Anti-inflammatory effects of elexacaftor/tezacaftor/ivacaftor in adults with cystic fibrosis heterozygous for F508del

PLoS One. 2024 May 31;19(5):e0304555. doi: 10.1371/journal.pone.0304555. eCollection 2024.

Abstract

Inflammation is a key driver in the pathogenesis of cystic fibrosis (CF). We assessed the effectiveness of elexacaftor/tezacaftor/ivacaftor (ETI) therapy on downregulating systemic and immune cell-derived inflammatory cytokines. We also monitored the impact of ETI therapy on clinical outcome. Adults with CF, heterozygous for F508del (n = 19), were assessed at baseline, one month and three months following ETI therapy, and clinical outcomes were measured, including sweat chloride, lung function, weight, neutrophil count and C-reactive protein (CRP). Cytokine quantifications were measured in serum and following stimulation of peripheral blood mononuclear cells (PBMCs) with lipopolysaccharide (LPS) and adenosine triphosphate and analysed using LEGEND plex™ Human Inflammation Panel 1 by flow cytometry (n = 19). ASC specks were measured in serum and caspase-1 activity and mRNA levels determined from stimulated PBMCs were determined. Patients remained stable over the study period. ETI therapy resulted in decreased sweat chloride concentrations (p < 0.0001), CRP (p = 0.0112) and neutrophil count (p = 0.0216) and increased percent predicted forced expiratory volume (ppFEV1) (p = 0.0399) from baseline to three months, alongside a trend increase in weight. Three months of ETI significantly decreased IL-18 (p< 0.0011, p < 0.0001), IL-1β (p<0.0013, p = 0.0476), IL-6 (p = 0.0109, p = 0.0216) and TNF (p = 0.0028, p = 0.0033) levels in CF serum and following PBMCs stimulation respectively. The corresponding mRNA levels were also found to be reduced in stimulated PBMCs, as well as reduced ASC specks and caspase-1 levels, indicative of NLRP3-mediated production of pro-inflammatory cytokines, IL-1β and IL-18. While ETI therapy is highly effective at reducing sweat chloride and improving lung function, it also displays potent anti-inflammatory properties, which are likely to contribute to improved long-term clinical outcomes.

MeSH terms

  • Adult
  • Aminophenols* / therapeutic use
  • Anti-Inflammatory Agents* / pharmacology
  • Anti-Inflammatory Agents* / therapeutic use
  • Benzodioxoles* / pharmacology
  • Benzodioxoles* / therapeutic use
  • C-Reactive Protein / metabolism
  • Cystic Fibrosis Transmembrane Conductance Regulator* / genetics
  • Cystic Fibrosis* / drug therapy
  • Cystic Fibrosis* / genetics
  • Cytokines* / blood
  • Cytokines* / metabolism
  • Female
  • Humans
  • Indoles* / pharmacology
  • Indoles* / therapeutic use
  • Leukocytes, Mononuclear / drug effects
  • Leukocytes, Mononuclear / metabolism
  • Male
  • Pyrazoles / pharmacology
  • Pyrazoles / therapeutic use
  • Pyridines / pharmacology
  • Pyridines / therapeutic use
  • Pyrroles / pharmacology
  • Pyrroles / therapeutic use
  • Pyrrolidines
  • Quinolones* / therapeutic use
  • Sweat / chemistry
  • Sweat / metabolism
  • Young Adult

Substances

  • Benzodioxoles
  • Aminophenols
  • Indoles
  • Cystic Fibrosis Transmembrane Conductance Regulator
  • Quinolones
  • ivacaftor
  • tezacaftor
  • Anti-Inflammatory Agents
  • Cytokines
  • elexacaftor
  • Pyrazoles
  • Pyridines
  • C-Reactive Protein
  • Pyrroles
  • Pyrrolidines

Grants and funding

This work was supported by Leeds Hospitals Charity, Cystic Fibrosis Trust Strategic Research Centre grant (SRC009) The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.