Role of sphingosine kinase 1 and sphingosine-1-phosphate in CD40 signaling and IgE class switching

FASEB Journal

Volumn 28, Issue 10, 2014, Pages 4347-4358

  Kim, Eugene Y ^a   Sturgill, Jamie L ^a   Hait, Nitai C ^a   Avni, Dorit ^a   Valencia, Evelyn C ^a   MacEyka, Michael ^a   Lima, Santiago ^a   Allegood, Jeremy ^a   Huang, Wei Ching ^a   Zhang, Shijun ^a   Milstien, Sheldon ^a   Conrad, Daniel ^a   Spiegel, Sarah ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

B cells; Inflammation; NF B; Sphingolipids

Indexed keywords

ANTIGEN; CD40 ANTIGEN; IMMUNOGLOBULIN E; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE KINASE 1; STRESS ACTIVATED PROTEIN KINASE; LYSOPHOSPHOLIPID; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; PHOSPHOTRANSFERASE; SPHINGOSINE; SPHINGOSINE 1-PHOSPHATE; SPHINGOSINE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELL DIFFERENTIATION; CELL MEMBRANE; CONTROLLED STUDY; GENE DELETION; GENE SWITCHING; GROWTH INHIBITION; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IMMUNIZATION; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE PROLIFERATION; MEDIATOR; MOUSE; NONHUMAN; PLASMA CELL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SPLEEN; T LYMPHOCYTE; TONSIL; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; CYTOLOGY; GENE REARRANGEMENT; GENETICS; HEK293 CELL LINE; METABOLISM; PROTEIN TRANSPORT;

ANIMALS; ANTIGENS, CD40; B-LYMPHOCYTES; CELL DIFFERENTIATION; CELL MEMBRANE; HEK293 CELLS; HUMANS; IMMUNOGLOBULIN CLASS SWITCHING; IMMUNOGLOBULIN E; LYSOPHOSPHOLIPIDS; MAP KINASE KINASE 4; MICE; MICE, INBRED C57BL; NF-KAPPA B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN TRANSPORT; SPHINGOSINE;

EID: 84907697183     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-251611     Document Type: Article

References (57)

1. Van Kooten, C., and Banchereau, J. (2000) CD40-CD40 ligand. J. Leukoc. Biol. 67, 2-17
2. Bishop, G. A. (2004) The multifaceted roles of TRAFs in the regulation of B-cell function. Nat. Rev. Immunol. 4, 775-786
3. Rickert, R. C., Jellusova, J., and Miletic, A. V. (2011) Signaling by the tumor necrosis factor receptor superfamily in B-cell biology and disease. Immunol. Rev. 244, 115-133
4. Kawabe, T., Naka, T., Yoshida, K., Tanaka, T., Fujiwara, H., Suematsu, S., Yoshida, N., Kishimoto, T., and Kikutani, H. (1994) The immune responses in CD40-deficient mice: impaired immunoglobulin class switching and germinal center formation. Immunity 1, 167-178
5. Jabara, H. H., Fu, S. M., Geha, R. S., and Vercelli, D. (1990) CD40 and IgE: synergism between anti-CD40 monoclonal antibody and interleukin 4 in the induction of IgE synthesis by highly purified human B cells. J. Exp. Med. 172, 1861-1864
6. Fuleihan, R., Ramesh, N., Loh, R., Jabara, H., Rosen, R. S., Chatila, T., Fu, S. M., Stamenkovic, I., and Geha, R. S. (1993) Defective expression of the CD40 ligand in X chromosomelinked immunoglobulin deficiency with normal or elevated IgM. Proc. Natl. Acad. Sci. U. S. A. 90, 2170-2173
7. Green, J. A., Suzuki, K., Cho, B., Willison, L. D., Palmer, D., Allen, C. D., Schmidt, T. H., Xu, Y., Proia, R. L., Coughlin, S. R., and Cyster, J. G. (2011) The sphingosine 1-phosphate receptor S1P(2) maintains the homeostasis of germinal center B cells and promotes niche confinement. Nat. Immunol. 12, 672-680
8. Spiegel, S., and Milstien, S. (2011) The outs and the ins of sphingosine-1-phosphate in immunity. Nat. Rev. Immunol. 11, 403-415
9. Cyster, J. G., and Schwab, S. R. (2012) Sphingosine-1-phosphate and lymphocyte egress from lymphoid organs. Annu. Rev. Immunol. 30, 69-94
10. Pappu, R., Schwab, S. R., Cornelissen, I., Pereira, J. P., Regard, J. B., Xu, Y., Camerer, E., Zheng, Y. W., Huang, Y., Cyster, J. G., and Coughlin, S. R. (2007) Promotion of lymphocyte egress into blood and lymph by distinct sources of sphingosine-1-phosphate. Science 316, 295-298
11. Grigorova, I. L., Schwab, S. R., Phan, T. G., Pham, T. H., Okada, T., and Cyster, J. G. (2009) Cortical sinus probing, S1P1- dependent entry and flow-based capture of egressing T cells. Nat. Immunol. 10, 58-65
12. Cinamon, G., Zachariah, M. A., Lam, O. M., Foss, F. W., Jr., and Cyster, J. G. (2008) Follicular shuttling of marginal zone B cells facilitates antigen transport. Nat. Immunol. 9, 54-62
13. Xia, P., Wang, L., Moretti, P. A., Albanese, N., Chai, F., Pitson, S. M., D'Andrea, R. J., Gamble, J. R., and Vadas, M. A. (2002) Sphingosine kinase interacts with TRAF2 and dissects tumor necrosis factor-alpha signaling. J. Biol. Chem. 277, 7996-8003
14. Pitson, S. M., Moretti, P. A., Zebol, J. R., Lynn, H. E., Xia, P., Vadas, M. A., and Wattenberg, B. W. (2003) Activation of sphingosine kinase 1 by ERK1/2-mediated phosphorylation. EMBO J. 22, 5491-5500
15. Baker, D. A., Barth, J., Chang, R., Obeid, L. M., and Gilkeson, G. S. (2010) Genetic sphingosine kinase 1 deficiency significantly decreases synovial inflammation and joint erosions in murine TNF-alpha-induced arthritis. J. Immunol. 185, 2570-2579
16. Alvarez, S. E., Harikumar, K. B., Hait, N. C., Allegood, J., Strub, G. M., Kim, E. Y., Maceyka, M., Jiang, H., Luo, C., Kordula, T., Milstien, S., and Spiegel, S. (2010) Sphingosine-1-phosphate is a missing cofactor for the E3 ubiquitin ligase TRAF2. Nature 465, 1084-1088
17. Harikumar, K. B., Yester, J. W., Surace, M. J., Oyeniran, C., Price, M. M., Huang, W.-C., Hait, N. C., Allegood, J. C., Yamada, A., Kong, X., Lazear, H. M., Bhardwaj, R., Takabe, K., Diamond, M. S., Luo, C., Milstien, S., Spiegel, S., and Kordula, T. (2014) K63-linked polyubiquitination of transcription factor IRF1 is essential for IL-1-induced production of chemokines CXCL10 and CCL5. Nat. Immunol. 15, 231-238
18. Vallabhapurapu, S., Matsuzawa, A., Zhang, W., Tseng, P. H., Keats, J. J., Wang, H., Vignali, D. A., Bergsagel, P. L., and Karin, M. (2008) Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiquitination cascade that activates NIK-dependent alternative NF-kappaB signaling. Nat. Immunol. 9, 1364-1370
19. Matsuzawa, A., Tseng, P. H., Vallabhapurapu, S., Luo, J. L., Zhang, W., Wang, H., Vignali, D. A., Gallagher, E., and Karin, M. (2008) Essential cytoplasmic translocation of a cytokine receptor-assembled signaling complex. Science 321, 663-668
20. Sturgill, J. L., Mathews, J., Scherle, P., and Conrad, D. H. (2011) Glutamate signaling through the kainate receptor enhances human immunoglobulin production. J. Neuroimmunol. 233, 80-89
21. Rabah, D., and Conrad, D. H. (2002) Effect of cell density on in vitro mouse immunoglobulin E production. Immunology 106, 503-510
22. Cho, S. W., Kilmon, M. A., Studer, E. J., van der Putten, H., and Conrad, D. H. (1997) B cell activation and Ig, especially IgE, production is inhibited by high CD23 levels in vivo and in vitro. Cell. Immunol. 180, 36-46
23. Mills, D. M., Bonizzi, G., Karin, M., and Rickert, R. C. (2007) Regulation of late B cell differentiation by intrinsic IKKalphadependent signals. Proc. Natl. Acad. Sci. U. S. A. 104, 6359-6364
24. Maceyka, M., Alvarez, S. E., Milstien, S., and Spiegel, S. (2008) Filamin A links sphingosine kinase 1 and sphingosine-1-phosphate receptor 1 at lamellipodia to orchestrate cell migration. Mol. Cell. Biol. 28, 5687-5697
25. Hait, N. C., Sarkar, S., Le Stunff, H., Mikami, A., Maceyka, M., Milstien, S., and Spiegel, S. (2005) Role of sphingosine kinase 2 in cell migration towards epidermal growth factor. J. Biol. Chem. 280, 29462-29469
26. Hait, N. C., Allegood, J., Maceyka, M., Strub, G. M., Harikumar, K. B., Singh, S. K., Luo, C., Marmorstein, R., Kordula, T., Milstien, S., and Spiegel, S. (2009) Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate. Science 325, 1254-1257
27. Pettus, B. J., Bielawski, J., Porcelli, A. M., Reames, D. L., Johnson, K. R., Morrow, J., Chalfant, C. E., Obeid, L. M., and Hannun, Y. A. (2003) The sphingosine kinase 1/sphingosine-1-phosphate pathway mediates COX-2 induction and PGE2 production in response to TNF-alpha. FASEB J. 17, 1411-1421
28. Billich, A., Bornancin, F., Mechtcheriakova, D., Natt, F., Huesken, D., and Baumruker, T. (2005) Basal and induced sphingosine kinase 1 activity in A549 carcinoma cells: function in cell survival and IL-1beta and TNF-alpha induced production of inflammatory mediators. Cell. Signal. 17, 1203-1217
29. De Palma, C., Meacci, E., Perrotta, C., Bruni, P., and Clementi, E. (2006) Endothelial nitric oxide synthase activation by tumor necrosis factor alpha through neutral sphingomyelinase 2, sphingosine kinase 1, and sphingosine 1 phosphate receptors: a novel pathway relevant to the pathophysiology of endothelium. Arterioscler. Thromb. Vasc. Biol. 26, 99-105
30. Scherer, E. Q., Yang, J., Canis, M., Reimann, K., Ivanov, K., Diehl, C. D., Backx, P. H., Wier, W. G., Strieth, S., Wangemann, P., Voigtlaender-Bolz, J., Lidington, D., and Bolz, S. S. (2010) Tumor necrosis factor-alpha enhances microvascular tone and reduces blood flow in the cochlea via enhanced sphingosine-1-phosphate signaling. Stroke 41, 2618-2624
31. Bishop, G. A., and Hostager, B. S. (2003) The CD40-CD154 interaction in B cell-T cell liaisons. Cytokine Growth Factor Rev. 14, 297-309
32. Gallagher, E., Enzler, T., Matsuzawa, A., Anzelon-Mills, A., Otero, D., Holzer, R., Janssen, E., Gao, M., and Karin, M. (2007) Kinase MEKK1 is required for CD40-dependent activation of the kinases Jnk and p38, germinal center formation, B cell proliferation and antibody production. Nat. Immunol. 8, 57-63
33. Chan, H., and Pitson, S. M. (2013) Post-translational regulation of sphingosine kinases. Biochim. Biophys. Acta 1831, 147-156
34. Spiegel, S., and Milstien, S. (2003) Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat. Rev. Mol. Cell Biol. 4, 397-407
35. Paugh, S. W., Paugh, B. S., Rahmani, M., Kapitonov, D., Almenara, J. A., Kordula, T., Milstien, S., Adams, J. K., Zipkin, R. E., Grant, S., and Spiegel, S. (2008) A selective sphingosine kinase 1 inhibitor integrates multiple molecular therapeutic targets in human leukemia. Blood 112, 1382-1391
36. Terstappen, L. W., Johnsen, S., Segers-Nolten, I. M., and Loken, M. R. (1990) Identification and characterization of plasma cells in normal human bone marrow by high-resolution flow cytometry. Blood 76, 1739-1747
37. Caven, T. H., Sturgill, J. L., and Conrad, D. H. (2007) 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. 247, 49-58
38. Schnute, M. E., McReynolds, M. D., Kasten, T., Yates, M., Jerome, G., Rains, J. W., Hall, T., Chrencik, J., Kraus, M., Cronin, C. N., Saabye, M., Highkin, M. K., Broadus, R., Ogawa, S., Cukyne, K., Zawadzke, L. E., Peterkin, V., Iyanar, K., Scholten, J. A., Wendling, J., Fujiwara, H., Nemirovskiy, O., Wittwer, A. J., and Nagiec, M. M. (2012) Modulation of cellular S1P levels with a novel, potent and specific inhibitor of sphingosine kinase-1. Biochem. J. 444, 79-88
39. Banchereau, J., Bazan, F., Blanchard, D., Briere, F., Galizzi, J. P., van Kooten, C., Liu, Y. J., Rousset, F., and Saeland, S. (1994) The CD40 antigen and its ligand. Annu. Rev. Immunol. 12, 881-922
40. Nagahashi, M., Ramachandran, S., Kim, E. Y., Allegood, J. C., Rashid, O. M., Yamada, A., Zhao, R., Milstien, S., Zhou, H., Spiegel, S., and Takabe, K. (2012) Sphingosine-1-phosphate produced by sphingosine kinase 1 promotes breast cancer progression by stimulating angiogenesis and lymphangiogenesis. Cancer Res. 72, 726-735
41. Price, M. M., Oskeritzian, C. A., Falanga, Y. T., Harikumar, K. B., Allegood, J. C., Alvarez, S. E., Conrad, D., Ryan, J. J., Milstien, S., and Spiegel, S. (2013) A specific sphingosine kinase 1 inhibitor attenuates airway hyperresponsiveness and inflammation in a mast cell-dependent murine model of allergic asthma. J. Allergy Clin. Immunol. 131, 501-511
42. Allende, M. L., Sasaki, T., Kawai, H., Olivera, A., Mi, Y., van Echten-Deckert, G., Hajdu, R., Rosenbach, M., Keohane, C. A., Mandala, S., Spiegel, S., and Proia, R. L. (2004) Mice deficient in sphingosine kinase 1 are rendered lymphopenic by FTY720. J. Biol. Chem. 279, 52487-52492
43. Olivera, A., Mizugishi, K., Tikhonova, A., Ciaccia, L., Odom, S., Proia, R. L., and Rivera, J. (2007) The sphingosine kinasesphingosine- 1-phosphate axis is a determinant of mast cell function and anaphylaxis. Immunity 26, 287-297
44. Snider, A. J., Kawamori, T., Bradshaw, S. G., Orr, K. A., Gilkeson, G. S., Hannun, Y. A., and Obeid, L. M. (2009) A role for sphingosine kinase 1 in dextran sulfate sodium-induced colitis. FASEB J. 23, 143-152
45. Nishiuma, T., Nishimura, Y., Okada, T., Kuramoto, E., Kotani, Y., Jahangeer, S., and Nakamura, S. (2008) Inhalation of sphingosine kinase inhibitor attenuates airway inflammation in asthmatic mouse model. Am. J. Physiol. Lung Cell. Mol. Physiol. 294, L1085-L1093
46. Chiba, Y., Takeuchi, H., Sakai, H., and Misawa, M. (2010) SKI-II, an inhibitor of sphingosine kinase, ameliorates antigen-induced bronchial smooth muscle hyperresponsiveness, but not airway inflammation, in mice. J. Pharmacol. Sci. 114, 304-310
47. Diesner, S. C., Olivera, A., Dillahunt, S., Schultz, C., Watzlawek, T., Forster-Waldl, E., Pollak, A., Jensen-Jarolim, E., Untersmayr, E., and Rivera, J. (2012) Sphingosine-kinase 1 and 2 contribute to oral sensitization and effector phase in a mouse model of food allergy. Immunol. Lett. 141, 210-219
48. Hasbold, J., Lyons, A. B., Kehry, M. R., and Hodgkin, P. D. (1998) Cell division number regulates IgG1 and IgE switching of B cells following stimulation by CD40 ligand and IL-4. Eur. J. Immunol. 28, 1040-1051
49. Elgueta, R., Benson, M. J., de Vries, V. C., Wasiuk, A., Guo, Y., and Noelle, R. J. (2009) Molecular mechanism and function of CD40/CD40L engagement in the immune system. Immunol. Rev. 229, 152-172
50. Li, Z. W., Omori, S. A., Labuda, T., Karin, M., and Rickert, R. C. (2003) IKK beta is required for peripheral B cell survival and proliferation. J. Immunol. 170, 4630-4637
51. Allende, M. L., Tuymetova, G., Lee, B. G., Bonifacino, E., Wu, Y. P., and Proia, R. L. (2010) S1P1 receptor directs the release of immature B cells from bone marrow into blood. J. Exp. Med. 207, 1113-1124
52. Donovan, E. E., Pelanda, R., and Torres, R. M. (2010) S1P3 confers differential S1P-induced migration by autoreactive and non-autoreactive immature B cells and is required for normal B-cell development. Eur. J. Immunol. 40, 688-698
53. Gohda, M., Kunisawa, J., Miura, F., Kagiyama, Y., Kurashima, Y., Higuchi, M., Ishikawa, I., Ogahara, I., and Kiyono, H. (2008) Sphingosine 1-phosphate regulates the egress of IgA plasmablasts from Peyer's patches for intestinal IgA responses. J. Immunol. 180, 5335-5343
54. Kabashima, K., Haynes, N. M., Xu, Y., Nutt, S. L., Allende, M. L., Proia, R. L., and Cyster, J. G. (2006) Plasma cell S1P1 expression determines secondary lymphoid organ retention versus bone marrow tropism. J. Exp. Med. 203, 2683-2690
55. Cinamon, G., Matloubian, M., Lesneski, M. J., Xu, Y., Low, C., Lu, T., Proia, R. L., and Cyster, J. G. (2004) Sphingosine 1-phosphate receptor 1 promotes B cell localization in the splenic marginal zone. Nat. Immunol. 5, 713-720
56. Grassme, H., Jendrossek, V., Bock, J., Riehle, A., and Gulbins, E. (2002) Ceramide-rich membrane rafts mediate CD40 clustering. J. Immunol. 168, 298-307
57. Henry, B., Ziobro, R., Becker, K. A., Kolesnick, R., and Gulbins, E. (2013) Acid sphingomyelinase. Handb. Exp. Pharmacol. 2013, 77-88