Increased airway epithelial Na+ absorption produces cystic fibrosis-like lung disease in mice

Nature Medicine

Volumn 10, Issue 5, 2004, Pages 487-493

  Mall, Marcus ^a   Grubb, Barbara R ^a   Harkema, Jack R ^b   O'Neal, Wanda K ^a   Boucher, Richard C ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORIDE ION; CYTOKINE; INTERLEUKIN 13; INTERLEUKIN 4; SODIUM ION; TRANSMEMBRANE CONDUCTANCE REGULATOR;

AIRWAY; ANIMAL CELL; ANIMAL MODEL; ARTICLE; BRONCHUS MUCUS; CONTROLLED STUDY; CYSTIC FIBROSIS; GENE MUTATION; GOBLET CELL; LUNG DISEASE; METAPLASIA; MOUSE; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; SODIUM ABSORPTION; TRANSGENIC MOUSE;

ANIMALS; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DISEASE MODELS, ANIMAL; EPITHELIAL SODIUM CHANNEL; EPITHELIUM; HUMANS; LUNG; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, TRANSGENIC; MUCUS; SODIUM; SODIUM CHANNELS;

ANIMALIA; BACTERIA (MICROORGANISMS); BRONCHUS; MUS MUSCULUS;

EID: 2442718786     PISSN: 10788956     EISSN: None     Source Type: Journal    
DOI: 10.1038/nm1028     Document Type: Article

References (50)

1. Kerem, B. et al. Identification of the cystic fibrosis gene: genetic analysis. Science 245, 1073-1080 (1989).
2. Welsh, M.J., Ramsey, B.W., Accurso, F. & Cutting, G.R. Cystic fibrosis. in The Metabolic & Molecular Bases of Inherited Disease (eds. Scriver, C.R., Beaudet, A.L., Sly, W.S. & Valle, D.) 5121-5188 (McGraw-Hill, New York, 2001).
3. Anderson, M.P. et al. Demonstration that CFTR is a chloride channel by alteration of its anion selectivity. Science 253, 202-205 (1991).
4. Smith, J.J., Travis, S.M., Greenberg, E.P. & Welsh, M.J. Cystic fibrosis airway epithelia fail to kill bacteria because of abnormal airway surface fluid. Cell 85, 229-236 (1996).
5. Zabner, J., Smith, J.J., Karp, P.H., Widdicombe, J.H. & Welsh, M.J. Loss of CFTR chloride channels alters salt absorption by cystic fibrosis airway epithelia in vitro. Mol. Cell 2, 397-403 (1998).
6. + channel is made of three homologous subunits. Nature 367, 463-467 (1994).
7. Stutts, M.J. et al. CFTR as a cAMP-dependent regulator of sodium channels. Science 269, 847-850 (1995).
8. + conductance when coexpressed in Xenopus oocytes. FEBS Lett. 381, 47-52 (1996).
9. + conductance is reduced by CFTR in normal but not in cystic fibrosis airways. J. Clin. Invest. 102, 15-21 (1998).
10. Matsui, H. et al. Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease. Cell 95, 1005-1015 (1998).
11. Knowles, M.R. & Boucher, R.C. Mucus clearance as a primary innate defense mechanism for mammalian airways. J. Clin. Invest. 109, 571-577 (2002).
12. Wine, J.J. The genesis of cystic fibrosis lung disease. J. Clin. Invest. 103, 309-312 (1999).
13. Guggino, W.B. Cystic fibrosis and the salt controversy. Cell 96, 607-610 (1999).
14. +] and pH but elevated viscosity. Proc. Natl. Acad. Sci. USA 98, 8119-8123 (2001).
15. Verkman, A.S., Song, Y. & Thiagarajah, J.R. Role of airway surface liquid and submucosal glands in cystic fibrosis lung disease. Am. J. Physiol. Cell. Physiol. 284, C2-C15 (2003).
16. Heeckeren, A. et al. Excessive inflammatory response of cystic fibrosis mice to bronchopulmonary infection with Pseudomonas aeruginosa. J. Clin. Invest. 100, 2810-2815 (1997).
17. Snouwaert, J.N. et al. An animal model for cystic fibrosis made by gene targeting. Science 257, 1083-1088 (1992).
18. Grubb, B.R. & Boucher, R.C. Pathophysiology of gene-targeted mouse models for cystic fibrosis. Physiol. Rev. 79, S193-S214 (1999).
19. Hackett, B.P. & Gitlin, J.D. Cell-specific expression of a Clara cell secretory protein-human growth hormone gene in the bronchiolar epithelium of transgenic mice. Proc. Natl. Acad, Sci. USA 89, 9079-9083 (1992).
20. Ahn, Y.J. et al. Cloning and functional expression of the mouse epithelial sodium channel. Am. J. Physiol. 277, F121-F129 (1999).
21. Sims, D.E. & Horne, M.M. Heterogeneity of the composition and thickness of tracheal mucus in rats. Am. J. Physiol. 273, L1036-L1041 (1997).
22. Grubb, B.R., Jones, J.H. & Boucher, R.C. Mucociliary transport determined by in vivo microdialysis in the airways of normal and CF mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 286, L588-L595 (2004).
23. Elias, J.A., Zhu, Z., Chupp, G. & Homer, R.J. Airway remodeling in asthma. J. Clin. Invest. 104, 1001-1006 (1999).
24. Boucher, R.C. Human airway ion transport. Part two. Am. J. Respir. Crit. Care Med. 150, 581-593 (1994).
25. Knowles, M.R. et al. Abnormal ion permeation through cystic fibrosis respiratory epithelium. Science 221, 1067-1070 (1983).
26. + transport in cystic fibrosis respiratory epithelia. Abnormal basal rate and response to adenylate cyclase activation. J. Clin. Invest. 78, 1245-1252 (1986).
27. Zuelzer, W.W. & Newton, W.A. The pathogenesis of fibrocystic disease of the pancreas; a study of 36 cases with special reference to the pulmonary lesions. Pediatrics 4, 53-69 (1949).
28. Wanner, A., Salathe, M. & O'Riordan, T.G. Mucociliary clearance in the airways. Am. J. Respir. Crit. Care Med. 154, 1868-1902 (1996).
29. Breuer, R., Christensen, T.G., Lucey, E.C., Stone, P.J. & Snider, G.L. An ultrastructural morphometric analysis of elastase-treated hamster bronchi shows discharge followed by progressive accumulation of secretory granules. Am. Rev. Respir. Dis. 136, 698-703 (1987).
30. Takeyama, K. et al. Neutrophil-dependent goblet cell degranulation: role of membrane-bound elastase and adhesion molecules. Am. J. Physiol. 275, L294-L302 (1998).
31. Voynow, J.A. et al. Neutrophil elastase increases MUC5AC mRNA and protein expression in respiratory epithelial cells. Am. J. Physiol. 276, L835-L843 (1999).
32. Nakamura, H., Yoshimura, K., McElvaney, N.G. & Crystal, R.G. Neutrophil elastase in respiratory epithelial lining fluid of individuals with cystic fibrosis induces interleukin-8 gene expression in a human bronchial epithelial cell line. J. Clin. Invest. 89, 1478-1484 (1992).
33. Takeyama, K. et al. Epidermal growth factor system regulates mucin production in airways. Proc. Natl. Acad, Sci. USA 96, 3081-3086 (1999).
34. Fujii, T., Hayashi, S., Hogg, J.C., Vincent, R. & Van Eeden, S.F. Particulate matter induces cytokine expression in human bronchial epithelial cells. Am. J. Respir. Cell. Mol. Biol. 25, 265-271 (2001).
35. Matthews, L.M., Spector, S., Lemm, J. & Potter, J.L. Studies on pulmonary secretions. Am. Rev. Respir. Dis. 88, 199-204 (1963).
36. Berger, M. Lung inflammation early in cystic fibrosis: bugs are indicted, but the defense is guilty. Am. J. Respir. Crit. Care Med. 165, 857-858 (2002).
37. Tarran, R. et al. The CF salt controversy: in vivo observations and therapeutic approaches. Mol. Cell 8, 149-158 (2001).
38. Chen, J., Knowles, H.J., Hebert, J.L. & Hackett, B.P. Mutation of the mouse hepatocyte nuclear factor/forkhead homologue 4 gene results in an absence of cilia and random left-right asymmetry. J. Clin. Invest. 102, 1077-1082 (1998).
39. Brody, S.L., Yan, X.H., Wuerffel, M.K., Song, S.K. & Shapiro, S.D. Ciliogenesis and left-right axis defects in forkhead factor HFH-4-null mice. Am. J. Respir. Cell. Mol. Biol. 23, 45-51 (2000).
40. Kobayashi, Y. et al. Hydrocephalus, situs inversus, chronic sinusitis, and male infertility in DNA polymerase lambda-deficient mice: possible implication for the pathogenesis of immotile cilia syndrome. Mol. Cell. Biol. 22, 2769-2776 (2002).
41. Ibanez-Tallon, I., Gorokhova, S. & Heintz, N. Loss of function of axonemal dynein Mdnah5 causes primary ciliary dyskinesia and hydrocephalus. Hum. Mol. Genet. 11, 715-721 (2002).
42. Puchelle, E., de Bentzmann, S. & Zahm, J.M. Physical and functional properties of airway secretions in cystic fibrosis - therapeutic approaches. Respiration 62 (suppl. 1), 2-12 (1995).
43. Kim, C.S., Rodriguez, C.R., Eldridge, M.A. & Sackner, M.A. Criteria for mucus transport in the airways by two-phase gas-liquid flow mechanism. J. Appl. Physiol. 60, 901-907 (1986).
44. Masilamani, S., Kim, G.H., Mitchell, C., Wade, J.B. & Knepper, M.A. Aldosterone-mediated regulation of ENaC α, β, and γ subunit proteins in rat kidney. J. Clin. Invest. 104, R19-R23 (1999).
45. Loffing, J. et al. Differential subcellular localization of ENaC subunits in mouse kidney in response to high- and low-Na diets. Am. J. Physiol. Renal Physiol. 279, F252-F258 (2000).
46. Fyfe, G.K. & Canessa, C.M. Subunit composition determines the single channel kinetics of the epithelial sodium channel. J. Gen. Physiol. 112, 423-432 (1998).
47. Baker, E.H. et al. Association of hypertension with T594M mutation in beta subunit of epithelial sodium channels in black people resident in London. Lancet 351, 1388-1392 (1998).
48. Ostrowski, L.E., Hutchins, J.R., Zakel, K. & O'Neal, W.K. Targeting expression of a transgene to the airway surface epithelium using a ciliated cell-specific promoter. Mol. Ther. 8, 637-645 (2003).
49. Grubb, B.R., Pace, A.J., Lee, E., Koller, B.H. & Boucher, R.C. Alterations in airway ion transport in NKCC1-deficient mice. Am. J. Physiol. Cell. Physiol. 281, C615-C623 (2001).
50. Grunig, G. et al. Requirement for IL-13 independently of IL-4 in experimental asthma. Science 282, 2261-2263 (1998).