Inhalation of the reactive aldehyde acrolein promotes antigen sensitization to ovalbumin and enhances neutrophilic inflammation

Journal of Immunotoxicology

Volumn 13, Issue 2, 2016, Pages 191-197

  O'Brien, Edmund ^a   Spiess, Page C ^a   Habibovic, Aida ^a   Hristova, Milena ^a   Bauer, Robert A ^a   Randall, Matthew J ^a   Poynter, Matthew E ^a   Van Der Vliet, Albert ^a  

^a UNIVERSITY OF VERMONT   (United States)

Author keywords

Acrolein; allergic asthma; inflammation; ovalbumin

Indexed keywords

ACROLEIN; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 5; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MESSENGER RNA; OVALBUMIN; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; IMMUNOGLOBULIN G;

ADAPTIVE IMMUNITY; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG MECHANISM; HISTOLOGY; IMMUNOLOGICAL TOLERANCE; INFLAMMATION; LEUKOCYTE DIFFERENTIAL COUNT; LUNG LAVAGE; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROVOCATION TEST; SENSITIZATION; TH2 CELL; ANIMAL; ASTHMA; CHEMICALLY INDUCED; IMMUNOLOGY; INHALATIONAL DRUG ADMINISTRATION; LUNG; PATHOLOGY;

ACROLEIN; ADMINISTRATION, INHALATION; ANIMALS; ASTHMA; CYTOKINES; IMMUNOGLOBULIN G; INFLAMMATION; LUNG; MALE; MICE; NEUTROPHILS; OVALBUMIN;

EID: 84953263005     PISSN: 1547691X     EISSN: 15476901     Source Type: Journal    
DOI: 10.3109/1547691X.2015.1033571     Document Type: Article

References (62)

1. Anandan, C., Nurmatov, U., van Schayck, O. C., and Sheikh, A. 2010. Is the prevalence of asthma declining? Systematic review of epidemiological studies. Allergy 65:152-167.
2. Bein, K., and Leikauf, G. D. 2011. Acrolein 0 A pulmonary hazard. Mol. Nutr. Food Res. 55:1342-1360.
3. Bevelander, M., Mayette, J., Whittaker, L. A., et al. 2007. Nitrogen dioxide promotes allergic sensitization to inhaled antigen. J. Immunol. 179:3680-3688.
4. Botelho, F. M., Nikota, J. K., Bauer, C. M., et al. 2012. Cigarette smokeinduced accumulation of lung dendritic cells is IL-1α-dependent in mice. Respir. Res. 13:81.
5. Centers for Disease Control and Prevention (CDC). 2004. The Health Consequences of Smoking: A Report of the Surgeon General. Atlanta, GA: CDC.
6. Chalmers, G. W., MacLeod, K. J., Thomson, L., et al. 2001. Smoking and airway inflammation in patients with mild asthma. Chest 120: 1917-1922.
7. Dick, S., Doust, E., Cowie, H., et al. 2014. Associations between environmental exposures and asthma control and exacerbations in young children: A systematic review. BMJ Open 4:e003827.
8. Dunbar, A., Gotsis, W., and Frishman, W. 2013. Second-hand tobacco smoke and cardiovascular disease risk: An epidemiological review. Cardiol. Rev. 21:94-100.
9. Faroon, O., Roney, N., Taylor, J., et al. 2008. Acrolein environmental levels and potential for human exposure. Toxicol. Ind. Health 24: 543-564.
10. Harris, C., and Hansen, J. M. 2012. Oxidative stress, thiols, and redox profiles. Meth. Mol. Biol. 889:325-346.
11. Hersoug, L. G., Husemoen, L. L., Sigsgaard, T., et al. 2010. Indoor exposure to environmental cigarette smoke, but not other inhaled particulates associates with respiratory symptoms and diminished lung function in adults. Respirology 15:993-1000.
12. Hieshima, K., Imai, T., Opdenakker, G., et al. 1997. Molecular cloning of a novel human CC chemokine liver and activation-regulated chemokine (LARC) expressed in liver. Chemotactic activity for lymphocytes and gene localization on chromosome 2. J. Biol. Chem. 272: 5846-5853.
13. Hjern, A., Hedberg, A., Haglund, B., and Rosen, M. 2001. Does tobacco smoke prevent atopic disorders? A study of two generations of Swedish residents. Clin. Exp. Allergy 31:908-914.
14. Holgate, S. T., Davies, D. E., Powel, R. M., et al. 2007. Local genetic and environmental factors in asthma disease pathogenesis: Chronicity and persistence mechanisms. Eur. Respir. J. 29:793-803.
15. Holgate, S. T., Roberts, G., Arshad, H. S., et al. 2009. The role of airway epithelium and its interaction with environmental factors in asthma pathogenesis. Proc. Am. Thorac. Soc. 6:655-659.
16. Hollingsworth, J. W., Free, M. E., Li, Z., et al. 2010. Ozone activates pulmonary dendritic cells and promotes allergic sensitization through a Toll-like receptor 4-dependent mechanism. J. Allergy Clin. Immunol. 125:1167-11670.
17. Hoyne, G. F., Tan, K., Corsin-Jimenez, M., et al. 2000. Immunological tolerance to inhaled antigen. Am. J. Respir. Crit. Care Med. 162: S169-174.
18. Hunt, A., Crawford, J. A., Rosenbaum, P. F., and Abraham, J. L. 2011. Levels of household particulate matter and environmental tobacco smoke exposure in the first year of life for a cohort at risk for asthma in urban Syracuse, NY. Environ. Int. 37:1196-1205.
19. Huxley, R. R., and Woodward, M. 2011. Cigarette smoking as a risk factor for coronary heart disease in women compared with men: A systematic review and meta-analysis of prospective cohort studies. Lancet 378:1297-1305.
20. Jung, J. W., Ju, Y. S., and Kang, H. R. 2012. Association between parental smoking behavior and children's respiratory morbidity: 5-year study in an urban city of South Korea. Pediatr. Pulmonol. 47:338-345.
21. Kasahara, D. I., Poynter, M. E., Othman, Z., et al. 2008. Acrolein inhalation suppresses lipopolysaccharide-induced inflammatory cytokine production but does not affect acute airway neutrophilia. J. Immunol. 181:736-745.
22. Kawaguchi, M., Kokubu, F., Fujita, J., et al. 2009. Role of IL-17F in asthma. Inflamm. Allergy Drug Targets 8:383-389.
23. Lanckacker, E. A., Tournoy, K. G., Hammad, H., et al. 2013. Short cigarette smoke exposure facilitates sensitization and asthma development in mice. Eur. Respir. J. 41:1189-1199.
24. Leikauf, G. D. 2002. Hazardous air pollutants and asthma. Environ. Health Perspect. 110:505-526.
25. -ΔΔCT method. Methods 25:402-408.
26. Mantel, P. Y., and Schmidt-Weber, C. B. 2011. Transforming growth factor-β: Recent advances on its role in immune tolerance. Meth. Mol. Biol. 677:303-338.
27. Melgert, B. N., Postma, D. S., Geerlings, M., et al. 2004. Short-term smoke exposure attenuates ovalbumin-induced airway inflammation in allergic mice. Am. J. Respir. Cell. Mol. Biol. 30:880-885.
28. Mitchell, E. A., Beasley, R., Keil, U., et al; and the ISAAC Phase Three Study Group. 2012. The association between tobacco and the risk of asthma, rhino-conjunctivitis and eczema in children and adolescents: Analysis from Phase Three of the ISAAC Program. Thorax 67: 941-949.
29. Moerloose, K. B., Robays, L. J., Maes, T., et al. 2006. Cigarette smoke exposure facilitates allergic sensitization in mice. Respir. Res. 7:49-57.
30. Mohammad, Y., Shaaban, R., Al-Zahad, B. A., et al. 2013. Impact of active and passive smoking as risk factors for asthma and COPD in women presenting to primary care in Syria: First report by the WHOGARD survey group. Int. J. Chron. Obstruct. Pulmon. Dis. 8:473-482.
31. Mukherjee, A. B., and Zhang, Z. 2011. Allergic Asthma: Influence of genetic and environmental factors. J. Biol. Chem. 286:32883-32889.
32. Murdoch, J. R., and Lloyd, C. M. 2010. Chronic inflammation and asthma. Mutat. Res. 690:24-39.
33. Murphy, D. M., and O'Byrne, P. M. 2010. Recent advances in the pathophysiology of asthma. Chest 137:1417-1426.
34. Myers, C. R., Myers, J. M., Kufahl, T. D., et al. 2011. The effects of acrolein on the thioredoxin system: Implication for redox-sensitive signaling. Mol. Nutr. Food Res. 55:1361-1374.
35. Oberg, M., Jaakkola, M. S., Woodward, A., et al. 2011. Worldwide burden of disease from exposure to second-hand smoke: A retrospective analysis of data from 192 countries. Lancet 377:139-146.
36. + T-cells expressing membrane-bound TGFβ and FOXP3. J. Clin. Invest. 114:28-38.
37. Papaioannou, A. I., Koutsokera, A., Tanou, K., et al. 2010. Acute effect of smoking in healthy and asthmatic smokers. Eur. J. Clin. Invest. 40: 103-109.
38. Rahman, I., and MacNee, W. 1999. Lung glutathione and oxidative stress: Implications in cigarette smoke-induced airway disease. Am. J. Physiol. 277:L1067-1088.
39. Reddy, S., Finkelstein, E. I., Wong, P. S., et al. 2002. Identification of glutathione modifications by cigarette smoke. Free Radic. Biol. Med. 33:1490-1498.
40. Riedel, F., Hasenauer, E., Barth, P. J., et al. 1996. Formaldehyde exposure enhances inhalative allergic sensitization in the guinea pig. Allergy 51: 94-99.
41. Robbins, C. S., Pouladi, M. A., Fattouh, R., et al. 2005. Mainstream cigarette smoke exposure attenuates airway immune inflammatory responses to surrogate and common environmental allergens in mice, despite evidence of increased systemic sensitization. J. Immunol. 175: 2834-2842.
42. Rodgman, A., and Perfetti, T. A., (Eds.). 2013. The Chemical Components of Tobacco and Tobacco Smoke. Boca Raton, FL: CRC Press.
43. Rumold, R., Jyrala, M., and Diaz-Sanchez, D. 2001. Secondhand smoke induces allergic sensitization in mice. J. Immunol. 167:4765-4770.
44. Scapini, P., Laudanna, C., Pinardi, C., et al. 2001. Neutrophils produce biologically-active macrophage inflammatory protein-3α (MIP-3α)/CCL20 and MIP-3β/CCL19. Eur. J. Immunol. 31:1981-1988.
45. Sears, M. R. 2014. Trends in the prevalence of asthma. Chest 145: 219-225.
46. Siroux, V., Pin, I., Oryszczyn, M. P., et al. 2000. 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. 15:470-477.
47. Spiess, P. C., Kasahara, D., Habibovic, A., et al. 2013. Acrolein exposure suppresses antigen-induced pulmonary inflammation. Respir. Res. 14: 107-120.
48. Song, J. J., Lee, J. D., Lee, B. D., et al. 2013. Effect of acrolein, a hazardous air pollutant in smoke, on human middle-ear epithelial cells. Int. J. Pediatr. Otorhino-laryngol. 77:1659-1664.
49. Stapleton, M., Howard-Thompson, A., George, C., et al. 2011. Smoking and asthma. J. Am. Board Fam. Med. 24:313-322.
50. Stevens, J. F., and Maier, C. S. 2008. Acrolein: Sources, metabolism, and biomolecular inter-actions relevant to human health and disease. Mol. Nutr. Food Res. 52:7-25.
51. Strachan, D. P. 2000. The role of environmental factors in asthma. Br. Med. Bull. 56:865-882.
52. Tamimi, A., Serdarevic, D., and Hanania, N. A. 2012. The effects of cigarette smoke on airway inflammation in asthma and COPD: Therapeutic implications. Respir. Med. 106:319-328.
53. Thatcher, T. H., Benson, R. P., Phipps, R. P., and Sime, P. J. 2008. Highdose but not low-dose mainstream cigarette smoke suppresses allergic airway inflammation by inhibiting T-cell function. Am. J. Physiol. 295: L412-L421.
54. To, T., Stanojevic, S., Moores, G., et al. 2012. Global asthma prevalence in adults: Findings from the cross-sectional world health survey. BMC Public Health 12:204-211.
55. Trimble, N. J., Botelho, F. M., Bauer, C. M., et al. 2009. Adjuvant and anti-inflammatory properties of cigarette smoke in murine allergic airway inflammation. Am. J. Respir. Cell. Mol. Biol. 40:38-46.
56. Troisi, R. J., Speizer, F. E., Rosner, B., et al. 1995. Cigarette smoking and incidence of chronic bronchitis and asthma in women. Chest 108: 1557-1561.
57. Tsai, C. H., Huang, J. H., Hwang, B. F., and Lee, Y. L. 2010. Household environmental tobacco smoke and risks of asthma, wheeze and bronchitic symptoms among children in Taiwan. Respir. Res. 11:11-20.
58. H2-driven airway inflammation and delays inhalational tolerance. Respir. Res. 9:1-14.
59. Wenzel, S. E., Szefler, S. J., Leung, D. Y., et al. 1997. Bronchoscopic evaluation of severe asthma: Persistent inflammation associated with high-dose glucocorticoids. Am. J. Respir. Crit. Care Med. 156: 737-742.
60. Wong, G. W., Leung, T. F., and Ko, F. W. 2013. Changing prevalence of allergic disease in the Asia-Pacific region. Allergy Asthma Immunol. Res. 5:251-257.
61. World Health Organization (WHO). 2007. Global Surveillance, Prevention, and Control of Chronic Respiratory Diseases: A Comprehensive Approach. Geneva: WHO.
62. World Health Organization (WHO). 2008. WHO Report on the Global Tobacco Epidemic, 2008: The MPOWER package. Geneva: WHO.