The energy sensor AMPK regulates T cell metabolic adaptation and effector responses in vivo

Immunity. 2015 Jan 20;42(1):41-54. doi: 10.1016/j.immuni.2014.12.030. Epub 2015 Jan 2.

Abstract

Naive T cells undergo metabolic reprogramming to support the increased energetic and biosynthetic demands of effector T cell function. However, how nutrient availability influences T cell metabolism and function remains poorly understood. Here we report plasticity in effector T cell metabolism in response to changing nutrient availability. Activated T cells were found to possess a glucose-sensitive metabolic checkpoint controlled by the energy sensor AMP-activated protein kinase (AMPK) that regulated mRNA translation and glutamine-dependent mitochondrial metabolism to maintain T cell bioenergetics and viability. T cells lacking AMPKα1 displayed reduced mitochondrial bioenergetics and cellular ATP in response to glucose limitation in vitro or pathogenic challenge in vivo. Finally, we demonstrated that AMPKα1 is essential for T helper 1 (Th1) and Th17 cell development and primary T cell responses to viral and bacterial infections in vivo. Our data highlight AMPK-dependent regulation of metabolic homeostasis as a key regulator of T cell-mediated adaptive immunity.

Publication types

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

MeSH terms

  • AMP-Activated Protein Kinases / genetics
  • AMP-Activated Protein Kinases / metabolism*
  • Adaptation, Physiological / immunology
  • Animals
  • CD4-Positive T-Lymphocytes / physiology*
  • CD8-Positive T-Lymphocytes / physiology*
  • Cells, Cultured
  • Cellular Reprogramming / genetics
  • Cellular Reprogramming / immunology
  • Energy Metabolism
  • Glucose / metabolism
  • Glutamine / metabolism
  • Humans
  • Immunomodulation
  • Influenza A Virus, H1N1 Subtype / immunology*
  • Lymphocyte Activation / genetics
  • Metabolomics
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Orthomyxoviridae Infections / immunology
  • Orthomyxoviridae Infections / metabolism*
  • Protein Biosynthesis / genetics

Substances

  • Glutamine
  • AMPK alpha1 subunit, mouse
  • AMP-Activated Protein Kinases
  • Glucose