T-bet and Eomes govern differentiation and function of mouse and human NK cells and ILC1

European Journal of Immunology

Volumn 48, Issue 5, 2018, Pages 738-750

  Zhang, Jiang ^a,b   Marotel, Marie ^a   Fauteux Daniel, Sébastien ^a   Mathieu, Anne Laure ^a   Viel, Sébastien ^a,c   Marçais, Antoine ^a   Walzer, Thierry ^a  

^a CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

^b EAST CHINA NORMAL UNIVERSITY   (China)

^c CENTRE HOSPITALIER LYON SUD   (France)

Author keywords

Eomes; ILCs; NK cell differentiation; T bet; T box transcription factors

Indexed keywords

INTERLEUKIN 2 RECEPTOR BETA; T BOX TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EOMES; TRANSCRIPTION FACTOR T BET; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; ZINC FINGER E BOX BINDING HOMEOBOX 2; DNA BINDING PROTEIN; EOMES PROTEIN, HUMAN; EOMES PROTEIN, MOUSE; T-BOX TRANSCRIPTION FACTOR TBX21;

CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CYTOKINE RELEASE; CYTOTOXIC LYMPHOCYTE; CYTOTOXICITY; HUMAN; INFECTION; LYMPHOID CELL; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; ANIMAL; CELL DIFFERENTIATION; COMMUNICABLE DISEASE; CYTOLOGY; GENETICS; IMMUNOLOGY; LYMPHOCYTE SUBPOPULATION; METABOLISM; NEOPLASM;

ANIMALS; CELL DIFFERENTIATION; COMMUNICABLE DISEASES; DNA-BINDING PROTEINS; HUMANS; KILLER CELLS, NATURAL; LYMPHOCYTE SUBSETS; MICE; NEOPLASMS; T-BOX DOMAIN PROTEINS; ZINC FINGER E-BOX BINDING HOMEOBOX 2;

EID: 85042528618     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201747299     Document Type: Review

References (135)

1. Herrmann, B. G., Labeit, S., Poustka, A., King, T. R. and Lehrach, H., Cloning of the T gene required in mesoderm formation in the mouse. Nature 1990. 343: 617–622.
2. Papaioannou, V. E., The T-box gene family: emerging roles in development, stem cells and cancer. Dev. Camb. Engl. 2014. 141: 3819–3833.
3. Chatr-Aryamontri, A., Oughtred, R., Boucher, L., Rust, J., Chang, C., Kolas, N. K., O'Donnell, L. et al., The BioGRID interaction database: 2017 update. Nucleic. Acids. Res. 2017. 45: D369–D379.
4. Szabo, S. J., Kim, S. T., Costa, G. L., Zhang, X., Fathman, C. G. and Glimcher, L. H., A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 2000. 100: 655–669.
5. Yang, Y., Ochando, J. C., Bromberg, J. S. and Ding, Y., Identification of a distant T-bet enhancer responsive to IL-12/Stat4 and IFNgamma/Stat1 signals. Blood 2007. 110: 2494–2500.
6. Kallies, A. and Good-Jacobson, K. L., Transcription factor T-bet orchestrates lineage development and function in the immune system. Trends Immunol. 2017. 38: 287–297.
7. Intlekofer, A. M., Takemoto, N., Wherry, E. J., Longworth, S. A., Northrup, J. T., Palanivel, V. R., Mullen, A. C. et al., Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat. Immunol. 2005. 6: 1236–1244.
8. 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.
9. Yang, Y., Xu, J., Niu, Y., Bromberg, J. S. and Ding, Y., T-bet and eomesodermin play critical roles in directing T cell differentiation to Th1 versus Th17. J. Immunol. 2008. 181: 8700–8710.
10. Suto, A., Wurster, A. L., Reiner, S. L. and Grusby, M. J., IL-21 inhibits IFN-gamma production in developing Th1 cells through the repression of Eomesodermin expression. J. Immunol. 2006. 177: 3721–3727.
11. Steiner, D. F., Thomas, M. F., Hu, J. K., Yang, Z., Babiarz, J. E., Allen, C. D. C., Matloubian, M. et al., MicroRNA-29 regulates T-box transcription factors and interferon-γ production in helper T cells. Immunity 2011. 35: 169–181.
12. Curran, M. A., Geiger, T. L., Montalvo, W., Kim, M., Reiner, S. L., Al-Shamkhani, A., Sun, J. C. et al., Systemic 4-1BB activation induces a novel T cell phenotype driven by high expression of Eomesodermin. J. Exp. Med. 2013. 210: 743–755.
13. Endo, Y., Iwamura, C., Kuwahara, M., Suzuki, A., Sugaya, K., Tumes, D. J., Tokoyoda, K. et al., Eomesodermin controls interleukin-5 production in memory T helper 2 cells through inhibition of activity of the transcription factor GATA3. Immunity 2011. 35: 733–745.
14. Ichiyama, K., Sekiya, T., Inoue, N., Tamiya, T., Kashiwagi, I., Kimura, A., Morita, R. et al., Transcription factor Smad-independent T helper 17 cell induction by transforming-growth factor-β is mediated by suppression of eomesodermin. Immunity 2011. 34: 741–754.
15. Beima, K. M., Miazgowicz, M. M., Lewis, M. D., Yan, P. S., Huang, T. H.-M. and Weinmann, A. S., T-bet binding to newly identified target gene promoters is cell type-independent but results in variable context-dependent functional effects. J. Biol. Chem. 2006. 281: 11992–12000.
16. 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.
17. Marçais, A., Viel, S., Grau, M., Henry, T., Marvel, J. and Walzer, T., Regulation of mouse NK cell development and function by cytokines. Front Immunol. 2013. 4: 450.
18. Vivier, E., Tomasello, E., Baratin, M., Walzer, T. and Ugolini, S., Functions of natural killer cells. Nat. Immunol. 2008. 9: 503–510.
19. Schoenborn, J. R. and Wilson, C. B., Regulation of interferon-gamma during innate and adaptive immune responses. Adv. Immunol. 2007. 96: 41–101.
20. Lanier, L. L., Up on the tightrope: natural killer cell activation and inhibition. Nat. Immunol. 2008. 9: 495–502.
21. Spits, H. and Santo, J. P. D., The expanding family of innate lymphoid cells: regulators and effectors of immunity and tissue remodeling. Nat. Publ. Group 2010. 12: 21–27.
22. Kim, S., Iizuka, K., Kang, H.-S. P., Dokun, A., French, A. R., Greco, S., Yokoyama, W. M., In vivo developmental stages in murine natural killer cell maturation. Nat. Immunol. 2002. 3: 523–528.
23. 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.
24. 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.
25. Walzer, T., Chiossone, L., Chaix, J., Calver, A., Carozzo, C., Garrigue-Antar, L., Jacques, Y. et al., Natural killer cell trafficking in vivo requires a dedicated sphingosine 1-phosphate receptor. Nat. Immunol. 2007. 8: 1337–1344.
26. Grégoire, C., Chasson, L., Luci, C., Tomasello, E., Geissmann, F., Vivier, E. and Walzer, T., The trafficking of natural killer cells. Immunol. Rev. 2007. 220: 169–182.
27. Mayol, K., Biajoux, V., Marvel, J., Balabanian, K. and Walzer, T., Sequential desensitization of CXCR4 and S1P5 controls natural killer cell trafficking. Blood 2011. 118: 4863–4871.
28. 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.
29. Despoix, N., Walzer, T., Jouve, N., Blot-Chabaud, M., Bardin, N., Paul, P., Lyonnet, L. et al., Mouse CD146/MCAM is a marker of natural killer cell maturation. Eur. J. Immunol. 2008. 38: 2855–2864.
30. Carotta, S., Pang, S. H. M., Nutt, S. L. and Belz, G. T., Identification of the earliest NK-cell precursor in the mouse BM. Blood 2011. 117: 5449–5452.
31. Rosmaraki, E. E., Douagi, I., Roth, C., Colucci, F., Cumano, A. and Di Santo, J. P., Identification of committed NK cell progenitors in adult murine bone marrow. Eur. J. Immunol. 2001. 31: 1900–1909.
32. Levanon, D., Negreanu, V., Lotem, J., Bone, K. R., Brenner, O., Leshkowitz, D. and Groner, Y., Transcription factor Runx3 regulates interleukin-15-dependent natural killer cell activation. Mol. Cell. Biol. 2014. 34: 1158–1169.
33. Seillet, C., Huntington, N. D., Gangatirkar, P., Axelsson, E., Minnich, M., Brady, H. J. M., Busslinger, M. et al., Differential requirement for Nfil3 during NK cell development. J. Immunol. 2014. 192: 2667–2676.
34. Male, V., Nisoli, I., Kostrzewski, T., Allan, D. S. J., Carlyle, J. R., Lord, G. M., Wack, A. et al., The transcription factor E4bp4/Nfil3 controls commitment to the NK lineage and directly regulates Eomes and Id2 expression. J. Exp. Med. 2014. 211: 635–642.
35. Ramirez, K., Chandler, K. J., Spaulding, C., Zandi, S., Sigvardsson, M., Graves, B. J. and Kee, B. L., Gene deregulation and chronic activation in natural killer cells deficient in the transcription factor ETS1. Immunity 2012. 36: 921–932.
36. Vong, Q. P., Leung, W.-H., Houston, J., Li, Y., Rooney, B., Holladay, M., Oostendorp, R. A. et al., TOX2 regulates human natural killer cell development by controlling T-BET expression. Blood 2014. 124: 3905–3913.
37. Daussy, C., Faure, F., Mayol, K., Viel, S., Gasteiger, G., Charrier, E., Bienvenu, J. et al., T-bet and Eomes instruct the development of two distinct natural killer cell lineages in the liver and in the bone marrow. J. Exp. Med. 2014. 211: 563–577.
38. Townsend, M. J., Weinmann, A. S., Matsuda, J. L., Salomon, R., Farnham, P. J., Biron, C. A., Gapin, L. et al., T-bet regulates the terminal maturation and homeostasis of NK and Valpha14i NKT cells. Immunity 2004. 20: 477–494.
39. van Helden, M. J., Goossens, S., Daussy, C., Mathieu, A.-L., Faure, F., Marçais, A., Vandamme, N. et al., Terminal NK cell maturation is controlled by concerted actions of T-bet and Zeb2 and is essential for melanoma rejection. J. Exp. Med. 2015. 212: 2015–2025.
40. Gordon, S. M., Chaix, J., Rupp, L. J., Wu, J., Madera, S., Sun, J. C., Lindsten, T. et al., The transcription factors T-bet and Eomes control key checkpoints of natural killer cell maturation. Immunity 2012. 36: 55–67.
41. Pikovskaya, O., Chaix, J., Rothman, N. J., Collins, A., Chen, Y.-H., Scipioni, A. M., Vivier, E. et al., Cutting edge: eomesodermin is sufficient to direct type 1 innate lymphocyte development into the conventional NK lineage. J. Immunol. 2016. 196: 1449–1454.
42. Sun, J. C., Ma, A. and Lanier, L. L., Cutting edge: IL-15-independent NK cell response to mouse cytomegalovirus infection. J. Immunol. 2009. 183: 2911–2914.
43. Lee, S.-H., Fragoso, M. F. and Biron, C. A., Cutting edge: a novel mechanism bridging innate and adaptive immunity: IL-12 induction of CD25 to form high-affinity IL-2 receptors on NK Cells. J. Immunol. 2012. 189: 2712–2716.
44. Bihl, F., Pecheur, J., Bréart, B., Poupon, G., Cazareth, J., Julia, V., Glaichenhaus, N. et al., Primed antigen-specific CD4+ T cells are required for NK cell activation in vivo upon Leishmania major infection. J. Immunol. 2010. 185: 2174–2181.
45. Gasteiger, G., Hemmers, S., Firth, M. A., Floc'h, A. L., Huse, M., Sun, J. C. and Rudensky, A. Y., IL-2–dependent tuning of NK cell sensitivity for target cells is controlled by regulatory T cells. J. Exp. Med. 2013. 210: 1167–1178.
46. Soderquest, K., Powell, N., Luci, C., Rooijen, N. V., Hidalgo, A., Geissmann, F., Walzer, T. et al., Monocytes control natural killer cell differentiation to effector phenotypes. Blood 2011. 117: 4511–4518.
47. Robbins, S. H., Tessmer, M. S., Van Kaer, L. and Brossay, L., Direct effects of T-bet and MHC class I expression, but not STAT1, on peripheral NK cell maturation. Eur. J. Immunol. 2005. 35: 757–765.
48. Jenne, C. N., Enders, A., Rivera, R., Watson, S. R., Bankovich, A. J., Pereira, J. P., Xu, Y. et al., T-bet-dependent S1P5 expression in NK cells promotes egress from lymph nodes and bone marrow. J. Exp. Med. 2009. 206: 2469–2481.
49. Drouillard, A., Mathieu, A. L., Marçais, A., Belot, A., Viel, S., Mingueneau, M., Guckian, K. et al., S1PR5 is essential for human natural killer cell migration toward sphingosine-1 phosphate. J. Allergy Clin. Immunol. 2017. S0091–S6749: 31898–31905.
50. Werneck, M. B. F., Lugo-Villarino, G., Hwang, E. S., Cantor, H. and Glimcher, L. H., T-bet plays a key role in NK-mediated control of melanoma metastatic disease. J. Immunol. 2008. 180: 8004–8010.
51. Harms Pritchard, G., Hall, A. O., Christian, D. A., Wagage, S., Fang, Q., Muallem, G., John, B. et al., Diverse roles for T-bet in the effector responses required for resistance to infection. J. Immunol. 2015. 194: 1131–1140.
52. Gheldof, A., Hulpiau, P., van Roy, F., De Craene, B. and Berx, G., Evolutionary functional analysis and molecular regulation of the ZEB transcription factors. Cell Mol. Life Sci. CMLS 2012. 69: 2527–2541.
53. Arnold, C. N., Pirie, E., Dosenovic, P., McInerney, G. M., Xia, Y., Wang, N., Li, X. et al., A forward genetic screen reveals roles for Nfkbid, Zeb1, and Ruvbl2 in humoral immunity. Proc. Natl Acad. Sci. 2012. 109: 12286–12293.
54. Kallies, A., Carotta, S., Huntington, N. D., Bernard, N. J., Tarlinton, D. M., Smyth, M. J., Nutt, S. L. et al., A role for Blimp1 in the transcriptional network controlling natural killer cell maturation. Blood 2011. 117: 1869–1879.
55. Kallies, A., Xin, A., Belz, G. T. and Nutt, S. L., Blimp-1 transcription factor is required for the differentiation of effector CD8(+) T cells and memory responses. Immunity 2009. 31: 283–295.
56. Dominguez, C. X., Amezquita, R. A., Guan, T., Marshall, H. D., Joshi, N. S., Kleinstein, S. H., Kaech, S. M. et al., The transcription factors ZEB2 and T-bet cooperate to program cytotoxic T cell terminal differentiation in response to LCMV viral infection. J. Exp. Med. 2015. 212: 2041–2056.
57. Omilusik, K. D., Best, J. A., Yu, B., Goossens, S., Weidemann, A., Nguyen, J. V., Seuntjens, E. et al., Transcriptional repressor ZEB2 promotes terminal differentiation of CD8+ effector and memory T cell populations during infection. J. Exp. Med. 2015. 212: 2027–2039.
58. Kaech, S. M. and Cui, W., Transcriptional control of effector and memory CD8+ T cell differentiation. Nat. Rev. Immunol. 2012. 12: 749–761.
59. Pipkin, M. E., Sacks, J. A., Cruz-Guilloty, F., Lichtenheld, M. G., Bevan, M. J. and Rao, A., Interleukin-2 and inflammation induce distinct transcriptional programs that promote the differentiation of effector cytolytic T cells. Immunity 2010. 32: 79–90.
60. Weinreich, M. A., Odumade, O. A., Jameson, S. C. and Hogquist, K. A., T cells expressing the transcription factor PLZF regulate the development of memory-like CD8+ T cells. Nat. Immunol. 2010. 11: 709–716.
61. Martinet, V., Tonon, S., Torres, D., Azouz, A., Nguyen, M., Kohler, A., Flamand, V. et al., Type I interferons regulate eomesodermin expression and the development of unconventional memory CD8(+) T cells. Nat. Commun. 2015. 6: 7089.
62. Viel, S., Marçais, A., Guimaraes, F. S.-F., Loftus, R., Rabilloud, J., Grau, M., Degouve, S. et al., TGF-β inhibits the activation and functions of NK cells by repressing the mTOR pathway. Sci. Signal. 2016. 9: ra19.
63. Rao, R. R., Li, Q., Odunsi, K. and Shrikant, P. A., The mTOR kinase determines effector versus memory CD8+ T cell fate by regulating the expression of transcription factors T-bet and Eomesodermin. Immunity 2010. 32: 1–12.
64. O'Sullivan, T. E., Johnson, L. R., Kang, H. H. and Sun, J. C., BNIP3- and BNIP3L-mediated mitophagy promotes the generation of natural killer cell memory. Immunity 2015. 43: 331–342.
65. Zhang, L., Tschumi, B. O., Lopez-Mejia, I. C., Oberle, S. G., Meyer, M., Samson, G., Rüegg, M. A. et al., Mammalian target of rapamycin complex 2 controls CD8 T cell memory differentiation in a Foxo1-dependent manner. Cell Rep. 2016. 14: 1206–1217.
66. Rao, R. R., Li, Q., Bupp, M. R. G. and Shrikant, P. A., Transcription factor Foxo1 represses T-bet-mediated effector functions and promotes memory CD8+ T cell differentiation. Immunity 2012. 36: 1–14.
67. Deng, Y., Kerdiles, Y., Chu, J., Yuan, S., Wang, Y., Chen, X., Mao, H. et al., Transcription factor foxo1 is a negative regulator of natural killer cell maturation and function. Immunity 2015. 42: 457–470.
68. Degouve, S., Tavares, A., Viel, S., Walzer, T. and Marçais, A., NKp46-mediated Dicer1 inactivation results in defective NK-cell differentiation and effector functions in mice. Eur. J. Immunol. 2016. 46: 1902–1911.
69. Peng, H., Jiang, X., Chen, Y., Sojka, D. K., Wei, H., Gao, X., Sun, R. et al., Liver-resident NK cells confer adaptive immunity in skin-contact inflammation. J. Clin. Invest. 2013. 123: 1444–1456.
70. Nakayamada, S., Kanno, Y., Takahashi, H., Jankovic, D., Lu, K. T., Johnson, T. A., Sun, H. W. et al., Early Th1 cell differentiation is marked by a Tfh cell-like transition. Immunity 2011. 35: 919–931.
71. Iwata, S., Mikami, Y., Sun, H.-W., Brooks, S. R., Jankovic, D., Hirahara, K., Onodera, A. et al., The transcription factor T-bet limits amplification of type I IFN transcriptome and circuitry in T helper 1 cells. Immunity 2017. 46: 983–991.e4.
72. Jenner, R. G., Townsend, M. J., Jackson, I., Sun, K., Bouwman, R. D., Young, R. A., Glimcher, L. H. et al., The transcription factors T-bet and GATA-3 control alternative pathways of T-cell differentiation through a shared set of target genes. Proc. Natl Acad. Sci. 2009. 106: 17876–17881.
73. Kanhere, A., Hertweck, A., Bhatia, U., Gökmen, M. R., Perucha, E., Jackson, I., Lord, G. M. et al., T-bet and GATA3 orchestrate Th1 and Th2 differentiation through lineage-specific targeting of distal regulatory elements. Nat. Commun. 2012. 3: 1268.
74. Hertweck, A., Evans, C. M., Eskandarpour, M., Lau, J. C. H., Oleinika, K., Jackson, I., Kelly, A. et al., T-bet activates Th1 genes through mediator and the super elongation complex. Cell Rep. 2016. 15: 2756–2770.
75. Teo, A. K. K., Arnold, S. J., Trotter, M. W. B., Brown, S., Ang, L. T., Chng, Z., Robertson, E. J. et al., Pluripotency factors regulate definitive endoderm specification through eomesodermin. Genes Dev. 2011. 25: 238–250.
76. Shih, H.-Y., Sciumè, G., Mikami, Y., Guo, L., Sun, H.-W., Brooks, S. R., Urban, J. F. Jr. et al., Developmental acquisition of regulomes underlies innate lymphoid cell functionality. Cell 2016. 165: 1120–1133.
77. Miller, S. A., Huang, A. C., Miazgowicz, M. M., Brassil, M. M. and Weinmann, A. S., Coordinated but physically separable interaction with H3K27-demethylase and H3K4-methyltransferase activities are required for T-box protein-mediated activation of developmental gene expression. Genes Dev. 2008. 22: 2980–2993.
78. Miller, S. A., Mohn, S. E. and Weinmann, A. S., Jmjd3 and UTX play a demethylase-independent role in chromatin remodeling to regulate T-box family member-dependent gene expression. Mol. Cell 2010. 40: 594–605.
79. Miller, S. A. and Weinmann, A. S., Molecular mechanisms by which T-bet regulates T-helper cell commitment. Immunol. Rev. 2010. 238: 233–246.
80. Sekimata, M., Pérez-Melgosa, M., Miller, S. A., Weinmann, A. S., Sabo, P. J., Sandstrom, R., Dorschner, M. O. et al., CCCTC-binding factor and the transcription factor T-bet orchestrate T helper 1 cell-specific structure and function at the interferon-gamma locus. Immunity 2009. 31: 551–564.
81. Way, S. S. and Wilson, C. B., Cutting edge: immunity and IFN-gamma production during Listeria monocytogenes infection in the absence of T-bet. J. Immunol. 2004. 173: 5918–5922.
82. Cruz-Guilloty, F., Pipkin, M. E., Djuretic, I. M., Levanon, D., Lotem, J., Lichtenheld, M. G., Groner, Y. et al., Runx3 and T-box proteins cooperate to establish the transcriptional program of effector CTLs. J. Exp. Med. 2009. 206: 9.
83. Pearce, E. L., Mullen, A. C., Martins, G. A., Krawczyk, C. M., Hutchins, A. S., Zediak, V. P., Banica, M. et al., Control of effector CD8+ T cell function by the transcription factor Eomesodermin. Science 2003. 302: 1041–1043.
84. Araki, Y., Fann, M., Wersto, R. and Weng, N.-P., Histone acetylation facilitates rapid and robust memory CD8 T cell response through differential expression of effector molecules (eomesodermin and its targets: perforin and granzyme B). J. Immunol. 2008. 180: 8102–8108.
85. Martín-Fontecha, A., Thomsen, L. L., Brett, S., Gerard, C., Lipp, M., Lanzavecchia, A. and Sallusto, F., Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat. Immunol. 2004. 5: 1260–1265.
86. Matsuda, J. L., George, T. C., Hagman, J. and Gapin, L., Temporal dissection of T-bet functions. J. Immunol. 2007. 178: 3457–3465.
87. Takeda, K., Cretney, E., Hayakawa, Y., Ota, T., Akiba, H., Ogasawara, K., Yagita, H. et al., TRAIL identifies immature natural killer cells in newborn mice and adult mouse liver. Blood 2005. 105: 2082–2089.
88. Klose, C. S. N. and Artis, D., Innate lymphoid cells as regulators of immunity, inflammation and tissue homeostasis. Nat. Immunol. 2016. 17: 765–774.
89. Vély, F., Barlogis, V., Vallentin, B., Neven, B., Piperoglou, C., Ebbo, M., Perchet, T. et al., Evidence of innate lymphoid cell redundancy in humans. Nat. Immunol. 2016. 17: 1291–1299.
90. Cortez, V. S. and Colonna, M., Diversity and function of group 1 innate lymphoid cells. Immunol. Lett. 2016. 179: 19–24.
91. Spits, H., Bernink, J. H. and Lanier, L., NK cells and type 1 innate lymphoid cells: partners in host defense. Nat. Immunol. 2016. 17: 758–764.
92. Bernink, J. H., Peters, C. P., Munneke, M., te Velde, A. A., Meijer, S. L., Weijer, K., Hreggvidsdottir, H. S. et al., Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat. Immunol. 2013. 14: 221–229.
93. Cathal, H., Robinson, M., Fahey, R., Whelan, S.-A., Houlihan, D., Geoghegan, J. and O'Farrelly, C., The human adult liver is enriched with tissue-resident Eomes(hi) T-bet(lo) CD56(bright) natural killer cells with reduced pro-inflammatory potential. Eur. J. Immunol. 2016. 46: 2111–2120.
94. Lugthart, G., Melsen, J. E., Vervat, C., van Ostaijen-Ten Dam, M. M., Corver, W. E., Roelen, D. L., van Bergen, J. et al., Human lymphoid tissues harbor a distinct CD69+CXCR6+ NK cell population. J. Immunol. 2016. 197: 78–84.
95. Hudspeth, K., Donadon, M., Cimino, M., Pontarini, E., Tentorio, P., Preti, M., Hong, M. et al., Human liver-resident CD56(bright)/CD16(neg) NK cells are retained within hepatic sinusoids via the engagement of CCR5 and CXCR6 pathways. J. Autoimmun. 2016. 66: 40–50.
96. Stegmann, K. A., Robertson, F., Hansi, N., Gill, U., Pallant, C., Christophides, T., Pallett, L. J. et al., CXCR6 marks a novel subset of T-bet(lo)Eomes(hi) natural killer cells residing in human liver. Sci. Rep. 2016. 6: 26157.
97. Collins, A., Rothman, N., Liu, K. and Reiner, S. L., Eomesodermin and T-bet mark developmentally distinct human natural killer cells. JCI Insight 2017. 2: e90063.
98. Freud, A. G. and Caligiuri, M. A., Human natural killer cell development. Immunol. Rev. 2006. 214: 56–72.
99. Marotel, M., Hasan, U., Viel, S., Marçais, A. and Walzer, T., Back to the drawing board: Understanding the complexity of hepatic innate lymphoid cells. Eur. J. Immunol. 2016. 46: 2095–2098.
100. Paust, S., Gill, H. S., Wang, B.-Z., Flynn, M. P., Moseman, E. A., Senman, B., Szczepanik, M. et al., Critical role for the chemokine receptor CXCR6 in NK cell-mediated antigen-specific memory of haptens and viruses. Nat. Immunol. 2010. 11: 1127–1135.
101. Rouzaire, P., Luci, C., Blasco, E., Bienvenu, J., Walzer, T., Nicolas, J.-F. and Hennino, A., Natural Killer cells and T cells induce different types of skin reactions during recall responses to haptens. Eur. J. Immunol. 2011. 42: 80–88.
102. Marquardt, N., Béziat, V., Nyström, S., Hengst, J., Ivarsson, M. A., Kekäläinen, E., Johansson, H. et al., Cutting edge: identification and characterization of human intrahepatic CD49a+ NK cells. J. Immunol. 2015. 194: 2467–2471.
103. Sullivan, B. M., Jobe, O., Lazarevic, V., Vasquez, K., Bronson, R., Glimcher, L. H. and Kramnik, I., Increased susceptibility of mice lacking T-bet to infection with Mycobacterium tuberculosis correlates with increased IL-10 and decreased IFN-gamma production. J. Immunol. 2005. 175: 4593–4602.
104. Ravindran, R., Foley, J., Stoklasek, T., Glimcher, L. H. and McSorley, S. J., Expression of T-bet by CD4 T cells is essential for resistance to Salmonella infection. J. Immunol. 2005. 175: 4603–4610.
105. Matsui, M., Moriya, O., Yoshimoto, T. and Akatsuka, T., T-bet is required for protection against vaccinia virus infection. J. Virol. 2005. 79: 12798–12806.
106. Beaulieu, A. M., Zawislak, C. L., Nakayama, T. and Sun, J. C., The transcription factor Zbtb32 controls the proliferative burst of virus-specific natural killer cells responding to infection. Nat. Immunol. 2014. 15: 546–553.
107. Lighvani, A. A., Frucht, D. M., Jankovic, D., Yamane, H., Aliberti, J., Hissong, B. D., Nguyen, B. V. et al., T-bet is rapidly induced by interferon-gamma in lymphoid and myeloid cells. Proc. Natl. Acad. Sci. USA 2001. 98: 15137–15142.
108. Arnold, S. J., Hofmann, U. K., Bikoff, E. K. and Robertson, E. J., Pivotal roles for eomesodermin during axis formation, epithelium-to-mesenchyme transition and endoderm specification in the mouse. Dev. Camb. Engl. 2008. 135: 501–511.
109. Russ, A. P., Wattler, S., Colledge, W. H., Aparicio, S. A., Carlton, M. B., Pearce, J. J., Barton, S. C. et al., Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 2000. 404: 95–99.
110. Bi, J. and Tian, Z., NK cell exhaustion. Front Immunol 2017. 8: 760.
111. Virgin, H. W., Wherry, E. J. and Ahmed, R., Redefining chronic viral infection. Cell 2009. 138: 30–50.
112. Kim, P. S. and Ahmed, R., Features of responding T cells in cancer and chronic infection. Curr. Opin. Immunol. 2010. 22: 223–230.
113. Wherry, E. J., T cell exhaustion. Nat. Immunol. 2011. 12: 492–499.
114. Parish, I. A. and Kaech, S. M., Diversity in CD8(+) T cell differentiation. Curr. Opin. Immunol. 2009. 21: 291–297.
115. Kao, C., Oestreich, K. J., Paley, M. A., Crawford, A., Angelosanto, J. M., Ali, M.-A. A., Intlekofer, A. M. et al., Transcription factor T-bet represses expression of the inhibitory receptor PD-1 and sustains virus-specific CD8+ T cell responses during chronic infection. Nat. Immunol. 2011. 12: 663–671.
116. Wherry, E. J., Ha, S.-J., Kaech, S. M., Haining, W. N., Sarkar, S., Kalia, V., Subramaniam, S. et al., Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 2007. 27: 670–684.
117. Buggert, M., Tauriainen, J., Yamamoto, T., Frederiksen, J., Ivarsson, M. A., Michaëlsson, J., Lund, O. et al., T-bet and Eomes are differentially linked to the exhausted phenotype of CD8+ T cells in HIV infection. PLoS Pathog. 2014. 10: e1004251.
118. Joshi, N. S., Cui, W., Chandele, A., Lee, H. K., Urso, D. R., Hagman, J., Gapin, L. et al., Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity 2007. 27: 281–295.
119. Takemoto, N., Intlekofer, A. M., Northrup, J. T., Wherry, E. J. and Reiner, S. L., Cutting edge: IL-12 inversely regulates T-bet and Eomesodermin expression during pathogen-induced CD8+ T cell differentiation. J. Immunol. 2006. 177: 7515–7519.
120. Kurktschiev, P. D., Raziorrouh, B., Schraut, W., Backmund, M., Wächtler, M., Wendtner, C.-M., Bengsch, B. et al., Dysfunctional CD8+ T cells in hepatitis B and C are characterized by a lack of antigen-specific T-bet induction. J. Exp. Med. 2014. 211: 2047–2059.
121. Snell, L. M., McGaha, T. L. and Brooks, D. G., Type I interferon in chronic virus infection and cancer. Trends Immunol. 2017. 38: 542–557.
122. Li, H., Zhai, N., Wang, Z., Song, H., Yang, Y., Cui, A., Li, T. et al., Regulatory NK cells mediated between immunosuppressive monocytes and dysfunctional T cells in chronic HBV infection. Gut 2017. pii: gutjnl-2017-314098.
123. Peng, S. L., Townsend, M. J., Hecht, J. L., White, I. A. and Glimcher, L. H., T-bet regulates metastasis rate in a murine model of primary prostate cancer. Cancer Res. 2004. 64: 452–455.
124. Zhu, Y., Ju, S., Chen, E., Dai, S., Li, C., Morel, P., Liu, L. et al., T-bet and eomesodermin are required for T cell-mediated antitumor immune responses. J. Immunol. 2010. 185: 3174–3183.
125. Gill, S., Vasey, A. E., De Souza, A., Baker, J., Smith, A. T., Kohrt, H. E., Florek, M. et al., Rapid development of exhaustion and down-regulation of eomesodermin limit the antitumor activity of adoptively transferred murine natural killer cells. Blood 2012. 119: 5758–5768.
126. Trotta, R., Dal Col, J., Yu, J., Ciarlariello, D., Thomas, B., Zhang, X., Allard, J. et al., TGF-beta utilizes SMAD3 to inhibit CD16-mediated IFN-gamma production and antibody-dependent cellular cytotoxicity in human NK cells. J. Immunol. 2008. 181: 3784–3792.
127. Gao, Y., Souza-Fonseca-Guimaraes, F., Bald, T., Ng, S. S., Young, A., Ngiow, S. F., Rautela, J. et al., Tumor immunoevasion by the conversion of effector NK cells into type 1 innate lymphoid cells. Nat. Immunol. 2017. 18: 1004–1015.
128. Cortez, V. S., Ulland, T. K., Cervantes-Barragan, L., Bando, J. K., Robinette, M. L., Wang, Q., White, A. J. et al., SMAD4 impedes the conversion of NK cells into ILC1-like cells by curtailing non-canonical TGF-β signaling. Nat. Immunol. 2017. 18: 995–1003.
129. Conidi, A., Cazzola, S., Beets, K., Coddens, K., Collart, C., Cornelis, F., Cox, L. et al., Few Smad proteins and many Smad-interacting proteins yield multiple functions and action modes in TGFβ/BMP signaling in vivo. Cytokine Growth Factor Rev. 2011. 22: 287–300.
130. Cortez, V. S., Cervantes-Barragan, L., Robinette, M. L., Bando, J. K., Wang, Y., Geiger, T. L., Gilfillan, S. et al., Transforming growth factor-β signaling guides the differentiation of innate lymphoid cells in salivary glands. Immunity 2016. 44: 1127–1139.
131. Mundy-Bosse, B. L., Scoville, S. D., Chen, L., McConnell, K., Mao, H. C., Ahmed, E. H., Zorko, N. et al., MicroRNA-29b mediates altered innate immune development in acute leukemia. J. Clin. Invest. 2016. 126: 4404–4416.
132. Cichocki, F., Valamehr, B., Bjordahl, R., Zhang, B., Rezner, B., Rogers, P., Gaidarova, S. et al., GSK 3 inhibition drives maturation of NK cells and enhances their antitumor activity. Cancer Res. 2017. 77: 5664–5675.
133. Berrien-Elliott, M. M., Yuan, J., Swier, L. E., Jackson, S. R., Chen, C. L., Donlin, M. J. and Teague, R. M., Checkpoint blockade immunotherapy relies on T-bet but not Eomes to induce effector function in tumor-infiltrating CD8+ T cells. Cancer Immunol. Res. 2015. 3: 116–124.
134. McLane, L. M., Banerjee, P. P., Cosma, G. L., Makedonas, G., Wherry, E. J., Orange, J. S. and Betts, M. R., Differential localization of T-bet and Eomes in CD8 T cell memory populations. J. Immunol. 2013. 190: 3207–3215.
135. Conlon, F. L., Fairclough, L., Price, B. M., Casey, E. S. and Smith, J. C., Determinants of T box protein specificity. Dev. Camb. Engl. 2001. 128: 3749–3758.