IL-5 links adaptive and natural immunity specific for epitopes of oxidized LDL and protects from atherosclerosis

J Clin Invest. 2004 Aug;114(3):427-37. doi: 10.1172/JCI20479.

Abstract

During atherogenesis, LDL is oxidized, generating various oxidation-specific neoepitopes, such as malondialdehyde-modified (MDA-modified) LDL (MDA-LDL) or the phosphorylcholine (PC) headgroup of oxidized phospholipids (OxPLs). These epitopes are recognized by both adaptive T cell-dependent (TD) and innate T cell-independent type 2 (TI-2) immune responses. We previously showed that immunization of mice with MDA-LDL induces a TD response and atheroprotection. In addition, a PC-based immunization strategy that leads to a TI-2 expansion of innate B-1 cells and secretion of T15/EO6 clonotype natural IgM antibodies, which bind the PC of OxPLs within oxidized LDL (OxLDL), also reduces atherogenesis. T15/EO6 antibodies inhibit OxLDL uptake by macrophages. We now report that immunization with MDA-LDL, which does not contain OxPL, unexpectedly led to the expansion of T15/EO6 antibodies. MDA-LDL immunization caused a preferential expansion of MDA-LDL-specific Th2 cells that prominently secreted IL-5. In turn, IL-5 provided noncognate stimulation to innate B-1 cells, leading to increased secretion of T15/EO6 IgM. Using a bone marrow transplant model, we also demonstrated that IL-5 deficiency led to decreased titers of T15/EO6 and accelerated atherosclerosis. Thus, IL-5 links adaptive and natural immunity specific to epitopes of OxLDL and protects from atherosclerosis, in part by stimulating the expansion of atheroprotective natural IgM specific for OxLDL.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Antibody Formation
  • Arteriosclerosis / prevention & control*
  • Bone Marrow Transplantation
  • Disease Models, Animal
  • Epitopes / immunology*
  • Female
  • Immunity, Innate*
  • Immunoglobulin M / metabolism
  • Interleukin-5 / deficiency
  • Interleukin-5 / genetics
  • Interleukin-5 / metabolism*
  • Lipoproteins, LDL / drug effects
  • Lipoproteins, LDL / immunology
  • Lipoproteins, LDL / metabolism*
  • Malondialdehyde / pharmacology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Th2 Cells / immunology

Substances

  • Epitopes
  • Immunoglobulin M
  • Interleukin-5
  • Lipoproteins, LDL
  • oxidized low density lipoprotein
  • Malondialdehyde