Synthetic allergen design reveals the significance of moderate affinity epitopes in mast cell degranulation

ACS Chemical Biology

Volumn 7, Issue 11, 2012, Pages 1796-1801

  Handlogten, Michael W ^a   Kiziltepe, Tanyel ^a,b   Alves, Nathan J ^a   Bilgicer, Basar ^a,b  

^a University of Notre Dame   (United States)

^b UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; EPITOPE; HAPTEN; HOMOTETRAVALENT SYNTHETIC ALLERGEN; IMMUNOGLOBULIN E; UNCLASSIFIED DRUG;

ANTIGEN ANTIBODY REACTION; ARTICLE; BINDING AFFINITY; CELL SURFACE; CHEMICAL STRUCTURE; MAST CELL DEGRANULATION; PRIORITY JOURNAL;

ALLERGENS; ANIMALS; ANTIBODY AFFINITY; CELL DEGRANULATION; CELL LINE; EPITOPES; HAPTENS; HUMANS; IMMUNOGLOBULIN E; MAST CELLS;

EID: 84869422848     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb300193f     Document Type: Article

References (35)

1. Metzger, H. (1992) Transmembrane signaling: the joy of aggregation J. Immunol. 149, 1477-1487
2. Blank, U. and Rivera, J. (2006) Assays for Regulated Exocytosis of Mast Cell Granules. In Current Protocols in Cell Biology, Chapter 15, Unit 15.11.
3. Andrews, N. L., Pfeiffer, J. R., Martinez, A. M., Haaland, D. M., Davis, R. W., Kawakami, T., Oliver, J. M., Wilson, B. S., and Lidke, D. S. (2009) Small, mobile Fc Epsilon R1 receptor aggregates are signaling competent Immunity 31, 469-479
4. Passante, E. and Frankish, N. (2009) The RBL-2H3 cell line: its provenance and suitability as a model for the mast cell Inflammation Res. 58, 737-745
5. Collins, A. M., Basil, M., Nguyen, K., and Thelian, D. (1996) Rat basophil leukaemia (RBL) cells sensitized with low affinity IgE respond to high valency antigen Clin. Exp. Allergy 26, 964-970
6. Collins, A. M., Thelian, D., and Basil, M. (1995) Antigen valency as a determinant of the responsiveness of IgE-sensitized rat basophil leukemia-cells Int. Arch. Allergy Immunol. 107, 547-556
7. Huang, Y., Liu, H., Xiong, X., Chen, Y., and Tan, W. (2009) Nanoparticle-mediated IgE-receptor aggregation and signaling in RBL mast cells J. Am. Chem. Soc. 131, 17328-17334
8. Handlogten, M. W., Kiziltepe, T., Moustakas, D. T., and Bilgicer, B. (2011) Design of a heterobivalent ligand to inhibit IgE clustering on mast cells Chem. Biol. 18, 1179-1188
9. Wang, J., Lin, J., Bardina, L., Goldis, M., Nowak-Wegrzyn, A., Shreffler, W. G., and Sampson, H. A. (2010) Correlation of IgE/IgG4 milk epitopes and affinity of milk-specific IgE antibodies with different phenotypes of clinical milk allergy J. Allergy Clin. Immunol. 125, 695-702
10. Cerecedo, I., Zamora, J., Shreffler, W. G., Lin, J., Bardina, L., Dieguez, M. C., Wang, J., Muriel, A., de la Hoz, B., and Sampson, H. A. (2008) Mapping of the IgE and IgG4 sequential epitopes of milk allergens with a peptide microarray-based immunoassay J. Allergy Clin. Immunol. 122, 589-594
11. James, L. C. and Tawfik, D. S. (2003) The specificity of cross-reactivity: promiscuous antibody binding involves specific hydrogen bonds rather than nonspecific hydrophobic stickiness Protein Sci. 12, 2183-2193
12. Xu, K. L., Goldstein, B., Holowka, D., and Baird, B. (1998) Kinetics of multivalent antigen DNP-BSA binding to IgE-Fc Epsilon RI in relationship to the stimulated tyrosine phosphorylation of Fc Epsilon RI J. Immunol. 160, 3225-3235
13. Hlavacek, W., Posner, R., and Perelson, A. (1999) Steric effects on multivalent ligand-receptor binding: exclusion of ligand sites by bound cell surface receptors Biophys. J. 76, 3031-3043
14. Pacios, L. F., Tordesillas, L., Cuesta-Herranz, J., Compes, E., Sanchez-Monge, R., Palacin, A., Salcedo, G., and Diaz-Perales, A. (2008) Mimotope mapping as a complementary strategy to define allergen IgE-epitopes: peach Pru p 3 allergen as a model Mol. Immunol. 45, 2269-2276
15. Rouge, P., Culerrier, R., Sabatiera, V., Granier, C., Rance, F., and Barre, A. (2009) Mapping and conformational analysis of IgE-binding epitopic regions on the molecular surface of the major Ara h 3 legumin allergen of peanut (Arachis hypogaea) Mol. Immunol. 46, 1067-1075
16. Christensen, L. H., Holm, J., Lund, G., Riise, E., and Lund, K. (2008) Several distinct properties of the IgE repertoire determine effector cell degranulation in response to allergen challenge J. Allergy Clin. Immunol. 122, 298-304
17. Tanabe, S. (2007) Epitope peptides and immunotherapy Curr. Protein Pept. Sci. 8, 109-118
18. Kiessling, L. L., Gestwicki, J. E., and Strong, L. E. (2006) Synthetic multivalent ligands as probes of signal transduction Angew. Chem., Int. Ed. 45, 2348-2368
19. Puffer, E. B., Pontrello, J. K., Hollenbeck, J. J., Kink, J. A., and Kiessling, L. L. (2007) Activating B cell signaling with defined multivalent ligands ACS Chem. Biol. 2, 252-262
20. Mammen, M., Choi, S.-K., and Whitesides, G. M. (1998) Polyvalent interactions in biological systems: implications for design and use of multivalent ligands and inhibitors Angew. Chem., Int. Ed. 37, 2754-2794
21. Posner, R. G., Subramanian, K., Goldstein, B., Thomas, J., Feder, T., Holowka, D., and Baird, B. (1995) Simultaneous cross-linking by two nontriggering bivalent ligands causes synergistic signaling of IgE RcεR1 complexes J. Immunol. 155, 3601-3609
22. Posner, R. G., Geng, D., Haymore, S., Bogert, J., Pecht, I., Licht, A., and Savage, P. B. (2007) Trivalent antigens for degranulation of mast cells Org. Lett. 9, 3551-3554
23. Sil, D., Lee, J. B., Luo, D., Holowka, D., and Baird, B. (2007) Trivalent ligands with rigid DNA spacers reveal structural requirements for IgE receptor signaling in RBL mast cells ACS Chem. Biol. 2, 674-684
24. Rabjohn, P., Helm, E., Stanley, J., West, C., Sampson, H., Burks, A., and Bannon, G. (1999) Molecular cloning and epitope analysis of the peanut allergen Ara h 3 J. Clin. Invest. 103, 535-542
25. Denery-Papini, S., Bodinier, M., Pineau, F., Triballeau, S., Tranquet, O., Adel-Patient, K., Moneret-Vautrin, D. A., Bakan, B., Marion, D., Mothes, T., Mameri, H., and Kasarda, D. (2011) Immunoglobulin-E-binding epitopes of wheat allergens in patients with food allergy to wheat and in mice experimentally sensitized to wheat proteins Clin. Exp. Allergy 41, 1478-1492
26. Bilgiçer, B., Moustakas, D. T., and Whitesides, G. M. (2007) A synthetic trivalent hapten that aggregates anti-2,4-DNP IgG into bicyclic trimers J. Am. Chem. Soc. 129, 3722-3728
27. Stefanick, J. F., Kiziltepe, T., Handlogten, M. W., Alves, N. J., and Bilgicer, B. (2012) Enhancement of antibody selectivity via bicyclic complex formation J.Phys. Chem. Lett. 3, 598-602
28. Roux, K. H., Strelets, L., Brekke, O. H., Sandlie, I., and Michaelsen, T. E. (1998) Comparisons of the ability of human IgG3 hinge mutants, IgM, IgE, and IgA2, to form small immune complexes: a role for flexibility and geometry J. Immunol. 161, 4083-4090
29. Strelets, L., Roux, K. H., Brekke, O. H., Sandlie, I., and Michaelsen, T. (1996) The role of the hinge region in human IgG immune complex formation FASEB J. 10, 973-973
30. Baird, E. J., Holowka, D., Coates, G. W., and Baird, B. (2003) Highly effective poly(ethylene glycol) architectures for specific inhibition of immune receptor activation Biochemistry 42, 12739-12748
31. Posner, R. G., Savage, P. B., Peters, A. S., Macias, A., DelGado, J., Zwartz, G., Sklar, L. A., and Hlavacek, W. S. (2002) A quantitative approach for studying IgE-Fc Epsilon RI aggregation Mol. Immunol. 38, 1221-1228
32. Rai, P., Padala, C., Poon, V., Saraph, A., Basha, S., Kate, S., Tao, K., Mogridge, J., and Kane, R. (2006) Statistical pattern matching facilitates the design of polyvalent inhibitors of anthrax and cholera toxins Nat. Biotechnol. 24, 582-586
33. Ortega, E., Schweitzerstenner, R., and Pecht, I. (1988) Possible orientational constraints determine secretory signals induced by aggregation of IgE receptors on mast-cells EMBO J. 7, 4101-4109
34. Seagrave, J. and Oliver, J. M. (1990) Antigen-dependent transition of IgE to a detergent-insoluble form is associated with reduced IgE receptor-dependent secretion from RBL-2H3 mast-cells J. Cell. Physiol. 144, 128-136
35. Andrews, N., Lidke, K. A., Hsieh, G., Wilson, B. S., Oliver, J. M., and Lidke, D. S. (2007) High affinity IgE receptor diffusional dynamics measured by single quantum dot tracking in resting and activated cells FASEB J. 21, A184-A184