C5L2, the Second C5a Anaphylatoxin Receptor, Suppresses LPS-Induced Acute Lung Injury

Am J Respir Cell Mol Biol. 2016 Nov;55(5):657-666. doi: 10.1165/rcmb.2016-0067OC.

Abstract

LPS-induced lung injury in the mouse is one of the most robust experimental models used for studies of acute lung injury (ALI) and acute respiratory distress syndrome in humans. Prior clinical and experimental studies support an important role for complement activation, particularly production of C5a, in the pathophysiology of human ALI/acute respiratory distress syndrome. In the mouse model, however, the precise role of C5a and its receptors is unclear. C5L2, an enigmatic second receptor for C5a, has been characterized, and results have generated substantial debate regarding its in vivo function. Our previous work with human neutrophils revealed a unique role for C5L2 in negatively modulating C5a-C5a receptor (C5aR)-mediated cellular activation, in which antibody-mediated blockade of C5L2 resulted in augmented C5a-C5aR responses. Here, we demonstrate that C5L2-/- mice (BALB/c background) administered intranasal LPS exhibit significantly more airway edema and hemorrhage than do wild-type animals. Bronchoalveolar lavage fluid and lung homogenates have significantly more neutrophils and myeloperoxidase activity, as well as proinflammatory cytokines and chemokines. When a blocking antibody against the C5aR was administered before LPS administration, the increased neutrophilic infiltration and cytokine levels were reversed. Thus, our data show not only that C5a contributes significantly to LPS-induced ALI in the mouse, but also that C5L2 plays an important antiinflammatory role in this model through actions resulting at least in part from negative modulation of C5a receptor activation.

Keywords: C5L2; C5a anaphylatoxin; LPS; acute lung injury.

MeSH terms

  • Acute Lung Injury / genetics
  • Acute Lung Injury / metabolism*
  • Acute Lung Injury / pathology*
  • Acute Lung Injury / physiopathology
  • Administration, Intranasal
  • Animals
  • Bronchoalveolar Lavage Fluid
  • Chemokines / genetics
  • Chemokines / metabolism
  • Edema / complications
  • Edema / pathology
  • Edema / physiopathology
  • Gene Expression Regulation
  • Hemorrhage / complications
  • Hemorrhage / pathology
  • Hemorrhage / physiopathology
  • Inflammation Mediators / metabolism
  • Lipopolysaccharides / administration & dosage
  • Lung / pathology
  • Mice, Inbred BALB C
  • Neutrophils / metabolism
  • Peroxidase / metabolism
  • Receptor, Anaphylatoxin C5a
  • Receptors, Chemokine / antagonists & inhibitors
  • Receptors, Chemokine / deficiency
  • Receptors, Chemokine / metabolism*
  • Respiratory Mechanics
  • Toll-Like Receptors / genetics
  • Toll-Like Receptors / metabolism

Substances

  • C5ar2 protein, mouse
  • Chemokines
  • Inflammation Mediators
  • Lipopolysaccharides
  • Receptor, Anaphylatoxin C5a
  • Receptors, Chemokine
  • Toll-Like Receptors
  • Peroxidase