Airway microbiota determines innate cell inflammatory or tissue remodeling profiles in lung transplantation

American Journal of Respiratory and Critical Care Medicine

Volumn 194, Issue 10, 2016, Pages 1252-1263

  Bernasconi, Eric ^a   Pattaroni, Celine ^a   Koutsokera, Angela ^a   Pison, Christophe ^b,c,d   Kessler, Romain ^e   Benden, Christian ^f   Soccal, Paola M ^g   Magnan, Antoine ^h   Aubert, John David ^a   Marsland, Benjamin J ^a   Nicod, Laurent P ^a  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b GRENOBLE UNIVERSITY HOSPITAL   (France)

^c UNIV GRENOBLE ALPES   (France)

^d Inserm1055   (France)

^e HÔPITAL CIVIL   (France)

^f UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^g GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^h NANTES UNIVERSITY HOSPITAL   (France)

Author keywords

Airway remodeling; Macrophages; Microbiome

Indexed keywords

BACTERIAL DNA; RNA 16S;

ADULT; AIRWAY; ARTICLE; CONTROLLED STUDY; DYSBIOSIS; FEMALE; GENE EXPRESSION PROFILING; GRAFT SURVIVAL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN TISSUE; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; LUNG ALVEOLUS MACROPHAGE; LUNG TRANSPLANTATION; MACROPHAGE FUNCTION; MAJOR CLINICAL STUDY; MALE; MICROBIAL COMMUNITY; MICROFLORA; NONHUMAN; PREVOTELLA; PRIORITY JOURNAL; PSEUDOMONAS; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA ANALYSIS; STAPHYLOCOCCUS; STREPTOCOCCUS; AIRWAY REMODELING; BRONCHOALVEOLAR LAVAGE FLUID; INFLAMMATION; MICROBIOLOGY; MIDDLE AGED; PATHOPHYSIOLOGY; PHYSIOLOGY; RESPIRATORY SYSTEM;

ADULT; AIRWAY REMODELING; BRONCHOALVEOLAR LAVAGE FLUID; FEMALE; GRAFT SURVIVAL; HUMANS; INFLAMMATION; LUNG TRANSPLANTATION; MALE; MICROBIOTA; MIDDLE AGED; RESPIRATORY SYSTEM;

EID: 84998813290     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201512-2424OC     Document Type: Article

References (39)

1. Dickson RP, Erb-Downward JR, Huffnagle GB. The role of the bacterial microbiome in lung disease. Expert Rev Respir Med 2013;7: 245-257.
2. Hilty M, Burke C, Pedro H, Cardenas P, Bush A, Bossley C, Davies J, Ervine A, Poulter L, Pachter L, et al. Disordered microbial communities in asthmatic airways. PLoS One 2010;5:e8578.
3. Larsen JM, Musavian HS, Butt TM, Ingvorsen C, Thysen AH, Brix S. Chronic obstructive pulmonary disease and asthma-associated Proteobacteria, but not commensal Prevotella spp., promote Toll-like receptor 2-independent lung inflammation and pathology. Immunology 2015;144:333-342.
4. Marsland BJ, Gollwitzer ES. Host-microorganism interactions in lung diseases. Nat Rev Immunol 2014;14:827-835.
5. Molyneaux PL, Cox MJ, Willis-Owen SA, Mallia P, Russell KE, Russell AM, Murphy E, Johnston SL, Schwartz DA, Wells AU, et al. The role of bacteria in the pathogenesis and progression of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2014;190:906-913.
6. Morris A, Beck JM, Schloss PD, Campbell TB, Crothers K, Curtis JL, Flores SC, Fontenot AP, Ghedin E, Huang L, et al.; Lung HIV Microbiome Project. Comparison of the respiratory microbiome in healthy nonsmokers and smokers. Am J Respir Crit Care Med 2013; 187:1067-1075.
7. Sze MA, Dimitriu PA, Hayashi S, Elliott WM, McDonough JE, Gosselink JV, Cooper J, Sin DD, Mohn WW, Hogg JC. The lung tissue microbiome in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2012;185:1073-1080.
8. Charlson ES, Bittinger K, Chen J, Diamond JM, Li H, Collman RG, Bushman FD. Assessing bacterial populations in the lung by replicate analysis of samples from the upper and lower respiratory tracts. PLoS One 2012;7:e42786.
9. Charlson ES, Bittinger K, Haas AR, Fitzgerald AS, Frank I, Yadav A, Bushman FD, Collman RG. Topographical continuity of bacterial populations in the healthy human respiratory tract. Am J Respir Crit Care Med 2011;184:957-963.
10. Dickson RP, Erb-Downward JR, Huffnagle GB. Towards an ecology of the lung: new conceptual models of pulmonary microbiology and pneumonia pathogenesis. Lancet Respir Med 2014;2:238-246.
11. Bassis CM, Erb-Downward JR, Dickson RP, Freeman CM, Schmidt TM, Young VB, Beck JM, Curtis JL, Huffnagle GB. Analysis of the upper respiratory tract microbiotas as the source of the lung and gastric microbiotas in healthy individuals. MBio 2015;6:e00037.
12. Borewicz K, Pragman AA, Kim HB, Hertz M, Wendt C, Isaacson RE. Longitudinal analysis of the lung microbiome in lung transplantation. FEMS Microbiol Lett 2013;339:57-65.
13. Charlson ES, Diamond JM, Bittinger K, Fitzgerald AS, Yadav A, Haas AR, Bushman FD, Collman RG. Lung-enriched organisms and aberrant bacterial and fungal respiratory microbiota after lung transplant. Am J Respir Crit Care Med 2012;186:536-545.
14. Dickson RP, Erb-Downward JR, Freeman CM, Walker N, Scales BS, Beck JM, Martinez FJ, Curtis JL, Lama VN, Huffnagle GB. Changes in the lung microbiome following lung transplantation include the emergence of two distinct Pseudomonas species with distinct clinical associations. PLoS One 2014;9:e97214.
15. Willner DL, Hugenholtz P, Yerkovich ST, Tan ME, Daly JN, Lachner N, Hopkins PM, Chambers DC. 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.
16. Nakajima T, Palchevsky V, Perkins DL, Belperio JA, Finn PW. Lung transplantation: infection, inflammation, and the microbiome. Semin Immunopathol 2011;33:135-156.
17. Gregson AL, Wang X, Weigt SS, Palchevskiy V, Lynch JP III, Ross DJ, Kubak BM, Saggar R, Fishbein MC, Ardehali A, 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.
18. 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.
19. Bernasconi E, Koutsokera A, Dumas D, Pattaroni C, Camara B, Marsland BJ, Benden C, Pison C, Aubert J-D, Nicod LP. Interactive plasticity of alveolar macrophages and microbiota in lung transplant recipient. Eur Respir J 2014;44:3311.
20. Bernasconi E, Koutsokera A, Pattaroni C, Dumas D, Camara B, Marsland BJ, Benden C, Pison C, Aubert J-D, Nicod LP. Correlative changes in macrophage polarization and pulmonary microbiota in lung transplant recipients. J Heart Lung Transplant 2015;34:S51.
21. Bernasconi E, Koutsokera A, Pattaroni C, Berutto C, Camara B, Marsland BJ, Benden C, Pison C, Aubert J-D, Nicod LP. SysCLAD FP7 Consortium. Alveolar macrophages and pulmonary microbiota are interconnected indicators of lung ecology post-transplantation. Eur Respir J 2015;46:OA3269.
22. Pison C, Magnan A, Botturi K, Seve M, Brouard S, Marsland BJ, Ernst F, Paprotka T, Deplanche K, Fritz A, et al.; SysCLAD consortium. Prediction of chronic lung allograft dysfunction: a systems medicine challenge. Eur RespirJ 2014;43:689-693.
23. Yadava K, Pattaroni C, Sichelstiel AK, Trompette A, Gollwitzer ES, Salami O, von Garnier C, Nicod LP, Marsland BJ. Microbiota promotes chronic pulmonary inflammation by enhancing IL-17A and autoantibodies. Am J Respir Crit Care Med 2016;193:975-987.
24. Bacchetti De Gregoris T, Aldred N, Clare AS, Burgess JG. Improvement of phylum-and class-specific primers for real-time PCR quantification of bacterial taxa. J Microbiol Methods 2011;86: 351-356.
25. Letunic I, Bork P. Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 2011;39: W475-W478.
26. Team RDC. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2008.
27. Legendre P, Gallagher ED. Ecologically meaningful transformations for ordination of species data. Oecologia 2001;129:271-280.
28. Borkham-Kamphorst E, Alexi P, Tihaa L, Haas U, Weiskirchen R. Platelet-derived growth factor-D modulates extracellular matrix homeostasis and remodeling through TIMP-1 induction and attenuation of MMP-2 and MMP-9 gelatinase activities. Biochem Biophys Res Commun 2015;457:307-313.
29. Martinez FO, Gordon S, Locati M, Mantovani A. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J Immunol 2006;177:7303-7311.
30. Murray PJ, Allen JE, Biswas SK, Fisher EA, Gilroy DW, Goerdt S, Gordon S, Hamilton JA, Ivashkiv LB, Lawrence T, et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 2014;41:14-20.
31. Pellicoro A, Ramachandran P, Iredale JP, Fallowfield JA. Liver fibrosis and repair: immune regulation of wound healing in a solid organ. Nat Rev Immunol 2014;14:181-194.
32. Remund KF, Best M, Egan JJ. Infections relevant to lung transplantation. Proc Am Thorac Soc 2009;6:94-100.
33. Erb-Downward JR, Thompson DL, Han MK, Freeman CM, McCloskey L, Schmidt LA, Young VB, Toews GB, Curtis JL, Sundaram B, et al. Analysis of the lung microbiome in the "healthy" smoker and in COPD. PLoS One 2011;6:e16384.
34. Brix S, Eriksen C, Larsen JM, Bisgaard H. Metagenomic heterogeneity explains dual immune effects of endotoxins. J Allergy Clin Immunol 2015;135:277-280.
35. Jin S, Mathis AS, Gioia K, Minko T, Friedman GS, Rosenblatt J, Peng F, Serur DS, Knipp GT. Effect of tacrolimus on the expression of macrophage scavenger and nuclear hormone receptors in THP-1-derived human macrophages. Transplantation 2004;77:1281-1287.
36. Paulus P, Holfeld J, Urbschat A, Mutlak H, Ockelmann PA, Tacke S, Zacharowski K, Reissig C, Stay D, Scheller B. Prednisolone as preservation additive prevents from ischemia reperfusion injury in a rat model of orthotopic lung transplantation. PLoS One 2013;8: e73298.
37. Kilian M, Riley DR, Jensen A, Bruggemann H, Tettelin H. Parallel evolution of Streptococcus pneumoniae and Streptococcus mitis to pathogenic and mutualistic lifestyles. MBio 2014;5:e01490-14.
38. Brandt LJ, Aroniadis OC, Mellow M, Kanatzar A, Kelly C, Park T, Stollman N, Rohlke F, Surawicz C. Long-term follow-up of colonoscopic fecal microbiota transplant for recurrent Clostridium difficile infection. Am J Gastroenterol 2012;107:1079-1087.
39. Stewart S, Fishbein MC, Snell GI, Berry GJ, Boehler A, Burke MM, Glanville A, Gould FK, Magro C, Marboe CC, et al. Revision of the 1996 working formulation for the standardization of nomenclature in the diagnosis of lung rejection. J Heart Lung Transplant 2007;26: 1229-1242.