CIC de novo loss of function variants contribute to cerebral folate deficiency by downregulating FOLR1 expression

J Med Genet. 2021 Jul;58(7):484-494. doi: 10.1136/jmedgenet-2020-106987. Epub 2020 Aug 20.

Abstract

Background Cerebral folate deficiency (CFD) syndrome is characterised by a low concentration of 5-methyltetrahydrofolate in cerebrospinal fluid, while folate levels in plasma and red blood cells are in the low normal range. Mutations in several folate pathway genes, including FOLR1 (folate receptor alpha, FRα), DHFR (dihydrofolate reductase) and PCFT (proton coupled folate transporter) have been previously identified in patients with CFD. Methods In an effort to identify causal mutations for CFD, we performed whole exome sequencing analysis on eight CFD trios and identified eight de novo mutations in seven trios. Results Notably, we found a de novo stop gain mutation in the capicua (CIC) gene. Using 48 sporadic CFD samples as a validation cohort, we identified three additional rare variants in CIC that are putatively deleterious mutations. Functional analysis indicates that CIC binds to an octameric sequence in the promoter regions of folate transport genes: FOLR1, PCFT and reduced folate carrier (Slc19A1; RFC1). The CIC nonsense variant (p.R353X) downregulated FOLR1 expression in HeLa cells as well as in the induced pluripotent stem cell (iPSCs) derived from the original CFD proband. Folate binding assay demonstrated that the p.R353X variant decreased cellular binding of folic acid in cells. Conclusion This study indicates that CIC loss of function variants can contribute to the genetic aetiology of CFD through regulating FOLR1 expression. Our study described the first mutations in a non-folate pathway gene that can contribute to the aetiology of CFD.

Keywords: clinical genetics; genetics; genome-wide; nutrition and metabolism.

Publication types

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

MeSH terms

  • Cells, Cultured
  • Cerebrum / metabolism*
  • Down-Regulation
  • Female
  • Folate Receptor 1 / deficiency
  • Folate Receptor 1 / genetics*
  • Folic Acid Deficiency / cerebrospinal fluid*
  • Folic Acid Deficiency / genetics
  • HEK293 Cells
  • Humans
  • Loss of Function Mutation*
  • Male
  • Nervous System Diseases / cerebrospinal fluid*
  • Nervous System Diseases / genetics
  • Neuroaxonal Dystrophies
  • Pedigree
  • Repressor Proteins / genetics*
  • Sequence Analysis, DNA
  • Tetrahydrofolates / cerebrospinal fluid*

Substances

  • CIC protein, human
  • FOLR1 protein, human
  • Folate Receptor 1
  • Repressor Proteins
  • Tetrahydrofolates
  • 5-methyltetrahydrofolate

Supplementary concepts

  • Neurodegeneration Due To Cerebral Folate Transport Deficiency