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Published in: Respiratory Research 1/2020

01-12-2020 | Respiratory Microbiota | Research

Differences in airway microbiome and metabolome of single lung transplant recipients

Authors: Nirmal S. Sharma, Grant Vestal, Keith Wille, Kapil N. Patel, Feng Cheng, Srinivas Tipparaju, Sultan Tousif, Mudassir M. Banday, Xin Xu, Landon Wilson, Viswam S. Nair, Casey Morrow, Don Hayes Jr, Andreas Seyfang, Stephen Barnes, Jessy S. Deshane, Amit Gaggar

Published in: Respiratory Research | Issue 1/2020

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Abstract

Background

Recent studies suggest that alterations in lung microbiome are associated with occurrence of chronic lung diseases and transplant rejection. To investigate the host-microbiome interactions, we characterized the airway microbiome and metabolome of the allograft (transplanted lung) and native lung of single lung transplant recipients.

Methods

BAL was collected from the allograft and native lungs of SLTs and healthy controls. 16S rRNA microbiome analysis was performed on BAL bacterial pellets and supernatant used for metabolome, cytokines and acetylated proline-glycine-proline (Ac-PGP) measurement by liquid chromatography-high-resolution mass spectrometry.

Results

In our cohort, the allograft airway microbiome was distinct with a significantly higher bacterial burden and relative abundance of genera Acinetobacter & Pseudomonas. Likewise, the expression of the pro-inflammatory cytokine VEGF and the neutrophil chemoattractant matrikine Ac-PGP in the allograft was significantly higher. Airway metabolome distinguished the native lung from the allografts and an increased concentration of sphingosine-like metabolites that negatively correlated with abundance of bacteria from phyla Proteobacteria.

Conclusions

Allograft lungs have a distinct microbiome signature, a higher bacterial biomass and an increased Ac-PGP compared to the native lungs in SLTs compared to the native lungs in SLTs. Airway metabolome distinguishes the allografts from native lungs and is associated with distinct microbial communities, suggesting a functional relationship between the local microbiome and metabolome.
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Literature
1.
go back to reference Annual Data Report of the US Organ Procurement and Transplantation Network. Preface. Am J Transplant. 2014;14(Suppl 1):5–7. Annual Data Report of the US Organ Procurement and Transplantation Network. Preface. Am J Transplant. 2014;14(Suppl 1):5–7.
2.
go back to reference Burton CM, Carlsen J, Mortensen J, Andersen CB, Milman N, Iversen M. Long-term survival after lung transplantation depends on development and severity of bronchiolitis obliterans syndrome. J Heart Lung Transplant. 2007;26(7):681–6.PubMedCrossRef Burton CM, Carlsen J, Mortensen J, Andersen CB, Milman N, Iversen M. Long-term survival after lung transplantation depends on development and severity of bronchiolitis obliterans syndrome. J Heart Lung Transplant. 2007;26(7):681–6.PubMedCrossRef
3.
go back to reference Huang YJ, Erb-Downward JR, Dickson RP, Curtis JL, Huffnagle GB, Han MK. Understanding the role of the microbiome in chronic obstructive pulmonary disease: principles, challenges, and future directions. Transl Res. 2017;179:71–83.PubMedCrossRef Huang YJ, Erb-Downward JR, Dickson RP, Curtis JL, Huffnagle GB, Han MK. Understanding the role of the microbiome in chronic obstructive pulmonary disease: principles, challenges, and future directions. Transl Res. 2017;179:71–83.PubMedCrossRef
4.
go back to reference O'Dwyer DN, Ashley SL, Gurczynski SJ, Xia M, Wilke C, Falkowski NR, et al. Lung microbiota contribute to pulmonary inflammation and disease progression in pulmonary fibrosis. Am J Respir Crit Care Med. 2019;199(9):1127–38.PubMedPubMedCentralCrossRef O'Dwyer DN, Ashley SL, Gurczynski SJ, Xia M, Wilke C, Falkowski NR, et al. Lung microbiota contribute to pulmonary inflammation and disease progression in pulmonary fibrosis. Am J Respir Crit Care Med. 2019;199(9):1127–38.PubMedPubMedCentralCrossRef
5.
go back to reference Bernasconi E, Pattaroni C, Koutsokera A, Pison C, Kessler R, Benden C, et al. Airway microbiota determines innate cell inflammatory or tissue remodeling profiles in lung transplantation. Am J Respir Crit Care Med. 2016;194(10):1252–63.PubMedCrossRef Bernasconi E, Pattaroni C, Koutsokera A, Pison C, Kessler R, Benden C, et al. Airway microbiota determines innate cell inflammatory or tissue remodeling profiles in lung transplantation. Am J Respir Crit Care Med. 2016;194(10):1252–63.PubMedCrossRef
6.
go back to reference Charlson ES, Diamond JM, Bittinger K, Fitzgerald AS, Yadav A, Haas AR, et al. Lung-enriched organisms and aberrant bacterial and fungal respiratory microbiota after lung transplant. Am J Respir Crit Care Med. 2012;186(6):536–45.PubMedPubMedCentralCrossRef Charlson ES, Diamond JM, Bittinger K, Fitzgerald AS, Yadav A, Haas AR, et al. Lung-enriched organisms and aberrant bacterial and fungal respiratory microbiota after lung transplant. Am J Respir Crit Care Med. 2012;186(6):536–45.PubMedPubMedCentralCrossRef
7.
go back to reference Litvak Y, Byndloss MX, Tsolis RM, Baumler AJ. Dysbiotic Proteobacteria expansion: a microbial signature of epithelial dysfunction. Curr Opin Microbiol. 2017;39:1–6.PubMedCrossRef Litvak Y, Byndloss MX, Tsolis RM, Baumler AJ. Dysbiotic Proteobacteria expansion: a microbial signature of epithelial dysfunction. Curr Opin Microbiol. 2017;39:1–6.PubMedCrossRef
8.
go back to reference Sharma NS, Wille KM, Athira S, Zhi D, Hough KP, Diaz-Guzman E, et al. Distal airway microbiome is associated with immunoregulatory myeloid cell responses in lung transplant recipients. J Heart Lung Transplant. 2017;S1053-2498(17):31898–3. Sharma NS, Wille KM, Athira S, Zhi D, Hough KP, Diaz-Guzman E, et al. Distal airway microbiome is associated with immunoregulatory myeloid cell responses in lung transplant recipients. J Heart Lung Transplant. 2017;S1053-2498(17):31898–3.
9.
go back to reference Ceccarani C, Foschi C, Parolin C, D'Antuono A, Gaspari V, Consolandi C, et al. Diversity of vaginal microbiome and metabolome during genital infections. Sci Rep. 2019;9(1):14095.PubMedPubMedCentralCrossRef Ceccarani C, Foschi C, Parolin C, D'Antuono A, Gaspari V, Consolandi C, et al. Diversity of vaginal microbiome and metabolome during genital infections. Sci Rep. 2019;9(1):14095.PubMedPubMedCentralCrossRef
10.
go back to reference Ding S, Ma Y, Liu G, Yan W, Jiang H, Fang J. Lactobacillus brevis alleviates DSS-induced colitis by reprograming intestinal microbiota and influencing serum Metabolome in murine model. Front Physiol. 2019;10:1152.PubMedPubMedCentralCrossRef Ding S, Ma Y, Liu G, Yan W, Jiang H, Fang J. Lactobacillus brevis alleviates DSS-induced colitis by reprograming intestinal microbiota and influencing serum Metabolome in murine model. Front Physiol. 2019;10:1152.PubMedPubMedCentralCrossRef
11.
go back to reference Schoeman JC, Harms AC, van Weeghel M, Berger R, Vreeken RJ, Hankemeier T. Development and application of a UHPLC-MS/MS metabolomics based comprehensive systemic and tissue-specific screening method for inflammatory, oxidative and nitrosative stress. Anal Bioanal Chem. 2018;410(10):2551–68.PubMedPubMedCentralCrossRef Schoeman JC, Harms AC, van Weeghel M, Berger R, Vreeken RJ, Hankemeier T. Development and application of a UHPLC-MS/MS metabolomics based comprehensive systemic and tissue-specific screening method for inflammatory, oxidative and nitrosative stress. Anal Bioanal Chem. 2018;410(10):2551–68.PubMedPubMedCentralCrossRef
12.
13.
go back to reference Slupsky CM, Cheypesh A, Chao DV, Fu H, Rankin KN, Marrie TJ, et al. Streptococcus pneumoniae and Staphylococcus aureus pneumonia induce distinct metabolic responses. J Proteome Res. 2009;8(6):3029–36.PubMedCrossRef Slupsky CM, Cheypesh A, Chao DV, Fu H, Rankin KN, Marrie TJ, et al. Streptococcus pneumoniae and Staphylococcus aureus pneumonia induce distinct metabolic responses. J Proteome Res. 2009;8(6):3029–36.PubMedCrossRef
14.
go back to reference Cribbs SK, Park Y, Guidot DM, Martin GS, Brown LA, Lennox J, et al. Metabolomics of bronchoalveolar lavage differentiate healthy HIV-1-infected subjects from controls. AIDS Res Hum Retrovir. 2014;30(6):579–85.PubMedCrossRefPubMedCentral Cribbs SK, Park Y, Guidot DM, Martin GS, Brown LA, Lennox J, et al. Metabolomics of bronchoalveolar lavage differentiate healthy HIV-1-infected subjects from controls. AIDS Res Hum Retrovir. 2014;30(6):579–85.PubMedCrossRefPubMedCentral
15.
go back to reference Ciaramelli C, Fumagalli M, Viglio S, Bardoni AM, Piloni D, Meloni F, et al. (1) H NMR to evaluate the Metabolome of Bronchoalveolar lavage fluid (BALf) in bronchiolitis Obliterans syndrome (BOS): toward the development of a new approach for biomarker identification. J Proteome Res. 2017;16(4):1669–82.PubMedCrossRef Ciaramelli C, Fumagalli M, Viglio S, Bardoni AM, Piloni D, Meloni F, et al. (1) H NMR to evaluate the Metabolome of Bronchoalveolar lavage fluid (BALf) in bronchiolitis Obliterans syndrome (BOS): toward the development of a new approach for biomarker identification. J Proteome Res. 2017;16(4):1669–82.PubMedCrossRef
16.
go back to reference Shaffer M, Armstrong AJS, Phelan VV, Reisdorph N, Lozupone CA. Microbiome and metabolome data integration provides insight into health and disease. Transl Res. 2017;189:51–64.PubMedPubMedCentralCrossRef Shaffer M, Armstrong AJS, Phelan VV, Reisdorph N, Lozupone CA. Microbiome and metabolome data integration provides insight into health and disease. Transl Res. 2017;189:51–64.PubMedPubMedCentralCrossRef
17.
go back to reference Evans CM, Fingerlin TE, Schwarz MI, Lynch D, Kurche J, Warg L, et al. Idiopathic pulmonary fibrosis: a genetic disease that involves Mucociliary dysfunction of the peripheral airways. Physiol Rev. 2016;96(4):1567–91.PubMedPubMedCentralCrossRef Evans CM, Fingerlin TE, Schwarz MI, Lynch D, Kurche J, Warg L, et al. Idiopathic pulmonary fibrosis: a genetic disease that involves Mucociliary dysfunction of the peripheral airways. Physiol Rev. 2016;96(4):1567–91.PubMedPubMedCentralCrossRef
18.
go back to reference Dransfield MT, Wilhelm AM, Flanagan B, Courville C, Tidwell SL, Raju SV, et al. Acquired cystic fibrosis transmembrane conductance regulator dysfunction in the lower airways in COPD. Chest. 2013;144(2):498–506.PubMedPubMedCentralCrossRef Dransfield MT, Wilhelm AM, Flanagan B, Courville C, Tidwell SL, Raju SV, et al. Acquired cystic fibrosis transmembrane conductance regulator dysfunction in the lower airways in COPD. Chest. 2013;144(2):498–506.PubMedPubMedCentralCrossRef
19.
go back to reference Westney GE, Kesten S, De Hoyos A, Chapparro C, Winton T, Maurer JR. Aspergillus infection in single and double lung transplant recipients. Transplantation. 1996;61(6):915–9.PubMedCrossRef Westney GE, Kesten S, De Hoyos A, Chapparro C, Winton T, Maurer JR. Aspergillus infection in single and double lung transplant recipients. Transplantation. 1996;61(6):915–9.PubMedCrossRef
20.
go back to reference Frost AE, Keller CA, Noon GP, Short HD, Cagle PT. Outcome of the native lung after single lung transplant. Multiorgan Transplant Group. Chest. 1995;107(4):981–4.PubMedCrossRef Frost AE, Keller CA, Noon GP, Short HD, Cagle PT. Outcome of the native lung after single lung transplant. Multiorgan Transplant Group. Chest. 1995;107(4):981–4.PubMedCrossRef
21.
go back to reference Dickson RP, Erb-Downward JR, Freeman CM, Walker N, Scales BS, Beck JM, et al. Changes in the lung microbiome following lung transplantation include the emergence of two distinct Pseudomonas species with distinct clinical associations. PLoS One. 2014;9(5):e97214.PubMedPubMedCentralCrossRef Dickson RP, Erb-Downward JR, Freeman CM, Walker N, Scales BS, Beck JM, et al. Changes in the lung microbiome following lung transplantation include the emergence of two distinct Pseudomonas species with distinct clinical associations. PLoS One. 2014;9(5):e97214.PubMedPubMedCentralCrossRef
22.
go back to reference Simon TD, Van Yserloo B, Nelson K, Gillespie D, Jensen R, McAllister JP 2nd, et al. Use of quantitative 16S rRNA PCR to determine bacterial load does not augment conventional cerebrospinal fluid (CSF) cultures among children undergoing treatment for CSF shunt infection. Diagn Microbiol Infect Dis. 2014;78(2):188–95.PubMedCrossRef Simon TD, Van Yserloo B, Nelson K, Gillespie D, Jensen R, McAllister JP 2nd, et al. Use of quantitative 16S rRNA PCR to determine bacterial load does not augment conventional cerebrospinal fluid (CSF) cultures among children undergoing treatment for CSF shunt infection. Diagn Microbiol Infect Dis. 2014;78(2):188–95.PubMedCrossRef
23.
go back to reference Grice EA, Kong HH, Renaud G, Young AC, Program NCS, Bouffard GG, et al. A diversity profile of the human skin microbiota. Genome Res. 2008;18(7):1043–50.PubMedPubMedCentralCrossRef Grice EA, Kong HH, Renaud G, Young AC, Program NCS, Bouffard GG, et al. A diversity profile of the human skin microbiota. Genome Res. 2008;18(7):1043–50.PubMedPubMedCentralCrossRef
24.
go back to reference Forsberg EM, Huan T, Rinehart D, Benton HP, Warth B, Hilmers B, et al. Data processing, multi-omic pathway mapping, and metabolite activity analysis using XCMS online. Nat Protoc. 2018;13(4):633–51.PubMedPubMedCentralCrossRef Forsberg EM, Huan T, Rinehart D, Benton HP, Warth B, Hilmers B, et al. Data processing, multi-omic pathway mapping, and metabolite activity analysis using XCMS online. Nat Protoc. 2018;13(4):633–51.PubMedPubMedCentralCrossRef
25.
go back to reference Chong J, Soufan O, Li C, Caraus I, Li S, Bourque G, et al. MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis. Nucleic Acids Res. 2018;46(W1):W486–W94.PubMedPubMedCentralCrossRef Chong J, Soufan O, Li C, Caraus I, Li S, Bourque G, et al. MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis. Nucleic Acids Res. 2018;46(W1):W486–W94.PubMedPubMedCentralCrossRef
26.
go back to reference Guijas C, Montenegro-Burke JR, Domingo-Almenara X, Palermo A, Warth B, Hermann G, et al. METLIN: a technology platform for identifying Knowns and unknowns. Anal Chem. 2018;90(5):3156–64.PubMedPubMedCentralCrossRef Guijas C, Montenegro-Burke JR, Domingo-Almenara X, Palermo A, Warth B, Hermann G, et al. METLIN: a technology platform for identifying Knowns and unknowns. Anal Chem. 2018;90(5):3156–64.PubMedPubMedCentralCrossRef
27.
go back to reference Li S, Park Y, Duraisingham S, Strobel FH, Khan N, Soltow QA, et al. Predicting network activity from high throughput metabolomics. PLoS Comput Biol. 2013;9(7):e1003123.PubMedPubMedCentralCrossRef Li S, Park Y, Duraisingham S, Strobel FH, Khan N, Soltow QA, et al. Predicting network activity from high throughput metabolomics. PLoS Comput Biol. 2013;9(7):e1003123.PubMedPubMedCentralCrossRef
28.
go back to reference Uppal K, Ma C, Go YM, Jones DP, Wren J. xMWAS: a data-driven integration and differential network analysis tool. Bioinformatics. 2018;34(4):701–2.PubMedCrossRef Uppal K, Ma C, Go YM, Jones DP, Wren J. xMWAS: a data-driven integration and differential network analysis tool. Bioinformatics. 2018;34(4):701–2.PubMedCrossRef
29.
go back to reference Kim BR, Shin J, Guevarra R, Lee JH, Kim DW, Seol KH, et al. Deciphering diversity indices for a better understanding of microbial communities. J Microbiol Biotechnol. 2017;27(12):2089–93.PubMedCrossRef Kim BR, Shin J, Guevarra R, Lee JH, Kim DW, Seol KH, et al. Deciphering diversity indices for a better understanding of microbial communities. J Microbiol Biotechnol. 2017;27(12):2089–93.PubMedCrossRef
31.
go back to reference O'Dwyer DN, Zhou X, Wilke CA, Xia M, Falkowski NR, Norman KC, et al. Lung Dysbiosis, Inflammation, and Injury in Hematopoietic Cell Transplantation. Am J Respir Crit Care Med. 2018;198(10):1312–21.PubMedPubMedCentralCrossRef O'Dwyer DN, Zhou X, Wilke CA, Xia M, Falkowski NR, Norman KC, et al. Lung Dysbiosis, Inflammation, and Injury in Hematopoietic Cell Transplantation. Am J Respir Crit Care Med. 2018;198(10):1312–21.PubMedPubMedCentralCrossRef
32.
go back to reference Dopkins N, Nagarkatti PS, Nagarkatti M. The role of gut microbiome and associated metabolome in the regulation of neuroinflammation in multiple sclerosis and its implications in attenuating chronic inflammation in other inflammatory and autoimmune disorders. Immunology. 2018;154(2):178–85.PubMedPubMedCentralCrossRef Dopkins N, Nagarkatti PS, Nagarkatti M. The role of gut microbiome and associated metabolome in the regulation of neuroinflammation in multiple sclerosis and its implications in attenuating chronic inflammation in other inflammatory and autoimmune disorders. Immunology. 2018;154(2):178–85.PubMedPubMedCentralCrossRef
33.
go back to reference Charlson ES, Bittinger K, Haas AR, Fitzgerald AS, Frank I, Yadav A, et al. Topographical continuity of bacterial populations in the healthy human respiratory tract. Am J Respir Crit Care Med. 2011;184(8):957–63.PubMedPubMedCentralCrossRef Charlson ES, Bittinger K, Haas AR, Fitzgerald AS, Frank I, Yadav A, et al. Topographical continuity of bacterial populations in the healthy human respiratory tract. Am J Respir Crit Care Med. 2011;184(8):957–63.PubMedPubMedCentralCrossRef
34.
go back to reference Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444(7122):1022–3.CrossRefPubMed Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444(7122):1022–3.CrossRefPubMed
35.
go back to reference Sharma NS, Lal CV, Li JD, Lou XY, Viera L, Abdallah T, et al. The neutrophil Chemoattractant peptide Proline-glycine-Proline is associated with acute respiratory distress syndrome (ARDS). Am J Physiol Lung Cell Mol Physiol. 2018;315(5):L653–61.PubMedPubMedCentralCrossRef Sharma NS, Lal CV, Li JD, Lou XY, Viera L, Abdallah T, et al. The neutrophil Chemoattractant peptide Proline-glycine-Proline is associated with acute respiratory distress syndrome (ARDS). Am J Physiol Lung Cell Mol Physiol. 2018;315(5):L653–61.PubMedPubMedCentralCrossRef
36.
go back to reference Hahn CS, Scott DW, Xu X, Roda MA, Payne GA, Wells JM, et al. The matrikine N-alpha-PGP couples extracellular matrix fragmentation to endothelial permeability. Sci Adv. 2015;1(3):e1500175.PubMedPubMedCentralCrossRef Hahn CS, Scott DW, Xu X, Roda MA, Payne GA, Wells JM, et al. The matrikine N-alpha-PGP couples extracellular matrix fragmentation to endothelial permeability. Sci Adv. 2015;1(3):e1500175.PubMedPubMedCentralCrossRef
37.
go back to reference Evans CR, Karnovsky A, Kovach MA, Standiford TJ, Burant CF, Stringer KA. Untargeted LC-MS metabolomics of bronchoalveolar lavage fluid differentiates acute respiratory distress syndrome from health. J Proteome Res. 2014;13(2):640–9.PubMedCrossRef Evans CR, Karnovsky A, Kovach MA, Standiford TJ, Burant CF, Stringer KA. Untargeted LC-MS metabolomics of bronchoalveolar lavage fluid differentiates acute respiratory distress syndrome from health. J Proteome Res. 2014;13(2):640–9.PubMedCrossRef
38.
go back to reference Prasain JK, Wilson LS, Arabshahi A, Grubbs C, Barnes S. Mass spectrometric evidence for the modification of small molecules in a cobalt-60-irradiated rodent diet. J Mass Spectrom. 2017;52(8):507–16.PubMedPubMedCentralCrossRef Prasain JK, Wilson LS, Arabshahi A, Grubbs C, Barnes S. Mass spectrometric evidence for the modification of small molecules in a cobalt-60-irradiated rodent diet. J Mass Spectrom. 2017;52(8):507–16.PubMedPubMedCentralCrossRef
39.
go back to reference Lal CV, Kandasamy J, Dolma K, Ramani M, Kumar R, Wilson L, et al. Early airway microbial metagenomic and metabolomic signatures are associated with development of severe bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol. 2018;315(5):L810–L5.PubMedPubMedCentralCrossRef Lal CV, Kandasamy J, Dolma K, Ramani M, Kumar R, Wilson L, et al. Early airway microbial metagenomic and metabolomic signatures are associated with development of severe bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol. 2018;315(5):L810–L5.PubMedPubMedCentralCrossRef
40.
go back to reference Gottlieb J, Mattner F, Weissbrodt H, Dierich M, Fuehner T, Strueber M, et al. Impact of graft colonization with gram-negative bacteria after lung transplantation on the development of bronchiolitis obliterans syndrome in recipients with cystic fibrosis. Respir Med. 2009;103(5):743–9.PubMedCrossRef Gottlieb J, Mattner F, Weissbrodt H, Dierich M, Fuehner T, Strueber M, et al. Impact of graft colonization with gram-negative bacteria after lung transplantation on the development of bronchiolitis obliterans syndrome in recipients with cystic fibrosis. Respir Med. 2009;103(5):743–9.PubMedCrossRef
42.
go back to reference 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(5):1037–45.PubMedCrossRef 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(5):1037–45.PubMedCrossRef
43.
go back to reference Lal CV, Xu X, Jackson P, Atkinson TP, Faye-Petersen OM, Kandasamy J, et al. Ureaplasma infection-mediated release of matrix metalloproteinase-9 and PGP: a novel mechanism of preterm rupture of membranes and chorioamnionitis. Pediatr Res. 2017;81(1–1):75–9.PubMedCrossRef Lal CV, Xu X, Jackson P, Atkinson TP, Faye-Petersen OM, Kandasamy J, et al. Ureaplasma infection-mediated release of matrix metalloproteinase-9 and PGP: a novel mechanism of preterm rupture of membranes and chorioamnionitis. Pediatr Res. 2017;81(1–1):75–9.PubMedCrossRef
44.
go back to reference Hardison MT, Galin FS, Calderon CE, Djekic UV, Parker SB, Wille KM, et al. The presence of a matrix-derived neutrophil chemoattractant in bronchiolitis obliterans syndrome after lung transplantation. J Immunol. 2009;182(7):4423–31.PubMedCrossRef Hardison MT, Galin FS, Calderon CE, Djekic UV, Parker SB, Wille KM, et al. The presence of a matrix-derived neutrophil chemoattractant in bronchiolitis obliterans syndrome after lung transplantation. J Immunol. 2009;182(7):4423–31.PubMedCrossRef
45.
go back to reference Martin C, Thevenot G, Danel S, Chapron J, Tazi A, Macey J, et al. Pseudomonas aeruginosa induces vascular endothelial growth factor synthesis in airway epithelium in vitro and in vivo. Eur Respir J. 2011;38(4):939–46.PubMedCrossRef Martin C, Thevenot G, Danel S, Chapron J, Tazi A, Macey J, et al. Pseudomonas aeruginosa induces vascular endothelial growth factor synthesis in airway epithelium in vitro and in vivo. Eur Respir J. 2011;38(4):939–46.PubMedCrossRef
46.
go back to reference Krenn K, Klepetko W, Taghavi S, Lang G, Schneider B, Aharinejad S. Recipient vascular endothelial growth factor serum levels predict primary lung graft dysfunction. Am J Transplant Off J Am Soc Transplant Am Soc Transplant Surg. 2007;7(3):700–6.CrossRef Krenn K, Klepetko W, Taghavi S, Lang G, Schneider B, Aharinejad S. Recipient vascular endothelial growth factor serum levels predict primary lung graft dysfunction. Am J Transplant Off J Am Soc Transplant Am Soc Transplant Surg. 2007;7(3):700–6.CrossRef
47.
go back to reference Krebs R, Tikkanen JM, Nykanen AI, Wood J, Jeltsch M, Yla-Herttuala S, et al. Dual role of vascular endothelial growth factor in experimental obliterative bronchiolitis. Am J Respir Crit Care Med. 2005;171(12):1421–9.PubMedCrossRef Krebs R, Tikkanen JM, Nykanen AI, Wood J, Jeltsch M, Yla-Herttuala S, et al. Dual role of vascular endothelial growth factor in experimental obliterative bronchiolitis. Am J Respir Crit Care Med. 2005;171(12):1421–9.PubMedCrossRef
48.
go back to reference Xu H, Abuduwufuer A, Lv W, Zhou Z, Yang Y, Zhang C, et al. The role of HIF-1alpha-VEGF pathway in bronchiolitis obliterans after lung transplantation. J Cardiothorac Surg. 2019;14(1):27.PubMedPubMedCentralCrossRef Xu H, Abuduwufuer A, Lv W, Zhou Z, Yang Y, Zhang C, et al. The role of HIF-1alpha-VEGF pathway in bronchiolitis obliterans after lung transplantation. J Cardiothorac Surg. 2019;14(1):27.PubMedPubMedCentralCrossRef
49.
go back to reference Hannun YA, Obeid LM. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol. 2008;9(2):139–50.PubMedCrossRef Hannun YA, Obeid LM. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol. 2008;9(2):139–50.PubMedCrossRef
50.
go back to reference Pchejetski D, Kunduzova O, Dayon A, Calise D, Seguelas MH, Leducq N, et al. Oxidative stress-dependent sphingosine kinase-1 inhibition mediates monoamine oxidase A-associated cardiac cell apoptosis. Circ Res. 2007;100(1):41–9.PubMedCrossRef Pchejetski D, Kunduzova O, Dayon A, Calise D, Seguelas MH, Leducq N, et al. Oxidative stress-dependent sphingosine kinase-1 inhibition mediates monoamine oxidase A-associated cardiac cell apoptosis. Circ Res. 2007;100(1):41–9.PubMedCrossRef
51.
go back to reference LaBauve AE, Wargo MJ. Detection of host-derived sphingosine by Pseudomonas aeruginosa is important for survival in the murine lung. PLoS Pathog. 2014;10(1):e1003889.PubMedPubMedCentralCrossRef LaBauve AE, Wargo MJ. Detection of host-derived sphingosine by Pseudomonas aeruginosa is important for survival in the murine lung. PLoS Pathog. 2014;10(1):e1003889.PubMedPubMedCentralCrossRef
52.
go back to reference Pewzner-Jung Y, Tavakoli Tabazavareh S, Grassme H, Becker KA, Japtok L, Steinmann J, et al. Sphingoid long chain bases prevent lung infection by Pseudomonas aeruginosa. EMBO Mol Med. 2014;6(9):1205–14.PubMedPubMedCentralCrossRef Pewzner-Jung Y, Tavakoli Tabazavareh S, Grassme H, Becker KA, Japtok L, Steinmann J, et al. Sphingoid long chain bases prevent lung infection by Pseudomonas aeruginosa. EMBO Mol Med. 2014;6(9):1205–14.PubMedPubMedCentralCrossRef
53.
go back to reference Becker KA, Li X, Seitz A, Steinmann J, Koch A, Schuchman E, et al. Neutrophils kill reactive oxygen species-resistant Pseudomonas aeruginosa by Sphingosine. Cell Physiol Biochem. 2017;43(4):1603–16.PubMedCrossRef Becker KA, Li X, Seitz A, Steinmann J, Koch A, Schuchman E, et al. Neutrophils kill reactive oxygen species-resistant Pseudomonas aeruginosa by Sphingosine. Cell Physiol Biochem. 2017;43(4):1603–16.PubMedCrossRef
55.
go back to reference Shockman GD. Bacterial cell wall synthesis: the effect of threonine depletion. J Biol Chem. 1959;234:2340–2.PubMed Shockman GD. Bacterial cell wall synthesis: the effect of threonine depletion. J Biol Chem. 1959;234:2340–2.PubMed
56.
go back to reference Ron-Harel N, Ghergurovich JM, Notarangelo G, LaFleur MW, Tsubosaka Y, Sharpe AH, et al. T cell activation depends on extracellular alanine. Cell Rep. 2019;28(12):3011–21 e4.PubMedCrossRefPubMedCentral Ron-Harel N, Ghergurovich JM, Notarangelo G, LaFleur MW, Tsubosaka Y, Sharpe AH, et al. T cell activation depends on extracellular alanine. Cell Rep. 2019;28(12):3011–21 e4.PubMedCrossRefPubMedCentral
57.
go back to reference Trompette A, Gollwitzer ES, Yadava K, Sichelstiel AK, Sprenger N, Ngom-Bru C, et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med. 2014;20(2):159–66.PubMedCrossRef Trompette A, Gollwitzer ES, Yadava K, Sichelstiel AK, Sprenger N, Ngom-Bru C, et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med. 2014;20(2):159–66.PubMedCrossRef
58.
go back to reference Koizumi C, Yamada M, Ishizaki K, Ueda T, Sakurai K. Anti-infective control in human bronchiolar epithelial cells by mucin phenotypic changes following uptake of N-acetyl-L-cysteine. Free Radic Res. 2015;49(12):1449–58.PubMedCrossRef Koizumi C, Yamada M, Ishizaki K, Ueda T, Sakurai K. Anti-infective control in human bronchiolar epithelial cells by mucin phenotypic changes following uptake of N-acetyl-L-cysteine. Free Radic Res. 2015;49(12):1449–58.PubMedCrossRef
59.
go back to reference Guilliams M, De Kleer I, Henri S, Post S, Vanhoutte L, De Prijck S, et al. Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF. J Exp Med. 2013;210(10):1977–92.PubMedPubMedCentralCrossRef Guilliams M, De Kleer I, Henri S, Post S, Vanhoutte L, De Prijck S, et al. Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF. J Exp Med. 2013;210(10):1977–92.PubMedPubMedCentralCrossRef
60.
go back to reference Nayak DK, Zhou F, Xu M, Huang J, Tsuji M, Hachem R, et al. Long-term persistence of donor alveolar macrophages in human lung transplant recipients that influences donor-specific immune responses. Am J Transplant Off J Am Soc Transplant Am Soc Transplant Surg. 2016;16(8):2300–11.CrossRef Nayak DK, Zhou F, Xu M, Huang J, Tsuji M, Hachem R, et al. Long-term persistence of donor alveolar macrophages in human lung transplant recipients that influences donor-specific immune responses. Am J Transplant Off J Am Soc Transplant Am Soc Transplant Surg. 2016;16(8):2300–11.CrossRef
61.
go back to reference Salter SJ, Cox MJ, Turek EM, Calus ST, Cookson WO, Moffatt MF, et al. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol. 2014;12:87.PubMedPubMedCentralCrossRef Salter SJ, Cox MJ, Turek EM, Calus ST, Cookson WO, Moffatt MF, et al. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol. 2014;12:87.PubMedPubMedCentralCrossRef
62.
go back to reference Eisenhofer R, Minich JJ, Marotz C, Cooper A, Knight R, Weyrich LS. Contamination in low microbial biomass microbiome studies: issues and recommendations. Trends Microbiol. 2019;27(2):105–17.PubMedCrossRef Eisenhofer R, Minich JJ, Marotz C, Cooper A, Knight R, Weyrich LS. Contamination in low microbial biomass microbiome studies: issues and recommendations. Trends Microbiol. 2019;27(2):105–17.PubMedCrossRef
63.
go back to reference Zaza G, Dalla Gassa A, Felis G, Granata S, Torriani S, Lupo A. Impact of maintenance immunosuppressive therapy on the fecal microbiome of renal transplant recipients: comparison between an everolimus- and a standard tacrolimus-based regimen. PLoS One. 2017;12(5):e0178228.PubMedPubMedCentralCrossRef Zaza G, Dalla Gassa A, Felis G, Granata S, Torriani S, Lupo A. Impact of maintenance immunosuppressive therapy on the fecal microbiome of renal transplant recipients: comparison between an everolimus- and a standard tacrolimus-based regimen. PLoS One. 2017;12(5):e0178228.PubMedPubMedCentralCrossRef
64.
go back to reference Sharma NS, Lal CV, Li JD, Lou XY, Viera L, Abdallah T, et al. The neutrophil chemoattractant peptide proline-glycine-proline is associated with acute respiratory distress syndrome. Am J Physiol Lung Cell Mol Physiol. 2018;315(5):L653–L61.PubMedPubMedCentralCrossRef Sharma NS, Lal CV, Li JD, Lou XY, Viera L, Abdallah T, et al. The neutrophil chemoattractant peptide proline-glycine-proline is associated with acute respiratory distress syndrome. Am J Physiol Lung Cell Mol Physiol. 2018;315(5):L653–L61.PubMedPubMedCentralCrossRef
65.
go back to reference Dickson RP, Erb-Downward JR, Freeman CM, McCloskey L, Beck JM, Huffnagle GB, et al. Spatial variation in the healthy human lung microbiome and the adapted island model of lung biogeography. Ann Am Thorac Soc. 2015;12(6):821–30.PubMedPubMedCentralCrossRef Dickson RP, Erb-Downward JR, Freeman CM, McCloskey L, Beck JM, Huffnagle GB, et al. Spatial variation in the healthy human lung microbiome and the adapted island model of lung biogeography. Ann Am Thorac Soc. 2015;12(6):821–30.PubMedPubMedCentralCrossRef
66.
go back to reference Caesar LK, Kellogg JJ, Kvalheim OM, Cech NB. Opportunities and limitations for untargeted mass spectrometry metabolomics to identify biologically active constituents in complex natural product mixtures. J Nat Prod. 2019;82(3):469–84.PubMedPubMedCentralCrossRef Caesar LK, Kellogg JJ, Kvalheim OM, Cech NB. Opportunities and limitations for untargeted mass spectrometry metabolomics to identify biologically active constituents in complex natural product mixtures. J Nat Prod. 2019;82(3):469–84.PubMedPubMedCentralCrossRef
Metadata
Title
Differences in airway microbiome and metabolome of single lung transplant recipients
Authors
Nirmal S. Sharma
Grant Vestal
Keith Wille
Kapil N. Patel
Feng Cheng
Srinivas Tipparaju
Sultan Tousif
Mudassir M. Banday
Xin Xu
Landon Wilson
Viswam S. Nair
Casey Morrow
Don Hayes Jr
Andreas Seyfang
Stephen Barnes
Jessy S. Deshane
Amit Gaggar
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Respiratory Research / Issue 1/2020
Electronic ISSN: 1465-993X
DOI
https://doi.org/10.1186/s12931-020-01367-3

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