Dietary compound kaempferol inhibits airway thickening induced by allergic reaction in a bovine serum albumin-induced model of asthma

International Journal of Molecular Sciences

Volumn 16, Issue 12, 2015, Pages 29980-29995

  Shin, Daekeun ^a   Park, Sin Hye ^a   Choi, Yean Jung ^a   Kim, Yun Ho ^a   Antika, Lucia Dwi ^a   Habibah, Nurina Umy ^a   Kang, Min Kyung ^a   Kang, Young Hee ^a  

^a Hallym University   (South Korea)

Author keywords

Airway thickening; Asthma; Bronchoconstriction; Cyclooxygenase 2; Kaempferol

Indexed keywords

BETA N ACETYLHEXOSAMINIDASE; BOVINE SERUM ALBUMIN; CYTOSOLIC PHOSPHOLIPASE A2; KAEMPFEROL; MITOGEN ACTIVATED PROTEIN KINASE; CYCLOOXYGENASE 2; KAEMPFEROL DERIVATIVE; PHOSPHOLIPASE A2; PROSTAGLANDIN; PROTEIN KINASE SYK; PROTEIN TYROSINE KINASE; SIGNAL PEPTIDE; SYK PROTEIN, MOUSE; SYK PROTEIN, RAT;

ALLERGIC REACTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTHMA; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HYPERPLASIA; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MAST CELL DEGRANULATION; MOUSE; MUSCLE HYPERTROPHY; NONHUMAN; PROSTAGLANDIN RELEASE; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; BIOLOGICAL MODEL; BIOSYNTHESIS; BOVINE; CHEMISTRY; COMPLICATION; DIET; DISEASE MODEL; DRUG EFFECTS; ENZYME INDUCTION; HYPERSENSITIVITY; LEUKOCYTE; LUNG; METABOLISM; PATHOLOGY; TIME FACTOR; TUMOR CELL LINE;

ANIMALS; ASTHMA; CATTLE; CELL LINE, TUMOR; CYCLOOXYGENASE 2; DIET; DISEASE MODELS, ANIMAL; ENZYME INDUCTION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HEXOSAMINIDASES; HYPERSENSITIVITY; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KAEMPFEROLS; LEUKOCYTES; LUNG; MALE; MICE, INBRED BALB C; MODELS, BIOLOGICAL; PHOSPHOLIPASES A2; PROSTAGLANDINS; PROTEIN-TYROSINE KINASES; RATS; SERUM ALBUMIN, BOVINE; SYK KINASE; TIME FACTORS;

EID: 84949989450     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms161226218     Document Type: Article

References (47)

1. Platts-Mills, T. A.; Woodfolk, J. A. Allergens and their role in the allergic immune response. Immunol. Rev. 2011, 242, 51-68. [CrossRef] [PubMed]
2. Broide, D. H. Allergic rhinitis: Pathophysiology. Allergy Asthma Proc. 2010, 31, 370-374. [CrossRef] [PubMed]
3. Galli, E.; Cicconi, R.; Rossi, P.; Casati, A.; Brunetti, E.; Mancino, G. Atopic dermatitis: Molecular mechanisms, clinical aspects and new therapeutical approaches. Curr. Mol. Med. 2003, 3, 127-138. [CrossRef] [PubMed]
4. Galli, S. J.; Tsai, M. IgE and mast cells in allergic disease. Nat. Med. 2012, 18, 693-704. [CrossRef] [PubMed]
5. Cromheecke, J. L.; Nguyen, K. T.; Huston, D. P. Emerging role of human basophil biology in health and disease. Curr. Allergy Asthma Rep. 2014, 14, 408. [CrossRef] [PubMed]
6. Amin, K. The role of mast cells in allergic inflammation. Respir. Med. 2012, 106, 9-14. [CrossRef] [PubMed]
7. Yokoi, H.; Choi, O. H.; Hubbard, W.; Lee, H. S.; Canning, B. J.; Lee, H. H.; Ryu, S. D.; von Gunten, S.; Bickel, C. A.; Hudson, S. A.; et al. Inhibition of Fc"RI-dependent mediator release and calcium flux from human mast cells by sialic acid-binding immunoglobulin-like lectin 8 engagement. J. Allergy Clin. Immunol. 2008, 121, 499-505. [CrossRef] [PubMed]
8. Reddy, S. T.; Wadleigh, D. J.; Herschman, H. R. Transcriptional regulation of the cyclooxygenase-2 gene in activated mast cells. J. Biol. Chem. 2000, 275, 3107-3113. [CrossRef] [PubMed]
9. Oh, Y. C.; Kang, O. H.; Choi, J. G.; Lee, Y. S.; Brice, O. O.; Jung, H. J.; Hong, S. H.; Lee, Y. M.; Shin, D. W.; Kim, Y. S.; et al. Anti-allergic activity of a platycodon root ethanol extract. Int. J. Mol. Sci. 2010, 11, 2746-2758. [CrossRef] [PubMed]
10. Kudo, M.; Melton, A. C.; Chen, C.; Engler, M. B.; Huang, K. E.; Ren, X.; Wang, Y.; Bernstein, X.; Li, J. T.; Atabai, K.; et al. IL-17A produced by αβ T cells drives airway hyper-responsiveness in mice and enhances mouse and human airway smooth muscle contraction. Nat. Med. 2012, 18, 547-554. [CrossRef] [PubMed]
11. Fujitani, Y.; Kanaoka, Y.; Aritake, K.; Uodome, N.; Okazaki-Hatake, K.; Urade, Y. Pronounced eosinophilic lung inflammation and Th2 cytokine release in human lipocalin-type prostaglandin D synthase transgenic mice. J. Immunol. 2002, 168, 443-449. [CrossRef] [PubMed]
12. Luster, A. D.; Tager, A. M. T-cell trafficking in asthma: Lipid mediators grease the way. Nat. Rev. Immunol. 2004, 4, 711-724. [CrossRef] [PubMed]
13. Chung, W. C.; Ryu, S. H.; Sun, H.; Zeldin, D. C.; Koo, J. S. CREB mediates prostaglandin F2α-induced MUC5AC overexpression. J. Immunol. 2009, 182, 2349-2356. [CrossRef] [PubMed]
14. Park, J. Y.; Pillinger, M. H.; Abramson, S. B. Prostaglandin E2 synthesis and secretion: The role of PGE2 synthases. Clin. Immunol. 2006, 119, 229-240. [CrossRef] [PubMed]
15. Lee, I. T.; Yang, C. M. Inflammatory signalings involved in airway and pulmonary diseases. Mediat. Inflamm. 2013, 2013. [CrossRef] [PubMed]
16. Sapirstein, A.; Bonventre, J. V. Specific physiological roles of cytosolic phospholipase A2 as defined by gene knockouts. Biochim. Biophys. Acta 2000, 1488, 139-148. [CrossRef]
17. Daham, K.; Song, W. L.; Lawson, J. A.; Kupczyk, M.; Gülich, A.; Dahlén, S. E.; FitzGerald, G. A.; Dahlén, B. Effects of celecoxib on major prostaglandins in asthma. Clin. Exp. Allergy 2011, 41, 36-45. [CrossRef] [PubMed]
18. Pang, L. COX-2 expression in asthmatic airways: The story so far. Thorax 2001, 56, 335-336. [CrossRef] [PubMed]
19. Stumm, C. L.; Wettlaufer, S. H.; Jancar, S.; Peters-Golden, M. Airway remodeling in murine asthma correlates with a defect in PGE2 synthesis by lung fibroblasts. Am. J. Physiol. Lung Cell. Mol. Physiol. 2011, 301, L636-L644. [CrossRef] [PubMed]
20. Card, J. W.; Voltz, J. W.; Carey, M. A.; Bradbury, J. A.; Degraff, L. M.; Lih, F. B.; Bonner, J. C.; Morgan, D. L.; Flake, G. P.; Zeldin, D. C. Cyclooxygenase-2 deficiency exacerbates bleomycin-induced lung dysfunction but not fibrosis. Am. J. Respir. Cell Mol. Biol. 2007, 37, 300-308. [CrossRef] [PubMed]
21. Lovgren, A. K.; Jania, L. A.; Hartney, J. M.; Parsons, K. K.; Audoly, L. P.; Fitzgerald, G. A.; Tilley, S. L.; Koller, B. H. COX-2-derived prostacyclin protects against bleomycin-induced pulmonary fibrosis. Am. J. Physiol. Lung Cell. Mol. Physiol. 2006, 291, L144-L156. [CrossRef] [PubMed]
22. Dempsey, E. C.; Cool, C. D.; Littler, C. M. Lung disease and PKCs. Pharmacol. Res. 2007, 55, 545-559. [CrossRef] [PubMed]
23. Gerthoffer, W. T.; Singer, C. A. MAPK regulation of gene expression in airway smooth muscle. Respir. Physiol. Neurobiol. 2003, 137, 237-250. [CrossRef]
24. Wu, T.; Han, C.; Shelhamer, J. H. Involvement of p38 and p42/44 MAP kinases and protein kinase C in the interferon-γ and interleukin-1α-induced phosphorylation of 85-kDa cytosolic phospholipase A2 in primary human bronchial epithelial cells. Cytokine 2004, 25, 11-20. [CrossRef] [PubMed]
25. Tourkina, E.; Gooz, P.; Pannu, J.; Bonner, M.; Scholz, D.; Hacker, S.; Silver, R. M.; Trojanowska, M.; Hoffman, S. Opposing effects of protein kinase Calpha and protein kinase Cepsilon on collagen expression by human lung fibroblasts are mediated via MEK/ERK and caveolin-1 signaling. J. Biol. Chem. 2005, 280, 13879-13887. [CrossRef] [PubMed]
26. Laporte, J. D.; Moore, P. E.; Abraham, J. H.; Maksym, G. N.; Fabry, B.; Panettieri, R. A., Jr.; Shore, S. A. Role of ERK MAP kinases in responses of cultured human airway smooth muscle cells to IL-1β. Am. J. Physiol. Lung Cell. Mol. Physiol. 1999, 277, L943-L951.
27. Lin, C. C.; Lee, I. T.; Yang, Y. L.; Lee, C. W.; Kou, Y. R.; Yang, C. M. Induction of COX-2/PGE2/IL-6 is crucial for cigarette smoke extract-induced airway inflammation: Role of TLR4-dependent NADPH oxidase activation. Free Radic. Biol. Med. 2010, 48, 240-254. [CrossRef] [PubMed]
28. García-Mediavilla, V.; Crespo, I.; Collado, P. S.; Esteller, A.; Sánchez-Campos, S.; Tuñón, M. J.; González-Gallego, J. The anti-inflammatory flavones quercetin and kaempferol cause inhibition of inducible nitric oxide synthase, cyclooxygenase-2 and reactive C-protein, and down-regulation of the nuclear factor kB pathway in Chang Liver cells. Eur. J. Pharmacol. 2007, 557, 221-229. [CrossRef] [PubMed]
29. Hämäläinen, M.; Nieminen, R.; Vuorela, P.; Heinonen, M.; Moilanen, E. Anti-inflammatory effects of flavonoids: Genistein, kaempferol, quercetin, and daidzein inhibit STAT-1 and NF-kB activations, whereas flavone, isorhamnetin, naringenin, and pelargonidin inhibit only NF-kB activation along with their inhibitory effect on iNOS expression and NO production in activated macrophages. Mediat. Inflamm. 2007, 2007. [CrossRef]
30. Kim, J. M.; Lee, E. K.; Kim, D. H.; Yu, B. P.; Chung, H. Y. Kaempferol modulates pro-inflammatory NF-kB activation by suppressing advanced glycation end products-induced NADPH oxidase. Age 2010, 32, 197-208. [CrossRef] [PubMed]
31. Gong, J. H.; Cho, I. H.; Shin, D.; Han, S. Y.; Park, S. H.; Kang, Y. H. Inhibition of airway epithelial-to-mesenchymal transition and fibrosis by kaempferol in endotoxin-induced epithelial cells and ovalbumin-sensitized mice. Lab. Investig. 2014, 94, 297-308. [CrossRef] [PubMed]
32. Gong, J. H.; Shin, D.; Han, S. Y.; Park, S. H.; Kang, M. K.; Kim, J. L.; Kang, Y. H. Blockade of airway inflammation by kaempferol via disturbing Tyk-STAT signaling in airway epithelial cells and in asthmatic mice. Evid. Based Complement. Altern. Med. 2013, 2013. [CrossRef] [PubMed]
33. Fahy, J. V.; Corry, D. B.; Boushey, H. A. Airway inflammation and remodeling in asthma. Curr. Opin. Pulm. Med. 2000, 6, 15-20. [CrossRef] [PubMed]
34. Sanderson, M. P.; Wex, E.; Kono, T.; Uto, K.; Schnapp, A. Syk and Lyn mediate distinct Syk phosphorylation events in Fc"RI-signal transduction: Implications for regulation of IgE-mediated degranulation. Mol. Immunol. 2010, 48, 171-178. [CrossRef] [PubMed]
35. Oh, H. A.; Han, N. R.; Kim, M. J.; Kim, H. M.; Jeong, H. J. Evaluation of the effect of kaempferol in a murine allergic rhinitis model. Eur. J. Pharmacol. 2013, 718, 48-56. [CrossRef] [PubMed]
36. Gong, J. H.; Shin, D.; Han, S. Y.; Kim, J. L.; Kang, Y. H. Kaempferol suppresses eosinophil infiltration and airway inflammation in airway epithelial cells and in mice with allergic asthma. J. Nutr. 2012, 142, 47-56. [CrossRef] [PubMed]
37. Lee, E. J.; Ji, G. E.; Sung, M. K. Quercetin and kaempferol suppress immunoglobulin E-mediated allergic inflammation in RBL-2H3 and Caco-2 cells. Inflamm. Res. 2010, 59, 847-854. [CrossRef] [PubMed]
38. Chung, M. J.; Pandey, R. P.; Choi, J. W.; Sohng, J. K.; Choi, D. J.; Park, Y. I. Inhibitory effects of kaempferol-3-O-rhamnoside on ovalbumin-induced lung inflammation in a mouse model of allergic asthma. Int. Immunopharmacol. 2015, 25, 302-310. [CrossRef] [PubMed]
39. Noble, P. B.; Pascoe, C. D.; Lan, B.; Ito, S.; Kistemaker, L. E.; Tatler, A. L.; Pera, T.; Brook, B. S.; Gosens, R.; West, A. R. Airway smooth muscle in asthma: Linking contraction and mechanotransduction to disease pathogenesis and remodelling. Pulm. Pharmacol. Ther. 2014, 29, 96-107. [CrossRef] [PubMed]
40. Brightling, C. E.; Bradding, P.; Symon, F. A.; Holgate, S. T.; Wardlaw, A. J.; Pavord, I. D. Mast-cell infiltration of airway smooth muscle in asthma. N. Engl. J. Med. 2002, 346, 1699-1705. [CrossRef] [PubMed]
41. Amin, K.; Janson, C.; Boman, G.; Venge, P. The extracellular deposition of mast cell products is increased in hypertrophic airways smooth muscles in allergic asthma but not in nonallergic asthma. Allergy 2005, 60, 1241-1247. [CrossRef] [PubMed]
42. Black, J. L.; Panettieri, R. A., Jr.; Banerjee, A.; Berger, P. Airway smooth muscle in asthma: Just a target for bronchodilation? Clin. Chest Med. 2012, 33, 543-558. [CrossRef] [PubMed]
43. Chambers, L. S.; Black, J. L.; Ge, Q.; Carlin, S. M.; Au, W. W.; Poniris, M.; Thompson, J.; Johnson, P. R.; Burgess, J. K. PAR-2 activation, PGE2, and COX-2 in human asthmatic and nonasthmatic airway smooth muscle cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2003, 285, L619-L627. [CrossRef] [PubMed]
44. Hewson, C. A.; Patel, S.; Calzetta, L.; Campwala, H.; Havard, S.; Luscombe, E.; Clarke, P. A.; Peachell, P. T.; Matera, M. G.; Cazzola, M.; et al. Preclinical evaluation of an inhibitor of cytosolic phospholipase A2α for the treatment of asthma. J. Pharmacol. Exp. Ther. 2012, 340, 656-665. [CrossRef] [PubMed]
45. Lee, Y. S.; Hur, S.; Kim, T. Y. Homoisoflavanone prevents mast cell activation and allergic responses by inhibition of Syk signaling pathway. Allergy 2014, 69, 453-462. [CrossRef] [PubMed]
46. Ramis, I.; Otal, R.; Carreño, C.; Domènech, A.; Eichhorn, P.; Orellana, A.; Maldonado, M.; de Alba, J.; Prats, N.; Fernández, J. C.; et al. A novel inhaled Syk inhibitor blocks mast cell degranulation and early asthmatic response. Pharmacol. Res. 2015, 99, 116-124. [CrossRef] [PubMed]
47. Moy, L. Y.; Jia, Y.; Caniga, M.; Lieber, G.; Gil, M.; Fernandez, X.; Sirkowski, E.; Miller, R.; Alexander, J. P.; Lee, H. H.; et al. Inhibition of spleen tyrosine kinase attenuates allergen-mediated airway constriction. Am. J. Respir. Cell Mol. Biol. 2013, 49, 1085-1092. [CrossRef] [PubMed]