Specialized proresolving mediators (SPMs) inhibit human B-cell IgE production

European Journal of Immunology

Volumn 46, Issue 1, 2016, Pages 81-91

  Kim, Nina ^a   Ramon, Sesquile ^a   Thatcher, Thomas H ^b   Woeller, Collynn F ^b   Sime, Patricia J ^b   Phipps, Richard P ^a,b  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

Author keywords

B cell; Human; IgE; Inflammation resolution; Proresolving mediator

Indexed keywords

17 HYDROXYDOCOSAHEXAENOIC ACID; ANTIINFLAMMATORY AGENT; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; IMMUNOLOGIC AGENT; INTERLEUKIN 4; PROTEIN BCL 6; RESOLVIN D1; STAT6 PROTEIN; UNCLASSIFIED DRUG; 17-HYDROXY-4,7,10,13,15,19-DOCOSAHEXAENOIC ACID; DOCOSAHEXAENOIC ACID;

ARTICLE; B CELL LYMPHOMA; B LYMPHOCYTE; BINDING COMPETITION; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GERM LINE; HUMAN; HUMAN CELL; IMMUNOGLOBULIN PRODUCTION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; NORMAL HUMAN; PRIORITY JOURNAL; PROMOTER REGION; TRANSCRIPTION REGULATION; UPREGULATION; BIOSYNTHESIS; CELL CULTURE; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE REARRANGEMENT; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; REAL TIME POLYMERASE CHAIN REACTION; SECRETION (PROCESS); WESTERN BLOTTING;

B-LYMPHOCYTES; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; DOCOSAHEXAENOIC ACIDS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HUMANS; IMMUNOGLOBULIN CLASS SWITCHING; IMMUNOGLOBULIN E; LYMPHOCYTE ACTIVATION; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84953836615     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201545673     Document Type: Article

References (43)

1. Serhan, C. N., The resolution of inflammation: the devil in the flask and in the details. FASEB J. 2011. 25: 1441-1448.
2. Serhan, C. N., Chiang, N. and Van Dyke, T. E., Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat. Rev. Immunol. 2008. 8: 349-361.
3. Serhan, C. N., Resolution phase of inflammation: novel endogenous anti-inflammatory and proresolving lipid mediators and pathways. Annu. Rev. Immunol. 2007. 25: 101-137.
4. Serhan, C. N., Hamberg, M. and Samuelsson, B., Lipoxins: novel series of biologically active compounds formed from arachidonic acid in human leukocytes. Proc. Natl. Acad. Sci. U S A 1984. 81: 5335-5339.
5. Arita, M., Bianchini, F., Aliberti, J., Sher, A., Chiang, N., Hong, S., Yang, R. et al., Stereochemical assignment, antiinflammatory properties, and receptor for the omega-3 lipid mediator resolvin E1. J. Exp. Med. 2005. 201: 713-722.
6. Serhan, C. N., Arita, M., Hong, S. and Gotlinger, K., Resolvins, docosatrienes, and neuroprotectins, novel omega-3-derived mediators, and their endogenous aspirin-triggered epimers. Lipids 2004. 39: 1125-1132.
7. Serhan, C. N., Yang, R., Martinod, K., Kasuga, K., Pillai, P. S., Porter, T. F., Oh, S. F. et al., Maresins: novel macrophage mediators with potent antiinflammatory and proresolving actions. J. Exp. Med. 2009. 206: 15-23.
8. Serhan, C. N., Krishnamoorthy, S., Recchiuti, A. and Chiang, N., Novel anti-inflammatory-pro-resolving mediators and their receptors. Curr. Top. Med. Chem. 2011. 11: 629-647.
9. Ramon, S., Gao, F., Serhan, C. N. and Phipps, R. P., Specialized proresolving mediators enhance human B cell differentiation to antibody-secreting cells. J. Immunol. 2012. 189: 1036-1042.
10. Dullaers, M., De Bruyne, R., Ramadani, F., Gould, H. J., Gevaert, P. and Lambrecht, B. N., The who, where, and when of IgE in allergic airway disease. J. Allergy Clin. Immunol. 2012. 129: 635-645.
11. Apter, A. J., Advances in adult asthma diagnosis and treatment in 2012: potential therapeutics and gene-environment interactions. J. Allergy Clin. Immunol. 2013. 131: 47-54.
12. Davis, L. A., Omalizumab: a novel therapy for allergic asthma. Ann. Pharmacother. 2004. 38: 1236-1242.
13. Allen, J. E. and Maizels, R. M., Diversity and dialogue in immunity to helminths. Nat. Rev. Immunol. 2011. 11: 375-388.
14. Rogerio, A. P., Haworth, O., Croze, R., Oh, S. F., Uddin, M., Carlo, T., Pfeffer, M. A. et al., Resolvin D1 and aspirin-triggered resolvin D1 promote resolution of allergic airways responses. J. Immunol. 2012. 189: 1983-1991.
15. Haworth, O., Cernadas, M., Yang, R., Serhan, C. N. and Levy, B. D., Resolvin E1 regulates interleukin 23, interferon-gamma and lipoxin A4 to promote the resolution of allergic airway inflammation. Nat. Immunol. 2008. 9: 873-879.
16. Krishnamoorthy, N., Burkett, P. R., Dalli, J., Abdulnour, R. E., Colas, R., Ramon, S., Phipps, R. P. et al., Cutting edge: maresin-1 engages regulatory T cells to limit type 2 innate lymphoid cell activation and promote resolution of lung inflammation. J. Immunol. 2014. 194(3): 863-867
17. Harris, M. B., Mostecki, J. and Rothman, P. B., Repression of an interleukin-4-responsive promoter requires cooperative BCL-6 function. J. Biol. Chem. 2005. 280: 13114-13121.
18. Caven, T. H., Shelburne, A., Sato, J., Chan-Li, Y., Becker, S. and Conrad, D. H., IL-21 dependent IgE production in human and mouse in vitro culture systems is cell density and cell division dependent and is augmented by IL-10. Cell. Immunol. 2005. 238: 123-134.
19. Caven, T. H., Sturgill, J. L. and Conrad, D. H., BCR ligation antagonizes the IL-21 enhancement of anti-CD40/IL-4 plasma cell differentiation and IgE production found in low density human B cell cultures. Cell. Immunol. 2007. 247: 49-58.
20. Harada, M., Magara-Koyanagi, K., Watarai, H., Nagata, Y., Ishii, Y., Kojo, S., Horiguchi, S. et al., IL-21-induced Bepsilon cell apoptosis mediated by natural killer T cells suppresses IgE responses. J. Exp. Med. 2006. 203: 2929-2937.
21. Ozcan, E., Rauter, I., Garibyan, L., Dillon, S. R. and Geha, R. S., Toll-like receptor 9, transmembrane activator and calcium-modulating cyclophilin ligand interactor, and CD40 synergize in causing B-cell activation. J. Allergy Clin. Immunol. 2011. 128: 601-609 e601-e604.
22. Gantner, F., Hermann, P., Nakashima, K., Matsukawa, S., Sakai, K. and Bacon, K. B., CD40-dependent and -independent activation of human tonsil B cells by CpG oligodeoxynucleotides. Eur. J. Immunol. 2003. 33: 1576-1585.
23. Bernasconi, N. L., Traggiai, E. and Lanzavecchia, A., Maintenance of serological memory by polyclonal activation of human memory B cells. Science 2002. 298: 2199-2202.
24. Pene, J., Rousset, F., Briere, F., Chretien, I., Paliard, X., Banchereau, J., Spits, H. et al., IgE production by normal human B cells induced by alloreactive T cell clones is mediated by IL-4 and suppressed by IFN-gamma. J. Immunol. 1988. 141: 1218-1224.
25. Hellman, L., Regulation of IgE homeostasis, and the identification of potential targets for therapeutic intervention. Biomed. Pharmacother. 2007. 61: 34-49.
26. Jabara, H. H., Schneider, L. C., Shapira, S. K., Alfieri, C., Moody, C. T., Kieff, E., Geha, R. S. et al., Induction of germ-line and mature C epsilon transcripts in human B cells stimulated with rIL-4 and EBV. J. Immunol. 1990. 145: 3468-3473.
27. Ichiki, T., Takahashi, W. and Watanabe, T., Regulation of the expression of human C epsilon germline transcript. Identification of a novel IL-4 responsive element. J. Immunol. 1993. 150: 5408-5417.
28. Linehan, L. A., Warren, W. D., Thompson, P. A., Grusby, M. J. and Berton, M. T., STAT6 is required for IL-4-induced germline Ig gene transcription and switch recombination. J. Immunol. 1998. 161: 302-310.
29. Dent, A. L., Shaffer, A. L., Yu, X., Allman, D. and Staudt, L. M., Control of inflammation, cytokine expression, and germinal center formation by BCL-6. Science 1997. 276: 589-592.
30. Cattoretti, G., Chang, C. C., Cechova, K., Zhang, J., Ye, B. H., Falini, B., Louie, D. C. et al., BCL-6 protein is expressed in germinal-center B cells. Blood 1995. 86: 45-53.
31. Phan, R. T., Saito, M., Kitagawa, Y., Means, A. R. and Dalla-Favera, R., Genotoxic stress regulates expression of the proto-oncogene Bcl6 in germinal center B cells. Nat. Immunol. 2007. 8: 1132-1139.
32. Nacionales, D. C., Weinstein, J. S., Yan, X. J., Albesiano, E., Lee, P. Y., Kelly-Scumpia, K. M., Lyons, R. et al., B cell proliferation, somatic hypermutation, class switch recombination, and autoantibody production in ectopic lymphoid tissue in murine lupus. J. Immunol. 2009. 182: 4226-4236.
33. Li, L., Wu, Y., Wang, Y., Wu, J., Song, L., Xian, W., Yuan, S. et al., Resolvin D1 promotes the interleukin-4-induced alternative activation in BV-2 microglial cells. J. Neuroinflammation 2014. 11: 72.
34. Harris, M. B., Chang, C. C., Berton, M. T., Danial, N. N., Zhang, J., Kuehner, D., Ye, B. H. et al., Transcriptional repression of Stat6-dependent interleukin-4-induced genes by BCL-6: specific regulation of iepsilon transcription and immunoglobulin E switching. Mol. Cell. Biol. 1999. 19: 7264-7275.
35. Shao, Y., Ling, C. C. and Liu, X. Q., High concentrations of glucose suppress etoposide-induced cell death of B-cell lymphoma through BCL-6. Biochem. Biophys. Res. Commun. 2014. 450: 227-233.
36. Arima, M., Fukuda, T. and Tokuhisa, T., Role of the transcriptional repressor BCL6 in allergic response and inflammation. World Allergy Organ J. 2008. 1: 115-122.
37. Norling, L. V., Dalli, J., Flower, R. J., Serhan, C. N. and Perretti, M., Resolvin D1 limits polymorphonuclear leukocyte recruitment to inflammatory loci: receptor-dependent actions. Arterioscler. Thromb. Vasc. Biol. 2012. 32: 1970-1978.
38. D'Amato, G., Stanziola, A., Sanduzzi, A., Liccardi, G., Salzillo, A., Vitale, C., Molino, A. et al., Treating severe allergic asthma with anti-IgE monoclonal antibody (omalizumab): a review. Multidiscip. Respir. Med. 2014. 9: 23.
39. D'Auria, E., Miraglia Del Giudice, M., Barberi, S., Mandelli, M., Verduci, E., Leonardi, S., Riva, E. et al., Omega-3 fatty acids and asthma in children. Allergy Asthma Proc. 2014. 35: 233-240.
40. Hodge, L., Salome, C. M., Hughes, J. M., Liu-Brennan, D., Rimmer, J., Allman, M., Pang, D. et al., Effect of dietary intake of omega-3 and omega-6 fatty acids on severity of asthma in children. Eur. Respir. J. 1998. 11: 361-365.
41. Nagakura, T., Matsuda, S., Shichijyo, K., Sugimoto, H. and Hata, K., Dietary supplementation with fish oil rich in omega-3 polyunsaturated fatty acids in children with bronchial asthma. Eur. Respir. J. 2000. 16: 861-865.
42. Ryan, E. P., Pollock, S. J., Murant, T. I., Bernstein, S. H., Felgar, R. E. and Phipps, R. P., Activated human B lymphocytes express cyclooxygenase-2 and cyclooxygenase inhibitors attenuate antibody production. J. Immunol. 2005. 174: 2619-2626.
43. Kehry, M. R. and Castle, B. E., Regulation of CD40 ligand expression and use of recombinant CD40 ligand for studying B cell growth and differentiation. Semin. Immunol. 1994. 6: 287-294.