Significance of glycosylphosphatidylinositol-anchored protein enrichment in lipid rafts for the control of autoimmunity

J Biol Chem. 2013 Aug 30;288(35):25490-25499. doi: 10.1074/jbc.M113.492611. Epub 2013 Jul 17.

Abstract

Glycosylphosphatidylinositols (GPI) are complex glycolipids that are covalently linked to the C terminus of proteins as a post-translational modification and tether proteins to the plasma membrane. One of the most striking features of GPI-anchored proteins (APs) is their enrichment in lipid rafts. The biosynthesis of GPI and its attachment to proteins occur in the endoplasmic reticulum. In the Golgi, GPI-APs are subjected to fatty acid remodeling, which replaces an unsaturated fatty acid at the sn-2 position of the phosphatidylinositol moiety with a saturated fatty acid. We previously reported that fatty acid remodeling is critical for the enrichment of GPI-APs in lipid rafts. To investigate the biological significance of GPI-AP enrichment in lipid rafts, we generated a PGAP3 knock-out mouse (PGAP3(-/-)) in which fatty acid remodeling of GPI-APs does not occur. We report here that a significant number of aged PGAP3(-/-) mice developed autoimmune-like symptoms, such as increased anti-DNA antibodies, spontaneous germinal center formation, and enlarged renal glomeruli with deposition of immune complexes and matrix expansion. A possible cause for this was the impaired engulfment of apoptotic cells by resident peritoneal macrophages in PGAP3(-/-) mice. Mice with conditional targeting of PGAP3 in either B or T cells did not develop such autoimmune-like symptoms. In addition, PGAP3(-/-) mice exhibited the tendency of Th2 polarization. These data demonstrate that PGAP3-dependent fatty acid remodeling of GPI-APs has a significant role in the control of autoimmunity, possibly by the regulation of apoptotic cell clearance and Th1/Th2 balance.

Keywords: Autoimmunity; Glycosylphosphatidylinositol Anchors; Lipid Raft; Lipid Structure; PGAP3; Phagocytosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Antinuclear / genetics
  • Antibodies, Antinuclear / immunology
  • Antibodies, Antinuclear / metabolism
  • Apoptosis / genetics
  • Apoptosis / immunology
  • Autoimmune Diseases / genetics
  • Autoimmune Diseases / immunology*
  • Autoimmune Diseases / metabolism
  • Autoimmune Diseases / pathology
  • B-Lymphocytes / immunology
  • B-Lymphocytes / metabolism
  • B-Lymphocytes / pathology
  • Carboxylic Ester Hydrolases / genetics
  • Carboxylic Ester Hydrolases / immunology
  • Carboxylic Ester Hydrolases / metabolism
  • Cells, Cultured
  • Glomerular Mesangium / immunology
  • Glomerular Mesangium / metabolism
  • Glomerular Mesangium / pathology
  • Glycosylphosphatidylinositols / genetics
  • Glycosylphosphatidylinositols / immunology*
  • Glycosylphosphatidylinositols / metabolism
  • Immune Complex Diseases / genetics
  • Immune Complex Diseases / immunology*
  • Immune Complex Diseases / metabolism
  • Membrane Microdomains / genetics
  • Membrane Microdomains / immunology*
  • Membrane Microdomains / metabolism
  • Membrane Microdomains / pathology
  • Membrane Proteins / genetics
  • Membrane Proteins / immunology*
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Inbred BALB C
  • Mice, Knockout
  • Th1 Cells / immunology
  • Th1 Cells / metabolism
  • Th1 Cells / pathology
  • Th2 Cells / immunology
  • Th2 Cells / metabolism
  • Th2 Cells / pathology

Substances

  • Antibodies, Antinuclear
  • Glycosylphosphatidylinositols
  • Membrane Proteins
  • Carboxylic Ester Hydrolases
  • PGAP3 protein, mouse