Organic cation transporter 1 (OCT1) modulates multiple cardiometabolic traits through effects on hepatic thiamine content

PLoS Biol. 2018 Apr 16;16(4):e2002907. doi: 10.1371/journal.pbio.2002907. eCollection 2018 Apr.

Abstract

A constellation of metabolic disorders, including obesity, dysregulated lipids, and elevations in blood glucose levels, has been associated with cardiovascular disease and diabetes. Analysis of data from recently published genome-wide association studies (GWAS) demonstrated that reduced-function polymorphisms in the organic cation transporter, OCT1 (SLC22A1), are significantly associated with higher total cholesterol, low-density lipoprotein (LDL) cholesterol, and triglyceride (TG) levels and an increased risk for type 2 diabetes mellitus, yet the mechanism linking OCT1 to these metabolic traits remains puzzling. Here, we show that OCT1, widely characterized as a drug transporter, plays a key role in modulating hepatic glucose and lipid metabolism, potentially by mediating thiamine (vitamin B1) uptake and hence its levels in the liver. Deletion of Oct1 in mice resulted in reduced activity of thiamine-dependent enzymes, including pyruvate dehydrogenase (PDH), which disrupted the hepatic glucose-fatty acid cycle and shifted the source of energy production from glucose to fatty acids, leading to a reduction in glucose utilization, increased gluconeogenesis, and altered lipid metabolism. In turn, these effects resulted in increased total body adiposity and systemic levels of glucose and lipids. Importantly, wild-type mice on thiamine deficient diets (TDs) exhibited impaired glucose metabolism that phenocopied Oct1 deficient mice. Collectively, our study reveals a critical role of hepatic thiamine deficiency through OCT1 deficiency in promoting the metabolic inflexibility that leads to the pathogenesis of cardiometabolic disease.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blood Glucose / metabolism
  • Cholesterol, HDL / blood
  • Cholesterol, LDL / blood
  • Diabetes Mellitus, Experimental / genetics*
  • Diabetes Mellitus, Experimental / metabolism
  • Diabetes Mellitus, Experimental / pathology
  • Diabetes Mellitus, Type 2 / genetics*
  • Diabetes Mellitus, Type 2 / metabolism
  • Diabetes Mellitus, Type 2 / pathology
  • Fatty Acids / metabolism
  • Gene Expression Regulation
  • Gluconeogenesis / genetics
  • Humans
  • Ketone Oxidoreductases / genetics
  • Ketone Oxidoreductases / metabolism
  • Lipid Metabolism / genetics
  • Liver / metabolism
  • Liver / pathology
  • Longevity / genetics*
  • Mice
  • Mice, Knockout
  • Obesity / genetics*
  • Obesity / metabolism
  • Obesity / pathology
  • Octamer Transcription Factor-1 / deficiency
  • Octamer Transcription Factor-1 / genetics*
  • Signal Transduction
  • Thiamine / metabolism*
  • Thiamine Deficiency / genetics*
  • Thiamine Deficiency / metabolism
  • Thiamine Deficiency / pathology
  • Triglycerides / blood

Substances

  • Blood Glucose
  • Cholesterol, HDL
  • Cholesterol, LDL
  • Fatty Acids
  • Octamer Transcription Factor-1
  • Pou2f1 protein, mouse
  • Triglycerides
  • Ketone Oxidoreductases
  • pyruvate dehydrogenase (NADP+)
  • Thiamine