TY - JOUR
T1 - A novel treatment of cystic fibrosis acting on-target
T2 - Cysteamine plus epigallocatechin gallate for the autophagy-dependent rescue of class II-mutated CFTR
AU - Tosco, A.
AU - De Gregorio, F.
AU - Esposito, S.
AU - De Stefano, D.
AU - Sana, I.
AU - Ferrari, E.
AU - Sepe, A.
AU - Salvadori, L.
AU - Buonpensiero, P.
AU - Di Pasqua, A.
AU - Grassia, R.
AU - Leone, C. A.
AU - Guido, S.
AU - De Rosa, G.
AU - Lusa, S.
AU - Bona, G.
AU - Stoll, G.
AU - Maiuri, M. C.
AU - Mehta, A.
AU - Kroemer, G.
AU - Maiuri, L.
AU - Raia, V.
N1 - Funding Information:
This study was supported by The European Institute for Research in Cystic Fibrosis (IERFC) non-profit foundation, Italian Cystic Fibrosis Association (LIFC) and Regional Cystic Fibrosis Associations of Campania, Sicilia, Lazio, Puglia (to Dr. L Maiuri, Dr. Raia), E-Rare (Rescue CFTR preclinic) (to Dr. L Maiuri and Dr. Kroemer); Telethon (#GGP12128) (to Dr. L Maiuri, Dr. Raia, Dr. MC Maiuri), Agence National de la Recherche (ANR) Projetsblancs; ANR under the frame of E-Rare-2, the ERA-Net for Research on Rare Diseases; Association pour la recherche sur le cancer (ARC); Cancéropôle Ile-de-France; Institut National du Cancer (INCa); Fondation Bettencourt-Schueller; Fondation de France; Fondation pour la Recherche Médicale (FRM); the European Commission (ArtForce); the European Research Council (ERC); the LabEx Immuno-Oncology; the SIRIC Stratified Oncology Cell DNA Repair and Tumor Immune Elimination (SOCRATE); the SIRIC Cancer Research and Personalized Medicine (CARPEM); and the Paris Alliance of Cancer Research Institutes (PACRI) (all to Dr. Kroemer). The funders of the study had no role in study design, data collection, data analysis, data interpretation or writing of the report.
PY - 2016/8/1
Y1 - 2016/8/1
N2 - We previously reported that the combination of two safe proteostasis regulators, cysteamine and epigallocatechin gallate (EGCG), can be used to improve deficient expression of the cystic fibrosis transmembrane conductance regulator (CFTR) in patients homozygous for the CFTR Phe508del mutation. Here we provide the proof-of-concept that this combination treatment restored CFTR function and reduced lung inflammation (P<0.001) in Phe508del/Phe508del or Phe508del/null-Cftr (but not in Cftr-null mice), provided that such mice were autophagy-competent. Primary nasal cells from patients bearing different class II CFTR mutations, either in homozygous or compound heterozygous form, responded to the treatment in vitro. We assessed individual responses to cysteamine plus EGCG in a single-centre, open-label phase-2 trial. The combination treatment decreased sweat chloride from baseline, increased both CFTR protein and function in nasal cells, restored autophagy in such cells, decreased CXCL8 and TNF-α in the sputum, and tended to improve respiratory function. These positive effects were particularly strong in patients carrying Phe508del CFTR mutations in homozygosity or heterozygosity. However, a fraction of patients bearing other CFTR mutations failed to respond to therapy. Importantly, the same patients whose primary nasal brushed cells did not respond to cysteamine plus EGCG in vitro also exhibited deficient therapeutic responses in vivo. Altogether, these results suggest that the combination treatment of cysteamine plus EGCG acts 'on-target' because it can only rescue CFTR function when autophagy is functional (in mice) and improves CFTR function when a rescuable protein is expressed (in mice and men). These results should spur the further clinical development of the combination treatment.
AB - We previously reported that the combination of two safe proteostasis regulators, cysteamine and epigallocatechin gallate (EGCG), can be used to improve deficient expression of the cystic fibrosis transmembrane conductance regulator (CFTR) in patients homozygous for the CFTR Phe508del mutation. Here we provide the proof-of-concept that this combination treatment restored CFTR function and reduced lung inflammation (P<0.001) in Phe508del/Phe508del or Phe508del/null-Cftr (but not in Cftr-null mice), provided that such mice were autophagy-competent. Primary nasal cells from patients bearing different class II CFTR mutations, either in homozygous or compound heterozygous form, responded to the treatment in vitro. We assessed individual responses to cysteamine plus EGCG in a single-centre, open-label phase-2 trial. The combination treatment decreased sweat chloride from baseline, increased both CFTR protein and function in nasal cells, restored autophagy in such cells, decreased CXCL8 and TNF-α in the sputum, and tended to improve respiratory function. These positive effects were particularly strong in patients carrying Phe508del CFTR mutations in homozygosity or heterozygosity. However, a fraction of patients bearing other CFTR mutations failed to respond to therapy. Importantly, the same patients whose primary nasal brushed cells did not respond to cysteamine plus EGCG in vitro also exhibited deficient therapeutic responses in vivo. Altogether, these results suggest that the combination treatment of cysteamine plus EGCG acts 'on-target' because it can only rescue CFTR function when autophagy is functional (in mice) and improves CFTR function when a rescuable protein is expressed (in mice and men). These results should spur the further clinical development of the combination treatment.
UR - http://www.scopus.com/inward/record.url?scp=84962121102&partnerID=8YFLogxK
U2 - 10.1038/cdd.2016.22
DO - 10.1038/cdd.2016.22
M3 - Article
C2 - 27035618
AN - SCOPUS:84962121102
SN - 1350-9047
VL - 23
SP - 1380
EP - 1393
JO - Cell Death and Differentiation
JF - Cell Death and Differentiation
IS - 8
ER -