Inhaled birch pollen extract induces airway hyperresponsiveness via oxidative stress but independently of pollen-intrinsic NADPH oxidase activity, or the TLR4-TRIF pathway

Journal of Immunology

Volumn 191, Issue 2, 2013, Pages 922-933

  Shalaby, Karim H ^a   Allard Coutu, Alexandra ^a   O'Sullivan, Michael J ^a   Nakada, Emily ^a   Qureshi, Salman T ^b   Day, Brian J ^c   Martin, James G ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MONTREAL GENERAL HOSPITAL   (Canada)

^c DEPARTMENT OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; DIMETHYLTHIOUREA; INTERLEUKIN 1 RECEPTOR; POLLEN EXTRACT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1;

ALLERGENICITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTHMA; BIRCH; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; POLLEN; PRIORITY JOURNAL; PROVOCATION TEST; RECEPTOR BLOCKING; RESPIRATORY TRACT ALLERGY; RESPIRATORY TRACT INFLAMMATION; RESPIRATORY TRACT MUCOSA; SENSITIZATION; SIGNAL TRANSDUCTION;

ACETYLCYSTEINE; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; ASTHMA; BETULA; FEMALE; INTERFERON-BETA; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; NADPH OXIDASE; OXIDATIVE STRESS; POLLEN; REACTIVE OXYGEN SPECIES; TH2 CELLS; THIOUREA; TOLL-LIKE RECEPTOR 4;

EID: 84880123038     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1103644     Document Type: Article

References (61)

1. Chung, K. F., and J. A. Marwick. 2010. Molecular mechanisms of oxidative stress in airways and lungs with reference to asthma and chronic obstructive pulmonary disease. Ann. N. Y. Acad. Sci. 1203: 85-91.
2. Comhair, S. A., and S. C. Erzurum. 2010. Redox control of asthma: molecular mechanisms and therapeutic opportunities. [Published erratum appears in 2010 Antioxid. Redox. Signal. 12: 321.] Antioxid. Redox Signal. 12: 93-124.
3. Takizawa, H. 2004. Diesel exhaust particles and their effect on induced cytokine expression in human bronchial epithelial cells. Curr. Opin. Allergy Clin. Immunol. 4: 355-359. (Pubitemid 39274075)
4. Fitzpatrick, A. M., W. G. Teague, F. Holguin, M. Yeh, and L. A. Brown; Severe Asthma Research Program. 2009. Airway glutathione homeostasis is altered in children with severe asthma: evidence for oxidant stress. J. Allergy Clin. Immunol. 123: 146-152, e8.
5. Smith, L. J., M. Shamsuddin, P. H. Sporn, M. Denenberg, and J. Anderson. 1997. Reduced superoxide dismutase in lung cells of patients with asthma. Free Radic. Biol. Med. 22: 1301-1307. (Pubitemid 27171974)
6. Boldogh, I., A. Bacsi, B. K. Choudhury, N. Dharajiya, R. Alam, T. K. Hazra, S. Mitra, R. M. Goldblum, and S. Sur. 2005. ROS generated by pollen NADPH oxidase provide a signal that augments antigen-induced allergic airway inflammation. J. Clin. Invest. 115: 2169-2179. (Pubitemid 41134158)
7. Dharajiya, N., B. K. Choudhury, A. Bacsi, I. Boldogh, R. Alam, and S. Sur. 2007. Inhibiting pollen reduced nicotinamide adenine dinucleotide phosphate oxidase-induced signal by intrapulmonary administration of antioxidants blocks allergic airway inflammation. J. Allergy Clin. Immunol. 119: 646-653. (Pubitemid 46335816)
8. Trompette, A., S. Divanovic, A. Visintin, C. Blanchard, R. S. Hegde, R. Madan, P. S. Thorne, M. Wills-Karp, T. L. Gioannini, J. P. Weiss, and C. L. Karp. 2009. Allergenicity resulting from functional mimicry of a Toll-like receptor complex protein. Nature 457: 585-588.
9. Hammad, H., M. Chieppa, F. Perros, M. A. Willart, R. N. Germain, and B. N. Lambrecht. 2009. House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells. Nat. Med. 15: 410-416.
10. Tan, A. M., H. C. Chen, P. Pochard, S. C. Eisenbarth, C. A. Herrick, and H. K. Bottomly. 2010. TLR4 signaling in stromal cells is critical for the initiation of allergic Th2 responses to inhaled antigen. J. Immunol. 184: 3535-3544.
11. Hollingsworth, J. W., II, D. N. Cook, D. M. Brass, J. K. Walker, D. L. Morgan, W. M. Foster, and D. A. Schwartz. 2004. The role of Toll-like receptor 4 in environmental airway injury in mice. Am. J. Respir. Crit. Care Med. 170: 126-132.
12. Kleeberger, S. R., S. P. Reddy, L. Y. Zhang, H. Y. Cho, and A. E. Jedlicka. 2001. Toll-like receptor 4 mediates ozone-induced murine lung hyperpermeability via inducible nitric oxide synthase. Am. J. Physiol. Lung Cell. Mol. Physiol. 280: L326-L333.
13. Tang, H., W. Cao, S. P. Kasturi, R. Ravindran, H. I. Nakaya, K. Kundu, N. Murthy, T. B. Kepler, B. Malissen, and B. Pulendran. 2010. The T helper type 2 response to cysteine proteases requires dendritic cell-basophil cooperation via ROS-mediated signaling. Nat. Immunol. 11: 608-617.
14. Imai, Y., K. Kuba, G. G. Neely, R. Yaghubian-Malhami, T. Perkmann, G. van Loo, M. Ermolaeva, R. Veldhuizen, Y. H. Leung, H. Wang, et al. 2008. Identification of oxidative stress and Toll-like receptor 4 signaling as a key pathway of acute lung injury. Cell 133: 235-249. (Pubitemid 351512299)
15. Gunawan, H., T. Takai, S. Kamijo, X. L. Wang, S. Ikeda, K. Okumura, and H. Ogawa. 2008. Characterization of proteases, proteins, and eicosanoid-like substances in soluble extracts from allergenic pollen grains. Int. Arch. Allergy Immunol. 147: 276-288.
16. Traidl-Hoffmann, C., V. Mariani, H. Hochrein, K. Karg, H. Wagner, J. Ring, M. J. Mueller, T. Jakob, and H. Behrendt. 2005. Pollen-associated phytoprostanes inhibit dendritic cell interleukin-12 production and augment T helper type 2 cell polarization. J. Exp. Med. 201: 627-636.
17. Imbusch, R., and M. J. Mueller. 2000. Formation of isoprostane F(2)-like compounds (phytoprostanes F(1)) from alpha-linolenic acid in plants. Free Radic. Biol. Med. 28: 720-726. (Pubitemid 30171285)
18. Wilson, R. H., G. S. Whitehead, H. Nakano, M. E. Free, J. K. Kolls, and D. N. Cook. 2009. Allergic sensitization through the airway primes Th17-dependent neutrophilia and airway hyperresponsiveness. Am. J. Respir. Crit. Care Med. 180: 720-730.
19. Park, C. S., T. B. Kim, K. Y. Lee, K. A. Moon, Y. J. Bae, M. K. Jang, Y. S. Cho, and H. B. Moon. 2009. Increased oxidative stress in the airway and development of allergic inflammation in a mouse model of asthma. Ann. Allergy Asthma Immunol. 103: 238-247.
20. Whitekus, M. J., N. Li, M. Zhang, M. Wang, M. A. Horwitz, S. K. Nelson, L. D. Horwitz, N. Brechun, D. Diaz-Sanchez, and A. E. Nel. 2002. Thiol antioxidants inhibit the adjuvant effects of aerosolized diesel exhaust particles in a murine model for ovalbumin sensitization. J. Immunol. 168: 2560-2567. (Pubitemid 34171861)
21. Heffner, J. E., and J. E. Repine. 1989. Pulmonary strategies of antioxidant defense. Am. Rev. Respir. Dis. 140: 531-554. (Pubitemid 19218371)
22. Jackson, J. H., C. W. White, N. B. Parker, J. W. Ryan, and J. E. Repine. 1985. Dimethylthiourea consumption reflects H2O2 concentrations and severity of acute lung injury. J. Appl. Physiol. 59: 1995-1998. (Pubitemid 16158264)
23. McGovern, T. K., W. S. Powell, B. J. Day, C. W. White, K. Govindaraju, H. Karmouty-Quintana, N. Lavoie, J. J. Tan, and J. G. Martin. 2010. Dimethylthiourea protects against chlorine induced changes in airway function in a murine model of irritant induced asthma. Respir. Res. 11: 138.
24. McGovern, T., B. J. Day, C. W. White, W. S. Powell, and J. G. Martin. 2011. AEOL10150: a novel therapeutic for rescue treatment after toxic gas lung injury. Free Radic. Biol. Med. 50: 602-608.
25. Wills-Karp, M. 2010. Allergen-specific pattern recognition receptor pathways. Curr. Opin. Immunol. 22: 777-782.
26. Blesa, S., J. Cortijo, M. Martinez-Losa, M. Mata, E. Seda, F. Santangelo, and E. J. Morcillo. 2002. Effectiveness of oral N-acetylcysteine in a rat experimental model of asthma. Pharmacol. Res. 45: 135-140. (Pubitemid 35425652)
27. Kloek, J., E. Mortaz, I. van Ark, C. M. Lilly, F. P. Nijkamp, and G. Folkerts. 2010. Glutathione prevents the early asthmatic reaction and airway hyperresponsiveness in guinea pigs. J. Physiol. Pharmacol. 61: 67-72.
28. Kim, S. R., K. S. Lee, S. J. Park, K. H. Min, M. H. Lee, K. A. Lee, O. Bartov, D. Atlas, and Y. C. Lee. 2011. A novel dithiol amide CB3 attenuates allergic airway disease through negative regulation of p38 mitogen-activated protein kinase. Am. J. Respir. Crit. Care Med. 183: 1015-1024.
29. Talati, M., B. Meyrick, R. S. Peebles, Jr., S. S. Davies, R. Dworski, R. Mernaugh, D. Mitchell, M. Boothby, L. J. Roberts, II, and J. R. Sheller. 2006. Oxidant stress modulates murine allergic airway responses. Free Radic. Biol. Med. 40: 1210-1219.
30. Wang, X. L., T. Takai, S. Kamijo, H. Gunawan, H. Ogawa, and K. Okumura. 2009. NADPH oxidase activity in allergenic pollen grains of different plant species. Biochem. Biophys. Res. Commun. 387: 430-434.
31. Cho, K. J., J. M. Seo, M. G. Lee, and J. H. Kim. 2010. BLT2 is upregulated in allergen-stimulated mast cells and mediates the synthesis of Th2 cytokines. J. Immunol. 185: 6329-6337.
32. Rangasamy, T., M. A. Williams, S. Bauer, M. A. Trush, J. Emo, S. N. Georas, and S. Biswal. 2010. Nuclear erythroid 2 p45-related factor 2 inhibits the maturation of murine dendritic cells by ragweed extract. Am. J. Respir. Cell Mol. Biol. 43: 276-285.
33. Csillag, A., I. Boldogh, K. Pazmandi, Z. Magyarics, P. Gogolak, S. Sur, E. Rajnavolgyi, and A. Bacsi. 2010. Pollen-induced oxidative stress influences both innate and adaptive immune responses via altering dendritic cell functions. J. Immunol. 184: 2377-2385.
34. Schütze, N., I. Lehmann, U. Bönisch, J. C. Simon, and T. Polte. 2010. Exposure to mycotoxins increases the allergic immune response in a murine asthma model. Am. J. Respir. Crit. Care Med. 181: 1188-1199.
35. Mariani, V., S. Gilles, T. Jakob, M. Thiel, M. J. Mueller, J. Ring, H. Behrendt, and C. Traidl-Hoffmann. 2007. Immunomodulatory mediators from pollen enhance the migratory capacity of dendritic cells and license them for Th2 attraction. J. Immunol. 178: 7623-7631. (Pubitemid 46898032)
36. Li, N., M. Wang, L. A. Bramble, D. A. Schmitz, J. J. Schauer, C. Sioutas, J. R. Harkema, and A. E. Nel. 2009. The adjuvant effect of ambient particulate matter is closely reflected by the particulate oxidant potential. Environ. Health Perspect. 117: 1116-1123.
37. Rangasamy, T., J. Guo, W. A. Mitzner, J. Roman, A. Singh, A. D. Fryer, M. Yamamoto, T. W. Kensler, R. M. Tuder, S. N. Georas, and S. Biswal. 2005. Disruption of Nrf2 enhances susceptibility to severe airway inflammation and asthma in mice. J. Exp. Med. 202: 47-59. (Pubitemid 41002909)
38. Li, N., M. Wang, T. D. Oberley, J. M. Sempf, and A. E. Nel. 2002. Comparison of the pro-oxidative and proinflammatory effects of organic diesel exhaust particle chemicals in bronchial epithelial cells and macrophages. J. Immunol. 169: 4531-4541. (Pubitemid 35178231)
39. Lambert, C. J., Jr., T. M. Egan, F. C. Detterbeck, B. A. Keagy, and B. R. Wilcox. 1991. Enhanced pulmonary function using dimethylthiourea for twelve-hour lung preservation. Ann. Thorac. Surg. 51: 924-929, discussion 929-930.
40. Oh, S. M., and A. L. Betz. 1991. Interaction between free radicals and excitatory amino acids in the formation of ischemic brain edema in rats. Stroke 22: 915-921.
41. Suntres, Z. E. 2011. Liposomal antioxidants for protection against oxidant-induced damage. J. Toxicol. 2011: 152474.
42. Lipinski, B. 2011. Hydroxyl radical and its scavengers in health and disease. Oxid. Med. Cell. Longev. 2011: 809696.
43. Bibi, H., B. Seifert, M. Oullette, and J. Belik. 1992. Intratracheal N-acetylcysteine use in infants with chronic lung disease. Acta Paediatr. 81: 335-339.
44. Reinero, C. R., T. M. Lee-Fowler, J. R. Dodam, L. A. Cohn, A. E. DeClue, and V. P. Guntur. 2011. Endotracheal nebulization of N-acetylcysteine increases airway resistance in cats with experimental asthma. J. Feline Med. Surg. 13: 69-73.
45. Fan, J., P. N. Shek, Z. E. Suntres, Y. H. Li, G. D. Oreopoulos, and O. D. Rotstein. 2000. Liposomal antioxidants provide prolonged protection against acute respiratory distress syndrome. Surgery 128: 332-338. (Pubitemid 30622502)
46. Williams, A. S., R. Issa, S. Y. Leung, P. Nath, G. D. Ferguson, B. L. Bennett, I. M. Adcock, and K. F. Chung. 2007. Attenuation of ozone-induced airway inflammation and hyper-responsiveness by c-Jun NH2 terminal kinase inhibitor SP600125. J. Pharmacol. Exp. Ther. 322: 351-359. (Pubitemid 46956362)
47. Williams, A. S., R. Issa, A. Durham, S. Y. Leung, A. Kapoun, S. Medicherla, L. S. Higgins, I. M. Adcock, and K. F. Chung. 2008. Role of p38 mitogen-activated protein kinase in ozone-induced airway hyperresponsiveness and inflammation. Eur. J. Pharmacol. 600: 117-122.
48. Williams, A. S., S. Y. Leung, P. Nath, N. M. Khorasani, P. Bhavsar, R. Issa, J. A. Mitchell, I. M. Adcock, and K. F. Chung. 2007. Role of TLR2, TLR4, and MyD88 in murine ozone-induced airway hyperresponsiveness and neutrophilia. J. Appl. Physiol. 103: 1189-1195. (Pubitemid 47610420)
49. Garantziotis, S., Z. Li, E. N. Potts, J. Y. Lindsey, V. P. Stober, V. V. Polosukhin, T. S. Blackwell, D. A. Schwartz, W. M. Foster, and J. W. Hollingsworth. 2010. TLR4 is necessary for hyaluronan-mediated airway hyperresponsiveness after ozone inhalation. Am. J. Respir. Crit. Care Med. 181: 666-675.
50. Li, Z., E. N. Potts, C. A. Piantadosi, W. M. Foster, and J. W. Hollingsworth. 2010. Hyaluronan fragments contribute to the ozone-primed immune response to lipopolysaccharide. J. Immunol. 185: 6891-6898.
51. Williams, A. S., P. Nath, S. Y. Leung, N. Khorasani, A. N.McKenzie, I.M. Adcock, and K. F. Chung. 2008. Modulation of ozone-induced airway hyperresponsiveness and inflammation by interleukin-13. Eur. Respir. J. 32: 571-578.
52. Pichavant, M., S. Goya, E. H. Meyer, R. A. Johnston, H. Y. Kim, P. Matangkasombut, M. Zhu, Y. Iwakura, P. B. Savage, R. H. DeKruyff, et al. 2008. Ozone exposure in a mouse model induces airway hyperreactivity that requires the presence of natural killer T cells and IL-17. J. Exp. Med. 205: 385-393. (Pubitemid 351281604)
53. Kong, X., R. Thimmulappa, P. Kombairaju, and S. Biswal. 2010. NADPH oxidase-dependent reactive oxygen species mediate amplified TLR4 signaling and sepsis-induced mortality in Nrf2-deficient mice. J. Immunol. 185: 569-577.
54. Taylor, K. R., K. Yamasaki, K. A. Radek, A. Di Nardo, H. Goodarzi, D. Golenbock, B. Beutler, and R. L. Gallo. 2007. Recognition of hyaluronan released in sterile injury involves a unique receptor complex dependent on Toll-like receptor 4, CD44, and MD-2. J. Biol. Chem. 282: 18265-18275. (Pubitemid 47100227)
55. Wright, S. D., R. A. Ramos, P. S. Tobias, R. J. Ulevitch, and J. C. Mathison. 1990. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249: 1431-1433.
56. Torres, D., A. Dieudonné, B. Ryffel, E. Vilain, M. Si-Tahar, M. Pichavant, P. Lassalle, F. Trottein, and P. Gosset. 2010. Double-stranded RNA exacerbates pulmonary allergic reaction through TLR3: implication of airway epithelium and dendritic cells. J. Immunol. 185: 451-459.
57. Zhao, H., S. W. Leu, L. Shi, R. Dedaj, G. Zhao, H. G. Garg, L. Shen, E. Lien, K. A. Fitzgerald, A. Shiedlin, et al. 2010. TLR4 is a negative regulator in noninfectious lung inflammation. J. Immunol. 184: 5308-5314.
58. Seregin, S. S., Y. A. Aldhamen, D. M. Appledorn, C. F. Aylsworth, S. Godbehere, C. J. Liu, D. Quiroga, and A. Amalfitano. 2011. TRIF is a critical negative regulator of TLR agonist mediated activation of dendritic cells in vivo. PLoS One 6: e22064.
59. Matheu, V., A. Treschow, V. Navikas, and S. Issazadeh-Navikas. 2003. Upregulation of B7 molecules (CD80 and CD86) and exacerbated eosinophilic pulmonary inflammatory response in mice lacking the IFN-beta gene. J. Allergy Clin. Immunol. 111: 550-557. (Pubitemid 36337876)
60. Hauck, P. R., and S. Williamson. 2001. The manufacture of allergenic extracts in North America. Clin. Rev. Allergy Immunol. 21: 93-110. (Pubitemid 33001084)
61. Agea, E., A. Russano, O. Bistoni, R. Mannucci, I. Nicoletti, L. Corazzi, A. D. Postle, G. De Libero, S. A. Porcelli, and F. Spinozzi. 2005. Human CD1-restricted T cell recognition of lipids from pollens. J. Exp. Med. 202: 295-308. (Pubitemid 41043825)