Dendritic cells support the in vivo development and maintenance of NK cells via IL-15 trans-presentation

Journal of Immunology

Volumn 183, Issue 8, 2009, Pages 4948-4956

  Castillo, Eliseo F ^a   Stonier, Spencer W ^a   Frasca, Loredana ^a,b   Schluns, Kimberly S ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GLYCOPROTEIN P 15095; INTERLEUKIN 15; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY A;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL INTERACTION; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; IMMUNOSTIMULATION; IN VIVO STUDY; MAST CELL DEGRANULATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; UPREGULATION; WILD TYPE;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD11C; CELL DEGRANULATION; DENDRITIC CELLS; INTERFERON-GAMMA; INTERLEUKIN-15; KILLER CELLS, NATURAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY A; RECEPTORS, INTERLEUKIN-15;

EID: 71649083586     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0900719     Document Type: Article

References (53)

1. Kim, S., K. Iizuka, H. L. Aguila, I. L. Weissman, and W. M. Yokoyama. 2000. In vivo natural killer cell activities revealed by natural killer cell-deficient mice. Proc. Natl. Acad. Sci. USA 97: 2731-2736.
2. Ljunggren, H. G., and K. J. Malmberg. 2007. Prospects for the use of NK cells in immunotherapy of human cancer. Nat. Rev. Immunol. 7: 329-339.
3. Lanier, L. L. 2008. Evolutionary struggles between NK cells and viruses. Nat. Rev. Immunol. 8: 259-268.
4. Kim, S., K. Iizuka, H. S. Kang, A. Dokun, A. R. French, S. Greco, and W. M. Yokoyama. 2002. In vivo developmental stages in murine natural killer cell maturation. Nat. Immunol. 3: 523-528. (Pubitemid 34662303)
5. Vosshenrich, C. A., T. Ranson, S. I. Samson, E. Corcuff, F. Colucci, E. E. Rosmaraki, and J. P. Di Santo. 2005. Roles for common cytokine receptor γ-chain-dependent cytokines in the generation, differentiation, and maturation of NK cell precursors and peripheral NK cells in vivo. J. Immunol. 174: 1213-1221.
6. Rosmaraki, E. E., I. Douagi, C. Roth, F. Colucci, A. Cumano, and J. P. Di Santo. 2001. Identification of committed NK cell progenitors in adult murine bone marrow. Eur. J. Immunol. 31: 1900-1909.
7. Huntington, N. D., C. A. Vosshenrich, and J. P. Di Santo. 2007. Developmental pathways that generate natural-killer-cell diversity in mice and humans. Nat. Rev. Immunol. 7: 703-714.
8. Kim, S., J. Poursine-Laurent, S. M. Truscott, L. Lybarger, Y. J. Song, L. Yang, A. R. French, J. B. Sunwoo, S. Lemieux, T. H. Hansen, and W. M. Yokoyama. 2005. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 436: 709-713.
9. Fernandez, N. C., E. Treiner, R. E. Vance, A. M. Jamieson, S. Lemieux, and D. H. Raulet. 2005. A subset of natural killer cells achieves self-tolerance without expressing inhibitory receptors specific for self-MHC molecules. Blood 105: 4416-4423.
10. Haller, O., and H. Wigzell. 1977. Suppression of natural killer cell activity with radioactive strontium: effector cells are marrow dependent. J. Immunol. 118: 1503-1506. (Pubitemid 8095893)
11. Fehniger, T. A., and M. A. Caligiuri. 2001. Interleukin 15: biology and relevance to human disease. Blood 97: 14-32.
12. Lodolce, J. P., D. L. Boone, S. Chai, R. E. Swain, T. Dassopoulos, S. Trettin, and A. Ma. 1998. IL-15 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation. Immunity 9: 669-676.
13. Kennedy, M. K., M. Glaccum, S. N. Brown, E. A. Butz, J. L. Viney, M. Embers, N. Matsuki, K. Charrier, L. Sedger, C. R. Willis, et al. 2000. Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J. Exp. Med. 191: 771-780.
14. Suzuki, H., G. S. Duncan, H. Takimoto, and T. W. Mak. 1997. Abnormal development of intestinal intraepithelial lymphocytes and peripheral natural killer cells in mice lacking the IL-2 receptor β chain. J. Exp. Med. 185: 499-505.
15. DiSanto, J. P., W. Muller, D. Guy-Grand, A. Fischer, and K. Rajewsky. 1995. Lymphoid development in mice with a targeted deletion of the interleukin 2 receptor γ chain. Proc. Natl. Acad. Sci. USA 92: 377-381.
16. Dubois, S., J. Mariner, T. A. Waldmann, and Y. Tagaya. 2002. IL-15Rα recycles and presents IL-15 In trans to neighboring cells. Immunity 17: 537-547.
17. Lodolce, J. P., P. R. Burkett, D. L. Boone, M. Chien, and A. Ma. 2001. T cell-independent interleukin 15Rα signals are required for bystander proliferation. J. Exp. Med. 194: 1187-1194.
18. Prlic, M., B. R. Blazar, M. A. Farrar, and S. C. Jameson. 2003. In vivo survival and homeostatic proliferation of natural killer cells. J. Exp. Med. 197: 967-976.
19. Koka, R., P. R. Burkett, M. Chien, S. Chai, F. Chan, J. P. Lodolce, D. L. Boone, and A. Ma. 2003. Interleukin (IL)-15Rα-deficient natural killer cells survive in normal but not IL-15Rα-deficient mice. J. Exp. Med. 197: 977-984.
20. Kawamura, T., R. Koka, A. Ma, and V. Kumar. 2003. Differential roles for IL-15Rα-chain in NK cell development and Ly-49 induction. J. Immunol. 171: 5085-5090. (Pubitemid 37432790)
21. + T cell homeostasis. J. Exp. Med. 200: 825-834.
22. Schluns, K. S., E. C. Nowak, A. Cabrera-Hernandez, L. Puddington, L. Lefrancois, and H. L. Aguila. 2004. Distinct cell types control lymphoid subset development by means of IL-15 and IL-15 receptor α expression. Proc. Natl. Acad. Sci. USA 101: 5616-5621.
23. Cooper, M. A., J. E. Bush, T. A. Fehniger, J. B. VanDeusen, R. E. Waite, Y. Liu, H. L. Aguila, and M. A. Caligiuri. 2002. In vivo evidence for a dependence on interleukin 15 for survival of natural killer cells. Blood 100: 3633-3638.
24. Minagawa, M., H. Watanabe, C. Miyaji, K. Tomiyama, H. Shimura, A. Ito, M. Ito, J. Domen, I. L. Weissman, and K. Kawai. 2002. Enforced expression of Bcl-2 restores the number of NK cells, but does not rescue the impaired development of NKT cells or intraepithelial lymphocytes, in IL-2/IL-15 receptor β-chain-deficient mice. J. Immunol. 169: 4153-4160.
25. Ranson, T., C. A. Vosshenrich, E. Corcuff, O. Richard, W. Muller, and J. P. Di Santo. 2003. IL-15 is an essential mediator of peripheral NK-cell homeostasis. Blood 101: 4887-4893. (Pubitemid 36857750)
26. Jamieson, A. M., P. Isnard, J. R. Dorfman, M. C. Coles, and D. H. Raulet. 2004. Turnover and proliferation of NK cells in steady state and lymphopenic conditions. J. Immunol. 172: 864-870.
27. Huntington, N. D., H. Puthalakath, P. Gunn, E. Naik, E. M. Michalak, M. J. Smyth, H. Tabarias, M. A. Degli-Esposti, G. Dewson, S. N. Willis, et al. 2007. Interleukin 15-mediated survival of natural killer cells is determined by interactions among Bim, Noxa, and Mcl-1. Nat. Immunol. 8: 856-863.
28. Degli-Esposti, M. A., and M. J. Smyth. 2005. Close encounters of different kinds: dendritic cells and NK cells take centre stage. Nat. Rev. Immunol. 5: 112-124.
29. Cooper, M. A., T. A. Fehniger, A. Fuchs, M. Colonna, and M. A. Caligiuri. 2004. NK cell and DC interactions. Trends Immunol. 25: 47-52.
30. Mortier, E., T. Woo, R. Advincula, S. Gozalo, and A. Ma. 2008. IL-15Rα chaperones IL-15 to stable dendritic cell membrane complexes that activate NK cells via trans presentation. J. Exp. Med. 205: 1213-1225.
31. Stonier, S. W., L. J. Ma, E. F. Castillo, and K. S. Schluns. 2008. Dendritic cells drive memory CD8 T cell homeostasis via IL-15 trans-presentation. Blood 112: 4546-4554.
32. Rubio, V., T. B. Stuge, N. Singh, M. R. Betts, J. S. Weber, M. Roederer, and P. P. Lee. 2003. Ex vivo identification, isolation and analysis of tumor-cytolytic T cells. Nat. Med. 9: 1377-1382.
33. Hayakawa, Y., and M. J. Smyth. 2006. CD27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J. Immunol. 176: 1517-1524. (Pubitemid 43134295)
34. Huntington, N. D., H. Tabarias, K. Fairfax, J. Brady, Y. Hayakawa, M. A. Degli-Esposti, M. J. Smyth, D. M. Tarlinton, and S. L. Nutt. 2007. NK cell maturation and peripheral homeostasis is associated with KLRG1 up-regulation. J. Immunol. 178: 4764-4770.
35. Vivier, E., E. Tomasello, M. Baratin, T. Walzer, and S. Ugolini. 2008. Functions of natural killer cells. Nat. Immunol. 9: 503-510.
36. Lucas, M., W. Schachterle, K. Oberle, P. Aichele, and A. Diefenbach. 2007. Dendritic cells prime natural killer cells by trans-presenting interleukin 15. Immunity 26: 503-517.
37. Hochweller, K., J. Striegler, G. J. Hammerling, and N. Garbi. 2008. A novel CD11c.DTR transgenic mouse for depletion of dendritic cells reveals their requirement for homeostatic proliferation of natural killer cells. Eur. J. Immunol. 38: 2776-2783.
38. Andrews, D. M., A. A. Scalzo, W. M. Yokoyama, M. J. Smyth, and M. A. Degli-Esposti. 2003. Functional interactions between dendritic cells and NK cells during viral infection. Nat. Immunol. 4: 175-181.
39. Koka, R., P. Burkett, M. Chien, S. Chai, D. L. Boone, and A. Ma. 2004. Cutting edge: murine dendritic cells require IL-15Rα to prime NK cells. J. Immunol. 173: 3594-3598.
40. Ogasawara, K., S. Hida, N. Azimi, Y. Tagaya, T. Sato, T. Yokochi-Fukuda, T. A. Waldmann, T. Taniguchi, and S. Taki. 1998. Requirement for IRF-1 in the microenvironment supporting development of natural killer cells. Nature 391: 700-703.
41. Iizuka, K., D. D. Chaplin, Y. Wang, Q. Wu, L. E. Pegg, W. M. Yokoyama, and Y. X. Fu. 1999. Requirement for membrane lymphotoxin in natural killer cell development. Proc. Natl. Acad. Sci. USA 96: 6336-6340.
42. Wu, Q., Y. Sun, J. Wang, X. Lin, Y. Wang, L. E. Pegg, A. Futterer, K. Pfeffer, and Y. X. Fu. 2001. Signal via lymphotoxin-βR on bone marrow stromal cells is required for an early checkpoint of NK cell development. J. Immunol. 166: 1684-1689.
43. Roth, C., C. Rothlin, S. Riou, D. H. Raulet, and G. Lemke. 2007. Stromal-cell regulation of natural killer cell differentiation. J. Mol. Med. 85: 1047-1056.
44. Ogawa, M., A. C. Larue, and C. J. Drake. 2006. Hematopoietic origin of fibroblasts/myofibroblasts: its pathophysiologic implications. Blood 108: 2893-2896.
45. Nagasawa, T. 2006. Microenvironmental niches in the bone marrow required for B cell development. Nat. Rev. Immunol. 6: 107-116.
46. Neely, G. G., S. M. Robbins, E. K. Amankwah, S. Epelman, H. Wong, J. C. Spurrell, K. K. Jandu, W. Zhu, D. K. Fogg, C. B. Brown, and C. H. Mody. 2001. Lipopolysaccharide-stimulated or granulocyte-macrophage colony-stimulating factor-stimulated monocytes rapidly express biologically active IL-15 on their cell surface independent of new protein synthesis. J. Immunol. 167: 5011-5017.
47. + T cells in vivo by IL-15. Immunity 8: 591-599.
48. Naik, S. H., P. Sathe, H. Y. Park, D. Metcalf, A. I. Proietto, A. Dakic, S. Carotta, M. O'Keeffe, M. Bahlo, A. Papenfuss, et al. 2007. Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat. Immunol. 8: 1217-1226.
49. - cells from multipotential murine bone marrow progenitors in a stroma-free culture: definition of cytokine requirements and developmental intermediates. J. Exp. Med. 186: 1609-1614.
50. + multipotent marrow progenitor cells. J. Immunol. 163: 2648-2656.
51. Roth, C., J. R. Carlyle, H. Takizawa, and D. H. Raulet. 2000. Clonal acquisition of inhibitory Ly49 receptors on developing NK cells is successively restricted and regulated by stromal class I MHC. Immunity 13: 143-153.
52. Huntington, N. D., N. Legrand, N. L. Alves, B. Jaron, K. Weijer, A. Plet, E. Corcuff, E. Mortier, Y. Jacques, H. Spits, and J. P. Di Santo. 2009. IL-15 trans-presentation promotes human NK cell development and differentiation in vivo. J. Exp. Med. 206: 25-34.
53. Tourkova, I. L., G. V. Shurin, G. S. Chatta, L. Perez, J. Finke, T. L. Whiteside, S. Ferrone, and M. R. Shurin. 2005. Restoration by IL-15 of MHC class I antigen-processing machinery in human dendritic cells inhibited by tumor-derived gangliosides. J. Immunol. 175: 3045-3052.