Type I IFN promotes NK cell expansion during viral infection by protecting NK cells against fratricide

Journal of Experimental Medicine

Volumn 213, Issue 2, 2016, Pages 225-233

  Madera, Sharline ^a,b   Rapp, Moritz ^a   Firth, Matthew A ^a   Beilke, Joshua N ^c   Lanier, Lewis L ^c   Sun, Joseph C ^a,b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD27 ANTIGEN; INTERFERON; NATURAL KILLER CELL RECEPTOR NKG2D; STAT1 PROTEIN; ALPHA BETA INTERFERON RECEPTOR; IFNAR1 PROTEIN, MOUSE; KLRK1 PROTEIN, MOUSE; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY K; PERFORIN; PERFORIN 1, MOUSE; STAT1 PROTEIN, MOUSE;

ADOPTIVE TRANSFER; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL DEATH; CELL EXPANSION; CELL PROLIFERATION; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; CYTOMEGALOVIRUS; DOWN REGULATION; INTRACELLULAR SIGNALING; MEMORY CELL; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; UPREGULATION; VIRUS INFECTION; ANIMAL; C57BL MOUSE; DEFICIENCY; GENETICS; HERPES VIRUS INFECTION; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; MUROMEGALOVIRUS; PATHOLOGY;

ANIMALS; APOPTOSIS; CELL PROLIFERATION; HERPESVIRIDAE INFECTIONS; INTERFERON TYPE I; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUROMEGALOVIRUS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; PERFORIN; RECEPTOR, INTERFERON ALPHA-BETA; STAT1 TRANSCRIPTION FACTOR;

EID: 84956617633     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20150712     Document Type: Article

References (45)

1. Andoniou, C.E., S.L. van Dommelen, V. Voigt, D.M. Andrews, G. Brizard, C. Asselin-Paturel, T. Delale, K.J. Stacey, G. Trinchieri, and M.A. Degli-Esposti. 2005. Interaction between conventional dendritic cells and natural killer cells is integral to the activation of effective antiviral immunity. Nat. Immunol. 6:1011-1019. http://dx.doi.org/10.1038/ni1244
2. Baranek, T., T.P. Manh, Y. Alexandre, M.A. Maqbool, J.Z. Cabeza, E. Tomasello, K. Crozat, G. Bessou, N. Zucchini, S.H. Robbins, et al. 2012. Differential responses of immune cells to type I interferon contribute to host resistance to viral infection. Cell Host Microbe. 12:571-584. http://dx.doi.org/10.1016/j.chom.2012.09.002
3. Beaulieu, A.M., C.L. Zawislak, T. Nakayama, and J.C. Sun. 2014. The transcription factor Zbtb32 controls the proliferative burst of virusspecific natural killer cells responding to infection. Nat. Immunol. 15:546-553. http://dx.doi.org/10.1038/ni.2876
4. Biron, C.A. 2001. Interferons α and β as immune regulators-a new look. Immunity. 14:661-664. http://dx.doi.org/10.1016/S1074-7613(01)00154-6
5. Biron, C.A., G. Sonnenfeld, and R.M. Welsh. 1984. Interferon induces natural killer cell blastogenesis in vivo. J. Leukoc. Biol. 35:31-37.
6. Biron, C.A., K.S. Byron, and J.L. Sullivan. 1989. Severe herpesvirus infections in an adolescent without natural killer cells. N. Engl. J. Med. 320:1731-1735. http://dx.doi.org/10.1056/NEJM198906293202605
7. Biron, C.A., K.B. Nguyen, G.C. Pien, L.P. Cousens, and T.P. Salazar-Mather. 1999. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu. Rev. Immunol. 17:189-220. http://dx.doi.org/10.1146/annurev.immunol.17.1.189
8. Brodin, P., T. Lakshmikanth, R. Mehr, M.H. Johansson, A.D. Duru, A. Achour, M. Salmon-Divon, K. Karre, P. Hoglund, and S. Johansson. 2010. Natural killer cell tolerance persists despite significant reduction of self MHC class I on normal target cells in mice. PLoS One. 5:e13174. http://dx.doi.org/10.1371/journal.pone.0013174
9. Bukowski, J.F., J.F. Warner, G. Dennert, and R.M. Welsh. 1985. Adoptive transfer studies demonstrating the antiviral effect of natural killer cells in vivo. J. Exp. Med. 161:40-52. http://dx.doi.org/10.1084/jem.161.1.40
10. Cervantes-Barragán, L., U. Kalinke, R. Züst, M. König, B. Reizis, C. López-Macías, V. Thiel, and B. Ludewig. 2009. Type I IFN-mediated protection of macrophages and dendritic cells secures control of murine coronavirus infection. J. Immunol. 182:1099-1106. http://dx.doi.org/10.4049/jimmunol.182.2.1099
11. Crouse, J., G. Bedenikovic, M. Wiesel, M. Ibberson, I. Xenarios, D. Von Laer, U. Kalinke, E. Vivier, S. Jonjic, and A. Oxenius. 2014. Type I interferons protect T cells against NK cell attack mediated by the activating receptor NCR1. Immunity. 40:961-973. http://dx.doi.org/10.1016/j.immuni.2014.05.003
12. Fodil-Cornu, N., S.H. Lee, S. Belanger, A.P. Makrigiannis, C.A. Biron, R.M. Buller, and S.M. Vidal. 2008. Ly49h-deficient C57BL/6 mice: a new mouse cytomegalovirus-susceptible model remains resistant to unrelated pathogens controlled by the NK gene complex. J. Immunol. 181:6394-6405. http://dx.doi.org/10.4049/jimmunol.181.9.6394
13. Fortin, C., X. Huang, and Y. Yang. 2013. Both NK cell-intrinsic and-extrinsic STAT1 signaling are required for NK cell response against vaccinia virus. J. Immunol. 191:363-368. http://dx.doi.org/10.4049/jimmunol.1202714
14. Gazit, R., R. Gruda, M. Elboim, T.I. Arnon, G. Katz, H. Achdout, J. Hanna, U. Qimron, G. Landau, E. Greenbaum, et al. 2006. Lethal influenza infection in the absence of the natural killer cell receptor gene Ncr1. Nat. Immunol. 7:517-523. http://dx.doi.org/10.1038/ni1322
15. Gerosa, F., M. Scardoni, M. Tommasi, C. Benati, L. Snelli, G. Gandini, M. Libonati, G. Tridente, and G. Carra. 1991. Interferon-α induces expression of the CD69 activation antigen in human resting NK cells, while interferon-γ and tumor necrosis factor-α are ineffective. Int. J. Cancer. 48:473-475.
16. Geurs, T.L., Y.M. Zhao, E.B. Hill, and A.R. French. 2009. Ly49H engagement compensates for the absence of type I interferon signaling in stimulating NK cell proliferation during murine cytomegalovirus infection. J. Immunol. 183:5830-5836. http://dx.doi.org/10.4049/jimmunol.0901520
17. González-Navajas, J.M., J. Lee, M. David, and E. Raz. 2012. Immunomodulatory functions of type I interferons. Nat. Rev. Immunol. 12:125-135.
18. Gough, D.J., N.L. Messina, C.J. Clarke, R.W. Johnstone, and D.E. Levy. 2012. Constitutive type I interferon modulates homeostatic balance through tonic signaling. Immunity. 36:166-174. http://dx.doi.org/10.1016/j.immuni.2012.01.011
19. Guan, J., S.M. Miah, Z.S. Wilson, T.K. Erick, C. Banh, and L. Brossay. 2014. Role of type I interferon receptor signaling on NK cell development and functions. PLoS One. 9:e111302. http://dx.doi.org/10.1371/journal.pone.0111302
20. Honda, K., T. Mizutani, and T. Taniguchi. 2004. Negative regulation of IFN-α/β signaling by IFN regulatory factor 2 for homeostatic development of dendritic cells. Proc. Natl. Acad. Sci. USA. 101:2416-2421. http://dx.doi.org/10.1073/pnas.0307336101
21. Joncker, N.T., N.C. Fernandez, E. Treiner, E. Vivier, and D.H. Raulet. 2009. NK cell responsiveness is tuned commensurate with the number of inhibitory receptors for self-MHC class I: the rheostat model. J. Immunol. 182:4572-4580. http://dx.doi.org/10.4049/jimmunol.0803900
22. Jonsson, A.H., L. Yang, S. Kim, S.M. Taffner, and W.M. Yokoyama. 2010. Effects of MHC class I alleles on licensing of Ly49A+ NK cells. J. Immunol. 184:3424-3432. http://dx.doi.org/10.4049/jimmunol.0904057
23. Le Bon, A., V. Durand, E. Kamphuis, C. Thompson, S. Bulfone-Paus, C. Rossmann, U. Kalinke, and D.F. Tough. 2006. Direct stimulation of T cells by type I IFN enhances the CD8+ T cell response during crosspriming. J. Immunol. 176:4682-4689. http://dx.doi.org/10.4049/jimmunol.176.8.4682
24. Li, X., S. Leung, S. Qureshi, J.E. Darnell Jr., and G.R. Stark. 1996. Formation of STAT1-STAT2 heterodimers and their role in the activation of IRF-1 gene transcription by interferon-α. J. Biol. Chem. 271:5790-5794. http://dx.doi.org/10.1074/jbc.271.10.5790
25. Madera, S., and J.C. Sun. 2015. Cutting edge: stage-specific requirement of IL-18 for antiviral NK cell expansion. J. Immunol. 194:1408-1412. http://dx.doi.org/10.4049/jimmunol.1402001
26. Marrack, P., J. Kappler, and T. Mitchell. 1999. Type I interferons keep activated T cells alive. J. Exp. Med. 189:521-530. http://dx.doi.org/10.1084/jem.189.3.521
27. Martinez, J., X. Huang, and Y. Yang. 2008. Direct action of type I IFN on NK cells is required for their activation in response to vaccinia viral infection in vivo. J. Immunol. 180:1592-1597. http://dx.doi.org/10.4049/jimmunol.180.3.1592
28. Meraz, M.A., J.M. White, K.C. Sheehan, E.A. Bach, S.J. Rodig, A.S. Dighe, D.H. Kaplan, J.K. Riley, A.C. Greenlund, D. Campbell, et al. 1996. Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell. 84:431-442. http://dx.doi.org/10.1016/S0092-8674(00)81288-X
29. Mizutani, T., N. Neugebauer, E.M. Putz, N. Moritz, O. Simma, E. Zebedin-Brandl, D. Gotthardt, W. Warsch, E. Eckelhart, H.P. Kantner, et al. 2012. Conditional IFN AR1 ablation reveals distinct requirements of Type I IFN signaling for NK cell maturation and tumor surveillance. OncoImmunology. 1:1027-1037. http://dx.doi.org/10.4161/onci.21284
30. Müller, U., U. Steinhoff, L.F. Reis, S. Hemmi, J. Pavlovic, R.M. Zinkernagel, and M. Aguet. 1994. Functional role of type I and type II interferons in antiviral defense. Science. 264:1918-1921. http://dx.doi.org/10.1126/science.8009221
31. Narni-Mancinelli, E., J. Chaix, A. Fenis, Y.M. Kerdiles, N. Yessaad, A. Reynders, C. Gregoire, H. Luche, S. Ugolini, E. Tomasello, et al. 2011. Fate mapping analysis of lymphoid cells expressing the NKp46 cell surface receptor. Proc. Natl. Acad. Sci. USA. 108:18324-18329. http://dx.doi.org/10.1073/pnas.1112064108
32. Nguyen, K.B., L.P. Cousens, L.A. Doughty, G.C. Pien, J.E. Durbin, and C.A. Biron. 2000. Interferon α/β-mediated inhibition and promotion of interferon γ: STAT1 resolves a paradox. Nat. Immunol. 1:70-76. http://dx.doi.org/10.1038/76940
33. Nguyen, K.B., T.P. Salazar-Mather, M.Y. Dalod, J.B. Van Deusen, X.Q. Wei, F.Y. Liew, M.A. Caligiuri, J.E. Durbin, and C.A. Biron. 2002. Coordinated and distinct roles for IFN-αβ, IL-12, and IL-15 regulation of NK cell responses to viral infection. J. Immunol. 169:4279-4287. http://dx.doi.org/10.4049/jimmunol.169.8.4279
34. Orange, J.S., and C.A. Biron. 1996. Characterization of early IL-12, IFN-αβ, and TNF effects on antiviral state and NK cell responses during murine cytomegalovirus infection. J. Immunol. 156:4746-4756.
35. Rager-Zisman, B., P.C. Quan, M. Rosner, J.R. Moller, and B.R. Bloom. 1987. Role of NK cells in protection of mice against herpes simplex virus-1 infection. J. Immunol. 138:884-888.
36. Sato, T., N. Onai, H. Yoshihara, F. Arai, T. Suda, and T. Ohteki. 2009. Interferon regulatory factor-2 protects quiescent hematopoietic stem cells from type I interferon-dependent exhaustion. Nat. Med. 15:696-700. http://dx.doi.org/10.1038/nm.1973
37. Schluns, K.S., and L. Lefrançois. 2003. Cytokine control of memory T-cell development and survival. Nat. Rev. Immunol. 3:269-279. http://dx.doi.org/10.1038/nri1052
38. Sun, J.C., and L.L. Lanier. 2011. NK cell development, homeostasis and function: parallels with CD8+ T cells. Nat. Rev. Immunol. 11:645-657. http://dx.doi.org/10.1038/nri3044
39. Sun, J.C., M.A. Williams, and M.J. Bevan. 2004. CD4+ T cells are required for the maintenance, not programming, of memory CD8+ T cells after acute infection. Nat. Immunol. 5:927-933. http://dx.doi.org/10.1038/ni1105
40. Sun, J.C., J.N. Beilke, and L.L. Lanier. 2009. Adaptive immune features of natural killer cells. Nature. 457:557-561. http://dx.doi.org/10.1038/nature07665
41. Sun, J.C., S. Madera, N.A. Bezman, J.N. Beilke, M.H. Kaplan, and L.L. Lanier. 2012. Proinflammatory cytokine signaling required for the generation of natural killer cell memory. J. Exp. Med. 209:947-954. http://dx.doi.org/10.1084/jem.20111760
42. Uzé, G., G. Schreiber, J. Piehler, and S. Pellegrini. 2007. The receptor of the type I interferon family. Curr. Top. Microbiol. Immunol. 316:71-95.
43. Vivier, E., D.H. Raulet, A. Moretta, M.A. Caligiuri, L. Zitvogel, L.L. Lanier, W.M. Yokoyama, and S. Ugolini. 2011. Innate or adaptive immunity? The example of natural killer cells. Science. 331:44-49. http://dx.doi.org/10.1126/science.1198687
44. Xu, H.C., M. Grusdat, A.A. Pandyra, R. Polz, J. Huang, P. Sharma, R. Deenen, K. Köhrer, R. Rahbar, A. Diefenbach, et al. 2014. Type I interferon protects antiviral CD8+ T cells from NK cell cytotoxicity. Immunity. 40:949-960. http://dx.doi.org/10.1016/j.immuni.2014.05.004
45. Züst, R., Y.X. Toh, I. Valdés, D. Cerny, J. Heinrich, L. Hermida, E. Marcos, G. Guillén, U. Kalinke, P.Y. Shi, and K. Fink. 2014. Type I interferon signals in macrophages and dendritic cells control dengue virus infection: implications for a new mouse model to test dengue vaccines. J. Virol. 88:7276-7285. http://dx.doi.org/10.1128/JVI.03827-13