Oleanolic acid suppresses ovalbumin-induced airway inflammation and Th2-mediated allergic asthma by modulating the transcription factors T-bet, GATA-3, RORγt and Foxp3 in asthmatic mice

International Immunopharmacology

Volumn 18, Issue 2, 2014, Pages 311-324

  Kim, Seung Hyung ^a   Hong, Jung Hee ^b   Lee, Young Cheol ^b  

^a Daejeon University   (South Korea)

^b Department of Computer and Electronic Physics   (South Korea)

Author keywords

Asthma; GATA 3; IL 17; Oleanolic acid; ROR t; Th2

Indexed keywords

ANTIASTHMATIC AGENT; CYCLOSPORIN A; IMMUNOGLOBULIN E; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 5; METHACHOLINE; OLEANOLIC ACID; RETINOID RELATED ORPHAN RECEPTOR GAMMA; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR T BET;

ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; DRUG MECHANISM; EOSINOPHIL COUNT; FEMALE; HISTOPATHOLOGY; LUNG LAVAGE; LUNG PARENCHYMA; MOUSE; MUCUS SECRETION; NEUTROPHIL COUNT; NONHUMAN; OVALBUMIN-INDUCED AIRWAY INFLAMMATION; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RESPIRATORY TRACT ALLERGY; TREATMENT OUTCOME; UPREGULATION;

ASTHMA; GATA-3; IL-17; OLEANOLIC ACID; RORΓT; TH2;

ALLERGENS; ANIMALS; ANTI-ASTHMATIC AGENTS; ASTHMA; BRONCHIAL HYPERREACTIVITY; BRONCHOALVEOLAR LAVAGE FLUID; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CYTOKINES; EOSINOPHILS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GATA3 TRANSCRIPTION FACTOR; LUNG; MICE; MICE, INBRED BALB C; NEUTROPHILS; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 3; OLEANOLIC ACID; OVALBUMIN; PNEUMONIA; T-BOX DOMAIN PROTEINS; TH2 CELLS;

EID: 84891848258     PISSN: 15675769     EISSN: 18781705     Source Type: Journal    
DOI: 10.1016/j.intimp.2013.12.009     Document Type: Article

References (50)

1. M.J. Schuijs, M.A. Willart, H. Hammad, and B.N. Lambrecht Cytokine targets in airway inflammation Curr Opin Pharmacol 13 2013 351 361
2. S. Greenfeder, S.P. Umland, F.M. Cuss, R.W. Chapman, and R.W. Egan Th2 cytokines and asthma. The role of interleukin-5 in allergic eosinophilic disease Respir Res 2 2001 71 79 (Pubitemid 34187910)
3. S.M. Pope, E.B. Brandt, A. Mishra, S.P. Hogan, N. Zimmermann, and K.I. Matthaei et al. IL-13 induces eosinophil recruitment into the lung by an IL-5- and eotaxin-dependent mechanism J Allergy Clin Immunol 108 2001 594 601 (Pubitemid 32978032)
4. C.M. Lloyd, and E.M. Hessel Functions of T cells in asthma: more than just T(H)2 cells Nat Rev Immunol 10 2010 838 848
5. J. Bousquet, P.K. Jeffery, W.W. Busse, M. Johnson, and A.M. Vignola Asthma. From bronchoconstriction to airways inflammation and remodeling Am J Respir Crit Care Med 161 2000 1720 1745 (Pubitemid 30329053)
6. C.J. Sanderson, D.J. Warren, and M. Strath Identification of a lymphokine that stimulates eosinophil differentiation in vitro. Its relationship to interleukin-3, and functional properties of eosinophils produced in cultures J Exp Med 162 1985 60
7. K.A. Mowen, and L.H. Glimcher Signaling pathways in Th2 development Immunol Rev 202 2004 203 222 (Pubitemid 39576914)
8. S. Finotto, and L. Glimcher T cell directives for transcriptional regulation in asthma Springer Semin Immunopathol 25 2004 281 294
9. D.H. Zhang, L. Yang, L. Cohn, L. Parkyn, R. Homer, and P. Ray et al. Inhibition of allergic inflammation in a murine model of asthma by expression of a dominant-negative mutant of GATA-3 Immunity 11 1999 473 482 (Pubitemid 29504202)
10. S. Finotto, G.T. De Sanctis, H.A. Lehr, U. Herz, M. Buerke, and M. Schipp et al. Treatment of allergic airway inflammation and hyperresponsiveness by antisense-induced local blockade of GATA-3 expression J Exp Med 193 2001 1247 1260 (Pubitemid 32524775)
11. O. Palomares, G. Yaman, A.K. Azkur, T. Akkoc, M. Akdis, and C.A. Akdis Role of Treg in immune regulation of allergic diseases Eur J Immunol 40 2010 1232 1240
12. Y.M. Fai, and C.C. Tao A review of presence of oleanolic acid in natural products Nat Prod Med 2 2009 77 290
13. X. Wang, X.-l. Ye, R. Liu, H.-L. Chen, H. Bai, and X. Liang et al. Antioxidant activities of oleanolic acid in vitro: possible role of Nrf2 and MAP kinases Chem Biol Interact 184 2010 328 337
14. N. Sultana, and A. Ata Oleanolic acid and related derivatives as medicinally important compounds J Enzyme Inhib Med Chem 23 2008 739 756
15. A. Petronelli, G. Pannitteri, and U. Testa Triterpenoids as new promising anticancer drugs Anti-Cancer Drugs 20 2009 880 892
16. P. Dzubak, M. Hajduch, D. Vydra, A. Hustova, M. Kvasnica, and D. Biedermann et al. Pharmacological activities of natural triterpenoids and their therapeutic implications Nat Prod Rep 23 2006 394 411 (Pubitemid 43847140)
17. E.M. Giner-Larza, S. Máñez, M.C. Recio, R.M. Giner, J.M. Prieto, and M. Cerdá-Nicolás et al. Oleanonic acid, a 3-oxotriterpene from Pistacia, inhibits leukotriene synthesis and has anti-inflammatory activity Eur J Pharmacol 428 2001 137 143 (Pubitemid 32971767)
18. J.Y. Lee, H. Moon, and C.J. Kim Effects of hydroxy pentacyclic triterpene acids from Forsythia viridissima on asthmatic responses to OVA challenge in conscious guinea pigs Biol Pharm Bull 33 2010 230 237
19. M.N. Laszczyk Pentacyclic triterpenes of the lupane, oleanane and ursane group as tools in cancer therapy Planta Med 75 2009 1549 1560
20. K. Kawahara, T. Hashiguchi, K. Masuda, A.R. Saniabadi, K. Kikuchi, and S. Tancharoen et al. Mechanism of HMGB1 release inhibition from RAW264.7 cells by oleanolic acid in PrunusmumeSieb. et Zucc Int J Mol Med 23 2009 615 620
21. E.J. Yang, W. Lee, S.K. Ku, K.S. Song, and J.S. Bae Anti-inflammatory activities of oleanolic acid on HMGB1 activated HUVECs Food Chem Toxicol 50 2012 1288 1294
22. J.K. Choi, H.M. Oh, S. Lee, J.W. Park, D. Khang, and S.W. Lee et al. Oleanolic acid acetate inhibits atopic dermatitis and allergic contact dermatitis in a murine model Toxicol Appl Pharmacol 269 2013 72 80
23. S.H. Kim, B.K. Kim, and Y.C. Lee Antiasthmatic effects of hesperidin, a potential Th2 cytokine antagonist, in a mouse model of allergic asthma Mediators Inflamm 2011 2011 485402
24. J. Li, L. Luo, X. Wang, B. Liao, and G. Li Inhibition of NF-kappaB expression and allergen-induced airway inflammation in a mouse allergic asthma model by andrographolide Cell Mol Immunol 6 2009 381 385
25. M.H. Kim, Y.C. Park, and U. Namgung Acupuncture-stimulated activation of sensory neurons J Acupunct Meridian Stud 5 2012 148 155
26. M. Ohshima, A. Yokoyama, H. Ohnishi, H. Hamada, N. Kohno, and J. Higaki et al. Overexpression of suppressor of cytokine signalling-5 augments eosinophilic airway inflammation in mice Clin Exp Allergy 37 2007 735 742 (Pubitemid 46643063)
27. W.W. Busse, and R.F. Lemanske Jr. Asthma N Engl J Med 344 2001 350 362 (Pubitemid 32107645)
28. K.H. Shalaby, and J.G. Martin Overview of asthma; the place of the T cell Curr Opin Pharmacol 10 2010 218 225
29. D.M. Conroy, and T.J. Williams Eotaxin and the attraction of eosinophils to the asthmatic lung Respir Res 2 2001 150 156 (Pubitemid 34187921)
30. T.K. Pareek, A. Belkadi, S. Kesavapany, A. Zaremba, S.L. Loh, and L. Bai et al. Triterpenoid modulation of IL-17 and Nrf-2 expression ameliorates neuroinflammation and promotes remyelination in autoimmune encephalomyelitis Sci Rep 1 2011 201
31. H.S. Kim, H.Y. Sung, M.S. Kim, J.L. Kim, M.K. Kang, and J.H. Gong et al. Oleanolic acid suppresses resistin induction in adipocytes by modulating Tyk-STAT signaling Nutr Res 33 2013 144 153
32. E. Nizankowska, J. Soja, G. Pinis, G. Bochenek, K. Sładek, and B. Domagała et al. Treatment of steroid-dependent bronchial asthma with cyclosporin Eur Respir J 8 1995 1091 1099
33. H. Nagai, S. Yamaguchi, H. Tanaka, and N. Inagaki Effect of some immunosuppressors on allergic bronchial inflammation and airway hyperresponsiveness in mice Int Arch Allergy Immunol 108 1995 189 195
34. S.Y. Eum, C. Créminon, S. Hailé, J. Lefort, and B.B. Vargaftig Inhibition of airways inflammation by dexamethasone is followed by reduced bronchial hyperreactivity in BP2 mice Clin Exp Allergy 26 1996 971 979 (Pubitemid 26281248)
35. G.R. Zosky, A.N. Larcombe, O.J. White, J.T. Burchell, C. von Garnier, and P.G. Holt et al. Airway hyperresponsiveness is associated with activated CD4 + T cells in the airways Am J Physiol Lung Cell Mol Physiol 297 2009 L373 L379
36. N. Miyahara, B.J. Swanson, K. Takeda, C. Taube, S. Miyahara, and T. Kodama et al. Effector CD8 + T cells mediate inflammation and airway hyper-responsiveness Nat Med 10 2004 865 869 (Pubitemid 39070861)
37. N. Enomoto, E. Hyde, J.Z. Ma, J. Yang, E. Forbes-Blom, and B. Delahunt et al. Allergen-specific CTL require perforin expression to suppress allergic airway inflammation J Immunol 188 2012 1734 1741
38. A. Hasegawa, and T. Nakayama Role of CD69 in the pathogenesis of inflammation Nihon Rinsho Meneki Gakkai Kaishi 33 2010 189 195
39. H. Chakir, H. Wang, D.E. Lefebvre, J. Webb, and F.W. Scott T-bet/GATA-3 ratio as a measure of the Th1/Th2 cytokine profile in mixed cell populations: predominant role of GATA-3 J Immunol Methods 278 2003 157 169 (Pubitemid 37281199)
40. C.T. Weaver, R.D. Hatton, P.R. Mangan, and L.E. Harrington IL-17 family cytokines and the expanding diversity of effector T cell lineages Annu Rev Immunol 25 2007 821 852 (Pubitemid 46697925)
41. S. Nakae, Y. Komiyama, A. Nambu, K. Sudo, M. Iwase, and I. Homma et al. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses Immunity 17 2002 375 387 (Pubitemid 35279557)
42. L.A. Tesmer, S.K. Lundy, S. Sarkar, and D.A. Fox Th17 cells in human disease Immunol Rev 223 2008 87 113 (Pubitemid 351986173)
43. E.S. Hwang Transcriptional regulation of T helper 17 cell differentiation Yonsei Med J 51 2010 484 491
44. A. Nataraju, D. Saini, S. Ramachandran, N. Benshoff, W. Liu, and W. Chapman et al. Oleanolic Acid, a plant triterpenoid, significantly improves survival and function of islet allograft Transplantation 88 2009 987 994
45. R. Martin, M. Hernández, C. Córdova, and M.L. Nieto Natural triterpenes modulate immune-inflammatory markers of experimental autoimmune encephalomyelitis: therapeutic implications for multiple sclerosis Br J Pharmacol 166 2012 1708 1723
46. K. Nemeth, A. Keane-Myers, J.M. Brown, D.D. Metcalfe, J.D. Gorham, and V.G. Bundoc et al. Bone marrow stromal cells use TGF-beta to suppress allergic responses in a mouse model of ragweed-induced asthma Proc Natl Acad Sci U S A 107 2010 5652 5657
47. S.G. Zheng Regulatory T, cells vs. Th17: differentiation of Th17 versus Treg, are the mutually exclusive? Am J Clin Exp Immunol 2 2013 94 106
48. E. Bettelli, M. Dastrange, and M. Oukka Foxp3 interacts with nuclear factor of activated T cells and NF-kappa B to repress cytokine gene expression and effector functions of T helper cells Proc Natl Acad Sci U S A 102 2005 5138 5143
49. A. Bharadwaj, and D.K. Agrawal Immunomodulation in asthma: a distant dream or a close reality? Int Immunopharmacol 4 2004 495 511 (Pubitemid 38501657)
50. H. Jin, Q. Luo, Y. Zheng, M. Nurahmat, J. Wu, and B. Li et al. CD4 + CD25 + Foxp3 + T cells contribute to the antiasthmatic effects of Astragalus membranaceus extract in a rat model of asthma Int Immunopharmacol 15 1 2013 42 49