Anti-Allergic Cromones Inhibit Histamine and Eicosanoid Release from Activated Human and Murine Mast Cells by Releasing Annexin A1

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Yazid, Samia ^b   Sinniah, Ajantha ^a   Solito, Egle ^a   Calder, Virginia ^b   Flower, Rod J ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANNEXIN; ANTIALLERGIC AGENT; CROMOGLYCATE DISODIUM; CROMONE; DEXAMETHASONE; HISTAMINE; ICOSANOID; KETOTIFEN; LIPOCORTIN 1; MONOCLONAL ANTIBODY; NEDOCROMIL; NEUTRALIZING ANTIBODY; PROSTAGLANDIN D2; PROTEIN KINASE C; RECOMBINANT ANX A1; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ALLERGY; ANIMAL CELL; ARTICLE; ASTHMA; BONE MARROW CELL; CELL CULTURE; CONTROLLED STUDY; CROSS LINKING; DRUG MECHANISM; ENZYME LINKED IMMUNOSORBENT ASSAY; HISTAMINE RELEASE; HUMAN; HUMAN CELL; INCUBATION TIME; MAST CELL; MOUSE; NONHUMAN; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; WILD TYPE;

ANIMALS; ANNEXIN A1; ANTI-ALLERGIC AGENTS; ANTI-ASTHMATIC AGENTS; ANTIBODIES, ANTI-IDIOTYPIC; CELLS, CULTURED; CROMOLYN SODIUM; DEXAMETHASONE; EICOSANOIDS; HISTAMINE RELEASE; HUMANS; IMMUNOGLOBULIN E; MAST CELLS; MICE; MICE, KNOCKOUT; NEDOCROMIL; PHOSPHORYLATION; PROSTAGLANDIN D2; RECOMBINANT PROTEINS;

EID: 84875057059     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058963     Document Type: Article

References (71)

1. Cox JS, (1967) Disodium cromoglycate (FPL 670) ('Intal'): a specific inhibitor of reaginic antibody-antigen mechanisms. Nature 216: 1328-1329.
2. Cook EB, Stahl JL, Barney NP, Graziano FM, (2002) Mechanisms of antihistamines and mast cell stabilizers in ocular allergic inflammation. Curr Drug Targets Inflamm Allergy 1: 167-180.
3. Grace RH, Gent AE, Hellier MD, (1987) Comparative trial of sodium cromoglycate enemas with prednisolone enemas in the treatment of ulcerative colitis. Gut 28: 88-92.
4. Rintala RJ, Lindahl H, (2001) Sodium cromoglycate in the management of chronic or recurrent enterocolitis in patients with Hirschsprung's disease. J Pediatr Surg 36: 1032-1035.
5. Murphy S, Kelly HW, (1987) Cromolyn sodium: a review of mechanisms and clinical use in asthma. Drug Intell Clin Pharm 21: 22-35.
6. Wasserman SI, (1995) Immunopharmacologic profile of nedocromil sodium. Allergy Proc 16: 67-71.
7. Abraham WM, (1989) Effect of nedocromil sodium on antigen-induced airway responses in allergic sheep. Drugs 37 (Suppl 1):: 78-86; discussion 127-136.
8. Abraham WM, Sielczak MW, Wanner A, Perruchoud AP, Blinder L, et al. (1988) Cellular markers of inflammation in the airways of allergic sheep with and without allergen-induced late responses. Am Rev Respir Dis 138: 1565-1571.
9. Corbel M, Lagente V, Theret N, Germain N, Clement B, et al. (1999) Comparative effects of betamethasone, cyclosporin and nedocromil sodium in acute pulmonary inflammation and metalloproteinase activities in bronchoalveolar lavage fluid from mice exposed to lipopolysaccharide. Pulm Pharmacol Ther 12: 165-171.
10. Du T, Sapienza S, Wang CG, Renzi PM, Pantano R, et al. (1996) Effect of nedocromil sodium on allergen-induced airway responses and changes in the quantity of airway smooth muscle in rats. J Allergy Clin Immunol 98: 400-407.
11. Evans TW, Rogers DF, Aursudkij B, Chung KF, Barnes PJ, (1988) Inflammatory mediators involved in antigen-induced airway microvascular leakage in guinea pigs. Am Rev Respir Dis 138: 395-399.
12. Folkerts G, De Clerck F, Reijnart I, Span P, Nijkamp FP, (1993) Virus-induced airway hyperresponsiveness in the guinea-pig: possible involvement of histamine and inflammatory cells. Br J Pharmacol 108: 1083-1093.
13. Lapa e SilvaJR, Ruffie C, Vargaftig BB, Pretolani M, (1995) Modulation of the bronchial inflammation in sensitized guinea-pigs by FK506, nedocromil sodium and dexamethasone. Eur Respir J 8: 1321-1327.
14. Barnes PJ, (1993) Anti-inflammatory therapy for asthma. Annu Rev Med 44: 229-242.
15. Bleecker ER, Mason PL, Moore WC (1996) Clinical effects of nedocromil sodium on allergen-related mechanisms. J Allergy Clin Immunol 98S118-123; discussion S140-112.
16. Viscardi RM, Hasday JD, Gumpper KF, Taciak V, Campbell AB, et al. (1997) Cromolyn sodium prophylaxis inhibits pulmonary proinflammatory cytokines in infants at high risk for bronchopulmonary dysplasia. Am J Respir Crit Care Med 156: 1523-1529.
17. Cox JS, (1970) Recent developments concerned with the mode of action of disodium cromoglycate (Intal). Arerugi 19: 832-835.
18. Cox JS, Altounyan RE, (1970) Nature and modes of action of disodium cromoglycate (Lomudal). Respiration 27 (Suppl):: 292-309.
19. Cox JS, Beach JE, Blair AM, Clarke AJ, King J, et al. (1970) Disodium cromoglycate (Intal). Adv Drug Res 5: 115-196.
20. Orr TS (1989) Development of preclinical models for testing antiasthma drugs. Drugs 37 Suppl 1: 113-116; discussion 127-136.
21. Galatowicz G, Ajayi Y, Stern ME, Calder VL, (2007) Ocular anti-allergic compounds selectively inhibit human mast cell cytokines in vitro and conjunctival cell infiltration in vivo. Clin Exp Allergy 37: 1648-1656.
22. Raud J, Konrad D, Dahlen SE, (1995) Delayed anti-inflammatory action of nedocromil sodium in the rat paw is dependent on de novo protein synthesis. Eur J Pharmacol 282: 207-211.
23. Tarayre JP, Delhon A, Aliaga M, Barbara M, Bruniquel F, et al. (1989) Pharmacological studies on zymosan inflammation in rats and mice. 2: Zymosan-induced pleurisy in rats. Pharmacol Res 21: 385-395.
24. Tarayre JP, Delhon A, Aliaga M, Barbara M, Bruniquel F, et al. (1989) Pharmacological studies on zymosan inflammation in rats and mice. 1: Zymosan-induced paw oedema in rats and mice. Pharmacol Res 21: 375-384.
25. Tarayre JP, Lauressergues H, (1982) Modulation by various locally applied anti-inflammatory and anti-allergic compounds of the immune and non-immune inflammation induced by picryl chloride in mice. Agents Actions 12: 662-670.
26. Zuo Y, Perkins NM, Tracey DJ, Geczy CL, (2003) Inflammation and hyperalgesia induced by nerve injury in the rat: a key role of mast cells. Pain 105: 467-479.
27. Kuriyama K, Hiyama Y, Nagatahira R, Okuda T, Saito K, et al. (1986) An antiallergic activity of disodium cromoglycate unrelated to mast cell activation. Agents Actions 18: 473-478.
28. Mattoli S, Mezzetti M, Fasoli A, Patalano F, Allegra L, (1990) Nedocromil sodium prevents the release of 15-hydroxyeicosatetraenoic acid from human bronchial epithelial cells exposed to toluene diisocyanate in vitro. Int Arch Allergy Appl Immunol 92: 16-22.
29. Radeau T, Godard P, Chavis C, Michel FB, Descomps B, et al. (1993) Effect of nedocromil sodium on sulfidopeptide leukotrienes-stimulated human alveolar macrophages in asthma. Pulm Pharmacol 6: 27-31.
30. D'Acquisto F, Perretti M, Flower RJ, (2008) Annexin-A1: a pivotal regulator of the innate and adaptive immune systems. Br J Pharmacol 155: 152-169.
31. Bandeira-Melo C, Bonavita AG, Diaz BL, PM ES, Carvalho VF, et al. (2005) A novel effect for annexin 1-derived peptide ac2-26: reduction of allergic inflammation in the rat. J Pharmacol Exp Ther 313: 1416-1422.
32. Lee SH, Kim DW, Kim HR, Woo SJ, Kim SM, et al. (2012) Anti-inflammatory effects of Tat-Annexin protein on ovalbumin-induced airway inflammation in a mouse model of asthma. Biochem Biophys Res Commun 417: 1024-1029.
33. Chung YW, Oh HY, Kim JY, Kim JH, Kim IY, (2004) Allergen-induced proteolytic cleavage of annexin-1 and activation of cytosolic phospholipase A2 in the lungs of a mouse model of asthma. Proteomics 4: 3328-3334.
34. Ng FS, Wong KY, Guan SP, Mustafa FB, Kajiji TS, et al. (2011) Annexin-1-deficient mice exhibit spontaneous airway hyperresponsiveness and exacerbated allergen-specific antibody responses in a mouse model of asthma. Clin Exp Allergy 41: 1793-1803.
35. Ahluwalia A, Mohamed RW, Flower RJ, (1994) Induction of lipocortin 1 by topical steroid in rat skin. Biochem Pharmacol 48: 1647-1654.
36. Goulding NJ, Godolphin JL, Sharland PR, Peers SH, Sampson M, et al. (1990) Anti-inflammatory lipocortin 1 production by peripheral blood leucocytes in response to hydrocortisone. Lancet 335: 1416-1418.
37. Peers SH, Smillie F, Elderfield AJ, Flower RJ, (1993) Glucocorticoid-and non-glucocorticoid induction of lipocortins (annexins) 1 and 2 in rat peritoneal leucocytes in vivo. Br J Pharmacol 108: 66-72.
38. Perretti M, Flower RJ, (1996) Measurement of lipocortin 1 levels in murine peripheral blood leukocytes by flow cytometry: modulation by glucocorticoids and inflammation. Br J Pharmacol 118: 605-610.
39. Mulla A, Leroux C, Solito E, Buckingham JC, (2005) Correlation between the antiinflammatory protein annexin 1 (lipocortin 1) and serum cortisol in subjects with normal and dysregulated adrenal function. J Clin Endocrinol Metab 90: 557-562.
40. Oliani SM, Christian HC, Manston J, Flower RJ, Perretti M, (2000) An immunocytochemical and in situ hybridization analysis of annexin 1 expression in rat mast cells: modulation by inflammation and dexamethasone. Lab Invest 80: 1429-1438.
41. Croxtall JD, Choudhury Q, Flower RJ, (2000) Glucocorticoids act within minutes to inhibit recruitment of signalling factors to activated EGF receptors through a receptor-dependent, transcription-independent mechanism. Br J Pharmacol 130: 289-298.
42. John CD, Christian HC, Morris JF, Flower RJ, Solito E, et al. (2003) Kinase-dependent regulation of the secretion of thyrotrophin and luteinizing hormone by glucocorticoids and annexin 1 peptides. J Neuroendocrinol 15: 946-957.
43. Solito E, Mulla A, Morris JF, Christian HC, Flower RJ, et al. (2003) Dexamethasone induces rapid serine-phosphorylation and membrane translocation of annexin 1 in a human folliculostellate cell line via a novel nongenomic mechanism involving the glucocorticoid receptor, protein kinase C, phosphatidylinositol 3-kinase, and mitogen-activated protein kinase. Endocrinology 144: 1164-1174.
44. Solito E, Christian HC, Festa M, Mulla A, Tierney T, et al. (2006) Post-translational modification plays an essential role in the translocation of annexin A1 from the cytoplasm to the cell surface. Faseb J 20: 1498-1500.
45. Bena S, Brancaleone V, Wang JM, Perretti M, Flower RJ (2012) Annexin A1 interaction with FPR2/ALX: identification of distinct domains and downstream associated signalling. J Biol Chem.
46. Gavins FN, Yona S, Kamal AM, Flower RJ, Perretti M, (2003) Leukocyte antiadhesive actions of annexin 1: ALXR- and FPR-related anti-inflammatory mechanisms. Blood 101: 4140-4147.
47. Hayhoe RP, Kamal AM, Solito E, Flower RJ, Cooper D, et al. (2006) Annexin 1 and its bioactive peptide inhibit neutrophil-endothelium interactions under flow: indication of distinct receptor involvement. Blood 107: 2123-2130.
48. Pieretti S, Di Giannuario A, De Felice M, Perretti M, Cirino G, (2004) Stimulus-dependent specificity for annexin 1 inhibition of the inflammatory nociceptive response: the involvement of the receptor for formylated peptides. Pain 109: 52-63.
49. Yazid S, Leoni G, Getting SJ, Cooper D, Solito E, et al. (2010) Antiallergic cromones inhibit neutrophil recruitment onto vascular endothelium via annexin-A1 mobilization. Arterioscler Thromb Vasc Biol 30: 1718-1724.
50. Yazid S, Solito E, Christian H, McArthur S, Goulding N, et al. (2009) Cromoglycate drugs suppress eicosanoid generation in U937 cells by promoting the release of Anx-A1. Biochem Pharmacol 77: 1814-1826.
51. Dahl C, Saito H, Nielsen HV, Schiotz PO, (2002) The establishment of a combined serum-free and serum-supplemented culture method of obtaining functional cord blood-derived human mast cells. J Immunol Methods 262: 137-143.
52. Shichijo M, Inagaki N, Nakai N, Kimata M, Nakahata T, et al. (1998) The effects of anti-asthma drugs on mediator release from cultured human mast cells. Clin Exp Allergy 28: 1228-1236.
53. Church MK, Hiroi J, (1987) Inhibition of IgE-dependent histamine release from human dispersed lung mast cells by anti-allergic drugs and salbutamol. Br J Pharmacol 90: 421-429.
54. Kay AB, Walsh GM, Moqbel R, MacDonald AJ, Nagakura T, et al. (1987) Disodium cromoglycate inhibits activation of human inflammatory cells in vitro. J Allergy Clin Immunol 80: 1-8.
55. Pearce FL, Befus AD, Gauldie J, Bienenstock J, (1982) Mucosal mast cells. II. Effects of anti-allergic compounds on histamine secretion by isolated intestinal mast cells. J Immunol 128: 2481-2486.
56. Oka T, Kalesnikoff J, Starkl P, Tsai M, Galli SJ, (2012) Evidence questioning cromolyn's effectiveness and selectivity as a 'mast cell stabilizer' in mice. Lab Invest 92: 1472-1482.
57. Okayama Y, Benyon RC, Rees PH, Lowman MA, Hillier K, et al. (1992) Inhibition profiles of sodium cromoglycate and nedocromil sodium on mediator release from mast cells of human skin, lung, tonsil, adenoid and intestine. Clin Exp Allergy 22: 401-409.
58. Sung CP, Saunders HL, Krell RD, Chakrin LW, (1977) Studies on the mechanism of tachyphylaxis to disodium cromoglycate. Int Arch Allergy Appl Immunol 55: 374-384.
59. Sung CP, Saunders HL, Lenhardt E, Chakrin LW, (1977) Further studies on the tachyphylaxis to DSCG. The effects of concentration and temperature. Int Arch Allergy Appl Immunol 55: 385-394.
60. Thomson DS, Evans DP, (1973) Inhibition of immediate hypersensitivity reactions by disodium cromoglycate. Clin Exp Immunol 13: 537-544.
61. Theoharides TC, Sieghart W, Greengard P, Douglas WW, (1980) Antiallergic drug cromolyn may inhibit histamine secretion by regulating phosphorylation of a mast cell protein. Science 207: 80-82.
62. Wells E, Mann J, (1983) Phosphorylation of a mast cell protein in response to treatment with anti-allergic compounds. Implications for the mode of action of sodium cromoglycate. Biochem Pharmacol 32: 837-842.
63. Theoharides TC, Wang L, Pang X, Letourneau R, Culm KE, et al. (2000) Cloning and cellular localization of the rat mast cell 78-kDa protein phosphorylated in response to the mast cell "stabilizer" cromolyn. J Pharmacol Exp Ther 294: 810-821.
64. Bansal SK, Jha A, Jaiswal AS, Chhabra SK, (1997) Increased levels of protein kinase C in lymphocytes in asthma: possible mechanism of regulation. Eur Respir J 10: 308-313.
65. Lucas AM, Shuster S, (1987) Cromolyn inhibition of protein kinase C activity. Biochem Pharmacol 36: 562-565.
66. Sagi-Eisenberg R, (1985) Possible role for a calcium-activated phospholipid-dependent protein kinase in mode of action of DSCG. Trends in Pharmacological Sciences 6: 198-200.
67. Wang L, Correia I, Basu S, Theoharides TC, (1999) Ca2+ and phorbol ester effect on the mast cell phosphoprotein induced by cromolyn. Eur J Pharmacol 371: 241-249.
68. Schwender CF, (1981) Human leukocyte alkaline phosphatase inhibition by allergic mediator release inhibitors. Biochem Pharmacol 30: 217-222.
69. Schwender CF, Sunday BR, Decker VL, (1982) Alkaline phosphatase inhibition by a series of pyrido[2,1-b]quinazolines: A possible relationship with cromolyn-like antiallergy activity. J Med Chem 25: 742-745.
70. Jenkins L, Brea J, Smith NJ, Hudson BD, Reilly G, et al. (2010) Identification of novel species-selective agonists of the G-protein-coupled receptor GPR35 that promote recruitment of beta-arrestin-2 and activate Galpha13. Biochem J 432: 451-459.
71. Yang Y, Lu JY, Wu X, Summer S, Whoriskey J, et al. (2010) G-protein-coupled receptor 35 is a target of the asthma drugs cromolyn disodium and nedocromil sodium. Pharmacology 86: 1-5.