Pseudomonas aeruginosa Induced Airway Epithelial Injury Drives Fibroblast Activation: A Mechanism in Chronic Lung Allograft Dysfunction

American Journal of Transplantation

Volumn 16, Issue 6, 2016, Pages 1751-1765

  Borthwick, L A ^a   Suwara, M I ^a   Carnell, S C ^a   Green, N J ^a   Mahida, R ^a   Dixon, D ^a   Gillespie, C S ^b   Cartwright, T N ^a   Horabin, J ^a   Walker, A ^a   Olin, E ^a   Rangar, M ^a,c   Gardner, A ^a   Mann, J ^a   Corris, P A ^a,c   Mann, D A ^a   Fisher, A J ^a,c  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c FREEMAN HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALARMIN; HIGH MOBILITY GROUP B1 PROTEIN; INTERLEUKIN 1ALPHA; INTERLEUKIN 8;

ACINETOBACTER BAUMANNII; ADULT; ARTICLE; ASPERGILLUS FUMIGATUS; ASPERGILLUS NIDULANS; BACTERIAL GROWTH; BRONCHIOLITIS OBLITERANS; BURKHOLDERIA CEPACIA COMPLEX; CANDIDA ALBICANS; CELL ACTIVATION; CLINICAL ARTICLE; CONDITIONED MEDIUM; CONTROLLED STUDY; DISEASE COURSE; ENTEROBACTER CLOACAE; EPITHELIUM CELL; ESCHERICHIA COLI; EXOPHIALA; FEMALE; GRAFT RECIPIENT; HAEMOPHILUS INFLUENZAE; HUMAN; HUMAN CELL; INFLAMMATION; KLEBSIELLA PNEUMONIAE; LONGITUDINAL STUDY; LUNG FIBROBLAST; LUNG LAVAGE; LUNG TRANSPLANTATION; MALE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MIDDLE AGED; PHENOTYPE; PRIORITY JOURNAL; PROTEUS MIRABILIS; PSEUDOMONAS AERUGINOSA; RESPIRATORY EPITHELIUM; SERRATIA; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; STENOTROPHOMONAS MALTOPHILIA;

EID: 84978878258     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.13690     Document Type: Article

References (49)

1. Todd JL, Palmer SM. Bronchiolitis obliterans syndrome: The final frontier for lung transplantation. Chest 2011; 140 : 502–508.
2. Sato M. Chronic lung allograft dysfunction after lung transplantation: The moving target. Gen Thorac Cardiovasc Surg 2013; 61 : 67–78.
3. Grossman EJ, Shilling RA. Bronchiolitis obliterans in lung transplantation: The good, the bad, and the future. Transl Res 2009; 153 : 153–165.
4. Weigt SS, DerHovanessian A, Wallace WD, Lynch JP 3rd, Belperio JA. Bronchiolitis obliterans syndrome: The Achilles’ heel of lung transplantation. Semin Respir Crit Care Med 2013; 34 : 336–351.
5. Neuringer IP, Chalermskulrat W, Aris R. Obliterative bronchiolitis or chronic lung allograft rejection: A basic science review. J Heart Lung Transplant 2005; 24 : 3–19.
6. Botha P, Archer L, Anderson RL, et al. Pseudomonas aeruginosa colonization of the allograft after lung transplantation and the risk of bronchiolitis obliterans syndrome. Transplantation 2008; 85 : 771–774.
7. Vos R, Vanaudenaerde BM, Geudens N, Dupont LJ, Van Raemdonck DE, Verleden GM. Pseudomonal airway colonisation: Risk factor for bronchiolitis obliterans syndrome after lung transplantation? Eur Respir J 2008; 31 : 1037–1045.
8. Zeglen S, Wojarski J, Wozniak-Grygiel E, et al. Frequency of Pseudomonas aeruginosa colonizations/infections in lung transplant recipients. Transpl Proc 2009; 41 : 3222–3224.
9. Kurland G, Michelson P. Bronchiolitis obliterans in children. Pediatr Pulmonol 2005; 39 : 193–208.
10. Hayes D Jr, Weiland A, Kirkby S, Galantowicz M, McConnell PI, Tobias JD. Gram-negative infection and bronchiectasis in lung transplant recipients with bronchiolitis obliterans syndrome. Thorac Cardiovasc Surg 2013; 61 : 240–245.
11. Vos R, Vanaudenaerde BM, Verleden SE, Van RD, Dupont LJ, Verleden GM. Azithromycin in posttransplant bronchiolitis obliterans syndrome. Chest 2011; 139 : 1246; author reply 7.
12. Willner DL, Hugenholtz P, Yerkovich ST, et al. Reestablishment of recipient-associated microbiota in the lung allograft is linked to reduced risk of bronchiolitis obliterans syndrome. Am J Respir Crit Care Med 2013; 187 : 640–647.
13. Adams BF, Brazelton T, Berry GJ, Morris RE. The role of respiratory epithelium in a rat model of obliterative airway disease. Transplantation 2000; 69 : 661–664.
14. Gregson AL, Wang X, Weigt SS, et al. Interaction between Pseudomonas and CXC chemokines increases risk of bronchiolitis obliterans syndrome and death in lung transplantation. Am J Respir Crit Care Med 2013; 187 : 518–526.
15. Sato M, Keshavjee S. Bronchiolitis obliterans syndrome: Alloimmune-dependent and -independent injury with aberrant tissue remodeling. Semin Thorac Cardiovasc Surg 2008; 20 : 173–182.
16. Estenne M, Hertz MI. Bronchiolitis obliterans after human lung transplantation. Am J Respir Crit Care Med 2002; 166 : 440–444.
17. Suwara MI, Green NJ, Borthwick LA, et al. IL-1alpha released from damaged epithelial cells is sufficient and essential to trigger inflammatory responses in human lung fibroblasts. Mucosal Immunol 2014; 7 : 684–693.
18. Tolle LB, Standiford TJ. Danger-associated molecular patterns (DAMPs) in acute lung injury. J Pathol 2013; 229 : 145–156.
19. Tracy EC, Bowman MJ, Henderson BW, Baumann H. Interleukin-1alpha is the major alarmin of lung epithelial cells released during photodynamic therapy to induce inflammatory mediators in fibroblasts. Br J Cancer 2012; 107 : 1534–1546.
20. Bianchi ME. DAMPs, PAMPs and alarmins: All we need to know about danger. J Leukoc Biol 2007; 81 : 1–5.
21. Said-Sadier N, Ojcius DM. Alarmins, inflammasomes and immunity. Biomed J 2012; 35 : 437–449.
22. Epler GR. Constrictive bronchiolitis obliterans: The fibrotic airway disorder. Expert Rev Respir Med 2007; 1 : 139–147.
23. Flavell SJ, Hou TZ, Lax S, Filer AD, Salmon M, Buckley CD. Fibroblasts as novel therapeutic targets in chronic inflammation. Br J Pharmacol 2008; 153 Suppl 1: S241–S246.
24. Pauwels NS, Bracke KR, Dupont LL, et al. Role of IL-1alpha and the Nlrp3/caspase-1/IL-1beta axis in cigarette smoke-induced pulmonary inflammation and COPD. Eur Respir J 2011; 38 : 1019–1028.
25. Ogushi F, Tani K, Endo T, et al. Autoantibodies to IL-1 alpha in sera from rapidly progressive idiopathic pulmonary fibrosis. J Med Invest 2001; 48 : 181–189.
26. Belperio JA, DiGiovine B, Keane MP, et al. Interleukin-1 receptor antagonist as a biomarker for bronchiolitis obliterans syndrome in lung transplant recipients. Transplantation 2002; 73 : 591–599.
27. Kaufman AM, Alabre CI, Rubash HE, Shanbhag AS. Human macrophage response to UHMWPE, TiAlV, CoCr, and alumina particles: Analysis of multiple cytokines using protein arrays. J Biomed Mater Res, Part A 2008; 84 : 464–474.
28. Carlsen TG, Kjaersgaard P, Jorgensen TL, et al. Interleukin-1alpha activation and localization in lipopolysaccharide-stimulated human monocytes and macrophages. J Immunol Methods 2015; 422: 59–71.
29. Martin TR, Hagimoto N, Nakamura M, Matute-Bello G. Apoptosis and epithelial injury in the lungs. Proc Am Thorac Soc 2005; 2 : 214–220.
30. Vareille M, Kieninger E, Edwards MR, Regamey N. The airway epithelium: Soldier in the fight against respiratory viruses. Clin Microbiol Rev 2011; 24 : 210–229.
31. Calderon-Garciduenas L, Osnaya N, Rodriguez-Alcaraz A, Villarreal-Calderon A. DNA damage in nasal respiratory epithelium from children exposed to urban pollution. Environ Mol Mutagen 1997; 30 : 11–20.
32. Aoshiba K, Nagai A. Oxidative stress, cell death, and other damage to alveolar epithelial cells induced by cigarette smoke. Tob Induc Dis 2003; 1 : 219–226.
33. Rabinovici R, Neville LF, Abdullah F, et al. Aspiration-induced lung injury: Role of complement. Crit Care Med 1995; 23 : 1405–1411.
34. Kosmider B, Messier EM, Chu HW, Mason RJ. Human alveolar epithelial cell injury induced by cigarette smoke. PLoS One 2011; 6 : e26059.
35. Borthwick LA, Corris PA, Mahida R, et al. TNFalpha from classically activated macrophages accentuates epithelial to mesenchymal transition in obliterative bronchiolitis. Am J Transplant 2013; 13 : 621–633.
36. Meyer KC, Raghu G, Verleden GM, et al. An international ISHLT/ATS/ERS clinical practice guideline: Diagnosis and management of bronchiolitis obliterans syndrome. Eur Respir J 2014; 44 : 1479–1503.
37. Elssner A, Vogelmeier C. The role of neutrophils in the pathogenesis of obliterative bronchiolitis after lung transplantation. Transpl Infect Dis 2001; 3 : 168–176.
38. Ohshimo S, Bonella F, Sommerwerck U, et al. Comparison of serum KL-6 versus bronchoalveolar lavage neutrophilia for the diagnosis of bronchiolitis obliterans in lung transplantation. J Heart Lung Transplant 2011; 30 : 1374–1380.
39. Vos R, Vanaudenaerde BM, Verleden SE, et al. A randomised controlled trial of azithromycin to prevent chronic rejection after lung transplantation. Eur Respir J 2011; 37 : 164–172.
40. Corris PA, Ryan VA, Small T, et al. A randomised controlled trial of azithromycin therapy in bronchiolitis obliterans syndrome (BOS) post lung transplantation. Thorax 2015; 70: 442–450.
41. Saito T, Liu M, Binnie M, et al. Distinct expression patterns of alveolar “alarmins” in subtypes of chronic lung allograft dysfunction. Am J Transplant 2014; 14 : 1425–1432.
42. Smith CR, Jaramillo A, Duffy BF, Mohanakumar T. Airway epithelial cell damage mediated by antigen-specific T cells: Implications in lung allograft rejection. Hum Immunol 2000; 61 : 985–992.
43. Fernandez FG, Jaramillo A, Chen C, et al. Airway epithelium is the primary target of allograft rejection in murine obliterative airway disease. Am J Transplant 2004; 4 : 319–325.
44. Guo L, Wei G, Zhu J, et al. IL-1 family members and STAT activators induce cytokine production by Th2, Th17, and Th1 cells. Proc Natl Acad Sci U S A 2009; 106 : 13463–13468.
45. Botelho FM, Nikota JK, Bauer CM, et al. Cigarette smoke-induced accumulation of lung dendritic cells is interleukin-1alpha-dependent in mice. Respir Res 2012; 13: 81.
46. Chan JK, Roth J, Oppenheim JJ, et al. Alarmins: Awaiting a clinical response. J Clin Invest 2012; 122 : 2711–2719.
47. Rao DA, Pober JS. Endothelial injury, alarmins, and allograft rejection. Crit Rev Immunol 2008; 28 : 229–248.
48. Hirsiger S, Simmen H-P, Werner CML, Wanner GA, Rittirsch D. Danger signals activating the immune response after trauma. Mediators Inflamm 2012; 2012: 315941.
49. Suwara MI, Vanaudenaerde BM, Verleden SE, et al. Mechanistic differences between phenotypes of chronic lung allograft dysfunction after lung transplantation. Transpl Int 2014; 27 : 857–867.