragangliomas are rare neuroendocrine tumours. Around 20-25 % of patients develop metastases, for which there is an urgent need of prognostic markers and therapeutic stratification strategies. The presence of a MAML3-fusion is associated with increased metastatic risk, but neither the processes underlying disease progression, nor targetable vulnerabilities have been addressed. We have compiled a cohort of 850 patients, which has shown a 3.65 % fusion prevalence and represents the largest MAML3-positive series reported to date. While MAML3-fusions mainly cause single pheochromocytomas, we also observed somatic post-zygotic events, resulting in multiple tumours in the same patient. MAML3-tumours show increased expression of neuroendocrine-to-mesenchymal transition markers, MYC-targets, and angiogenesis-related genes, leading to a distinct tumour microenvironment with unique vascular and immune profiles. Importantly, our findings have identified MAML3-tumours specific vulnerabilities beyond Wnt-pathway dysregulation, such as a rich vascular network, and overexpression of PD-L1 and CD40, suggesting potential therapeutic targets.

Keywords: MAML3 screening procedure; MAML3-fusion; metastasis; paraganglioma; pheochromocytoma; tumour microenvironment; vasculature.

MeSH terms

  • Adrenal Gland Neoplasms* / genetics
  • Adrenal Gland Neoplasms* / pathology
  • Adult
  • DNA-Binding Proteins / genetics
  • Female
  • Humans
  • Male
  • Neoplasm Metastasis
  • Paraganglioma* / genetics
  • Paraganglioma* / pathology
  • Pheochromocytoma* / genetics
  • Pheochromocytoma* / pathology
  • Trans-Activators / genetics
  • Transcription Factors / genetics
  • Tumor Microenvironment* / immunology

Substances

  • MAML3 protein, human
  • Trans-Activators
  • Transcription Factors
  • DNA-Binding Proteins