Mature resting Ly6Chigh natural killer cells can be reactivated by IL-15

European Journal of Immunology

Volumn 44, Issue 9, 2014, Pages 2638-2647

  Omi, Ai ^a   Enomoto, Yutaka ^a   Kiniwa, Tsuyoshi ^a   Miyata, Naoko ^a   Miyajima, Atsushi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Innate immunity; Interleukin; Memory; NK cell; Viral infection

Indexed keywords

CYTOKINE; GAMMA INTERFERON; GRANZYME; GZMB PROTEIN, MOUSE; INTERFERON INDUCING AGENT; INTERLEUKIN 15; LY 6C ANTIGEN, MOUSE; LY ANTIGEN; LY-6C ANTIGEN, MOUSE; POLYINOSINIC POLYCYTIDYLIC ACID;

ANIMAL; ARTICLE; CELL PROLIFERATION; IMMUNOLOGY; INNATE IMMUNITY; MEMORY; MOUSE; NATURAL KILLER CELL; NK CELL; VIRUS INFECTION;

INNATE IMMUNITY; INTERLEUKIN; MEMORY; NK CELL; VIRAL INFECTION;

ANIMALS; ANTIGENS, LY; CELL PROLIFERATION; GRANZYMES; INTERFERON INDUCERS; INTERFERON-GAMMA; INTERLEUKIN-15; KILLER CELLS, NATURAL; MICE; POLY I-C;

EID: 84907855803     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201444570     Document Type: Article

References (50)

1. Vivier, E., Tomasello, E., Baratin, M., Walzer, T. and Ugolini, S., Functions of natural killer cells. Nat. Immunol. 2008. 9: 503-510.
2. Sun, J. C. and Lanier, L. L., NK cell development, homeostasis and function: parallels with CD8(+) T cells. Nat. Rev. Immunol. 2011. 11: 645-657.
3. Cerwenka, A. and Lanier, L. L., Natural killer cells, viruses and cancer. Nat. Rev. Immunol. 2001. 1: 41-49.
4. Yokoyama, W. M. and Plougastel, B. F., Immune functions encoded by the natural killer gene complex. Nat. Rev. Immunol. 2003. 3: 304-316.
5. Spits, H., Artis, D., Colonna, M., Diefenbach, A., Di Santo, J. P., Eberl, G., Koyasu, S. et al., Innate lymphoid cells-a proposal for uniform nomenclature. Nat. Rev. Immunol. 2013. 13: 145-149.
6. Kim, S., Iizuka, K., Kang, H. S., Dokun, A., French, A. R., Greco, S. and Yokoyama, W. M., In vivo developmental stages in murine natural killer cell maturation. Nat. Immunol. 2002. 3: 523-528.
7. Strowig, T., Brilot, F. and Munz, C., Noncytotoxic functions of NK cells: direct pathogen restriction and assistance to adaptive immunity. J. Immunol. 2008. 180: 7785-7791.
8. Herberman, R. B., Nunn, M. E. and Lavrin, D. H., Natural cytotoxic reactivity ofmouse lymphoid cells against syngeneic acid allogeneic tumors. I. Distribution of reactivity and specificity. Int. J. Cancer. 1975. 16: 216-229.
9. Kiessling, R., Klein, E. andWigzell, H., "Natural" killer cells in the mouse. I. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Specificity and distribution according to genotype. Eur. J. Immunol. 1975. 5: 112-117.
10. Lanier, L. L., Le, A. M., Phillips, J. H., Warner, N. L. and Babcock, G. F., Subpopulations of human natural killer cells defined by expression of the Leu-7 (HNK-1) and Leu-11 (NK-15) antigens. J. Immunol. 1983. 131: 1789-1796.
11. dim natural killer cell subsets. J. Immunol. 1998. 161: 400-408.
12. dim NK cells. Eur. J. Immunol. 2001. 31: 3121-3127.
13. Cooper, M. A., Fehniger, T. A., Turner, S. C., Chen, K. S., Ghaheri, B. A., Ghayur, T., Carson, W. E., et al., Human natural killer cells: a unique innate immunoregulatory role for the CD56(bright) subset. Blood 2001. 97: 3146-3151.
14. Hayakawa, Y. and Smyth, M. J., CD27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J. Immunol. 2006. 176: 1517-1524.
15. Huntington, N. D., Tabarias, H., Fairfax, K., Brady, J., Hayakawa, Y., Degli-Esposti, M. A., Smyth, M. J. et al., NK cell maturation and peripheral homeostasis is associated with KLRG1 up-regulation. J. Immunol. 2007. 178: 4764-4770.
16. Yu, J., Wei, M., Mao, H., Zhang, J., Hughes, T., Mitsui, T., Park, I. K. et al., CD94 defines phenotypically and functionally distinct mouseNK cell subsets. J. Immunol. 2009. 183: 4968-4974.
17. Bamezai, A., Mouse Ly-6 proteins and their extended family: markers of cell differentiation and regulators of cell signaling. Arch. Immunol. Ther. Exp. (Warsz) 2004. 52: 255-266.
18. Jutila, M. A., Kroese, F. G., Jutila, K. L., Stall, A. M., Fiering, S., Herzenberg, L. A., Berg, E. L., et al., Ly-6C is a monocyte/macrophage and endothelial cell differentiation antigen regulated by interferon-gamma. Eur. J. Immunol. 1988. 18: 1819-1826.
19. Jutila, D. B., Kurk, S. and Jutila, M. A., Differences in the expression of Ly-6C on neutrophils and monocytes following PI-PLC hydrolysis and cellular activation. Immunol. Lett. 1994. 41: 49-57.
20. Hanninen, A., Maksimow, M., Alam, C., Morgan, D. J. and Jalkanen, S., Ly6C supports preferential homing of central memory CD8+ T cells into lymph nodes. Eur. J. Immunol. 2011. 41: 634-644.
21. + T cells. J. Immunol. 1995. 155: 1873- 1883.
22. Bezman, N. A., Kim, C. C., Sun, J. C., Min-Oo, G., Hendricks, D. W., Kamimura, Y., Best, J. A. et al., Molecular definition of the identity and activation of natural killer cells. Nat. Immunol. 2012. 13: 1000-1009.
23. Sato, N., Yahata, T., Santa, K., Ohta, A., Ohmi, Y., Habu, S. and Nishimura, T., Functional characterization of NK1.1+Ly-6C+ cells. Immunol. Lett. 1996. 54: 5-9.
24. Chiossone, L., Chaix, J., Fuseri, N., Roth, C., Vivier, E. and Walzer, T., Maturation of mouse NK cells is a 4-stage developmental program. Blood 2009. 113: 5488-5496.
25. Moretta, A., Poggi, A., Pende, D., Tripodi, G., Orengo, A. M., Pella, N., Augugliaro, R. et al., CD69-mediated pathway of lymphocyte activation: anti-CD69 monoclonal antibodies trigger the cytolytic activity of different lymphoid effector cells with the exception of cytolytic T lymphocytes expressing T cell receptor alpha/beta. J. Exp. Med. 1991. 174: 1393-1398.
26. Falco, M., Marcenaro, E., Romeo, E., Bellora, F., Marras, D., Vely, F., Ferracci, G. et al., Homophilic interaction of NTBA, a member of the CD2 molecular family: induction of cytotoxicity and cytokine release in human NK cells. Eur. J. Immunol. 2004. 34: 1663-1672.
27. Flaig, R.M., Stark, S. andWatzl, C., Cutting edge: NTB-A activatesNKcells via homophilic interaction. J. Immunol. 2004. 172: 6524-6527.
28. Nieto, M., Rodriguez-Fernandez, J. L., Navarro, F., Sancho, D., Frade, J. M., Mellado, M., Martinez, A. C. et al., Signaling through CD43 induces natural killer cell activation, chemokine release, and PYK-2 activation. Blood 1999. 94: 2767-2777.
29. Andrews, D. M., Scalzo, A. A., Yokoyama, W. M., Smyth, M. J. and Degli-Esposti, M. A., Functional interactions between dendritic cells and NK cells during viral infection. Nat. Immunol. 2003. 4: 175-181.
30. Kuribayashi, K., Gillis, S., Kern, D. E. and Henney, C. S., Murine NK cell cultures: effects of interleukin-2 and interferon on cell growth and cytotoxic reactivity. J. Immunol. 1981. 126: 2321-2327.
31. Meazza, R., Azzarone, B., Orengo, A. M. and Ferrini, S., Role of commongamma chain cytokines in NK cell development and function: perspectives for immunotherapy. J. Biomed. Biotechnol. 2011. 2011: 861920.
32. Russell, J. H. and Ley, T. J., Lymphocyte-mediated cytotoxicity. Annu. Rev. Immunol. 2002. 20: 323-370.
33. Andrade, F., Roy, S., Nicholson, D., Thornberry, N., Rosen, A. and Casciola-Rosen, L., Granzyme B directly and efficiently cleaves several downstream caspase substrates: implications for CTL-induced apoptosis. Immunity 1998. 8: 451-460.
34. Alter, G., Malenfant, J. M. and Altfeld, M., CD107a as a functional marker for the identification of natural killer cell activity. J. Immunol. Methods 2004. 294: 15-22.
35. Ogasawara, K., Hida, S., Azimi, N., Tagaya, Y., Sato, T., Yokochi-Fukuda, T., Waldmann, T. A. et al., Requirement for IRF-1 in the microenvironment supporting development of natural killer cells. Nature 1998. 391: 700-703.
36. Kennedy, M. K., Glaccum, M., Brown, S. N., Butz, E. A., Viney, J. L., Embers, M., Matsuki, N. et al., Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J. Exp. Med. 2000. 191: 771-780.
37. Zhang, G., Budker, V. and Wolff, J. A., High levels of foreign gene expression in hepatocytes after tail vein injections of naked plasmid DNA. Hum. Gene Ther. 1999. 10: 1735-1737.
38. Zhang, G., Gao, X., Song, Y. K., Vollmer, R., Stolz, D. B., Gasiorowski, J. Z., Dean, D. A., et al., Hydroporation as the mechanism of hydrodynamic delivery. Gene Ther. 2004. 11: 675-682.
39. Inagaki, F. F., Tanaka,M., Inagaki, N. F., Yagai, T., Sato, Y., Sekiguchi, K., Oyaizu, N. et al., Nephronectin is upregulated in acute and chronic hepatitis and aggravates liver injury by recruiting CD4 positive cells. Biochem. Biophys. Res. Commun. 2013. 430: 751-756.
40. Lucas, M., Schachterle, W., Oberle, K., Aichele, P. and Diefenbach, A., Dendritic cells prime natural killer cells by trans-presenting interleukin 15. Immunity 2007. 26: 503-517.
41. Eidenschenk, C., Crozat, K., Krebs, P., Arens, R., Popkin, D.,Arnold, C. N., Blasius, A. L. et al., Flt3 permits survival during infection by rendering dendritic cells competent to activate NK cells. Proc. Natl. Acad. Sci. USA 2010. 107: 9759-9764.
42. Stonier, S. W. and Schluns, K. S., Trans-presentation: a novelmechanism regulating IL-15 delivery and responses. Immunol. Lett. 2010. 127: 85-92.
43. Napolitani, G., Rinaldi, A., Bertoni, F., Sallusto, F. and Lanzavecchia, A., Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nat. Immunol. 2005. 6: 769-776.
44. Zhu, Q., Egelston, C., Vivekanandhan, A., Uematsu, S., Akira, S., Klinman, D. M., Belyakov, I. M. et al., Toll-like receptor ligands synergize through distinct dendritic cell pathways to induce T cell responses: implications for vaccines. Proc. Natl. Acad. Sci. USA 2008. 105: 16260-16265.
45. Caligiuri, M. A., Human natural killer cells. Blood 2008. 112: 461-469.
46. Kaech, S. M., Tan, J. T., Wherry, E. J., Konieczny, B. T., Surh, C. D. and Ahmed, R., Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 2003. 4: 1191-1198.
47. Wherry, E. J. and Ahmed, R., Memory CD8 T-cell differentiation during viral infection. J. Virol. 2004. 78: 5535-5545.
48. O'Leary, J. G., Goodarzi, M., Drayton, D. L. and von Andrian, U. H., T celland B cell-independent adaptive immunity mediated by natural killer cells. Nat. Immunol. 2006. 7: 507-516.
49. Sun, J. C., Beilke, J. N. and Lanier, L. L., Adaptive immune features of natural killer cells. Nature 2009. 457: 557-561.
50. Sun, J. C., Beilke, J. N., Bezman, N. A. and Lanier, L. L., Homeostatic proliferation generates long-lived natural killer cells that respond against viral infection. J. Exp. Med. 2011. 208: 357-368.