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Loss of ERG function causes lymphatic vessel malformations and primary lymphoedema

Pirri, D.; Maude, H.; Stroobants, A.; Ogmem, K.; Sackey, E.; Dobbins, S.; Grigoriadis, D.; Del Rey Jimenez, J. C.; Al-Ansari, D. E.; Frudd, K.; Saginc, G.; Peghaire, C.; Sutanto, S.; Vujic, T.; Moy, R.; Gresham, D. O. F.; Manolias, A.; Nagy, D.; Riches, K.; Dean, J.; Turner, C. L.; Ellard, S.; Elmslie, F.; Keeley, V.; Jeffery, S.; Mortimer, P.; Gordon, K.; Paschalaki, K. E.; Mäkinen, T.; Celiz, A.; Gould, I. R.; Mansour, S.; Martin-Almedina, S.; Randi, A. M.; Cebola, I.; Ostergaard, P.; Birdsey, G. M.

2025-03-14 cardiovascular medicine
10.1101/2025.03.10.25323421 medRxiv
Show abstract

Transcription factor networks are crucial for the regulation of endothelial cell gene expression during vascular development and homeostasis. A recent analysis of 269 rare diseases in 77,539 individuals revealed an association between loss-of-function variants in ERG, encoding an ETS transcription factor, with primary lymphoedema. However, the pathogenicity of such variants and possible mechanisms of ERG-associated lymphatic vessel dysfunction remains to be established. Here, we have further identified and characterised lymphoedema-associated ERG genetic variants, revealing pathogenic mechanisms ranging from differential ERG subcellular localisation to altered DNA-binding and impaired transactivation. We confirm a role for ERG in regulating lymphangiogenesis using in vitro assays and a lymphatic endothelium-specific Erg deletion mouse model. Furthermore, we characterise the transcriptional and epigenomic landscape of human dermal lymphatic endothelial cells, identifying a unique role for ERG in regulating lymphatic gene programs, including the establishment of cooperative TF networks with PROX1 and GATA2. Our studies identify ERG as a master regulator of lymphatic endothelial cell transcriptional networks and uncover the mechanisms that underpin a novel causative gene for primary lymphoedema.

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