Aging Suppresses Sphingosine-1-Phosphate Chaperone ApoM in Circulation Resulting in Maladaptive Organ Repair

Dev Cell. 2020 Jun 22;53(6):677-690.e4. doi: 10.1016/j.devcel.2020.05.024. Epub 2020 Jun 15.

Abstract

Here, we show that the liver-derived apolipoprotein M (ApoM) protects the lung and kidney from pro-fibrotic insults and that this circulating factor is attenuated in aged mice. Aged mouse hepatocytes exhibit transcriptional suppression of ApoM. This leads to reduced sphingosine-1-phosphate (S1P) signaling via the S1P receptor 1 (S1PR1) in the vascular endothelial cells of lung and kidney. Suboptimal S1PR1 angiocrine signaling causes reduced resistance to injury-induced vascular leak and leads to organ fibrosis. Plasma transfusion from Apom transgenic mice but not Apom knockout mice blocked fibrosis in the lung. Similarly, infusion of recombinant therapeutics, ApoM-Fc fusion protein enhanced kidney and lung regeneration and attenuated fibrosis in aged mouse after injury. Furthermore, we identified that aging alters Sirtuin-1-hepatic nuclear factor 4α circuit in hepatocytes to downregulate ApoM. These data reveal an integrative organ adaptation that involves circulating S1P chaperone ApoM+ high density lipoprotein (HDL), which signals via endothelial niche S1PR1 to spur regeneration over fibrosis.

Keywords: aging; endothelial cell; fibrosis; kidney repair; lipoprotein; lung regeneration; sphingosine-1-phosphate receptor; vascular barrier; vascular niche.

Publication types

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

MeSH terms

  • Aging / blood
  • Aging / metabolism*
  • Aging / pathology
  • Animals
  • Apolipoproteins M / blood
  • Apolipoproteins M / genetics
  • Apolipoproteins M / metabolism*
  • Cell Communication
  • Cells, Cultured
  • Endothelium, Vascular / metabolism
  • Female
  • Fibrosis
  • Hepatocytes / metabolism
  • Kidney / growth & development
  • Kidney / metabolism*
  • Kidney / pathology
  • Lung / growth & development
  • Lung / metabolism*
  • Lung / pathology
  • Lysophospholipids / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Regeneration*
  • Sphingosine / analogs & derivatives*
  • Sphingosine / metabolism
  • Sphingosine-1-Phosphate Receptors / metabolism

Substances

  • ApoM protein, mouse
  • Apolipoproteins M
  • Lysophospholipids
  • S1pr1 protein, mouse
  • Sphingosine-1-Phosphate Receptors
  • sphingosine 1-phosphate
  • Sphingosine