Functional education of invariant NKT cells by dendritic cell tuning of SHP-1

Journal of Immunology

Volumn 190, Issue 7, 2013, Pages 3299-3308

  Napolitano, Anna ^a   Pittoni, Paola ^a,e   Beaudoin, Lucie ^b   Lehuen, Agnes ^b   Voehringer, David ^c   MacDonald, H Robson ^d   Dellabona, Paolo ^a   Casorati, Giulia ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b INSERM   (France)

^c UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^d UNIVERSITY OF LAUSANNE   (Switzerland)

^e NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CD1D ANTIGEN; PROTEIN TYROSINE PHOSPHATASE SHP 1; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ARTICLE; CHIMERA; CONTROLLED STUDY; DENDRITIC CELL; HETEROZYGOTE; IMMUNE RESPONSE; IMMUNOREGULATION; LYMPHOCYTE MIGRATION; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; THYMOCYTE; TRANSGENIC MOUSE; UPREGULATION;

ANIMALS; ANTIGENS, CD1D; CLUSTER ANALYSIS; DENDRITIC CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENOMIC IMPRINTING; HUMANS; HYPERSENSITIVITY; MICE; MICE, KNOCKOUT; NATURAL KILLER T-CELLS; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 6; THYMUS GLAND;

EID: 84875459721     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203466     Document Type: Article

References (49)

1. Bendelac, A., P. B. Savage, and L. Teyton. 2007. The biology of NKT cells. Annu. Rev. Immunol. 25: 297-336.
2. Kinjo, Y., and K. Ueno. 2011. iNKT cells in microbial immunity: recognition of microbial glycolipids. Microbiol. Immunol. 55: 472-482.
3. Kinjo, Y., P. Illarionov, J. L. Vela, B. Pei, E. Girardi, X. Li, Y. Li, M. Imamura, Y. Kaneko, A. Okawara, et al. 2011. Invariant natural killer T cells recognize glycolipids from pathogenic Gram-positive bacteria. Nat. Immunol. 12: 966-974.
4. Brennan, P. J., R. V. Tatituri, M. Brigl, E. Y. Kim, A. Tuli, J. P. Sanderson, S. D. Gadola, F. F. Hsu, G. S. Besra, and M. B. Brenner. 2011. Invariant natural killer T cells recognize lipid self antigen induced by microbial danger signals. Nat. Immunol. 12: 1202-1211.
5. Paget, C., T. Mallevaey, A. O. Speak, D. Torres, J. Fontaine, K. C. Sheehan, M. Capron, B. Ryffel, C. Faveeuw, M. Leite de Moraes, et al. 2007. Activation of invariant NKT cells by toll-like receptor 9-stimulated dendritic cells requires type I interferon and charged glycosphingolipids. Immunity 27: 597-609.
6. Salio, M., A. O. Speak, D. Shepherd, P. Polzella, P. A. Illarionov, N. Veerapen, G. S. Besra, F. M. Platt, and V. Cerundolo. 2007. Modulation of human natural killer T cell ligands on TLR-mediated antigen-presenting cell activation. Proc. Natl. Acad. Sci. USA 104: 20490-20495.
7. Wei, D. G., H. Lee, S. H. Park, L. Beaudoin, L. Teyton, A. Lehuen, and A. Bendelac. 2005. Expansion and long-range differentiation of the NKT cell lineage in mice expressing CD1d exclusively on cortical thymocytes. J. Exp. Med. 202: 239-248.
8. Schümann, J., P. Pittoni, E. Tonti, H. R. Macdonald, P. Dellabona, and G. Casorati. 2005. Targeted expression of human CD1d in transgenic mice reveals independent roles for thymocytes and thymic APCs in positive and negative selection of Valpha14i NKT cells. J. Immunol. 175: 7303-7310.
9. Brigl, M., and M. B. Brenner. 2004. CD1: antigen presentation and T cell function. Annu. Rev. Immunol. 22: 817-890.
10. Novak, J., L. Beaudoin, S. Park, T. Griseri, L. Teyton, A. Bendelac, and A. Lehuen. 2007. Prevention of type 1 diabetes by invariant NKT cells is independent of peripheral CD1d expression. J. Immunol. 178: 1332-1340.
11. Tonti, E., G. Galli, C. Malzone, S. Abrignani, G. Casorati, and P. Dellabona. 2009. NKT-cell help to B lymphocytes can occur independently of cognate interaction. Blood 113: 370-376.
12. Ohnmacht, C., A. Pullner, S. B. King, I. Drexler, S. Meier, T. Brocker, and D. Voehringer. 2009. Constitutive ablation of dendritic cells breaks self-tolerance of CD4 T cells and results in spontaneous fatal autoimmunity. J. Exp. Med. 206: 549-559.
13. Philpott, K. L., J. L. Viney, G. Kay, S. Rastan, E. M. Gardiner, S. Chae, A. C. Hayday, and M. J. Owen. 1992. Lymphoid development in mice congenitally lacking T cell receptor alpha beta-expressing cells. Science 256: 1448-1452.
14. Bellone, M., M. Ceccon, M. Grioni, E. Jachetti, A. Calcinotto, A. Napolitano, M. Freschi, G. Casorati, and P. Dellabona. 2010. iNKT cells control mouse spontaneous carcinoma independently of tumor-specific cytotoxic T cells. PLoS ONE 5: e8646.
15. Reich, M., T. Liefeld, J. Gould, J. Lerner, P. Tamayo, and J. P. Mesirov. 2006. GenePattern 2.0. Nat. Genet. 38: 500-501.
16. Eden, E., R. Navon, I. Steinfeld, D. Lipson, and Z. Yakhini. 2009. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10: 48.
17. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
18. Schümann, J., R. B. Voyle, B. Y. Wei, and H. R. MacDonald. 2003. Cutting edge: influence of the TCRV beta domain on the avidity of CD1d:alpha-galactosylceramide binding by invariant V alpha 14 NKT cells. J. Immunol. 170: 5815-5819.
19. Rhee, I., and A. Veillette. 2012. Protein tyrosine phosphatases in lymphocyte activation and autoimmunity. Nat. Immunol. 13: 439-447.
20. Lorenz, U. 2009. SHP-1 and SHP-2 in T cells: two phosphatases functioning at many levels. Immunol. Rev. 228: 342-359.
21. Gray-Owen, S. D., and R. S. Blumberg. 2006. CEACAM1: contact-dependent control of immunity. Nat. Rev. Immunol. 6: 433-446.
22. Turnbull, I. R., and M. Colonna. 2007. Activating and inhibitory functions of DAP12. Nat. Rev. Immunol. 7: 155-161.
23. Nimmerjahn, F., and J. V. Ravetch. 2008. Fcgamma receptors as regulators of immune responses. Nat. Rev. Immunol. 8: 34-47.
24. Lanier, L. L. 2008. Up on the tightrope: natural killer cell activation and inhibition. Nat. Immunol. 9: 495-502.
25. Lowin-Kropf, B., B. Kunz, F. Beermann, and W. Held. 2000. Impaired natural killing of MHC class I-deficient targets by NK cells expressing a catalytically inactive form of SHP-1. J. Immunol. 165: 1314-1321.
26. Kozlowski, M., I. Mlinaric-Rascan, G. S. Feng, R. Shen, T. Pawson, and K. A. Siminovitch. 1993. Expression and catalytic activity of the tyrosine phosphatase PTP1C is severely impaired in motheaten and viable motheaten mice. J. Exp. Med. 178: 2157-2163.
27. Johnson, K. G., F. G. LeRoy, L. K. Borysiewicz, and R. J. Matthews. 1999. TCR signaling thresholds regulating T cell development and activation are dependent upon SHP-1. J. Immunol. 162: 3802-3813.
28. Green, M. C., and L. D. Shultz. 1975. Motheaten, an immunodeficient mutant of the mouse. I. Genetics and pathology. J. Hered. 66: 250-258.
29. Bezbradica, J. S., A. K. Stanic, N. Matsuki, H. Bour-Jordan, J. A. Bluestone, J. W. Thomas, D. Unutmaz, L. Van Kaer, and S. Joyce. 2005. Distinct roles of dendritic cells and B cells in Va14Ja18 natural T cell activation in vivo. J. Immunol. 174: 4696-4705.
30. Kitamura, D., J. Roes, R. Kühn, and K. Rajewsky. 1991. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature 350: 423-426.
31. Ngo, V. N., R. J. Cornall, and J. G. Cyster. 2001. Splenic T zone development is B cell dependent. J. Exp. Med. 194: 1649-1660.
32. Jeannet, G., J. D. Coudert, and W. Held. 2006. T and B lymphocytes exert distinct effects on the homeostasis of NK cells. Eur. J. Immunol. 36: 2725-2734.
33. Moran, A. E., K. L. Holzapfel, Y. Xing, N. R. Cunningham, J. S. Maltzman, J. Punt, and K. A. Hogquist. 2011. T cell receptor signal strength in Treg and iNKT cell development demonstrated by a novel fluorescent reporter mouse. J. Exp. Med. 208: 1279-1289.
34. Chun, T., M. J. Page, L. Gapin, J. L. Matsuda, H. Xu, H. Nguyen, H. S. Kang, A. K. Stanic, S. Joyce, W. A. Koltun, et al. 2003. CD1d-expressing dendritic cells but not thymic epithelial cells can mediate negative selection of NKT cells. J. Exp. Med. 197: 907-918.
35. Chang, P. P., P. Barral, J. Fitch, A. Pratama, C. S. Ma, A. Kallies, J. J. Hogan, V. Cerundolo, S. G. Tangye, R. Bittman, et al. 2012. Identification of Bcl-6-dependent follicular helper NKT cells that provide cognate help for B cell responses. Nat. Immunol. 13: 35-43.
36. Tonti, E., M. Fedeli, A. Napolitano, M. Iannacone, U. H. von Andrian, L. G. Guidotti, S. Abrignani, G. Casorati, and P. Dellabona. 2012. Follicular helper NKT cells induce limited B cell responses and germinal center formation in the absence of CD4(+) T cell help. J. Immunol. 188: 3217-3222.
37. King, I. L., A. Fortier, M. Tighe, J. Dibble, G. F. Watts, N. Veerapen, A. M. Haberman, G. S. Besra, M. Mohrs, M. B. Brenner, and E. A. Leadbetter. 2012. Invariant natural killer T cells direct B cell responses to cognate lipid antigen in an IL-21-dependent manner. Nat. Immunol. 13: 44-50.
38. Barral, P., M. D. Sánchez-Niño, N. van Rooijen, V. Cerundolo, and F. D. Batista. 2012. The location of splenic NKT cells favours their rapid activation by bloodborne antigen. EMBO J. 31: 2378-2390.
39. Geissmann, F., T. O. Cameron, S. Sidobre, N. Manlongat, M. Kronenberg, M. J. Briskin, M. L. Dustin, and D. R. Littman. 2005. Intravascular immune surveillance by CXCR6+ NKT cells patrolling liver sinusoids. PLoS Biol. 3: e113.
40. Barral, P., P. Polzella, A. Bruckbauer, N. van Rooijen, G. S. Besra, V. Cerundolo, and F. D. Batista. 2010. CD169(+) macrophages present lipid antigens to mediate early activation of iNKT cells in lymph nodes. Nat. Immunol. 11: 303-312.
41. Bai, L., M. G. Constantinides, S. Y. Thomas, R. Reboulet, F. Meng, F. Koentgen, L. Teyton, P. B. Savage, and A. Bendelac. 2012. Distinct APCs explain the cytokine bias of a-galactosylceramide variants in vivo. J. Immunol. 188: 3053-3061.
42. Lang, G. A., T. S. Devera, and M. L. Lang. 2008. Requirement for CD1d expression by B cells to stimulate NKT cell-enhanced antibody production. Blood 111: 2158-2162.
43. McNab, F. W., S. P. Berzins, D. G. Pellicci, K. Kyparissoudis, K. Field, M. J. Smyth, and D. I. Godfrey. 2005. The influence of CD1d in postselection NKT cell maturation and homeostasis. J. Immunol. 175: 3762-3768.
44. Zimmer, M. I., A. Colmone, K. Felio, H. Xu, A. Ma, and C. R. Wang. 2006. A cell-type specific CD1d expression program modulates invariant NKT cell development and function. J. Immunol. 176: 1421-1430.
45. Facciotti, F., G. S. Ramanjaneyulu, M. Lepore, S. Sansano, M. Cavallari, M. Kistowska, S. Forss-Petter, G. Ni, A. Colone, A. Singhal, et al. 2012. Peroxisome-derived lipids are self antigens that stimulate invariant natural killer T cells in the thymus. Nat. Immunol. 13: 474-480.
46. Wingender, G., D. Stepniak, P. Krebs, L. Lin, S. McBride, B. Wei, J. Braun, S. K. Mazmanian, and M. Kronenberg. 2012. Intestinal microbes affect phenotypes and functions of invariant natural killer T cells in mice. Gastroenterology 143: 418-428.
47. McNab, F. W., D. G. Pellicci, K. Field, G. Besra, M. J. Smyth, D. I. Godfrey, and S. P. Berzins. 2007. Peripheral NK1.1 NKT cells are mature and functionally distinct from their thymic counterparts. J. Immunol. 179: 6630-6637.
48. Gordy, L. E., J. S. Bezbradica, A. I. Flyak, C. T. Spencer, A. Dunkle, J. Sun, A. K. Stanic, M. R. Boothby, Y. W. He, Z. Zhao, et al. 2011. IL-15 regulates homeostasis and terminal maturation of NKT cells. J. Immunol. 187: 6335-6345.
49. Wang, X., K. A. Bishop, S. Hegde, L. A. Rodenkirch, J. W. Pike, and J. E. Gumperz. 2012. Human invariant natural killer T cells acquire transient innate responsiveness via histone H4 acetylation induced by weak TCR stimulation. J. Exp. Med. 209: 987-1000.