Cystic fibrosis swine fail to secrete airway surface liquid in response to inhalation of pathogens

Nature Communications

Volumn 8, Issue 1, 2017, Pages

  Luan, Xiaojie ^a   Belev, George ^b   Tam, Julian S ^c   Jagadeeshan, Santosh ^a   Hassan, Noman ^a   Gioino, Paula ^a   Grishchenko, Nikolay ^a   Huang, Yanyun ^d   Carmalt, James L ^e   Duke, Tanya ^e   Jones, Teela ^e   Monson, Bev ^e   Burmester, Monique ^e   Simovich, Tomer ^f   Yilmaz, Orhan ^a   Campanucci, Veronica A ^a   MacHen, Terry E ^g   Chapman, L Dean ^a   Ianowski, Juan P ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b CANADIAN LIGHT SOURCE INC   (Canada)

^c UNIVERSITY OF SASKATCHEWAN   (Canada)

^d Prairie Diagnostic Services   (Canada)

^e UNIVERSITY OF SASKATCHEWAN   (Canada)

^f UNIVERSITY OF MELBOURNE   (Australia)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLAGELLIN; PATTERN RECOGNITION RECEPTOR; TOLL LIKE RECEPTOR; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR;

ABNORMALITY; BACTERIUM; GENETIC ANALYSIS; LABORATORY METHOD; MEMBRANE; MUTATION; PATHOGEN; PIG; RESPIRATORY DISEASE; SECRETION;

AIRWAY; AIRWAY SURFACE LIQUID; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACILLUS SUBTILIS; BACTERIAL CLEARANCE; CONTROLLED STUDY; CYSTIC FIBROSIS; ESCHERICHIA COLI; EX VIVO STUDY; EXPERIMENTAL PIG; HAEMOPHILUS; IMAGING; IN VIVO STUDY; INFECTIOUS AGENT; INHALATION; INNATE IMMUNITY; LUNG FLUID; NONHUMAN; PSEUDOMONAS AERUGINOSA; REFRACTION INDEX; SECRETION (PROCESS); SENSORY NERVE CELL; SURFACE PROPERTY; SYNCHROTRON; X RAY; ANIMAL; DIAGNOSTIC IMAGING; DISEASE MODEL; EXPOSURE; GENETICS; LUNG; MALE; METABOLISM; PIG; RADIOGRAPHY; RESPIRATORY MUCOSA;

SUIDAE;

ANIMALS; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DISEASE MODELS, ANIMAL; INHALATION EXPOSURE; LUNG; MALE; PSEUDOMONAS AERUGINOSA; RADIOGRAPHY; RESPIRATORY MUCOSA; SWINE;

EID: 85030778856     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-00835-7     Document Type: Article

References (42)

1. Stoltz, D. A., Meyerholz, D. K. & Welsh, M. J. Origins of cystic fibrosis lung disease. N. Engl. J. Med. 372, 351-362 (2015).
2. Ostedgaard, L. S. et al. The DeltaF508 mutation causes CFTR misprocessing and cystic fibrosis-like disease in pigs. Sci. Transl. Med. 3, 74ra24 (2011).
3. Stoltz, D. A. et al. Cystic fibrosis pigs develop lung disease and exhibit defective bacterial eradication at birth. Sci. Transl. Med. 2, 29-31 (2010).
4. Pezzulo, A. A. et al. Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung. Nature 487, 109-114 (2012).
5. Sun, X. et al. Disease phenotype of a ferret CFTR-knockout model of cystic fibrosis. J. Clin. Invest. 120, 3149-3160 (2010).
6. Joo, N. S., Cho, H. J., Khansaheb, M. & Wine, J. J. Hyposecretion of fluid from tracheal submucosal glands of CFTR-deficient pigs. J. Clin. Invest. 120, 3161-3166 (2010).
7. Joo, N. S. et al. Absent secretion to vasoactive intestinal peptide in cystic fibrosis airway glands. J. Biol. Chem. 277, 50710-50715 (2002).
8. Ianowski, J. P., Choi, J. Y., Wine, J. J. & Hanrahan, J. W. Mucus secretion by single tracheal submucosal glands from normal and cystic fibrosis transmembrane conductance regulator knockout mice. J. Physiol. 580, 301-314 (2007).
9. Knowles, M. R. & Boucher, R. C. Mucus clearance as a primary innate defense mechanism for mammalian airways. J. Clin. Invest. 109, 571-577 (2002).
10. 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).
11. Roy, M. G. et al. Muc5b is required for airway defence. Nature 505, 412-416 (2014).
12. Wine, J. J. Parasympathetic control of airway submucosal glands: central reflexes and the airway intrinsic nervous system. Auton. Neurosci. 133, 35-54 (2007).
13. Widdicombe, J. H. & Wine, J. J. Airway gland structure and function. Physiol. Rev. 95, 1241-1319 (2015).
14. Ballard, S. T. & Inglis, S. K. Liquid secretion properties of airway submucosal glands. J. Physiol. 556, 1-10 (2004).
15. Baniak, N., Luan, X., Grunow, A., Machen, T. E. & Ianowski, J. P. The cytokines interleukin-1beta and tumor necrosis factor-alpha stimulate CFTR-mediated fluid secretion by swine airway submucosal glands. Am. J. Physiol. Lung Cell Mol. Physiol. 303, L327-L333 (2012).
16. Martens, C. J. et al. Mucous solids and liquid secretion by airways: studies with normal pig, cystic fibrosis human, and non-cystic fibrosis human bronchi. Am. J. Physiol. Lung Cell Mol. Physiol. 301, L236-L246 (2011).
17. Ianowski, J. P., Choi, J. Y., Wine, J. J. & Hanrahan, J. W. Substance P stimulates CFTR-dependent fluid secretion by mouse tracheal submucosal glands. Pflugers Arch. 457, 529-537 (2008).
18. Luan, X. et al. Pseudomonas aeruginosa triggers CFTR-mediated airway surface liquid secretion in swine trachea. Proc. Natl Acad. Sci. USA 111, 12930-12935 (2014).
19. Lewis, R. A. et al. Dynamic imaging of the lungs using X-ray phase contrast. Phys. Med. Biol. 50, 5031-5040 (2005).
20. Kawai, T. & Akira, S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11, 373-384 (2010).
21. Hybiske, K., Ichikawa, J. K., Huang, V., Lory, S. J. & Machen, T. E. Cystic fibrosis airway epithelial cell polarity and bacterial flagellin determine host response to Pseudomonas aeruginosa. Cell Microbiol. 6, 49-63 (2004).
22. Illek, B. et al. Flagellin-stimulated Cl-secretion and innate immune responses in airway epithelia: role for p38. Am. J. Physiol. Lung Cell Mol. Physiol. 295, L531-L542 (2008).
23. Mohamed, F. B. et al. A crucial role of flagellin in the induction of airway mucus production by Pseudomonas aeruginosa. PLoS ONE 7, e39888 (2012).
24. Reiniger, N. et al. Resistance to Pseudomonas aeruginosa chronic lung infection requires cystic fibrosis transmembrane conductance regulator-modulated interleukin-1 (IL-1) release and signaling through the IL-1 receptor. Infect. Immun. 75, 1598-1608 (2007).
25. Bartlett, J. A. et al. Newborn cystic fibrosis pigs have a blunted early response to an inflammatory stimulus. Am. J. Respir. Crit. Care Med. 194, 845-854 (2016).
26. Allen, T. G. & Burnstock, G. A voltage-clamp study of the electrophysiological characteristics of the intramural neurones of the rat trachea. J. Physiol. 423, 593-614 (1990).
27. Ueki, I., German, V. F. & Nadel, J. A. Micropipette measurement of airway submucosal gland secretion autonomic effects. Am. Rev. Respir. Dis. 121, 351-357 (1980).
28. Cho, H. J., Joo, N. S. & Wine, J. J. Defective fluid secretion from submucosal glands of nasal turbinates from CFTR-/-and CFTR (ΔF508/ΔF508) pigs. PLoS ONE 6, e24424 (2011).
29. Stoltz, D. A. et al. Intestinal CFTR expression alleviates meconium ileus in cystic fibrosis pigs. J. Clin. Invest. 123, 2685-2693 (2013).
30. Wysokinski, T. W. et al. Beamlines of the biomedical imaging and therapy facility at the Canadian Light Source-Part 1. Nucl. Instrum. Methods Phys. Res. A 582, 73-76 (2007).
31. Schurch, S., Gehr, P., Im Hof, V., Geiser, M. & Green, F. Surfactant displaces particles toward the epithelium in airways and alveoli. Respir. Physiol. 80, 17-32 (1990).
32. Rapacchietta, A., Neumann, A. & Omenyi, S. Force and free-energy analyses of small particles at fluid interfaces. J. Colloid Interface Sci. 59, 541-554 (1977).
33. Hamed, R. & Fiegel, J. Synthetic tracheal mucus with native rheological and surface tension properties. J. Biomed. Mater. Res. A 102, 1788-1798 (2013).
34. Yuan, Y. & Lee, T. Contact angle and wetting properties. Surf. Sci. Technol. 51, 3-34 (2013).
35. Van Vlierberghe, S., Graulus, G. J., Samal, S. & Dubruel, P. in Biomedical foams for tissue engineering applications (ed. Netti, P. A.) 335-390 (Woodhead, 2014).
36. Tay, B., Kim, J. & Srinivasan, M. In vivo mechanical behavior of intra-abdominal organs. IEEE Trans. Biomed. Eng. 53, 2129-2138 (2006).
37. Cash, H. A., Woods, D. E., McCullough, B., Johanson, W. G. Jr. & Bass, J. A. A rat model of chronic respiratory infection with Pseudomonas aeruginosa. Am. Rev. Respir. Dis. 119, 453-459 (1979).
38. Chmiel, J. F., Konstan, M. W. & Berger, M. Murine models of CF airway infection and inflammation. Methods Mol. Med. 70, 495-515 (2002).
39. Hoffmann, N. et al. Novel mouse model of chronic Pseudomonas aeruginosa lung infection mimicking cystic fibrosis. Infect. Immun. 73, 2504-2514 (2005).
40. Rubenstein, E. et al. Transvenous coronary angiography in humans using synchrotron radiation. Proc. Natl Acad. Sci. USA 83, 9724-9728 (1986).
41. Joo, N. S., Wu, J. V., Krouse, M. E., Saenz, Y. & Wine, J. J. Optical method for quantifying rates of mucus secretion from single submucosal glands. Am. J. Physiol. Lung Cell Mol. Physiol. 281, L458-L468 (2001).
42. Joo, N. S., Saenz, Y., Krouse, M. E. & Wine, J. J. Mucus secretion from single submucosal glands of pig. Stimulation by carbachol and vasoactive intestinal peptide. J. Biol. Chem. 277, 28167-28175 (2002).