FDA-approved drug screening in patient-derived organoids demonstrates potential of drug repurposing for rare cystic fibrosis genotypes.


Journal

Journal of cystic fibrosis : official journal of the European Cystic Fibrosis Society
ISSN: 1873-5010
Titre abrégé: J Cyst Fibros
Pays: Netherlands
ID NLM: 101128966

Informations de publication

Date de publication:
May 2023
Historique:
received: 13 09 2022
revised: 06 01 2023
accepted: 03 03 2023
medline: 12 6 2023
pubmed: 6 5 2023
entrez: 5 5 2023
Statut: ppublish

Résumé

Preclinical cell-based assays that recapitulate human disease play an important role in drug repurposing. We previously developed a functional forskolin induced swelling (FIS) assay using patient-derived intestinal organoids (PDIOs), allowing functional characterization of CFTR, the gene mutated in people with cystic fibrosis (pwCF). CFTR function-increasing pharmacotherapies have revolutionized treatment for approximately 85% of people with CF who carry the most prevalent F508del-CFTR mutation, but a large unmet need remains to identify new treatments for all pwCF. We used 76 PDIOs not homozygous for F508del-CFTR to test the efficacy of 1400 FDA-approved drugs on improving CFTR function, as measured in FIS assays. The most promising hits were verified in a secondary FIS screen. Based on the results of this secondary screen, we further investigated CFTR elevating function of PDE4 inhibitors and currently existing CFTR modulators. In the primary screen, 30 hits were characterized that elevated CFTR function. In the secondary validation screen, 19 hits were confirmed and categorized in three main drug families: CFTR modulators, PDE4 inhibitors and tyrosine kinase inhibitors. We show that PDE4 inhibitors are potent CFTR function inducers in PDIOs where residual CFTR function is either present, or created by additional compound exposure. Additionally, upon CFTR modulator treatment we show rescue of CF genotypes that are currently not eligible for this therapy. This study exemplifies the feasibility of high-throughput compound screening using PDIOs. We show the potential of repurposing drugs for pwCF carrying non-F508del genotypes that are currently not eligible for therapies. We screened 1400 FDA-approved drugs in CF patient-derived intestinal organoids using the previously established functional FIS assay, and show the potential of repurposing PDE4 inhibitors and CFTR modulators for rare CF genotypes.

Sections du résumé

BACKGROUND BACKGROUND
Preclinical cell-based assays that recapitulate human disease play an important role in drug repurposing. We previously developed a functional forskolin induced swelling (FIS) assay using patient-derived intestinal organoids (PDIOs), allowing functional characterization of CFTR, the gene mutated in people with cystic fibrosis (pwCF). CFTR function-increasing pharmacotherapies have revolutionized treatment for approximately 85% of people with CF who carry the most prevalent F508del-CFTR mutation, but a large unmet need remains to identify new treatments for all pwCF.
METHODS METHODS
We used 76 PDIOs not homozygous for F508del-CFTR to test the efficacy of 1400 FDA-approved drugs on improving CFTR function, as measured in FIS assays. The most promising hits were verified in a secondary FIS screen. Based on the results of this secondary screen, we further investigated CFTR elevating function of PDE4 inhibitors and currently existing CFTR modulators.
RESULTS RESULTS
In the primary screen, 30 hits were characterized that elevated CFTR function. In the secondary validation screen, 19 hits were confirmed and categorized in three main drug families: CFTR modulators, PDE4 inhibitors and tyrosine kinase inhibitors. We show that PDE4 inhibitors are potent CFTR function inducers in PDIOs where residual CFTR function is either present, or created by additional compound exposure. Additionally, upon CFTR modulator treatment we show rescue of CF genotypes that are currently not eligible for this therapy.
CONCLUSION CONCLUSIONS
This study exemplifies the feasibility of high-throughput compound screening using PDIOs. We show the potential of repurposing drugs for pwCF carrying non-F508del genotypes that are currently not eligible for therapies.
ONE-SENTENCE SUMMARY UNASSIGNED
We screened 1400 FDA-approved drugs in CF patient-derived intestinal organoids using the previously established functional FIS assay, and show the potential of repurposing PDE4 inhibitors and CFTR modulators for rare CF genotypes.

Identifiants

pubmed: 37147251
pii: S1569-1993(23)00067-X
doi: 10.1016/j.jcf.2023.03.004
pii:
doi:

Substances chimiques

Cystic Fibrosis Transmembrane Conductance Regulator 126880-72-6
Phosphodiesterase 4 Inhibitors 0
Colforsin 1F7A44V6OU

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

548-559

Informations de copyright

Copyright © 2023. Published by Elsevier B.V.

Déclaration de conflit d'intérêts

Declaration of Competing Interest J.M.B. reports personal fees from Vertex Pharmaceuticals, Proteostasis Therapeutics, Eloxx Pharmaceuticals, Teva Pharmaceutical Industries and Galapagos, outside the submitted work; In addition, J.M.B. has a patent(s) related to the FIS-assay with royalties paid. C.K.v.d.E. reports grants from GSK, grants from Nutricia, TEVA, Gilead, Vertex, ProQR, Proteostasis, Galapagos NV and Eloxx outside the submitted work; In addition, C.K.v.d.E. has a patent 10006904 with royalties paid. G.H.K. reports grants from Lung Foundation of the Netherlands, Vertex Pharmaceuticals, UBBO EMMIUS foundation, GSK, TEVA the Netherlands, ZON-MW (Vici-grant), European Union (H2020), outside the submitted work; and he has participated in advisory boards meetings to GSK and PURE-IMS outside the submitted work (Money to institution). All other authors have nothing to disclose.

Auteurs

E de Poel (E)

Department of Pediatric Respiratory Medicine, Wilhelmina Children's Hospital, University Medical Center, Utrecht University, Utrecht, EA 3584, the Netherlands; Regenerative Medicine Utrecht, University Medical Center, Utrecht University, Utrecht, CT 3584, the Netherlands.

S Spelier (S)

Department of Pediatric Respiratory Medicine, Wilhelmina Children's Hospital, University Medical Center, Utrecht University, Utrecht, EA 3584, the Netherlands; Regenerative Medicine Utrecht, University Medical Center, Utrecht University, Utrecht, CT 3584, the Netherlands.

M C Hagemeijer (MC)

Department of Pediatric Respiratory Medicine, Wilhelmina Children's Hospital, University Medical Center, Utrecht University, Utrecht, EA 3584, the Netherlands; Regenerative Medicine Utrecht, University Medical Center, Utrecht University, Utrecht, CT 3584, the Netherlands; Center for Lysosomal and Metabolic Diseases, Department of Clinical Genetics, Erasmus University Medical Center, Rotterdam, GD 3015, the Netherlands.

P van Mourik (P)

Department of Pediatric Respiratory Medicine, Wilhelmina Children's Hospital, University Medical Center, Utrecht University, Utrecht, EA 3584, the Netherlands.

S W F Suen (SWF)

Department of Pediatric Respiratory Medicine, Wilhelmina Children's Hospital, University Medical Center, Utrecht University, Utrecht, EA 3584, the Netherlands; Regenerative Medicine Utrecht, University Medical Center, Utrecht University, Utrecht, CT 3584, the Netherlands.

A M Vonk (AM)

Department of Pediatric Respiratory Medicine, Wilhelmina Children's Hospital, University Medical Center, Utrecht University, Utrecht, EA 3584, the Netherlands; Regenerative Medicine Utrecht, University Medical Center, Utrecht University, Utrecht, CT 3584, the Netherlands.

J E Brunsveld (JE)

Department of Pediatric Respiratory Medicine, Wilhelmina Children's Hospital, University Medical Center, Utrecht University, Utrecht, EA 3584, the Netherlands; Regenerative Medicine Utrecht, University Medical Center, Utrecht University, Utrecht, CT 3584, the Netherlands.

G N Ithakisiou (GN)

Department of Pediatric Respiratory Medicine, Wilhelmina Children's Hospital, University Medical Center, Utrecht University, Utrecht, EA 3584, the Netherlands; Regenerative Medicine Utrecht, University Medical Center, Utrecht University, Utrecht, CT 3584, the Netherlands.

E Kruisselbrink (E)

Department of Pediatric Respiratory Medicine, Wilhelmina Children's Hospital, University Medical Center, Utrecht University, Utrecht, EA 3584, the Netherlands; Regenerative Medicine Utrecht, University Medical Center, Utrecht University, Utrecht, CT 3584, the Netherlands.

H Oppelaar (H)

Department of Pediatric Respiratory Medicine, Wilhelmina Children's Hospital, University Medical Center, Utrecht University, Utrecht, EA 3584, the Netherlands; Regenerative Medicine Utrecht, University Medical Center, Utrecht University, Utrecht, CT 3584, the Netherlands.

G Berkers (G)

Department of Pediatric Respiratory Medicine, Wilhelmina Children's Hospital, University Medical Center, Utrecht University, Utrecht, EA 3584, the Netherlands.

K M de Winter de Groot (KM)

Department of Pediatric Respiratory Medicine, Wilhelmina Children's Hospital, University Medical Center, Utrecht University, Utrecht, EA 3584, the Netherlands.

S Heida-Michel (S)

Department of Pediatric Respiratory Medicine, Wilhelmina Children's Hospital, University Medical Center, Utrecht University, Utrecht, EA 3584, the Netherlands.

S R Jans (SR)

Department of Pediatric Respiratory Medicine, Wilhelmina Children's Hospital, University Medical Center, Utrecht University, Utrecht, EA 3584, the Netherlands.

H van Panhuis (H)

Department of Pediatric Respiratory Medicine, Wilhelmina Children's Hospital, University Medical Center, Utrecht University, Utrecht, EA 3584, the Netherlands.

M Bakker (M)

Department of Pulmonology, Erasmus MC, University Medical Center, Rotterdam, GD 3015, the Netherlands.

R van der Meer (R)

Haga Teaching Hospital, The Hague, CH 2545, the Netherlands.

J Roukema (J)

Radboud University Medical Center, Radboud Institute for Health Sciences, Nijmegen, XZ 6525, the Netherlands.

E Dompeling (E)

Maastricht University Medical Center, Maastricht, HX 6229, the Netherlands.

E J M Weersink (EJM)

Amsterdam University Medical Center, location AMC, Amsterdam, AZ 1105, the Netherlands.

G H Koppelman (GH)

University of Groningen, University Medical Center Groningen, Beatrix Children's Hospital, Department of Pediatric Pulmonology and Pediatric Allergology, Groningen, the Netherlands; University of Groningen, University Medical Center Groningen, Groningen Research Institute for Asthma and COPD (GRIAC), Groningen, the Netherlands.

A R Blaazer (AR)

Division of Medicinal Chemistry, Vrije Universiteit Amsterdam, Amsterdam, HZ 1081, the Netherlands.

J E Muijlwijk-Koezen (JE)

Division of Medicinal Chemistry, Vrije Universiteit Amsterdam, Amsterdam, HZ 1081, the Netherlands.

C K van der Ent (CK)

Department of Pediatric Respiratory Medicine, Wilhelmina Children's Hospital, University Medical Center, Utrecht University, Utrecht, EA 3584, the Netherlands.

J M Beekman (JM)

Department of Pediatric Respiratory Medicine, Wilhelmina Children's Hospital, University Medical Center, Utrecht University, Utrecht, EA 3584, the Netherlands; Regenerative Medicine Utrecht, University Medical Center, Utrecht University, Utrecht, CT 3584, the Netherlands; Centre for Living Technologies, Alliance TU/e, WUR, UU, UMC Utrecht, Princetonlaan 6, Utrecht, CB 3584, the Netherlands. Electronic address: J.Beekman@umcutrecht.nl.

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