Probing cellular and molecular mechanisms of cigarette smoke-induced immune response in the progression of chronic obstructive pulmonary disease using multiscale network modeling

PLoS ONE

Volumn 11, Issue 9, 2016, Pages

  Pan, Zhichao ^a   Yu, Haishan ^a   Liao, Jie Lou ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CIGARETTE SMOKE;

ARTICLE; CHRONIC OBSTRUCTIVE LUNG DISEASE; DISEASE COURSE; DISEASE PREDISPOSITION; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; LUNG PARENCHYMA; MOLECULAR MECHANICS; POSITIVE FEEDBACK; SENSITIVITY ANALYSIS; SIMULATION; SMOKING CESSATION;

EID: 84991746970     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0163192     Document Type: Article

References (84)

1. Barnes PJ (2014) Cellular and molecular mechanisms of chronic obstructive pulmonary disease. Clin Chest Med 35:71-86. doi: 10.1016/j.ccm.2013.10.004 PMID: 24507838
2. Faner R, Cruz T, Agusti A (2013) Immune response in chronic obstructive pulmonary disease. Expert Rev Clin Immunol 9: 821-833. doi: 10.1586/1744666X.2013.828875 PMID: 24070046
3. Cosio MG, Saetta M, Agusti A (2009) Immunologic aspects of chronic obstructive pulmonary disease. N Eng J Med 360: 2445-2454.
4. Rennard SI, Drummond MB (2015) Early chronic obstructive pulmonary disease: definition, assessment, and prevention. Lancet 385:1778-1788. doi: 10.1016/S0140-6736(15)60647-X PMID: 25943942
5. Houghton AM (2013) Mechanistic links between COPD and lung cancer. Nat Rev Cancer 13:233-245. doi: 10.1038/nrc3477 PMID: 23467302
6. Barnes PJ (2013) New anti-inflammatory targets for chronic obstructive pulmonary disease. Nat Rev Drug Discov 12: 543-559. PMID: 23977698
7. Brusselle GG, Joos GF, Bracke KR (2011) New insights into the immunology of chronic obstructive pulmonary disease. Lancet 378:1015-1026. doi: 10.1016/S0140-6736(11)60988-4 PMID: 21907865
8. Young RP, Hopkins R, Black PN, Eddy C, Wu L, Gamble G. D. et al. (2006) Functional variants of antioxidant genes in smokers with COPD and in those with normal lung function. Thorax 61: 394-399. PMID: 16467073
9. Bossé Y (2012) Updates on the COPD gene list. Int J Chron Obstruct Pulmon Dis 7: 607-631. doi: 10. 2147/COPD.S35294 PMID: 23055711
10. Barjaktarevic IZ, Arredondo AF, Cooper CB (2015) Positioning new pharmacotherapies for COPD. Int J Chron Obstruct Pulmon Dis 10:1427-1442. doi: 10.2147/COPD.S83758 PMID: 26244017
11. Dewar M, Curry RW Jr (2006) Chronic obstructive pulmonary disease diagnostic considerations. Am Fam Physician 73: 669-676. PMID: 16506711
12. Stampfli MR, Anderson GP (2009) How cigarette smoke skews immune responses to promote infection, lung disease and cancer. Nat Rev Immunol 9: 377-384. doi: 10.1038/nri2530 PMID: 19330016
13. Shaw JG, Vaughan A, Dent AG, O'Hare PE, Goh F, Rayleen V. et al. (2014) Biomarkers of progression of chronic obstructive pulmonary disease (COPD). J Thorac Dis 6:1532-1547. doi: 10.3978/j.issn.2072-1439.2014.11.33 PMID: 25478195
14. Caramori G, Adcock IM, Stefano AD, Chung KF (2014) Cytokine inhibition in the treatment of COPD. Int J Chron Obstruct Pulmon Dis 9: 397-412. doi: 10.2147/COPD.S42544 PMID: 24812504
15. Celli BR, Locantore N, Yates J, Tal-Singer R., Miller BE, Bakke P, et al. (2012) Inflammatory biomarkers improve clinical prediction of mortality in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 185:1065-1072. doi: 10.1164/rccm.201110-1792OC PMID: 22427534
16. Agusti A, Edwards LD, Rennard SI, MacNee W, Tal-Singer R, Miller BE, et al. (2012) Persistent systemic inflammation is associated with poor clinical outcomes in COPD: A novel phenotype. PLos One 7: e37483. doi: 10.1371/journal.pone.0037483 PMID: 22624038
17. Agusti A, Gea J, Faner R (2016) Biomarkers, the control panel and personalized COPD medicine. Respirology 21: 24-33. doi: 10.1111/resp.12585
18. Dentener MA, Creutzberg EC, Pennings H-J, Rijkers GT, Mercken E, Wouters EFM (2008) Effect of infliximab on local and systemic inflammation in chronic obstructive pulmonary disease: a pilot study. Respiration 76: 275-82. doi: 10.1159/000117386 PMID: 18277064
19. Matera MG, Calzetta L, Cazzola M (2010) TNF-α inhibitors in asthma and COPD: We must not throw the baby out with the bathwater. Pulm Pharmacol Ther 23:121-128. doi: 10.1016/j.pupt.2009.10.007 PMID: 19853667
20. Holloway RA, Donnelly LE (2013) Immunopathogenesis of chronic obstructive pulmonary disease. Curr Opin Pulm Med 19: 95-102. doi: 10.1097/MCP.0b013e32835cfff5 PMID: 23325031
21. Hussell T, Bell TJ (2014) Alveolar macrophages: plasticity in a tissue-specific context. Nat Rev Immunol 14: 81-93. doi: 10.1038/nri3600 PMID: 24445666
22. Barnes PJ (2009) The cytokine network in chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol 41: 631-638. doi: 10.1165/rcmb.2009-0220TR PMID: 19717810
23. Boorsma CE, Draijer C, Melgert BN (2013) Macrophage heterogeneity in respiratory diseases. Mediat Inflamm 2103:1-19.
24. Hautamaki RD, Kobayashi DK, Senior RM, Shapiro SD (1997) Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice. Science 277: 2002-2004. PMID: 9302297
25. Ofulue AF, Ko M (1999) Effects of depletion of neutrophils or macrophages on development of cigarette smoke-induced emphysema. Am J Physiol Lung Cell Mol Physiol 277: L97-L105.
26. Mosser DM, Edwards JP (2008) Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8: 958-969. doi: 10.1038/nri2448 PMID: 19029990
27. Houghton AM, Quintero PA, Perkins DL, Kobayashi DK, Kelley DG, Marconcini LA, et al. (2006) Elastin fragments drive disease progression in a murine model of emphysema. J Clin Investi 116: 753-759.
28. Brandt E, Woerly G, Younes AB, Loiseau S, Capron M (2000) IL-4 production by human polymorphonuclear neutrophils. J Leukoc Biol 68:125-130. PMID: 10914499
29. Konigshoff M, Kneidinger N, Eickelberg O (2009) TGF-β signalling in COPD: deciphering genetic and cellular susceptibilities for future therapeutic regimens. Swiss Med WKLY 139:554-563. PMID: 19838873
30. Stoll P, Ulrich M, Bratke K, Garbe K, Virchow JC, Lommatzsch M (2015) Imbalance of dendritic cell costimulation in COPD. Respiratory Res 16:19. doi: 10.1186/s12931-015-0174-x
31. Van Pottelberge GR, Bracke KR, Demedts IK, Rijck KD, Reinartz SM, van Drunen CM, et al. (2010) Selective accumulation of langerhans-type dendritic cells in small airways of patients with COPD. RespirRes 11:35. doi: 10.1186/1465-9921-11-35 PMID: 20307269
32. Torres-Aguilar H, Blank M, Jara LJ, Shoenfeld Y (2010) Tolerogenic dendritic cells in autoimmune diseases: crucial players in induction and prevention of autoimmunity. Autoimmun Rev 10: 8-17. doi: 10. 1016/j.autrev.2010.07.015 PMID: 20678591
33. Barnes PJ (2008) The cytokine network in asthma and chronic obstructive pulmonary disease. J Clin Invest 118: 3546-3556. doi: 10.1172/JCI36130 PMID: 18982161
34. Trinchieri G, Pflanz S, Kastelein RA (2003) The IL-12 family of heterodimeric cytokines: new players in the regulation of T cell responses. Immunity 19: 641-644. PMID: 14614851
35. Milich DR, Wolf SF, Hughes JL, Jones JE (1995) Interleukin 12 suppresses autoantibody production by reversing helper T-cell phenotype in hepatitis B antigen transgenic mice. Proc Natl Acad Sci USA 92: 6847-6851. PMID: 7624330
36. Wan YY, Flavell RA (2007) Regulatory T cells, transforming growth factor-β, and immune suppression. Proc Am Thorac Soc 4: 271-276. PMID: 17607012
37. Barnes PJ (2008) Immunology of asthma and chronic obstructive pulmonary disease. Nat Rev Immunol 8:183-192. doi: 10.1038/nri2254 PMID: 18274560
38. Kimura A, Kishimoto T (2010) IL-6: Regulator of Treg/Th17 balance. Eur J Immunol 40: 2830-2835.
39. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Mukka M, et al (2006) Reciprocal developmental pathways for the generation of pathogenic effector Th17 and regulatory T cells. Nature 441: 235-238. PMID: 16648838
40. Mangan PR, Harrington LE, O'Quinn DB, Helms WS, Bullard DC, Elson CO, et al. (2006) Transforming growth factor-beta induces development of the Th-17 lineage. Nature 441:231-234. PMID: 16648837
41. Ogura H., Murakami M, Okuyama Y, Tsuruoka M, Kitabayashi C. Kanamoto M. et al. (2008) Interleukin-17 promotes autoimmunity by triggering a positive-feedback loop via interleukin-6 induction. Immunity 29: 628-636. doi: 10.1016/j.immuni.2008.07.018 PMID: 18848474
42. Duan MC, Huang Y, Zhong XN, Tang HJ (2012) Th17 cell enhances CD8 T-cell cytotoxicity via IL-21 production in emphysema mice. Mediat Inflamm 2012:1-12.
43. Fujimoto M, Nakano M, Terabe F, Kawahata H. Ohkawara T. Han Y, et al (2011) The influence of excessive IL-6 production in vivo on the development and function of Foxp3+ regulatory T cells. J Immunol 186: 32-40. doi: 10.4049/jimmunol.0903314 PMID: 21106853
44. Alon U. (2007) An introduction to systems biology: Design principles of biological circuits, Vol. 10. Chapman & Hall/CRC, London.
45. Tian XJ, Zhang H, Xing J (2013) Coupled reversible and irreversible bistable switches underlying TGFβ-induced epithelial to mesenchymal transition. Biophys J 105:1079-1089. doi: 10.1016/j.bpj.2013.07.011 PMID: 23972859
46. Saetta M, Shiner RJ, Angus GE, Kim WD, Wang NS, King M, et al. (1985) Destructive index: a measurement of lung parenchymal destruction in smokers. Am Rev Respir Dis 131:764-769. PMID: 4003921
47. D'hulst AI, Vermaelen KY, Brusselle GG, Joos GF, Pauwels RA (2005) Time course of cigarette smoke-induced pulmonary inflammation in mice. Eur Respir J 26: 204-213. PMID: 16055867
48. Robbesom AA, Koenders MMJF, Smits NC, Hafmans T, Versteeg EMM, Bulten J, et al. (2008) Aberrant fibrillin-1 expression in early emphysematous human lung: a proposed predisposition for emphysema. Modern Pathol 21: 297-307.
49. Day J, Friedman A, Schlesinger LS (2009) Modeling the immune rheostat of macrophages in the lung in response to infection. Proc Natl Acad Sci USA 106:11246-11251. doi: 10.1073/pnas.0904846106 PMID: 19549875
50. Katakura T, Miyazaki M, Kobayashi M, Herndon DN, Suzuki F. (2004) CCL17 and IL-10 as effectors that enable alternatively activated macrophages to inhibit the generation of classically activated macrophages. J. Immunol. 172:1407-1413. PMID: 14734716
51. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A (2001) Interleukin-10 and the receptor. Annu Rev Immunol 19:683-765. PMID: 11244051
52. Saraiva M, O'Garra A (2010) The regulation of IL-10 production by immune cells. Nat Rev Immunol 10:170-181. doi: 10.1038/nri2711 PMID: 20154735
53. Marino S, Hogue IB, Ray CJ, Kirschner DE (2008) A methodology for performing global uncertainty and sensitivity analysis in systems biology. J Theor Biol 254:178-196. doi: 10.1016/j.jtbi.2008.04.011 PMID: 18572196
54. Kuschner WG, D'Alessandro A, Wong H, Blanc PD (1996) Dose-dependent cigarette smoking-related inflammatory response in healthy adults. Eur Respir J 9:1989-1994. PMID: 8902455
55. Hacievliyagil SS, Gunen H, Temel I (2006) Association between cytokines in induced sputum and severity of chronic obstructive pulmonary disease. Respir Med 100:846-854. PMID: 16214322
56. Domagała-Kulawik J, Kraszewska I, Chazan R (2003) The cellular composition and macrophage phenotype in induced sputum in smokers and ex-Smokers with COPD. CHEST, 123:1054-1059. PMID: 12684293
57. Kunz LIZ, Lapperre TS, Snoeck-Stroband JB, Budulac SE, Timens W, van Wijngaarden S, et al (2011) Smoking status and anti-inflammatory macrophages in bronchoalveolar lavage and induced sputum in COPD. Respira Res 12: 34.
58. 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: 459-465. doi: 10. 3109/15412555.2013.770456 PMID: 23537276
59. + T cells contribute to effector T-cell dysfunction in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 190: 40-50. doi: 10.1164/rccm.201312-2293OC PMID: 24825462
60. Kim V, Cornwell WD, Oros M, Durra H, Criner GH, Rogers TJ (2015) Plasma chemokine signature correlates with lung goblet cell hyperplasia in smokers with and without chronic obstructive pulmonary disease. BMC Pulm Med 15:111. doi: 10.1186/s12890-015-0103-2 PMID: 26424214
61. Yerkovich ST, Hales BJ, Carroll ML, Burel JG, Towers MA, Smith DJ, et al (2012) Reduced rhinovirusspecific antibodies are associated with acute exacerbations of chronic obstructive pulmonary disease requiring hospitalization. BMC Pulm Med 12:37. doi: 10.1186/1471-2466-12-37 PMID: 22849333
62. + cells in peripheral blood of patients with COPD. Respir Med 101:1338-1343. PMID: 17118637
63. Vargas-Rojas MI, Ramirez-Venegas A, Limón-Camacho L, Ochoa L, Hernandez-Zenteno R, Sansores RH (2011) Increase of Th17 cells in peripheral blood of patients with chronic obstructive pulmonary disease. Respir Med 105:1648-1654. doi: 10.1016/j.rmed.2011.05.017 PMID: 21763119
64. Stoll P, Heinz AS, Bratke K, Bier A, Garbe K, Kuepper M, et al. (2014) Impact of smoking on dendritic cell phenotypes in the airway lumen of patients with COPD. Resp Res 15:48.
65. Godtfredsen NS, Lam TH, Hansel TT, Leon ME, Gray N, Dresler C et al. (2008) COPD-related morbidity and mortality after smoking cessation: status of the evidence. Eur Respir J 32: 844-853. doi: 10. 1183/09031936.00160007 PMID: 18827152
66. Braber S, Henricks PAJ, Nijkamp FP, Kraneveld AD, Folkerts G (2010) Inflammatory changes in the airways of mice caused by cigarette smoke exposure are only partially reversed after smoking cessation. Resp Res 11: 99-110.
67. Janciauskiene SM, Bals R, Koczulla R, Vogelmeier C, Köhnlein T, Welte T (2011) The discovery of α-1 antitrypsin and its role in health and disease. Respir Med 105:1129-1139. doi: 10.1016/j.rmed.2011.02.002 PMID: 21367592
68. Shapiro SD, Goldstein NM, Houghton AM, Kobayashi DK, Kelley D, Belaaouaj A (2003) Neutrophil elastase contributes to cigarette smoke-induced emphysema in mice. Amer J Pathol 163: 2329-2335.
69. Wigginton JE, Kirschner D (2001) A model to predict cell-mediated immune regulatory mechanisms during human infection with Mycobacterium tuberculosis. Immunol 166:1951-1967.
70. Chen K, Pociask DA, McAleer JP, Chan YR, Alcorn JF, Kreindler JL, et al (2011) IL-17RA is required for CCL2 expression, macrophage recruitment, and emphysema in response to cigarette smoke. PLoS ONE 6(5): e20333. doi: 10.1371/journal.pone.0020333 PMID: 21647421
71. +T cells are required for inflammation and destruction in cigarette smoke-induced emphysema in mice. J Immunol 178: 8090-8096. PMID: 17548647
72. Woodruff PG, Agusti A, Roche AN, Singh D, Martinez FJ (2015) Current concepts in targeting chronic obstructive pulmonary disease pharmacotherapy: making progress towards personalized management. Lancet 385:1789-1798. doi: 10.1016/S0140-6736(15)60693-6 PMID: 25943943
73. Neurath MF, Finotto S (2011) IL-6 signaling in autoimmunity, chronic inflammation and inflammation-associated cancer. Cytokine Growth Factor Rev 22: 83-89. doi: 10.1016/j.cytogfr.2011.02.003 PMID: 21377916
74. Tanaka T, Narazaki M, Ogata A, Kishimoto T (2014) A new era for the treatment of inflammatory autoimmune diseases by interleukin-6 blockade strategy. Semin Immunol 26: 88-96. doi: 10.1016/j.smim.2014.01.009 PMID: 24594001
75. H17 cells in chronic inflammation. Nat Rev Drug Disc 11:763-776.
76. Cox LA Jr (2011) A causal model of chronic obstructive pulmonary disease (COPD) risk. Risk Analysis 31: 38-62. doi: 10.1111/j.1539-6924.2010.01487.x PMID: 20846171
77. Cox LA Jr (2009) A mathematical model of protease-antiprotease homeostasis failure in chronic obstructive pulmonary disease (COPD). Risk Analysis 4: 576-586.
78. Mannino DM, Buist AS (2007) Global burden of COPD: risk factors, prevalence, and future trends. Lancet 370: 765-773. PMID: 17765526
79. Wedzicha JA, Seemungal TAR (2007) COPD exacerbations: defining their cause and prevention. Lancet 370: 786-796. PMID: 17765528
80. Suki B, Sato S, Parameswaran H, Szabari MV, Takahashi A, Bartolak-Suki E (2013) Emphysema and mechanical stress-induced lung remodeling. Physiology 28: 404-413. doi: 10.1152/physiol.00041.2013 PMID: 24186935
81. Houghton AM (2013) Mechanistic links between COPD and lung cancer. Nat Rev Cancer 13: 233-245. doi: 10.1038/nrc3477 PMID: 23467302
82. Goldkorn T, Filosto S, Chung S (2014) Lung injury and lung cancer caused by cigarette smoke-induced oxidative stress: molecular mechanisms and therapeutic opportunities involving the ceramide-generating machinery and epidermal growth factor receptor. Antioxid Redox Sign 21: 2149-2174.
83. Houghton AM, Shapiro SD. Inflammation and lung cancer: The relationship to chronic obstructive pulmonary disease. In: Dubinett SM, editor. Inflammation and lung cancer. Springer; 2015. pp. 1-22.
84. Bozinovski S, Vlahos R, Anthony D, McQualter J, Anderson G, Irving L, et al. (2016) COPD and squamous cell lung cancer: aberrant inflammation and immunity is the common link. British Journal of Pharmacology 173: 635-648. doi: 10.1111/bph.13198 PMID: 26013585