Mucociliary Clearance Defects in a Murine In Vitro Model of Pneumococcal Airway Infection

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Fliegauf, Manfred ^a   Sonnen, Andreas F P ^a   Kremer, Bernhard ^a   Henneke, Philipp ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

F ACTIN; PNEUMOLYSIN;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CILIARY BEAT FREQUENCY; CILIARY MOTILITY; CILIATED EPITHELIUM; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOARCHITECTURE; EX VIVO STUDY; EXPERIMENTAL MODEL; EXPLANT; FLOW RATE; FLUID FLOW; IN VITRO STUDY; MOUSE; MUCOCILIARY CLEARANCE; MUTANT; NONHUMAN; PNEUMOCOCCAL INFECTION; PROTEIN LOCALIZATION; RESPIRATORY EPITHELIUM; RESPIRATORY TRACT INFECTION; VIDEO MICROSCOPY; WILD TYPE;

ACTINS; ANIMALS; BACTERIAL PROTEINS; CELL CULTURE TECHNIQUES; CILIA; EPITHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNITY, INNATE; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, VIDEO; MUCOCILIARY CLEARANCE; PNEUMOCOCCAL INFECTIONS; RESPIRATORY TRACT INFECTIONS; STREPTOCOCCUS PNEUMONIAE; STREPTOLYSINS;

EID: 84875085205     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059925     Document Type: Article

References (54)

1. Hippenstiel S, Opitz B, Schmeck B, Suttorp N (2006) Lung epithelium as a sentinel and effector system in pneumonia-molecular mechanisms of pathogen recognition and signal transduction. Respir Res 7: 97. Available: http://respiratory-research.com/content/7/1/97. Accessed 2013 Feb 25.
2. Kadioglu A, Weiser JN, Paton JC, Andrew PW, (2008) The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat Rev Microbiol 6: 288-301.
3. van der Poll T, Opal SM, (2009) Pathogenesis, treatment, and prevention of pneumococcal pneumonia. Lancet 374: 1543-1556.
4. Calbo E, Garau J, (2010) Of mice and men: innate immunity in pneumococcal pneumonia. Int J Antimicrob Agents 35: 107-113.
5. García-Suárez Mdel M, Flórez N, Astudillo A, Vázquez F, Villaverde R et al. (2007) The role of pneumolysin in mediating lung damage in a lethal pneumococcal pneumonia murine model. Respir Res 8: 3. Available: http://respiratory-research.com/content/8/1/3. Accessed 2013 Feb 25.
6. Fahy JV, Dickey BF, (2010) Airway mucus function and dysfunction. N Engl J Med 363: 2233-2247.
7. Knowles MR, Boucher RC, (2002) Mucus clearance as a primary innate defense mechanism for mammalian airways. J Clin Invest 109: 571-577.
8. Smith DJ, Gaffney EA, Blake JR, (2008) Modelling mucociliary clearance. Respir Physiol Neurobiol 163: 178-188.
9. Hammerschmidt S, Paterson GK, Bergmann S, Mitchell TJ (2006) Pathogenesis of Streptococcus pneumoniae infections: adaptive immunity, innate immunity, cell biology, virulence factors. In: Suttorp N, Marre R, editors. Advances in Infectious Diseases: Community acquired Pneumonia. Birkhäuser Verlag, Basel, Schweiz 139-181.
10. Happel KI, Bagby GJ, Nelson S, (2004) Host defense and bacterial pneumonia. Semin Respir Crit Care Med 25: 43-52.
11. Marks LR, Parameswaran GI, Hakansson AP, (2012) Pneumococcal interactions with epithelial cells are crucial for optimal biofilm formation and colonization in vitro and in vivo. Infect Immun 80: 2744-2760.
12. Hornef MW, Normark S, Henriques-Normark B, Rhen M, (2005) Bacterial evasion of innate defense at epithelial linings. Chem Immunol Allergy 86: 72-98.
13. Antunes MB, Woodworth BA, Bhargave G, Xiong G, Aguilar JL, et al. (2007) Murine nasal septa for respiratory epithelial air-liquid interface cultures. Biotechniques 43: 195-196.
14. Woodworth BA, Antunes MB, Bhargave G, Palmer JN, Cohen NA, (2007) Murine tracheal and nasal septal epithelium for air-liquid interface cultures: a comparative study. Am J Rhinol 21: 533-537.
15. Rayner CF, Jackson AD, Rutman A, Dewar A, Mitchell TJ, et al. (1995) Interaction of pneumolysin-sufficient and-deficient isogenic variants of Streptococcus pneumoniae with human respiratory mucosa. Infect Immun 63: 442-447.
16. Iliev AI, Djannatian JR, Nau R, Mitchell TJ, Wouters FS, (2007) Cholesterol-dependent actin remodeling via RhoA and Rac1 activation by the Streptococcus pneumoniae toxin pneumolysin. Proc Natl Acad Sci USA 104: 2897-2902.
17. Hirst RA, Mohammed BJ, Mitchell TJ, Andrew PW, O'Callaghan C, (2004) Streptococcus pneumoniae-induced inhibition of rat ependymal cilia is attenuated by antipneumolysin antibody. Infect Immun 72: 6694-6698.
18. Hirst RA, Kadioglu A, O'callaghan C, Andrew PW, (2004) The role of pneumolysin in pneumococcal pneumonia and meningitis. Clin Exp Immunol 138: 195-201.
19. Hirst RA, Rutman A, Sikand K, Andrew PW, Mitchell TJ, et al. (2000) Effect of pneumolysin on rat brain ciliary function: comparison of brain slices with cultured ependymal cells. Pediatr Res 47: 381-384.
20. Hirst RA, Sikand KS, Rutman A, Mitchell TJ, Andrew PW, et al. (2000) Relative roles of pneumolysin and hydrogen peroxide from Streptococcus pneumoniae in inhibition of ependymal ciliary beat frequency. Infect Immun 68: 1557-1562.
21. Mohammed BJ, Mitchell TJ, Andrew PW, Hirst RA, O'Callaghan C, (1999) The effect of the pneumococcal toxin, pneumolysin on brain ependymal cilia. Microb Pathog 27: 303-309.
22. Feldman C, Cockeran R, Jedrzejas MJ, Mitchell TJ, Anderson R, (2007) Hyaluronidase augments pneumolysin-mediated injury to human ciliated epithelium. Int J Infect Dis 11: 11-15.
23. Bailey KL, Levan TD, Yanov DA, Pavlik JA, Devasure JM et al. (2012) Non-typeable Haemophilus influenzae decreases cilia beating via protein kinase C epsilon. Respir Res 13: 49. Available: http://respiratory-research.com/content/13/1/49. Accessed 2013 Feb 25.
24. Gudis D, Zhao KQ, Cohen NA, (2012) Acquired cilia dysfunction in chronic rhinosinusitis. Am J Rhinol Allergy 26: 1-6.
25. Shen JC, Cope E, Chen B, Leid JG, Cohen NA, (2012) Regulation of murine sinonasal cilia function by microbial secreted factors. Int Forum Allergy Rhinol 2: 104-110.
26. Steinfort C, Wilson R, Mitchell T, Feldman C, Rutman A, et al. (1989) Effect of Streptococcus pneumoniae on human respiratory epithelium in vitro. Infect Immun 57: 2006-2013.
27. Feldman C, Mitchell TJ, Andrew PW, Boulnois GJ, Read RC, et al. (1990) The effect of Streptococcus pneumoniae pneumolysin on human respiratory epithelium in vitro. Microb Pathog 9: 275-284.
28. Hirst RA, Gosai B, Rutman A, Andrew PW, O'Callaghan C, (2003) Streptococcus pneumoniae damages the ciliated ependyma of the brain during meningitis. Infect Immun 71: 6095-6100.
29. Feldman C, Anderson R, Cockeran R, Mitchell T, Cole P, et al. (2002) The effects of pneumolysin and hydrogen peroxide, alone and in combination, on human ciliated epithelium in vitro. Respir Med 96: 580-585.
30. Button B, Cai LH, Ehre C, Kesimer M, Hill DB, et al. (2012) A periciliary brush promotes the lung health by separating the mucus layer from airway epithelia. Science 337: 937-941.
31. O'Callaghan CL, Sikand K, Rutman A, Hirst RA, (2008) The effect of viscous loading on brain ependymal cilia. Neurosci Lett 439: 56-60.
32. Thomas B, Rutman A, O'Callaghan C, (2009) Disrupted ciliated epithelium shows slower ciliary beat frequency and increased dyskinesia. Eur Respir J 34: 401-404.
33. Chilvers MA, O'Callaghan C, (2000) Analysis of ciliary beat pattern and beat frequency using digital high speed imaging: comparison with the photomultiplier and photodiode methods. Thorax 55: 314-317.
34. Chilvers MA, Rutman A, O'Callaghan C, (2003) Ciliary beat pattern is associated with specific ultrastructural defects in primary ciliary dyskinesia. J Allergy Clin Immunol 112: 518-524.
35. Kadioglu A, Brewin H, Härtel T, Brittan JL, Klein M, et al. (2010) Pneumococcal protein PavA is important for nasopharyngeal carriage and development of sepsis. Mol Oral Microbiol 25: 50-60.
36. Briles DE, Hollingshead SK, Paton JC, Ades EW, Novak L, et al. (2003) Immunizations with pneumococcal surface protein A and pneumolysin are protective against pneumonia in a murine model of pulmonary infection with Streptococcus pneumoniae. J Infect Dis 188: 339-348.
37. Benton KA, Everson MP, Briles DE, (1995) A pneumolysin-negative mutant of Streptococcus pneumoniae causes chronic bacteremia rather than acute sepsis in mice. Infect Immun 63: 448-455.
38. Berry AM, Yother J, Briles DE, Hansman D, Paton JC, (1989) Reduced virulence of a defined pneumolysin-negative mutant of Streptococcus pneumoniae. Infect Immun 57: 2037-2042.
39. Sisson JH, Stoner JA, Ammons BA, Wyatt TA, (2003) All-digital image capture and whole-field analysis of ciliary beat frequency. J Microsc 211: 103-111.
40. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671-675.
41. Francis RJ, Chatterjee B, Loges NT, Zentgraf H, Omran H, et al. (2009) Initiation and maturation of cilia-generated flow in newborn and postnatal mouse airway. Am J Physiol Lung Cell Mol Physiol 296: 1067-1075.
42. Werner ME, Hwang P, Huisman F, Taborek P, Yu CC, et al. (2011) Actin and microtubules drive differential aspects of planar cell polarity in multiciliated cells. J Cell Biol 195: 19-26.
43. St Johnston D, Sanson B, (2011) Epithelial polarity and morphogenesis. Curr Opin Cell Biol 23: 540-546.
44. Pan J, You Y, Huang T, Brody SL, (2007) RhoA-mediated apical actin enrichment is required for ciliogenesis and promoted by Foxj1 J Cell Sci. 120: 1868-1876.
45. Van Itallie CM, Fanning AS, Bridges A, Anderson JM, (2009) ZO-1 stabilizes the tight junction solute barrier through coupling to the perijunctional cytoskeleton. Mol Biol Cell 20: 3930-3940.
46. Aktories K, Lang AE, Schwan C, Mannherz HG, (2011) Actin as target for modification by bacterial protein toxins. FEBS J 278: 4526-4543.
47. Clarke TB, Francella N, Huegel A, Weiser JN, (2011) Invasive bacterial pathogens exploit TLR-mediated downregulation of tight junction components to facilitate translocation across the epithelium. Cell Host Microbe 9: 404-414.
48. Jain R, Pan J, Driscoll JA, Wisner JW, Huang T, et al. (2010) Temporal relationship between primary and motile ciliogenesis in airway epithelial cells. Am J Respir Cell Mol Biol 43: 731-739.
49. Wallingford JB, (2010) Planar cell polarity signaling, cilia and polarized ciliary beating. Curr Opin Cell Biol 22: 597-604.
50. Vladar EK, Bayly RD, Sangoram AM, Scott MP, Axelrod JD, (2012) Microtubules Enable the Planar Cell Polarity of Airway Cilia. Curr Biol 22: 2203-2212.
51. Park TJ, Mitchell BJ, Abitua PB, Kintner C, Wallingford JB, (2008) Dishevelled controls apical docking and planar polarization of basal bodies in ciliated epithelial cells. Nat Genet 40: 871-879.
52. Melkamu T, Squillace D, Kita H, O'Grady SM, (2009) Regulation of TLR2 expression and function in human airway epithelial cells. J Membr Biol 229: 101-113.
53. Lin CF, Tsai CH, Cheng CH, Chen YS, Tournier F, et al. (2007) Expression of Toll-like receptors in cultured nasal epithelial cells. Acta Otolaryngol 127: 395-402.
54. von Bernuth H, Picard C, Jin Z, Pankla R, Xiao H, et al. (2008) Pyogenic bacterial infections in humans with MyD88 deficiency. Science 321: 691-696.