T/B-cell interactions are more transient in response to weak stimuli in SLE-prone mice

European Journal of Immunology

Volumn 44, Issue 12, 2014, Pages 3522-3531

  Sinai, Parisa ^a,b   Dozmorov, Igor M ^b   Song, Ran ^b   Schwartzberg, Pamela L ^c   Wakeland, Edward K ^b   Wülfing, Christoph ^a,b  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

Author keywords

Actin; Imaging; Immunological synapse; Protein kinase C; Systemic lupus erythematosus

Indexed keywords

ACTIN; CD150 ANTIGEN; PROTEIN KINASE C; T LYMPHOCYTE RECEPTOR; VAV PROTEIN; PRKCE PROTEIN, MOUSE; PROTEIN KINASE C EPSILON; VAV1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CELL INTERACTION; CONTROLLED STUDY; DISEASE PREDISPOSITION; GENE EXPRESSION; IMMUNOREACTIVITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; ANIMAL; CELL COMMUNICATION; FEMALE; GENE EXPRESSION REGULATION; GERMINAL CENTER; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; PATHOLOGY;

ANIMALS; B-LYMPHOCYTES; CELL COMMUNICATION; FEMALE; GENE EXPRESSION REGULATION; GERMINAL CENTER; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; MICE; PROTEIN KINASE C-EPSILON; PROTO-ONCOGENE PROTEINS C-VAV; T-LYMPHOCYTES;

EID: 84924302055     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201444602     Document Type: Article

References (37)

1. Fairhurst, A. M., Wandstrat, A. E. and Wakeland, E. K., Systemic lupus erythematosus: multiple immunological phenotypes in a complex genetic disease. Adv. Immunol. 2006. 92: 1-69.
2. Crispin, J. C., Kyttaris, V. C., Terhorst, C. and Tsokos, G. C., T cells as therapeutic targets in SLE. Nat. Rev. Rheumatol. 2010. 6: 317-325.
3. Wang, A., Batteux, F. and Wakeland, E. K., The role of SLAM/CD2 polymorphisms in systemic autoimmunity. Curr. Opin. Immunol. 2010. 22: 706-714.
4. Schwartzberg, P. L., Mueller, K. L., Qi, H. and Cannons, J. L., SLAM receptors and SAP influence lymphocyte interactions, development and function. Nat. Rev. Immunol. 2009. 9: 39-46.
5. Calpe, S., Wang, N., Romero, X., Berger, S. B., Lanyi, A., Engel, P. and Terhorst, C., The SLAM and SAP gene families control innate and adaptive immune responses. Adv. Immunol. 2008. 97: 177-250.
6. Cannons, J. L., Wu, J. Z., Gomez-Rodriguez, J., Zhang, J., Dong, B., Liu, Y., Shaw, S. et al., Biochemical and genetic evidence for a SAP-PKC-theta interaction contributing to IL-4 regulation. J. Immunol. 2010. 185: 2819-2827.
7. Zhong, M. C. and Veillette, A., Control of T lymphocyte signaling by Ly108, a signaling lymphocytic activation molecule family receptor implicated in autoimmunity. J. Biol. Chem. 2008. 283: 19255-19264.
8. Qi, H., From SAP-less T cells to helpless B cells and back: dynamic TB cell interactions underlie germinal center development and function. Immunol. Rev. 2012. 247: 24-35.
9. Cannons, J. L., Qi, H., Lu, K. T., Dutta, M., Gomez-Rodriguez, J., Cheng, J., Wakeland, E. K. et al., Optimal germinal center responses require a multistage T cell: B cell adhesion process involving integrins, SLAMassociated protein, and CD84. Immunity 2010. 32: 253-265.
10. Kageyama, R., Cannons, J. L., Zhao, F., Yusuf, I., Lao, C., Locci, M., Schwartzberg, P. L. et al., The receptor Ly108 functions as a SAP adaptordependent on-off switch for T cell help to B cells and NKT cell development. Immunity 2012. 36: 986-1002.
11. Barnden, M. J., Allison, J., Heath, W. R. and Carbone, F. R., Defective TCR expression in transgenic mice constructed using cDNA-based alpha-and beta-chain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 1998. 76: 34-40.
12. Schubert, D. A., Gordo, S., Sabatino, J. J., Jr., Vardhana, S., Gagnon, E., Sethi, D. K., Seth, N. P. et al., Self-reactive human CD4 T cell clones form unusual immunological synapses. J. Exp. Med. 2012. 209: 335-352.
13. Robertson, J. M., Jensen, P. E. and Evavold, B. D., DO11.10 and OT-II T cells recognize a C-terminal ovalbumin 323-339 epitope. J. Immunol. 2000. 164: 4706-4712.
14. Roybal, K. T., Sinai, P., Verkade, P., Murphy, R. F. and Wülfing, C., The actin-driven spatiotemporal organization of T-cell signaling at the system scale. Immunol. Rev. 2013. 256: 133-147.
15. Singleton, K. L., Gosh, M., Dandekar, R. D., Au-Yeung, B. B., Ksionda, O., Tybulewicz, V. L., Altman, A. et al., Itk controls the spatiotemporal organization of T cell activation. Sci. Signal. 2011. 4: ra66.
16. Billadeau, D. D., Nolz, J. C. and Gomez, T. S., Regulation of T-cell activation by the cytoskeleton. Nat. Rev. Immunol. 2007. 7: 131-143.
17. Tybulewicz, V. L., Vav-family proteins in T-cell signalling. Curr. Opin. Immunol. 2005. 17: 267-274.
18. Sims, T. N., Soos, T. J., Xenias, H. S., Dubin-Thaler, B., Hofman, J. M., Waite, J. C., Cameron, T. O. et al., Opposing effects of PKCtheta andWASp on symmetry breaking and relocation of the immunological synapse. Cell 2007. 129: 773-785.
19. Zhao, F., Cannons, J. L., Dutta, M., Griffiths, G. M. and Schwartzberg, P. L., Positive and negative signaling through SLAM receptors regulate synapse organization and thresholds of cytolysis. Immunity 2012. 36: 1003-1016.
20. Sinai, P., Nguyen, C., Schatzle, J. D. and Wülfing, C., Transience in polarization of cytolytic effectors is required for efficient killing and controlled by Cdc42. Proc. Natl. Acad. Sci. USA 2010. 107: 11912-11917.
21. Schwickert, T. A., Victora, G. D., Fooksman, D. R., Kamphorst, A. O., Mugnier, M. R., Gitlin, A. D., Dustin, M. L. et al., A dynamic T cell-limited checkpoint regulates affinity-dependent B cell entry into the germinal center. J. Exp. Med. 2011. 208: 1243-1252.
22. Allen, C. D., Okada, T. and Cyster, J. G., Germinal-center organization and cellular dynamics. Immunity 2007. 27: 190-202.
23. Sun, Z., Arendt, C. W., Ellmeier, W., Schaeffer, E. M., Sunshine, M. J., Gandhi, L., Annes, J. et al., PKC-theta is required for TCR-induced NFkappaB activation in mature but not immature T lymphocytes. Nature 2000. 404: 402-407.
24. Becart, S., Balancio, A. J., Charvet, C., Feau, S., Sedwick, C. E. and Altman, A., Tyrosine-phosphorylation-dependent translocation of the SLAT protein to the immunological synapse is required for NFAT transcription factor activation. Immunity 2008. 29: 704-719.
25. Fanzo, J. C., Yang, W., Jang, S. Y., Gupta, S., Chen, Q., Siddiq, A., Greenberg, S. et al., Loss of IRF-4-binding protein leads to the spontaneous development of systemic autoimmunity. J. Clin. Invest. 2006. 116: 703-714.
26. Haraldsson, M. K., Louis-Dit-Sully, C. A., Lawson, B. R., Sternik, G., Santiago-Raber, M. L., Gascoigne, N. R., Theofilopoulos, A. N. et al., The lupus-related Lmb3 locus contains a disease-suppressing Coronin-1A gene mutation. Immunity 2008. 28: 40-51.
27. Davis, D. M., Mechanisms and functions for the duration of intercellular contacts made by lymphocytes. Nat. Rev. Immunol. 2009. 9: 543-555.
28. Semmrich, M., Smith, A., Feterowski, C., Beer, S., Engelhardt, B., Busch, D. H., Bartsch, B. et al., Importance of integrin LFA-1 deactivation for the generation of immune responses. J. Exp. Med. 2005. 201: 1987-1998.
29. Qi, H., Cannons, J. L., Klauschen, F., Schwartzberg, P. L. and Germain, R. N., SAP-controlled T-B cell interactions underlie germinal centre formation. Nature 2008. 455: 764-769.
30. Keszei, M., Detre, C., Rietdijk, S. T., Munoz, P., Romero, X., Berger, S. B., Calpe, S. et al., A novel isoform of the Ly108 gene ameliorates murine lupus. J Exp. Med. 2011. 208: 811-822.
31. Dutta, M. and Schwartzberg, P. L., Characterization of Ly108 in the thymus: evidence for distinct properties of a novel form of Ly108. J. Immunol. 2012. 188: 3031-3041.
32. Bubier, J. A., Sproule, T. J., Foreman, O., Spolski, R., Shaffer, D. J., Morse, H. C., 3rd, Leonard, W. J. et al., A critical role for IL-21 receptor signaling in the pathogenesis of systemic lupus erythematosus in BXSB-Yaa mice. Proc. Natl. Acad. Sci. USA 2009. 106: 1518-1523.
33. Kumar, K. R., Li, L., Yan, M., Bhaskarabhatla, M., Mobley, A. B., Nguyen, C., Mooney, J. M. et al., Regulation of B cell tolerance by the lupus susceptibility gene Ly108. Science 2006. 312: 1665-1669.
34. Blanco, P., Palucka, A. K., Gill, M., Pascual, V. and Banchereau, J., Induction of dendritic cell differentiation by IFN-alpha in systemic lupus erythematosus. Science 2001. 294: 1540-1543.
35. Singleton, K. L., Roybal, K. T., Sun, Y., Fu, G., Gascoigne, N. R., van Oers, N. S. and Wülfing, C., Spatiotemporal patterning during T cell activation is highly diverse. Sci. Signal. 2009. 2: ra15.
36. Tskvitaria-Fuller, I., Seth, A., Mistry, N., Gu, H., Rosen, M. K. and Wülfing, C., Specific patterns of Cdc42 activity are related to distinct elements of T cell polarization. J. Immunol. 2006. 177: 1708-1720.
37. Dozmorov, I. and Lefkovits, I., Internal standard-based analysis of microarray data. Part 1: analysis of differential gene expressions. Nucleic Acids Res. 2009. 37: 6323-6339.