TGF-β is a potent inducer of Nerve Growth Factor in articular cartilage via the ALK5-Smad2/3 pathway. Potential role in OA related pain?

Osteoarthritis Cartilage. 2015 Mar;23(3):478-86. doi: 10.1016/j.joca.2014.12.005. Epub 2014 Dec 18.

Abstract

Objective: Pain is the main problem for patients with osteoarthritis (OA). Pain is linked to inflammation, but in OA a subset of patients suffers from pain without inflammation, indicating an alternative source of pain. Nerve Growth Factor (NGF) inhibition is very efficient in blocking pain during OA, but the source of NGF is unclear. We hypothesize that damaged cartilage in OA releases Transforming Growth Factor-β (TGF-β), which in turn stimulates chondrocytes to produce NGF.

Design: Murine and human chondrocyte cell lines, primary bovine and human chondrocytes, and cartilage explants from bovine metacarpal joints and human OA joints were stimulated with TGF-β1 and/or Interleukin-1 (IL-1)β. We analyzed NGF expression on mRNA level with QPCR and stained human OA cartilage for NGF immunohistochemically. Cultures were additionally pre-incubated with inhibitors for TAK1, Smad2/3 or Smad1/5/8 signaling to identify the TGF-β pathway inducing NGF.

Results: NGF expression was consistently induced in higher levels by TGF-β than IL-1 in all of our experiments: murine, bovine and human origin, in cell lines, primary chondrocytes and explants cultures. TAK1 inhibition consistently reduced TGF-β-induced NGF whereas it fully blocked IL-1β-induced NGF expression. In contrast, ALK5-Smad2/3 inhibition fully blocked TGF-β-induced NGF expression. Despite the large variation in basal NGF in human OA samples (mRNA and histology), TGF-β exposure led to a consistent high level of NGF induction.

Conclusion: We show for the first time that TGF-β induces NGF expression in chondrocytes, in a ALK5-Smad2/3 dependent manner. This reveals a potential alternative non-inflammatory source of pain in OA.

Keywords: Cartilage; NGF; Pain; Smad; TGF-β.

MeSH terms

  • Animals
  • Cartilage, Articular / drug effects*
  • Cartilage, Articular / metabolism
  • Cattle
  • Cell Line
  • Chondrocytes / drug effects*
  • Chondrocytes / metabolism
  • Humans
  • Interleukin-1beta / pharmacology*
  • Mice
  • Nerve Growth Factor / drug effects*
  • Nerve Growth Factor / genetics
  • Nerve Growth Factor / metabolism
  • Osteoarthritis / complications
  • Osteoarthritis / genetics
  • Osteoarthritis / metabolism*
  • Pain / etiology
  • Pain / genetics
  • Pain / metabolism*
  • Protein Serine-Threonine Kinases / drug effects
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism
  • RNA, Messenger / metabolism*
  • Real-Time Polymerase Chain Reaction
  • Receptor, Transforming Growth Factor-beta Type I
  • Receptors, Transforming Growth Factor beta / drug effects
  • Receptors, Transforming Growth Factor beta / genetics
  • Receptors, Transforming Growth Factor beta / metabolism
  • Signal Transduction
  • Smad2 Protein / drug effects
  • Smad2 Protein / genetics
  • Smad2 Protein / metabolism
  • Smad3 Protein / drug effects
  • Smad3 Protein / genetics
  • Smad3 Protein / metabolism
  • Transforming Growth Factor beta1 / pharmacology*

Substances

  • Interleukin-1beta
  • RNA, Messenger
  • Receptors, Transforming Growth Factor beta
  • Smad2 Protein
  • Smad3 Protein
  • Transforming Growth Factor beta1
  • Nerve Growth Factor
  • Protein Serine-Threonine Kinases
  • Receptor, Transforming Growth Factor-beta Type I
  • TGFBR1 protein, human
  • Tgfbr1 protein, mouse