Intravenous gammaglobulin suppresses inflammation through a novel T(H)2 pathway

Nature. 2011 Jun 19;475(7354):110-3. doi: 10.1038/nature10134.

Abstract

High-dose intravenous immunoglobulin is a widely used therapeutic preparation of highly purified immunoglobulin G (IgG) antibodies. It is administered at high doses (1-2 grams per kilogram) for the suppression of autoantibody-triggered inflammation in a variety of clinical settings. This anti-inflammatory activity of intravenous immunoglobulin is triggered by a minor population of IgG crystallizable fragments (Fcs), with glycans terminating in α2,6 sialic acids (sFc) that target myeloid regulatory cells expressing the lectin dendritic-cell-specific ICAM-3 grabbing non-integrin (DC-SIGN; also known as CD209). Here, to characterize this response in detail, we generated humanized DC-SIGN mice (hDC-SIGN), and demonstrate that the anti-inflammatory activity of intravenous immunoglobulin can be recapitulated by the transfer of bone-marrow-derived sFc-treated hDC-SIGN(+) macrophages or dendritic cells into naive recipients. Furthermore, sFc administration results in the production of IL-33, which, in turn, induces expansion of IL-4-producing basophils that promote increased expression of the inhibitory Fc receptor FcγRIIB on effector macrophages. Systemic administration of the T(H)2 cytokines IL-33 or IL-4 upregulates FcγRIIB on macrophages, and suppresses serum-induced arthritis. Consistent with these results, transfer of IL-33-treated basophils suppressed induced arthritic inflammation. This novel DC-SIGN-T(H)2 pathway initiated by an endogenous ligand, sFc, provides an intrinsic mechanism for maintaining immune homeostasis that could be manipulated to provide therapeutic benefit in autoimmune diseases.

Publication types

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

MeSH terms

  • Animals
  • Arthritis / drug therapy
  • Arthritis / immunology
  • Arthritis / pathology
  • Autoimmune Diseases / drug therapy
  • Autoimmune Diseases / immunology
  • Basophils / drug effects
  • Basophils / immunology
  • Basophils / metabolism
  • Bone Marrow
  • Cell Adhesion Molecules / genetics
  • Cell Adhesion Molecules / immunology
  • Cell Adhesion Molecules / metabolism
  • Crystallization
  • Dendritic Cells / cytology
  • Dendritic Cells / immunology
  • Humans
  • Immunoglobulin G / chemistry
  • Immunoglobulin G / immunology
  • Immunoglobulin G / metabolism
  • Immunoglobulin G / pharmacology
  • Immunoglobulins, Intravenous / chemistry
  • Immunoglobulins, Intravenous / immunology*
  • Immunoglobulins, Intravenous / metabolism
  • Immunoglobulins, Intravenous / pharmacology
  • Inflammation / drug therapy
  • Inflammation / immunology*
  • Interleukin-33
  • Interleukin-4 / immunology
  • Interleukin-4 / metabolism
  • Interleukins / immunology
  • Interleukins / metabolism
  • Interleukins / pharmacology
  • Lectins, C-Type / genetics
  • Lectins, C-Type / immunology
  • Lectins, C-Type / metabolism
  • Ligands
  • Macrophages / cytology
  • Macrophages / immunology
  • Mice
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / immunology
  • Receptors, Cell Surface / metabolism
  • Receptors, IgG / immunology
  • Receptors, IgG / metabolism
  • Th2 Cells / drug effects
  • Th2 Cells / immunology*

Substances

  • Cell Adhesion Molecules
  • DC-specific ICAM-3 grabbing nonintegrin
  • Fc gamma receptor IIB
  • Il33 protein, mouse
  • Immunoglobulin G
  • Immunoglobulins, Intravenous
  • Interleukin-33
  • Interleukins
  • Lectins, C-Type
  • Ligands
  • Receptors, Cell Surface
  • Receptors, IgG
  • Interleukin-4