Simvastatin suppresses airway IL-17 and upregulates IL-10 in patients with stable COPD

Chest

Volumn 148, Issue 5, 2015, Pages 1164-1176

  Maneechotesuwan, Kittipong ^a   Wongkajornsilp, Adisak ^a   Adcock, Ian M ^b   Barnes, Peter J ^b  

^a MAHIDOL UNIVERSITY   (Thailand)

^b NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 2 ADRENERGIC RECEPTOR STIMULATING AGENT; BIOLOGICAL MARKER; CORTICOSTEROID; CYTOKINE; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 22; INTERLEUKIN 6; INTERLEUKIN 8; KYNURENINE; MESSENGER RNA; MUSCARINIC RECEPTOR BLOCKING AGENT; PLACEBO; SIMVASTATIN; TRYPTOPHAN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; IL10 PROTEIN, HUMAN; IL17A PROTEIN, HUMAN; RNA;

AGED; ARTICLE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CHRONIC OBSTRUCTIVE LUNG DISEASE ASSESSMENT TEST; CLINICAL ARTICLE; CLINICAL ASSESSMENT; CONTROLLED STUDY; CROSSOVER PROCEDURE; DOUBLE BLIND PROCEDURE; ENZYME ACTIVITY; FORCED EXPIRATORY VOLUME; HUMAN; HUMAN CELL; INFLAMMATORY CELL; MACROPHAGE; NEUTROPHIL COUNT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL; RESPIRATORY TRACT INFLAMMATION; SCORING SYSTEM; SPUTUM CYTODIAGNOSIS; SYMPTOMATOLOGY; TH17 CELL; TREATMENT OUTCOME; UPREGULATION; BIOSYNTHESIS; FEMALE; GENE EXPRESSION REGULATION; GENETICS; LIQUID CHROMATOGRAPHY; MALE; METABOLISM; MIDDLE AGED; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPUTUM; VERY ELDERLY;

AGED; AGED, 80 AND OVER; CHROMATOGRAPHY, LIQUID; CROSS-OVER STUDIES; DOUBLE-BLIND METHOD; FEMALE; GENE EXPRESSION REGULATION; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; INTERLEUKIN-10; INTERLEUKIN-17; MALE; MIDDLE AGED; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; SIMVASTATIN; SPUTUM;

EID: 84941026547     PISSN: 00123692     EISSN: 19313543     Source Type: Journal    
DOI: 10.1378/chest.14-3138     Document Type: Article

References (70)

1. Caramori G, Adcock IM, Di Stefano A, Chung KF. Cytokine inhibition in the treatment of COPD. Int J Chron Obstruct Pulmon Dis. 2014; 9: 397-412.
2. Alcorn JF, Crowe CR, Kolls JK. TH17 cells in asthma and COPD. Annu Rev Physiol. 2010; 72: 495-516.
3. McAleer JP, Kolls JK. Directing traffic: IL-17 and IL-22 coordinate pulmonary immune defense. Immunol Rev. 2014; 260 (1): 129-144.
4. Kolls JK, Lindén A. Interleukin-17 family members and inflammation. Immunity. 2004; 21 (4): 467-476.
5. Chang Y, Al-Alwan L, Audusseau S, et al. Genetic deletion of IL-17A reduces cigarette smoke-induced inflammation and alveolar type II cell apoptosis. Am J Physiol Lung Cell Mol Physiol. 2014; 306 (2): L132-L143.
6. Doe C, Bafadhel M, Siddiqui S, et al. Expression of the T helper 17-associated cytokines IL-17A and IL-17F in asthma and COPD. Chest. 2010; 138(5): 1140-1147.
7. Chang Y, Nadigel J, Boulais N, et al. CD8 positive T cells express IL-17 in patients with chronic obstructive pulmonary disease. Respir Res. 2011; 12: 43.
8. Zhou L, Chong MM, Littman DR. Plasticity of CD4 1 T cell lineage differentiation. Immunity. 2009; 30 (5): 646-655.
9. Criado G, Simelyte E, Inglis JJ, Essex D, Williams RO. Indoleamine 2,3 dioxygenasemediated tryptophan catabolism regulates accumulation of Th 1/Th 17 cells in the joint in collagen-induced arthritis. Arthritis Rheum. 2009; 60 (5): 1342-1351.
10. Wang H, Ying H, Wang S, et al. Imbalance of peripheral blood Th 17 and Treg responses in patients with chronic obstructive pulmonary disease. Clin Respir J. 2015; 9 (3): 330-341.
11. Maneechotesuwan K, Kasetsinsombat K, Wongkajornsilp A, Barnes PJ. Decreased indoleamine 2,3-dioxygenase activity and IL-10/IL-17A ratio in patients with COPD. Thorax. 2013; 68 (4): 330-337.
12. Weitz-Schmidt G. Statins as antiinflammatory agents. Trends Pharmacol Sci. 2002; 23 (10): 482-486.
13. Munford RS. Statins and the acute-phase response. N Engl J Med. 2001; 344 (26): 2016-2018.
14. Sparrow CP, Burton CA, Hernandez M, et al. Simvastatin has anti-inflammatory and antiatherosclerotic activities independent of plasma cholesterol lowering. Arterioscler Thromb Vasc Biol. 2001; 21(1): 115-121.
15. Maneechotesuwan K, Kasetsinsombat K, Wamanuttajinda V, Wongkajornsilp A, Barnes PJ. Statins enhance the effects of corticosteroids on the balance between regulatory T cells and Th 17 cells. Clin Exp Allergy. 2013; 43 (2): 212-222.
16. Ulivieri C, Baldari CT. Statins: from cholesterol-lowering drugs to novel immunomodulators for the treatment of Th 17-mediated autoimmune diseases. Pharmacol Res. 2014; 88: 41-52.
17. Murphy DM, Forrest IA, Corris PA, et al. Simvastatin attenuates release of neutrophilic and remodeling factors from primary bronchial epithelial cells derived from stable lung transplant recipients. Am J Physiol Lung Cell Mol Physiol. 2008; 294 (3): L592-L599.
18. Davidson WJ, Verity WS, Traves SL, et al. effect of incremental exercise on airway and systemic inflammation in patients with COPD. J Appl Physiol (1985). 2012; 112(12): 2049-2056.
19. Pelegrino NR, Tanni SE, Amaral RA, Angeleli AY, Correa C, Godoy I. effects of active smoking on airway and systemic inflammation profiles in patients with chronic obstructive pulmonary disease. Am J Med Sci. 2013; 345 (6): 440-445.
20. Prachason T, Konhan K, Pongnarin P, et al. Activation of indoleamine 2,3-dioxygenase in patients with scrub typhus and its role in growth restriction of Orientia tsutsugamushi. P LoS Negl Trop Dis. 2012; 6 (7): e1731.
21. Cosio MG. Autoimmunity, T-cells and STAT-4 in the pathogenesis of chronic obstructive pulmonary disease. Eur Respir J. 2004; 24 (1): 3-5.
22. Agustí A, MacNee W, Donaldson K, Cosio M. Hypothesis: does COPD have an autoimmune component? Thorax. 2003; 58 (10): 832-834.
23. Di Stefano A, Caramori G, Capelli A, et al. STAT4 activation in smokers and patients with chronic obstructive pulmonary disease. Eur Respir J. 2004; 24 (1): 78-85.
24. Vargas-Rojas MI, Ramírez-Venegas A, Limón-Camacho L, Ochoa L, Hernández-Zenteno R, Sansores RH. Increase of Th 17 cells in peripheral blood of patients with chronic obstructive pulmonary disease. Respir Med. 2011; 105(11): 1648-1654.
25. Molet S, Hamid Q, Davoine F, et al. IL-17 is increased in asthmatic airways and induces human bronchial fibroblasts to produce cytokines. J Allergy Clin Immunol. 2001; 108 (3): 430-438.
26. Di Stefano A, Caramori G, Gnemmi I, et al. T helper type 17-related cytokine expression is increased in the bronchial mucosa of stable chronic obstructive pulmonary disease patients. Clin Exp Immunol. 2009; 157 (2): 316-324.
27. Sonnenberg GF, Nair MG, Kirn TJ, Zaph C, Fouser LA, Artis D. Pathological versus protective functions of IL-22 in airway inflammation are regulated by IL-17A. J Exp Med. 2010; 207 (6): 1293-1305.
28. Zhang X, Jin J, Peng X, Ramgolam VS, Markovic-Plese S. Simvastatin inhibits IL-17 secretion by targeting multiple IL-17-regulatory cytokines and by inhibiting the expression of IL-17 transcription factor RORC in CD4 1 lymphocytes. J Immunol. 2008; 180 (10): 6988-6996.
29. Zhang X, Tao Y, Troiani L, Markovic-Plese S. Simvastatin inhibits IFN regulatory factor 4 expression and Th 17 cell differentiation in CD4 1 T cells derived from patients with multiple sclerosis. J Immunol. 2011; 187 (6): 3431-3437.
30. Zhang X, Tao Y, Wang J, Garcia-Mata R, Markovic-Plese S. Simvastatin inhibits secretion of Th 17-polarizing cytokines and antigen presentation by DCs in patients with relapsing remitting multiple sclerosis. Eur J Immunol. 2013; 43 (1): 281-289.
31. Wang H, Peng W, Weng Y, et al. Imbalance of Th 17/Treg cells in mice with chronic cigarette smoke exposure. Int Immunopharmacol. 2012; 14 (4): 504-512.
32. Isajevs S, Taivans I, Strazda G, et al. Decreased FOXP3 expression in small airways of smokers with COPD. Eur Respir J. 2009; 33 (1): 61-67.
33. Freeman CM, McCubbrey AL, Crudgington S, et al. Basal gene expression by lung CD4 1 T cells in chronic obstructive pulmonary disease identifies independent molecular correlates of airflow obstruction and emphysema extent. PLoS ONE. 2014; 9 (5): e96421.
34. Soler N, Ewig S, Torres A, Filella X, Gonzalez J, Zaubet A. Airway inflammation and bronchial microbial patterns in patients with stable chronic obstructive pulmonary disease. Eur Respir J. 1999; 14 (5): 1015-1022.
35. Mezrich JD, Fechner JH, Zhang X, Johnson BP, Burlingham WJ, Bradfield CA. An interaction between kynurenine and the aryl hydrocarbon receptor can generate regulatory T cells. J Immunol. 2010; 185 (6): 3190-3198.
36. Julliard W, Fechner JH, Mezrich JD. The aryl hydrocarbon receptor meets immunology: friend or foe? A little of both. Front Immunol. 2014; 5: 458.
37. Fessler MB, Young SK, Jeyaseelan S, et al. A role for hydroxy-methylglutaryl coenzyme a reductase in pulmonary inflammation and host defense. Am J Respir Crit Care Med. 2005; 171 (6): 606-615.
38. Chen K, Pociask DA, McAleer JP, et al. IL-17RA is required for CCL2 expression, macrophage recruitment, and emphysema in response to cigarette smoke. PLoS ONE. 2011; 6 (5): e20333.
39. Hothersall EJ, Chaudhuri R, McSharry C, et al. effects of atorvastatin added to inhaled corticosteroids on lung function and sputum cell counts in atopic asthma. Thorax. 2008; 63 (12): 1070-1075.
40. Weathington NM, van Houwelingen AH, Noerager BD, et al. A novel peptide CXCR ligand derived from extracellular matrix degradation during airway inflammation. Nat Med. 2006; 12 (3): 317-323.
41. Braber S, Overbeek SA, Koelink PJ, et al. CXCR2 antagonists block the N-Ac-PGPinduced neutrophil influx in the airways of mice, but not the production of the chemokine CXCL1. Eur J Pharmacol. 2011; 668 (3): 443-449.
42. Pfister RR, Haddox JL, Sommers CI, Lam KW. Identification and synthesis of chemotactic tripeptides from alkalidegraded whole cornea. A study of N-acetyl-proline-glycine-proline and N-methyl-proline-glycine-proline. Invest Ophthalmol Vis Sci. 1995; 36(7): 1306-1316.
43. O'Reilly P, Jackson PL, Noerager B, et al. N-alpha-PGP and PGP, potential biomarkers and therapeutic targets for COPD. Respir Res. 2009; 10: 38.
44. Overbeek SA, Braber S, Koelink PJ, et al. Cigarette smoke-induced collagen destruction; key to chronic neutrophilic airway inflammation? PLoS ONE. 2013; 8 (1): e55612.
45. O'Reilly PJ, Jackson PL, Wells JM, Dransfield MT, Scanlon PD, Blalock JE. Sputum PGP is reduced by azithromycin treatment in patients with COPD and correlates with exacerbations. BMJ Open. 2013; 3 (12): e004140.
46. Albert RK, Connett J, Bailey WC, et al; COPD Clinical Research Network. Azithromycin for prevention of exacerbations of COPD. N Engl J Med. 2011; 365 (8): 689-698.
47. Zhou Q, Liao JK. Pleiotropic effects of statins.-Basic research and clinical perspectives-. Circ J. 2010; 74 (5): 818-826.
48. Young RP, Hopkins R, Eaton TE. Pharmacological actions of statins: potential utility in COPD. Eur Respir Rev. 2009; 18 (114): 222-232.
49. Bhowmik A, Seemungal TA, Sapsford RJ, Wedzicha JA. Relation of sputum inflammatory markers to symptoms and lung function changes in COPD exacerbations. Thorax. 2000; 55 (2): 114-120.
50. Tumkaya M, Atis S, Ozge C, Delialioglu N, Polat G, Kanik A. Relationship between airway colonization, inflammation and exacerbation frequency in COPD. Respir Med. 2007; 101 (4): 729-737.
51. Gessner C, Scheibe R, Wötzel M, et al. Exhaled breath condensate cytokine patterns in chronic obstructive pulmonary disease. Respir Med. 2005; 99 (10): 1229-1240.
52. Mancini GB, Etminan M, Zhang B, Levesque LE, FitzGerald JM, Brophy JM. Reduction of morbidity and mortality by statins, angiotensin-converting enzyme inhibitors, and angiotensin receptor blockers in patients with chronic obstructive pulmonary disease. J Am Coll Cardiol. 2006; 47 (12): 2554-2560.
53. Wang MT, Lo YW, Tsai CL, et al. Statin use and risk of COPD exacerbation requiring hospitalization. Am J Med. 2013;126: 598-606.e2.
54. Huang CC, Chan WL, Chen YC, et al. Statin use and hospitalization in patients with chronic obstructive pulmonary disease: a nationwide population-based cohort study in Taiwan. Clin Ther. 2011; 33 (10): 1365-1370.
55. Blamoun AI, Batty GN, DeBari VA, Rashid AO, Sheikh M, Khan MA. Statins may reduce episodes of exacerbation and the requirement for intubation in patients with COPD: evidence from a retrospective cohort study. Int J Clin Pract. 2008; 62 (9): 1373-1378.
56. Alexeeff SE, Litonjua AA, Sparrow D, Vokonas PS, Schwartz J. Statin use reduces decline in lung function: VA Normative Aging Study. Am J Respir Crit Care Med. 2007; 176 (8): 742-747.
57. Sichelstiel A, Yadava K, Trompette A, et al. Targeting IL-1 b and IL-17A driven inflammation during influenza-induced exacerbations of chronic lung inflammation. PLoS ONE. 2014; 9 (2): e98440.
58. Frost FJ, Petersen H, Tollestrup K, Skipper B. Influenza and COPD mortality protection as pleiotropic, dose-dependent effects of statins. Chest. 2007; 131 (4): 1006-1012.
59. Lawes CM, Thornley S, Young R, et al. Statin use in COPD patients is associated with a reduction in mortality: a national cohort study. Prim Care Respir J. 2012; 21 (1): 35-40.
60. Lahousse L, Loth DW, Joos GF, et al. Statins, systemic inflammation and risk of death in COPD: the Rotterdam study. Pulm Pharmacol Ther. 2013; 26 (2): 212-217.
61. Bartziokas K, Papaioannou AI, Minas M, et al. Statins and outcome after hospitalization for COPD exacerbation: a prospective study. Pulm Pharmacol Ther. 2011; 24 (5): 625-631.
62. Ingebrigtsen TS, Marott JL, Nordestgaard BG, Lange P, Hallas J, Vestbo J. Statin use and exacerbations in individuals with chronic obstructive pulmonary disease. Thorax. 2015; 70 (1): 33-40.
63. Criner GJ, Connett JE, Aaron SD, et al; COPD Clinical Research Network; Canadian Institutes of Health Research. Simvastatin for the prevention of exacerbations in moderate-to-severe COPD. N Engl J Med. 2014; 370 (23): 2201-2210.
64. Young RP, Hopkins RJ, Agusti A. Statins as adjunct therapy in COPD: how do we cope after STATCOPE? Thorax. 2014; 69 (10): 891-894.
65. Dahl M, Vestbo J, Lange P, Bojesen SE, Tybjaerg-Hansen A, Nordestgaard BG. C-reactive protein as a predictor of prognosis in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2007; 175 (3): 250-255.
66. Fabbri LM, Beghé B, Agusti A. Cardiovascular mechanisms of death in severe COPD exacerbation: time to think and act beyond guidelines. Thorax. 2011; 66 (9): 745-747.
67. Maclay JD, MacNee W. Cardiovascular disease in COPD: mechanisms. Chest. 2013; 143 (3): 798-807.
68. Sharif R, Parekh TM, Pierson KS, Kuo YF, Sharma G. Predictors of early readmission among patients 40 to 64 years of age hospitalized for chronic obstructive pulmonary disease. Ann Am Thorac Soc. 2014; 11 (5): 685-694.
69. Nishimura K, Nishimura T, Onishi K, Oga T, Hasegawa Y, Jones PW. Changes in plasma levels of B-type natriuretic peptide with acute exacerbations of chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis. 2014; 9: 155-162.
70. Calverley PM, Anderson JA, Celli B, et al; TORCH investigators. Salmeterol and fluticasone propionate and survival in chronic obstructive pulmonary disease. N Engl J Med. 2007; 356 (8): 775-789.