SLAM-SAP signaling promotes differentiation of IL-17-producing T cells and progression of experimental autoimmune encephalomyelitis

Journal of Immunology

Volumn 193, Issue 12, 2014, Pages 5841-5853

  Huang, Yu Hsuan ^a,b   Tsai, Kevin ^a,b   Ma, Caixia ^a,c   Vallance, Bruce A ^a,c   Priatel, John J ^a,b   Tan, Rusung ^a,b,d  

^a BC CHILDREN S HOSPITAL   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d SIDRA MEDICAL AND RESEARCH CENTER   (Qatar)

Author keywords

[No Author keywords available]

Indexed keywords

CD150 ANTIGEN; INTERLEUKIN 17; PROTEIN ANTIBODY; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN; CELL SURFACE RECEPTOR; GAMMA INTERFERON; INTERLEUKIN 4; LEUKOCYTE ANTIGEN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; SH2D1A PROTEIN, MOUSE; SIGNAL PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; DISEASE SEVERITY; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; IMMUNOPATHOGENESIS; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; PROTEIN DEFICIENCY; SIGNAL TRANSDUCTION; SPLEEN CELL; T LYMPHOCYTE; TC17 CELL; TH17 CELL; WILD TYPE; ANIMAL; BIOSYNTHESIS; CELL DIFFERENTIATION; CYTOLOGY; DISEASE COURSE; GENE EXPRESSION; GENETICS; IMMUNIZATION; IMMUNOLOGY; IMMUNOPHENOTYPING; KNOCKOUT MOUSE; METABOLISM; PHENOTYPE; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; ANTIGENS, CD; CELL DIFFERENTIATION; DISEASE PROGRESSION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GENE EXPRESSION; IMMUNIZATION; IMMUNOPHENOTYPING; INTERFERON-GAMMA; INTERLEUKIN-17; INTERLEUKIN-4; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, KNOCKOUT; MYELIN-OLIGODENDROCYTE GLYCOPROTEIN; PHENOTYPE; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS; TH17 CELLS;

EID: 84916892229     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301435     Document Type: Article

References (73)

1. Zhu, J., and W. E. Paul. 2010. Peripheral CD4+ T-cell differentiation regulated by networks of cytokines and transcription factors. Immunol. Rev. 238: 247-262.
2. Ghoreschi, K., A. Laurence, X. P. Yang, K. Hirahara, and J. J. O'Shea. 2011. T helper 17 cell heterogeneity and pathogenicity in autoimmune disease. Trends Immunol. 32: 395-401.
3. Ivanov, I. I., B. S. McKenzie, L. Zhou, C. E. Tadokoro, A. Lepelley, J. J. Lafaille, D. J. Cua, and D. R. Littman. 2006. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126: 1121-1133.
4. Intlekofer, A. M., A. Banerjee, N. Takemoto, S. M. Gordon, C. S. Dejong, H. Shin, C. A. Hunter, E. J. Wherry, T. Lindsten, and S. L. Reiner. 2008. Anomalous type 17 response to viral infection by CD8+ T cells lacking T-bet and eomesodermin. Science 321: 408-411.
5. Liu, S. J., J. P. Tsai, C. R. Shen, Y. P. Sher, C. L. Hsieh, Y. C. Yeh, A. H. Chou, S. R. Chang, K. N. Hsiao, F. W. Yu, and H. W. Chen. 2007. Induction of a distinct CD8 Tnc17 subset by transforming growth factor-beta and interleukin-6. J. Leukoc. Biol. 82: 354-360.
6. Manel, N., D. Unutmaz, and D. R. Littman. 2008. The differentiation of human T (H)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor RORgammat. Nat. Immunol. 9: 641-649.
7. Huber, M., S. Heink, H. Grothe, A. Guralnik, K. Reinhard, K. Elflein, T. Hünig, H. W. Mittrücker, A. Brüstle, T. Kamradt, and M. Lohoff. 2009. A Th17-like developmental process leads to CD8(+) Tc17 cells with reduced cytotoxic activity. Eur. J. Immunol. 39: 1716-1725.
8. Korn, T., E. Bettelli, M. Oukka, and V. K. Kuchroo. 2009. IL-17 and Th17 Cells. Annu. Rev. Immunol. 27: 485-517.
9. Ciric, B., M. El-behi, R. Cabrera, G. X. Zhang, and A. Rostami. 2009. IL-23 drives pathogenic IL-17-producing CD8+ T cells. J. Immunol. 182: 5296-5305.
10. Kuang, D. M., C. Peng, Q. Zhao, Y. Wu, L. Y. Zhu, J. Wang, X. Y. Yin, L. Li, and L. Zheng. 2010. Tumor-activated monocytes promote expansion of IL-17-producing CD8+ T cells in hepatocellular carcinoma patients. J. Immunol. 185: 1544-1549.
11. Yeh, N., N. L. Glosson, N. Wang, L. Guindon, C. McKinley, H. Hamada, Q. Li, R. W. Dutton, P. Shrikant, B. Zhou, et al. 2010. Tc17 cells are capable of mediating immunity to vaccinia virus by acquisition of a cytotoxic phenotype. J. Immunol. 185: 2089-2098.
12. Marwaha, A. K., N. J. Leung, A. N. McMurchy, and M. K. Levings. 2012. TH17 Cells in Autoimmunity and Immunodeficiency: Protective or Pathogenic? Front. Immunol. 3: 129.
13. Hamada, H., Mde. L. Garcia-Hernandez, J. B. Reome, S. K. Misra, T. M. Strutt, K. K. McKinstry, A. M. Cooper, S. L. Swain, and R. W. Dutton. 2009. Tc17, a unique subset of CD8 T cells that can protect against lethal influenza challenge. J. Immunol. 182: 3469-3481.
14. Tajima, M., D. Wakita, D. Noguchi, K. Chamoto, Z. Yue, K. Fugo, H. Ishigame, Y. Iwakura, H. Kitamura, and T. Nishimura. 2008. IL-6-dependent spontaneous proliferation is required for the induction of colitogenic IL-17-producing CD8+ T cells. J. Exp. Med. 205: 1019-1027.
15. Tzartos, J. S., M. A. Friese, M. J. Craner, J. Palace, J. Newcombe, M. M. Esiri, and L. Fugger. 2008. Interleukin-17 production in central nervous system-infiltrating T cells and glial cells is associated with active disease in multiple sclerosis. Am. J. Pathol. 172: 146-155.
16. Caruso, R., D. Fina, O. A. Paoluzi, G. Del Vecchio Blanco, C. Stolfi, A. Rizzo, F. Caprioli, M. Sarra, F. Andrei, M. C. Fantini, et al. 2008. IL-23-mediated regulation of IL-17 production in Helicobacter pylori-infected gastric mucosa. Eur. J. Immunol. 38: 470-478.
17. Res, P. C., G. Piskin, O. J. de Boer, C. M. van der Loos, P. Teeling, J. D. Bos, and M. B. Teunissen. 2010. Overrepresentation of IL-17A and IL-22 producing CD8 T cells in lesional skin suggests their involvement in the pathogenesis of psoriasis. PLoS ONE 5: e14108.
18. Huber, M., S. Heink, A. Pagenstecher, K. Reinhard, J. Ritter, A. Visekruna, A. Guralnik, N. Bollig, K. Jeltsch, C. Heinemann, et al. 2013. IL-17A secretion by CD8+ T cells supports Th17-mediated autoimmune encephalomyelitis. J. Clin. Invest. 123: 247-260.
19. Grafmueller, S., E. Billerbeck, H. E. Blum, C. Neumann-Haefelin, and R. Thimme. 2012. Differential antigen specificity of hepatitis C virus-specific interleukin 17- and interferon γ-producing CD8(+) T cells during chronic infection. J. Infect. Dis. 205: 1142-1146.
20. Marwaha, A. K., S. Q. Crome, C. Panagiotopoulos, K. B. Berg, H. Qin, Q. Ouyang, L. Xu, J. J. Priatel, M. K. Levings, and R. Tan. 2010. Cutting edge: Increased IL-17-secreting T cells in children with new-onset type 1 diabetes. J. Immunol. 185: 3814-3818.
21. Honkanen, J., J. K. Nieminen, R. Gao, K. Luopajarvi, H. M. Salo, J. Ilonen, M. Knip, T. Otonkoski, and O. Vaarala. 2010. IL-17 immunity in human type 1 diabetes. J. Immunol. 185: 1959-1967.
22. Hofstetter, H. H., S. M. Ibrahim, D. Koczan, N. Kruse, A. Weishaupt, K. V. Toyka, and R. Gold. 2005. Therapeutic efficacy of IL-17 neutralization in murine experimental autoimmune encephalomyelitis. Cell. Immunol. 237: 123-130.
23. Komiyama, Y., S. Nakae, T. Matsuki, A. Nambu, H. Ishigame, S. Kakuta, K. Sudo, and Y. Iwakura. 2006. IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J. Immunol. 177: 566-573.
24. McGeachy, M. J., Y. Chen, C. M. Tato, A. Laurence, B. Joyce-Shaikh, W. M. Blumenschein, T. K. McClanahan, J. J. O'Shea, and D. J. Cua. 2009. The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo. Nat. Immunol. 10: 314-324.
25. Cannons, J. L., S. G. Tangye, and P. L. Schwartzberg. 2011. SLAM family receptors and SAP adaptors in immunity. Annu. Rev. Immunol. 29: 665-705.
26. Dong, Z., and A. Veillette. 2010. How do SAP family deficiencies compromise immunity? Trends Immunol. 31: 295-302.
27. Howie, D., M. Simarro, J. Sayos, M. Guirado, J. Sancho, and C. Terhorst. 2002. Molecular dissection of the signaling and costimulatory functions of CD150 (SLAM): CD150/SAP binding and CD150-mediated costimulation. Blood 99: 957-965.
28. Cannons, J. L., J. Z. Wu, J. Gomez-Rodriguez, J. Zhang, B. Dong, Y. Liu, S. Shaw, K. A. Siminovitch, and P. L. Schwartzberg. 2010. Biochemical and genetic evidence for a SAP-PKC-theta interaction contributing to IL-4 regulation. J. Immunol. 185: 2819-2827.
29. Latour, S., G. Gish, C. D. Helgason, R. K. Humphries, T. Pawson, and A. Veillette. 2001. Regulation of SLAM-mediated signal transduction by SAP, the X-linked lymphoproliferative gene product. Nat. Immunol. 2: 681-690.
30. Sayos, J., C. Wu, M. Morra, N. Wang, X. Zhang, D. Allen, S. van Schaik, L. Notarangelo, R. Geha, M. G. Roncarolo, et al. 1998. The X-linked lympho-proliferative-disease gene product SAP regulates signals induced through the coreceptor SLAM. Nature 395: 462-469.
31. Dong, Z., M. E. Cruz-Munoz, M. C. Zhong, R. Chen, S. Latour, and A. Veillette. 2009. Essential function for SAP family adaptors in the surveillance of hematopoietic cells by natural killer cells. Nat. Immunol. 10: 973-980.
32. Dong, Z., D. Davidson, L. A. Pérez-Quintero, T. Kurosaki, W. Swat, and A. Veillette. 2012. The adaptor SAP controls NK cell activation by regulating the enzymes Vav-1 and SHIP-1 and by enhancing conjugates with target cells. Immunity 36: 974-985.
33. Zhao, F., J. L. Cannons, M. Dutta, G. M. Griffiths, and P. L. Schwartzberg. 2012. Positive and negative signaling through SLAM receptors regulate synapse organization and thresholds of cytolysis. Immunity 36: 1003-1016.
34. Palendira, U., C. Low, A. Chan, A. D. Hislop, E. Ho, T. G. Phan, E. Deenick, M. C. Cook, D. S. Riminton, S. Choo, et al. 2011. Molecular pathogenesis of EBV susceptibility in XLP as revealed by analysis of female carriers with heterozygous expression of SAP. PLoS Biol. 9: e1001187.
35. Veillette, A., S. Zhang, X. Shi, Z. Dong, D. Davidson, and M. C. Zhong. 2008. SAP expression in T cells, not in B cells, is required for humoral immunity. Proc. Natl. Acad. Sci. USA 105: 1273-1278.
36. Crotty, S., E. N. Kersh, J. Cannons, P. L. Schwartzberg, and R. Ahmed. 2003. SAP is required for generating long-term humoral immunity. Nature 421: 282-287.
37. Cannons, J. L., H. Qi, K. T. Lu, M. Dutta, J. Gomez-Rodriguez, J. Cheng, E. K. Wakeland, R. N. Germain, and P. L. Schwartzberg. 2010. Optimal germinal center responses require a multistage T cell:B cell adhesion process involving integrins, SLAM-associated protein, and CD84. Immunity 32: 253-265.
38. Qi, H., J. L. Cannons, F. Klauschen, P. L. Schwartzberg, and R. N. Germain. 2008. SAP-controlled T-B cell interactions underlie germinal centre formation. Nature 455: 764-769.
39. Pasquier, B., L. Yin, M. C. Fondanèche, F. Relouzat, C. Bloch-Queyrat, N. Lambert, A. Fischer, G. de Saint-Basile, and S. Latour. 2005. Defective NKT cell development in mice and humans lacking the adapter SAP, the X-linked lymphoproliferative syndrome gene product. J. Exp. Med. 201: 695-701.
40. Chung, B., A. Aoukaty, J. Dutz, C. Terhorst, and R. Tan. 2005. Signaling lymphocytic activation molecule-associated protein controls NKT cell functions. J. Immunol. 174: 3153-3157.
41. Nichols, K. E., J. Hom, S. Y. Gong, A. Ganguly, C. S. Ma, J. L. Cannons, S. G. Tangye, P. L. Schwartzberg, G. A. Koretzky, and P. L. Stein. 2005. Regulation of NKT cell development by SAP, the protein defective in XLP. Nat. Med. 11: 340-345.
42. Wu, C., K. B. Nguyen, G. C. Pien, N. Wang, C. Gullo, D. Howie, M. R. Sosa, M. J. Edwards, P. Borrow, A. R. Satoskar, et al. 2001. SAP controls T cell responses to virus and terminal differentiation of TH2 cells. Nat. Immunol. 2: 410-414.
43. Roncagalli, R., J. E. Taylor, S. Zhang, X. Shi, R. Chen, M. E. Cruz-Munoz, L. Yin, S. Latour, and A. Veillette. 2005. Negative regulation of natural killer cell function by EAT-2, a SAP-related adaptor. Nat. Immunol. 6: 1002-1010.
44. Ryz, N. R., S. J. Patterson, Y. Zhang, C. Ma, T. Huang, G. Bhinder, X. Wu, J. Chan, A. Glesby, H. P. Sham, et al. 2012. Active vitamin D (1,25-dihydroxyvitamin D3) increases host susceptibility to Citrobacter rodentium by suppressing mucosal Th17 responses. Am. J. Physiol. Gastrointest. Liver Physiol. 303: G1299-G1311.
45. Czar, M. J., E. N. Kersh, L. A. Mijares, G. Lanier, J. Lewis, G. Yap, A. Chen, A. Sher, C. S. Duckett, R. Ahmed, and P. L. Schwartzberg. 2001. Altered lymphocyte responses and cytokine production in mice deficient in the X-linked lymphoproliferative disease gene SH2D1A/DSHP/SAP. Proc. Natl. Acad. Sci. USA 98: 7449-7454.
46. Cocks, B. G., C. C. Chang, J. M. Carballido, H. Yssel, J. E. de Vries, and G. Aversa. 1995. A novel receptor involved in T-cell activation. Nature 376: 260-263.
47. Torchinsky, M. B., J. Garaude, A. P. Martin, and J. M. Blander. 2009. Innate immune recognition of infected apoptotic cells directs T(H)17 cell differentiation. Nature 458: 78-82.
48. Mangan, P. R., L. E. Harrington, D. B. O'Quinn, W. S. Helms, D. C. Bullard, C. O. Elson, R. D. Hatton, S. M. Wahl, T. R. Schoeb, and C. T. Weaver. 2006. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441: 231-234.
49. Curtis, M. M., and S. S. Way. 2009. Interleukin-17 in host defence against bacterial, mycobacterial and fungal pathogens. Immunology 126: 177-185.
50. Annunziato, F., and S. Romagnani. 2010. The transient nature of the Th17 phenotype. Eur. J. Immunol. 40: 3312-3316.
51. Bida, A. T., J. L. Upshaw Neff, C. J. Dick, R. A. Schoon, A. Brickshawana, C. C. Chini, and D. D. Billadeau. 2011. 2B4 utilizes ITAM-containing receptor complexes to initiate intracellular signaling and cytolysis. Mol. Immunol. 48: 1149-1159.
52. Proust, R., J. Bertoglio, and F. Gesbert. 2012. The adaptor protein SAP directly associates with CD3ζ chain and regulates T cell receptor signaling. PLoS ONE 7: e43200.
53. Snow, A. L., R. A. Marsh, S. M. Krummey, P. Roehrs, L. R. Young, K. Zhang, J. van Hoff, D. Dhar, K. E. Nichols, A. H. Filipovich, et al. 2009. Restimulation-induced apoptosis of T cells is impaired in patients with X-linked lymphoproliferative disease caused by SAP deficiency. J. Clin. Invest. 119: 2976-2989.
54. Baldanzi, G., A. Pighini, V. Bettio, E. Rainero, S. Traini, F. Chianale, P. E. Porporato, N. Filigheddu, R. Mesturini, S. Song, et al. 2011. SAP-mediated inhibition of diacylglycerol kinase α regulates TCR-induced diacylglycerol signaling. J. Immunol. 187: 5941-5951.
55. Cannons, J. L., L. J. Yu, B. Hill, L. A. Mijares, D. Dombroski, K. E. Nichols, A. Antonellis, G. A. Koretzky, K. Gardner, and P. L. Schwartzberg. 2004. SAP regulates T(H)2 differentiation and PKC-theta-mediated activation of NF-kappaB1. Immunity 21: 693-706.
56. Hwang, E. S. 2010. Transcriptional regulation of T helper 17 cell differentiation. Yonsei Med. J. 51: 484-491.
57. Schraml, B. U., K. Hildner, W. Ise, W. L. Lee, W. A. Smith, B. Solomon, G. Sahota, J. Sim, R. Mukasa, S. Cemerski, et al. 2009. The AP-1 transcription factor Batf controls T(H)17 differentiation. Nature 460: 405-409.
58. Chatterjee, M., C. M. Hedrich, T. Rauen, C. Ioannidis, C. Terhorst, and G. C. Tsokos. 2012. CD3-T cell receptor co-stimulation through SLAMF3 and SLAMF6 receptors enhances RORγt recruitment to the IL17A promoter in human T lymphocytes. J. Biol. Chem. 287: 38168-38177.
59. Ueda, A., L. Zhou, and P. L. Stein. 2012. Fyn promotes Th17 differentiation by regulating the kinetics of RORγt and Foxp3 expression. J. Immunol. 188: 5247-5256.
60. Komori, H., H. Furukawa, S. Mori, M. R. Ito, M. Terada, M. C. Zhang, N. Ishii, N. Sakuma, M. Nose, and M. Ono. 2006. A signal adaptor SLAM-associated protein regulates spontaneous autoimmunity and Fas-dependent lymphoproliferation in MRL-Faslpr lupus mice. J. Immunol. 176: 395-400.
61. Hron, J. D., L. Caplan, A. J. Gerth, P. L. Schwartzberg, and S. L. Peng. 2004. SH2D1A regulates T-dependent humoral autoimmunity. J. Exp. Med. 200: 261-266.
62. Bygrave, A. E., K. L. Rose, J. Cortes-Hernandez, J. Warren, R. J. Rigby, H. T. Cook, M. J. Walport, T. J. Vyse, and M. Botto. 2004. Spontaneous autoimmunity in 129 and C57BL/6 mice-implications for autoimmunity described in gene-targeted mice. PLoS Biol. 2: E243.
63. Chervonsky, A. V. 2013. Microbiota and autoimmunity. Cold Spring Harb. Perspect. Biol. 5: a007294.
64. Van Kaer, L. 2007. NKT cells: T lymphocytes with innate effector functions. Curr. Opin. Immunol. 19: 354-364.
65. Miyamoto, K., S. Miyake, and T. Yamamura. 2001. A synthetic glycolipid prevents autoimmune encephalomyelitis by inducing TH2 bias of natural killer T cells. Nature 413: 531-534.
66. Singh, A. K., M. T. Wilson, S. Hong, D. Olivares-Villagómez, C. Du, A. K. Stanic, S. Joyce, S. Sriram, Y. Koezuka, and L. Van Kaer. 2001. Natural killer T cell activation protects mice against experimental autoimmune encephalomyelitis. J. Exp. Med. 194: 1801-1811.
67. Furlan, R., A. Bergami, D. Cantarella, E. Brambilla, M. Taniguchi, P. Dellabona, G. Casorati, and G. Martino. 2003. Activation of invariant NKT cells by alphaGalCer administration protects mice from MOG35-55-induced EAE: critical roles for administration route and IFN-gamma. Eur. J. Immunol. 33: 1830-1838.
68. Weber, M. S., T. Prod'homme, J. C. Patarroyo, N. Molnarfi, T. Karnezis, K. Lehmann-Horn, D. M. Danilenko, J. Eastham-Anderson, A. J. Slavin, C. Linington, et al. 2010. B-cell activation influences T-cell polarization and outcome of anti-CD20 B-cell depletion in central nervous system autoimmunity. Ann. Neurol. 68: 369-383.
69. Cross, A. H., J. L. Stark, J. Lauber, M. J. Ramsbottom, and J. A. Lyons. 2006. Rituximab reduces B cells and T cells in cerebrospinal fluid of multiple sclerosis patients. J. Neuroimmunol. 180: 63-70.
70. Becher, B., and B. M. Segal. 2011. T(H)17 cytokines in autoimmune neuroinflammation. Curr. Opin. Immunol. 23: 707-712.
71. Begovich, A. B., M. Chang, S. J. Caillier, D. Lew, J. J. Catanese, J. Wang, S. L. Hauser, and J. R. Oksenberg. 2007. The autoimmune disease-associated IL12B and IL23R polymorphisms in multiple sclerosis. Hum. Immunol. 68: 934-937.
72. Ferrante, P., M. L. Fusi, M. Saresella, D. Caputo, M. Biasin, D. Trabattoni, A. Salvaggio, E. Clerici, J. E. de Vries, G. Aversa, et al. 1998. Cytokine production and surface marker expression in acute and stable multiple sclerosis: altered IL-12 production and augmented signaling lymphocytic activation molecule (SLAM)-expressing lymphocytes in acute multiple sclerosis. J. Immunol. 160: 1514-1521.
73. Chatterjee, M., T. Rauen, K. Kis-Toth, V. C. Kyttaris, C. M. Hedrich, C. Terhorst, and G. C. Tsokos. 2012. Increased expression of SLAM receptors SLAMF3 and SLAMF6 in systemic lupus erythematosus T lymphocytes promotes Th17 differentiation. J. Immunol. 188: 1206-1212.