Lesions from patients with sporadic cerebral cavernous malformations harbor somatic mutations in the CCM genes: evidence for a common biochemical pathway for CCM pathogenesis

Hum Mol Genet. 2014 Aug 15;23(16):4357-70. doi: 10.1093/hmg/ddu153. Epub 2014 Apr 3.

Abstract

Cerebral cavernous malformations (CCMs) are vascular lesions affecting the central nervous system. CCM occurs either sporadically or in an inherited, autosomal dominant manner. Constitutional (germline) mutations in any of three genes, KRIT1, CCM2 and PDCD10, can cause the inherited form. Analysis of CCM lesions from inherited cases revealed biallelic somatic mutations, indicating that CCM follows a Knudsonian two-hit mutation mechanism. It is still unknown, however, if the sporadic cases of CCM also follow this genetic mechanism. We extracted DNA from 11 surgically excised lesions from sporadic CCM patients, and sequenced the three CCM genes in each specimen using a next-generation sequencing approach. Four sporadic CCM lesion samples (36%) were found to contain novel somatic mutations. Three of the lesions contained a single somatic mutation, and one lesion contained two biallelic somatic mutations. Herein, we also describe evidence of somatic mosaicism in a patient presenting with over 130 CCM lesions localized to one hemisphere of the brain. Finally, in a lesion regrowth sample, we found that the regrown CCM lesion contained the same somatic mutation as the original lesion. Together, these data bolster the idea that all forms of CCM have a genetic underpinning of the two-hit mutation mechanism in the known CCM genes. Recent studies have found aberrant Rho kinase activation in inherited CCM pathogenesis, and we present evidence that this pathway is activated in sporadic CCM patients. These results suggest that all CCM patients, including those with the more common sporadic form, are potentially amenable to the same therapy.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Apoptosis Regulatory Proteins / genetics*
  • Carrier Proteins / genetics*
  • Central Nervous System Neoplasms / genetics*
  • Central Nervous System Neoplasms / pathology
  • Endothelial Cells / metabolism
  • Hemangioma, Cavernous, Central Nervous System / genetics*
  • Hemangioma, Cavernous, Central Nervous System / pathology
  • Humans
  • KRIT1 Protein
  • Membrane Proteins / genetics*
  • Microtubule-Associated Proteins / genetics*
  • Mutation*
  • Proto-Oncogene Proteins / genetics*
  • rho-Associated Kinases / metabolism

Substances

  • Apoptosis Regulatory Proteins
  • CCM2 protein, human
  • Carrier Proteins
  • KRIT1 Protein
  • KRIT1 protein, human
  • Membrane Proteins
  • Microtubule-Associated Proteins
  • PDCD10 protein, human
  • Proto-Oncogene Proteins
  • rho-Associated Kinases