Complement alternative pathway acts as a positive feedback amplification of neutrophil activation

Blood. 2011 Jan 27;117(4):1340-9. doi: 10.1182/blood-2010-05-283564. Epub 2010 Nov 9.

Abstract

Complement alternative pathway plays an important, but not clearly understood, role in neutrophil-mediated diseases. We here show that neutrophils themselves activate complement when stimulated by cytokines or coagulation-derived factors. In whole blood, tumor necrosis factor/formyl-methionyl-leucyl-phenylalanine or phorbol myristate acetate resulted in C3 fragments binding on neutrophils and monocytes, but not on T cells. Neutrophils, stimulated by tumor necrosis factor, triggered the alternative pathway on their surface in normal and C2-depleted, but not in factor B-depleted serum and on incubation with purified C3, factors B and D. This occurred independently of neutrophil proteases, oxidants, or apoptosis. Neutrophil-secreted properdin was detected on the cell surface and could focus "in situ" the alternative pathway activation. Importantly, complement, in turn, led to further activation of neutrophils, with enhanced CD11b expression and oxidative burst. Complement-induced neutrophil activation involved mostly C5a and possibly C5b-9 complexes, detected on tumor necrosis factor- and serum-activated neutrophils. In conclusion, neutrophil stimulation by cytokines results in an unusual activation of autologous complement by healthy cells. This triggers a new amplification loop in physiologic innate immunity: Neutrophils activate the alternative complement pathway and release C5 fragments, which further amplify neutrophil proinflammatory responses. This mechanism, possibly required for effective host defense, may be relevant to complement involvement in neutrophil-mediated diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Blood / drug effects
  • Blood / immunology
  • Cells, Cultured
  • Complement Activation / drug effects
  • Complement Activation / physiology
  • Complement C3 / metabolism
  • Complement C5 / metabolism
  • Complement Pathway, Alternative / drug effects
  • Complement Pathway, Alternative / physiology*
  • Feedback, Physiological / drug effects
  • Feedback, Physiological / physiology
  • Humans
  • N-Formylmethionine Leucyl-Phenylalanine / analogs & derivatives
  • N-Formylmethionine Leucyl-Phenylalanine / pharmacology
  • Neutrophil Activation* / drug effects
  • Neutrophil Activation* / immunology
  • Neutrophil Activation* / physiology
  • Neutrophils / drug effects
  • Neutrophils / immunology
  • Neutrophils / metabolism
  • Neutrophils / physiology
  • Tetradecanoylphorbol Acetate / pharmacology
  • Tumor Necrosis Factor-alpha / pharmacology

Substances

  • Complement C3
  • Complement C5
  • Tumor Necrosis Factor-alpha
  • N-Formylmethionine Leucyl-Phenylalanine
  • methionyl-leucyl-phenylalanine
  • Tetradecanoylphorbol Acetate