Cerebral Vein Malformations Result from Loss of Twist1 Expression and BMP Signaling from Skull Progenitor Cells and Dura

Dev Cell. 2017 Sep 11;42(5):445-461.e5. doi: 10.1016/j.devcel.2017.07.027. Epub 2017 Aug 30.

Abstract

Dural cerebral veins (CV) are required for cerebrospinal fluid reabsorption and brain homeostasis, but mechanisms that regulate their growth and remodeling are unknown. We report molecular and cellular processes that regulate dural CV development in mammals and describe venous malformations in humans with craniosynostosis and TWIST1 mutations that are recapitulated in mouse models. Surprisingly, Twist1 is dispensable in endothelial cells but required for specification of osteoprogenitor cells that differentiate into preosteoblasts that produce bone morphogenetic proteins (BMPs). Inactivation of Bmp2 and Bmp4 in preosteoblasts and periosteal dura causes skull and CV malformations, similar to humans harboring TWIST1 mutations. Notably, arterial development appears normal, suggesting that morphogens from the skull and dura establish optimal venous networks independent from arterial influences. Collectively, our work establishes a paradigm whereby CV malformations result from primary or secondary loss of paracrine BMP signaling from preosteoblasts and dura, highlighting unique cellular interactions that influence tissue-specific angiogenesis in mammals.

Keywords: BMP2; BMP4; ICP; Twist1; cerebral veins; coronal suture; craniosynostosis; osteoblast; skull; venous angiogenesis.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Bone Morphogenetic Proteins / metabolism*
  • Cell Differentiation
  • Cerebral Arteries / growth & development
  • Cerebral Arteries / pathology
  • Cerebral Veins / abnormalities*
  • Cerebral Veins / metabolism*
  • Cerebral Veins / pathology
  • Cranial Sutures / pathology
  • Craniosynostoses / genetics
  • Craniosynostoses / pathology
  • Dura Mater / pathology
  • Female
  • Humans
  • Mesoderm / metabolism
  • Mice
  • Mice, Mutant Strains
  • Mutation / genetics
  • Neural Crest / pathology
  • Nuclear Proteins / metabolism*
  • Osteoblasts
  • Paracrine Communication
  • Signal Transduction*
  • Skull / pathology*
  • Stem Cells / metabolism*
  • Transverse Sinuses / pathology
  • Twist-Related Protein 1 / metabolism*

Substances

  • Bone Morphogenetic Proteins
  • Nuclear Proteins
  • TWIST1 protein, human
  • Twist-Related Protein 1
  • Twist1 protein, mouse