A human importin-β-related disorder: Syndromic thoracic aortic aneurysm caused by bi-allelic loss-of-function variants in IPO8

Am J Hum Genet. 2021 Jun 3;108(6):1115-1125. doi: 10.1016/j.ajhg.2021.04.019. Epub 2021 May 18.

Abstract

Importin 8, encoded by IPO8, is a ubiquitously expressed member of the importin-β protein family that translocates cargo molecules such as proteins, RNAs, and ribonucleoprotein complexes into the nucleus in a RanGTP-dependent manner. Current knowledge of the cargoes of importin 8 is limited, but TGF-β signaling components such as SMAD1-4 have been suggested to be among them. Here, we report that bi-allelic loss-of-function variants in IPO8 cause a syndromic form of thoracic aortic aneurysm (TAA) with clinical overlap with Loeys-Dietz and Shprintzen-Goldberg syndromes. Seven individuals from six unrelated families showed a consistent phenotype with early-onset TAA, motor developmental delay, connective tissue findings, and craniofacial dysmorphic features. A C57BL/6N Ipo8 knockout mouse model recapitulates TAA development from 8-12 weeks onward in both sexes but most prominently shows ascending aorta dilatation with a propensity for dissection in males. Compliance assays suggest augmented passive stiffness of the ascending aorta in male Ipo8-/- mice throughout life. Immunohistological investigation of mutant aortic walls reveals elastic fiber disorganization and fragmentation along with a signature of increased TGF-β signaling, as evidenced by nuclear pSmad2 accumulation. RT-qPCR assays of the aortic wall in male Ipo8-/- mice demonstrate decreased Smad6/7 and increased Mmp2 and Ccn2 (Ctgf) expression, reinforcing a role for dysregulation of the TGF-β signaling pathway in TAA development. Because importin 8 is the most downstream TGF-β-related effector implicated in TAA pathogenesis so far, it offers opportunities for future mechanistic studies and represents a candidate drug target for TAA.

Keywords: Loeys-Dietz syndrome; Shprintzen-Goldberg syndrome; TGF-beta; importin 8; knockout mouse model; thoracic aortic aneurysm.

Publication types

  • Case Reports
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • Aortic Aneurysm, Thoracic / etiology*
  • Aortic Aneurysm, Thoracic / metabolism
  • Aortic Aneurysm, Thoracic / pathology
  • Child
  • Child, Preschool
  • Female
  • Humans
  • Loss of Function Mutation*
  • Loss of Heterozygosity*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Pedigree
  • Phenotype*
  • Signal Transduction
  • Syndrome
  • Transforming Growth Factor beta / genetics
  • Transforming Growth Factor beta / metabolism
  • Young Adult
  • beta Karyopherins / genetics*
  • beta Karyopherins / metabolism

Substances

  • IPO8 protein, human
  • Transforming Growth Factor beta
  • beta Karyopherins