Reprogramming macrophages to an anti-inflammatory phenotype by helminth antigens reduces murine atherosclerosis

FASEB J. 2014 Jan;28(1):288-99. doi: 10.1096/fj.13-235911. Epub 2013 Sep 16.

Abstract

Atherosclerosis is a lipid-driven inflammatory disease of the vessel wall, characterized by the chronic activation of macrophages. We investigated whether the helminth-derived antigens [soluble egg antigens (SEAs)] could modulate macrophage inflammatory responses and protect against atherosclerosis in mice. In bone marrow-derived macrophages, SEAs induce anti-inflammatory macrophages, typified by high levels of IL-10 and reduced secretion of proinflammatory mediators. In hyperlipidemic LDLR(-/-) mice, SEA treatment reduced plaque size by 44%, and plaques were less advanced compared with PBS-injected littermate controls. The atheroprotective effect of SEAs was found to be mainly independent of cholesterol lowering and T-lymphocyte responses but instead could be attributed to diminished myeloid cell activation. SEAs reduced circulating neutrophils and inflammatory Ly6C(high) monocytes, and macrophages showed high IL-10 production. In line with the observed systemic effects, atherosclerotic lesions of SEA-treated mice showed reduced intraplaque inflammation as inflammatory markers [TNF-α, monocyte chemotactic protein 1 (MCP-1), intercellular adhesion molecule-1 (ICAM-1), vascular cell adhesion molecule-1 (VCAM-1), and CD68], neutrophil content, and newly recruited macrophages were decreased. We show that SEA treatment protects against atherosclerosis development by dampening inflammatory responses. In the future, helminth-derived components may provide novel opportunities to treat chronic inflammatory diseases, as they diminish systemic inflammation and reduce the activation of immune cells.

Keywords: immune modulation; inflammation; monocytes; mouse; schistosome.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, Helminth / metabolism*
  • Atherosclerosis / metabolism*
  • Atherosclerosis / therapy*
  • Chemokine CCL2 / metabolism
  • Macrophages / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Mutant Strains
  • Receptors, LDL / genetics
  • Receptors, LDL / metabolism
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Antigens, Helminth
  • Chemokine CCL2
  • Receptors, LDL
  • Tumor Necrosis Factor-alpha