Apoptotic process in cystic fibrosis cells

Apoptosis

Volumn 18, Issue 9, 2013, Pages 1029-1038

  Soleti, Raffaella ^a,b   Porro, Chiara ^c   Martínez, Maria Carmen ^a,b  

^a LUNAM Universite   (France)

^b UNIVERSITÉ D'ANGERS   (France)

^c UNIVERSITY OF FOGGIA   (Italy)

Author keywords

Apoptosis; Cystic fibrosis; Efferocytosis; Epithelial cell; Inflammation; Polymorphonuclear neutrophil

Indexed keywords

CHLORIDE CHANNEL; COMPLEMENTARY DNA; CYCLIN DEPENDENT KINASE INHIBITOR 2A; CYCLOHEXIMIDE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPITHELIAL SODIUM CHANNEL; GLUTATHIONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; LEUKOCYTE ELASTASE; MUCIN; PHOSPHATIDYLSERINE; REACTIVE OXYGEN METABOLITE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

AMINO ACID SUBSTITUTION; APOPTOSIS; ARTICLE; BACTERIAL COLONIZATION; BRONCHIECTASIS; CELL MEMBRANE; CELL SURVIVAL; CHLORIDE TRANSPORT; CYSTIC FIBROSIS; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; EPITHELIUM CELL; EXOCYTOSIS; GENE THERAPY; HOMEOSTASIS; HOMOLOGOUS RECOMBINATION; HUMAN; INFLAMMATION; INFLAMMATORY CELL; INNATE IMMUNITY; LUNG FUNCTION; MUCOCILIARY CLEARANCE; NEUTROPHIL; PATHOGENESIS; PATHOPHYSIOLOGY; PHAGOCYTOSIS; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; RESPIRATORY EPITHELIUM; ANIMAL; CYTOLOGY; GENETICS; IMMUNOLOGY; MUTATION;

BACTERIA (MICROORGANISMS);

ANIMALS; APOPTOSIS; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPITHELIAL CELLS; HUMANS; MUTATION;

EID: 84881475286     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-013-0874-y     Document Type: Article

References (91)

1. Griesenbach U, Alton EW (2011) Current status and future directions of gene and cell therapy for cystic fibrosis. BioDrugs 25:77-88
2. Cohen TS, Prince A (2012) Cystic fibrosis: a mucosal immunodeficiency syndrome. Nat Med 18:509-519
3. Cystic fibrosis foundation website. http://www.cff.org/AboutCF/. Accessed Feb 2013
4. Kerem B, Rommens JM, Buchanan JA, Markiewicz D, Cox TK, Chakravarti A, Buchwald M, Tsui LC (1989) Identification of the cystic fibrosis gene: genetic analysis. Science 245:1073-1080
5. Riordan JR, Rommens JM, Kerem B, Alon N, Rozmahel R, Grzelczak Z, Zielenski J, Lok S, Plavsic N, Chou JL et al (1989) Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science 245:1066-1073
6. Cantin A (1995) Cystic fibrosis lung inflammation: early, sustained, and severe. Am J Respir Crit Care Med 151:939-941
7. Nichols D, Chmiel J, Berger M (2008) Chronic inflammation in the cystic fibrosis lung: alterations in inter- and intra-cellular signaling. Clin Rev Allergy Immunol 34:146-162
8. Farrell PM, Rosenstein BJ, White TB, Accurso FJ, Castellani C, Cutting GR, Durie PR, Legrys VA, Massie J, Parad RB, Rock MJ, Campbell PW 3rd, Cystic Fibrosis Foundation (2008) Guidelines for diagnosis of cystic fibrosis in newborn through older adults: Cystic Fibrosis Foundation consensus report. J Pediatr 153:S4-S14
9. Maiuri L, Raia V, De Marco G, Coletta S, de Ritis G, Londei M, Auricchio S (1997) DNA fragmentation is a feature of cystic fibrosis epithelial cells: a disease with inappropriate apoptosis? FEBS Lett 408:225-231
10. Zwaal RFA, Comfurius P, Bevers EM (2005) Surface exposure of phosphatidylserine in pathological cells. Cell Mol Life Sci 62:971-988
11. De Boeck K, Wilschanski M, Castellani C, Taylor C, Cuppens H, Dodge J, Sinaasappel M, Diagnostic Working Group (2006) Cystic fibrosis: terminology and diagnostic algorithms. Thorax 61:627-635
12. Stick SM, Brennan S, Murray C, Douglas T, von Ungern-Sternberg BS, Garratt LW, Gangell CL, De Klerk N, Linnane B, Ranganathan S, Robinson P, Robertson C, Sly PD, Australian Respiratory Early Surveillance Team for Cystic Fibrosis (AREST CF) (2009) Bronchiectasis in infants and preschool children diagnosed with cystic fibrosis after newborn screening. J Pediatr 155:623-628
13. Linnane BM, Hall GL, Nolan G, Brennan S, Stick SM, Sly PD, Robertson CF, Robinson PJ, Franklin PJ, Turner SW, Ranganathan SC, AREST-CF (2008) Lung function in infants with cystic fibrosis diagnosed by newborn screening. Am J Respir Crit Care Med 178:1238-1244
14. Sly PD, Brennan S, Gangell C, de Klerk N, Murray C, Mott L, Stick SM, Robinson PJ, Robertson CF, Ranganathan SC, Australian Respiratory Early Surveillance Team for Cystic Fibrosis (AREST-CF) (2009) Lung disease at diagnosis in infants with cystic fibrosis detected by newborn screening. Am J Respir Crit Care Med 180:146-152
15. Muhlebach MS, Stewart PW, Leigh MW, Noah TL (1999) Quantitation of inflammatory responses to bacteria in young cystic fibrosis and control patients. Am J Respir Crit Care Med 160:186-191
16. Pillarisetti N, Williamson E, Linnane B, Skoric B, Robertson CF, Robinson P, Massie J, Hall GL, Sly P, Stick S, Ranganathan S, Australian Respiratory Early Surveillance Team for Cystic Fibrosis (AREST CF) (2011) Infection, inflammation, and lung function decline in infants with cystic fibrosis. Am J Respir Crit Care Med 184:75-81
17. Basu S, Fenton MJ (2004) Toll-like receptors: function and roles in lung disease. Am J Physiol Lung Cell Mol Physiol 286:L887-L892
18. Zaman MM, Gelrud A, Junaidi O, Regan MM, Warny M, Shea JC, Kelly C, O'Sullivan BP, Freedman SD (2004) Interleukin 8 secretion from monocytes of subjects heterozygous for the deltaF508 cystic fibrosis transmembrane conductance regulator gene mutation is altered. Clin Diagn Lab Immunol 11:819-824
19. Vandivier RW, Fadok VA, Hoffmann PR, Bratton DL, Penvari C, Brown KK, Brain JD, Accurso FJ, Henson PM (2002) Elastase-mediated phosphatidylserine receptor cleavage impairs apoptotic cell clearance in cystic fibrosis and bronchiectasis. J Clin Invest 109:661-670
20. Day BJ (2005) Glutathione: a radical treatment for cystic fibrosis lung disease? Chest 127:12-14
21. Roum JH, Borok Z, McElvaney NG, Grimes GJ, Bokser AD, Buhl R, Crystal RG (1999) Glutathione aerosol suppresses lung epithelial surface inflammatory cell-derived oxidants in cystic fibrosis. J Appl Physiol 87:438-443
22. Velsor LW, Kariya C, Kachadourian R, Day BJ (2006) Mitochondrial oxidative stress in the lungs of cystic fibrosis transmembrane conductance regulator protein mutant mice. Am J Respir Cell Mol Biol 35:579-586
23. Kelly-Aubert M, Trudel S, Fritsch J, Nguyen-Khoa T, Baudouin-Legros M, Moriceau S, Jeanson L, Djouadi F, Matar C, Conti M, Ollero M, Brouillard F, Edelman A (2011) GSH monoethyl ester rescues mitochondrial defects in cystic fibrosis models. Hum Mol Genet 20:2745-2759
24. Pier GB (2012) The challenges and promises of new therapies. J Exp Med 209:1235-1239
25. Jouret F, Bernard A, Hermans C, Dom G, Terryn S, Leal T, Lebecque P, Cassiman JJ, Scholte BJ, de Jonge HR, Courtoy PJ, Devuyst O (2007) Cystic fibrosis is associated with a defect in apical receptor-mediated endocytosis in mouse and human kidney. J Am Soc Nephrol 18:707-718
26. Raggi C, Fujiwara K, Leal T, Jouret F, Devuyst O, Terryn S (2011) Decreased renal accumulation of aminoglycoside reflects defective receptor-mediated endocytosis in cystic fibrosis and Dent's disease. Pflugers Arch 462:851-860
27. Howard M, Jilling T, DuVall M, Frizzell RA (1996) cAMP-regulated trafficking of epitope-tagged CFTR. Kidney Int 49:1642-1648
28. Vandivier RW, Richens TR, Horstmann SA, deCathelineau AM, Ghosh M, Reynolds SD, Xiao YQ, Riches DW, Plumb J, Vachon E, Downey GP, Henson PM (2009) Dysfunctional cystic fibrosis transmembrane conductance regulator inhibits phagocytosis of apoptotic cells with proinflammatory consequences. Am J Physiol Lung Cell Mol Physiol 297:L677-L686
29. Tsui LC, Buchwald M, Barker D, Braman JC, Knowlton R, Schumm JW, Eiberg H, Mohr J, Kennedy D, Plavsic N et al (1985) Cystic fibrosis locus defined by a genetically linked polymorphic DNA marker. Science 230:1054-1057
30. Wainwright BJ, Scambler PJ, Schmidtke J, Watson EA, Law HY, Farrall M, Cooke HJ, Eiberg H, Williamson R (1985) Localization of cystic fibrosis locus to human chromosome 7cen-q22. Nature 318:384385
31. Ford RC, Birtley J, Rosenberg MF, Zhang L (2011) CFTR three-dimensional structure. Methods Mol Biol 741:329-346
32. Gadsby DC, Vergani P, Csanady L (2006) The ABC protein turned chloride channel whose failure causes cystic fibrosis. Nature 440:477-483
33. Lewis HA, Buchanan SG, Burley SK, Conners K, Dickey M, Dorwart M, Fowler R, Gao X, Guggino WB, Hendrickson WA, Hunt JF, Kearins MC, Lorimer D, Maloney PC, Post KW, Rajashankar KR, Rutter ME, Sauder JM, Shriver S, Thibodeau PH, Thomas PJ, Zhang M, Zhao X, Emtage S (2004) Structure of nucleotide-binding domain 1 of the cystic fibrosis transmembrane conductance regulator. EMBO J 23:282-293
34. Linsdell P (2006) Mechanism of chloride permeation in the cystic fibrosis transmembrane conductance regulator chloride channel. Exp Physiol 91:123129
35. Wang W, El Hiani Y, Linsdell P (2011) Alignment of transmembrane regions in the cystic fibrosis transmembrane conductance regulator chloride channel pore. J Gen Physiol 138:165-178
36. Chen TY, Hwang TC (2008) CLC-0 and CFTR: chloride channels evolved from transporters. Physiol Rev 88:351-387
37. Hwang TC, Sheppard DN (2009) Gating of the CFTR Cl- channel by ATP-driven nucleotide-binding domain dimerisation. J Physiol 587:2151-2161
38. Vergani P, Lockless SW, Nairn AC, Gadsby DC (2005) CFTR channel opening by ATP-driven tight dimerization of its nucleotide-binding domains. Nature 433:876-880
39. Serohijos AW, Hegedus T, Aleksandrov AA, He L, Cui L, Dokholyan NV, Riordan JR (2008) Phenylalanine-508 mediates a cytoplasmic-membrane domain contact in the CFTR 3D structure crucial to assembly and channel function. Proc Natl Acad Sci USA 105:3256-3261
40. Gelman MS, Kopito RR (2002) Rescuing protein conformation: prospects for pharmacological therapy in cystic fibrosis. J Clin Invest 110:1591-1597
41. Varga K, Jurkuvenaite A, Wakefield J, Hong JS, Guimbellot JS, Venglarik CJ, Niraj A, Mazur M, Sorscher EJ, Collawn JF, Bebok Z (2004) Efficient intracellular processing of the endogenous cystic fibrosis transmembrane conductance regulator in epithelial cell lines. J Biol Chem 279:22578-22584
42. Lukacs GL, Mohamed A, Kartner N, Chang XB, Riordan JR, Grinstein S (1994) Conformational maturation of CFTR but not its mutant counterpart (delta F508) occurs in the endoplasmic reticulum requires ATP. EMBO J 13:6076-6086
43. Ward CL, Kopito RR (1994) Intracellular turnover of cystic fibrosis transmembrane conductance regulator. Inefficient processing and rapid degradation of wild-type and mutant protein. J Biol Chem 269:25710-25718
44. Drumm M (1999) What happens to deltaF508 in vivo? J Clin Invest 103:1369-1370
45. Cheng SH, Gregory RJ, Marshall J, Paul S, Souza DW, White GA, O'Riordan CR, Smith AE (1990) Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Cell 63:827-834
46. Qu BH, Thomas PJ (1996) Alteration of the cystic fibrosis transmembrane conductance regulator folding pathway. J Biol Chem 271:7261-7264
47. Lukacs GL, Chang XB, Bear C, Kartner N, Mohamed A, Riordan JR, Grinstein S (1993) The delta F508 mutation decreases the stability of cystic fibrosis transmembrane conductance regulator in the plasma membrane. Determination of functional half-lives on transfected cells. J Biol Chem 268:21592-21598
48. Dalemans W, Barbry P, Champigny G, Jallat S, Dott K, Dreyer D, Crystal RG, Pavirani A, Lecocq JP, Lazdunski M (1991) Altered chloride ion channel kinetics associated with the delta F508 cystic fibrosis mutation. Nature 354:526-528
49. Rubenstein RC (2005) Novel, mechanism-based therapies for cystic fibrosis. Curr Opin Pediatr 17:385-392
50. Rowe SM, Miller S, Sorscher EJ (2005) Cystic fibrosis. N Engl J Med 352:1992-2001
51. Sharma M, Pampinella F, Nemes C, Benharouga M, So J, Du K, Bache KG, Papsin B, Zerangue N, Stenmark H, Lukacs GL (2004) Misfolding diverts CFTR from recycling to degradation: quality control at early endosomes. J Cell Biol 164:923-933
52. Zielenski J (2000) Genotype and phenotype in cystic fibrosis. Respiration 67:117-133
53. Grove DE, Rosser MF, Watkins RL, Cyr DM (2011) Analysis of CFTR folding and degradation in transiently transfected cells. Methods Mol Biol 741:219-232
54. Bartoszewski R, Rab A, Jurkuvenaite A, Mazur M, Wakefield J, Collawn JF, Bebok Z (2008) Activation of the unfolded protein response by {delta}F508 CFTR. Am J Respir Cell Mol Biol 39:448-457
55. Bartoszewski R, Rab A, Twitty G, Stevenson L, Fortenberry J, Piotrowski A, Dumanski JP, Bebok Z (2008) The mechanism of cystic fibrosis transmembrane conductance regulator transcriptional repression during the unfolded protein response. J Biol Chem 283:12154-12165
56. Kerbiriou M, Le Drévo MA, Férec C, Trouvé P (2007) Coupling cystic fibrosis to endoplasmic reticulum stress: differential role of Grp78 and ATF6. Biochim Biophys Acta 1772:1236-1249
57. Kerbiriou M, Teng L, Benz N, Trouvé P, Férec C (2009) The calpain, caspase 12, caspase 3 cascade leading to apoptosis is altered in F508del-CFTR expressing cells. PLoS One 4:e8436
58. Jacquot J, Tabary O, Le Rouzic P, Clement A (2008) Airway epithelial cell inflammatory signalling in cystic fibrosis. Int J Biochem Cell Biol 40:1703-1715
59. Chmiel JF, Davis PB (2003) State of the art: why do the lungs of patients with cystic fibrosis become infected and why can't they clear the infection? Respir Res 4:8
60. Boucher RC (2007) Cystic fibrosis: a disease of vulnerability to airway surface dehydration. Trends Mol Med 13:231-240
61. Donaldson SH, Bennett WD, Zeman KL, Knowles MR, Tarran R, Boucher RC (2006) Mucus clearance and lung function in cystic fibrosis with hypertonic saline. N Engl J Med 354:241-250
62. Durieu I, Amsellem C, Paulin C, Chambe MT, Bienvenu J, Bellon G, Pacheco Y (1999) Fas and Fas ligand expression in cystic fibrosis airway epithelium. Thorax 54:1093-1098
63. Rottner M, Kunzelmann C, Mergey M, Freyssinet JM, Martinez MC (2007) Exaggerated apoptosis and NF-kappaB activation in pancreatic and tracheal cystic fibrosis cells. FASEB J 21:2939-2948
64. Rottner M, Tual-Chalot S, Mostefai HA, Andriantsitohaina R, Freyssinet JM, Martínez MC (2011) Increased oxidative stress induces apoptosis in human cystic fibrosis cells. PLoS One 6:e24880
65. Chaudhary N, Datta K, Askin FB, Staab JF, Marr KA (2012) Cystic fibrosis transmembrane conductance regulator regulates epithelial cell response to Aspergillus and resultant pulmonary inflammation. Am J Respir Crit Care Med 185:301-310
66. Bodas M, Min T, Vij N (2011) Critical role of CFTR dependent lipid-rafts in cigarette smoke induced lung epithelial injury. Am J Physiol 300:L811-L820
67. Yalçin E, Talim B, Ozçelik U, Doǧru D, Cobanoǧlu N, Pekcan S, Kiper N (2009) Does defective apoptosis play a role in cystic fibrosis lung disease? Arch Med Res 40:561-564
68. Rajan S, Cacalano G, Bryan R, Ratner AJ, Sontich CU, van Heerckeren A, Davis P, Prince A (2000) Pseudomonas aeruginosa induction of apoptosis in respiratory epithelial cells: analysis of the effects of cystic fibrosis transmembrane conductance regulator dysfunction and bacterial virulence factors. Am J Respir Cell Mol Biol 23:304-312
69. Gottlieb RA, Dosanjh A (1996) Mutant cystic fibrosis transmembrane conductance regulator inhibits acidification and apoptosis in C127 cells: possible relevance to cystic fibrosis. Proc Natl Acad Sci USA 93:3587-3591
70. Tabary O, Corvol H, Boncoeur E, Chadelat K, Fitting C, Cavaillon JM, Clément A, Jacquot J (2006) Adherence of airway neutrophils and inflammatory response are increased in CF airway epithelial cell-neutrophil interactions. Am J Physiol Lung Cell Mol Physiol 290:L588-L596
71. McKeon DJ, Condliffe AM, Cowburn AS, Cadwallader KC, Farahi N, Bilton D, Chilvers ER (2008) Prolonged survival of neutrophils from patients with Delta F508 CFTR mutations. Thorax 63:660-661
72. Moriceau S, Kantari C, Mocek J, Davezac N, Gabillet J, Guerrera IC, Brouillard F, Tondelier D, Sermet-Gaudelus I, Danel C, Lenoir G, Daniel S, Edelman A, Witko-Sarsat V (2009) Coronin-1 is associated with neutrophil survival and is cleaved during apoptosis: potential implication in neutrophils from cystic fibrosis patients. J Immunol 182:7254-7763
73. Moriceau S, Lenoir G, Witko-Sarsat V (2010) In cystic fibrosis homozygotes and heterozygotes, neutrophil apoptosis is delayed and modulated by diamide or roscovitine: evidence for an innate neutrophil disturbance. J Innate Immun 2:260-266
74. Saba S, Soong G, Greenberg S, Prince A (2002) Bacterial stimulation of epithelial G-CSF and GM-CSF expression promotes PMN survival in CF airways. Am J Respir Cell Mol Biol 27:561-567
75. Baumann R, Casaulta C, Simon D, Conus S, Yousefi S, Simon HU (2003) Macrophage migration inhibitory factor delays apoptosis in neutrophils by inhibiting the mitochondria-dependent death pathway. FASEB J 17:2221-2230
76. Martinez MC, Tual-Chalot S, Leonetti D, Andriantsitohaina R (2011) Microparticles: targets and tools in cardiovascular disease. Trends Pharmacol Sci 32:659-665
77. Porro C, Lepore S, Trotta T, Castellani S, Ratclif L, Battaglino A, Di Gioia S, Martínez MC, Conese M, Maffione AB (2010) Isolation and characterization of microparticles in sputum from cystic fibrosis patients. Respir Res 11:94
78. Porro C, Di Gioia S, Trotta T, Lepore S, Panaro MA, Battaglino A, Ratclif L, Castellani S, Bufo P, Martinez MC, Conese M (2013) Pro-inflammatory effect of cystic fibrosis sputum microparticles in the murine lung. J Cyst Fibros. doi: 10.1016/j.jcf.2013.03.002
79. Heutinck KM, ten Berge IJ, Hack CE, Hamann J, Rowshani AT (2010) Serine proteases of the human immune system in health and disease. Mol Immunol 47:1943-1955
80. Zemans RL, Colgan SP, Downey GP (2009) Transepithelial migration of neutrophils: mechanisms and implications for acute lung injury. Am J Respir Cell Mol Biol 40:519-535
81. Fischer BM, Wong JK, Degan S, Kummarapurugu AB, Zheng S, Haridass P, Voynow JA (2013) Increased expression of senescence markers in cystic fibrosis airways. Am J Physiol Lung Cell Mol Physiol 30:394-400
82. Le Gars M, Descamps D, Roussel D, Saussereau E, Guillot L, Ruffin M, Tabary O, Hong SS, Boulanger P, Paulais M, Malleret L, Belaaouaj A, Edelman A, Huerre M, Chignard M, Sallenave JM (2013) Neutrophil elastase degrades cystic fibrosis transmembrane conductance regulator via calpains and disables channel function in vitro and in vivo. Am J Respir Crit Care Med 187:170-179
83. Suzuki T, Moraes TJ, Vachon E, Ginzberg HH, Huang TT, Matthay MA, Hollenberg MD, Marshall J, McCulloch CA, Abreu MT, Chow CW, Downey GP (2005) Proteinase-activated receptor 1 mediates elastase-induced apoptosis of human lung epithelial cells. Am J Respir Cell Mol Biol 33:231-247
84. Henson PM, Bratton DL, Fadok VA (2001) Apoptotic cell removal. Curr Biol 11:R795-R805
85. Vandivier RW, Henson PM, Douglas IS (2006) Burying the dead: the impact of failed apoptotic cell removal (efferocytosis) on chronic inflammatory lung disease. Chest 129:1673-1682
86. Khan TZ, Wagener JS, Bost T, Martinez J, Accurso FJ, Riches DW (1995) Early pulmonary inflammation in infants with cystic fibrosis. Am J Respir Crit Care Med 151:1075-1082
87. Gonzalez G, Vituret C, Di Pietro A, Chanson M, Boulanger P, Hong SS (2012) Microparticle-mediated transfer of the viral receptors CAR and CD46, and the CFTR channel in a CHO cell model confers new functions to target cells. PLoS One 7:e52326
88. Rogers CS, Hao Y, Rokhlina T, Samuel M, Stoltz DA, Li Y, Petroff E, Vermeer DW, Kabel AC, Yan Z, Spate L, Wax D, Murphy CN, Rieke A, Whitworth K, Linville ML, Korte SW, Engelhardt JF, Welsh MJ, Prather RS (2008) Production of CFTR-null and CFTR-ΔF508 heterozygous pigs by adeno-associated virus-mediated gene targeting and somatic cell nuclear transfer. J Clin Invest 118:1571-1577
89. Ostedgaard LS, Meyerholz DK, Chen JH, Pezzulo AA, Karp PH, Rokhlina T, Ernst SE, Hanfland RA, Reznikov LR, Ludwig PS, Rogan MP, Davis GJ, Dohrn CL, Wohlford-Lenane C, Taft PJ, Rector MV, Hornick E, Nassar BS, Samuel M, Zhang Y, Richter SS, Uc A, Shilyansky J, Prather RS, McCray PB Jr, Zabner J, Welsh MJ, Stoltz DA (2011) The ΔF508 mutation causes CFTR misprocessing and cystic fibrosis-like disease in pigs. Sci Transl Med 3:74ra24
90. Sun X, Sui H, Fisher JT, Yan Z, Liu X, Cho HJ, Joo NS, Zhang Y, Zhou W, Yi Y, Kinyon JM, Lei-Butters DC, Griffin MA, Naumann P, Luo M, Ascher J, Wang K, Frana T, Wine JJ, Meyerholz DK, Engelhardt JF (2010) Disease phenotype of a ferret CFTR-knockout model of cystic fibrosis. J Clin Invest 120:3149-3160
91. Keiser NW, Engelhardt JF (2011) New animal models of cystic fibrosis: what are they teaching us? Curr Opin Pulm Med 17:478-483