Critical role for the chemokine receptor CXCR6 in homeostasis and activation of CD1d-restricted NKT cells

Journal of Immunology

Volumn 181, Issue 1, 2008, Pages 81-91

  Germanov, Elitza ^a   Veinotte, Linnea ^a   Cullen, Robyn ^a   Chamberlain, Erin ^a   Butcher, Eugene C ^b,c   Johnston, Brent ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VA PALO ALTO HEALTH CARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD1D ANTIGEN; CHEMOKINE RECEPTOR CXCR6; CXCL16 CHEMOKINE; GAMMA INTERFERON; INTERLEUKIN 4; CD1 ANTIGEN; CHEMOKINE RECEPTOR CXCR; CXCR6 PROTEIN, MOUSE; CYTOKINE;

ANIMAL CELL; ARTICLE; BONE MARROW; CELL ACTIVATION; CELL FUNCTION; CELL MATURATION; CELL STIMULATION; CELL SURVIVAL; CYTOKINE PRODUCTION; HOMEOSTASIS; IMMUNE RESPONSE; LIVER; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR UPREGULATION; SPLEEN; THYMUS; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; CELL MOTION; CYTOLOGY; FEMALE; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MALE; METABOLISM; MOUSE MUTANT; REGULATORY T LYMPHOCYTE; UPREGULATION;

ANIMALS; ANTIGENS, CD1; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; CYTOKINES; FEMALE; HOMEOSTASIS; LIVER; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, CXCR; T-LYMPHOCYTES, REGULATORY; THYMUS GLAND; UP-REGULATION;

EID: 47949107462     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.1.81     Document Type: Article

References (62)

1. Godfrey, D. I., H. R. MacDonald, M. Kronenberg, M. J. Smyth, and K. L. Van. 2004. NKT cells: what's in a name? Nat. Rev. Immunol. 4: 231-237.
2. Godfrey, D. I., K. J. Hammond, L. D. Poulton, M. J. Smyth, and A. G. Baxter. 2000. NKT cells: facts, functions and fallacies. Immunol. Today 21: 573-583.
3. - T cells in mice and humans. J. Exp. Med. 180: 1097-1106.
4. - T cells. J. Exp. Med. 180: 1171-1176.
5. Benlagha, K., A. Weiss, A. Beavis, L. Teyton, and A. Bendelac. 2000. In vivo identification of glycoliptd antigen-specific T cells using fluorescent CDld tetramers. J. Exp. Med. 191: 1895-1903.
6. Matsuda, J. L., O. V. Naidenko, L. Gapin, T. Nakayama, M. Taniguchi, C. R. Wang, Y. Koezuka, and M. Kronenberg. 2000. Tracking the response of natural killer T cells to a glycolipid antigen using CDld tetramers. J. Exp. Med. 192: 741-754.
7. Kronenberg, M. 2005. Toward an understanding of NKT cell biology: progress and paradoxes. Annu. Rev. Immunol. 23: 877-900.
8. + T cells. Eur. J. Immunol. 27: 1576-1579.
9. Gapin, L., J. L. Matsuda, C. D. Surh, and M. Kronenberg. 2001. NKT cells derive from double-positive thymocytes that are positively selected by CD1d. Nat. Immunol. 2: 971-978.
10. Dao, T., D. Guo, A. Ploss, A. Stolzer, C. Saylor, T. E. Boursalian, J. S. Im, and D. B. Sant'Angelo. 2004. Development of CD1d-restricted NKT cells in the mouse thymus. Eur. J. Immunol. 34: 3542-3552.
11. Benlagha, K., D. G. Wei, J. Veiga, L. Teyton, and A. Bendelac. 2005. Characterization of the early stages of thymic NKT cell development. J. Exp. Med. 202: 485-492.
12. + cells. J. Immunol. 164: 2412-2418.
13. 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 CDld exclusively on cortical thymocytes. J. Exp. Med. 202: 239-248.
14. Benlagha, K., T. Kyin, A. Beavis, L. Teyton, and A. Bendelac. 2002. A thymic precursor to the NK T cell lineage. Science 296: 553-555.
15. + CD1d-dependent precursor stage. J. Exp. Med. 195: 835-844.
16. + NKT cells in the thymus. J. Immunol. 176: 4059-4065.
17. Matsuda, J. L., L. Gapin, J. L. Baron, S. Sidobre, D. B. Stetson, M. Mohrs, R. M. Locksley, and M. Kronenberg. 2003. Mouse Vα14i natural killer T cells are resistant to cytokine polarization in vivo. Proc. Natl. Acad. Sci. USA 100: 8395-8400.
18. Crowe, N. Y., A. P. Uldrich, K. Kyparissoudis, K. J. Hammond, Y. Hayakawa, S. Sidobre, R. Keating, M. Kronenberg, M. J. Smyth, and D. I. Godfrey. 2003. Glycolipid antigen drives rapid expansion and sustained cytokine production by NK T cells. J. Immunol. 171: 4020-4027.
19. Fujii, S., K. Shimizu, M. Kronenberg, and R. M. Steinman. 2002. Prolonged IFNγ-producing NKT response induced with α-galactosylceramide- loaded DCs. Nat. Immunol. 3: 867-874.
20. Seino, K., S. Motohashi, T. Fujisawa, T. Nakayama, and M. Taniguchi. 2006. Natural killer T cell-mediated antitumor immune responses and their clinical applications. Cancer Sci. 97: 807-812.
21. Tupin, E., Y. Kinjo, and M. Kronenberg. 2007. The unique role of natural killer T cells in the response to microorganisms. Nat. Rev. Microbiol. 5: 405-417.
22. Van Kaer, L. 2005. a-Galactosylceramide therapy for autoimmune diseases: prospects and obstacles. Nat. Rev. Immunol. 5: 31-42.
23. Nowak, M., and J. Stein-Streilein. 2007. Invariant NKT cells and tolerance. Int. Rev. Immunol. 26: 95-119.
24. Kawano, T., J. Cui, Y. Koezuka, I. Toura, Y. Kaneko, H. Sato, E. Kondo, M. Harada, H. Koseki, T. Nakayama, et al. 1998. Natural killer-like nonspecific tumor cell lysis mediated by specific Iigand-activated Vαl4 NKT cells. Proc. Natl. Acad. Sci. USA 95: 5690-5693.
25. Toura, I., T. Kawano, Y. Akutsu, T. Nakayama, T. Ochiai, and M. Taniguchi. 1999. Cutting edge: inhibition of experimental tumor metastasis by dendritic cells pulsed with α-galactosylceramide. J. Immunol. 163: 2387-2391.
26. Hayakawa, Y., S. Rovero, G. Forni, and M. J. Smyth. 2003. α-Galactosylceramide (KRN7000) suppression of chemical- and oncogene-dependent carcinogenesis. Proc. Natl. Acad. Sci. USA 100: 9464-9469.
27. Sharif, S., G. A. Arreaza, P. Zucker, Q. S. Mi, J. Sondhi, O. V. Naidenko. M. Kronenberg, Y. Koezuka, T. L. Delovitch, J. M. Gombert, et al. 2001. Activation of natural killer T cells by α-galactosylceramide treatment prevents the onset and recurrence of autoimmune type 1 diabetes. Nat. Med. 7: 1057-1062.
28. Jahng, A. W., I. Maricic, B. Pedersen, N. Burdin, O. Naidenko, M. Kronenberg, Y. Koezuka, and V. Kumar. 2001. Activation of natural killer T cells potentiates or prevents experimental autoimmune encephalomyelitis. J. Exp. Med. 194: 1789-1799.
29. Saubermann, L. J., P. Beck, Y. P. De Jong, R. S. Pitman, M. S. Ryan, H. S. Kim, M. Exley, S. Snapper, S. P. Balk, S. J. Hagen, et al. 2000. Activation of natural killer T cells by α-galactosylceramide in the presence of CD1d provides protection against colitis in mice. Gastroenterology 119: 119-128.
30. Chiba, A., S. Oki, K. Miyamoto, H. Hashimoto, T. Yamamura, and S. Miyake. 2004. Suppression of collagen-induced arthritis by natural killer T cell activation with OCH, a sphingosine-truncated analog of α- galactosylceramide. Arthritis Rheum. 50: 305-313.
31. 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.
32. Fujii, S., K. Shimizu, H. Hemmi, M. Fukui, A. J. Bonito, G. Chen, R. W. Franck, M. Tsuji, and R. M. Steinman. 2006. Glycolipid α-C- galactosylceramide is a distinct inducer of dendritic cell function during innate and adaptive immune responses of mice. Proc. Natl. Acad. Sci. USA 103: 11252-11257.
33. Hayakawa, Y., K. Takeda, H. Yagita, L. Van Kaer, I. Saiki, and K. Okumura. 2001. Differential regulation of Th1 and Th2 functions of NKT cells by CD28 and CD40 costimulatory pathways. J. Immunol. 166: 6012-6018.
34. 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 α-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.
35. Matsumoto, G., E. Kubota, Y. Omi, U. Lee, and J. M. Penninger. 2004. Essential role of LFA-1 in activating Th2-like responses by a- galactosylceramide-activated NKT cells. J. Immunol. 173: 4976-4984.
36. Ikarashi, Y., R. Mikami, A. Bendelac, M. Terme, N. Chaput, M. Terada, T. Tursz, E. Angevin, F. A. Lemonnier, H. Wakasugi, and L. Zitvogel. 2001. Dendritic cell maturation overrules H-2D-mediated natural killer T (NKT) cell inhibition: critical role for B7 in CD1d-dependent NKT cell interferon γ production. J. Exp. Med. 194: 1179-1186.
37. Johnston, B., and E. C. Butcher. 2002. Chemokines in rapid leukocyte adhesion triggering and migration. Semin. Immunol. 14: 83-92.
38. Ebert, L. M., P. Schaerli, and B. Moser. 2005. Chemokine-mediated control of T cell traffic in lymphoid and peripheral tissues. Mol. Immunol. 42: 799-809.
39. Campbell, D. J., C. H. Kim, and E. C. Butcher. 2003. Chemokines in the systemic organization of immunity. Immunol. Rev. 195: 58-71.
40. Viola, A., R. L. Contento, and B. Molon. 2006. T cells and their partners: the chemokine dating agency. Trends Immunol. 27: 421-427.
41. + NKT cell subsets with distinct cytokine-producing capacity. Blood 100: 11-16.
42. Thomas, S. Y., R. Hou, J. E. Boyson, T. K. Means, C. Hess, D. P. Olson, J. L. Strominger, M. B. Brenner, J. E. Gumpcrz, S. B. Wilson, and A. D. Luster. 2003. CD1d-restricted NKT cells express a chemokine receptor profile indicative of Th1-type inflammatory homing cells. J. Immunol. 171: 2571-2580.
43. Johnston, B., C. H. Kim, D. Soler, M. Emoto, and E. C. Butcher. 2003. Differential chemokine responses and homing patterns of murine TCRαβ NKT cell subsets. J. Immunol. 171: 2960-2969.
44. Matloubian, M., A. David, S. Engel, J. E. Ryan, and J. G. Cyster. 2000. A transmembrane CXC chemokine is a ligand for HIV-coreceptor Bonzo. Nat. Immunol. 1: 298-304.
45. + NKT cells patrolling liver sinusoids. PLoS Biol 3: e113.
46. Jiang, X., T. Shimaoka, S. Kojo, M. Harada, H. Watarai, H. Wakao, N. Ohkohchi, S. Yonehara, M. Taniguchi, and K. Seino. 2005. Cutting edge: critical role of CXCLI6/CXCR6 in NKT cell trafficking in allograft tolerance. J. Immunol. 175: 2051-2055.
47. Kim, C. H., E. J. Kunkel, J. Boisvert, B. Johnston, J. J. Campbell, M. C. Genovese, H. B. Greenbcrg, and E. C. Butcher. 2001. Bonzo/CXCR6 expression defines type 1-polarized T-cell subsets with extralymphoid tissue homing potential. J. Clin. Invest. 107: 595-601.
48. + lymphocytes to inflamed liver. J. Immunol. 174: 277-283.
49. Fukumoto, N., T. Shimaoka, H. Fujimura, S. Sakoda, M. Tanaka, T. Kita, and S. Yonehara. 2004. Critical roles of CXC chemokine ligand 16/scavenger receptor that binds phosphatidylserine and oxidized lipoprotein in the pathogenesis of both acute and adoptive transfer experimental autoimmune encephalomyelitis. J. Immunol. 173: 1620-1627.
50. Agostini, C, A. Cabrelle, F. Calabrese, M. Bortoli, E. Scquizzato, S. Carraro, M. Miorin, B. Beghe, L. Trentin, R. Zambello, et al. 2005. Role for CXCR6 and its ligand CXCLI6 in the pathogenesis of T-cell alveolilis in sarcoidosis. Am. J. Respir. Crit. Care Med. 172: 1290-1298.
51. Nanki, T., T. Shimaoka, K. Hayashida, K. Taniguchi, S. Yonehara, and N. Miyasaka. 2005. Pathogenic role of the CXCL16-CXCR6 pathway in rheumatoid arthritis. Arthritis Rheum. 52: 3004-3014.
52. Unutmaz, D., W. Xiang, M. J. Sunshine, J. Campbell, E. Butcher, and D. R. Littman. 2000. The primate lentiviral receptor Bonzo/STRL33 is coordinately regulated with CCR5 and its expression pattern is conserved between human and mouse. J. Immunol. 165: 3284-3292.
53. Wiibanks, A., S. C. Zondlo, K. Murphy, S. Mak, D. Soler, P. Langdon, D. P. Andrew, L. Wu, and M. Briskin. 2001. Expression cloning of the STRL33/BONZO/TYMSTR ligand reveals elements of CC, CXC, and CX3C chemokines. J. Immunol. 166:5145-5154.
54. Lazarus, N. H., E. J. Kunkel, B. Johnston, E. Wilson, K. R. Youngman, and E. C. Butcher. 2003. A common mucosal chemokine (mucosae-associated epithelial chemokine/CCL28) selectively attracts IgA plasmablasts. J. Immunol. 170: 3799-3805.
55. Campbell, J. J., E. P. Bowman, K. Murphy, K. R. Youngman, M. A. Siani, D. A. Thompson, L. Wu, A. Zlotnik, and E. C. Butcher. 1998. 6-C-kine (SLC), a lymphocyte adhesion-triggering chemokine expressed by high endothelium, is an agonist for the MIP-3β receptor CCR7. J. Cell Biol. 141: 1053-1059.
56. 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.
57. Stetson, D. B., M. Mohrs, R. L. Reinhardt, J. L. Baron, Z. E. Wang, L. Gapin, M. Kronenberg, and R. M. Locksley. 2003. Constitutive cytokine mRNAs mark natural killer (NK) and NK T cells poised for rapid effector function. J. Exp. Med. 198: 1069-1076.
58. Meyer, E. H., M. A. Wurbel, T. L. Staton, M. Pichavant, M. J. Kan, P. B. Savage, R. H. DeKruyff, E. C. Butcher, J. J. Campbell, and D. T. Umetsu. 2007. iNKT cells require CCR4 to localize to the airways and to induce airway hyperreactivity. J. Immunol. 179: 4661-4671.
59. Shimaoka, T., K. Seino, N. Kume, M. Minami, C. Nishime, M. Suematsu, T. Kita, M. Taniguchi, K. Matsushima, and S. Yonehara. 2007. Critical role for CXC chemokine ligand 16 (SR-PSOX) in Th1 response mediated by NKT cells. J. Immunol. 179: 8172-8179.
60. Crowe, N. Y., J. M. Coquet, S. P. Berzins, K. Kyparissoudis, R. Keating, D. G. Pellicci, Y. Hayakawa, D. I. Godfrey, and M. J. Smyth. 2005. Differential antitumor immunity mediated by NKT cell subsets in vivo. J. Exp. Med. 202: 1279-1288.
61. Trobonjaca, Z., F. Leithauser, P. Moller, R. Schirmbeck, and J. Reimann. 2001. Activating immunity in the liver. I. Liver dendritic cells (but not hepatocytes) are potent activators of IFN-γrelease by liver NKT cells. J. Immunol. 167: 1413-1422.
62. Friedman, R. S., J. Jacobelli, and M. F. Krummel. 2006. Surface-bound chemokines capture and prime T cells for synapse formation. Nat. Immunol. 7: 1101-1108.