Polyphenols differentially inhibit degranulation of distinct subsets of vesicles in mast cells by specific interaction with granule-type-dependent SNARE complexes

Biochemical Journal

Volumn 450, Issue 3, 2013, Pages 537-546

  Yang, Yoosoo ^a,b   Oh, Jung Mi ^a   Heo, Paul ^a   Shin, Jae Yoon ^a   Kong, Byoungjae ^a   Shin, Jonghyeok ^a   Lee, Ji Chun ^a   Oh, Jeong Su ^a   Park, Kye Won ^a   Lee, Choong Hwan ^c   Shin, Yeon Kyun ^b,d   Kweon, Dae Hyuk ^a  

^a Sungkyunkwan University   (South Korea)

^b Korea Institute of Science and Technology   (South Korea)

^c Konkuk University   (South Korea)

^d IOWA STATE UNIVERSITY   (United States)

Author keywords

hexosaminidase; Degranulation; Histamine; Membrane fusion; Polyphenol; Soluble N ethylmaleimide sensitive factor attachment protein receptor (SNARE)

Indexed keywords

N ETHYLMALEIMIDE SENSITIVE FACTOR; POLYPHENOL; SNARE PROTEIN; SYNAPTOBREVIN 1; SYNTAXIN;

ARTICLE; CELL GRANULE; CELL INTERACTION; CELL MEMBRANE; CELL TYPE; COMPLEX FORMATION; EXOCYTOSIS; GENE; GENE EXPRESSION; IMMUNOPRECIPITATION; MAST CELL; MAST CELL DEGRANULATION; PRIORITY JOURNAL; SECRETORY GRANULE;

BETA-N-ACETYLHEXOSAMINIDASES; CELL DEGRANULATION; CELLS, CULTURED; CYTOPLASMIC GRANULES; DOWN-REGULATION; DRUG EVALUATION, PRECLINICAL; HISTAMINE; HUMANS; MAST CELLS; MULTIPROTEIN COMPLEXES; POLYPHENOLS; PROTEIN BINDING; SNARE PROTEINS; SUBSTRATE SPECIFICITY; TRANSPORT VESICLES;

EID: 84874591436     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20121256     Document Type: Article

References (49)

1. Park, H. H., Lee, S., Son, H. Y., Park, S. B., Kim, M. S., Choi, E. J., Singh, T. S., Ha, J. H., Lee, M. G., Kim, J. E. et al. (2008) Flavonoids inhibit histamine release and expression of proinflammatory cytokines in mast cells. Arch. Pharm. Res. 31, 1303-1311
2. Hounsome, N., Hounsome, B., Tomos, D. and Edwards-Jones, G. (2008) Plant metabolites and nutritional quality of vegetables. J. Food Sci. 73, R48-R65
3. Manach, C., Scalbert, A., Morand, C., Remesy, C. and Jimenez, L. (2004) Polyphenols: food sources and bioavailability. Am. J. Clin. Nutr. 79, 727-747
4. Mennen, L. I., Walker, R., Bennetau-Pelissero, C. and Scalbert, A. (2005) Risks and safety of polyphenol consumption. Am. J. Clin. Nutr. 81, S326-S329
5. Akazome, Y., Kametani, N., Kanda, T., Shimasaki, H. and Kobayashi, S. (2010) Evaluation of safety of excessive intake and efficacy of long-term intake of beverages containing apple polyphenols. J. Oleo Sci. 59, 321-338
6. Ross, J. A. and Kasum, C. M. (2002) Dietary flavonoids: bioavailability, metabolic effects, and safety. Annu. Rev. Nutr. 22, 19-34
7. Noguchi, Y., Fukuda, K., Matsushima, A., Haishi, D., Hiroto, M., Kodera, Y., Nishimura, H. and Inada, Y. (1999) Inhibition of Df-protease associated with allergic diseases by polyphenol. J. Agric. Food Chem. 47, 2969-2972
8. Garcia, V., Arts, I. C., Sterne, J. A., Thompson, R. L. and Shaheen, S. O. (2005) Dietary intake of flavonoids and asthma in adults. Eur. Respir. J. 26, 449-452
9. Seifried, H. E., Anderson, D. E., Fisher, E. I. and Milner, J. A. (2007) A review of the interaction among dietary antioxidants and reactive oxygen species. J. Nutr. Biochem. 18, 567-579
10. Chung, S.-Y. and Champagne, E. T. (2009) Reducing the allergenic capacity of peanut extracts and liquid peanut butter by phenolic compounds. Food Chem. 115, 1345-1349
11. Nozaki, A., Hori, M., Kimura, T., Ito, H. and Hatano, T. (2009) Interaction of polyphenols with proteins: binding of (-)-epigallocatechin gallate to serum albumin, estimated by induced circular dichroism. Chem. Pharm. Bull. 57, 224-228
12. Labuckas, D. O., Maestri, D. M., Perelló, M., Martínez, M. L. and Lamarque, A. L. (2008) Phenolics from walnut (Juglans regia L.) kernels: antioxidant activity and interactions with proteins. Food Chem. 107, 607-612
13. Williamson, M. P., McCormick, T. G., Nance, C. L. and Shearer, W. T. (2006) Epigallocatechin gallate, the main polyphenol in green tea, binds to the T-cell receptor, CD4: potential for HIV-1 therapy. J. Allergy Clin. Immunol. 118, 1369-1374
14. Khan, N., Afaq, F., Saleem, M., Ahmad, N. and Mukhtar, H. (2006) Targeting multiple signaling pathways by green tea polyphenol (-)-epigallocatechin-3-gallate. Cancer Res. 66, 2500-2505
15. Biesalski, H. K. (2007) Polyphenols and inflammation: basic interactions. Curr. Opin. Clin. Nutr. Metab. Care 10, 724-728
16. Santangelo, C., Vari, R., Scazzocchio, B., Di Benedetto, R., Filesi, C. and Masella, R. (2007) Polyphenols, intracellular signalling and inflammation. Ann. Ist. Super. Sanita 43, 394-405
17. Kanda, T., Akiyama, H., Yanagida, A., Tanabe, M., Goda, Y., Toyoda, M., Teshima, R. and Saito, Y. (1998) Inhibitory effects of apple polyphenol on induced histamine release from RBL-2H3 cells and rat mast cells. Biosci., Biotechnol., Biochem. 62, 1284-1289
18. Abraham, S. N. and Malaviya, R. (1997) Mast cells in infection and immunity. Infect. Immun. 65, 3501-3508
19. Metcalfe, D. D., Baram, D. and Mekori, Y. A. (1997) Mast cells. Physiol. Rev. 77, 1033-1079
20. Raposo, G., Tenza, D., Mecheri, S., Peronet, R., Bonnerot, C. and Desaymard, C. (1997) Accumulation of major histocompatibility complex class II molecules in mast cell secretory granules and their release upon degranulation. Mol. Biol. Cell 8, 2631-2645
21. Baram, D., Adachi, R., Medalia, O., Tuvim, M., Dickey, B. F., Mekori, Y. A. and Sagi-Eisenberg, R. (1999) Synaptotagmin II negatively regulates Ca2+ -triggered exocytosis of lysosomes in mast cells. J. Exp. Med. 189, 1649-1658
22. Sollner, T., Bennett, M. K., Whiteheart, S. W., Scheller, R. H. and Rothman, J. E. (1993) A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75, 409-418
23. Blank, U., Cyprien, B., Martin-Verdeaux, S., Paumet, F., Pombo, I., Rivera, J., Roa, M. and Varin-Blank, N. (2002) SNAREs and associated regulators in the control of exocytosis in the RBL-2H3 mast cell line. Mol. Immunol. 38, 1341-1345
24. Suzuki, K. and Verma, I. M. (2008) Phosphorylation of SNAP-23 by IκB kinase 2 regulates mast cell degranulation. Cell 134, 485-495
25. Stow, J. L., Manderson, A. P. and Murray, R. Z. (2006) SNAREing immunity: the role of SNAREs in the immune system. Nat. Rev. Immunol. 6, 919-929
26. Guo, Z., Turner, C. and Castle, D. (1998) Relocation of the t-SNARE SNAP-23 from lamellipodia-like cell surface projections regulates compound exocytosis in mast cells. Cell 94, 537-548
27. Puri, N. and Roche, P. A. (2006) Ternary SNARE complexes are enriched in lipid rafts during mast cell exocytosis. Traffic 7, 1482-1494
28. Pombo, I., Rivera, J. and Blank, U. (2003) Munc18-2/syntaxin3 complexes are spatially separated from syntaxin3-containing SNARE complexes. FEBS Lett. 550, 144-148
29. Lippert, U., Ferrari, D. M. and Jahn, R. (2007) Endobrevin/VAMP8 mediates exocytotic release of hexosaminidase from rat basophilic leukaemia cells. FEBS Lett. 581, 3479-3484
30. Salinas, E., Quintanar-Stephano, A., Cordova, L. E. and Ouintanar, J. L. (2008) Allergen-sensitization increases mast-cell expression of the exocytotic proteins SNAP-23 and syntaxin 4, which are involved in histamine secretion. J. Invest. Allergol. Clin. Immunol. 18, 366-371
31. Puri, N. and Roche, P. A. (2008) Mast cells possess distinct secretory granule subsets whose exocytosis is regulated by different SNARE isoforms. Proc. Natl. Acad. Sci. U.S.A. 105, 2580-2585
32. Woska, Jr, J. R. and Gillespie, M. E. (2011) Small-interfering RNA-mediated identification and regulation of the ternary SNARE complex mediating RBL-2H3 mast cell degranulation. Scand. J. Immunol. 73, 8-17
33. Yang, Y., Shin, J. Y., Oh, J. M., Jung, C. H., Hwang, Y., Kim, S., Kim, J. S., Yoon, K. J., Ryu, J. Y., Shin, J. et al. (2010) Dissection of SNARE-driven membrane fusion and neuroexocytosis by wedging small hydrophobic molecules into the SNARE zipper. Proc. Natl. Acad. Sci. U.S.A. 107, 22145-22150
34. Yang, Y., Choi, J. K., Jung, C. H., Koh, H. J., Heo, P., Shin, J. Y., Kim, S., Park, W. S., Shin, H. J. and Kweon, D. H. (2012) SNARE-wedging polyphenols as small molecular botox. Planta Med. 78, 233-236
35. Schwartz, L. B., Austen, K. F. and Wasserman, S. I. (1979) Immunologic release of β-hexosaminidase and β-glucuronidase from purified rat serosal mast cells. J. Immunol. 123, 1445-1450
36. Kawasaki, Y., Saitoh, T., Okabe, T., Kumakura, K. and Ohara-Imaizumi, M. (1991) Visualization of exocytotic secretory processes of mast cells by fluorescence techniques. Biochim. Biophys. Acta 1067, 71-80
37. Tewtrakul, S. and Itharat, A. (2006) Anti-allergic substances from the rhizomes of Dioscorea membranacea. Bioorg. Med. Chem. 14, 8707-8711
38. Jung, C. H., Yang, Y. S., Kim, J. S., Shin, J. I., Jin, Y. S., Shin, J. Y., Lee, J. H., Chung, K. M., Hwang, J. S., Oh, J. M. et al. (2008) A search for synthetic peptides that inhibit soluble N-ethylmaleimide sensitive-factor attachment receptor-mediated membrane fusion. FEBS J. 275, 3051-3063
39. Weber, T., Zemelman, B. V., McNew, J. A., Westermann, B., Gmachl, M., Parlati, F., Sollner, T. H. and Rothman, J. E. (1998) SNAREpins: minimal machinery for membrane fusion. Cell 92, 759-772
40. Qin, C., Xie, M. X. and Liu, Y. (2007) Characterization of the myricetin-human serum albumin complex by spectroscopic and molecular modeling approaches. Biomacromolecules 8, 2182-2189
41. Schwartz, L. B., Lewis, R. A., Seldin, D. and Austen, K. F. (1981) Acid hydrolases and tryptase from secretory granules of dispersed human lung mast cells. J. Immunol. 126, 1290-1294
42. Fujimura, Y., Tachibana, H., Maeda-Yamamoto, M., Miyase, T., Sano, M. and Yamada, K. (2002) Antiallergic tea catechin, (-)-epigallocatechin-3-O-(3-O- methyl)-gallate, suppresses FcεRI expression in human basophilic KU812 cells. J. Agric. Food Chem. 50, 5729-5734
43. Tong, J., Borbat, P. P., Freed, J. H. and Shin, Y. K. (2009) A scissors mechanism for stimulation of SNARE-mediated lipid mixing by cholesterol. Proc. Natl. Acad. Sci. U.S.A. 106, 5141-5146
44. Puri, N., Kruhlak, M. J., Whiteheart, S. W. and Roche, P. A. (2003) Mast cell degranulation requires N-ethylmaleimide-sensitive factor-mediated SNARE disassembly. J. Immunol. 171, 5345-5352
45. Fujimura, Y., Tachibana, H. and Yamada, K. (2001) A tea catechin suppresses the expression of the high-affinity IgE receptor FcεRI in human basophilic KU812 cells. J. Agric. Food Chem. 49, 2527-2531
46. Yano, S., Tachibana, H. and Yamada, K. (2005) Flavones suppress the expression of the high-affinity IgE receptor FcεRI in human basophilic KU812 cells. J. Agric. Food. Chem. 53, 1812-1817
47. Morabito, N., Crisafulli, A., Vergara, C., Gaudio, A., Lasco, A., Frisina, N., D'Anna, R., Corrado, F., Pizzoleo, M. A., Cincotta, M. et al. (2002) Effects of genistein and hormone-replacement therapy on bone loss in early postmenopausal women: a randomized double-blind placebo-controlled study. J. Bone Miner. Res. 17, 1904-1912
48. Scalbert, A. and Williamson, G. (2000) Dietary intake and bioavailability of polyphenols. J. Nutr. 130, S2073-S2085
49. Manach, C., Williamson, G., Morand, C., Scalbert, A. and Rémésy, C. (2005) Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies. Am. J. Clin. Nutr. 81, S230-S242