Identification of ApoA4 as a sphingosine 1-phosphate chaperone in ApoM- and albumin-deficient mice

J Lipid Res. 2019 Nov;60(11):1912-1921. doi: 10.1194/jlr.RA119000277. Epub 2019 Aug 28.

Abstract

HDL-bound ApoM and albumin are protein chaperones for the circulating bioactive lipid, sphingosine 1-phosphate (S1P); in this role, they support essential extracellular S1P signaling functions in the vascular and immune systems. We previously showed that ApoM- and albumin-bound S1P exhibit differences in receptor activation and biological functions. Whether the physiological functions of S1P require chaperones is not clear. We examined ApoM-deficient, albumin-deficient, and double-KO (DKO) mice for circulatory S1P and its biological functions. In albumin-deficient mice, ApoM was upregulated, thus enabling S1P functions in embryonic development and postnatal adult life. The Apom:Alb DKO mice reproduced, were viable, and exhibited largely normal vascular and immune functions, which suggested sufficient extracellular S1P signaling. However, Apom:Alb DKO mice had reduced levels (∼25%) of plasma S1P, suggesting that novel S1P chaperones exist to mediate S1P functions. In this study, we report the identification of ApoA4 as a novel S1P binding protein. Recombinant ApoA4 bound to S1P, activated multiple S1P receptors, and promoted vascular endothelial barrier function, all reflective of its function as a S1P chaperone in the absence of ApoM and albumin. We suggest that multiple S1P chaperones evolved to support complex and essential extracellular signaling functions of this lysolipid mediator in a redundant manner.

Keywords: apolipoprotein A4; apolipoprotein M; apolipoproteins; high density lipoprotein; lipid transport; lysophospholipid; sphingosine 1-phosphate receptors.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Apolipoproteins A / chemistry
  • Apolipoproteins A / metabolism*
  • Apolipoproteins M / deficiency*
  • Apolipoproteins M / genetics
  • Gene Knockout Techniques
  • Lysophospholipids / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Serum Albumin / deficiency*
  • Sphingosine / analogs & derivatives*
  • Sphingosine / metabolism
  • Sphingosine-1-Phosphate Receptors / metabolism

Substances

  • Apolipoproteins A
  • Apolipoproteins M
  • Lysophospholipids
  • Serum Albumin
  • Sphingosine-1-Phosphate Receptors
  • apolipoprotein A-IV
  • sphingosine 1-phosphate
  • Sphingosine