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Genetic dysregulation of an endothelial Ras signaling network in vein of Galen malformations

Zhao, S.; Mekbib, K. Y.; van der Ent, M. A.; Allington, G.; Prendergast, A.; Chau, J. E.; Smith, H.; Shohfi, J.; Ocken, J.; Duran, D.; Furey, C. G.; Le, H. T.; Duy, P. Q.; Reeves, B. C.; Zhang, J.; Nelson-Williams, C.; Chen, D.; Li, B.; Nottoli, T.; Bai, S.; Rolle, M.; Zeng, X.; Dong, W.; Fu, P.-Y.; Wang, Y.-C.; Mane, S.; Piwowarczyk, P.; Fehnel, K. P.; See, A. P.; Iskandar, B. J.; Aagaard-Kienitz, B.; Kundishora, A. J.; DeSpenza, T.; Greenberg, A. B. W.; Kidanemariam, S. M.; Prendergast, A.; Johnston, J. M.; Jackson, E.; Storm, P. B.; Lang, S.-S.; Butler, W. E.; Carter, B. S.; Chapman, P.; St

2023-03-22 genomics
10.1101/2023.03.18.532837 bioRxiv
Show abstract

To elucidate the pathogenesis of vein of Galen malformations (VOGMs), the most common and severe congenital brain arteriovenous malformation, we performed an integrated analysis of 310 VOGM proband-family exomes and 336,326 human cerebrovasculature single-cell transcriptomes. We found the Ras suppressor p120 RasGAP (RASA1) harbored a genome-wide significant burden of loss-of-function de novo variants (p=4.79x10-7). Rare, damaging transmitted variants were enriched in Ephrin receptor-B4 (EPHB4) (p=1.22x10-5), which cooperates with p120 RasGAP to limit Ras activation. Other probands had pathogenic variants in ACVRL1, NOTCH1, ITGB1, and PTPN11. ACVRL1 variants were also identified in a multi-generational VOGM pedigree. Integrative genomics defined developing endothelial cells as a key spatio-temporal locus of VOGM pathophysiology. Mice expressing a VOGM-specific EPHB4 kinase-domain missense variant exhibited constitutive endothelial Ras/ERK/MAPK activation and impaired hierarchical development of angiogenesis-regulated arterial-capillary-venous networks, but only when carrying a "second-hit" allele. These results illuminate human arterio-venous development and VOGM pathobiology and have clinical implications.

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