Food allergen-induced mast cell degranulation is dependent on PI3K-mediated reactive oxygen species production and upregulation of store-operated calcium channel subunits

Scandinavian Journal of Immunology

Volumn 78, Issue 1, 2013, Pages 35-43

  Yang, B ^a   Yang, C ^a   Wang, P ^b   Li, J ^a   Huang, H ^a   Ji, Q ^a   Liu, J ^a   Liu, Z ^a  

^a Shenzhen University School of Medicine   (China)

^b Shenzhen Institute for Drug Control   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; FOOD ALLERGEN; HISTAMINE; IMMUNOGLOBULIN E; INTRACELLULAR CALCIUM SENSING PROTEIN; MESSENGER RNA; OVALBUMIN; PHOSPHATIDYLINOSITOL 3 KINASE; REACTIVE OXYGEN METABOLITE; STROMAL INTERACTION MOLECULE 1; THAPSIGARGIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM TRANSPORT; CELL STRUCTURE; CONFOCAL MICROSCOPE; ELECTRON MICROSCOPE; FEMALE; IN VITRO STUDY; MAST CELL DEGRANULATION; NONHUMAN; PERITONEUM LAVAGE; PERITONEUM MAST CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RAT; RECEPTOR UPREGULATION; SUPERNATANT; TH2 CELL; WESTERN BLOTTING;

ANIMALS; CALCIUM; CALCIUM CHANNELS; CELL DEGRANULATION; FEMALE; FOOD HYPERSENSITIVITY; IMMUNOGLOBULIN E; MAST CELLS; MEMBRANE GLYCOPROTEINS; OVALBUMIN; PHOSPHATIDYLINOSITOL 3-KINASES; RATS; RATS, INBRED BN; REACTIVE OXYGEN SPECIES; TH2 CELLS; UP-REGULATION;

EID: 84880276072     PISSN: 03009475     EISSN: 13653083     Source Type: Journal    
DOI: 10.1111/sji.12062     Document Type: Article

References (43)

1. Gupta R, Sheikh A, Strachan DP, Anderson HR. Time trends in allergic disorders in the UK. Thorax 2007;62:91-6.
2. Poulos LM, Waters AM, Correll PK, Loblay RH, Marks GB. Trends in hospitalizations for anaphylaxis, angioedema, and urticaria in Australia, 1993-1994 to 2004-2005. J Allergy Clin Immunol 2007;120:878-84.
3. Lin RY, Anderson AS, Shah SN, Nurruzzaman F. Increasing anaphylaxis hospitalizations in the first 2 decades of life: New York State, 1990-2006. Ann Allergy Asthma Immunol 2008;101:387-93.
4. Sampson HA. Epidemiology of food allergy. Pediatr Allergy Immunol 1996;7:42-50.
5. Grundy J, Matthews S, Bateman B, Dean T, Arshad SH. Rising prevalence of allergy to peanut in children: data from 2 sequential cohorts. J Allergy Clin Immunol 2002;110:784-9.
6. Untersmayr E, Jensen-Jarolim E. Mechanisms of type I food allergy. Pharmacol Ther 2006;112:787-98.
7. Montalto M, Santoro L, D'Onofrio F et al. Adverse reactions to food: allergies and intolerances. Dig Dis 2008;26:96-103.
8. Stenton GR, Vliagoftis H, Befus AD. Role of intestinal mast cells in modulating gastrointestinal pathophysiology. Ann Allergy Asthma Immunol 1998;81:1-11; quiz 2-5.
9. Yu LC, Perdue MH. Role of mast cells in intestinal mucosal function: studies in models of hypersensitivity and stress. Immunol Rev 2001;179:61-73.
10. Crowe SE, Soda K, Stanisz AM, Perdue MH. Intestinal permeability in allergic rats: nerve involvement in antigen-induced changes. Am J Physiol 1993;264:G617-23.
11. Lorentz A, Schwengberg S, Sellge G, Manns MP, Bischoff SC. Human intestinal mast cells are capable of producing different cytokine profiles: role of IgE receptor cross-linking and IL-4. J Immunol 2000;164:43-8.
12. Blank U, Rivera J. The ins and outs of IgE-dependent mast-cell exocytosis. Trends Immunol 2004;25:266-73.
13. Fewtrell C, Sherman E. IgE receptor-activated calcium permeability pathway in rat basophilic leukemia cells: measurement of the unidirectional influx of calcium using quin2-buffered cells. Biochemistry 1987;26:6995-7003.
14. Ma HT, Peng Z, Hiragun T, Iwaki S, Gilfillan AM, Beaven MA. Canonical transient receptor potential 5 channel in conjunction with Orai1 and STIM1 allows Sr2+ entry, optimal influx of Ca2+, and degranulation in a rat mast cell line. J Immunol 2008;180:2233-9.
15. Sanchez-Miranda E, Ibarra-Sanchez A, Gonzalez-Espinosa C. Fyn kinase controls FcepsilonRI receptor-operated calcium entry necessary for full degranulation in mast cells. Biochem Biophys Res Commun 2010;391:1714-20.
16. Soboloff J, Spassova MA, Tang XD, Hewavitharana T, Xu W, Gill DL. Orai1 and STIM reconstitute store-operated calcium channel function. J Biol Chem 2006;281:20661-5.
17. Knippels LM, Penninks AH, Spanhaak S, Houben GF. Oral sensitization to food proteins: a Brown Norway rat model. Clin Exp Allergy 1998;28:368-75.
18. Ghannadan M, Baghestanian M, Wimazal F et al. Phenotypic characterization of human skin mast cells by combined staining with toluidine blue and CD antibodies. J Invest Dermatol 1998;111:689-95.
19. Swindle EJ, Metcalfe DD, Coleman JW. Rodent and human mast cells produce functionally significant intracellular reactive oxygen species but not nitric oxide. J Biol Chem 2004;279:48751-9.
20. Yang C, Mo X, Lv J et al. Lipopolysaccharide enhances FcεRI-mediated mast cell degranulation by increasing Ca2+ entry through store-operated Ca2+ channels: implications for LPS exacerbating allergic asthma. Exp Physiol 2012;97:1315-27.
21. De Jonge F, De Laet A, Van Nassauw L et al. In vitro activation of murine DRG neurons by CGRP-mediated mucosal mast cell degranulation. Am J Physiol Gastrointest Liver Physiol 2004;287:G178-91.
22. Rao JN, Rathor N, Zou T et al. STIM1 translocation to the plasma membrane enhances intestinal epithelial restitution by inducing TRPC1-mediated Ca2+ signaling after wounding. Am J Physiol Cell Physiol 2010;299:C579-88.
23. Putney JW Jr. New molecular players in capacitative Ca2+ entry. J Cell Sci 2007;120:1959-65.
24. Deng X, Wang Y, Zhou Y, Soboloff J, Gill DL. STIM and Orai: dynamic intermembrane coupling to control cellular calcium signals. J Biol Chem 2009;284:22501-5.
25. Kuehn HS, Swindle EJ, Kim MS, Beaven MA, Metcalfe DD, Gilfillan AM. 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 2008;181:7706-12.
26. Poulsen LK, Hansen TK, Norgaard A, Vestergaard H, Stahl Skov P, Bindslev-Jensen C. Allergens from fish and egg. Allergy 2001;56 (Suppl. 67):39-42.
27. Knippels LM, van der Kleij HP, Koppelman SJ, Houben GF, Penninks AH. Comparison of antibody responses to hen's egg and cow's milk proteins in orally sensitized rats and food-allergic patients. Allergy 2000;55:251-8.
28. Jia XD, Li N, Wu YN, Yang XG. Studies on BN rats model to determine the potential allergenicity of proteins from genetically modified foods. World J Gastroenterol 2005;11:5381-4.
29. Putney JW Jr. A model for receptor-regulated calcium entry. Cell Calcium 1986;7:1-12.
30. Roos J, DiGregorio PJ, Yeromin AV et al. STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol 2005;169:435-45.
31. Galli SJ, Nakae S, Tsai M. Mast cells in the development of adaptive immune responses. Nat Immunol 2005;6:135-42.
32. Swindle EJ, Metcalfe DD. The role of reactive oxygen species and nitric oxide in mast cell-dependent inflammatory processes. Immunol Rev 2007;217:186-205.
33. Inoue T, Suzuki Y, Yoshimaru T, Ra C. Reactive oxygen species produced up- or downstream of calcium influx regulate proinflammatory mediator release from mast cells: role of NADPH oxidase and mitochondria. Biochim Biophys Acta 2008;1783:789-802.
34. Anastasiou D, Poulogiannis G, Asara JM et al. Inhibition of pyruvate kinase M2 by reactive oxygen species contributes to cellular antioxidant responses. Science 2011;334:1278-83.
35. Cantrell DA. Phosphoinositide 3-kinase signalling pathways. J Cell Sci 2001;114:1439-45.
36. Vanhaesebroeck B, Waterfield MD. Signaling by distinct classes of phosphoinositide 3-kinases. Exp Cell Res 1999;253:239-54.
37. Ptasznik A, Prossnitz ER, Yoshikawa D, Smrcka A, Traynor-Kaplan AE, Bokoch GM. A tyrosine kinase signaling pathway accounts for the majority of phosphatidylinositol 3, 4, 5-trisphosphate formation in chemoattractant-stimulated human neutrophils. J Biol Chem 1996;271:25204-7.
38. Sasaki T, Irie-Sasaki J, Jones RG et al. Function of PI3Kgamma in thymocyte development, T cell activation, and neutrophil migration. Science 2000;287:1040-6.
39. Woo CH, Eom YW, Yoo MH et al. Tumor necrosis factor-alpha generates reactive oxygen species via a cytosolic phospholipase A2-linked cascade. J Biol Chem 2000;275:32357-62.
40. Bae YS, Sung JY, Kim OS et al. Platelet-derived growth factor-induced H(2)O(2) production requires the activation of phosphatidylinositol 3-kinase. J Biol Chem 2000;275:10527-31.
41. Colavitti R, Pani G, Bedogni B et al. Reactive oxygen species as downstream mediators of angiogenic signaling by vascular endothelial growth factor receptor-2/KDR. J Biol Chem 2002;277:3101-8.
42. Suzuki Y, Yoshimaru T, Matsui T et al. Fc epsilon RI signaling of mast cells activates intracellular production of hydrogen peroxide: role in the regulation of calcium signals. J Immunol 2003;171:6119-27.
43. Swindle EJ, Coleman JW, DeLeo FR, Metcalfe DD. FcepsilonRI- and Fcgamma receptor-mediated production of reactive oxygen species by mast cells is lipoxygenase- and cyclooxygenase-dependent and NADPH oxidase-independent. J Immunol 2007;179:7059-71.