Identification of transmembrane protein 168 mutation in familial Brugada syndrome

  • FASEB J. 2020 May;34(5):6399-6417. doi: 10.1096/fj.201902991R.
Akio Shimizu  1 Dimitar P Zankov  1  2 Akira Sato  1 Masahiro Komeno  1 Futoshi Toyoda  3 Satoru Yamazaki  4 Toshinori Makita  5 Taichi Noda  6 Masahito Ikawa  6 Yoshihiro Asano  7 Yohei Miyashita  8 Seiji Takashima  9 Hiroshi Morita  10 Taisuke Ishikawa  11 Naomasa Makita  11 Masahito Hitosugi  12 Hiroshi Matsuura  3 Seiko Ohno  2  13 Minoru Horie  13 Hisakazu Ogita  1
Affiliations
  • 1. Division of Molecular Medical Biochemistry, Department of Biochemistry and Molecular Biology, Shiga University of Medical Science, Otsu, Japan.
  • 2. Department of Bioscience and Genetics, National Cerebral and Cardiovascular Center, Suita, Japan.
  • 3. Division of Cell Physiology, Department of Physiology, Shiga University of Medical Science, Otsu, Japan.
  • 4. Department of Molecular Pharmacology, National Cerebral and Cardiovascular Center, Suita, Japan.
  • 5. Division of Cardiac Electrophysiology, Department of Cardiovascular Center, Osaka Red Cross Hospital, Osaka, Japan.
  • 6. Animal Resource Center for Infectious Diseases, Research Institute for Microbial Diseases, Osaka University, Suita, Japan.
  • 7. Department of Cardiovascular Medicine, Osaka University Graduate School of Medicine, Suita, Japan.
  • 8. Department of Legal Medicine, Osaka University Graduate School of Medicine, Suita, Japan.
  • 9. Department of Medical Biochemistry, Osaka University Graduate School of Medicine, Suita, Japan.
  • 10. Department of Cardiovascular Therapeutics, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University, Okayama, Japan.
  • 11. Omics Research Center, National Cerebral and Cardiovascular Center, Suita, Japan.
  • 12. Department of Legal Medicine, Shiga University of Medical Science, Otsu, Japan.
  • 13. Center for Epidemiologic Research in Asia, Shiga University of Medical Science, Otsu, Japan.
Abstract

Brugada syndrome (BrS) is an inherited channelopathy responsible for almost 20% of sudden cardiac deaths in patients with nonstructural cardiac diseases. Approximately 70% of BrS patients, the causative gene mutation(s) remains unknown. In this study, we used whole exome Sequencing to investigate candidate mutations in a family clinically diagnosed with BrS. A heterozygous 1616G>A substitution (R539Q mutation) was identified in the transmembrane protein 168 (TMEM168) gene of symptomatic individuals. Similar to endogenous TMEM168, both TMEM168 wild-type (WT) and mutant proteins that were ectopically induced in HL-1 cells showed nuclear membrane localization. A significant decrease in Na+ current and Nav 1.5 protein expression was observed in HL-1 cardiomyocytes expressing mutant TMEM168. Ventricular tachyarrhythmias and conduction disorders were induced in the heterozygous Tmem168 1616G>A knock-in mice by pharmacological stimulation, but not in WT mice. Na+ current was reduced in ventricular cardiomyocytes isolated from the Tmem168 knock-in heart, and Nav 1.5 expression was also impaired. This impairment was dependent on increased Nedd4-2 binding to Nav 1.5 and subsequent ubiquitination. Collectively, our results show an association between the TMEM168 1616G>A mutation and arrhythmogenesis in a family with BrS.

Keywords
fatal ventricular arrhythmia; sodium channel; ubiquitination.