Human genetic deficiencies reveal the roles of complement in the inflammatory network: lessons from nature

Proc Natl Acad Sci U S A. 2009 Sep 15;106(37):15861-6. doi: 10.1073/pnas.0903613106. Epub 2009 Aug 26.

Abstract

Complement component C5 is crucial for experimental animal inflammatory tissue damage; however, its involvement in human inflammation is incompletely understood. The responses to gram-negative bacteria were here studied taking advantage of human genetic complement-deficiencies--nature's own knockouts--including a previously undescribed C5 defect. Such deficiencies provide a unique tool for investigating the biological role of proteins. The experimental conditions allowed cross-talk between the different inflammatory pathways using a whole blood model based on the anticoagulant lepirudin, which does not interfere with the complement system. Expression of tissue factor, cell adhesion molecules, and oxidative burst depended highly on C5, mediated through the activation product C5a, whereas granulocyte enzyme release relied mainly on C3 and was C5a-independent. Release of cytokines and chemokines was mediated to varying degrees by complement and CD14; for example, interleukin (IL)-1beta and IL-8 were more dependent on complement than IFN-gamma and IL-6, which were highly dependent on CD14. IL-1 receptor antagonist (IL-1ra) and IFN-gamma inducible protein 10 (IP-10) were fully dependent on CD14 and inversely regulated by complement, that is, complement deficiency and complement inhibition enhanced their release. Granulocyte responses were mainly complement-dependent, whereas monocyte responses were more dependent on CD14. Notably, all responses were abolished by combined neutralization of complement and CD14. The present study provides important insight into the comprehensive role of complement in human inflammatory responses to gram-negative bacteria.

Publication types

  • Case Reports
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Case-Control Studies
  • Cell Adhesion / immunology
  • Complement Activation
  • Complement C2 / deficiency
  • Complement C2 / genetics
  • Complement C5 / deficiency
  • Complement C5 / genetics
  • Complement System Proteins / deficiency*
  • Complement System Proteins / genetics*
  • Escherichia coli / immunology
  • Female
  • Gram-Negative Bacteria / immunology
  • Gram-Negative Bacteria / pathogenicity
  • Humans
  • Immunity, Innate / genetics
  • In Vitro Techniques
  • Inflammation / etiology
  • Inflammation / genetics*
  • Inflammation / immunology*
  • Lipopolysaccharide Receptors / metabolism
  • Male
  • Models, Immunological
  • Monocytes / immunology
  • Monocytes / microbiology
  • Neisseria meningitidis / immunology
  • Phagocytosis
  • Respiratory Burst / immunology
  • Thromboplastin / biosynthesis

Substances

  • Complement C2
  • Complement C5
  • Lipopolysaccharide Receptors
  • Complement System Proteins
  • Thromboplastin