Thrombospondin1 (TSP1) replacement prevents cerebral cavernous malformations

J Exp Med. 2017 Nov 6;214(11):3331-3346. doi: 10.1084/jem.20171178. Epub 2017 Sep 28.

Abstract

KRIT1 mutations are the most common cause of cerebral cavernous malformation (CCM). Acute Krit1 gene inactivation in mouse brain microvascular endothelial cells (BMECs) changes expression of multiple genes involved in vascular development. These changes include suppression of Thbs1, which encodes thrombospondin1 (TSP1) and has been ascribed to KLF2- and KLF4-mediated repression of Thbs1 In vitro reconstitution of TSP1 with either full-length TSP1 or 3TSR, an anti-angiogenic TSP1 fragment, suppresses heightened vascular endothelial growth factor signaling and preserves BMEC tight junctions. Furthermore, administration of 3TSR prevents the development of lesions in a mouse model of CCM1 (Krit1ECKO ) as judged by histology and quantitative micro-computed tomography. Conversely, reduced TSP1 expression contributes to the pathogenesis of CCM, because inactivation of one or two copies of Thbs1 exacerbated CCM formation. Thus, loss of Krit1 function disables an angiogenic checkpoint to enable CCM formation. These results suggest that 3TSR, or other angiogenesis inhibitors, can be repurposed for TSP1 replacement therapy for CCMs.

MeSH terms

  • Animals
  • Cells, Cultured
  • Endothelial Cells / metabolism
  • Gene Expression Profiling / methods
  • Genetic Therapy / methods*
  • HEK293 Cells
  • Hemangioma, Cavernous, Central Nervous System / genetics
  • Hemangioma, Cavernous, Central Nervous System / metabolism*
  • Hemangioma, Cavernous, Central Nervous System / therapy*
  • Humans
  • KRIT1 Protein / genetics
  • KRIT1 Protein / metabolism*
  • Kruppel-Like Factor 4
  • Kruppel-Like Transcription Factors / genetics
  • Kruppel-Like Transcription Factors / metabolism
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • RNA Interference
  • Thrombospondin 1 / genetics
  • Thrombospondin 1 / metabolism*

Substances

  • KLF4 protein, human
  • KRIT1 Protein
  • Klf2 protein, mouse
  • Klf4 protein, mouse
  • Kruppel-Like Factor 4
  • Kruppel-Like Transcription Factors
  • Thrombospondin 1
  • Thbs1 protein, mouse