Thymoquinone suppressses in vitro production of IL-5 and IL-13 by mast cells in response to lipopolysaccharide stimulation

Inflammation Research

Volumn 56, Issue 8, 2007, Pages 345-351

  El Gazzar, M A ^a,b  

^a UNIVERSITY OF COLORADO   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Inflammation mast cell; Th2 cytokines; Thymoquinone; Transcription factors

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; INTERLEUKIN 13; INTERLEUKIN 5; MESSENGER RNA; PROTEIN C FOS; STRESS ACTIVATED PROTEIN KINASE; THYMOQUINONE; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR GATA; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR GATA 2; TRANSCRIPTION FACTOR NFAT;

ALLERGIC ASTHMA; ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL STIMULATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; IN VIVO STUDY; INFLAMMATORY DISEASE; MAST CELL DEGRANULATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TH2 CELL; TRANSCRIPTION INITIATION; WESTERN BLOTTING;

ANIMALS; ANTI-INFLAMMATORY AGENTS; BENZOQUINONES; CELLS, CULTURED; GATA1 TRANSCRIPTION FACTOR; GATA2 TRANSCRIPTION FACTOR; INTERLEUKIN-13; INTERLEUKIN-5; LIPOPOLYSACCHARIDES; MAST CELLS; NF-KAPPA B; PROMOTER REGIONS (GENETICS); RATS; TRANSCRIPTION FACTOR AP-1;

EID: 34547744423     PISSN: 10233830     EISSN: 1420908X     Source Type: Journal    
DOI: 10.1007/s00011-007-7051-0     Document Type: Article

References (56)

1. Masuda A, Yoshikai Y, Aiba K, Matsuguchi T. Th2 cytokine production from mast cells is directly induced by lipopolysaccharide and distinctly regulated by c-Jun N-terminal kinase and p38 pathways. J Immunol 2002; 169: 3801-10.
2. He SH. Key role of mast cells and their major secretory products in inflammatory bowel disease. World J Gastroenterolol 2004; 10: 309-18.
3. Woolley DE. The mast cell in inflammatory arthritis. N Engl J Med 2003; 348:1709-11.
4. Metcalfe DD, Baram D, Mekori YA. Mast cells. Physiol Rev 1997; 77: 1033-79.
5. Galli SJ, Gordon JR, Wershil BK. Mast cell cytokines in allergy and inflammation. Agents Actions Suppl 1993; 43: 209-20.
6. Gon Y, Nunomura S, Ra C. Common and distinct signalling cascades in the production of tumor necrosis factor-α and interleukin-13 induced by lipopolysacchride in RBL-2H3 cells. Clin Exp Allergy 2005; 35: 635-42.
7. Marone G, Galli SJ, Kitamura Y. Probing the roles of mast cells and basophils in natural and aquired immunity, physiology and disease. Trends Immunol 2002; 23:425-27.
8. Eisenbarth SC, Piggott DA, Huleatt JW, Visintin I, Herrick CA, Bottomly K. Lipopolysaccharide-enhanced, toll-like receptor 4-dependent T helper cell type 2 responses to inhaled antigen. J Exp Med 2002; 196: 1645-51.
9. Burd PR, Thompson WC, Max EE, Mills FC. Activated mast cells produce IL-13. J Exp Med 1995; 181: 1373-80.
10. Bradding P. Human mast cell cytokines. Clin Exp Allergy 1996;26:13-19.
11. Nigo YI, Yamashita M , Hirahara K, Shinnakasu R, Inami M, Kimura M, Hasegawa A, Yoichi Kohno Y, Nakayama T. Regulation of allergic airway inflammation through Toll-like receptor 4-mediated modification of mast cell function. Proc Natl Acad Sci USA 2006; 103: 2286-91.
12. Braun-Fahrlander C, Riedler J, Herz U, Eder W, Waser M, Grize L, Maisch S, Carr D, Gerlach F, Bufe A, Lauener PR, Schierl R, Renz H, Nowak D, von Mutius E. Environmental exposure to endotoxin and its relation to asthma in school-age children. N Engl J Med 2002; 347:869-77.
13. Hamelmann E, Gelfand EW. IL-5-induced airway eosinophilia-the key to asthma. Immunol Rev 2001; 179: 182-91.
14. Foster PS, Hogan SP, Ramsay AJ, Matthaei KI, Young IG. Interleukin 5 deficiency abolishes eosinophilia, airways hyperreactivity, and lung damage in a mouse asthma model. J Exp Med 1996; 183: 195-201.
15. Zhu Z, Homer RJ, Wang Z, Chen Q, Geba GP, Wang J, Zhang Y, Elias JA. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J Clin Invest 1999; 103: 779-88.
16. Houghton PJ, Zerka R, DL-Heras B, Hoult JR. Fixed oil of Nigella sativa and derived thymoquinone inhibit eicosanoid generation in leukocytes and membrane lipid perioxidation. Planta Medica 1995; 61: 33-6.
17. Mutabagani A, El-Mahdy SA. Study of the anti-inflammatory activity of Nigella sativa L and thymoquinone in rats. Saudi Pharm J 1997; 5: 110-13.
18. Mahgoub AA. Thymoquinone protect against experimental colitis in rats. Toxicology Letters 2003; 143: 133-43.
19. El Gazzar M, El Mezayen R, Marecki JC, Nicolls MR, Canastar A, Dreskin SC. Anti-inflammatory effect of thymoquinone in a mouse model of allergic lung inflammation. Int Immunopharmacol 2006; 6:1135-42.
20. Deskin SC, Pribluda VS, Metzger H. IgE receptor-mediated hydrolysis of phosphoinositides by cytoplasts from rat basophilic leukemia cells. J Immunol 1989; 142:4407-15.
21. Seldin DC, Adelman S, Austen KF, Stevens RL, Hein A, Caulfield JP, Woodbury RG. Homology of the rat basophilic leukemia cell and the rat mucosal mast cell. Proc Natl Acad Sci USA 1985; 82: 3871-5.
22. Prieschl EE, Gouilleux-Gruart V, Walker C, Harrer NE, Baumruker T. A nuclear factor of activated T cell-like transcription factor in mast cells is involved in IL-5 gene regulation after IgE antigen stimulation. J Immunol 1995; 154: 6112-9.
23. Masuda A, Yoshikai Y, Kume H, Matsuguchi T. The interaction between GATA proteins and activator protein-1 promotes the transcription of IL-13 in mast cells. J Immunol 2004; 173: 5564-73.
24. Hirasawa N, Izumi S, Linwong W, Obuchi K. Inhibition by dexamethasone of IL-13 production via glucocorticoid receptor-mediated inhibition of c-Jun phosphorylation. FEBS Letters 2003; 554: 489-93.
25. Buitkamp J, Jann O, Fries R. The cattle interleukin-13 gene: genomic organization, chromosomal location, and evolution of the promoter. Immunogenetics 2000; 49: 872-8.
26. Razin E, Szallasi Z, Kazanietz MG, Blumberg PM, Rivera J. Protein kinases C-beta and C-epsilon link the mast cell high-affinity receptor for IgE to the expression of c-fos and c-jun. Proc Natl Acad Sci U S A 1994; 16: 7722-6.
27. Monticelli S, Solymar DC, Rao A. Role of NFAT proteins in IL-13 gene transcription in mast cells.
28. Costa JJ, Weller PF, Galli SJ. The cells of the allergic response: mast cells, basophils, and eosinophils. JAMA 1997; 278: 1815-22.
29. Tulic MK, Wale JL, Holt PG, Sly PD. Modification of the inflammatory reponse to allergen challenge after exposure to bacterial lipopolyssacharide. Am J Respir Cell Mol Biol 2000; 22: 604-12.
30. Strohmeier GR, Walsh JH, Klings ES, Farber HW, Cruikshank WW, Center DM, Fenton MJ. Lipopolyssacharide binding protein potentiates airway reactivity in a murine model of allergic asthma. J Immunol 2001; 166: 2063-70.
31. Holgate ST. Cytokine and anti-cytokine therapy for the treatment of asthma and allergic disease. Cytokine 2004; 28: 152-7.
32. Shakoory B, Fitzgerald SM, Lee SA, Chi LD, Krishnaswamy G. The role of mast cell-derived cytokines in eosinophil biology. J Interferon Cytokine Res 2004; 24: 271-81.
33. Soler M, Matz J, Townley R, Buhl R, O'Brien J, Fox H, Thirlwell J, Gupta N, Della Cioppa G. The anti-IgE antibody omalizumab reduces exacerbations and steroid requirement in allergic asthmatics. Eur Respir J 2001; 18: 254-61.
34. Kips JC, O'Connor BJ, Langley SJ, Woodcock A, Kerstjens HA, Postma DS, Danzig M, Cuss F, Pauwels RA. Effect of SCH55700, a humanized anti-human interleukin-5 antibody, in severe persistent asthma: a pilot study. Am J Respir Crit Care Med 2003; 167: 1655-9.
35. Grunig G, Warnock M, Wakil AE, Venkayya R, Brombacher F, Rennick DM, Sheppard D, Mohrs M, Donaldson DD, Locksley RM, Corry DB. Requirement for IL-13 independently of IL-4 in experimental asthma. Science 1998; 282:2261-3.
36. Wills-Karp M, Luyimbazi J, Xu X, Schofield B, Neben TY, Karp CL, Donaldson DD. Interleukin-13: central mediator of allergic asthma. Science 1998; 282:2258-61.
37. Zhu Z, Homer RJ, Wang Z, Chen Q, Geba GP, Wang J, Zhang Y, Elias JA. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J Clin Invest 1999; 103: 779-88.
38. de Vries JE. The role of IL-13 and its receptor in allergy and in-flammatory responses. J Allergy Clin Immunol 1998; 102: 165-9.
39. Akdis M, Blaser K, Akdis CA. T regulatory cells in allergy: novel concepts in the pathogenesis, prevention, and treatment of allergic diseases. J Allergy Clin Immunol 2005; 116: 961-8.
40. Barnes PJ. Cytokine modulators as novel therapies for asthma. Annu Rev Pharmacol Toxicol 2002; 42: 81-98.
41. Adachi M, Oda N, Kokubu F, Minoguchi K. IL-10 induces a Th2 cell tolerance in allergic asthma. Int Arch Allergy Immunol 1999; 118: 391-4.
42. Chung F. Anti-inflammatory cytokines in asthma and allergy; interleukin-10, interleukin-12, interferon-gamma. Mediators Inflamm 2001; 10: 51-9.
43. de Waal MR, Abrams J, Bennett B, Figdor CG, de Vries JE. Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J Exp Med 1991; 174: 1209-20.
44. Lang R, Patel D, Morris JJ, Rutschman RL, Murray PJ. Shaping gene expression in activated and resting primary macrophages by IL-10. J Immunol 2002; 169: 2253-63.
45. Lee HJ, O'Garra A, Arai K, Arai N. Characterization of cis-regulatory elements and nuclear factors conferring Th2-specific expression of the IL-5 gene: A role for a GATA-binding protein. J Immunol 1998: 160: 2343-52.
46. Schwenger GT, Fournier R, Kok CC, Mordvinov VA, Yeoman D, Sanderson CJ. GATA-3 has dual regulatory functions in human interleukin-5 transcription. J Biol Chem 2001; 276:48502-9.
47. Zon LI, Gurish MF, Stevens RL, Mather C, Renyolds DS, Austen KF, Orkin SH. GATA-binding transcription factors in mast cells regulate the promoter of the mast cell carboxypeptidase A gene. J Biol Chem 1991; 266: 22948-53.
48. Nakamura Y, Ghaffar O, Olivenstein R, Taha RA, Soussi-Gounni A, Zhang DH, Ray A, Hamid Q. Gene expression of the GATA-3 transcription factor is increased in atopic asthma. J Allergy Clin Immunol 1999; 103: 215-22.
49. Zhang DH, Yang L, Cohn L, Parkyn L, Homer R, Ray P, Ray A. Inhibition of allergic airway inflammation in a murine model of asthma by expression of a dominant negative mutant of GATA-3. Immunity 1999; 11: 473-82.
50. Kurata H, Lee HJ, O'Garra A, Arai N. Ectopic expression of activated Stat6 induces the expression of Th2-specific cytokines and transcription factors in developing Th1 cells. Immunity 1999; 11: 677-88.
51. Ho IC, Glimcher LH. Transcription: tantalizing times for T cells. Cell 2002; 109: S109-20.
52. Murphy KM, Ouyang W, Farrar JD, Yang J, Ranganath S, Asnagli H, Afkarian M, Murphy TL. Signaling and transcription in T helper development. Ann Rev Immunol 2000; 18: 451-94.
53. Lorentz A, Klopp I, Gebhardt T, Manns MP, Biscoff SC. Role of activator protein 1, nuclear factor-kB, and nuclear factor of activated T cells in IgE receptor-mediated cytokine expression in human mast cells. J Allergy Clin Immunol 2003; 111: 1062-8.
54. Klein M, Klein-Hessling S, Palmetshofer A, Serfling E, Tertilt C, Bopp T, Heib V, Becker M, Taube C, Schild H, Schmitt E, Stassen M. Specific and redundant roles for NF-AT transcription factors in the expression of mast cell-drived cytokines. J Immunol 2006; 117: 6667-74.
55. McBride K, Charron F, Lefebvre C, Nemer M. Interaction with GATA transcription factors provides a mechanism for cell-specific effects of c-Fos. Oncogene. 2003; 22: 8403-8412.
56. Zheng W, Flavell RA. The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell 1997; 89: 587-96.