Human Neutrophil Elastase Degrades SPLUNC1 and Impairs Airway Epithelial Defense against Bacteria

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Jiang, Di ^a   Wenzel, Sally E ^b   Wu, Qun ^a   Bowler, Russell P ^a   Schnell, Christina ^a   Chu, Hong Wei ^a  

^a DEPARTMENT OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; LEUKOCYTE ELASTASE; RECOMBINANT PROTEIN; SPLUNC1 PROTEIN; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL LOAD; CELL LEVEL; CHRONIC OBSTRUCTIVE LUNG DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE EXACERBATION; EPITHELIUM CELL; FEMALE; HAEMOPHILUS INFECTION; HAEMOPHILUS INFLUENZAE; HOST RESISTANCE; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG PARENCHYMA; MALE; MOUSE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN FUNCTION; RESPIRATORY EPITHELIUM; TISSUE LEVEL;

ANIMALS; CELLS, CULTURED; EPITHELIAL CELLS; GLYCOPROTEINS; HAEMOPHILUS INFECTIONS; HAEMOPHILUS INFLUENZAE; HUMANS; LEUKOCYTE ELASTASE; LUNG; MICE; MICE, KNOCKOUT; NEUTROPHIL INFILTRATION; PHOSPHOPROTEINS; PROTEOLYSIS; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; RECOMBINANT PROTEINS; RESPIRATORY MUCOSA;

BACTERIA (MICROORGANISMS); HAEMOPHILUS INFLUENZAE; MUS;

EID: 84878540443     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064689     Document Type: Article

References (33)

1. Anzueto A, Sethi S, Martinez FJ, (2007) Exacerbations of chronic obstructive pulmonary disease. Proc Am Thorac Soc 4: 554-564.
2. Martinez FJ, Curtis JL, Albert R, (2008) Role of macrolide therapy in chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis 3: 331-350.
3. Murphy TF, Brauer AL, Grant BJ, Sethi S, (2005) Moraxella catarrhalis in chronic obstructive pulmonary disease: burden of disease and immune response. Am J Respir Crit Care Med 172: 195-199.
4. Cockayne DA, Cheng DT, Waschki B, Sridhar S, Ravindran P, et al. (2012) Systemic biomarkers of neutrophilic inflammation, tissue injury and repair in COPD patients with differing levels of disease severity. PLoS One 7: e38629.
5. Bafadhel M, McCormick M, Saha S, McKenna S, Shelley M, et al. (2012) Profiling of sputum inflammatory mediators in asthma and chronic obstructive pulmonary disease. Respiration 83: 36-44.
6. Boschetto P, Quintavalle S, Zeni E, Leprotti S, Potena A, et al. (2006) Association between markers of emphysema and more severe chronic obstructive pulmonary disease. Thorax 61: 1037-1042.
7. Ilumets H, Rytila PH, Sovijarvi AR, Tervahartiala T, Myllarniemi M, et al. (2008) Transient elevation of neutrophil proteinases in induced sputum during COPD exacerbation. Scand J Clin Lab Invest 68: 618-623.
8. Hirche TO, Crouch EC, Espinola M, Brokelman TJ, Mecham RP, et al. (2004) Neutrophil serine proteinases inactivate surfactant protein D by cleaving within a conserved subregion of the carbohydrate recognition domain. J Biol Chem 279: 27688-27698.
9. von Bredow C, Wiesener A, Griese M, (2003) Proteolysis of surfactant protein D by cystic fibrosis relevant proteases. Lung 181: 79-88.
10. Guarnieri F, Spencer JL, Lucey EC, Nugent MA, Stone PJ, (2010) A human surfactant peptide-elastase inhibitor construct as a treatment for emphysema. Proc Natl Acad Sci U S A 107: 10661-10666.
11. Hobbs CA, Blanchard MG, Kellenberger S, Bencharit S, Cao R, et al. (2012) Identification of SPLUNC1's ENaC-inhibitory domain yields novel strategies to treat sodium hyperabsorption in cystic fibrosis airways. FASEB J 26: 4348-4359.
12. Weston WM, LeClair EE, Trzyna W, McHugh KM, Nugent P, et al. (1999) Differential display identification of plunc, a novel gene expressed in embryonic palate, nasal epithelium, and adult lung. J Biol Chem 274: 13698-13703.
13. Campos MA, Abreu AR, Nlend MC, Cobas MA, Conner GE, et al. (2004) Purification and characterization of PLUNC from human tracheobronchial secretions. Am J Respir Cell Mol Biol 30: 184-192.
14. Di YP, Harper R, Zhao Y, Pahlavan N, Finkbeiner W, et al. (2003) Molecular cloning and characterization of spurt, a human novel gene that is retinoic acid-inducible and encodes a secretory protein specific in upper respiratory tracts. J Biol Chem 278: 1165-1173.
15. Bingle CD, Bingle L, (2000) Characterisation of the human plunc gene, a gene product with an upper airways and nasopharyngeal restricted expression pattern. Biochim Biophys Acta 1493: 363-367.
16. LeClair EE, (2003) Four reasons to consider a novel class of innate immune molecules in the oral epithelium. J Dent Res 82: 944-950.
17. Bingle CD, Gorr SU, (2004) Host defense in oral and airway epithelia: chromosome 20 contributes a new protein family. Int J Biochem Cell Biol 36: 2144-2152.
18. Chu HW, Thaikoottathil J, Rino JG, Zhang G, Wu Q, et al. (2007) Function and regulation of SPLUNC1 protein in Mycoplasma infection and allergic inflammation. J Immunol 179: 3995-4002.
19. Gally F, Di YP, Smith SK, Minor MN, Liu Y, et al. (2011) SPLUNC1 promotes lung innate defense against Mycoplasma pneumoniae infection in mice. Am J Pathol 178: 2159-2167.
20. Ghafouri B, Kihlstrom E, Tagesson C, Lindahl M, (2004) PLUNC in human nasal lavage fluid: multiple isoforms that bind to lipopolysaccharide. Biochim Biophys Acta 1699: 57-63.
21. Ghafouri B, Irander K, Lindbom J, Tagesson C, Lindahl M, (2006) Comparative proteomics of nasal fluid in seasonal allergic rhinitis. J Proteome Res 5: 330-338.
22. Steiling K, Kadar AY, Bergerat A, Flanigon J, Sridhar S, et al. (2009) Comparison of proteomic and transcriptomic profiles in the bronchial airway epithelium of current and never smokers. PLoS One 4: e5043.
23. Chu HW, Gally F, Thaikoottathil J, Janssen-Heininger YM, Wu Q, et al. (2010) SPLUNC1 regulation in airway epithelial cells: role of Toll-like receptor 2 signaling. Respir Res 11: 155.
24. Thaikoottathil JV, Martin RJ, Di PY, Minor M, Case S, et al. (2012) SPLUNC1 Deficiency Enhances Airway Eosinophilic Inflammation in Mice. Am J Respir Cell Mol Biol 47: 253-260.
25. Bergsson G, Reeves EP, McNally P, Chotirmall SH, Greene CM, et al. (2009) LL-37 complexation with glycosaminoglycans in cystic fibrosis lungs inhibits antimicrobial activity, which can be restored by hypertonic saline. J Immunol 183: 543-551.
26. Wu Q, Jiang D, Smith S, Thaikoottathil J, Martin RJ, et al. (2012) IL-13 dampens human airway epithelial innate immunity through induction of IL-1 receptor-associated kinase M. J Allergy Clin Immunol 129: 825-833 e822.
27. Lee HY, Andalibi A, Webster P, Moon SK, Teufert K, et al. (2004) Antimicrobial activity of innate immune molecules against Streptococcus pneumoniae, Moraxella catarrhalis and nontypeable Haemophilus influenzae. BMC Infect Dis 4: 12.
28. Ren D, Daines DA (2011) Use of the EpiAirway model for characterizing long-term host-pathogen interactions. J Vis Exp: e3261.
29. Gallelli L, Pelaia G, Fratto D, Muto V, Falcone D, et al. (2010) Effects of budesonide on P38 MAPK activation, apoptosis and IL-8 secretion, induced by TNF-alpha and Haemophilus influenzae in human bronchial epithelial cells. Int J Immunopathol Pharmacol 23: 471-479.
30. Hirche TO, Benabid R, Deslee G, Gangloff S, Achilefu S, et al. (2008) Neutrophil elastase mediates innate host protection against Pseudomonas aeruginosa. J Immunol 181: 4945-4954.
31. Lukinskiene L, Liu Y, Reynolds SD, Steele C, Stripp BR, et al. (2011) Antimicrobial activity of PLUNC protects against Pseudomonas aeruginosa infection. J Immunol 187: 382-390.
32. Peterson MW, Walter ME, Nygaard SD, (1995) Effect of neutrophil mediators on epithelial permeability. Am J Respir Cell Mol Biol 13: 719-727.
33. Zhang W, Case S, Bowler RP, Martin RJ, Jiang D, et al. (2011) Cigarette smoke modulates PGE(2) and host defence against Moraxella catarrhalis infection in human airway epithelial cells. Respirology 16: 508-516.