Anti-tumor necrosis factor VNAR single domains reduce lethality and regulate underlying inflammatory response in a murine model of endotoxic shock

BMC Immunol. 2013 Apr 2:14:17. doi: 10.1186/1471-2172-14-17.

Abstract

Background: In sepsis, tumor necrosis factor (TNF) is the key factor triggering respiratory burst, tissue injury and disseminated coagulation. Anti-TNF strategies based on monoclonal antibodies or F(ab')₂ fragments have been used in sepsis with contradictory results. Immunoglobulin new antigen receptors (IgNAR) are a unique subset of antibodies consisting of five constant (CNAR) and one variable domains (VNAR). VNAR domains are the smallest, naturally occurring, antibody-based immune recognition units, having potential use as therapy. Our aim was to explore the impact of an anti-TNF VNAR on survival in an experimental model of endotoxic shock. Also, mRNA expression and serum protein of several inflammatory molecules were measured.

Results: Endotoxic shock was induced by lipopolysaccharide (LPS) in male Balb/c mice. Animals were treated with anti-TNF VNAR domains, F(ab')₂ antibody fragments, or saline solution 15 minutes before, 2 h and 24 h after lethal dose₁₀₀ (LD₁₀₀) LPS administration. TNF blockade with either VNAR domains or F(ab')₂ fragments were associated with lower mortality (60% and 75%, respectively) compared to LD₁₀₀. Challenge with LPS induced significant production of serum TNF and interleukins -10 and -6 at 3 h. After that, significant reduction of IL-6 at 24 h (vs 3 h) was shown only in the VNAR group. Nitrites level also increased in response to LPS. In liver, TNF and IL-10 mRNA expression showed a pro-inflammatory imbalance in response to LPS. Blocking TNF was associated with a shift towards an anti-inflammatory status; however, polarization was more pronounced in animals receiving F(ab')₂ fragments than in those with VNAR therapy. With regard to IL-6, gene expression was increased at 3 h in all groups. TNF blockade was associated with rapid and sustained suppression of IL-6 expression, even more evident in the VNAR group. Finally, expression of inducible-nitric oxide synthase (iNOS) increased in response to LPS at 3 h, but this was decreased at 24 h only in the anti-TNF VNAR group.

Conclusions: Anti-TNF VNAR single domains improved survival in a murine model of endotoxic shock. Protection was associated with regulation in the TNF/IL-10 balance, attenuation of IL-6 and iNOS gene expression in the liver as well as decreased serum IL-6 concentration.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biomarkers / blood
  • Disease Models, Animal
  • Humans
  • Inflammation / blood
  • Inflammation / complications*
  • Inflammation / drug therapy*
  • Inflammation / pathology
  • Interleukin-10 / metabolism
  • Interleukin-6 / metabolism
  • Lipopolysaccharides
  • Liver / metabolism
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Nitrates / metabolism
  • Nitric Oxide Synthase Type II / metabolism
  • Protein Structure, Tertiary
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Shock, Septic / blood
  • Shock, Septic / complications*
  • Shock, Septic / drug therapy*
  • Single-Domain Antibodies / therapeutic use*
  • Survival Analysis
  • Treatment Outcome
  • Tumor Necrosis Factor-alpha / immunology*

Substances

  • Biomarkers
  • Interleukin-6
  • Lipopolysaccharides
  • Nitrates
  • RNA, Messenger
  • Single-Domain Antibodies
  • Tumor Necrosis Factor-alpha
  • Interleukin-10
  • Nitric Oxide Synthase Type II