Heparin enhances uptake of platelet factor 4/heparin complexes by monocytes and macrophages

J Thromb Haemost. 2015 Aug;13(8):1416-27. doi: 10.1111/jth.13003. Epub 2015 Jul 14.

Abstract

Background: Heparin-induced thrombocytopenia (HIT) is an iatrogenic complication of heparin therapy caused by antibodies to a self-antigen, platelet factor (4) and heparin. The reasons why antibodies form to PF4/heparin, but not to PF4 bound to other cellular glycosaminoglycans are poorly understood.

Objective: To investigate differences in cellular responses to cell-bound PF4 and PF4/heparin complexes, we studied the internalization of each by peripheral blood-derived monocytes, dendritic cells and neutrophils.

Methods and results: Using unlabeled and fluorescently-labeled antigen and/or labeled monoclonal antibody to PF4/heparin complexes (KKO), we show that PF4/heparin complexes are taken up by monocytes in a heparin-dependent manner and are internalized by human monocytes and dendritic cells, but not by neutrophils. Complexes of PF4/low-molecular-weight heparin and complexes composed of heparin and murine PF4, protamine or lysozyme are internalized similarly, suggesting a common endocytic pathway. Uptake of complexes is mediated by macropinocytosis, as shown by inhibition using cytochalasin D and amiloride. Internalized complexes are transported intact to late endosomes, as indicated by co-staining of vesicles with KKO and lysosomal associated membrane protein-2 (LAMP-2). Lastly, we show that cellular uptake is accompanied by expression of MHCII and CD83 co-stimulatory molecules.

Conclusions: Taken together, these studies establish a distinct role for heparin in enhancing antigen uptake and activation of the initial steps in the cellular immune response to PF4-containing complexes.

Keywords: heparin; monocytes; phagocytosis; pinocytosis; platelet factor 4.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Anticoagulants / immunology
  • Anticoagulants / metabolism
  • Anticoagulants / toxicity*
  • Antigens, CD / metabolism
  • CD83 Antigen
  • Cells, Cultured
  • Dendritic Cells / drug effects
  • Dendritic Cells / metabolism
  • Endosomes / drug effects
  • Endosomes / metabolism
  • Heparin / immunology
  • Heparin / metabolism
  • Heparin / toxicity*
  • Histocompatibility Antigens Class II / metabolism
  • Humans
  • Immunoglobulins / metabolism
  • Lysosomal-Associated Membrane Protein 2 / metabolism
  • Lysosomes / drug effects
  • Lysosomes / metabolism
  • Macrophages / drug effects*
  • Macrophages / immunology
  • Macrophages / metabolism
  • Membrane Glycoproteins / metabolism
  • Monocytes / drug effects*
  • Monocytes / immunology
  • Monocytes / metabolism
  • Phagocytosis / drug effects*
  • Pinocytosis / drug effects*
  • Platelet Factor 4 / immunology
  • Platelet Factor 4 / metabolism*
  • Protein Binding
  • Time Factors

Substances

  • Anticoagulants
  • Antigens, CD
  • Histocompatibility Antigens Class II
  • Immunoglobulins
  • LAMP2 protein, human
  • Lysosomal-Associated Membrane Protein 2
  • Membrane Glycoproteins
  • Platelet Factor 4
  • Heparin