Regulation of cytosolic phospholipase A 2 phosphorylation by proteolytic cleavage of annexin A1 in activated mast cells

Journal of Immunology

Volumn 188, Issue 11, 2012, Pages 5665-5673

  Kwon, Joon Hyun ^a   Lee, Jea Hwang ^a   Kim, Ki Soon ^a   Chung, Youn Wook ^b   Kim, Ick Young ^a  

^a Korea University   (South Korea)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CYTOSOLIC PHOSPHOLIPASE A2; ICOSANOID; LIPOCORTIN 1;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL ACTIVATION; CELL MEMBRANE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOSOL; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FATTY ACID SYNTHESIS; MAST CELL; MAST CELL DEGRANULATION; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; RAT; UPREGULATION;

ANIMALS; ANNEXIN A1; CELL LINE; CELLS, CULTURED; EICOSANOIDS; INFLAMMATION MEDIATORS; MAST CELLS; MICE; MICE, INBRED C57BL; PHOSPHOLIPASES A2, CYTOSOLIC; PHOSPHORYLATION; PROTEOLYSIS;

EID: 84862094449     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102306     Document Type: Article

References (50)

1. Abraham, S. N., and A. L. St John. 2010. Mast cell-orchestrated immunity to pathogens. Nat. Rev. Immunol. 10: 440-452.
2. Hofmann, A. M., and S. N. Abraham. 2009. New roles for mast cells in modulating allergic reactions and immunity against pathogens. Curr. Opin. Immunol. 21: 679-686.
3. Brown, J. M., T. M. Wilson, and D. D. Metcalfe. 2008. The mast cell and allergic diseases: role in pathogenesis and implications for therapy. Clin. Exp. Allergy 38: 4-18. (Pubitemid 350233400)
4. Gilfillan, A. M., and C. Tkaczyk. 2006. Integrated signalling pathways for mast-cell activation. Nat. Rev. Immunol. 6: 218-230. (Pubitemid 43290991)
5. Rivera, J. 2006. Adaptors discriminate mast-cell cytokine production from eicosanoid production and degranulation. Trends Immunol. 27: 251-253. (Pubitemid 43850402)
6. Mekori, Y. A., and D. D. Metcalfe. 2000. Mast cells in innate immunity. Immunol. Rev. 173: 131-140. (Pubitemid 30095217)
7. Bruhns, P., S. Frëmont, and M. Daëron. 2005. Regulation of allergy by Fc receptors. Curr. Opin. Immunol. 17: 662-669.
8. Beaven, M. A., and R. A. Baumgartner. 1996. Downstream signals initiated in mast cells by Fc epsilon RI and other receptors. Curr. Opin. Immunol. 8: 766-772.
9. Gerke, V., and S. E. Moss. 2002. Annexins: from structure to function. Physiol. Rev. 82: 331-371. (Pubitemid 34654456)
10. Lim, L. H., and S. Pervaiz. 2007. Annexin 1: the new face of an old molecule. FASEB J. 21: 968-975. (Pubitemid 46495688)
11. Wang, W., and C. E. Creutz. 1994. Role of the amino-terminal domain in regulating interactions of annexin I with membranes: effects of amino-terminal truncation and mutagenesis of the phosphorylation sites. Biochemistry 33: 275-282. (Pubitemid 24046524)
12. Rescher, U., V. Goebeler, A. Wilbers, and V. Gerke. 2006. Proteolytic cleavage of annexin 1 by human leukocyte elastase. Biochim. Biophys. Acta 1763: 1320-1324. (Pubitemid 44779860)
13. Vong, L., F. D'Acquisto, M. Pederzoli-Ribeil, L. Lavagno, R. J. Flower, V. Witko-Sarsat, and M. Perretti. 2007. Annexin 1 cleavage in activated neutrophils: a pivotal role for proteinase 3. J. Biol. Chem. 282: 29998-30004. (Pubitemid 350035249)
14. Sakaguchi, M., H. Murata, H. Sonegawa, Y. Sakaguchi, J. Futami, M. Kitazoe, H. Yamada, and N. H. Huh. 2007. Truncation of annexin A1 is a regulatory lever for linking epidermal growth factor signaling with cytosolic phospholipase A2 in normal and malignant squamous epithelial cells. J. Biol. Chem. 282: 35679-35686. (Pubitemid 350277150)
15. Solito, E., A. Mulla, J. F. Morris, H. C. Christian, R. J. Flower, and J. C. Buckingham. 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. (Pubitemid 36428456)
16. Pepinsky, R. B., and L. K. Sinclair. 1986. Epidermal growth factor-dependent phosphorylation of lipocortin. Nature 321: 81-84. (Pubitemid 16080891)
17. Williams, S. L., I. R. Milne, C. J. Bagley, J. R. Gamble, M. A. Vadas, S. M. Pitson, and Y. Khew-Goodall. 2010. A proinflammatory role for proteolytically cleaved annexin A1 in neutrophil transendothelial migration. J. Immunol. 185: 3057-3063.
18. Pederzoli-Ribeil, M., F. Maione, D. Cooper, A. Al-Kashi, J. Dalli, M. Perretti, and F. D'Acquisto. 2010. Design and characterization of a cleavage-resistant Annexin A1 mutant to control inflammation in the microvasculature. Blood 116: 4288-4296.
19. Chung, Y. W., H. Y. Oh, J. Y. Kim, J. H. Kim, and I. Y. Kim. 2004. Allergeninduced proteolytic cleavage of annexin-1 and activation of cytosolic phospholipase A2 in the lungs of a mouse model of asthma. Proteomics 4: 3328-3334.
20. Samuelsson, B. 1987. An elucidation of the arachidonic acid cascade. Discovery of prostaglandins, thromboxane and leukotrienes. Drugs 33(Suppl. 1): 2-9. (Pubitemid 17070100)
21. Eum, S. Y., K. Maghni, Q. Hamid, H. Campbell, D. H. Eidelman, and J. G. Martin. 2003. Involvement of the cysteinyl-leukotrienes in allergen-induced airway eosinophilia and hyperresponsiveness in the mouse. Am. J. Respir. Cell Mol. Biol. 28: 25-32. (Pubitemid 36017047)
22. Ghosh, M., D. E. Tucker, S. A. Burchett, and C. C. Leslie. 2006. Properties of the Group IV phospholipase A2 family. Prog. Lipid Res. 45: 487-510.
23. Glover, S., M. S. de Carvalho, T. Bayburt, M. Jonas, E. Chi, C. C. Leslie, and M. H. Gelb. 1995. Translocation of the 85-kDa phospholipase A2 from cytosol to the nuclear envelope in rat basophilic leukemia cells stimulated with calcium ionophore or IgE/antigen. J. Biol. Chem. 270: 15359-15367.
24. Evans, J. H., D. M. Spencer, A. Zweifach, and C. C. Leslie. 2001. Intracellular calcium signals regulating cytosolic phospholipase A2 translocation to internal membranes. J. Biol. Chem. 276: 30150-30160.
25. Lin, L. L., M. Wartmann, A. Y. Lin, J. L. Knopf, A. Seth, and R. J. Davis. 1993. cPLA2 is phosphorylated and activated by MAP kinase. Cell 72: 269-278. (Pubitemid 23044941)
26. Hefner, Y., A. G. Borsch-Haubold, M. Murakami, J. I. Wilde, S. Pasquet, D. Schieltz, F. Ghomashchi, J. R. Yates, III, C. G. Armstrong, A. Paterson, et al. 2000. Serine 727 phosphorylation and activation of cytosolic phospholipase A2 by MNK1-related protein kinases. J. Biol. Chem. 275: 37542-37551. (Pubitemid 32004863)
27. Hirasawa, N., F. Santini, and M. A. Beaven. 1995. Activation of the mitogen-activated protein kinase/cytosolic phospholipase A2 pathway in a rat mast cell line. Indications of different pathways for release of arachidonic acid and secretory granules. J. Immunol. 154: 5391-5402.
28. Kim, S., J. Ko, J. H. Kim, E. C. Choi, and D. S. Na. 2001. Differential effects of annexins I, II, III, and V on cytosolic phospholipase A2 activity: specific interaction model. FEBS Lett. 489: 243-248. (Pubitemid 32126417)
29. Kim, K. M., D. K. Kim, Y. M. Park, C. K. Kim, and D. S. Na. 1994. Annexin-I inhibits phospholipase A2 by specific interaction, not by substrate depletion. FEBS Lett. 343: 251-255. (Pubitemid 24136523)
30. 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.
31. 2+ mobilization in FcepsilonRI signaling to degranulation in mast cells. J. Allergy Clin. Immunol. 114: 1085-1092.
32. Funk, C. D. 2001. Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294: 1871-1875. (Pubitemid 33101574)
33. Kamal, A. M., R. J. Flower, and M. Perretti. 2005. An overview of the effects of annexin 1 on cells involved in the inflammatory process. Mem. Inst. Oswaldo Cruz 100(Suppl. 1): 39-47.
34. Warne, J. P., C. D. John, H. C. Christian, J. F. Morris, R. J. Flower, D. Sugden, E. Solito, G. E. Gillies, and J. C. Buckingham. 2006. Gene deletion reveals roles for annexin A1 in the regulation of lipolysis and IL-6 release in epididymal adipose tissue. Am. J. Physiol. Endocrinol. Metab. 291: E1264-E1273. (Pubitemid 44904034)
35. -/- mouse. FASEB J. 17: 253-255.
36. Yang, Y. H., E. F. Morand, S. J. Getting, M. Paul-Clark, D. L. Liu, S. Yona, R. Hannon, J. C. Buckingham, M. Perretti, and R. J. Flower. 2004. Modulation of inflammation and response to dexamethasone by Annexin 1 in antigen-induced arthritis. Arthritis Rheum. 50: 976-984. (Pubitemid 38326199)
37. Yazid, S., S. S. Ayoub, E. Solito, S. McArthur, P. Vo, N. Dufton, and R. J. Flower. 2010. Anti-allergic drugs and the Annexin-A1 system. Pharmacol. Rep. 62: 511-517.
38. Lloret, S., and J. J. Moreno. 1994. Effect of nonapeptide fragments of uteroglobin and lipocortin I on oedema and mast cell degranulation. Eur. J. Pharmacol. 264: 379-384. (Pubitemid 24335480)
39. Bandeira-Melo, C., A. G. Bonavita, B. L. Diaz, P. M. E Silva, V. F. Carvalho, P. J. Jose, R. J. Flower, M. Perretti, and M. A. Martins. 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.
40. Kimata, M., N. Inagaki, T. Kato, T. Miura, I. Serizawa, and H. Nagai. 2000. Roles of mitogen-activated protein kinase pathways for mediator release from human cultured mast cells. Biochem. Pharmacol. 60: 589-594. (Pubitemid 30389626)
41. Kuehn, H. S., E. J. Swindle, M. S. Kim, M. A. Beaven, D. D. Metcalfe, and A. M. Gilfillan. 2008. The phosphoinositide 3-kinase-dependent activation of Btk is required for optimal eicosanoid production and generation of reactive oxygen species in antigen-stimulated mast cells. J. Immunol. 181: 7706-7712.
42. Qiu, Z. H., M. A. Gijón, M. S. de Carvalho, D. M. Spencer, and C. C. Leslie. 1998. The role of calcium and phosphorylation of cytosolic phospholipase A2 in regulating arachidonic acid release in macrophages. J. Biol. Chem. 273: 8203-8211.
43. Schalkwijk, C. G., M. A. van der Heijden, G. Bunt, R. Maas, L. G. Tertoolen, P. M. van Bergen en Henegouwen, A. J. Verkleij, H. van den Bosch, and J. Boonstra. 1996. Maximal epidermal growth-factor-induced cytosolic phospholipase A2 activation in vivo requires phosphorylation followed by an increased intracellular calcium concentration. Biochem. J. 313: 91-96.
44. Wong, A., M. N. Cook, S. M. Hwang, H. M. Sarau, J. J. Foley, and S. T. Crooke. 1992. Stimulation of leukotriene production and membrane translocation of 5-lipoxygenase by cross-linking of the IgE receptors in RBL-2H3 cells. Biochemistry 31: 4046-4053.
45. Hundley, T. R., A. R. Prasad, and M. A. Beaven. 2001. Elevated levels of cyclooxygenase-2 in antigen-stimulated mast cells is associated with minimal activation of p38 mitogen-activated protein kinase. J. Immunol. 167: 1629-1636. (Pubitemid 32703165)
46. Evans, J. H., D. J. Fergus, and C. C. Leslie. 2002. Inhibition of the MEK1/ERK pathway reduces arachidonic acid release independently of cPLA2 phosphorylation and translocation. BMC Biochem. 3: 30.
47. Tucker, D. E., M. Ghosh, F. Ghomashchi, R. Loper, S. Suram, B. S. John, M. Girotti, J. G. Bollinger, M. H. Gelb, and C. C. Leslie. 2009. Role of phosphorylation and basic residues in the catalytic domain of cytosolic phospholipase A2alpha in regulating interfacial kinetics and binding and cellular function. J. Biol. Chem. 284: 9596-9611.
48. Oliani, S. M., H. C. Christian, J. Manston, R. J. Flower, and M. Perretti. 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.
49. Kim, S. W., H. J. Rhee, J. Ko, Y. J. Kim, H. G. Kim, J. M. Yang, E. C. Choi, and D. S. Na. 2001. Inhibition of cytosolic phospholipase A2 by annexin I. Specific interaction model and mapping of the interaction site. J. Biol. Chem. 276: 15712-15719.
50. Herbert, S. P., A. F. Odell, S. Ponnambalam, and J. H. Walker. 2007. The confluence-dependent interaction of cytosolic phospholipase A2-alpha with annexin A1 regulates endothelial cell prostaglandin E2 generation. J. Biol. Chem. 282: 34468-34478.