Slam haplotypes modulate the response to lipopolysaccharide in vivo through control of NKT cell number and function

Journal of Immunology

Volumn 185, Issue 1, 2010, Pages 144-156

  Aktan, Idil ^a   Chant, Alan ^a   Borg, Zachary D ^a   Damby, David E ^a   Leenstra, Paige C ^a   Lilley, Graham W G ^a   Petty, Joseph ^b   Suratt, Benjamin T ^b   Teuscher, Cory ^a,b   Wakeland, Edward K ^c   Poynter, Matthew E ^b   Boyson, Jonathan E ^a  

^a UNIVERSITY OF VERMONT   (United States)

^b UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR6; COMPLEMENTARY DNA; CYTOKINE; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 4; INTERLEUKIN 6; LIGAND; LIPOPOLYSACCHARIDE; RECOMBINANT GAMMA INTERFERON; RNA; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR; CD150 ANTIGEN; CELL SURFACE RECEPTOR; LEUKOCYTE ANTIGEN;

ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; EX VIVO STUDY; FLOW CYTOMETRY; GENE LOCUS; HAPLOTYPE; IMMUNE RESPONSE; IN VIVO CULTURE; INNATE IMMUNITY; LIVER; MACROPHAGE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SPLEEN CELL; T LYMPHOCYTE SUBPOPULATION; THYMOCYTE; ANIMAL; BONE MARROW CELL; C57BL MOUSE; CELL CULTURE; CONGENIC STRAIN; CYTOLOGY; GENETICS; IMMUNOLOGY; LYMPHOCYTE COUNT; METABOLISM; MOUSE MUTANT; NATURAL KILLER T CELL; NONOBESE DIABETIC MOUSE; PHYSIOLOGY; SPLEEN;

ANIMALS; ANTIGENS, CD; BONE MARROW CELLS; CELLS, CULTURED; HAPLOTYPES; IMMUNITY, INNATE; LIPOPOLYSACCHARIDES; LIVER; LYMPHOCYTE COUNT; MACROPHAGES; MICE; MICE, CONGENIC; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, KNOCKOUT; NATURAL KILLER T-CELLS; RECEPTORS, CELL SURFACE; SPLEEN;

EID: 77956217960     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902658     Document Type: Article

References (69)

1. Kronenberg, M. 2005. Toward an understanding of NKT cell biology: progress and paradoxes. Annu. Rev. Immunol. 23: 877-900.
2. Kawano, T., J. Cui, Y. Koezuka, I. Toura, Y. Kaneko, K. Motoki, H. Ueno, R. Nakagawa, H. Sato, E. Kondo, et al. 1997. CD1d-restricted and TCR-mediated activation of valpha14 NKT cells by glycosylceramides. Science 278: 1626-1629.
3. Bendelac, A. 1995. Positive selection of mouse NK1+ T cells by CD1-expressing cortical thymocytes. J. Exp. Med. 182: 2091-2096.
4. Spada, F. M., Y. Koezuka, and S. A. Porcelli. 1998. CD1d-restricted recognition of synthetic glycolipid antigens by human natural killer T cells. J. Exp. Med. 188: 1529-1534.
5. Yoshimoto, T., and W. E. Paul. 1994. CD4pos, NK1.1pos T cells promptly produce interleukin 4 in response to in vivo challenge with anti-CD3. J. Exp. Med. 179: 1285-1295.
6. Coquet, J. M., S. Chakravarti, K. Kyparissoudis, F. W. McNab, L. A. Pitt, B. S. McKenzie, S. P. Berzins, M. J. Smyth, and D. I. Godfrey. 2008. Diverse cytokine production by NKT cell subsets and identification of an IL-17-producing CD4-NK1.1- NKT cell population. Proc. Natl. Acad. Sci. USA 105: 11287-11292.
7. Michel, M. L., A. C. Keller, C. Paget, M. Fujio, F. Trottein, P. B. Savage, C. H. Wong, E. Schneider, M. Dy, and M. C. Leite-de-Moraes. 2007. Identification of an IL-17-producing NK1.1(neg) iNKT cell population involved in airway neutrophilia. J. Exp. Med. 204: 995-1001.
8. Carnaud, C., D. Lee, O. Donnars, S. H. Park, A. Beavis, Y. Koezuka, and A. Bendelac. 1999. Cutting edge: Cross-talk between cells of the innate immune system: NKT cells rapidly activate NK cells. J. Immunol. 163: 4647-4650.
9. Eberl, G., and H. R. MacDonald. 2000. Selective induction of NK cell proliferation and cytotoxicity by activated NKT cells. Eur. J. Immunol. 30: 985-992.
10. Kitamura, H., K. Iwakabe, T. Yahata, S. Nishimura, A. Ohta, Y. Ohmi, M. Sato, K. Takeda, K. Okumura, L. Van Kaer, et al. 1999. The natural killer T (NKT) cell ligand alpha-galactosylceramide demonstrates its immunopotentiating effect by inducing interleukin (IL)-12 production by dendritic cells and IL-12 receptor expression on NKT cells. J. Exp. Med. 189: 1121-1128.
11. Kitamura, H., A. Ohta, M. Sekimoto, M. Sato, K. Iwakabe, M. Nakui, T. Yahata, H. Meng, T. Koda, S. Nishimura, et al. 2000. alpha-galactosylceramide induces early B-cell activation through IL-4 production by NKT cells. Cell. Immunol. 199: 37-42.
12. Prigozy, T. I., O. Naidenko, P. Qasba, D. Elewaut, L. Brossay, A. Khurana, T. Natori, Y. Koezuka, A. Kulkarni, and M. Kronenberg. 2001. Glycolipid antigen processing for presentation by CD1d molecules. Science 291: 664-667.
13. Mattner, J., K. L. Debord, N. Ismail, R. D. Goff, C. Cantu, III, D. Zhou, P. Saint-Mezard, V. Wang, Y. Gao, N. Yin, et al. 2005. Exogenous and endogenous glycolipid antigens activate NKT cells during microbial infections. Nature 434: 525-529.
14. Sriram, V., W. Du, J. Gervay-Hague, and R. R. Brutkiewicz. 2005. Cell wall glycosphingolipids of Sphingomonas paucimobilis are CD1d-specific ligands for NKT cells. Eur. J. Immunol. 35: 1692-1701.
15. Kinjo, Y., D. Wu, G. Kim, G. W. Xing, M. A. Poles, D. D. Ho, M. Tsuji, K. Kawahara, C. H. Wong, and M. Kronenberg. 2005. Recognition of bacterial glycosphingolipids by natural killer T cells. Nature 434: 520-525.
16. Kinjo, Y., E. Tupin, D. Wu, M. Fujio, R. Garcia-Navarro, M. R. Benhnia, D. M. Zajonc, G. Ben-Menachem, G. D. Ainge, G. F. Painter, et al. 2006. Natural killer T cells recognize diacylglycerol antigens from pathogenic bacteria. Nat. Immunol. 7: 978-986.
17. Brigl, M., L. Bry, S. C. Kent, J. E. Gumperz, and M. B. Brenner. 2003. Mechanism of CD1d-restricted natural killer T cell activation during microbial infection. Nat. Immunol. 4: 1230-1237.
18. Marschner, A., S. Rothenfusser, V. Hornung, D. Prell, A. Krug, M. Kerkmann, D. Wellisch, H. Poeck, A. Greinacher, T. Giese, et al. 2005. CpG ODN enhance antigen-specific NKT cell activation via plasmacytoid dendritic cells. Eur. J. Immunol. 35: 2347-2357.
19. 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.
20. 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.
21. Nagarajan, N. A., and M. Kronenberg. 2007. Invariant NKT cells amplify the innate immune response to lipopolysaccharide. J. Immunol. 178: 2706-2713. (Pubitemid 46335652)
22. Wesley, J. D., M. S. Tessmer, D. Chaukos, and L. Brossay. 2008. NK cell-like behavior of Valpha14i NKT cells during MCMV infection. PLoS Pathog. 4: e1000106.
23. De Santo, C., M. Salio, S. H. Masri, L. Y. Lee, T. Dong, A. O. Speak, S. Porubsky, S. Booth, N. Veerapen, G. S. Besra, et al. 2008. Invariant NKT cells reduce the immunosuppressive activity of influenza A virus-induced myeloid-derived suppressor cells in mice and humans. J. Clin. Invest. 118: 4036-4048.
24. Sada-Ovalle, I., A. Chiba, A. Gonzales, M. B. Brenner, and S. M. Behar. 2008. Innate invariant NKT cells recognize Mycobacterium tuberculosis-infected macrophages, produce interferon-gamma, and kill intracellular bacteria. PLoS Pathog. 4: e1000239.
25. Dieli, F., G. Sireci, D. Russo, M. Taniguchi, J. Ivanyi, C. Fernandez, M. Troye-Blomberg, G. De Leo, and A. Salerno. 2000. Resistance of natural killer T cell-deficient mice to systemic Shwartzman reaction. J. Exp. Med. 192: 1645-1652.
26. Hu, C. K., F. Venet, D. S. Heffernan, Y. L. Wang, B. Horner, X. Huang, C. S. Chung, S. H. Gregory, and A. Ayala. 2009. The role of hepatic invariant NKT cells in systemic/local inflammation and mortality during polymicrobial septic shock. J. Immunol. 182: 2467-2475.
27. Gombert, J. M., A. Herbelin, E. Tancrède-Bohin, M. Dy, C. Carnaud, and J. F. Bach. 1996. Early quantitative and functional deficiency of NK1+-like thymocytes in the NOD mouse. Eur. J. Immunol. 26: 2989-2998.
28. Godfrey, D. I., S. J. Kinder, P. Silvera, and A. G. Baxter. 1997. Flow cytometric study of T cell development in NOD mice reveals a deficiency in alphabetaTCR+CDR-CD8- thymocytes. J. Autoimmun. 10: 279-285.
29. Singh, A. K., J. Q. Yang, V. V. Parekh, J. Wei, C. R. Wang, S. Joyce, R. R. Singh, and L. Van Kaer. 2005. The natural killer T cell ligand alpha-galactosylceramide prevents or promotes pristane-induced lupus in mice. Eur. J. Immunol. 35: 1143-1154.
30. Rymarchyk, S., H. Lowenstein, J. Mayette, S. R. Foster, D. E. Damby, I. W. Howe, I. Aktan, R. E. Meyer, M. E. Poynter, and J. E. Boyson. 2008. Widespread natural variation in murine natural killer T-cell number and function. Immunology 125: 331-343.
31. Hammond, K. J., D. G. Pellicci, L. D. Poulton, O. V. Naidenko, A. A. Scalzo, A. G. Baxter, and D. I. Godfrey. 2001. CD1d-restricted NKT cells: an interstrain comparison. J. Immunol. 167: 1164-1173.
32. Matsuki, N., A. K. Stanic, M. E. Embers, L. Van Kaer, L. Morel, and S. Joyce. 2003. Genetic dissection of V alpha 14J alpha 18 natural T cell number and function in autoimmune-prone mice. J. Immunol. 170: 5429-5437.
33. Jordan, M. A., J. M. Fletcher, D. Pellicci, and A. G. Baxter. 2007. Slamf1, the NKT cell control gene Nkt1. J. Immunol. 178: 1618-1627.
34. Griewank, K., C. Borowski, S. Rietdijk, N. Wang, A. Julien, D. G. Wei, A. A. Mamchak, C. Terhorst, and A. Bendelac. 2007. Homotypic interactions mediated by Slamf1 and Slamf6 receptors control NKT cell lineage development. Immunity 27: 751-762.
35. 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.
36. Wandstrat, A. E., C. Nguyen, N. Limaye, A. Y. Chan, S. Subramanian, X. H. Tian, Y. S. Yim, A. Pertsemlidis, H. R. Garner, Jr., L. Morel, and E. K. Wakeland. 2004. Association of extensive polymorphisms in the SLAM/CD2 gene cluster with murine lupus. Immunity 21: 769-780.
37. Limaye, N., K. A. Belobrajdic, A. E. Wandstrat, F. Bonhomme, S. V. Edwards, and E. K. Wakeland. 2008. Prevalence and evolutionary origins of autoimmune susceptibility alleles in natural mouse populations. Genes Immun. 9: 61-68.
38. Suratt, B. T., J. M. Petty, S. K. Young, K. C. Malcolm, J. G. Lieber, J. A. Nick, J. A. Gonzalo, P. M. Henson, and G. S. Worthen. 2004. Role of the CXCR4/SDF-1 chemokine axis in circulating neutrophil homeostasis. Blood 104: 565-571.
39. Suratt, B. T., S. K. Young, J. Lieber, J. A. Nick, P. M. Henson, and G. S. Worthen. 2001. Neutrophil maturation and activation determine anatomic site of clearance from circulation. Am. J. Physiol. Lung Cell. Mol. Physiol. 281: L913-L921.
40. Grivennikov, S. I., A. V. Tumanov, D. J. Liepinsh, A. A. Kruglov, B. I. Marakusha, A. N. Shakhov, T. Murakami, L. N. Drutskaya, I. Förster, B. E. Clausen, et al. 2005. Distinct and nonredundant in vivo functions of TNF produced by t cells and macrophages/neutrophils: protective and deleterious effects. Immunity 22: 93-104.
41. Sultzer, B. M. 1972. Genetic control of host responses to endotoxin. Infect. Immun. 5: 107-113.
42. Poltorak, A., X. He, I. Smirnova, M. Y. Liu, C. Van Huffel, X. Du, D. Birdwell, E. Alejos, M. Silva, C. Galanos, et al. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282: 2085-2088.
43. Smirnova, I., A. Poltorak, E. K. Chan, C. McBride, and B. Beutler. 2000. Phylogenetic variation and polymorphism at the toll-like receptor 4 locus (TLR4). Genome Biol. 1: RESEARCH002.
44. 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.
45. Monticelli, L. A., Y. Yang, J. Knell, L. M. D'Cruz, M. A. Cannarile, I. Engel, M. Kronenberg, and A. W. Goldrath. 2009. Transcriptional regulator Id2 controls survival of hepatic NKT cells. Proc. Natl. Acad. Sci. USA 106: 19461-19466.
46. Germanov, E., L. Veinotte, R. Cullen, E. Chamberlain, E. C. Butcher, and B. Johnston. 2008. Critical role for the chemokine receptor CXCR6 in homeostasis and activation of CD1d-restricted NKT cells. J. Immunol. 181: 81-91.
47. Rhead, B., D. Karolchik, R. M. Kuhn, A. S. Hinrichs, A. S. Zweig, P. A. Fujita, M. Diekhans, K. E. Smith, K. R. Rosenbloom, B. J. Raney, A. Pohl, M. Pheasant, L. R. Meyer, K. Learned, F. Hsu, J. Hillman-Jackson, R. A. Harte, B. Giardine, T. R. Dreszer, H. Clawson, G. P. Barber, D. Haussler, and W. J. Kent. 2010. The UCSC Genome Browser database: update 2010. Nucleic Acids Res. 38: D613-D619.
48. Peck, S. R., and H. E. Ruley. 2000. Ly108: a new member of the mouse CD2 family of cell surface proteins. Immunogenetics 52: 63-72.
49. Kumar, K. R., L. Li, M. Yan, M. Bhaskarabhatla, A. B. Mobley, C. Nguyen, J. M. Mooney, J. D. Schatzle, E. K. Wakeland, and C. Mohan. 2006. Regulation of B cell tolerance by the lupus susceptibility gene Ly108. Science 312: 1665-1669.
50. Nieuwenhuis, E. E., T. Matsumoto, M. Exley, R. A. Schleipman, J. Glickman, D. T. Bailey, N. Corazza, S. P. Colgan, A. B. Onderdonk, and R. S. Blumberg. 2002. CD1d-dependent macrophage-mediated clearance of Pseudomonas aeruginosa from lung. Nat. Med. 8: 588-593.
51. Olson, C. M., Jr., T. C. Bates, H. Izadi, J. D. Radolf, S. A. Huber, J. E. Boyson, and J. Anguita. 2009. Local production of IFN-gamma by invariant NKT cells modulates acute Lyme carditis. J. Immunol. 182: 3728-3734.
52. Hazlett, L. D., Q. Li, J. Liu, S. McClellan, W. Du, and R. P. Barrett. 2007. NKT cells are critical to initiate an inflammatory response after Pseudomonas aeruginosa ocular infection in susceptible mice. J. Immunol. 179: 1138-1146.
53. Song, L., S. Asgharzadeh, J. Salo, K. Engell, H. W. Wu, R. Sposto, T. Ara, A. M. Silverman, Y. A. DeClerck, R. C. Seeger, and L. S. Metelitsa. 2009. Valpha24-invariant NKT cells mediate antitumor activity via killing of tumor-associated macrophages. J. Clin. Invest. 119: 1524-1536.
54. Kim, E. Y., J. T. Battaile, A. C. Patel, Y. You, E. Agapov, M. H. Grayson, L. A. Benoit, D. E. Byers, Y. Alevy, J. Tucker, et al. 2008. Persistent activation of an innate immune response translates respiratory viral infection into chronic lung disease. Nat. Med. 14: 633-640.
55. Sköld, M., X. Xiong, P. A. Illarionov, G. S. Besra, and S. M. Behar. 2005. Interplay of cytokines and microbial signals in regulation of CD1d expression and NKT cell activation. J. Immunol. 175: 3584-3593.
56. 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. (Pubitemid 40504552)
57. 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.
58. Schmieg, J., G. Yang, R. W. Franck, N. Van Rooijen, and M. Tsuji. 2005. Glycolipid presentation to natural killer T cells differs in an organ-dependent fashion. Proc. Natl. Acad. Sci. USA 102: 1127-1132.
59. Wesley, J. D., S. H. Robbins, S. Sidobre, M. Kronenberg, S. Terrizzi, and L. Brossay. 2005. Cutting edge: IFN-gamma signaling to macrophages is required for optimal Valpha14i NKT/NK cell cross-talk. J. Immunol. 174: 3864-3868.
60. Ogasawara, K., K. Takeda, W. Hashimoto, M. Satoh, R. Okuyama, N. Yanai, M. Obinata, K. Kumagai, H. Takada, H. Hiraide, and S. Seki. 1998. Involvement of NK1+ T cells and their IFN-gamma production in the generalized Shwartzman reaction. J. Immunol. 160: 3522-3527.
61. Beutler, B., I. W. Milsark, and A. C. Cerami. 1985. Passive immunization against cachectin/tumor necrosis factor protects mice from lethal effect of endotoxin. Science 229: 869-871.
62. Esteban, L. M., T. Tsoutsman, M. A. Jordan, D. Roach, L. D. Poulton, A. Brooks, O. V. Naidenko, S. Sidobre, D. I. Godfrey, and A. G. Baxter. 2003. Genetic control of NKT cell numbers maps to major diabetes and lupus loci. J. Immunol. 171: 2873-2878.
63. Poulton, L. D., M. J. Smyth, C. G. Hawke, P. Silveira, D. Shepherd, O. V. Naidenko, D. I. Godfrey, and A. G. Baxter. 2001. Cytometric and functional analyses of NK and NKT cell deficiencies in NOD mice. Int. Immunol. 13: 887-896.
64. Baev, D. V., S. Caielli, F. Ronchi, M. Coccia, F. Facciotti, K. E. Nichols, and M. Falcone. 2008. Impaired SLAM-SLAM homotypic interaction between invariant NKT cells and dendritic cells affects differentiation of IL-4/IL-10-secreting NKT2 cells in nonobese diabetic mice. J. Immunol. 181: 869-877.
65. Wang, N., A. Satoskar, W. Faubion, D. Howie, S. Okamoto, S. Feske, C. Gullo, K. Clarke, M. R. Sosa, A. H. Sharpe, and C. Terhorst. 2004. The cell surface receptor SLAM controls T cell and macrophage functions. J. Exp. Med. 199: 1255-1264.
66. Graham, D. B., M. P. Bell, M. M. McCausland, C. J. Huntoon, J. van Deursen, W. A. Faubion, S. Crotty, and D. J. McKean. 2006. Ly9 (CD229)-deficient mice exhibit T cell defects yet do not share several phenotypic characteristics associated with SLAM- and SAP-deficient mice. J. Immunol. 176: 291-300.
67. Zhong, M. C., and A. Veillette. 2008. Control of T lymphocyte signaling by Ly108, a signaling lymphocytic activation molecule family receptor implicated in autoimmunity. J. Biol. Chem. 283: 19255-19264.
68. Howie, D., F. S. Laroux, M. Morra, A. R. Satoskar, L. E. Rosas, W. A. Faubion, A. Julien, S. Rietdijk, A. J. Coyle, C. Fraser, and C. Terhorst. 2005. Cutting edge: the SLAM family receptor Ly108 controls T cell and neutrophil functions. J. Immunol. 174: 5931-5935. (Pubitemid 40663778)
69. Veillette, A., M. E. Cruz-Munoz, and M. C. Zhong. 2006. SLAM family receptors and SAP-related adaptors: matters arising. Trends Immunol. 27: 228-234.