FcεRI β-chain ITAM amplifies PI3K-signaling to ensure synergistic degranulation response via FcεRI and adenosine receptors

European Journal of Immunology

Volumn 40, Issue 4, 2010, Pages 1205-1217

  Nunomura, Satoshi ^a   Gon, Yasuhiro ^a   Yoshimaru, Tetsuro ^a   Kashiwakura, Junichi ^b   Kawakami, Toshiaki ^b   Ra, Chisei ^a  

^a NIHON UNIVERSITY   (Japan)

^b LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

Asthma; Mast cells; Signal transduction

Indexed keywords

ADENOSINE; ADENOSINE RECEPTOR; FC EPSILON RECEPTOR I BETA CHAIN; FC RECEPTOR; GRB2 ASSOCIATED BINDER 2; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; ITAM PROTEIN; NON T CELL ACTIVATION LINKER; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN; UNCLASSIFIED DRUG; FC EPSILON RECEPTOR I BETA CHAIN, MOUSE; FC-EPSILON RECEPTOR I BETA-CHAIN, MOUSE; GAB2 PROTEIN, MOUSE; HYBRID PROTEIN; IMMUNOGLOBULIN E; IMMUNOGLOBULIN E RECEPTOR; PHOSPHOPROTEIN; PHOSPHOTYROSINE;

ANIMAL CELL; ARTICLE; CELL MUTANT; CONTROLLED STUDY; GENE MUTATION; IMMUNOSTIMULATION; MAST CELL; MAST CELL DEGRANULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CALCIUM SIGNALING; DEGRANULATION; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; MOUSE STRAIN; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING; PROTEIN TERTIARY STRUCTURE; SITE DIRECTED MUTAGENESIS;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADENOSINE; ANIMALS; CALCIUM SIGNALING; CELL DEGRANULATION; IMMUNOGLOBULIN E; MAST CELLS; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; MUTAGENESIS, SITE-DIRECTED; PHOSPHOPROTEINS; PHOSPHORYLATION; PHOSPHOTYROSINE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; RECEPTOR CROSS-TALK; RECEPTORS, IGE; RECEPTORS, PURINERGIC P1; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION;

EID: 77951037178     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200939651     Document Type: Article

References (45)

1. Metzger, H., The receptor with high affinity for IgE. Immunol. Rev. 1992. 125: 37-48.
2. Gould, H. J., Sutton, B. J., Beavil, A. J., Beavil, R. L., McCloskey, N., Coker, H. A., Fear, D. and Smurthwaite, L., The biology of IGE and the basis of allergic disease. Annu. Rev. Immunol. 2003. 21: 579-628.
3. Iwaki, S., Tkaczyk, C., Satterthwaite, A. B., Halcomb, K., Beaven, M. A., Metcalfe, D. D. and Gilfillan, A. M., Btk plays a crucial role in the amplification of FcεRI-mediated mast cell activation by kit. J. Biol. Chem. 2005. 280: 40261-40270.
4. Qiao, H., Andrade, M. V., Lisboa, F. A., Morgan, K. and Beaven, M. A., FcεR1 and toll-like receptors mediate synergistic signals to markedly augment production of inflammatory cytokines in murine mast cells. Blood 2006. 107: 610-618. (Pubitemid 43076385)
5. Toda, M., Dawson, M., Nakamura, T., Munro, P. M., Richardson, R. M., Bailly, M. and Ono, S. J., Impact of engagement of FcεRI and CC chemokine receptor 1 on mast cell activation and motility. J. Bio.l Chem. 2004. 279: 48443-48448. (Pubitemid 39541002)
6. Haskó , G., and Cronstein, B. N., Adenosine: an endogenous regulator of innate immunity. Trends Immunol. 2004. 25: 33-39.
7. Driver, A. G., Kukoly, C. A., Ali, S. and Mustafa, S. J., Adenosine in bronchoalveolar lavage fluid in asthma. Am. Rev. Respir. Dis. 1993. 148: 91-97.
8. Laffargue, M., Calvez, R., Finan, P., Trifilieff, A., Barbier, M., Altruda, F., Hirsch, E. andWymann, M. P., Phosphoinositide 3-kinase γ is an essential amplifier of mast cell function. Immunity 2002.16: 441-451.
9. Bohnacker, T., Marone, R., Collmann, E., Calvez, R., Hirsch, E. and Wymann, M. P., PI3Kγ adaptor subunits define coupling to degranulation and cell motility by distinct PtdIns(3,4,5)P3 pools in mast cells. Sci. Signal. 2009. 2: ra27.
10. Bryant, D. H. and Burns, M. H., Bronchial histamine reactivity: its relationship to the reactivity of the bronchi to allergens. Clin. Allergy 1976. 6: 523-532.
11. Dohi, M., Okudaira, H., Sugiyama, H., Tsurumachi, K., Suko, M., Nakagawa, T. and Morita, Y. et al., Bronchial responsiveness to mite allergen in atopic dermatitis without asthma. Int. Arch. Allergy Appl. Immunol. 1990. 92: 138-142.
12. M'Raihi, L., Charpin, D., Thibaudon, M. and Vervloet, D., Bronchial challenge to house dust can induce immediate bronchoconstriction in allergic asthmatic patients. Ann. Allergy 1990. 65: 485-488.
13. Ali, H., Cunha-Melo, J. R., Saul, W. F. and Beaven, M. A., Activation of phospholipase C via adenosine receptors provides synergistic signals for secretion in antigen-stimulated RBL-2H3 cells. Evidence for a novel adenosine receptor. J. Biol. Chem. 1990. 265: 745-753.
14. Ali, H., Choi, O. H., Fraundorfer, P. F., Yamada, K., Gonzaga, H. M. and Beaven, M. A., Sustained activation of phospholipase D via adenosine A3 receptors is associated with enhancement of antigen- and Ca(21)-ionophore- induced secretion in a rat mast cell line. J. Pharmacol. Exp. Ther. 1996. 276: 837-845.
15. Ramkumar, V., Stiles, G. L., Beaven, M. A. and Ali, H., The A3 adenosine receptor is the unique adenosine receptor which facilitates release of allergic mediators in mast cells. J. Biol. Chem. 1993. 268: 16887-16890.
16. Salvatore, C. A., Tilley, S. L., Latour, A. M., Fletcher, D. S., Koller, B. H. and Jacobson, M. A., Disruption of the A(3) adenosine receptor gene in mice and its effect on stimulated inflammatory cells. J. Biol. Chem. 2000. 275: 4429-4434.
17. Kim, M. S., Rådinger, M. and Gilfillan, A. M., The multiple roles of phosphoinositide 3-kinase in mast cell biology. Trends Immunol. 2008. 29: 493-501.
18. Xiao, W., Nishimoto, H., Hong, H., Kitaura, J., Nunomura, S., Maeda-Yamamoto, M., Kawakami, Y., et al., Positive and negative regulation of mast cell activation by Lyn via the FcεRI. J. Immunol. 2005. 175: 6885-6892. (Pubitemid 41598934)
19. Nunomura, S., Yoshimaru, T. and Ra, C., Na-Tosyl-Phe chloromethyl ketone prevents granule movement and mast cell synergistic degranulation elicited by costimulation of antigen and adenosine. Life Sci. 2008. 83: 242-249.
20. Nunomura, S., Gon, Y., Yoshimaru, T., Suzuki, Y., Nishimoto, H., Kawakami, T. and Ra, C., Role of the FcεRI β-chain ITAM as a signal regulator for mast cell activation with monomeric IgE. Int. Immunol. 2005. 17: 685-694.
21. Furumoto, Y., Nunomura, S., Terada, T., Rivera, J. and Ra, C., The FcεRIb immunoreceptor tyrosine-based activation motif exerts inhibitory control on MAPK and IΚB kinase phosphorylation and mast cell cytokine production. J. Biol. Chem. 2004. 279: 49177-49187.
22. Burrows, B., Martinez, F. D., Halonen, M., Barbee, R. A. and Cline, M. G., Association of asthma with serum IgE levels and skin-test reactivity to allergens. N. Engl. J. Med. 1989. 320: 271-277.
23. Hsu, C. and MacGlashan, D., Jr., IgE antibody up-regulates high affinity IgE binding on murine bone marrow-derived mast cells. Immunol. Lett. 1996. 52: 129-134.
24. Yamaguchi, M., Lantz, C. S., Oettgen, H. C., Katona, I. M., Fleming, T., Miyajima, I., Kinet, J. P. and Galli, S. J., IgE enhances mouse mast cell FcεRI expression in vitro and in vivo: evidence for a novel amplification mechanism in IgE-dependent reactions. J. Exp. Med. 1997. 185: 663-672.
25. Kubo, S., Matsuoka, K., Taya, C., Kitamura, F., Takai, T., Yonekawa, H. and Karasuyama, H., Drastic up-regulation of FcεRI on mast cells is induced by IgE binding through stabilization and accumulation of FcεRI on the cell surface. J. Immunol. 2001. 167: 3427-3434. (Pubitemid 32852588)
26. Kubota, T., Mukai, K., Minegishi, Y. and Karasuyama, H., Different stabilities of the structurally related receptors for IgE and IgG on the cell surface are determined by length of the stalk region in their α-chains. J. Immunol. 2006. 176: 7008-7014. (Pubitemid 43787881)
27. Gu, H., Saito,K., Klaman, L.D., Shen, J., Fleming, T.,Wang, Y., Pratt, J.C. et al., Essential role for Gab2 in the allergic response. Nature 2001. 412: 186-190. (Pubitemid 32674715)
28. Yu, M., Lowell, C. A., Neel, B. G. and Gu, H., Scaffolding adapter Grb2-associated binder 2 requires Syk to transmit signals from FcεRI. J. Immunol. 2006. 176: 2421-2429. (Pubitemid 43201692)
29. Chan, J., Liao, W., Lau, H. Y. and Wong, W. S., Gab2 antisense oligonucleotide blocks rat basophilic leukemic cell functions. Int. Immunopharmacol. 2007. 7: 937-944.
30. Tkaczyk, C., Horejsi, V., Iwaki, S., Draber, P., Samelson, L. E., Satterthwaite, A. B., Nahm, D. H. et al., NTAL phosphorylation is a pivotal link between the signaling cascades leading to human mast cell degranulation following Kit activation and FcεRI aggregation. Blood 2004. 104: 207-214. (Pubitemid 38879859)
31. Iwaki, S., Spicka, J., Tkaczyk, C., Jensen, B. M., Furumoto, Y., Charles, N., and Kovarova, M. et al., Kit- and FceRI-induced differential phosphorylation of the transmembrane adaptor molecule NTAL/LAB/LAT2 allows flexibility in its scaffolding function in mast cells. Cell Signal. 2008. 20: 195-205. (Pubitemid 350138381)
32. Tarlo, S. M., Broder, I., Corey, P., Chan-Yeung, M., Ferguson, A., Becker, A., Rogers, C. et al., The role of symptomatic colds in asthma exacerbations: Influence of outdoor allergens and air pollutants. J. Allergy Clin. Immunol. 2001. 108: 52-58.
33. Cohn, L., Elias, J. A. and Chupp, G. L., Asthma: mechanisms of disease persistence and progression. Annu. Rev. Immunol. 2004. 22: 789-815.
34. Lukacs, N. W., Smit, J., Lindell, D., and Schaller, M., Respiratory syncytial virus-induced pulmonary disease and exacerbation of allergic asthma. Contrib. Microbiol. 2007. 14: 68-82.
35. Bartlett, N. W., Walton, R. P., Edwards, M. R., Aniscenko, J., Caramori, G., Zhu, J., Glanville, N. et al., Mouse models of rhinovirus-induced disease and exacerbation of allergic airway inflammation. Nat. Med. 2008. 14: 199-204.
36. Kuehn, H. S., Beaven, M. A., Ma, H. T., Kim, M. S., Metcalfe, D. D. and Gilfillan, A. M., Synergistic activation of phospholipases Cγ and Cβ: a novel mechanism for PI3K-independent enhancement of FcεRI-induced mast cell mediator release. Cell Signal. 2008. 20: 625-636.
37. Ali, K., Bilancio, A., Thomas, M., Pearce, W., Gilfillan, A. M., Tkaczyk, C., Kuehn, N. et al., Essential role for the p110δ phosphoinositide 3-kinase in the allergic response. Nature 2004. 431: 1007-1011. (Pubitemid 39434424)
38. Crouin, C., Arnaud, M., Gesbert, F., Camonis, J. and Bertoglio, J., A yeast two-hybrid study of human p97/Gab2 interactions with its SH2 domain-containing binding partners. FEBS Lett. 2001. 495: 148-153. (Pubitemid 32397695)
39. Nishida, K., Yamasaki, S., Ito, Y., Kabu, K., Hattori, K., Tezuka, T., Nishizumi, H. et al., FceRI-mediated mast cell degranulation requires calcium-independent microtubule-dependent translocation of granules to the plasma membrane. J. Cell. Biol. 2005. 170: 115-126.
40. Huang, F., Tong, X., Deng, H., Fu, L. and Zhang, R., Inhibition of the antigen-induced activation of RBL-2H3 cells by Gab2 siRNA. Cell. Mol. Immunol. 2008. 5: 433-438.
41. D'Amato, G., Role of anti-IgE monoclonal antibody (omalizumab) in the treatment of bronchial asthma and allergic respiratory diseases. Eur. J. Pharmacol. 2006. 533: 302-307.
42. Boulet, L. P., Chapman, K. R., Côté, J., Kalra, S., Bhagat, R., Swystun, V. A ., Laviolette, M. et al., Inhibitory effects of an anti-IgE antibody E25 on allergen-induced early asthmatic response.Am. J. Respir. Crit. CareMed. 1997. 155: 1835-1840.
43. Djukanović, R .,Wilson, S. J., Kraft, M., Jarjour, N. N., Steel,M., Chung, K . F., Bao, W. et al., Effects of treatment with anti-immunoglobulin E antibody omalizumab on airway inflammation in allergic asthma. Am. J. Respir. Crit. Care Med. 2004. 170: 583-593.
44. Yagi, T., Aizawa, S., Tokunaga, T., Shigetani, Y., Takeda, N. and Ikawa, Y., A role for Fyn tyrosine kinase in the suckling behaviour of neonatal mice. Nature 1993. 366: 742-745. (Pubitemid 24038514)
45. Hiraoka, S., Furumoto, Y., Koseki, H., Takagaki, Y., Taniguchi, M., Okumura, K. and Ra, C., Fc receptor b subunit is required for full activation of mast cells through Fc receptor engagement. Int. Immunol. 1999. 11: 199-207.