Differential localization and anabolic responsiveness of mTOR complexes in human skeletal muscle in response to feeding and exercise

Am J Physiol Cell Physiol. 2017 Dec 1;313(6):C604-C611. doi: 10.1152/ajpcell.00176.2017. Epub 2017 Sep 27.

Abstract

Mechanistic target of rapamycin (mTOR) resides as two complexes within skeletal muscle. mTOR complex 1 [mTORC1-regulatory associated protein of mTOR (Raptor) positive] regulates skeletal muscle growth, whereas mTORC2 [rapamycin-insensitive companion of mTOR (Rictor) positive] regulates insulin sensitivity. To examine the regulation of these complexes in human skeletal muscle, we utilized immunohistochemical analysis to study the localization of mTOR complexes before and following protein-carbohydrate feeding (FED) and resistance exercise plus protein-carbohydrate feeding (EXFED) in a unilateral exercise model. In basal samples, mTOR and the lysosomal marker lysosomal associated membrane protein 2 (LAMP2) were highly colocalized and remained so throughout. In the FED and EXFED states, mTOR/LAMP2 complexes were redistributed to the cell periphery [wheat germ agglutinin (WGA)-positive staining] (time effect; P = 0.025), with 39% (FED) and 26% (EXFED) increases in mTOR/WGA association observed 1 h post-feeding/exercise. mTOR/WGA colocalization continued to increase in EXFED at 3 h (48% above baseline) whereas colocalization decreased in FED (21% above baseline). A significant effect of condition (P = 0.05) was noted suggesting mTOR/WGA colocalization was greater during EXFED. This pattern was replicated in Raptor/WGA association, where a significant difference between EXFED and FED was noted at 3 h post-exercise/feeding (P = 0.014). Rictor/WGA colocalization remained unaltered throughout the trial. Alterations in mTORC1 cellular location coincided with elevated S6K1 kinase activity, which rose to a greater extent in EXFED compared with FED at 1 h post-exercise/feeding (P < 0.001), and only remained elevated in EXFED at the 3 h time point (P = 0.037). Collectively these data suggest that mTORC1 redistribution within the cell is a fundamental response to resistance exercise and feeding, whereas mTORC2 is predominantly situated at the sarcolemma and does not alter localization.

Keywords: Raptor; Rictor; lysosome; mTORC1; mTORC2.

MeSH terms

  • Adult
  • Dietary Carbohydrates / administration & dosage
  • Dietary Proteins / administration & dosage
  • Eating*
  • Energy Metabolism*
  • Exercise*
  • Humans
  • Lysosomal-Associated Membrane Protein 2 / metabolism
  • Lysosomes / enzymology
  • Male
  • Mechanistic Target of Rapamycin Complex 1 / metabolism*
  • Mechanistic Target of Rapamycin Complex 2 / metabolism*
  • Muscle Contraction
  • Protein Transport
  • Proto-Oncogene Proteins c-akt / metabolism
  • Quadriceps Muscle / enzymology*
  • Rapamycin-Insensitive Companion of mTOR Protein / metabolism
  • Regulatory-Associated Protein of mTOR / metabolism
  • Resistance Training
  • Ribosomal Protein S6 Kinases, 70-kDa / metabolism
  • Sarcolemma / enzymology
  • Time Factors
  • Young Adult

Substances

  • Dietary Carbohydrates
  • Dietary Proteins
  • LAMP2 protein, human
  • Lysosomal-Associated Membrane Protein 2
  • RICTOR protein, human
  • RPTOR protein, human
  • Rapamycin-Insensitive Companion of mTOR Protein
  • Regulatory-Associated Protein of mTOR
  • Mechanistic Target of Rapamycin Complex 1
  • Mechanistic Target of Rapamycin Complex 2
  • Proto-Oncogene Proteins c-akt
  • Ribosomal Protein S6 Kinases, 70-kDa
  • ribosomal protein S6 kinase, 70kD, polypeptide 1