The Bone Marrow Protects and Optimizes Immunological Memory during Dietary Restriction

Cell. 2019 Aug 22;178(5):1088-1101.e15. doi: 10.1016/j.cell.2019.07.049.

Abstract

Mammals evolved in the face of fluctuating food availability. How the immune system adapts to transient nutritional stress remains poorly understood. Here, we show that memory T cells collapsed in secondary lymphoid organs in the context of dietary restriction (DR) but dramatically accumulated within the bone marrow (BM), where they adopted a state associated with energy conservation. This response was coordinated by glucocorticoids and associated with a profound remodeling of the BM compartment, which included an increase in T cell homing factors, erythropoiesis, and adipogenesis. Adipocytes, as well as CXCR4-CXCL12 and S1P-S1P1R interactions, contributed to enhanced T cell accumulation in BM during DR. Memory T cell homing to BM during DR was associated with enhanced protection against infections and tumors. Together, this work uncovers a fundamental host strategy to sustain and optimize immunological memory during nutritional challenges that involved a temporal and spatial reorganization of the memory pool within "safe haven" compartments.

Publication types

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

MeSH terms

  • Animals
  • Bone Marrow / immunology
  • Bone Marrow / metabolism*
  • CD8-Positive T-Lymphocytes / cytology
  • CD8-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / metabolism
  • Caloric Restriction / veterinary
  • Cell Line, Tumor
  • Chemokine CXCL12 / metabolism
  • Diet, Reducing / veterinary
  • Energy Metabolism
  • Gene Expression Regulation
  • Glucocorticoids
  • Immunologic Memory*
  • Melanoma, Experimental / mortality
  • Melanoma, Experimental / pathology
  • Mice
  • Mice, Inbred C57BL
  • Proto-Oncogene Proteins c-akt / metabolism
  • Receptors, CXCR4 / metabolism
  • Survival Rate
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism
  • TOR Serine-Threonine Kinases / metabolism

Substances

  • Chemokine CXCL12
  • Glucocorticoids
  • Receptors, CXCR4
  • mTOR protein, mouse
  • Proto-Oncogene Proteins c-akt
  • TOR Serine-Threonine Kinases