Antibody/receptor protein immunocomplex in human and mouse cortical nerve endings amplifies complement-induced glutamate release

Neurosci Lett. 2015 Jul 23:600:50-5. doi: 10.1016/j.neulet.2015.06.001. Epub 2015 Jun 3.

Abstract

Previous studies have demonstrated that complement alone releases glutamate from human and mouse cortical terminals in an antibody-independent manner. In order to expand our knowledge on complement-mediated effects, we investigated whether the presence of an antigen-antibody complex in synaptosomal plasmamembranes could also trigger complement-induced functional responses that might affect neurotransmitter release. To this aim, we focused on the chemokine 5 receptor (CCR5) expressed in human and mouse cortical glutamate terminals, whose activation by CCL5 elicits [(3)H]D-aspartate ([(3)H]D-ASP) release. Preincubating synaptosomes with an antibody recognizing the NH2 terminus of the CCR5 protein (anti-NH2-CCR5 antibody) abolished the CCL5-induced [(3)H]D-ASP release. Similarly, enriching synaptosomes with an antibody recognizing the COOH terminus of CCR5 (anti-COOH-CCR5 antibody) prevented the CCL5-induced [(3)H]D-ASP release. The antagonist-like activity of the anti-NH2-CCR5 antibody turned to facilitation when anti-NH2-CCR5-treated synaptosomes were exposed to complement. In these terminals, the releasing effect was significantly higher than that elicited by complement in untreated synaptosomes. On the contrary, the complement-induced [(3)H]D-ASP release from anti-COOH-CCR5 antibody-entrapped synaptosomes did not differ from that from untreated synaptosomes. Preincubating synaptosomes with anti-beta tubulin III antibody, used as negative control, neither prevented the CCL5-induced releasing effect nor it amplified the complement-induced [(3)H]D-ASP release. Finally, serum lacking the C1q protein, i.e. the protein essential to promote the antibody-mediated activation of complement, elicited a comparable [(3)H]D-ASP release from both untreated and anti-NH2-CCR5 antibody-treated synaptosomes. Thus, we propose that antibodies raised against the outer sequence of a receptor protein can trigger the activation of the complement through the classic, C1q-mediated antibody-dependent pathway, which results in an abnormal release of glutamate that could be deleterious to central nervous system.

Keywords: Anti-ccr5 antibody; BBB; CCR5; CCRs; Complement; C–C chemokine receptors; Glutamate; Human cortex; Mouse cortex; RANTES; blood-brain barrier; expressed and secreted; regulated upon activation normal T cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Animals
  • Antibodies / pharmacology*
  • Aspartic Acid / metabolism
  • Cerebral Cortex / drug effects*
  • Cerebral Cortex / metabolism
  • Chemokine CCL5 / metabolism
  • Chemokine CCL5 / pharmacology
  • Complement C1q / metabolism*
  • Complement Pathway, Classical
  • Female
  • Glutamic Acid / metabolism*
  • Humans
  • Male
  • Mice, Inbred C57BL
  • Middle Aged
  • Nerve Endings / drug effects*
  • Nerve Endings / metabolism
  • Receptors, CCR5 / immunology*
  • Species Specificity
  • Synaptosomes / metabolism

Substances

  • Antibodies
  • Chemokine CCL5
  • Receptors, CCR5
  • Aspartic Acid
  • Glutamic Acid
  • Complement C1q