Ragweed pollen-mediated IgE-independent release of biogenic amines from mast cells via induction of mitochondrial dysfunction

Molecular Immunology

Volumn 46, Issue 13, 2009, Pages 2505-2514

  Chodaczek, Grzegorz ^a   Bacsi, Attila ^b   Dharajiya, Nilesh ^a   Sur, Sanjiv ^a   Hazra, Tapas K ^a   Boldogh, Istvan ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF DEBRECEN   (Hungary)

Author keywords

Degranulation; Mast cells; Mitochondria; Reactive oxygen species

Indexed keywords

BETA N ACETYLHEXOSAMINIDASE; BIOGENIC AMINE; HISTAMINE; IMMUNOGLOBULIN E; INTERLEUKIN 4; POLLEN EXTRACT; PROTEIN KINASE C DELTA; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; REACTIVE OXYGEN METABOLITE; SEROTONIN;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVATION; ENZYME RELEASE; MAST CELL; MAST CELL DEGRANULATION; NONHUMAN; PRIORITY JOURNAL; RAGWEED POLLEN;

AMBROSIA; ANIMALS; BENZOPHENANTHRIDINES; CELL LINE, TUMOR; DOSE-RESPONSE RELATIONSHIP, DRUG; EXOCYTOSIS; FLOW CYTOMETRY; HISTAMINE RELEASE; IMMUNOGLOBULIN E; INTERLEUKIN-4; MAST CELLS; MITOCHONDRIA; PLANT EXTRACTS; POLLEN; PROTEIN KINASE C; REACTIVE OXYGEN SPECIES; SEROTONIN; VACUOLAR PROTON-TRANSLOCATING ATPASES;

AMBROSIA; EQUUS ASINUS;

EID: 67650409701     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2009.05.023     Document Type: Article

References (80)

1. Alfonso A., Cabado A.G., Vieytes M.R., and Botana L.M. Calcium-pH crosstalks in rat mast cells: cytosolic alkalinization, but not intracellular calcium release, is a sufficient signal for degranulation. Br. J. Pharmacol. 130 (2000) 1809-1816
2. Alvarez de Toledo G., Fernandez-Chacon R., and Fernandez J.M. Release of secretory products during transient vesicle fusion. Nature 363 (1993) 554-558
3. Bachelet M., Marchand F., Souil E., Francois D., Mariethoz E., Weyer A., and Polla B.S. Expression and localization of heat shock proteins in rat basophilic leukemia cells: differential modulation by degranulation, thermal or oxidative stress. Allergy 57 (2002) 791-797
4. Bacsi A., Choudhury B.K., Dharajiya N., Sur S., and Boldogh I. Subpollen particles: carriers of allergenic proteins and oxidases. J. Allergy Clin. Immunol. 118 (2006) 844-850
5. Bacsi A., Dharajiya N., Choudhury B.K., Sur S., and Boldogh I. Effect of pollen-mediated oxidative stress on immediate hypersensitivity reactions and late-phase inflammation in allergic conjunctivitis. J. Allergy Clin. Immunol. 116 (2005) 836-843
6. Bacsi A., Woodberry M., Widger W., Papaconstantinou J., Mitra S., Peterson J.W., and Boldogh I. Localization of superoxide anion production to mitochondrial electron transport chain in 3-NPA-treated cells. Mitochondrion 6 (2006) 235-244
7. Bagarozzi Jr. D.A., Potempa J., and Travis J. Purification and characterization of an arginine-specific peptidase from ragweed (Ambrosia artemisiifolia) pollen. Am. J. Respir. Cell Mol. Biol. 18 (1998) 363-369
8. Banan A., Fields J.Z., Farhadi A., Talmage D.A., Zhang L., and Keshavarzian A. Activation of delta-isoform of protein kinase C is required for oxidant-induced disruption of both the microtubule cytoskeleton and permeability barrier of intestinal epithelia. J. Pharmacol. Exp. Ther. 303 (2002) 17-28
9. Beyenbach K.W., and Wieczorek H. The V-type H+ ATPase: molecular structure and function, physiological roles and regulation. J. Exp. Biol. 209 (2006) 577-589
10. Boldogh I., Bacsi A., Choudhury B.K., Dharajiya N., Alam R., Hazra T.K., Mitra S., Goldblum R.M., and Sur S. ROS generated by pollen NADPH oxidase provide a signal that augments antigen-induced allergic airway inflammation. J. Clin. Invest. 115 (2005) 2169-2179
11. Burgoyne R.D., and Morgan A. Secretory granule exocytosis. Physiol. Rev. 83 (2003) 581-632
12. Camacho M., Machado J.D., Alvarez J., and Borges R. Intravesicular calcium release mediates the motion and exocytosis of secretory organelles: a study with adrenal chromaffin cells. J. Biol. Chem. 283 (2008) 22383-22389
13. Chen Y.W., Lang M.L., and Wade W.F. Protein kinase C-alpha and -delta are required for FcalphaR (CD89) trafficking to MHC class II compartments and FcalphaR-mediated antigen presentation. Traffic 5 (2004) 577-594
14. 2+ mobilization in FcepsilonRI signaling to degranulation in mast cells. J. Allergy Clin. Immunol. 114 (2004) 1085-1092
15. Corry D.B., and Kheradmand F. Biology and therapeutic potential of the interleukin-4/interleukin-13 signaling pathway in asthma. Am. J. Respir. Med. 1 (2002) 185-193
16. Degli Esposti M., Ghelli A., Crimi M., Estornell E., Fato R., and Lenaz G. Complex I and complex III of mitochondria have common inhibitors acting as ubiquinone antagonists. Biochem. Biophys. Res. Commun. 190 (1993) 1090-1096
17. Del Prete A., Zaccagnino P., Di Paola M., Saltarella M., Oliveros Celis C., Nico B., Santoro G., and Lorusso M. Role of mitochondria and reactive oxygen species in dendritic cell differentiation and functions. Free Radic. Biol. Med. 44 (2008) 1443-1451
18. Demo S.D., Masuda E., Rossi A.B., Throndset B.T., Gerard A.L., Chan E.H., Armstrong R.J., Fox B.P., Lorens J.B., Payan D.G., Scheller R.H., and Fisher J.M. Quantitative measurement of mast cell degranulation using a novel flow cytometric annexin-V binding assay. Cytometry 36 (1999) 340-348
19. Fernandez-Chacon R., and Alvarez de Toledo G. Cytosolic calcium facilitates release of secretory products after exocytotic vesicle fusion. FEBS Lett. 363 (1995) 221-225
20. Frossi B., De Carli M., Daniel K.C., Rivera J., and Pucillo C. Oxidative stress stimulates IL-4 and IL-6 production in mast cells by an APE/Ref-1-dependent pathway. Eur. J. Immunol. 33 (2003) 2168-2177
21. Frossi B., De Carli M., and Pucillo C. The mast cell: an antenna of the microenvironment that directs the immune response. J. Leukoc. Biol. 75 (2004) 579-585
22. Frossi B., Rivera J., Hirsch E., and Pucillo C. Selective activation of Fyn/PI3K and p38 MAPK regulates IL-4 production in BMMC under nontoxic stress condition. J. Immunol. 178 (2007) 2549-2555
23. 2 impairs inflammatory mediator release from immunologically stimulated RBL-2H3 cells through a redox-sensitive, calcium-dependent mechanism. Inflamm. Res. 50 (2001) 341-349
24. Gunawan H., Takai T., Kamijo S., Wang X.L., Ikeda S., Okumura K., and Ogawa H. Characterization of proteases, proteins, and eicosanoid-like substances in soluble extracts from allergenic pollen grains. Int. Arch. Allergy Immunol. 147 (2008) 276-288
25. Ha H.C., and Snyder S.H. Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 13978-13982
26. 2+ and guanine nucleotides: an all-or-none event. J. Cell Biol. 123 (1993) 585-593
27. Hunt L.W., Gleich G.J., Kita H., Weiler D.A., Schroeder D.R., Vuk-Pavlovic Z., and Sur S. Removal of bronchoalveolar cells augments the late eosinophilic response to segmental allergen challenge. Clin. Exp. Allergy 32 (2002) 210-216
28. Hunt N.H., Cook E.P., and Fragonas J.C. Interference with oxidative processes inhibits proliferation of human peripheral blood lymphocytes and murine B-lymphocytes. Int. J. Immunopharmacol. 13 (1991) 1019-1026
29. Inoue T., Suzuki Y., Yoshimaru T., and 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 1783 (2008) 789-802
30. Isersky C., Taurog J.D., Poy G., and Metzger H. Triggering of cultured neoplastic mast cells by antibodies to the receptor for IgE. J. Immunol. 121 (1978) 549-558
31. Johansen T. Energy metabolism in rat mast cells in relation to histamine secretion. Pharmacol. Toxicol. 61 Suppl. 2 (1987) 1-20
32. Kojima T., Obata K., Mukai K., Sato S., Takai T., Minegishi Y., and Karasuyama H. Mast cells and basophils are selectively activated in vitro and in vivo through CD200R3 in an IgE-independent manner. J. Immunol. 179 (2007) 7093-7100
33. 2. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 11233-11237
34. Kotake Y. Pharmacologic properties of phenyl N-tert-butylnitrone. Antioxid. Redox Signal. 1 (1999) 481-499
35. Lindstedt K.A., and Kovanen P.T. Isolation of mast cell granules. Curr. Protoc. Cell Biol. (2006) (Chapter 3, Unit 3.16)
36. Litonjua A.A., Carey V.J., Burge H.A., Weiss S.T., and Gold D.R. Parental history and the risk for childhood asthma. Does mother confer more risk than father?. Am. J. Respir. Crit. Care Med. 158 (1998) 176-181
37. Liu Y., Graham C., Parravicini V., Brown M.J., Rivera J., and Shaw S. Protein kinase C theta is expressed in mast cells and is functionally involved in Fcepsilon receptor I signaling. J. Leukoc. Biol. 69 (2001) 831-840
38. Llado A., Tebar F., Calvo M., Moreto J., Sorkin A., and Enrich C. Protein kinaseCdelta-calmodulin crosstalk regulates epidermal growth factor receptor exit from early endosomes. Mol. Biol. Cell 15 (2004) 4877-4891
39. Logan M.R., Odemuyiwa S.O., and Moqbel R. Understanding exocytosis in immune and inflammatory cells: the molecular basis of mediator secretion. J. Allergy Clin. Immunol. 111 (2003) 923-932 (quiz 933)
40. Loschen G., Azzi A., Richter C., and Flohe L. Superoxide radicals as precursors of mitochondrial hydrogen peroxide. FEBS Lett. 42 (1974) 68-72
41. Lu M., Vergara S., Zhang L., Holliday L.S., Aris J., and Gluck S.L. The amino-terminal domain of the E subunit of vacuolar H(+)-ATPase (V-ATPase) interacts with the H subunit and is required for V-ATPase function. J. Biol. Chem. 277 (2002) 38409-38415
42. Ma J.S., Haydar T.F., and Radoja S. Protein kinase C delta localizes to secretory lysosomes in CD8+ CTL and directly mediates TCR signals leading to granule exocytosis-mediated cytotoxicity. J. Immunol. 181 (2008) 4716-4722
43. Matsui T., Suzuki Y., Yamashita K., Yoshimaru T., Suzuki-Karasaki M., Hayakawa S., Yamaki M., and Shimizu K. Diphenyleneiodonium prevents reactive oxygen species generation, tyrosine phosphorylation, and histamine release in RBL-2H3 mast cells. Biochem. Biophys. Res. Commun. 276 (2000) 742-748
44. Menon I.A., Shirwadkar S., and Ranadive N.S. Nature of the oxygen species generated by xanthine oxidase involved in secretory histamine release from mast cells. Biochem. Cell Biol. 67 (1989) 397-403
45. Metcalfe D.D., Baram D., and Mekori Y.A. Mast cells. Physiol. Rev. 77 (1997) 1033-1079
46. Mortaz E., Redegeld F.A., Sarir H., Karimi K., Raats D., Nijkamp F.P., and Folkerts G. Cigarette smoke stimulates the production of chemokines in mast cells. J. Leukoc. Biol. 83 (2008) 575-580
47. Munitz A., Piliponsky A.M., and Levi-Schaffer F. IgE-independent activation of human mast cells indicates their role in the late phase reaction of allergic inflammation. Cell Tissue Bank 4 (2003) 25-28
48. Nagata M. Inflammatory cells and oxygen radicals. Curr. Drug Targets Inflamm. Allergy 4 (2005) 503-504
49. Nelson N., Perzov N., Cohen A., Hagai K., Padler V., and Nelson H. The cellular biology of proton-motive force generation by V-ATPases. J. Exp. Biol. 203 (2000) 89-95
50. Nishida K., Yamasaki S., Ito Y., Kabu K., Hattori K., Tezuka T., Nishizumi H., Kitamura D., Goitsuka R., Geha R.S., Yamamoto T., Yagi T., and Hirano T. Fc{epsilon}RI-mediated mast cell degranulation requires calcium-independent microtubule-dependent translocation of granules to the plasma membrane. J. Cell Biol. 170 (2005) 115-126
51. Obermuller S., Lindqvist A., Karanauskaite J., Galvanovskis J., Rorsman P., and Barg S. Selective nucleotide-release from dense-core granules in insulin-secreting cells. J. Cell Sci. 118 (2005) 4271-4282
52. Ohmori H., Komoriya K., Azuma A., Kurozumi S., and Hashimoto Y. Xanthine oxidase-induced histamine release from isolated rat peritoneal mast cells: involvement of hydrogen peroxide. Biochem. Pharmacol. 28 (1979) 333-334
53. Panduri V., Weitzman S.A., Chandel N.S., and Kamp D.W. Mitochondrial-derived free radicals mediate asbestos-induced alveolar epithelial cell apoptosis. Am. J. Physiol. Lung Cell Mol. Physiol. 286 (2004) L1220-1227
54. Park S.K., and Beaven M.A. Mechanism of upregulation of the inhibitory regulator, src-like adaptor protein (SLAP), by glucocorticoids in mast cells. Mol. Immunol. 46 (2009) 492-497
55. Parravicini V., Gadina M., Kovarova M., Odom S., Gonzalez-Espinosa C., Furumoto Y., Saitoh S., Samelson L.E., O'Shea J.J., and Rivera J. Fyn kinase initiates complementary signals required for IgE-dependent mast cell degranulation. Nat. Immunol. 3 (2002) 741-748
56. Pernas-Sueiras O., Alfonso A., Vieytes M.R., and Botana L.M. PKC and cAMP positively modulate alkaline-induced exocytosis in the human mast cell line HMC-1. J. Cell. Biochem. 99 (2006) 1651-1663
57. Pihel K., Hsieh S., Jorgenson J.W., and Wightman R.M. Quantal corelease of histamine and 5-hydroxytryptamine from mast cells and the effects of prior incubation. Biochemistry 37 (1998) 1046-1052
58. Puri N., and Roche P.A. Mast cells possess distinct secretory granule subsets whose exocytosis is regulated by different SNARE isoforms. Proc. Natl. Acad. Sci. U.S.A. 105 (2008) 2580-2585
59. Raby B.A., Klanderman B., Murphy A., Mazza S., Camargo Jr. C.A., Silverman E.K., and Weiss S.T. A common mitochondrial haplogroup is associated with elevated total serum IgE levels. J. Allergy Clin. Immunol. 120 (2007) 351-358
60. Raha S., and Robinson B.H. Mitochondria, oxygen free radicals, disease and ageing. Trends Biochem. Sci. 25 (2000) 502-508
61. Rajotte D., Stearns C.D., and Kabcenell A.K. Isolation of mast cell secretory lysosomes using flow cytometry. Cytometry A 55 (2003) 94-101
62. Rivera J., and Gilfillan A.M. Molecular regulation of mast cell activation. J. Allergy Clin. Immunol. 117 (2006) 1214-1225 (quiz 1226)
63. Saroussi S., and Nelson N. Vacuolar H(+)-ATPase-an enzyme for all seasons. Pflugers Arch. 457 (2009) 581-587
64. Schumacher K. Endomembrane proton pumps: connecting membrane and vesicle transport. Curr. Opin. Plant Biol. 9 (2006) 595-600
65. Seldin D.C., Adelman S., Austen K.F., Stevens R.L., Hein A., Caulfield J.P., and Woodbury R.G. Homology of the rat basophilic leukemia cell and the rat mucosal mast cell. Proc. Natl. Acad. Sci. U.S.A. 82 (1985) 3871-3875
66. Smith A.J., Pfeiffer J.R., Zhang J., Martinez A.M., Griffiths G.M., and Wilson B.S. Microtubule-dependent transport of secretory vesicles in RBL-2H3 cells. Traffic 4 (2003) 302-312
67. St-Pierre J., Buckingham J.A., Roebuck S.J., and Brand M.D. Topology of superoxide production from different sites in the mitochondrial electron transport chain. J. Biol. Chem. 277 (2002) 44784-44790
68. Stassen M., Hultner L., and Schmitt E. Classical and alternative pathways of mast cell activation. Crit. Rev. Immunol. 22 (2002) 115-140
69. 2+ dependence of mast cell degranulation. J. Leukoc. Biol. 79 (2006) 508-518
70. Swindle E.J., Hunt J.A., and Coleman J.W. A comparison of reactive oxygen species generation by rat peritoneal macrophages and mast cells using the highly sensitive real-time chemiluminescent probe pholasin: inhibition of antigen-induced mast cell degranulation by macrophage-derived hydrogen peroxide. J. Immunol. 169 (2002) 5866-5873
71. Traidl-Hoffmann C., Kasche A., Jakob T., Huger M., Plotz S., Feussner I., Ring J., and Behrendt H. Lipid mediators from pollen act as chemoattractants and activators of polymorphonuclear granulocytes. J. Allergy Clin. Immunol. 109 (2002) 831-838
72. Turrens J.F. Mitochondrial formation of reactive oxygen species. J. Physiol. 552 (2003) 335-344
73. Uvnas B. The molecular mechanism of nondegranulative release of biogenic amines. J. Physiol. Pharmacol. 42 (1991) 211-219
74. Wang Y., and Floor E. Hydrogen peroxide inhibits the vacuolar H+-ATPase in brain synaptic vesicles at micromolar concentrations. J. Neurochem. 70 (1998) 646-652
75. Williams R.M., and Webb W.W. Single granule pH cycling in antigen-induced mast cell secretion. J. Cell Sci. 113 Part 21 (2000) 3839-3850
76. Wrede C.E., Dickson L.M., Lingohr M.K., Briaud I., and Rhodes C.J. Fatty acid and phorbol ester-mediated interference of mitogenic signaling via novel protein kinase C isoforms in pancreatic beta-cells (INS-1). J. Mol. Endocrinol. 30 (2003) 271-286
77. Xia T., Kovochich M., and Nel A.E. Impairment of mitochondrial function by particulate matter (PM) and their toxic components: implications for PM-induced cardiovascular and lung disease. Front. Biosci. 12 (2007) 1238-1246
78. Xiong S., and Rodgers K. Effects of malathion metabolites on degranulation of and mediator release by human and rat basophilic cells. J. Toxicol. Environ. Health 51 (1997) 159-175
79. Yepez-Mulia L., Montano-Escalona C., Fonseca-Linan R., Munoz-Cruz S., Arizmendi-Puga N., Boireau P., and Ortega-Pierres G. Differential activation of mast cells by antigens from Trichinella spiralis muscle larvae, adults, and newborn larvae. Vet. Parasitol. 159 (2009) 253-257
80. 2+ influx. Free Radic. Biol. Med. 40 (2006) 1949-1959