Fatty acid transport protein 1 (FATP1) localizes in mitochondria in mouse skeletal muscle and regulates lipid and ketone body disposal

PLoS One. 2014 May 23;9(5):e98109. doi: 10.1371/journal.pone.0098109. eCollection 2014.

Abstract

FATP1 mediates skeletal muscle cell fatty acid import, yet its intracellular localization and metabolic control role are not completely defined. Here, we examine FATP1 localization and metabolic effects of its overexpression in mouse skeletal muscle. The FATP1 protein was detected in mitochondrial and plasma membrane fractions, obtained by differential centrifugation, of mouse gastrocnemius muscle. FATP1 was most abundant in purified mitochondria, and in the outer membrane and soluble intermembrane, but not in the inner membrane plus matrix, enriched subfractions of purified mitochondria. Immunogold electron microscopy localized FATP1-GFP in mitochondria of transfected C2C12 myotubes. FATP1 was overexpressed in gastrocnemius mouse muscle, by adenovirus-mediated delivery of the gene into hindlimb muscles of newborn mice, fed after weaning a chow or high-fat diet. Compared to GFP delivery, FATP1 did not alter body weight, serum fed glucose, insulin and triglyceride levels, and whole-body glucose tolerance, in either diet. However, fatty acid levels were lower and β-hydroxybutyrate levels were higher in FATP1- than GFP-mice, irrespective of diet. Moreover, intramuscular triglyceride content was lower in FATP1- versus GFP-mice regardless of diet, and β-hydroxybutyrate content was unchanged in high-fat-fed mice. Electroporation-mediated FATP1 overexpression enhanced palmitate oxidation to CO2, but not to acid-soluble intermediate metabolites, while CO2 production from β-hydroxybutyrate was inhibited and that from glucose unchanged, in isolated mouse gastrocnemius strips. In summary, FATP1 was localized in mitochondria, in the outer membrane and intermembrane parts, of mouse skeletal muscle, what may be crucial for its metabolic effects. Overexpressed FATP1 enhanced disposal of both systemic fatty acids and intramuscular triglycerides. Consistently, it did not contribute to the high-fat diet-induced metabolic dysregulation. However, FATP1 lead to hyperketonemia, likely secondary to the sparing of ketone body oxidation by the enhanced oxidation of fatty acids.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3-Hydroxybutyric Acid / metabolism
  • Adenoviridae / genetics
  • Animals
  • Blood Glucose / metabolism
  • Cell Line
  • Coenzyme A-Transferases / genetics
  • Diet, High-Fat / adverse effects
  • Fatty Acid Transport Proteins / genetics
  • Fatty Acid Transport Proteins / metabolism*
  • Fatty Acids / metabolism
  • Gene Expression Regulation / drug effects
  • Hydroxymethylglutaryl-CoA Synthase / genetics
  • Insulin / metabolism
  • Ketone Bodies / metabolism*
  • Lipid Metabolism* / drug effects
  • Mice
  • Mitochondria / drug effects
  • Mitochondria / metabolism*
  • Muscle Cells / cytology
  • Muscle Cells / drug effects
  • Muscle Cells / metabolism
  • Muscle, Skeletal / cytology*
  • Muscle, Skeletal / drug effects
  • Oxidation-Reduction
  • Palmitates / metabolism
  • Protein Kinases / genetics
  • Protein Transport / drug effects
  • Triglycerides / metabolism

Substances

  • Blood Glucose
  • Fatty Acid Transport Proteins
  • Fatty Acids
  • Insulin
  • Ketone Bodies
  • Palmitates
  • Slc27a1 protein, mouse
  • Triglycerides
  • Hydroxymethylglutaryl-CoA Synthase
  • Protein Kinases
  • pyruvate dehydrogenase kinase 4
  • Coenzyme A-Transferases
  • 3-ketoacid CoA-transferase
  • 3-Hydroxybutyric Acid

Grants and funding

This study was supported by the following grants: SAF2009-07559 and SAF2012-37480 from the Spanish Ministerio de Ciencia e Innovación (MCI); and PI 08/0733, PI08/1195, CIBERDEM de Diabetes y Enfermedades Metabólicas Asociadas (CB07/08/0012). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.