ETFDH Mutations and Flavin Adenine Dinucleotide Homeostasis Disturbance Are Essential for Developing Riboflavin-Responsive Multiple Acyl-Coenzyme A Dehydrogenation Deficiency

Ann Neurol. 2018 Nov;84(5):659-673. doi: 10.1002/ana.25338. Epub 2018 Oct 19.

Abstract

Objective: Riboflavin-responsive multiple acyl-coenzyme A dehydrogenation deficiency (RR-MADD) is an inherited fatty acid metabolism disorder mainly caused by genetic defects in electron transfer flavoprotein-ubiquinone oxidoreductase (ETF:QO). The variant ETF:QO protein folding deficiency, which can be corrected by therapeutic dosage of riboflavin supplement, has been identified in HEK-293 cells and is believed to be the molecular mechanism of this disease. To verify this hypothesis in vivo, we generated Etfdh (h)A84T knockin (KI) mice.

Methods: Tissues from these mice as well as muscle biopsies and fibroblasts from 7 RR-MADD patients were used to examine the flavin adenine dinucleotide (FAD) concentration and ETF:QO protein amount.

Results: All of the homozygous KI mice (Etfdh (h)A84T/(h)A84T , KI/KI) were initially normal. After being given a high-fat and vitamin B2 -deficient (HF-B2 D) diet for 5 weeks, they developed weight loss, movement ability defects, lipid storage in muscle and liver, and elevated serum acyl-carnitine levels, which are clinically and biochemically similar to RR-MADD patients. Both ETF:QO protein and FAD concentrations were significantly decreased in tissues of HF-B2 D-KI/KI mice and in cultured fibroblasts from RR-MADD patients. After riboflavin treatment, ETF:QO protein increased in proportion to elevated FAD concentrations, but not related to mRNA levels. These results were further confirmed in cultured fibroblasts from RR-MADD patients.

Interpretation: For the first time, we successfully developed a RR-MADD mice model and confirmed that FAD homeostasis disturbances played a crucial role on the pathomechanism of RR-MADD in this mouse model and culture cells from patients. Supplementation of riboflavin may stabilize variant ETF:QO protein by rebuilding FAD homeostasis. Ann Neurol 2018;84:667-681.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Disease Models, Animal
  • Electron-Transferring Flavoproteins / genetics*
  • Female
  • Flavin-Adenine Dinucleotide / metabolism*
  • Gene Knock-In Techniques
  • Homeostasis / physiology
  • Humans
  • Iron-Sulfur Proteins / genetics*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Multiple Acyl Coenzyme A Dehydrogenase Deficiency / genetics*
  • Multiple Acyl Coenzyme A Dehydrogenase Deficiency / metabolism*
  • Multiple Acyl Coenzyme A Dehydrogenase Deficiency / physiopathology*
  • Mutation
  • Oxidoreductases Acting on CH-NH Group Donors / genetics*

Substances

  • Electron-Transferring Flavoproteins
  • Iron-Sulfur Proteins
  • Flavin-Adenine Dinucleotide
  • Oxidoreductases Acting on CH-NH Group Donors
  • electron-transferring-flavoprotein dehydrogenase