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Distinct cellular roles for PDCD10 define a gut-brain axis in cerebral cavernous malformation.

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Area of Science:

  • Genetics
  • Neuroscience
  • Gastroenterology

Background:

  • Cerebral cavernous malformation (CCM) is a genetic cerebrovascular disorder.
  • Mutations in KRIT1, CCM2, or PDCD10 cause familial CCM, with PDCD10 mutations leading to earlier, more severe disease.
  • Existing research suggests a gut-brain axis in CCM, linked to gut microbiome-derived lipopolysaccharide stimulating TLR4 and MEKK3 signaling.

Purpose of the Study:

  • To define the gut-brain axis in CCM and explain the severe prognosis associated with PDCD10 mutations.
  • To investigate the role of the gut barrier integrity as a determinant of CCM disease course.
  • To explore therapeutic strategies targeting the gut-brain axis in CCM.

Main Methods:

  • Utilized a mouse model of CCM, chemically disrupting the gut barrier with dextran sulfate sodium.
  • Generated mice with genetic loss of Pdcd10 or Krit1 specifically in gut epithelial cells.
  • Assessed CCM formation following loss of Mucin-2 or exposure to dietary emulsifiers.
  • Evaluated the effect of dexamethasone treatment on CCM formation in mice.

Main Results:

  • Gut barrier disruption, independent of microbiome composition, significantly augmented CCM formation.
  • Genetic loss of Pdcd10 in gut epithelial cells, but not Krit1, led to colonic mucosal barrier disruption and increased CCM burden.
  • Loss of Mucin-2 or exposure to dietary emulsifiers mimicked the effect of Pdcd10 loss, increasing CCM burden.
  • Dexamethasone treatment potently inhibited CCM formation by acting on both brain endothelial and gut epithelial cells.

Conclusions:

  • The gut barrier integrity is a critical determinant of CCM disease severity, particularly in PDCD10-deficient individuals.
  • PDCD10 plays a crucial role in maintaining gut epithelial function and colonic mucosal barrier integrity.
  • These findings establish a gut-brain CCM disease axis where gut epithelial function is as vital as brain endothelial signaling, offering new therapeutic targets.