Hypoxic epithelial necrosis triggers neutrophilic inflammation via IL-1 receptor signaling in cystic fibrosis lung disease

American Journal of Respiratory and Critical Care Medicine

Volumn 191, Issue 8, 2015, Pages 902-913

  Fritzsching, Benedikt ^a,b   Zhou Suckow, Zhe ^a,b   Trojanek, Joanna B ^a,b   Schubert, Susanne C ^a,b   Schatterny, Jolanthe ^a,b   Hirtz, Stephanie ^a,b   Agrawal, Raman ^a,b   Muley, Thomas ^b,c   Kahn, Nicolas ^b,c   Sticht, Carsten ^a   Gunkel, Nikolas ^d   Welte, Tobias ^e,f   Randell, Scott H ^g   Länger, Florian ^e,f   Schnabel, Philipp ^a,b   Herth, Felix J F ^b,c   Mall, Marcus A ^a,b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b German Center for Lung Research   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^e HANNOVER MEDICAL SCHOOL   (Germany)

^f Biomedical Research in Endstage and Obstructive Lung Disease Hannover (BREATH)   (Germany)

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

Author keywords

Airway epithelium; Airway inflammation; Chronic obstructive pulmonary disease; Cystic fibrosis; Mucus obstruction

Indexed keywords

CHEMOATTRACTANT; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1ALPHA; RECOMBINANT INTERLEUKIN 1 RECEPTOR BLOCKING AGENT;

ADULT; AIRWAY; AIRWAY OBSTRUCTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL INFECTION; BRONCHUS MUCUS; CELL DEATH; CHRONIC OBSTRUCTIVE LUNG DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; CYSTIC FIBROSIS; EMPHYSEMA; GENE DELETION; HUMAN; HUMAN TISSUE; HYPOXIA; KERATINOCYTE; LUNG FIBROSIS; LUNG INJURY; LUNG LAVAGE; LUNG PARENCHYMA; MORTALITY; MOUSE; NEUTROPHIL; NEUTROPHILIA; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTECTION; RESPIRATORY EPITHELIUM; RESPIRATORY TRACT DISEASE; RESPIRATORY TRACT INFLAMMATION; SIGNAL TRANSDUCTION; ADOLESCENT; AGED; ANIMAL; ANOXIA; C57BL MOUSE; DISEASE MODEL; EPITHELIUM; FEMALE; INFLAMMATION; MALE; METABOLISM; MICROARRAY ANALYSIS; MIDDLE AGED; NECROSIS; PATHOLOGY; PHYSIOLOGY; PROCEDURES;

ADOLESCENT; ADULT; AGED; ANIMALS; ANOXIA; CYSTIC FIBROSIS; DISEASE MODELS, ANIMAL; EPITHELIUM; FEMALE; HUMANS; INFLAMMATION; MALE; MICE; MICE, INBRED C57BL; MICROARRAY ANALYSIS; MIDDLE AGED; NECROSIS; NEUTROPHILS; RECEPTORS, INTERLEUKIN-1; SIGNAL TRANSDUCTION;

EID: 84927792201     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201409-1610OC     Document Type: Article

References (53)

1. 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). Lung disease at diagnosis in infants with cystic fibrosis detected by newborn screening. Am J Respir Crit Care Med 2009;180:146-152.
2. Grasemann H, Ratjen F. Early lung disease in cystic fibrosis. Lancet Respir Med 2013;1:148-157.
3. Voynow JA, Fischer BM, Zheng S. Proteases and cystic fibrosis. Int J Biochem Cell Biol 2008;40:1238-1245.
4. Sly PD, Gangell CL, Chen L, Ware RS, Ranganathan S, Mott LS, Murray CP, Stick SM; AREST CF Investigators. Risk factors for bronchiectasis in children with cystic fibrosis. N Engl J Med 2013;368:1963-1970.
5. Sagel SD, Wagner BD, Anthony MM, Emmett P, Zemanick ET. Sputum biomarkers of inflammation and lung function decline in children with cystic fibrosis. Am J Respir Crit Care Med 2012;186:857-865.
6. Le Gars M, Descamps D, Roussel D, Saussereau E, Guillot L, Ruffin M, Tabary O, Hong SS, Boulanger P, Paulais M, et al. 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 2013;187:170-179.
7. Caldwell RA, Boucher RC, Stutts MJ. Neutrophil elastase activates nearsilent epithelial Na1 channels and increases airway epithelial Na1 transport. Am J Physiol Lung Cell Mol Physiol 2005;288:L813-L819.
8. Taggart CC, Greene CM, Carroll TP, O'Neill SJ, McElvaney NG. Elastolytic proteases: inflammation resolution and dysregulation in chronic infective lung disease. Am J Respir Crit Care Med 2005;171: 1070-1076.
9. Gehrig S, Duerr J, Weitnauer M, Wagner CJ, Graeber SY, Schatterny J, Hirtz S, Belaaouaj A, Dalpke AH, Schultz C, et al. Lack of neutrophil elastase reduces inflammation, mucus hypersecretion, and emphysema, but not mucus obstruction, in mice with cystic fibrosislike lung disease. Am J Respir Crit Care Med 2014;189:1082-1092.
10. Voynow JA, Gendler SJ, Rose MC. Regulation of mucin genes in chronic inflammatory airway diseases. Am J Respir Cell Mol Biol 2006;34:661-665.
11. Moghaddam SJ, Clement CG, De la Garza MM, Zou X, Travis EL, Young HW, Evans CM, Tuvim MJ, Dickey BF. Haemophilus influenzae lysate induces aspects of the chronic obstructive pulmonary disease phenotype. Am J Respir Cell Mol Biol 2008;38: 629-638.
12. Chen CJ, Kono H, Golenbock D, Reed G, Akira S, Rock KL. Identification of a key pathway required for the sterile inflammatory response triggered by dying cells. Nat Med 2007;13:851-856.
13. Lukens JR, Gross JM, Kanneganti TD. IL-1 family cytokines trigger sterile inflammatory disease. Front Immunol 2012;3:315.
14. Watters TM, Kenny EF, O'Neill LA. Structure, function and regulation of the Toll/IL-1 receptor adaptor proteins. Immunol Cell Biol 2007;85:411-419.
15. Dinarello CA, Simon A, van der Meer JW. Treating inflammation by blocking interleukin-1 in a broad spectrum of diseases. Nat Rev Drug Discov 2012;11:633-652.
16. Stutts MJ, Knowles MR, Gatzy JT, Boucher RC. Oxygen consumption and ouabain binding sites in cystic fibrosis nasal epithelium. Pediatr Res 1986;20:1316-1320.
17. Worlitzsch D, Tarran R, Ulrich M, Schwab U, Cekici A, Meyer KC, Birrer P, Bellon G, Berger J, Weiss T, et al. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest 2002;109:317-325.
18. + absorption produces cystic fibrosis-like lung disease in mice. Nat Med 2004;10:487-493.
19. Zhou Z, Duerr J, Johannesson B, Schubert SC, Treis D, Harm M, Graeber SY, Dalpke A, Schultz C, Mall MA. The ENaCoverexpressing mouse as a model of cystic fibrosis lung disease. J Cyst Fibros 2011;10:S172-S182.
20. + channel over expressing mice. Am J Respir Crit Care Med 2008;177:730-742.
21. Johannesson B, Hirtz S, Schatterny J, Schultz C, Mall MA. CFTR regulates early pathogenesis of chronic obstructive lung disease in bENaC-overexpressing mice. PLoS One 2012;7:e44059.
22. Zhou Z, Treis D, Schubert SC, Harm M, Schatterny J, Hirtz S, Duerr J, Boucher RC, Mall MA. Preventive but not late amiloride therapy reduces morbidity and mortality of lung disease in betaENa Coverexpressing mice. Am J Respir Crit Care Med 2008;178: 1245-1256.
23. Zhou-Suckow ZFB, Schatterny J, Hirtz S, Mall MA. Hypoxic epithelial necrosis, IL-1 receptor, siganling and neutrophilic airway inflammation in bENaC-overexpressing mice [abstract]. Pediatr Pulmonol 2013;48:A181.
24. Vestbo J, Hurd SS, Agustí AG, Jones PW, Vogelmeier C, Anzueto A, Barnes PJ, Fabbri LM, Martinez FJ, Nishimura M, et al. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary. Am J Respir Crit Care Med 2013;187:347-365.
25. Glaccum MB, Stocking KL, Charrier K, Smith JL, Willis CR, Maliszewski C, Livingston DJ, Peschon JJ, Morrissey PJ. Phenotypic and functional characterization of mice that lack the type I receptor for IL-1. J Immunol 1997;159:3364-3371.
26. Saetta M, Shiner RJ, Angus GE, Kim WD, Wang NS, King M, Ghezzo H, Cosio MG. Destructive index: a measurement of lung parenchymal destruction in smokers. Am Rev Respir Dis 1985;131:764-769.
27. Trojanek JB, Cobos-Correa A, Diemer S, Kormann M, Schubert SC, Zhou-Suckow Z, Agrawal R, Duerr J, Wagner CJ, Schatterny J, et al. Airway mucus obstruction triggers macrophage activation and matrix metalloproteinase 12-dependent emphysema. Am J Respir Cell Mol Biol 2014;51:709-720.
28. Botelho FM, Bauer CM, Finch D, Nikota JK, Zavitz CC, Kelly A, Lambert KN, Piper S, Foster ML, Goldring JJ, et al. IL-1α/IL-1R1 expression in chronic obstructive pulmonary disease and mechanistic relevance to smoke-induced neutrophilia in mice. PLoS One 2011;6:e28457.
29. Kloosterman WP, Wienholds E, de Bruijn E, Kauppinen S, Plasterk RH. In situ detection of miRNAs in animal embryos using LNA-modified oligonucleotide probes. Nat Methods 2006;3:27-29.
30. Wielpütz MO, Eichinger M, Zhou Z, Leotta K, Hirtz S, Bartling SH, Semmler W, Kauczor HU, Puderbach M, Mall MA. In vivo monitoring of cystic fibrosis-like lung disease in mice by volumetric computed tomography. Eur Respir J 2011;38:1060-1070.
31. Hoenderdos K, Condliffe A. The neutrophil in chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol 2013; 48:531-539.
32. Muhlebach MS, Noah TL. Endotoxin activity and inflammatory markers in the airways of young patients with cystic fibrosis. Am J Respir Crit Care Med 2002;165:911-915.
33. Berger M. Lung inflammation early in cystic fibrosis: bugs are indicted, but the defense is guilty. Am J Respir Crit Care Med 2002;165: 857-858.
34. Livraghi-Butrico A, Kelly EJ, Klem ER, Dang H, Wolfgang MC, Boucher RC, Randell SH, O'Neal WK. Mucus clearance, MyD88-dependent and MyD88-independent immunity modulate lung susceptibility to spontaneous bacterial infection and inflammation. Mucosal Immunol 2012;5:397-408.
35. Fujisawa T, Chang MM, Velichko S, Thai P, Hung LY, Huang F, Phuong N, Chen Y, Wu R. NF-κB mediates IL-1β- and IL-17A-induced MUC5B expression in airway epithelial cells. Am J Respir Cell Mol Biol 2011;45:246-252.
36. Chen Y, Garvin LM, Nickola TJ, Watson AM, Colberg-Poley AM, Rose MC. IL-1β induction of MUC5AC gene expression is mediated by CREB and NF-κB and repressed by dexamethasone. Am J Physiol Lung Cell Mol Physiol 2014;306:L797-L807.
37. Jono H, Xu H, Kai H, Lim DJ, Kim YS, Feng XH, Li JD. Transforming growth factor-beta-Smad signaling pathway negatively regulates nontypeable Haemophilus influenzae-induced MUC5AC mucin transcription via mitogen-activated protein kinase (MAPK) phosphatase-1-dependent inhibition of p38 MAPK. J Biol Chem 2003;278:27811-27819.
38. Tunney MM, Field TR, Moriarty TF, Patrick S, Doering G, Muhlebach MS, Wolfgang MC, Boucher R, Gilpin DF, McDowell A, et al. Detection of anaerobic bacteria in high numbers in sputum from patients with cystic fibrosis. Am J Respir Crit Care Med 2008;177: 995-1001.
39. Majno G, Joris I. Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 1995;146:3-15.
40. Mall MA, Hartl D. CFTR: cystic fibrosis and beyond. Eur Respir J 2014; 44:1042-1054.
41. Cantin AM, Hanrahan JW, Bilodeau G, Ellis L, Dupuis A, Liao J, Zielenski J, Durie P. Cystic fibrosis transmembrane conductance regulator function is suppressed in cigarette smokers. Am J Respir Crit Care Med 2006;173:1139-1144.
42. Clunes LA, Davies CM, Coakley RD, Aleksandrov AA, Henderson AG, Zeman KL, Worthington EN, Gentzsch M, Kreda SM, Cholon D, et al. Cigarette smoke exposure induces CFTR internalization and insolubility, leading to airway surface liquid dehydration. FASEB J 2012;26:533-545.
43. Dransfield MT, Wilhelm AM, Flanagan B, Courville C, Tidwell SL, Raju SV, Gaggar A, Steele C, Tang LP, Liu B, et al. Acquired cystic fibrosis transmembrane conductance regulator dysfunction in the lower airways in COPD. Chest 2013;144:498-506.
44. Hogg JC, Chu F, Utokaparch S, Woods R, Elliott WM, Buzatu L, Cherniack RM, Rogers RM, Sciurba FC, Coxson HO, et al. The nature of small-airway obstruction in chronic obstructive pulmonary disease. N Engl J Med 2004;350:2645-2653.
45. Fehrenbach H, Voswinckel R, Michl V, Mehling T, Fehrenbach A, Seeger W, Nyengaard JR. Neoalveolarisation contributes to compensatory lung growth following pneumonectomy in mice. Eur Respir J 2008;31:515-522.
46. Hoffman AM, Shifren A, Mazan MR, Gruntman AM, Lascola KM, Nolen-Walston RD, Kim CF, Tsai L, Pierce RA, Mecham RP, et al. Matrix modulation of compensatory lung regrowth and progenitor cell proliferation in mice. Am J Physiol Lung Cell Mol Physiol 2010;298: L158-L168.
47. Döring G, Bragonzi A, Paroni M, Aktürk FF, Cigana C, Schmidt A, Gilpin D, Heyder S, Born T, Smaczny C, et al. BIIL 284 reduces neutrophil numbers but increases P. aeruginosa bacteremia and inflammation in mouse lungs. J Cyst Fibros 2014;13:156-163.
48. Stoltz DA, Meyerholz DK, Pezzulo AA, Ramachandran S, Rogan MP, Davis GJ, Hanfland RA, Wohlford-Lenane C, Dohrn CL, Bartlett JA, et al. Cystic fibrosis pigs develop lung disease and exhibit defective bacterial eradication at birth. Sci Transl Med 2010;2:29ra31.
49. Sun X, Olivier AK, Liang B, Yi Y, Sui H, Evans TI, Zhang Y, Zhou W, Tyler SR, Fisher JT, et al. Lung phenotype of juvenile and adult cystic fibrosis transmembrane conductance regulator-knockout ferrets. Am J Respir Cell Mol Biol 2014;50:502-512.
50. Hoegger MJ, Fischer AJ, McMenimen JD, Ostedgaard LS, Tucker AJ, Awadalla MA, Moninger TO, Michalski AS, Hoffman EA, Zabner J, et al. Cystic fibrosis. Impaired mucus detachment disrupts mucociliary transport in a piglet model of cystic fibrosis. Science 2014;345:818-822.
51. Pezzulo AA, Tang XX, Hoegger MJ, Alaiwa MH, Ramachandran S, Moninger TO, Karp PH, Wohlford-Lenane CL, Haagsman HP, van Eijk M, et al. Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung. Nature 2012;487:109-113.
52. Keiser NW, Birket SE, Evans IA, Tyler SR, Crooke AK, Sun X, Zhou W, Nellis JR, Stroebele EK, Chu KK, et al. Defective innate immunity and hyper-inflammation in newborn CFTR-knockout ferret lungs. Am J Respir Cell Mol Biol (In press)
53. Zuelzer WW, Newton WA Jr. The pathogenesis of fibrocystic disease of the pancreas; a study of 36 cases with special reference to the pulmonary lesions. Pediatrics 1949;4:53-69.