Effects of conventional tobacco smoke and nicotine-free cigarette smoke on airway inflammation, airway remodelling and lung function in a triple allergen model of severe asthma

Clinical and Experimental Allergy

Volumn 46, Issue 7, 2016, Pages 957-972

  Tilp, C ^a   Bucher, H ^a   Haas, H ^a   Duechs, M J ^a   Wex, E ^a   Erb, K J ^a  

^a BOEHRINGER INGELHEIM PHARMA GMBH AND CO KG   (Germany)

Author keywords

anti inflammatory properties; cigarette smoke; nicotine; severe asthma; TLR 4

Indexed keywords

ALLERGEN; ALUMINUM POTASSIUM SULFATE; CIGARETTE SMOKE; COLLAGEN TYPE 1; HOUSE DUST ALLERGEN; IMMUNOGLOBULIN E; INTERLEUKIN 4; INTERLEUKIN 5; NICOTINE; OVALBUMIN; TOBACCO CIGARETTE SMOKE; TOBACCO SMOKE; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

AIRWAY REMODELING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; COCKROACH; CONTROLLED STUDY; EOSINOPHIL COUNT; EXPOSURE; FEMALE; IMMUNOGLOBULIN BLOOD LEVEL; LUNG FUNCTION; MOUSE; MOUSE MODEL; NIPPOSTRONGYLUS BRASILIENSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RESPIRATORY TRACT ALLERGY; SENSITIZATION; SIGNAL TRANSDUCTION; SPLEEN CELL; TH2 CELL;

EID: 84976494611     PISSN: 09547894     EISSN: 13652222     Source Type: Journal    
DOI: 10.1111/cea.12665     Document Type: Article

References (64)

1. Wenzel S. Severe asthma: from characteristics to phenotypes to endotypes. Clin Exp Allergy 2012; 42:650–8.
2. Chung KF, Wenzel SE, Brozek JL et al. International ERS/ATS guidelines on definition, evaluation and treatment of severe asthma. Eur Respir J 2013; 00:erj02020-2013.
3. Hjern A, Hedberg A, Haglund B, Rosen M. Does tobacco smoke prevent atopic disorders? A study of two generations of Swedish residents. Clin Exp Allergy 2001; 31:908–14.
4. Meghji Z, Dua B, Watson RM, Gauvreau GM, O'Byrne PM. Allergen inhalation challenge in smoking compared with non-smoking asthmatic subjects. Clin Exp Allergy 2011; 41:1084–90.
5. Troisi RJ, Speizer FE, Rosner B, Trichopoulos D, Willett WC. Cigarette smoking and incidence of chronic bronchitis and asthma in women. CHEST J 1995; 108:1557–61.
6. Jarvis D, Chinn S, Luczynska C, Burney P. The association of smoking with sensitization to common environmental allergens: results from the European Community Respiratory Health Survey. J Allergy Clin Immunol 1999; 104:934–40.
7. Polosa R, Thomson NC. Smoking and asthma: dangerous liaisons. Eur Respir J 2013; 41:716–26.
8. Siroux VIMN, Pin I, Oryszczyn MP, Le Moual N, Kauffmann F. Relationships of active smoking to asthma and asthma severity in the EGEA Study. Epidemiological study on the Genetics and Environment of Asthma. Eur Respir J 2000; 15:470–7.
9. Stapleton M, Howard-Thompson A, George C, Hoover RM, Self TH. Smoking and asthma. J Am Board Fam Med 2011; 24:313–22.
10. Nagasaki T, Matsumoto H. Influences of smoking and aging on allergic airway inflammation in asthma. Allergol Int 2013; 62:171–9.
11. Peters JM, Avol E, Navidi W et al. A, study of twelve Southern California communities with differing levels and types of air pollution: I. Prevalence of respiratory morbidity. Am J Respir Crit Care Med 1999; 159:760–7.
12. Price D, Bjermer L, Popov TA, Chisholm A. Integrating evidence for managing asthma in patients who smoke. Allergy Asthma Immunol Res 2014; 6:114–20.
13. Wenzel SE. Asthma phenotypes: the evolution from clinical to molecular approaches. Nat Med 2012; 18:716–25.
14. Barnes PJ. Corticosteroid resistance in patients with asthma and chronic obstructive pulmonary disease. J Allergy Clin Immunol 2013; 131:636–45.
15. Kim DY, Kwon EY, Hong GU, Lee YS, Lee SH, Ro JY. Cigarette Smoke exacerbates mouse allergic asthma through Smad proteins expressed in mast cells. Respir Res 2011; 12:49.
16. Lanckacker EA, Tournoy KG, Hammad H et al. Short cigarette smoke exposure facilitates sensitisation and asthma development in mice. Eur Respir J 2013; 41:1189–99.
17. Moerloose KB, Pauwels RA, Joos GF. Short-term cigarette smoke exposure enhances allergic airway inflammation in mice. Am J Respir Crit Care Med 2005; 172:168–72.
18. Song DJ, Min MG, Miller M, Cho JY, Yum HY, Broide DH. Toll-like receptor-9 agonist inhibits airway inflammation, remodeling and hyperreactivity in mice exposed to chronic environmental tobacco smoke and allergen. Int Arch Allergy Immunol 2009; 151:285–96.
19. Van Hove CL, Moerloose K, Maes T, Joos GF, Tournoy KG. Cigarette smoke enhances Th-2 driven airway inflammation and delays inhalational tolerance. Respir Res 2008; 9:42–8.
20. Botelho FM, Llop-Guevara A, Trimble NJ et al. Cigarette smoke differentially affects eosinophilia and remodeling in a model of house dust mite asthma. Am J Respir Cell Mol Biol 2011; 45:753–60.
21. Hizume DC, Toledo AC, Moriya HT et al. Cigarette smoke dissociates inflammation and lung remodeling in OVA-sensitized and challenged mice. Respir Physiol Neurobiol 2012; 181:167–76.
22. Thatcher TH, Benson RP, Phipps RP, Sime PJ. High-dose but not low-dose mainstream cigarette smoke suppresses allergic airway inflammation by inhibiting T cell function. Am J Physiol Lung Cell Mol Physiol 2008; 295:L412–21.
23. Trimble NJ, Botelho FM, Bauer CM, Fattouh R, Stampfli MR. Adjuvant and anti-inflammatory properties of cigarette smoke in murine allergic airway inflammation. Am J Respir Cell Mol Biol 2009; 40:38–46.
24. Melgert BN, Postma DS, Geerlings M et al. Short-term smoke exposure attenuates ovalbumin-induced airway inflammation in allergic mice. Am J Respir Cell Mol Biol 2004; 30:880–5.
25. Mortaz E, Folkerts G, Engels F, Nijkamp FP, Redegeld FA. Cigarette smoke suppresses in vitro allergic activation of mouse mast cells. Clin Exp Allergy 2009; 39:679–87.
26. Yamamoto T, Kodama T, Lee J et al. Anti-allergic role of cholinergic neuronal pathway via alpha 7 nicotinic ACh receptors on mucosal mast cells in a murine food allergy model. PLoS ONE 2014; 9:e85888.
27. Melgert BN, Timens W, Kerstjens HA et al. Effects of 4 months of smoking in mice with ovalbumin-induced airway inflammation. Clin Exp Allergy 2007; 37:1798–808.
28. Duechs MJ, Tilp C, Tomsic C, Gantner F, Erb KJ. Development of a novel severe triple allergen asthma model in mice which is resistant to dexamethasone and partially resistant to TLR7 and TLR9 agonist treatment. PLoS ONE 2014; 9:e91223.
29. Schymeinsky J, Mayer H, Tomsic C et al. The absence of Mrp4 has No effect on the recruitment of neutrophils and eosinophils into the lung after LPS, cigarette smoke or allergen challenge. PLoS ONE 2013; 8:e61193.
30. Wohlleben G, Trujillo C, Müller J et al. Helminth infection modulates the development of allergen-induced airway inflammation. Int Immunol 2004; 16:585–96.
31. Pichavant M, Goya S, Hamelmann E, Gelfand EW, Umetsu DT. Animal models of airway sensitization. Curr Protoc Immunol 2007; 79:15–8.
32. Arnson Y, Shoenfeld Y, Amital H. Effects of tobacco smoke on immunity, inflammation and autoimmunity. J Autoimmun 2010; 34:J258–65.
33. Mishra NC, Langley RJ, Singh SP et al. Nicotine primarily suppresses lung Th2 but not goblet cell and muscle cell responses to allergens. J Immunol 2008; 180:7655–63.
34. Streck E, Jörres RA, Huber RM, Bergner A. Effects of cigarette smoke extract and nicotine on bronchial tone and acetylcholine-induced airway contraction in mouse lung slices. J Investig Allergol Clin Immunol 2010; 20:324.
35. AlSharari SD, Akbarali HI, Abdullah RA et al. Novel insights on the effect of nicotine in a murine colitis model. J Pharmacol Exp Ther 2013; 344:207–17.
36. Matta SG, Balfour DJ, Benowitz NL et al. Guidelines on nicotine dose selection for in vivo research. Psychopharmacology 2007; 190:269–319.
37. Eisner MD, Klein J, Hammond SK, Koren G, Lactao G, Iribarren C. Directly measured second hand smoke exposure and asthma health outcomes. Thorax 2005; 60:814–21.
38. Mackay D, Haw S, Ayres JG, Fischbacher C, Pell JP. Smoke-free legislation and hospitalizations for childhood asthma. N Engl J Med 2010; 363:1139–45.
39. Nagasaki T, Matsumoto H, Nakaji H et al. Smoking attenuates the age-related decrease in IgE levels and maintains eosinophilic inflammation. Clin Exp Allergy 2013; 43:608–15.
40. Thomson NC, Chaudhuri R, Livingston E. Asthma and cigarette smoking. Eur Respir J 2004; 24:822–33.
41. Min MG, Song DJ, Miller M et al. Coexposure to environmental tobacco smoke increases levels of allergen-induced airway remodeling in mice. J Immunol 2007; 178:5321–8.
42. Blümer N, Herz U, Wegmann M, Renz H. Prenatal lipopolysaccharide-exposure prevents allergic sensitization and airway inflammation, but not airway responsiveness in a murine model of experimental asthma. Clin Exp Allergy 2005; 35:397–402.
43. Duechs MJ, Hahn C, Benediktus E et al. TLR agonist mediated suppression of allergic responses is associated with increased innate inflammation in the airways. Pulm Pharmacol Ther 2011; 24:203–14.
44. Hollingsworth JW, Whitehead GS, Lin KL et al. TLR4 signaling attenuates ongoing allergic inflammation. J Immunol 2006; 176:5856–62.
45. Rodriguez D, Keller AC, Faquim-Mauro EL et al. Bacterial lipopolysaccharide signaling through toll-like receptor 4 suppresses asthma-like responses via nitric oxide synthase 2 activity. J Immunol 2003; 171:1001–8.
46. Hasday JD, Bascom R, Costa JJ, Fitzgerald T, Dubin W. Bacterial endotoxin is an active component of cigarette smoke. CHEST J 1999; 115:829–35.
47. Mills CM, Hill SA, Marks R. Transdermal nicotine suppresses cutaneous inflammation. Arch Dermatol 1997; 133:823–5.
48. Razani-Boroujerdi S, Singh SP, Knall C et al. Chronic nicotine inhibits inflammation and promotes influenza infection. Cell Immunol 2004; 230:1–9.
49. Sopori M. Effects of cigarette smoke on the immune system. Nat Rev Immunol 2002; 2:372–7.
50. Sopori ML, Kozak W. Immunomodulatory effects of cigarette smoke. J Neuroimmunol 1998; 83:148–56.
51. Ulloa L. The vagus nerve and the nicotinic anti-inflammatory pathway. Nat Rev Drug Discovery 2005; 4:673–84.
52. Xu Y, Li H, Bajrami B et al. Cigarette smoke (CS) and nicotine delay neutrophil spontaneous death via suppressing production of diphosphoinositol pentakisphosphate. Proc Natl Acad Sci 2013; 110:7726–31.
53. Iho S, Tanaka Y, Takauji R et al. Nicotine induces human neutrophils to produce IL-8 through the generation of peroxynitrite and subsequent activation of NF-KB. J Leukoc Biol 2003; 74:942–51.
54. Maes T, Provoost S, Lanckacker EA et al. Mouse models to unravel the role of inhaled pollutants on allergic sensitization and airway inflammation. Respir Res 2010; 11:1–16.
55. Spiess PC, Kasahara D, Habibovic A et al. Acrolein exposure suppresses antigen-induced pulmonary inflammation. Respir Res 2013; 14:107.
56. Ameredes BT, Otterbein LE, Kohut LK, Gligonic AL, Calhoun WJ, Choi AM. Low-dose carbon monoxide reduces airway hyperresponsiveness in mice. Am J Physiol Lung Cell Mol Physiol 2003; 285:L1270–6.
57. Motterlini R. Carbon monoxide-releasing molecules (CO-RMs): vasodilatory, anti-ischaemic and anti-inflammatory activities. Biochem Soc Trans 2007; 35:1142–6.
58. Otterbein LE, Bach FH, Alam J et al. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 2000; 6:422–8.
59. Otterbein LE. Carbon monoxide: innovative anti-inflammatory properties of an age-old gas molecule. Antioxid Redox Signal 2002; 4:309–19.
60. Van der Vaart H, Postma DS, Timens W, Ten Hacken NHT. Acute effects of cigarette smoke on inflammation and oxidative stress: a review. Thorax 2004; 59:713–21.
61. Kostikas K, Papatheodorou G, Psathakis K, Panagou P, Loukides S. Prostaglandin E2 in the expired breath condensate of patients with asthma. Eur Respir J 2003; 22:743–7.
62. Gauvreau GM, Watson RM, O'Byrne PM. Protective effects of inhaled PGE2 on allergen-induced airway responses and airway inflammation. Am J Respir Crit Care Med 1999; 159:31–6.
63. Peters SP, Schulman ES, MacGlashan DW, Schleimer RP, Newball HH, Lichtenstein LM. Pharmacologic and biochemical studies of human lung mast cells (MC). J Allergy Clin Immunol 1962; 69:150.
64. Gaschler GJ, Zavitz CCJ, Bauer CMT, Stämpfli MR. Mechanisms of clearance of nontypeable haemophilus influenzae from cigarette smoke-exposed mouse lungs. Eur Respir J 2010; 36:1131–42.