Nicotine drives neutrophil extracellular traps formation and accelerates collagen-induced arthritis

Rheumatology (Oxford). 2017 Apr 1;56(4):644-653. doi: 10.1093/rheumatology/kew449.

Abstract

Objectives: The aim was to investigate the effects of nicotine on neutrophil extracellular traps (NETs) formation in current and non-smokers and on a murine model of RA.

Methods: We compared spontaneous and phorbol 12-myristate 13-acetate-induced NETosis between current and non-smokers by DNA release binding. Nicotine-induced NETosis from non-smokers was assessed by DNA release binding, NET-specific (myeloperoxidase (MPO)-DNA complex) ELISA and real-time fluorescence microscopy. We also used immunofluorescent staining to detect nicotinic acetylcholine receptors (nAChRs) on neutrophils and performed a functional analysis to assess the role of nAChRs in nicotine-induced NETosis. Finally, we investigated the effects of systemic nicotine exposure on arthritis severity and NETosis in the CIA mouse model.

Results: Neutrophils derived from current smokers displayed elevated levels of spontaneous and phorbol 12-myristate 13-acetate-induced NETosis. Nicotine induced dose-dependent NETosis in ex vivo neutrophils from healthy non-smokers, and co-incubation with ACPA-immune complexes or TNF-α facilitated a synergistic effect on NETosis. Real-time fluorescence microscopy revealed robust formation of NET-like structures in nicotine-exposed neutrophils. Immunofluorescent staining demonstrated the presence of the α7 subunit of the nAChR on neutrophils. Stimulation of neutrophils with an α7-specific nAChR agonist induced NETosis, whereas pretreatment with an nAChR antagonist attenuated nicotine-induced NETosis. Nicotine administration to mice with CIA exacerbated inflammatory arthritis, with higher plasma levels of NET-associated MPO-DNA complex.

Conclusion: We demonstrate that nicotine is a potent inducer of NETosis, which may play an important role in accelerating arthritis in the CIA model. This study generates awareness of and the mechanisms by which nicotine-containing products, including e-cigarettes, may have deleterious effects on patients with RA.

Keywords: animal model; collagen-induced arthritis; neutrophil extracellular traps; nicotine; rheumatoid arthritis.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Arthritis, Experimental / etiology
  • Arthritis, Rheumatoid / etiology*
  • Cartilage / physiology
  • Dose-Response Relationship, Drug
  • Electronic Nicotine Delivery Systems
  • Enzyme-Linked Immunosorbent Assay
  • Extracellular Traps / drug effects*
  • Humans
  • Infusions, Subcutaneous
  • Male
  • Mice, Inbred DBA
  • Neutrophils / drug effects
  • Nicotine / administration & dosage
  • Nicotine / pharmacology*
  • Nicotinic Agonists / administration & dosage
  • Nicotinic Agonists / pharmacology*
  • Peroxidase / metabolism
  • Smoking / adverse effects
  • Tetradecanoylphorbol Acetate / pharmacology

Substances

  • Nicotinic Agonists
  • Nicotine
  • Peroxidase
  • Tetradecanoylphorbol Acetate