Cystic fibrosis: a model for precision medicine

References

• Dean M, Rzhetsky A, Allikmets R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res. 2001;11(7):1156–1166.
   PubMed Web of Science ®Google Scholar
• Caputo A, Caci E, Ferrera L, et al. TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity. Science. 2008;322(5901):590–594.
   PubMed Web of Science ®Google Scholar
• Wang XF, Zhou CX, Shi QX, et al. Involvement of CFTR in uterine bicarbonate secretion and the fertilizing capacity of sperm. Nat Cell Biol. 2003;5(10):902–906.
   PubMed Web of Science ®Google Scholar
• Kogan I, Ramjeesingh M, Li C, et al. CFTR directly mediates nucleotide-regulated glutathione flux. Embo J. 2003;22(9):1981–1989.
   PubMed Web of Science ®Google Scholar
• Riordan JR, Rommens JM, Kerem B, et al. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science. 1989;245(4922):1066–1073.
   PubMed Web of Science ®Google Scholar
• Sosnay PR, Siklosi KR, Van Goor F, et al. Defining the disease liability of variants in the cystic fibrosis transmembrane conductance regulator gene. Nat Genet. 2013;45(10):1160–1167.
   PubMed Web of Science ®Google Scholar
• Elborn JS. Cystic fibrosis. Lancet. 2016;388(10059):2519–2531.
   PubMed Web of Science ®Google Scholar
• Keiser NW, Engelhardt JF. New animal models of cystic fibrosis: what are they teaching us? Curr Opin Pulm Med. 2011;17(6):478–483.
   PubMed Web of Science ®Google Scholar
• Castellani C, Assael BM Cystic fibrosis: a clinical view. Cell Mol Life Sci. 2017;74(1):129–140.
   PubMed Web of Science ®Google Scholar
• Plant BJ, Goss CH, Plant WD, et al. Management of comorbidities in older patients with cystic fibrosis. Lancet Respir Med. 2013;1(2):164–174.
   PubMed Web of Science ®Google Scholar
• Castellani C, Cuppens H, Macek M Jr., et al. Consensus on the use and interpretation of cystic fibrosis mutation analysis in clinical practice. J Cyst Fibros. 2008;7(3):179–196.
   PubMed Web of Science ®Google Scholar
• Kerem B, Chiba-Falek O, Kerem E Cystic fibrosis in Jews: frequency and mutation distribution. Genet Test. 1997;1(1):35–39.
   PubMedGoogle Scholar
• Castellani C, Southern KW, Brownlee K, et al. European best practice guidelines for cystic fibrosis neonatal screening. J Cyst Fibros. 2009;8(3):153–173.
   PubMed Web of Science ®Google Scholar
• Farrell PM, Rosenstein BJ, White TB, et al. Guidelines for diagnosis of cystic fibrosis in newborns through older adults: cystic fibrosis foundation consensus report. J Pediatr. 2008;153(2):S4–S14.
   PubMed Web of Science ®Google Scholar
• De Boeck K, Wilschanski M, Castellani C, et al. Cystic fibrosis: terminology and diagnostic algorithms. Thorax. 2006;61(7):627–635.
   PubMed Web of Science ®Google Scholar
• De Boeck K, Vermeulen F, Dupont L. The diagnosis of cystic fibrosis. Presse Med. 2017; 46 (6 Pt 2): e97–e108.
   PubMed Web of Science ®Google Scholar
• Drumm ML, Konstan MW, Schluchter MD, et al. Genetic modifiers of lung disease in cystic fibrosis. N Engl J Med. 2005;353(14):1443–1453.
   PubMed Web of Science ®Google Scholar
• Hiemstra PS, McCray PB Jr., Bals R. The innate immune function of airway epithelial cells in inflammatory lung disease. Eur Respir J. 2015;45(4):1150–1162.
   PubMed Web of Science ®Google Scholar
• Matsui H, Grubb BR, Tarran R, et al. Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell. 1998;95(7):1005–1015.
   PubMed Web of Science ®Google Scholar
• Moraes TJ, Plumb J, Martin R, et al. Abnormalities in the pulmonary innate immune system in cystic fibrosis. Am J Respir Cell Mol Biol. 2006;34(3):364–374.
   PubMed Web of Science ®Google Scholar
• Davis SD, Fordham LA, Brody AS, et al. Computed tomography reflects lower airway inflammation and tracks changes in early cystic fibrosis. Am J Respir Crit Care Med. 2007;175(9):943–950.
   PubMed Web of Science ®Google Scholar
• Martin C, Hamard C, Kanaan R, et al. Causes of death in French cystic fibrosis patients: the need for improvement in transplantation referral strategies! J Cyst Fibros. 2016;15(2):204–212.
   PubMed Web of Science ®Google Scholar
• Sly PD, Gangell CL, Chen L, et al. Risk factors for bronchiectasis in children with cystic fibrosis. N Engl J Med. 2013;368(21):1963–1970.
   PubMed Web of Science ®Google Scholar
• Mott LS, Park J, Murray CP, et al. Progression of early structural lung disease in young children with cystic fibrosis assessed using CT. Thorax. 2012;67(6):509–516.
   PubMed Web of Science ®Google Scholar
• Sly PD, Brennan S, Gangell C, et al. Lung disease at diagnosis in infants with cystic fibrosis detected by newborn screening. Am J Respir Crit Care Med. 2009;180(2):146–152.
   PubMed Web of Science ®Google Scholar
• Stick SM, Brennan S, Murray C, et al. Bronchiectasis in infants and preschool children diagnosed with cystic fibrosis after newborn screening. J Pediatr. 2009;155(5):623–8 e1.
   PubMed Web of Science ®Google Scholar
• Dorsey J, Gonska T. Bacterial overgrowth, dysbiosis, inflammation, and dysmotility in the cystic fibrosis intestine. J Cyst Fibros. 2017;16(Suppl 2):S14–S23.
   PubMedGoogle Scholar
• Flass T, Narkewicz MR. Cirrhosis and other liver disease in cystic fibrosis. J Cyst Fibros. 2013;12(2):116–124.
   PubMed Web of Science ®Google Scholar
• Rowland M, Bourke B. Liver disease in cystic fibrosis. Curr Opin Pulm Med. 2011;17(6):461–466.
   PubMed Web of Science ®Google Scholar
• Rowland M, Gallagher CG, O’Laoide R, et al. Outcome in cystic fibrosis liver disease. Am J Gastroenterol. 2011;106(1):104–109.
   PubMed Web of Science ®Google Scholar
• Kelly A, Moran A. Update on cystic fibrosis-related diabetes. J Cyst Fibros. 2013;12(4):318–331.
   PubMed Web of Science ®Google Scholar
• Quon BS, Mayer-Hamblett N, Aitken ML, et al. Risk factors for chronic kidney disease in adults with cystic fibrosis. Am J Respir Crit Care Med. 2011;184(10):1147–1152.
   PubMed Web of Science ®Google Scholar
• Mahadeva R, Webb K, Westerbeek RC, et al. Clinical outcome in relation to care in centres specialising in cystic fibrosis: cross sectional study. BMJ. 1998;316(7147):1771–1775.
   PubMed Web of Science ®Google Scholar
• Elkins MR, Robinson M, Rose BR, et al. A controlled trial of long-term inhaled hypertonic saline in patients with cystic fibrosis. N Engl J Med. 2006;354(3):229–240.
   PubMed Web of Science ®Google Scholar
• Quan JM, Tiddens HA, Sy JP, et al. A two-year randomized, placebo-controlled trial of dornase alfa in young patients with cystic fibrosis with mild lung function abnormalities. J Pediatr. 2001;139(6):813–820.
   PubMed Web of Science ®Google Scholar
• Db S, Rc B, Rosenfeld M, et al. Failure to recover to baseline pulmonary function after cystic fibrosis pulmonary exacerbation. Am J Respir Crit Care Med. 2010;182(5):627–632.
   PubMed Web of Science ®Google Scholar
• MacKenzie T, Gifford AH, Sabadosa KA, et al. Longevity of patients with cystic fibrosis in 2000 to 2010 and beyond: survival analysis of the cystic fibrosis foundation patient registry. Ann Intern Med. 2014;161(4):233–241.
   PubMed Web of Science ®Google Scholar
• Doring G, Flume P, Heijerman H, et al. Treatment of lung infection in patients with cystic fibrosis: current and future strategies. J Cyst Fibros. 2012;11(6):461–479.
   PubMed Web of Science ®Google Scholar
• Quittner AL, Abbott J, Georgiopoulos AM, et al. International committee on mental health in cystic fibrosis: cystic fibrosis foundation and European cystic fibrosis society consensus statements for screening and treating depression and anxiety. Thorax. 2016;71(1):26–34.
   PubMed Web of Science ®Google Scholar
• Quittner AL, Goldbeck L, Abbott J, et al. Prevalence of depression and anxiety in patients with cystic fibrosis and parent caregivers: results of the international depression epidemiological study across nine countries. Thorax. 2014;69(12):1090–1097.
   PubMed Web of Science ®Google Scholar
• Cystic Fibrosis Foundation Drug Development Pipeline 2017 [cited 15 Dec 2017]. Available from: https://www.cff.org/Trials/Pipeline.
   Google Scholar
• Pedemonte N, Lukacs GL, Du K, et al. Small-molecule correctors of defective DeltaF508-CFTR cellular processing identified by high-throughput screening. J Clin Invest. 2005;115(9):2564–2571.
   PubMed Web of Science ®Google Scholar
• Dekkers JF, Van Der Ent CK, Beekman JM. Novel opportunities for CFTR-targeting drug development using organoids. Rare Dis. 2013;1:e27112.
   PubMedGoogle Scholar
• Dekkers JF, Wiegerinck CL, De Jonge HR, et al. A functional CFTR assay using primary cystic fibrosis intestinal organoids. Nat Med. 2013;19(7):939–945.
   PubMed Web of Science ®Google Scholar
• Okiyoneda T, Veit G, Dekkers JF, et al. Mechanism-based corrector combination restores DeltaF508-CFTR folding and function. Nat Chem Biol. 2013;9(7):444–454.
   PubMed Web of Science ®Google Scholar
• Schwank G, Koo BK, Sasselli V, et al. Functional repair of CFTR by CRISPR/Cas9 in intestinal stem cell organoids of cystic fibrosis patients. Cell Stem Cell. 2013;13(6):653–658.
   PubMed Web of Science ®Google Scholar
• Beekman JM. Individualized medicine using intestinal responses to CFTR potentiators and correctors. Pediatr Pulmonol. 2016;51(S44):S23–S34.
   PubMedGoogle Scholar
• Dekkers JF, Gogorza Gondra RA, Kruisselbrink E, et al. Optimal correction of distinct CFTR folding mutants in rectal cystic fibrosis organoids. Eur Respir J. 2016;48(2):451–458.
   PubMed Web of Science ®Google Scholar
• Dekkers R, Vijftigschild LA, Vonk AM, et al. A bioassay using intestinal organoids to measure CFTR modulators in human plasma. J Cyst Fibros. 2015;14(2):178–181.
   PubMed Web of Science ®Google Scholar
• Noordhoek J, Gulmans V, Van Der Ent K, et al. Intestinal organoids and personalized medicine in cystic fibrosis: a successful patient-oriented research collaboration. Curr Opin Pulm Med. 2016;22(6):610–616.
   PubMed Web of Science ®Google Scholar
• Zomer-Van Ommen DD, Vijftigschild LA, Kruisselbrink E, et al. Limited premature termination codon suppression by read-through agents in cystic fibrosis intestinal organoids. J Cyst Fibros. 2016;15(2):158–162.
   PubMed Web of Science ®Google Scholar
• Wiszniewski L, Jornot L, Dudez T, et al. Long-term cultures of polarized airway epithelial cells from patients with cystic fibrosis. Am J Respir Cell Mol Biol. 2006;34(1):39–48.
   PubMed Web of Science ®Google Scholar
• De Courcey F, Av Z, Atherton-Watson H, et al. Development of primary human nasal epithelial cell cultures for the study of cystic fibrosis pathophysiology. Am J Physiol Cell Physiol. 2012;303(11):C1173–9.
   PubMed Web of Science ®Google Scholar
• Mosler K, Coraux C, Fragaki K, et al. Feasibility of nasal epithelial brushing for the study of airway epithelial functions in CF infants. J Cyst Fibros. 2008;7(1):44–53.
   PubMed Web of Science ®Google Scholar
• Guimbellot JS, Leach JM, Chaudhry IG, et al. Nasospheroids permit measurements of CFTR-dependent fluid transport. JCI Insight. 2017;2(22). pii: 95734. doi: 10.1172/jci.insight.95734 [Epub ahead of print].
   PubMed Web of Science ®Google Scholar
• Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126(4):663–676.
   PubMed Web of Science ®Google Scholar
• Ohnuki M, Takahashi K, Yamanaka S. Generation and characterization of human induced pluripotent stem cells. Curr Protoc Stem Cell Biol. 2009; Chapter 4:Unit 4A 2.
   PubMedGoogle Scholar
• Aasen T, Raya A, Barrero MJ, et al. Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes. Nat Biotechnol. 2008;26(11):1276–1284.
   PubMed Web of Science ®Google Scholar
• Haase A, Olmer R, Schwanke K, et al. Generation of induced pluripotent stem cells from human cord blood. Cell Stem Cell. 2009;5(4):434–441.
   PubMed Web of Science ®Google Scholar
• Lachmann N, Happle C, Ackermann M, et al. Gene correction of human induced pluripotent stem cells repairs the cellular phenotype in pulmonary alveolar proteinosis. Am J Respir Crit Care Med. 2014;189(2):167–182.
   PubMed Web of Science ®Google Scholar
• Amato F, Seia M, Giordano S, et al. Gene mutation in microRNA target sites of CFTR gene: a novel pathogenetic mechanism in cystic fibrosis? PLoS One. 2013;8(3):e60448.
   PubMed Web of Science ®Google Scholar
• Ramachandran S, Karp PH, Osterhaus SR, et al. Post-transcriptional regulation of cystic fibrosis transmembrane conductance regulator expression and function by microRNAs. Am J Respir Cell Mol Biol. 2013;49(4):544–551.
   PubMed Web of Science ®Google Scholar
• Amato F, Tomaiuolo R, Nici F, et al. Exploitation of a very small peptide nucleic acid as a new inhibitor of miR-509-3p involved in the regulation of cystic fibrosis disease-gene expression. Biomed Res Int. 2014;2014:610718.
   PubMed Web of Science ®Google Scholar
• Katsirntaki K, Mauritz C, Olmer R, et al. Bronchoalveolar sublineage specification of pluripotent stem cells: effect of dexamethasone plus cAMP-elevating agents and keratinocyte growth factor. Tissue Eng Part A. 2015; 21 (3–4): 669–682.
   PubMed Web of Science ®Google Scholar
• Huang SX, Islam MN, O’Neill J, et al. Efficient generation of lung and airway epithelial cells from human pluripotent stem cells. Nat Biotechnol. 2014;32(1):84–91.
   PubMed Web of Science ®Google Scholar
• Schmeckebier S, Mauritz C, Katsirntaki K, et al. Keratinocyte growth factor and dexamethasone plus elevated cAMP levels synergistically support pluripotent stem cell differentiation into alveolar epithelial type II cells. Tissue Eng Part A. 2013; 19 (7–8): 938–951.
   PubMed Web of Science ®Google Scholar
• Wong AP, Bear CE, Chin S, et al. Directed differentiation of human pluripotent stem cells into mature airway epithelia expressing functional CFTR protein. Nat Biotechnol. 2012;30(9):876–882.
   PubMed Web of Science ®Google Scholar
• Crane AM, Kramer P, Bui JH, et al. Targeted correction and restored function of the CFTR gene in cystic fibrosis induced pluripotent stem cells. Stem Cell Reports. 2015;4(4):569–577.
   PubMed Web of Science ®Google Scholar
• Jih KY, Hwang TC. Vx-770 potentiates CFTR function by promoting decoupling between the gating cycle and ATP hydrolysis cycle. Proc Natl Acad Sci U S A. 2013;110(11):4404–4409.
   PubMed Web of Science ®Google Scholar
• Sawicki GS, McKone EF, Pasta DJ, et al. Sustained benefit from ivacaftor demonstrated by combining clinical trial and cystic fibrosis patient registry data. Am J Respir Crit Care Med. 2015;192(7):836–842.
   PubMed Web of Science ®Google Scholar
• Davies JC, Wainwright CE, Canny GJ, et al. Efficacy and safety of ivacaftor in patients aged 6 to 11 years with cystic fibrosis with a G551D mutation. Am J Respir Crit Care Med. 2013;187(11):1219–1225.
   PubMed Web of Science ®Google Scholar
• McKone EF, Borowitz D, Drevinek P, et al. Long-term safety and efficacy of ivacaftor in patients with cystic fibrosis who have the Gly551Asp-CFTR mutation: a phase 3, open-label extension study (PERSIST). Lancet Respir Med. 2014;2(11):902–910.
   PubMed Web of Science ®Google Scholar
• Ramsey BW, Davies J, McElvaney NG, et al. A CFTR potentiator in patients with cystic fibrosis and the G551D mutation. N Engl J Med. 2011;365(18):1663–1672.
   PubMed Web of Science ®Google Scholar
• De Boeck K, Munck A, Walker S, et al. Efficacy and safety of ivacaftor in patients with cystic fibrosis and a non-G551D gating mutation. J Cyst Fibros. 2014;13(6):674–680.
   PubMed Web of Science ®Google Scholar
• Davies JC, Cunningham S, Harris WT, et al. Safety, pharmacokinetics, and pharmacodynamics of ivacaftor in patients aged 2–5 years with cystic fibrosis and a CFTR gating mutation (KIWI): an open-label, single-arm study. Lancet Respir Med. 2016;4(2):107–115.
   PubMed Web of Science ®Google Scholar
• Flume PA, Liou TG, Borowitz DS, et al. Ivacaftor in subjects with cystic fibrosis who are homozygous for the F508del-CFTR mutation. Chest. 2012;142(3):718–724.
   PubMed Web of Science ®Google Scholar
• Wagener JS, Millar SJ, Mayer-Hamblett N, et al. Lung function decline is delayed but not decreased in patients with cystic fibrosis and the R117H gene mutation. J Cyst Fibros. 2017; pii: S1569-1993(17)30912-8. doi: 10.1016/j.jcf.2017.10.003. [Epub ahead of proint].
   Google Scholar
• Rowe SM, Daines C, Ringshausen FC, et al. Tezacaftor-ivacaftor in residual-function heterozygotes with cystic fibrosis. N Engl J Med. 2017;377(21):2024–2035.
   PubMed Web of Science ®Google Scholar
• Elborn JS, Ramsey BW, Boyle MP, et al. Efficacy and safety of lumacaftor/ivacaftor combination therapy in patients with cystic fibrosis homozygous for Phe508del CFTR by pulmonary function subgroup: a pooled analysis. Lancet Respir Med. 2016;4(8):617–626.
   PubMed Web of Science ®Google Scholar
• Milla CE, Ratjen F, Marigowda G, et al. Lumacaftor/ivacaftor in patients aged 6–11 years with cystic fibrosis and homozygous for F508del-CFTR. Am J Respir Crit Care Med. 2017;195(7):912–920.
   PubMed Web of Science ®Google Scholar
• Ratjen F, Hug C, Marigowda G, et al. Efficacy and safety of lumacaftor and ivacaftor in patients aged 6-11 years with cystic fibrosis homozygous for F508del-CFTR: a randomised, placebo-controlled phase 3 trial. Lancet Respir Med. 2017;5(7):557–567.
   PubMed Web of Science ®Google Scholar
• Taylor-Cousar JL, Munck A, McKone EF, et al. Tezacaftor-ivacaftor in patients with cystic fibrosis homozygous for Phe508del. N Engl J Med. 2017;377(21):2013–2023.
   PubMed Web of Science ®Google Scholar
• Griesenbach U, Geddes DM, Alton EW. Gene therapy for cystic fibrosis: an example for lung gene therapy. Gene Ther. 2004;11 Suppl 1:S43–50.
   PubMedGoogle Scholar
• Alton E, Armstrong DK, Ashby D, et al. Repeated nebulisation of non-viral CFTR gene therapy in patients with cystic fibrosis: a randomised, double-blind, placebo-controlled, phase 2b trial. Lancet Respir Med. 2015;3(9):684–691.
   PubMed Web of Science ®Google Scholar
• Mali P, Yang L, Esvelt KM, et al. RNA-guided human genome engineering via Cas9. Science. 2013;339(6121):823–826.
   PubMed Web of Science ®Google Scholar
• Cong L, Ran FA, Cox D, et al. Multiplex genome engineering using CRISPR/Cas systems. Science. 2013;339(6121):819–823.
   PubMed Web of Science ®Google Scholar
• Firth AL, Menon T, Parker GS, et al. Functional gene correction for cystic fibrosis in lung epithelial cells generated from patient iPSCs. Cell Rep. 2015;12(9):1385–1390.
   PubMed Web of Science ®Google Scholar
• Oglesby IK, Bray IM, Chotirmall SH, et al. miR-126 is downregulated in cystic fibrosis airway epithelial cells and regulates TOM1 expression. J Immunol. 2010;184(4):1702–1709.
   PubMed Web of Science ®Google Scholar
• Oglesby IK, Chotirmall SH, McElvaney NG, et al. Regulation of cystic fibrosis transmembrane conductance regulator by microRNA-145, −223, and −494 is altered in DeltaF508 cystic fibrosis airway epithelium. J Immunol. 2013;190(7):3354–3362.
   PubMed Web of Science ®Google Scholar
• Gillen AE, Gosalia N, Leir SH, et al. MicroRNA regulation of expression of the cystic fibrosis transmembrane conductance regulator gene. Biochem J. 2011;438(1):25–32.
   PubMed Web of Science ®Google Scholar
• Megiorni F, Cialfi S, Dominici C, et al. Synergistic post-transcriptional regulation of the cystic fibrosis transmembrane conductance regulator (CFTR) by miR-101 and miR-494 specific binding. PLoS One. 2011;6(10):e26601.
   PubMed Web of Science ®Google Scholar
• Hassan F, Nuovo GJ, Crawford M, et al. MiR-101 and miR-144 regulate the expression of the CFTR chloride channel in the lung. PLoS One. 2012;7(11):e50837.
   PubMed Web of Science ®Google Scholar
• Viart V, Bergougnoux A, Bonini J, et al. Transcription factors and miRNAs that regulate fetal to adult CFTR expression change are new targets for cystic fibrosis. Eur Respir J. 2015;45(1):116–128.
   PubMed Web of Science ®Google Scholar
• Rab A, Rowe SM, Raju SV, et al. Cigarette smoke and CFTR: implications in the pathogenesis of COPD. Am J Physiol Lung Cell Mol Physiol. 2013;305(8):L530–41.
   PubMed Web of Science ®Google Scholar
• Cantin AM. Cystic fibrosis transmembrane conductance regulator. Implications in cystic fibrosis and chronic obstructive pulmonary disease. Ann Am Thorac Soc. 2016;13 Suppl 2:S150–5.
   PubMedGoogle Scholar
• Johannesson B, Hirtz S, Schatterny J, et al. CFTR regulates early pathogenesis of chronic obstructive lung disease in betaENaC-overexpressing mice. PLoS One. 2012;7(8):e44059.
   PubMed Web of Science ®Google Scholar