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Clinical Reviews in Allergy & Immunology
Published in: Clinical Reviews in Allergy & Immunology 2/2023

Open Access 11-03-2022 | Respiratory Microbiota

The Airway Microbiome-IL-17 Axis: a Critical Regulator of Chronic Inflammatory Disease

Authors: Jenny M. Mannion, Rachel M. McLoughlin, Stephen J. Lalor

Published in: Clinical Reviews in Allergy & Immunology | Issue 2/2023

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Abstract

The respiratory tract is home to a diverse microbial community whose influence on local and systemic immune responses is only beginning to be appreciated. Increasing reports have linked changes in this microbiome to a range of pulmonary and extrapulmonary disorders, including asthma, chronic obstructive pulmonary disease and rheumatoid arthritis. Central to many of these findings is the role of IL-17-type immunity as an important driver of inflammation. Despite the crucial role played by IL-17-mediated immune responses in protection against infection, overt Th17 cell responses have been implicated in the pathogenesis of several chronic inflammatory diseases. However, our knowledge of the influence of bacteria that commonly colonise the respiratory tract on IL-17-driven inflammatory responses remains sparse. In this article, we review the current knowledge on the role of specific members of the airway microbiota in the modulation of IL-17-type immunity and discuss how this line of research may support the testing of susceptible individuals and targeting of inflammation at its earliest stages in the hope of preventing the development of chronic disease.
Literature
1.
Pickard JM, Zeng MY, Caruso R, Nunez G (2017) Gut microbiota: role in pathogen colonization, immune responses, and inflammatory disease. Immunol Rev 279(1):70–89PubMedPubMedCentralCrossRef
2.
Bouskra D, Brezillon C, Berard M, Werts C, Varona R, Boneca IG, Eberl G (2008) Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature 456(7221):507–510PubMedCrossRef
3.
Yun Y, Srinivas G, Kuenzel S, Linnenbrink M, Alnahas S, Bruce KD, Steinhoff U, Baines JF, Schaible UE (2014) Environmentally determined differences in the murine lung microbiota and their relation to alveolar architecture. PLoS One 9(12):e113466
4.
Cryan JF, Dinan TG (2012) Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 13(10):701–712PubMedCrossRef
5.
Hilty M, Burke C, Pedro H, Cardenas P, Bush A, Bossley C, Davies J, Ervine A, Poulter L, Pachter L, Moffatt MF, Cookson WO (2010) Disordered microbial communities in asthmatic airways. PLoS One 5(1):e8578
6.
Erb-Downward JR, Thompson DL, Han MK, Freeman CM, McCloskey L, Schmidt LA, Young VB, Toews GB, Curtis JL, Sundaram B, Martinez FJ, Huffnagle GB (2011) Analysis of the lung microbiome in the healthy smoker and in COPD. PLoS One 6(2):e16384
7.
Cox MJ, Allgaier M, Taylor B, Baek MS, Huang YJ, Daly RA, Karaoz U, Andersen GL, Brown R, Fujimura KE, Wu B, Tran D, Koff J, Kleinhenz ME, Nielson D, Brodie EL, Lynch SV (2010) Airway microbiota and pathogen abundance in age-stratified cystic fibrosis patients. PLoS One 5(6):e11044
8.
Demoruelle MK, Norris J, Holers V, Harris J, Deane K (2014) The lung microbiome differs in asymptomatic subjects at elevated risk of future rheumatoid arthritis compared with healthy control subjects. Ann Am Thorac Soc 11:S74CrossRef
9.
10.
Effros RM (2006) Anatomy, development, and physiology of the lungs. GI Motility
11.
Gusareva ES, Acerbi E, Lau KJX, Luhung I, Premkrishnan BNV, Kolundzija S, Purbojati RW, Wong A, Houghton JNI, Miller D, Gaultier NE, Heinle CE, Clare ME, Vettath VK, Kee C, Lim SBY, Chenard C, Phung WJ, Kushwaha KK, Nee AP, Putra A, Panicker D, Yanqing K, Hwee YZ, Lohar SR, Kuwata M, Kim HL, Yang L, Uchida A, Drautz-Moses DI, Junqueira ACM, Schuster SC (2019) Microbial communities in the tropical air ecosystem follow a precise diel cycle. Proc Natl Acad Sci U S A 116(46):23299–23308PubMedPubMedCentralCrossRef
12.
Dickson RP, Erb-Downward JR, Martinez FJ, Huffnagle GB (2016) The Microbiome and the Respiratory Tract. Annu Rev Physiol 78:481–504PubMedCrossRef
13.
Man WH, de Steenhuijsen Piters WA, Bogaert D (2017) The microbiota of the respiratory tract: gatekeeper to respiratory health. Nat Rev Micro 15(5):259–270CrossRef
14.
Zhou Y, Mihindukulasuriya KA, Gao H, La Rosa PS, Wylie KM, Martin JC, Kota K, Shannon WD, Mitreva M, Sodergren E, Weinstock GM (2014) Exploration of bacterial community classes in major human habitats. Genome Biol 15(5):R66PubMedPubMedCentralCrossRef
15.
Edouard S, Million M, Bachar D, Dubourg G, Michelle C, Ninove L, Charrel R, Raoult D (2018) The nasopharyngeal microbiota in patients with viral respiratory tract infections is enriched in bacterial pathogens. Eur J Clin Microbiol Infect Dis 37(9):1725–1733PubMedCrossRef
16.
Le Bars P, Matamoros S, Montassier E, Le Vacon F, Potel G, Soueidan A, Jordana F, de La Cochetiere MF (2017) The oral cavity microbiota: between health, oral disease, and cancers of the aerodigestive tract. Can J Microbiol 63(6):475–492PubMedCrossRef
17.
Charlson ES, Chen J, Custers-Allen R, Bittinger K, Li H, Sinha R, Hwang J, Bushman FD, Collman RG (2010) Disordered microbial communities in the upper respiratory tract of cigarette smokers. PLoS One 5(12):e15216
18.
Pettigrew MM, Laufer AS, Gent JF, Kong Y, Fennie KP, Metlay JP (2012) Upper respiratory tract microbial communities, acute otitis media pathogens, and antibiotic use in healthy and sick children. Appl Environ Microbiol 78(17):6262–6270PubMedPubMedCentralCrossRef
19.
Teo SM, Mok D, Pham K, Kusel M, Serralha M, Troy N, Holt BJ, Hales BJ, Walker ML, Hollams E, Bochkov YA, Grindle K, Johnston SL, Gern JE, Sly PD, Holt PG, Holt KE, Inouye M (2015) The infant nasopharyngeal microbiome impacts severity of lower respiratory infection and risk of asthma development. Cell Host Microbe 17(5):704–715PubMedPubMedCentralCrossRef
20.
LeVine AM, Whitsett JA, Gwozdz JA, Richardson TR, Fisher JH, Burhans MS, Korfhagen TR (2000) Distinct effects of surfactant protein A or D deficiency during bacterial infection on the lung. J Immunol 165(7):3934–3940PubMedCrossRef
21.
Bassis CM, Erb-Downward JR, Dickson RP, Freeman CM, Schmidt TM, Young VB, Beck JM, Curtis JL, Huffnagle GB (2015) Analysis of the upper respiratory tract microbiotas as the source of the lung and gastric microbiotas in healthy individuals. MBio 6(2):e00037
22.
Huffnagle GB, Dickson RP, Lukacs NW (2017) The respiratory tract microbiome and lung inflammation: a two-way street. Mucosal Immunol 10(2):299–306PubMedCrossRef
23.
Cameron SJS, Lewis KE, Huws SA, Hegarty MJ, Lewis PD, Pachebat JA, Mur LAJ (2017) A pilot study using metagenomic sequencing of the sputum microbiome suggests potential bacterial biomarkers for lung cancer. PLoS One 12(5):e0177062-e
24.
Ren Y, Su H, She Y, Dai C, Xie D, Narrandes S, Huang S, Chen C, Xu W (2019) Whole genome sequencing revealed microbiome in lung adenocarcinomas presented as ground-glass nodules. Transl Lung Cancer Res 8(3):235–246PubMedPubMedCentralCrossRef
25.
Jin C, Lagoudas GK, Zhao C, Bullman S, Bhutkar A, Hu B, Ameh S, Sandel D, Liang XS, Mazzilli S, Whary MT, Meyerson M, Germain R, Blainey PC, Fox JG, Jacks T (2019) Commensal microbiota promote lung cancer development via gammadelta T cells. Cell 176(5):998-1013.e16PubMedPubMedCentralCrossRef
26.
Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM, Weaver CT (2005) Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 6(11):1123–1132PubMedCrossRef
27.
Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, Wang Y, Hood L, Zhu Z, Tian Q, Dong C (2005) A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 6(11):1133–1141PubMedPubMedCentralCrossRef
28.
29.
Molet S, Hamid Q, Davoine F, Nutku E, Taha R, Page N, Olivenstein R, Elias J, Chakir J (2001) IL-17 is increased in asthmatic airways and induces human bronchial fibroblasts to produce cytokines. J Allergy Clin Immunol 108(3):430–438PubMedCrossRef
30.
Halwani R, Sultana A, Vazquez-Tello A, Jamhawi A, Al-Masri AA, Al-Muhsen S (2017) Th-17 regulatory cytokines IL-21, IL-23, and IL-6 enhance neutrophil production of IL-17 cytokines during asthma. J Asthma 54(9):893–904PubMedCrossRef
31.
Yang D, Chen X, Wang J, Lou Q, Lou Y, Li L, Wang H, Chen J, Wu M, Song X, Qian Y (2019) Dysregulated lung commensal bacteria drive interleukin-17B production to promote pulmonary fibrosis through their outer membrane vesicles. Immunity 50(3):692-706.e7PubMedCrossRef
32.
Wilson MS, Madala SK, Ramalingam TR, Gochuico BR, Rosas IO, Cheever AW, Wynn TA (2010) Bleomycin and IL-1beta-mediated pulmonary fibrosis is IL-17A dependent. J Exp Med 207(3):535–552PubMedPubMedCentralCrossRef
33.
Paats MS, Bergen IM, Hoogsteden HC, van der Eerden MM, Hendriks RW (2012) Systemic CD4+ and CD8+ T-cell cytokine profiles correlate with GOLD stage in stable COPD. Eur Respir J 40(2):330–337PubMedCrossRef
34.
Di Stefano A, Caramori G, Gnemmi I, Contoli M, Vicari C, Capelli A, Magno F, D’Anna SE, Zanini A, Brun P, Casolari P, Chung KF, Barnes PJ, Papi A, Adcock I, Balbi B (2009) T helper type 17-related cytokine expression is increased in the bronchial mucosa of stable chronic obstructive pulmonary disease patients. Clin Exp Immunol 157(2):316–324PubMedPubMedCentralCrossRef
35.
Eustace A, Smyth LJC, Mitchell L, Williamson K, Plumb J, Singh D (2011) Identification of cells expressing IL-17A and IL-17F in the lungs of patients with COPD. Chest 139(5):1089–1100PubMedCrossRef
36.
Vargas-Rojas MI, Ramírez-Venegas A, Limón-Camacho L, Ochoa L, Hernández-Zenteno R, Sansores RH (2011) Increase of Th17 cells in peripheral blood of patients with chronic obstructive pulmonary disease. Respir Med 105(11):1648–1654PubMedCrossRef
37.
Zhang J, Chu S, Zhong X, Lao Q, He Z, Liang Y (2013) Increased expression of CD4+IL-17+ cells in the lung tissue of patients with stable chronic obstructive pulmonary disease (COPD) and smokers. Int Immunopharmacol 15(1):58–66PubMedCrossRef
38.
Xu W, Li R, Sun Y (2019) Increased IFN-γ-producing Th17/Th1 cells and their association with lung function and current smoking status in patients with chronic obstructive pulmonary disease. BMC Pulm Med 19(1):137PubMedPubMedCentralCrossRef
39.
Tan H-L, Regamey N, Brown S, Bush A, Lloyd CM, Davies JC (2011) The Th17 pathway in cystic fibrosis lung disease. Am J Respir Crit Care Med 184(2):252–258PubMedCrossRef
40.
Brodlie M, McKean MC, Johnson GE, Anderson AE, Hilkens CM, Fisher AJ, Corris PA, Lordan JL, Ward C (2011) Raised interleukin-17 is immunolocalised to neutrophils in cystic fibrosis lung disease. The Eur Respir J 37(6):1378–1385PubMedCrossRef
41.
Chen ACH, Martin ML, Lourie R, Rogers GB, Burr LD, Hasnain SZ, Bowler SD, McGuckin MA, Serisier DJ (2015) Adult non-cystic fibrosis bronchiectasis is characterised by airway luminal Th17 pathway activation. PLoS One 10(3):e0119325-e
42.
McInnes IB, Schett G (2011) The pathogenesis of rheumatoid arthritis. N Engl J Med 365(23):2205–2219PubMedCrossRef
43.
44.
Van Hamburg JP, Asmawidjaja PS, Davelaar N, Mus AM, Colin EM, Hazes JM, Dolhain RJ, Lubberts E (2011) Th17 cells, but not Th1 cells, from patients with early rheumatoid arthritis are potent inducers of matrix metalloproteinases and proinflammatory cytokines upon synovial fibroblast interaction, including autocrine interleukin-17A production. Arthritis Rheum 63(1):73–83PubMedCrossRef
45.
Chalan P, Kroesen B-J, van der Geest KSM, Huitema MG, Abdulahad WH, Bijzet J, Brouwer E, Boots AMH (2013) Circulating CD4+CD161+ T lymphocytes are increased in seropositive arthralgia patients but decreased in patients with newly diagnosed rheumatoid arthritis. PLoS One 8(11):e79370
46.
Kouri V-P, Olkkonen J, Ainola M, Li T-F, Björkman L, Konttinen YT, Mandelin J (2013) Neutrophils produce interleukin-17B in rheumatoid synovial tissue. Rheumatology 53(1):39–47PubMedCrossRef
47.
Liu D, Cao T, Wang N, Liu C, Ma N, Tu R, Min X (2016) IL-25 attenuates rheumatoid arthritis through suppression of Th17 immune responses in an IL-13-dependent manner. Sci Rep 6(1):36002PubMedPubMedCentralCrossRef
48.
Akitsu A, Ishigame H, Kakuta S, Chung SH, Ikeda S, Shimizu K, Kubo S, Liu Y, Umemura M, Matsuzaki G, Yoshikai Y, Saijo S, Iwakura Y (2015) IL-1 receptor antagonist-deficient mice develop autoimmune arthritis due to intrinsic activation of IL-17-producing CCR2(+)Vgamma6(+)gammadelta T cells. Nat Commun 6:7464PubMedCrossRef
49.
Cornelissen F, Mus AM, Asmawidjaja PS, van Hamburg JP, Tocker J, Lubberts E (2009) Interleukin-23 is critical for full-blown expression of a non-autoimmune destructive arthritis and regulates interleukin-17A and RORgammat in gammadelta T cells. Arthritis Res Ther 11(6):R194PubMedPubMedCentralCrossRef
50.
Ito Y, Usui T, Kobayashi S, Iguchi-Hashimoto M, Ito H, Yoshitomi H, Nakamura T, Shimizu M, Kawabata D, Yukawa N, Hashimoto M, Sakaguchi N, Sakaguchi S, Yoshifuji H, Nojima T, Ohmura K, Fujii T, Mimori T (2009) Gamma/delta T cells are the predominant source of interleukin-17 in affected joints in collagen-induced arthritis, but not in rheumatoid arthritis. Arthritis Rheum 60(8):2294–2303PubMedCrossRef
51.
Roark CL, French JD, Taylor MA, Bendele AM, Born WK, O’Brien RL (2007) Exacerbation of collagen-induced arthritis by oligoclonal, IL-17-producing gamma delta T cells. J Immunol 179(8):5576–5583PubMedCrossRef
52.
McGinley AM, Edwards SC, Raverdeau M, Mills KHG (2018) Th17 cells, γδ T cells and their interplay in EAE and multiple sclerosis. J Autoimmun 87:97–108CrossRef
53.
Fletcher JM, Lonergan R, Costelloe L, Kinsella K, Moran B, Farrelly C, Tubridy N, Mills KHG (2009) CD39<sup>+</sup>Foxp3<sup>+</sup> regulatory T cells suppress pathogenic Th17 cells and are impaired in multiple sclerosis. J Immunol 183(11):7602PubMedCrossRef
54.
Hirota K, Duarte JH, Veldhoen M, Hornsby E, Li Y, Cua DJ, Ahlfors H, Wilhelm C, Tolaini M, Menzel U, Garefalaki A, Potocnik AJ, Stockinger B (2011) Fate mapping of IL-17-producing T cells in inflammatory responses. Nat Immunol 12(3):255–263PubMedPubMedCentralCrossRef
55.
Tzartos JS, Friese MA, Craner MJ, Palace J, Newcombe J, Esiri MM, Fugger L (2008) Interleukin-17 production in central nervous system-infiltrating T cells and glial cells is associated with active disease in multiple sclerosis. Am J Pathol 172(1):146–155PubMedPubMedCentralCrossRef
56.
McGeachy MJ, Bak-Jensen KS, Chen Y, Tato CM, Blumenschein W, McClanahan T, Cua DJ (2007) TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat Immunol 8(12):1390–1397PubMedCrossRef
57.
Hatfield JK, Brown MA (2015) Group 3 innate lymphoid cells accumulate and exhibit disease-induced activation in the meninges in EAE. Cell Immunol 297(2):69–79PubMedCrossRef
58.
Sutton CE, Lalor SJ, Sweeney CM, Brereton CF, Lavelle EC, Mills KH (2009) Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity 31(2):331–341PubMedCrossRef
59.
Li J, Casanova JL, Puel A (2018) Mucocutaneous IL-17 immunity in mice and humans: host defense vs. excessive inflammation. Mucosal Immunol 11(3):581–9
60.
Peck A, Mellins ED (2010) Precarious balance: Th17 cells in host defense. Infect Immun 78(1):32–38PubMedCrossRef
61.
Ye P, Rodriguez FH, Kanaly S, Stocking KL, Schurr J, Schwarzenberger P, Oliver P, Huang W, Zhang P, Zhang J, Shellito JE, Bagby GJ, Nelson S, Charrier K, Peschon JJ, Kolls JK (2001) Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J Exp Med 194(4):519–527PubMedPubMedCentralCrossRef
62.
63.
Berer K, Mues M, Koutrolos M, Rasbi ZA, Boziki M, Johner C, Wekerle H, Krishnamoorthy G (2011) Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature 479(7374):538–541PubMedCrossRef
64.
Horai R, Silver PB, Chen J, Agarwal RK, Chong WP, Jittayasothorn Y, Mattapallil MJ, Nguyen S, Natarajan K, Villasmil R, Wang P, Karabekian Z, Lytton SD, Chan CC, Caspi RR (2013) Breakdown of immune privilege and spontaneous autoimmunity in mice expressing a transgenic T cell receptor specific for a retinal autoantigen. J Autoimmun 44:21–33PubMedPubMedCentralCrossRef
65.
Maeda Y, Takeda K (2019) Host-microbiota interactions in rheumatoid arthritis. Exp Mol Med 51(12):1–6PubMedCrossRef
66.
Zakostelska Z, Malkova J, Klimesova K, Rossmann P, Hornova M, Novosadova I, Stehlikova Z, Kostovcik M, Hudcovic T, Stepankova R, Juzlova K, Hercogova J, Tlaskalova-Hogenova H, Kverka M (2016) Intestinal microbiota promotes psoriasis-like skin inflammation by enhancing Th17 response. PLoS One 11(7):e0159539
67.
McGeachy MJ, Chen Y, Tato CM, Laurence A, Joyce-Shaikh B, Blumenschein WM, McClanahan TK, O’Shea JJ, Cua DJ (2009) The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo. Nat Immunol 10(3):314–324PubMedPubMedCentralCrossRef
68.
Feng T, Qin H, Wang L, Benveniste EN, Elson CO, Cong Y (2011) Th17 cells induce colitis and promote Th1 cell responses through IL-17 induction of innate IL-12 and IL-23 production. J Immunol 186(11):6313–6318PubMedCrossRef
69.
Godinez I, Keestra AM, Spees A, Baumler AJ (2011) The IL-23 axis in Salmonella gastroenteritis. Cell Microbiol 13(11):1639–1647PubMedCrossRef
70.
Lee SJ, McLachlan JB, Kurtz JR, Fan D, Winter SE, Baumler AJ, Jenkins MK, McSorley SJ (2012) Temporal expression of bacterial proteins instructs host CD4 T cell expansion and Th17 development. PLoS Pathog 8(1):e1002499
71.
Gollwitzer ES, Saglani S, Trompette A, Yadava K, Sherburn R, McCoy KD, Nicod LP, Lloyd CM, Marsland BJ (2014) Lung microbiota promotes tolerance to allergens in neonates via PD-L1. Nat Med 20(6):642–647PubMedCrossRef
72.
Herbst T, Sichelstiel A, Schär C, Yadava K, Bürki K, Cahenzli J, McCoy K, Marsland BJ, Harris NL (2011) Dysregulation of allergic airway inflammation in the absence of microbial colonization. Am J Respir Crit Care Med 184(2):198–205PubMedCrossRef
73.
Olszak T, An D, Zeissig S, Vera MP, Richter J, Franke A, Glickman JN, Siebert R, Baron RM, Kasper DL, Blumberg RS (2012) Microbial exposure during early life has persistent effects on natural killer T cell function. Science 336(6080):489–493PubMedPubMedCentralCrossRef
74.
Hill DA, Siracusa MC, Abt MC, Kim BS, Kobuley D, Kubo M, Kambayashi T, Larosa DF, Renner ED, Orange JS, Bushman FD, Artis D (2012) Commensal bacteria-derived signals regulate basophil hematopoiesis and allergic inflammation. Nat Med 18(4):538–546PubMedPubMedCentralCrossRef
75.
Russell SL, Gold MJ, Hartmann M, Willing BP, Thorson L, Wlodarska M, Gill N, Blanchet MR, Mohn WW, McNagny KM, Finlay BB (2012) Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Rep 13(5):440–447PubMedPubMedCentralCrossRef
76.
Fujimura KE, Sitarik AR, Havstad S, Lin DL, Levan S, Fadrosh D, Panzer AR, LaMere B, Rackaityte E, Lukacs NW, Wegienka G, Boushey HA, Ownby DR, Zoratti EM, Levin AM, Johnson CC, Lynch SV (2016) Neonatal gut microbiota associates with childhood multisensitized atopy and T cell differentiation. Nat Med 22(10):1187–1191PubMedPubMedCentralCrossRef
77.
Preston JA, Thorburn AN, Starkey MR, Beckett EL, Horvat JC, Wade MA, Sullivan BJ, Thomas R, Beagley KW, Gibson PG, Foster PS, Hansbro PM (2011) Streptococcus pneumoniae infection suppresses allergic airways disease by inducing regulatory T-cells. Eur Respir J 37(1):53PubMedCrossRef
78.
Huang YJ, Nariya S, Harris JM, Lynch SV, Choy DF, Arron JR, Boushey H (2015) The airway microbiome in patients with severe asthma: Associations with disease features and severity. J Allergy Clin Immunol 136(4):874–884PubMedPubMedCentralCrossRef
79.
Zhang Q, Cox M, Liang Z, Brinkmann F, Cardenas PA, Duff R, Bhavsar P, Cookson W, Moffatt M, Chung KF (2016) Airway microbiota in severe asthma and relationship to asthma severity and phenotypes. PLoS One 11(4):e0152724
80.
Huang YJ, Marsland BJ, Bunyavanich S, O’Mahony L, Leung DY, Muraro A, Fleisher TA (2017) The microbiome in allergic disease: Current understanding and future opportunities-2017 PRACTALL document of the American Academy of Allergy, Asthma & Immunology and the European Academy of Allergy and Clinical Immunology. J Allergy Clin Immunol 139(4):1099–1110PubMedPubMedCentralCrossRef
81.
Jounio U, Juvonen R, Bloigu A, Silvennoinen-Kassinen S, Kaijalainen T, Kauma H, Peitso A, Saukkoriipi A, Vainio O, Harju T, Leinonen M (2010) Pneumococcal carriage is more common in asthmatic than in non-asthmatic young men. Clin Respir J 4(4):222-9
82.
Marri PR, Stern DA, Wright AL, Billheimer D, Martinez FD. Asthma-associated differences in microbial composition of induced sputum (2013) J Allergy Clin Immunol 131(2):346–52.e1–3
83.
Green BJ, Wiriyachaiporn S, Grainge C, Rogers GB, Kehagia V, Lau L, Carroll MP, Bruce KD, Howarth PH (2014) Potentially pathogenic airway bacteria and neutrophilic inflammation in treatment resistant severe asthma. PLoS One 9(6):e100645-e
84.
Bisgaard H, Hermansen MN, Buchvald F, Loland L, Halkjaer LB, Bonnelykke K, Brasholt M, Heltberg A, Vissing NH, Thorsen SV, Stage M, Pipper CB (2007) Childhood asthma after bacterial colonization of the airway in neonates. N Engl J Med 357(15):1487–1495PubMedCrossRef
85.
Larsen JM, Brix S, Thysen AH, Birch S, Rasmussen MA, Bisgaard H (2014) Children with asthma by school age display aberrant immune responses to pathogenic airway bacteria as infants. J Allergy Clin Immunol 133(4):1008–1013PubMedCrossRef
86.
Folsgaard NV, Schjorring S, Chawes BL, Rasmussen MA, Krogfelt KA, Brix S, Bisgaard H (2013) Pathogenic bacteria colonizing the airways in asymptomatic neonates stimulates topical inflammatory mediator release. Am J Respir Crit Care Med 187(6):589–595PubMedCrossRef
87.
Jatakanon A, Uasuf C, Maziak W, Lim S, Chung KF, Barnes PJ (1999) Neutrophilic inflammation in severe persistent asthma. Am J Respir Crit Care Med 160(5 Pt 1):1532–1539PubMedCrossRef
88.
Green RH, Brightling CE, Woltmann G, Parker D, Wardlaw AJ, Pavord ID (2002) Analysis of induced sputum in adults with asthma: identification of subgroup with isolated sputum neutrophilia and poor response to inhaled corticosteroids. Thorax 57(10):875–879PubMedPubMedCentralCrossRef
89.
Agache I, Ciobanu C, Agache C, Anghel M (2010) Increased serum IL-17 is an independent risk factor for severe asthma. Respir Med 104(8):1131–1137PubMedCrossRef
90.
Taylor SL, Leong LEX, Choo JM, Wesselingh S, Yang IA, Upham JW, Reynolds PN, Hodge S, James AL, Jenkins C, Peters MJ, Baraket M, Marks GB, Gibson PG, Simpson JL, Rogers GB (2018) Inflammatory phenotypes in patients with severe asthma are associated with distinct airway microbiology. J Allergy Clin Immunol 141(1):94-103.e15
91.
Bisgaard H, Hermansen MN, Bonnelykke K, Stokholm J, Baty F, Skytt NL, Aniscenko J, Kebadze T, Johnston SL (2010) Association of bacteria and viruses with wheezy episodes in young children: prospective birth cohort study. BMJ (Clinical research ed) 341:c4978
92.
Wood LG, Simpson JL, Hansbro PM, Gibson PG (2010) Potentially pathogenic bacteria cultured from the sputum of stable asthmatics are associated with increased 8-isoprostane and airway neutrophilia. Free Radic Res 44(2):146–154PubMedCrossRef
93.
Simpson JL, Daly J, Baines KJ, Yang IA, Upham JW, Reynolds PN, Hodge S, James AL, Hugenholtz P, Willner D, Gibson PG (2016) Airway dysbiosis: Haemophilus influenzae and Tropheryma in poorly controlled asthma. Eur Respir J 47(3):792–800PubMedCrossRef
94.
Yang B, Liu R, Yang T, Jiang X, Zhang L, Wang L, Wang Q, Luo Z, Liu E, Fu Z (2015) Neonatal Streptococcus pneumoniae infection may aggravate adulthood allergic airways disease in association with IL-17A. PLoS One 10(3):e0123010
95.
McCann JR, Mason SN, Auten RL, St. Geme III JW, Seed PC (2016) Early-life intranasal colonization with nontypeable Haemophilus influenzae exacerbates juvenile airway disease in mice. Infect Immun 84(7):2022-2030
96.
Yang X, Wang Y, Zhao S, Wang R, Wang C (2018) Long-term exposure to low-dose Haemophilus influenzae during allergic airway disease drives a steroid-resistant neutrophilic inflammation and promotes airway remodeling. Oncotarget 9(38):24898–24913PubMedPubMedCentralCrossRef
97.
Essilfie A-T, Simpson JL, Horvat JC, Preston JA, Dunkley ML, Foster PS, Gibson PG, Hansbro PM (2011) Haemophilus influenzae infection drives IL-17-mediated neutrophilic allergic airways disease. PLoS Pathog 7(10):e1002244
98.
Alnahas S, Hagner S, Raifer H, Kilic A, Gasteiger G, Mutters R, Hellhund A, Prinz I, Pinkenburg O, Visekruna A, Garn H, Steinhoff U (2017) IL-17 and TNF-α are key mediators of Moraxella catarrhalis triggered exacerbation of allergic airway inflammation. Front Immunol 8(1562)
99.
Wilson RH, Whitehead GS, Nakano H, Free ME, Kolls JK, Cook DN (2009) Allergic sensitization through the airway primes Th17-dependent neutrophilia and airway hyperresponsiveness. Am J Respir Crit Care Med 180(8):720–730PubMedPubMedCentralCrossRef
100.
Wakashin H, Hirose K, Maezawa Y, Kagami S, Suto A, Watanabe N, Saito Y, Hatano M, Tokuhisa T, Iwakura Y, Puccetti P, Iwamoto I, Nakajima H (2008) IL-23 and Th17 cells enhance Th2-cell-mediated eosinophilic airway inflammation in mice. Am J Respir Crit Care Med 178(10):1023–1032PubMedCrossRef
101.
Lee HS, Park DE, Lee JW, Chang Y, Kim HY, Song WJ, Kang HR, Park HW, Chang YS, Cho SH (2017) IL-23 secreted by bronchial epithelial cells contributes to allergic sensitization in asthma model: role of IL-23 secreted by bronchial epithelial cells. Am J Physiol Lung Cell Mol Physiol 312(1):L13-L21
102.
Lee HS, Park DE, Lee JW, Sohn KH, Cho SH, Park HW (2020) Role of interleukin-23 in the development of nonallergic eosinophilic inflammation in a murine model of asthma. Exp Mol Med 52(1):92–104PubMedPubMedCentralCrossRef
103.
Larsen JM, Steen-Jensen DB, Laursen JM, Sondergaard JN, Musavian HS, Butt TM, Brix S (2012) Divergent pro-inflammatory profile of human dendritic cells in response to commensal and pathogenic bacteria associated with the airway microbiota. PLoS One 7(2):e31976
104.
105.
Segal LN, Alekseyenko AV, Clemente JC, Kulkarni R, Wu B, Chen H, Berger KI, Goldring RM, Rom WN, Blaser MJ, Weiden MD (2013) Enrichment of lung microbiome with supraglottic taxa is associated with increased pulmonary inflammation. Microbiome 1:19
106.
Segal LN, Clemente JC, Tsay JC, Koralov SB, Keller BC, Wu BG, Li Y, Shen N, Ghedin E, Morris A, Diaz P, Huang L, Wikoff WR, Ubeda C, Artacho A, Rom WN, Sterman DH, Collman RG, Blaser MJ, Weiden MD (2016) Enrichment of the lung microbiome with oral taxa is associated with lung inflammation of a Th17 phenotype. Nat Microbiol 1:16031PubMedPubMedCentralCrossRef
107.
Dy R, Sethi S (2016) The lung microbiome and exacerbations of COPD. Curr Opin Pulm Med 22(3):196–202PubMedCrossRef
108.
Mayhew D, Devos N, Lambert C, Brown JR, Clarke SC, Kim VL, Magid-Slav M, Miller BE, Ostridge KK, Patel R, Sathe G, Simola DF, Staples KJ, Sung R, Tal-Singer R, Tuck AC, Van Horn S, Weynants V, Williams NP, Devaster JM, Wilkinson TMA (2018) Longitudinal profiling of the lung microbiome in the AERIS study demonstrates repeatability of bacterial and eosinophilic COPD exacerbations. Thorax 73(5):422–430PubMedCrossRef
109.
Sze MA, Dimitriu PA, Suzuki M, McDonough JE, Campbell JD, Brothers JF, Erb-Downward JR, Huffnagle GB, Hayashi S, Elliott WM, Cooper J, Sin DD, Lenburg ME, Spira A, Mohn WW, Hogg JC (2015) Host response to the lung microbiome in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 192(4):438–445PubMedPubMedCentralCrossRef
110.
Wang Z, Maschera B, Lea S, Kolsum U, Michalovich D, Van Horn S, Traini C, Brown JR, Hessel EM, Singh D (2019) Airway host-microbiome interactions inchronic obstructive pulmonary disease. Respir Res 20(1):113
111.
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(2):195–199PubMedPubMedCentralCrossRef
112.
Zou Y, Chen X, Liu J, Zhou DB, Kuang X, Xiao J, Yu Q, Lu X, Li W, Xie B, Chen Q (2017) Serum IL-1β and IL-17 levels in patients with COPD: associations with clinical parameters. Int J Chron Obstruct Pulmon Dis 12:1247–1254PubMedPubMedCentralCrossRef
113.
Zhang L, Cheng Z, Liu W, Wu K (2013) Expression of interleukin (IL)-10, IL-17A and IL-22 in serum and sputum of stable chronic obstructive pulmonary disease patients. COPD 10(4):459–465PubMedCrossRef
114.
Ponce-Gallegos MA, Perez-Rubio G, Ambrocio-Ortiz E, Partida-Zavala N, Hernandez-Zenteno R, Flores-Trujillo F, Garcia-Gomez L, Hernandez-Perez A, Ramirez-Venegas A, Falfan-Valencia R (2020) Genetic variants in IL17A and serum levels of IL-17A are associated with COPD related to tobacco smoking and biomass burning. Sci Rep 10(1):784PubMedPubMedCentralCrossRef
115.
Park H, Shin JW, Park S-G, Kim W (2014) Microbial communities in the upper respiratory tract of patients with asthma and chronic obstructive pulmonary disease. PLoS One 9(10):e109710
116.
Yadava K, Pattaroni C, Sichelstiel AK, Trompette A, Gollwitzer ES, Salami O, von Garnier C, Nicod LP, Marsland BJ (2015) Microbiota promotes chronic pulmonary inflammation by enhancing IL-17A and autoantibodies. Am J Respir Crit Care Med 193(9):975–987CrossRef
117.
Xiong J, Tian J, Zhou L, Le Y, Sun Y (2020) Interleukin-17A Deficiency Attenuated Emphysema and Bone Loss in Mice Exposed to Cigarette Smoke. Int J Chron Obstruct Pulmon Dis 15:301–310PubMedPubMedCentralCrossRef
118.
Chen K, Pociask DA, McAleer JP, Chan YR, Alcorn JF, Kreindler JL, Keyser MR, Shapiro SD, Houghton AM, Kolls JK, Zheng M (2011) IL-17RA is required for CCL2 expression, macrophage recruitment, and emphysema in response to cigarette smoke. PLoS One 6(5):e20333
119.
Roos AB, Sethi S, Nikota J, Wrona CT, Dorrington MG, Sanden C, Bauer CM, Shen P, Bowdish D, Stevenson CS, Erjefalt JS, Stampfli MR (2015) IL-17A and the promotion of neutrophilia in acute exacerbation of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 192(4):428–437PubMedCrossRef
120.
121.
122.
Gaggar A, Hector A, Bratcher PE, Mall MA, Griese M, Hartl D (2011) The role of matrix metalloproteinases in cystic fibrosis lung disease. Eur Respir J 38(3):721–727PubMedPubMedCentralCrossRef
123.
Meyer KC, Lewandoski JR, Zimmerman JJ, Nunley D, Calhoun WJ, Dopico GA (1991) Human neutrophil elastase and elastase/alpha 1-antiprotease complex in cystic fibrosis. Comparison with interstitial lung disease and evaluation of the effect of intravenously administered antibiotic therapy. Am Rev Respir Dis 144(3 Pt 1):580–5
124.
Decraene A, Willems-Widyastuti A, Kasran A, De Boeck K, Bullens DM, Dupont LJ (2010) Elevated expression of both mRNA and protein levels of IL-17A in sputum of stable Cystic Fibrosis patients. Respir Res 11(1):177PubMedPubMedCentralCrossRef
125.
Brodlie M, McKean MC, Johnson GE, Anderson AE, Hilkens CMU, Fisher AJ, Corris PA, Lordan JL, Ward C (2011) Raised interleukin-17 is immunolocalised to neutrophils in cystic fibrosis lung disease. Eur Respir J 37(6):1378–1385PubMedCrossRef
126.
McAllister F, Henry A, Kreindler JL, Dubin PJ, Ulrich L, Steele C, Finder JD, Pilewski JM, Carreno BM, Goldman SJ, Pirhonen J, Kolls JK (2005) Role of IL-17A, IL-17F, and the IL-17 receptor in regulating growth-related oncogene-alpha and granulocyte colony-stimulating factor in bronchial epithelium: implications for airway inflammation in cystic fibrosis. J Immunol 175(1):404–412PubMedCrossRef
127.
Dubin PJ, McAllister F, Kolls JK (2007) Is cystic fibrosis a TH17 disease? Inflamm Res 56(6):221–227PubMedCrossRef
128.
Chan YR, Chen K, Duncan SR, Lathrop KL, Latoche JD, Logar AJ, Pociask DA, Wahlberg BJ, Ray P, Ray A, Pilewski JM, Kolls JK (2013) Patients with cystic fibrosis have inducible IL-17+IL-22+ memory cells in lung draining lymph nodes. J Allergy Clin Immunol 131(4):1117–29, 29.e1–5
129.
Frayman KB, Wylie KM, Armstrong DS, Carzino R, Davis SD, Ferkol TW, Grimwood K, Storch GA, Ranganathan SC (2019) Differences in the lower airway microbiota of infants with and without cystic fibrosis. J Cyst Fibros 18(5):646–652PubMedCrossRef
130.
Muhlebach MS, Zorn BT, Esther CR, Hatch JE, Murray CP, Turkovic L, Ranganathan SC, Boucher RC, Stick SM, Wolfgang MC (2018) Initial acquisition and succession of the cystic fibrosis lung microbiome is associated with disease progression in infants and preschool children. PLoS Pathog 14(1):e1006798-e
131.
Taylor SL, Leong LEX, Ivey KL, Wesselingh S, Grimwood K, Wainwright CE, Rogers GB (2020) Total bacterial load, inflammation, and structural lung disease in paediatric cystic fibrosis. J Cyst Fibros
132.
McGuigan L, Callaghan M (2015) The evolving dynamics of the microbial community in the cystic fibrosis lung. Environ Microbiol 17(1):16–28PubMedCrossRef
133.
Acosta N, Heirali A, Somayaji R, Surette MG, Workentine ML, Sibley CD, Rabin HR, Parkins MD (2018) Sputum microbiota is predictive of long-term clinical outcomes in young adults with cystic fibrosis. Thorax 73(11):1016–1025PubMedCrossRef
134.
Martiniano SL, Nick JA, Daley CL (2016) Nontuberculous Mycobacterial Infections in Cystic Fibrosis. Clin Chest Med 37(1):83–96PubMedCrossRef
135.
136.
Breuer O, Schultz A, Turkovic L, de Klerk N, Keil AD, Brennan S, Harrison J, Robertson C, Robinson PJ, Sly PD, Ranganathan S, Stick SM, Caudri D (2019) Changing prevalence of lower airway infections in young children with cystic fibrosis. Am J Respir Crit Care Med 200(5):590–599PubMedCrossRef
137.
Garcia-Nuñez M, Garcia-Gonzalez M, Pomares X, Montón C, Millares L, Quero S, Prina E, Asensio O, Bosque M, Capilla S, Cuevas O, Monsó E (2020) The respiratory microbiome in cystic fibrosis: compartment patterns and clinical relationships in early stage disease. Front Microbiol 11(1463)
138.
Fodor AA, Klem ER, Gilpin DF, Elborn JS, Boucher RC, Tunney MM, Wolfgang MC (2012) The adult cystic fibrosis airway microbiota is stable over time and infection type, and highly resilient to antibiotic treatment of exacerbations. PLoS One 7(9):e45001
139.
Sagel SD, Wagner BD, Anthony MM, Emmett P, Zemanick ET (2012) Sputum biomarkers of inflammation and lung function decline in children with cystic fibrosis. Am J Respir Crit Care Med 186(9):857–865PubMedPubMedCentralCrossRef
140.
Surette MG (2014) The cystic fibrosis lung microbiome. Ann Am Thorac Soc 11(Supplement 1):S61–S65PubMedCrossRef
141.
Cuthbertson L, Walker AW, Oliver AE, Rogers GB, Rivett DW, Hampton TH, Ashare A, Elborn JS, De Soyza A, Carroll MP, Hoffman LR, Lanyon C, Moskowitz SM, O'Toole GA, Parkhill J, Planet PJ, Teneback CC, Tunney MM, Zuckerman JB, Bruce KD, van der Gast CJ (2020) Lung function and microbiota diversity in cystic fibrosis. Microbiome 8(1):45
142.
Zemanick ET, Wagner BD, Robertson CE, Ahrens RC, Chmiel JF, Clancy JP, Gibson RL, Harris WT, Kurland G, Laguna TA, McColley SA, McCoy K, Retsch-Bogart G, Sobush KT, Zeitlin PL, Stevens MJ, Accurso FJ, Sagel SD, Harris JK (2017) Airway microbiota across age and disease spectrum in cystic fibrosis. Eur Respir J 50(5):1700832PubMedPubMedCentralCrossRef
143.
Armougom F, Bittar F, Stremler N, Rolain JM, Robert C, Dubus JC, Sarles J, Raoult D, La Scola B (2009) Microbial diversity in the sputum of a cystic fibrosis patient studied with 16S rDNA pyrosequencing. Eur J Clin Microbiol Infect Dis 28(9):1151–1154PubMedCrossRef
144.
Guss AM, Roeselers G, Newton IL, Young CR, Klepac-Ceraj V, Lory S, Cavanaugh CM (2011) Phylogenetic and metabolic diversity of bacteria associated with cystic fibrosis. ISME J 5(1):20–29PubMedCrossRef
145.
Acosta N, Whelan FJ, Somayaji R, Poonja A, Surette MG, Rabin HR, Parkins MD (2017) The evolving cystic fibrosis microbiome: a comparative cohort study spanning 16 years. Ann Am Thorac Soc 14(8):1288–1297PubMedCrossRef
146.
Rogers GB, Hart CA, Mason JR, Hughes M, Walshaw MJ, Bruce KD (2003) Bacterial diversity in cases of lung infection in cystic fibrosis patients: 16S ribosomal DNA (rDNA) length heterogeneity PCR and 16S rDNA terminal restriction fragment length polymorphism profiling. J Clin Microbiol 41(8):3548–3558PubMedPubMedCentralCrossRef
147.
Hogan DA, Willger SD, Dolben EL, Hampton TH, Stanton BA, Morrison HG, Sogin ML, Czum J, Ashare A (2016) Analysis of lung microbiota in bronchoalveolar lavage, protected brush and sputum samples from subjects with mild-to-moderate cystic fibrosis lung disease. PLoS One 11(3):e0149998
148.
Berdah L, Taytard J, Leyronnas S, Clement A, Boelle PY, Corvol H (2018) Stenotrophomonas maltophilia: a marker of lung disease severity. Pediatr Pulmonol 53(4):426–430PubMedPubMedCentralCrossRef
149.
Bayes HK, Ritchie ND, Evans TJ (2016) Interleukin-17 is required for control of chronic lung infection caused by Pseudomonas aeruginosa. Infect Immun 84(12):3507–3516PubMedPubMedCentralCrossRef
150.
Taylor PR, Bonfield TL, Chmiel JF, Pearlman E (2016) Neutrophils from F508del cystic fibrosis patients produce IL-17A and express IL-23 - dependent IL-17RC. Clin Immunol 170:53–60PubMedCrossRef
151.
Hsu D, Taylor P, Fletcher D, van Heeckeren R, Eastman J, van Heeckeren A, Davis P, Chmiel JF, Pearlman E, Bonfield TL (2016) Interleukin-17 pathophysiology and therapeutic intervention in cystic fibrosis lung infection and inflammation. Infect Immun 84(9):2410–2421PubMedPubMedCentralCrossRef
152.
Dubin PJ, Kolls JK (2007) IL-23 mediates inflammatory responses to mucoid Pseudomonas aeruginosa lung infection in mice. Am J Physiol Lung Cell Mol Physiol 292(2):L519–28
153.
Magis-Escurra C, Reijers MH (2015) Bronchiectasis. BMJ. Clin Evid 2015:1507
154.
Schäfer J, Griese M, Chandrasekaran R, Chotirmall SH, Hartl D (2018) Pathogenesis, imaging and clinical characteristics of CF and non-CF bronchiectasis. BMC Pulm Med 18(1):79
155.
O’Brien C, Guest PJ, Hill SL, Stockley RA (2000) Physiological and radiological characterisation of patients diagnosed with chronic obstructive pulmonary disease in primary care. Thorax 55(8):635–642PubMedPubMedCentralCrossRef
156.
Van der Gast CJ, Cuthbertson L, Rogers GB, Pope C, Marsh RL, Redding GJ, Bruce KD, Chang AB, Hoffman LR (2014) Three clinically distinct chronic pediatric airway infections share a common core microbiota. Ann Am Thorac Soc 11(7):1039–1048PubMedPubMedCentralCrossRef
157.
Cox MJ, Turek EM, Hennessy C, Mirza GK, James PL, Coleman M, Jones A, Wilson R, Bilton D, Cookson WO, Moffatt MF, Loebinger MR (2017) Longitudinal assessment of sputum microbiome by sequencing of the 16S rRNA gene in non-cystic fibrosis bronchiectasis patients. PLoS One 12(2):e0170622
158.
Rogers GB, van der Gast CJ, Cuthbertson L, Thomson SK, Bruce KD, Martin ML, Serisier DJ (2013) Clinical measures of disease in adult non-CF bronchiectasis correlate with airway microbiota composition. Thorax 68(8):731–737PubMedCrossRef
159.
Fowler SJ, French J, Screaton NJ, Foweraker J, Condliffe A, Haworth CS, Exley AR, Bilton D (2006) Nontuberculous mycobacteria in bronchiectasis: prevalence and patient characteristics. Eur Respir J 28(6):1204–1210PubMedCrossRef
160.
Tunney MM, Einarsson GG, Wei L, Drain M, Klem ER, Cardwell C, Ennis M, Boucher RC, Wolfgang MC, Elborn JS (2013) Lung microbiota and bacterial abundance in patients with bronchiectasis when clinically stable and during exacerbation. Am J Respir Crit Care Med 187(10):1118–1126PubMedPubMedCentralCrossRef
161.
Fouka E, Lamprianidou E, Arvanitidis K, Filidou E, Kolios G, Miltiades P, Paraskakis E, Antoniadis A, Kotsianidis I, Bouros D (2014) Low-dose clarithromycin therapy modulates Th17 response in non-cystic fibrosis bronchiectasis patients. Lung 192(6):849–855PubMedCrossRef
162.
Maher TM, Wells AU, Laurent GJ (2007) Idiopathic pulmonary fibrosis: multiple causes and multiple mechanisms? Eur Respir J 30(5):835–839PubMedCrossRef
163.
Hams E, Armstrong ME, Barlow JL, Saunders SP, Schwartz C, Cooke G, Fahy RJ, Crotty TB, Hirani N, Flynn RJ, Voehringer D, McKenzie ANJ, Donnelly SC, Fallon PG (2014) IL-25 and type 2 innate lymphoid cells induce pulmonary fibrosis. Proc Natl Acad Sci U S A 111(1):367–372PubMedCrossRef
164.
Gasse P, Riteau N, Vacher R, Michel ML, Fautrel A, di Padova F, Fick L, Charron S, Lagente V, Eberl G, Le Bert M, Quesniaux VF, Huaux F, Leite-de-Moraes M, Ryffel B, Couillin I (2011) IL-1 and IL-23 mediate early IL-17A production in pulmonary inflammation leading to late fibrosis. PLoS One 6(8):e23185
165.
Cortez DM, Feldman MD, Mummidi S, Valente AJ, Steffensen B, Vincenti M, Barnes JL, Chandrasekar B (2007) IL-17 stimulates MMP-1 expression in primary human cardiac fibroblasts via p38 MAPK- and ERK1/2-dependent C/EBP-beta, NF-kappaB, and AP-1 activation. Am J Physiol Heart Circ Physiol 293(6):H3356–H3365PubMedCrossRef
166.
Kinder BW, Brown KK, Schwarz MI, Ix JH, Kervitsky A, King TE Jr (2008) Baseline BAL neutrophilia predicts early mortality in idiopathic pulmonary fibrosis. Chest 133(1):226–232PubMedCrossRef
167.
O’Dwyer DN, Ashley SL, Gurczynski SJ, Xia M, Wilke C, Falkowski NR, Norman KC, Arnold KB, Huffnagle GB, Salisbury ML, Han MK, Flaherty KR, White ES, Martinez FJ, Erb-Downward JR, Murray S, Moore BB, Dickson RP (2019) Lung microbiota contribute to pulmonary inflammation and disease progression in pulmonary fibrosis. Am J Respir Crit Care Med 199(9):1127–1138PubMedPubMedCentralCrossRef
168.
Invernizzi R, Barnett J, Rawal B, Nair A, Ghai P, Kingston S, Chua F, Wu Z, Wells AU, Renzoni ER, Nicholson AG, Rice A, Lloyd CM, Byrne AJ, Maher TM, Devaraj A, Molyneaux PL (2020) Bacterial burden in the lower airways predicts disease progression in idiopathic pulmonary fibrosis and is independent of radiological disease extent. Eur Respir J 1901519
169.
Shulgina L, Cahn AP, Chilvers ER, Parfrey H, Clark AB, Wilson EC, Twentyman OP, Davison AG, Curtin JJ, Crawford MB, Wilson AM (2013) Treating idiopathic pulmonary fibrosis with the addition of co-trimoxazole: a randomised controlled trial. Thorax 68(2):155–162PubMedCrossRef
170.
Kawamura K, Ichikado K, Yasuda Y, Anan K, Suga M (2017) Azithromycin for idiopathic acute exacerbation of idiopathic pulmonary fibrosis: a retrospective single-center study. BMC Pulm Med 17(1):94PubMedPubMedCentralCrossRef
171.
Han MK, Zhou Y, Murray S, Tayob N, Noth I, Lama VN, Moore BB, White ES, Flaherty KR, Huffnagle GB, Martinez FJ (2014) Lung microbiome and disease progression in idiopathic pulmonary fibrosis: an analysis of the COMET study. Lancet Respir Med 2(7):548–556PubMedPubMedCentralCrossRef
172.
Molyneaux PL, Cox MJ, Willis-Owen SAG, Mallia P, Russell KE, Russell A-M, Murphy E, Johnston SL, Schwartz DA, Wells AU, Cookson WOC, Maher TM, Moffatt MF (2014) The role of bacteria in the pathogenesis and progression of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 190(8):906–913PubMedPubMedCentralCrossRef
173.
Tong X, Su F, Xu X, Xu H, Yang T, Xu Q, Dai H, Huang K, Zou L, Zhang W, Pei S, Xiao F, Li Y, Wang C (2019) Alterations to the lung microbiome in idiopathic pulmonary fibrosis patients. Front Cell Infect Microbiol 9:149
174.
Kotake S, Udagawa N, Takahashi N, Matsuzaki K, Itoh K, Ishiyama S, Saito S, Inoue K, Kamatani N, Gillespie MT, Martin TJ, Suda T (1999) IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest 103(9):1345–1352PubMedPubMedCentralCrossRef
175.
Ruscitti P, Di Benedetto P, Berardicurti O, Liakouli V, Carubbi F, Cipriani P, Giacomelli R (2018) Adipocytokines in rheumatoid arthritis: the hidden link between inflammation and cardiometabolic comorbidities. J Immunol Res 2018:8410182PubMedPubMedCentralCrossRef
176.
Sato K, Takayanagi H (2006) Osteoclasts, rheumatoid arthritis, and osteoimmunology. Curr Opin Rheumatol 18(4):419–426PubMedCrossRef
177.
Murphy CA, Langrish CL, Chen Y, Blumenschein W, McClanahan T, Kastelein RA, Sedgwick JD, Cua DJ (2003) Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med 198(12):1951–1957PubMedPubMedCentralCrossRef
178.
Guo W, Yu D, Wang X, Luo C, Chen Y, Lei W, Wang C, Ge Y, Xue W, Tian Q, Gao X, Yao W (2016) Anti-inflammatory effects of interleukin-23 receptor cytokine-binding homology region rebalance T cell distribution in rodent collagen-induced arthritis. Oncotarget 7(22):31800–31813PubMedPubMedCentralCrossRef
179.
Chalan P, Kroesen BJ, van der Geest KS, Huitema MG, Abdulahad WH, Bijzet J, Brouwer E, Boots AM (2013) Circulating CD4+CD161+ T lymphocytes are increased in seropositive arthralgia patients but decreased in patients with newly diagnosed rheumatoid arthritis. PLoS One 8(11):e79370
180.
Yago T, Nanke Y, Kawamoto M, Furuya T, Kobashigawa T, Kamatani N, Kotake S (2007) IL-23 induces human osteoclastogenesis via IL-17 in vitro, and anti-IL-23 antibody attenuates collagen-induced arthritis in rats. Arthritis Res Ther 9(5):R96PubMedPubMedCentralCrossRef
181.
Mitsdoerffer M, Lee Y, Jager A, Kim HJ, Korn T, Kolls JK, Cantor H, Bettelli E, Kuchroo VK (2010) Proinflammatory T helper type 17 cells are effective B-cell helpers. Proc Natl Acad Sci U S A 107(32):14292–14297PubMedPubMedCentralCrossRef
182.
Deane KD, Norris JM, Holers VM (2010) Preclinical rheumatoid arthritis: identification, evaluation, and future directions for investigation. Rheum Dis Clin North Am 36(2):213–241PubMedPubMedCentralCrossRef
183.
MacGregor AJ, Snieder H, Rigby AS, Koskenvuo M, Kaprio J, Aho K, Silman AJ (2000) Characterizing the quantitative genetic contribution to rheumatoid arthritis using data from twins. Arthritis Rheum 43(1):30–37PubMedCrossRef
184.
Svard A, Kastbom A, Reckner-Olsson A, Skogh T (2008) Presence and utility of IgA-class antibodies to cyclic citrullinated peptides in early rheumatoid arthritis: the Swedish TIRA project. Arthritis Res Ther 10(4):R75PubMedPubMedCentralCrossRef
185.
Willis VC, Demoruelle MK, Derber LA, Chartier-Logan CJ, Parish MC, Pedraza IF, Weisman MH, Norris JM, Holers VM, Deane KD (2013) Sputum autoantibodies in patients with established rheumatoid arthritis and subjects at risk of future clinically apparent disease. Arthritis Rheum 65(10):2545–2554PubMedPubMedCentral
186.
Wu HJ, Ivanov II, Darce J, Hattori K, Shima T, Umesaki Y, Littman DR, Benoist C, Mathis D (2010) Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 32(6):815–827PubMedPubMedCentralCrossRef
187.
Tan TG, Sefik E, Geva-Zatorsky N, Kua L, Naskar D, Teng F, Pasman L, Ortiz-Lopez A, Jupp R, Wu HJ, Kasper DL, Benoist C, Mathis D (2016) Identifying species of symbiont bacteria from the human gut that, alone, can induce intestinal Th17 cells in mice. Proc Natl Acad Sci U S A 113(50):E8141–E8150PubMedPubMedCentralCrossRef
188.
Evans-Marin H, Rogier R, Koralov SB, Manasson J, Roeleveld D, van der Kraan PM, Scher JU, Koenders MI, Abdollahi-Roodsaz S (2018) Microbiota-dependent involvement of Th17 cells in murine models of inflammatory arthritis. Arthritis Rheumatol 70(12):1971–1983PubMedPubMedCentralCrossRef
189.
O’Dell JR, Blakely KW, Mallek JA, Eckhoff PJ, Leff RD, Wees SJ, Sems KM, Fernandez AM, Palmer WR, Klassen LW, Paulsen GA, Haire CE, Moore GF (2001) Treatment of early seropositive rheumatoid arthritis: a two-year, double-blind comparison of minocycline and hydroxychloroquine. Arthritis Rheum 44(10):2235–2241PubMedCrossRef
190.
Maeda Y, Kumanogoh A, Takeda K (2016) Altered composition of gut microbiota in rheumatoid arthritis patients. Nihon Rinsho Meneki Gakkai Kaishi 39(1):59–63PubMedCrossRef
191.
Scher JU, Sczesnak A, Longman RS, Segata N, Ubeda C, Bielski C, Rostron T, Cerundolo V, Pamer EG, Abramson SB, Huttenhower C, Littman DR (2013) Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. eLife 2:e01202
192.
Zhang X, Zhang D, Jia H, Feng Q, Wang D, Liang D, Wu X, Li J, Tang L, Li Y, Lan Z, Chen B, Li Y, Zhong H, Xie H, Jie Z, Chen W, Tang S, Xu X, Wang X, Cai X, Liu S, Xia Y, Li J, Qiao X, Al-Aama JY, Chen H, Wang L, Wu QJ, Zhang F, Zheng W, Li Y, Zhang M, Luo G, Xue W, Xiao L, Li J, Chen W, Xu X, Yin Y, Yang H, Wang J, Kristiansen K, Liu L, Li T, Huang Q, Li Y, Wang J (2015) The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat Med 21(8):895–905PubMedCrossRef
193.
Chen J, Wright K, Davis JM, Jeraldo P, Marietta EV, Murray J, Nelson H, Matteson EL, Taneja V (2016) An expansion of rare lineage intestinal microbes characterizes rheumatoid arthritis. Genome Med 8(1):43PubMedPubMedCentralCrossRef
194.
Scher JU, Joshua V, Artacho A, Abdollahi-Roodsaz S, Öckinger J, Kullberg S, Sköld M, Eklund A, Grunewald J, Clemente JC, Ubeda C, Segal LN, Catrina AI (2016) The lung microbiota in early rheumatoid arthritis and autoimmunity. Microbiome 4(1):60PubMedPubMedCentralCrossRef
195.
Quirke AM, Perry E, Cartwright A, Kelly C, De Soyza A, Eggleton P, Hutchinson D, Venables PJ (2015) Bronchiectasis is a model for chronic bacterial infection inducing autoimmunity in rheumatoid arthritis. Arthritis Rheumatol 67(9):2335–2342PubMedPubMedCentralCrossRef
196.
Zaccardelli A, Liu X, Ford JA, Cui J, Lu B, Chu SH, Schur PH, Speyer CB, Costenbader KH, Robinson WH, Sokolove J, Karlson EW, Camargo CA Jr, Sparks JA (2019) Asthma and elevation of anti-citrullinated protein antibodies prior to the onset of rheumatoid arthritis. Arthritis Res Ther 21(1):246PubMedPubMedCentralCrossRef
197.
Symmons DP, Bankhead CR, Harrison BJ, Brennan P, Barrett EM, Scott DG, Silman AJ (1997) Blood transfusion, smoking, and obesity as risk factors for the development of rheumatoid arthritis: results from a primary care-based incident case-control study in Norfolk. England Arthritis Rheum 40(11):1955–1961PubMedCrossRef
198.
Klareskog L, Stolt P, Lundberg K, Kallberg H, Bengtsson C, Grunewald J, Ronnelid J, Harris HE, Ulfgren AK, Rantapaa-Dahlqvist S, Eklund A, Padyukov L, Alfredsson L (2006) A new model for an etiology of rheumatoid arthritis: smoking may trigger HLA-DR (shared epitope)-restricted immune reactions to autoantigens modified by citrullination. Arthritis Rheum 54(1):38–46PubMedCrossRef
199.
Reynisdottir G, Olsen H, Joshua V, Engstrom M, Forsslund H, Karimi R, Skold CM, Nyren S, Eklund A, Grunewald J, Catrina AI (2016) Signs of immune activation and local inflammation are present in the bronchial tissue of patients with untreated early rheumatoid arthritis. Ann Rheum Dis 75(9):1722–1727PubMedCrossRef
200.
Rangel-Moreno J, Hartson L, Navarro C, Gaxiola M, Selman M, Randall TD (2006) Inducible bronchus-associated lymphoid tissue (iBALT) in patients with pulmonary complications of rheumatoid arthritis. J Clin Invest 116(12):3183–3194PubMedPubMedCentralCrossRef
201.
Tong Y, Zheng L, Qing P, Zhao H, Li Y, Su L, Zhang Q, Zhao Y, Luo Y, Liu Y (2019) Oral microbiota perturbations are linked to high risk for rheumatoid arthritis. Front Cell Infect Microbiol 9:475PubMedCrossRef
202.
Moutsopoulos NM, Kling HM, Angelov N, Jin W, Palmer RJ, Nares S, Osorio M, Wahl SM (2012) Porphyromonas gingivalis promotes Th17 inducing pathways in chronic periodontitis. J Autoimmun 39(4):294–303PubMedPubMedCentralCrossRef
203.
Mikuls TR, Payne JB, Yu F, Thiele GM, Reynolds RJ, Cannon GW, Markt J, McGowan D, Kerr GS, Redman RS, Reimold A, Griffiths G, Beatty M, Gonzalez SM, Bergman DA, Hamilton BC 3rd, Erickson AR, Sokolove J, Robinson WH, Walker C, Chandad F, O’Dell JR (2014) Periodontitis and Porphyromonas gingivalis in patients with rheumatoid arthritis. Arthritis Rheumatol 66(5):1090–1100PubMedPubMedCentralCrossRef
204.
Quirke AM, Lugli EB, Wegner N, Hamilton BC, Charles P, Chowdhury M, Ytterberg AJ, Zubarev RA, Potempa J, Culshaw S, Guo Y, Fisher BA, Thiele G, Mikuls TR, Venables PJ (2014) Heightened immune response to autocitrullinated Porphyromonas gingivalis peptidylarginine deiminase: a potential mechanism for breaching immunologic tolerance in rheumatoid arthritis. Ann Rheum Dis 73(1):263–269PubMedCrossRef
205.
de Aquino SG, Abdollahi-Roodsaz S, Koenders MI, van de Loo FAJ, Pruijn GJM, Marijnissen RJ, Walgreen B, Helsen MM, van den Bersselaar LA, de Molon RS, Campos MJA, Cunha FQ, Cirelli JA, van den Berg WB (2014) Periodontal pathogens directly promote autoimmune experimental arthritis by inducing a TLR2- and IL-1–driven Th17 response. J Immunol 192(9):4103PubMedCrossRef
206.
Moen K, Brun JG, Valen M, Skartveit L, Eribe EK, Olsen I, Jonsson R (2006) Synovial inflammation in active rheumatoid arthritis and psoriatic arthritis facilitates trapping of a variety of oral bacterial DNAs. Clin Exp Rheumatol 24(6):656–663PubMed
207.
Martinez-Martinez RE, Abud-Mendoza C, Patino-Marin N, Rizo-Rodriguez JC, Little JW, Loyola-Rodriguez JP (2009) Detection of periodontal bacterial DNA in serum and synovial fluid in refractory rheumatoid arthritis patients. J Clin Periodontol 36(12):1004–1010PubMedCrossRef
208.
McDonald WI, Sears TA (1970) The effects of experimental demyelination on conduction in the central nervous system. Brain 93(3):583–598PubMedCrossRef
209.
Cua DJ, Sherlock J, Chen Y, Murphy CA, Joyce B, Seymour B, Lucian L, To W, Kwan S, Churakova T, Zurawski S, Wiekowski M, Lira SA, Gorman D, Kastelein RA, Sedgwick JD (2003) Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421(6924):744–748PubMedCrossRef
210.
Langrish CL, Chen Y, Blumenschein WM, Mattson J, Basham B, Sedgwick JD, McClanahan T, Kastelein RA, Cua DJ (2005) IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 201(2):233–240PubMedPubMedCentralCrossRef
211.
Van Langelaar J, van der Vuurst de Vries RM, Janssen M, Wierenga-Wolf AF, Spilt IM, Siepman TA, Dankers W, Verjans GM, De Vries HE, Lubberts E, Hintzen RQ (2018) T helper 17.1 cells associate with multiple sclerosis disease activity: perspectives for early intervention. Brain 141(5):1334–49
212.
Correale J, Fiol M, Gilmore W (2006) The risk of relapses in multiple sclerosis during systemic infections. Neurology 67(4):652–659PubMedCrossRef
213.
Odoardi F, Sie C, Streyl K, Ulaganathan VK, Schlager C, Lodygin D, Heckelsmiller K, Nietfeld W, Ellwart J, Klinkert WE, Lottaz C, Nosov M, Brinkmann V, Spang R, Lehrach H, Vingron M, Wekerle H, Flugel-Koch C, Flugel A (2012) T cells become licensed in the lung to enter the central nervous system. Nature 488(7413):675-9
214.
Glenn JD, Liu C, Whartenby KA (2019) Frontline Science: Induction of experimental autoimmune encephalomyelitis mobilizes Th17-promoting myeloid derived suppressor cells to the lung. J Leukoc Biol 105(5):829–841PubMedCrossRef
215.
Edwards SC, Higgins SC, Mills KHG (2015) Respiratory infection with a bacterial pathogen attenuates CNS autoimmunity through IL-10 induction. Brain Behav Immun 50:41–46PubMedCrossRef
216.
Kanayama M, Danzaki K, He Y-W, Shinohara ML (2016) Lung inflammation stalls Th17-cell migration en route to the central nervous system during the development of experimental autoimmune encephalomyelitis. Int Immunol 28(9):463–469PubMedPubMedCentralCrossRef
217.
Chu F, Shi M, Lang Y, Shen D, Jin T, Zhu J, Cui L (2018) Gut Microbiota in Multiple Sclerosis and Experimental Autoimmune Encephalomyelitis: Current Applications and Future Perspectives. Mediators Inflamm 2018:8168717PubMedPubMedCentralCrossRef
218.
Mirza A, Forbes JD, Zhu F, Bernstein CN, Van Domselaar G, Graham M, Waubant E, Tremlett H (2020) The multiple sclerosis gut microbiota: a systematic review. Mult Scler Relat Disord 37:101427
219.
220.
Huang W, Thomas B, Flynn RA, Gavzy SJ, Wu L, Kim SV, Hall JA, Miraldi ER, Ng CP, Rigo F, Meadows S, Montoya NR, Herrera NG, Domingos AI, Rastinejad F, Myers RM, Fuller-Pace FV, Bonneau R, Chang HY, Acuto O, Littman DR (2015) DDX5 and its associated lncRNA Rmrp modulate TH17 cell effector functions. Nature 528(7583):517–522PubMedPubMedCentralCrossRef
221.
Sanjurjo L, Aran G, Roher N, Valledor AF, Sarrias MR (2015) AIM/CD5L: a key protein in the control of immune homeostasis and inflammatory disease. J Leukoc Biol 98(2):173–184PubMedCrossRef
222.
Wang C, Yosef N, Gaublomme J, Wu C, Lee Y, Clish CB, Kaminski J, Xiao S, Meyer Zu Horste G, Pawlak M, Kishi Y, Joller N, Karwacz K, Zhu C, Ordovas-Montanes M, Madi A, Wortman I, Miyazaki T, Sobel RA, Park H, Regev A, Kuchroo VK (2015) CD5L/AIM regulates lipid biosynthesis and restrains Th17 cell pathogenicity. Cell 163(6):1413–27
Metadata
Title
The Airway Microbiome-IL-17 Axis: a Critical Regulator of Chronic Inflammatory Disease
Authors
Jenny M. Mannion
Rachel M. McLoughlin
Stephen J. Lalor
Publication date
11-03-2022
Publisher
Springer US
Published in
Clinical Reviews in Allergy & Immunology / Issue 2/2023
Print ISSN: 1080-0549
Electronic ISSN: 1559-0267
DOI
https://doi.org/10.1007/s12016-022-08928-y

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