Influence of highly effective modulator therapy on the sputum proteome in cystic fibrosis

J Cyst Fibros. 2024 Mar;23(2):269-277. doi: 10.1016/j.jcf.2023.10.019. Epub 2023 Nov 10.

Abstract

Background: There have been dramatic clinical improvements in people with cystic fibrosis (PwCF) commenced on the cystic fibrosis conductance regulator (CFTR) modulator elexacaftor/tezacaftor/ivacaftor (ETI). Sputum proteomics is a powerful research technique capable of identifying important airway disease mechanisms. Using this technique, we evaluated how ETI changes the sputum proteome in PwCF.

Methods: Sputum samples from 21 CF subjects pre- and post- ETI, 6 CF controls ineligible for ETI, and 15 healthy controls were analysed by liquid chromatography mass spectrometry.

Results: Post-ETI, mean FEV1 % increased by 13.7 % (SD 7.9). Principal component and hierarchical clustering analysis revealed that the post-ETI proteome shifted to an intermediate state that was distinct from pre-ETI and healthy controls, even for those achieving normal lung function. Functional analysis showed incomplete resolution of neutrophilic inflammation. The CF control sputum proteome did not alter. At the protein-level many more proteins increased in abundance than decreased following ETI therapy (80 vs 30; adjusted p value <0.05), including many that have anti-inflammatory properties. Of those proteins that reduced in abundance many were pro-inflammatory neutrophil-derived proteins. Several important respiratory proteases were unchanged.

Conclusions: Sputum proteomics can provide insights into CF lung disease mechanisms and how they are modified by therapeutic intervention, in this case ETI. This study identifies imbalances in pro- and anti- inflammatory proteins in sputum that partially resolve with ETI even in those achieving normal spirometry values. This post-ETI intermediate state could contribute to ongoing airway damage and therefore its relevance to clinical outcomes needs to be established.

Keywords: CFTR modulation; Cystic fibrosis; Elexacaftor/tezacaftor/ivacaftor; Sputum proteomics.

MeSH terms

  • Adult
  • Aminophenols* / therapeutic use
  • Benzodioxoles* / therapeutic use
  • Chloride Channel Agonists / therapeutic use
  • Cystic Fibrosis Transmembrane Conductance Regulator
  • Cystic Fibrosis* / drug therapy
  • Cystic Fibrosis* / metabolism
  • Cystic Fibrosis* / physiopathology
  • Drug Combinations*
  • Female
  • Forced Expiratory Volume
  • Humans
  • Indoles* / therapeutic use
  • Male
  • Proteome* / analysis
  • Proteomics / methods
  • Pyrazoles / therapeutic use
  • Pyridines
  • Quinolines
  • Quinolones* / therapeutic use
  • Sputum* / metabolism
  • Young Adult

Substances

  • elexacaftor, ivacaftor, tezacaftor drug combination