Naturally occurring UBIAD1 mutations differentially affect menaquinone biosynthesis and vitamin K-dependent carboxylation

FEBS J. 2022 May;289(9):2613-2627. doi: 10.1111/febs.16291. Epub 2021 Dec 1.

Abstract

UbiA prenyltransferase domain-containing protein-1 (UBIAD1) is responsible for the biosynthesis of menaquinone-4 (MK-4), a cofactor for extrahepatic carboxylation of vitamin K-dependent (VKD) proteins. Genetic variations of UBIAD1 are mainly associated with Schnyder corneal dystrophy (SCD), a disease characterized by abnormal accumulation of cholesterol in the cornea. Results from in vitro studies demonstrate that SCD-associated UBIAD1 mutations are defective in MK-4 biosynthesis. However, SCD patients do not exhibit typical phenotypes associated with defects of MK-4 or VKD carboxylation. Here, we coupled UBIAD1's biosynthetic activity of MK-4 with VKD carboxylation in HEK293 cells that stably express a chimeric VKD reporter protein. The endogenous Ubiad1 gene in these cells was knocked out by CRISPR-Cas9-mediated genome editing. The effect of UBIAD1 mutations on MK-4 biosynthesis and VKD carboxylation was evaluated in Ubiad1-deficient reporter cells by determining the production of MK-4 or by measuring the efficiency of reporter-protein carboxylation. Our results show that the hot-spot mutation N102S has a moderate impact on MK-4 biosynthesis (retained ˜ 82% activity) but does not affect VKD carboxylation. However, the G186R mutation significantly affected both MK-4 biosynthesis and VKD carboxylation. Other mutations exhibit varying degrees of effects on MK-4 biosynthesis and VKD carboxylation. These results are consistent with in vivo results obtained from gene knock-in mice and SCD patients. Our findings suggest that UBIAD1's MK-4 biosynthetic activity does not directly correlate with the phenotypes of SCD patients. The established cell-based assays in this study provide a powerful tool for the functional studies of UBIAD1 in a cellular milieu.

Keywords: Schnyder corneal dystrophy; UBIAD1; cholesterol; menaquinone; vitamin K-dependent carboxylation.

Publication types

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

MeSH terms

  • Animals
  • Corneal Dystrophies, Hereditary
  • Dimethylallyltranstransferase* / genetics
  • Dimethylallyltranstransferase* / metabolism
  • HEK293 Cells
  • Humans
  • Mice
  • Mutation
  • Vitamin K 2 / metabolism
  • Vitamin K* / genetics
  • Vitamin K* / metabolism

Substances

  • Vitamin K 2
  • Vitamin K
  • Dimethylallyltranstransferase
  • Ubiad1 protein, mouse

Supplementary concepts

  • Corneal Dystrophy, Crystalline, of Schnyder