Nfil3 is crucial for development of innate lymphoid cells and host protection against intestinal pathogens

Journal of Experimental Medicine

Volumn 211, Issue 9, 2014, Pages 1723-1731

  Geiger, Theresa L ^a   Abt, Michael C ^a   Gasteiger, Georg ^a   Firth, Matthew A ^a   O'Connor, Margaret H ^a   Geary, Clair D ^a   O'Sullivan, Timothy E ^a   van den Brink, Marcel R ^a,b   Pamer, Eric G ^a,b   Hanash, Alan M ^a   Sun, Joseph C ^a,b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; TRANSCRIPTION FACTOR NFIL3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL INFECTION; BONE MARROW; CELL LINEAGE; CELL MATURATION; CITROBACTER RODENTIUM; CLOSTRIDIUM DIFFICILE; CONTROLLED STUDY; HOST; INFECTION SENSITIVITY; INFLAMMATION; INNATE IMMUNITY; INTESTINE FLORA; INTRAABDOMINAL FAT; LUNG; LYMPHOID CELL; LYMPHOID TISSUE INDUCER LIKE CELL; MICROBIAL COMMUNITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TYPE 1 INNATE LYMPHOID CELL; TYPE 2 INNATE LYMPHOID CELL; TYPE 3 INNATE LYMPHOID CELL;

ANIMALS; ANTIGENS, LY; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL LINEAGE; CITROBACTER RODENTIUM; CLOSTRIDIUM DIFFICILE; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; INTESTINES; KILLER CELLS, NATURAL; LYMPHOCYTE SUBSETS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; RNA, MESSENGER; TRANSPLANTATION CHIMERA;

EID: 84906534108     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20140212     Document Type: Article

References (64)

1. Buffie, C.G., I. Jarchum, M. Equinda, L. Lipuma, A. Gobourne, A. Viale, C. Ubeda, J. Xavier, and E.G. Pamer. 2012. Profound alterations of intestinal microbiota following a single dose of clindamycin results in sustained susceptibility to Clostridium difficile-induced colitis. Infect. Immun. 80:62-73. http://dx.doi.org/10.1128/IAI.05496-11
2. Cella, M., A. Fuchs, W. Vermi, F. Facchetti, K. Otero, J.K. Lennerz, J.M. Doherty, J.C. Mills, and M. Colonna. 2009. A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature. 457:722-725. http://dx.doi.org/10.1038/nature07537
3. Cherrier, M., S. Sawa, and G. Eberl. 2012. Notch, Id2, and RORγt sequentially orchestrate the fetal development of lymphoid tissue inducer cells. J. Exp. Med. 209:729-740. http://dx.doi.org/10.1084/jem.20111594
4. Constantinides, M.G., B.D. McDonald, P.A. Verhoef, and A. Bendelac. 2014. A committed precursor to innate lymphoid cells. Nature. 508:397-401. http://dx.doi.org/10.1038/nature13047
5. Eberl, G., S. Marmon, M.J. Sunshine, P.D. Rennert, Y. Choi, and D.R. Littman. 2004. An essential function for the nuclear receptor RORγt in the generation of fetal lymphoid tissue inducer cells. Nat. Immunol. 5:64-73. http://dx.doi.org/10.1038/ni1022
6. Elinav, E., T. Strowig, A.L. Kau, J. Henao-Mejia, C.A. Thaiss, C.J. Booth, D.R. Peaper, J. Bertin, S.C. Eisenbarth, J.I. Gordon, and R.A. Flavell. 2011. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell. 145:745-757. http://dx.doi.org/10.1016/j.cell.2011.04.022
7. Fathman, J.W., D. Bhattacharya, M.A. Inlay, J. Seita, H. Karsunky, and I.L. Weissman. 2011. Identification of the earliest natural killer cell-committed progenitor in murine bone marrow. Blood. 118:5439-5447. http://dx.doi.org/10.1182/blood-2011-04-348912
8. Firth, M.A., S. Madera, A.M. Beaulieu, G. Gasteiger, E.F. Castillo, K.S. Schluns, M. Kubo, P.B. Rothman, E. Vivier, and J.C. Sun. 2013. Nfil3-independent lineage maintenance and antiviral response of natural killer cells. J. Exp. Med. 210:2981-2990. http://dx.doi.org/10.1084/jem.20130417
9. Fuchs, A., W. Vermi, J.S. Lee, S. Lonardi, S. Gilfillan, R.D. Newberry, M. Cella, and M. Colonna. 2013. Intraepithelial type 1 innate lymphoid cells are a unique subset of IL-12-and IL-15-responsive IFN-γ-producing cells. Immunity. 38:769-781. http://dx.doi.org/10.1016/j.immuni.2013.02.010
10. Furusawa, J., K. Moro, Y. Motomura, K. Okamoto, J. Zhu, H. Takayanagi, M. Kubo, and S. Koyasu. 2013. Critical role of p38 and GATA3 in natural helper cell function. J. Immunol. 191:1818-1826. http://dx.doi.org/10.4049/jimmunol.1300379
11. Gascoyne, D.M., E. Long, H. Veiga-Fernandes, J. de Boer, O. Williams, B. Seddon, M. Coles, D. Kioussis, and H.J. Brady. 2009. The basic leucine zipper transcription factor E4BP4 is essential for natural killer cell development. Nat. Immunol. 10:1118-1124. http://dx.doi.org/10.1038/ni.1787
12. Halim, T.Y., A. MacLaren, M.T. Romanish, M.J. Gold, K.M. McNagny, and F. Takei. 2012. Retinoic-acid-receptor-related orphan nuclear receptor α is required for natural helper cell development and allergic inflammation. Immunity. 37:463-474. http://dx.doi.org/10.1016/j.immuni.2012.06.012
13. Hanash, A.M., J.A. Dudakov, G. Hua, M.H. O'Connor, L.F. Young, N.V. Singer, M.L. West, R.R. Jenq, A.M. Holland, L.W. Kappel, et al. 2012. Interleukin-22 protects intestinal stem cells from immune-mediated tissue damage and regulates sensitivity to graft versus host disease. Immunity. 37:339-350. http://dx.doi.org/10.1016/j.immuni.2012.05.028
14. Hoyler, T., C.S. Klose, A. Souabni, A. Turqueti-Neves, D. Pfeifer, E.L. Rawlins, D. Voehringer, M. Busslinger, and A. Diefenbach. 2012. The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells. Immunity. 37:634-648. http://dx.doi.org/10.1016/j.immuni.2012.06.020
15. Ikushima, S., T. Inukai, T. Inaba, S.D. Nimer, J.L. Cleveland, and A.T. Look. 1997. Pivotal role for the NFIL3/E4BP4 transcription factor in interleukin 3-mediated survival of pro-B lymphocytes. Proc. Natl. Acad. Sci. USA. 94:2609-2614. http://dx.doi.org/10.1073/pnas.94.6.2609
16. Kamizono, S., G.S. Duncan, M.G. Seidel, A. Morimoto, K. Hamada, G. Grosveld, K. Akashi, E.F. Lind, J.P. Haight, P.S. Ohashi, et al. 2009. Nfil3/E4bp4 is required for the development and maturation of NK cells in vivo. J. Exp. Med. 206:2977-2986. http://dx.doi.org/10.1084/jem.20092176
17. Kashiwada, M., D.M. Levy, L. McKeag, K. Murray, A.J. Schroder, S.M. Canfield, G. Traver, and P.B. Rothman. 2010. IL-4-induced transcription factor NFIL3/E4BP4 controls IgE class switching. Proc. Natl. Acad. Sci. USA. 107:821-826. http://dx.doi.org/10.1073/pnas.0909235107
18. Kashiwada, M., S.L. Cassel, J.D. Colgan, and P.B. Rothman. 2011a. NFIL3/E4BP4 controls type 2 T helper cell cytokine expression. EMBO J. 30:2071-2082. http://dx.doi.org/10.1038/emboj.2011.111
19. + dendritic cell development. Blood. 117:6193-6197. http://dx.doi.org/10.1182/blood-2010-07-295873
20. Kelly, C.P., and J.T. LaMont. 2008. Clostridium difficile-more difficult than ever. N. Engl. J. Med. 359:1932-1940. http://dx.doi.org/10.1056/NEJMra0707500
21. Kiss, E.A., C. Vonarbourg, S. Kopfmann, E. Hobeika, D. Finke, C. Esser, and A. Diefenbach. 2011. Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science. 334:1561-1565. http://dx.doi.org/10.1126/science.1214914
22. + type 2 innate lymphoid cells. Proc. Natl. Acad. Sci. USA. 110:10240-10245. http://dx.doi.org/10.1073/pnas.1217158110
23. + innate lymphoid cells. Nature. 494:261-265. http://dx.doi.org/10.1038/nature11813
24. Klose, C.S., M. Flach, L. Mohle, L. Rogell, T. Hoyler, K. Ebert, C. Fabiunke, D. Pfeifer, V. Sexl, D. Fonseca-Pereira, et al. 2014. Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell. 157:340-356. http://dx.doi.org/10.1016/j.cell.2014.03.030
25. Kobayashi, T., K. Matsuoka, S.Z. Sheikh, H.Z. Elloumi, N. Kamada, T. Hisamatsu, J.J. Hansen, K.R. Doty, S.D. Pope, S.T. Smale, et al. 2011. NFIL3 is a regulator of IL-12 p40 in macrophages and mucosal immunity. J. Immunol. 186:4649-4655. http://dx.doi.org/10.4049/jimmunol.1003888
26. Kobayashi, T., E.C. Steinbach, S.M. Russo, K. Matsuoka, T. Nochi, N. Maharshak, L.B. Borst, B. Hostager, J.V. Garcia-Martinez, P.B. Rothman, et al. 2014. NFIL3-deficient mice develop microbiota-dependent, IL-12/23-driven spontaneous colitis. J. Immunol. 192:1918-1927. http://dx.doi.org/10.4049/jimmunol.1301819
27. Lee, J.S., M. Cella, K.G. McDonald, C. Garlanda, G.D. Kennedy, M. Nukaya, A. Mantovani, R. Kopan, C.A. Bradfield, R.D. Newberry, and M. Colonna. 2012. AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch. Nat. Immunol. 13:144-151. http://dx.doi.org/10.1038/ni.2187
28. Liang, H.E., R.L. Reinhardt, J.K. Bando, B.M. Sullivan, I.C. Ho, and R.M. Locksley. 2012. Divergent expression patterns of IL-4 and IL-13 define unique functions in allergic immunity. Nat. Immunol. 13:58-66. http://dx.doi.org/10.1038/ni.2182
29. Luci, C., A. Reynders, I.I. Ivanov, C. Cognet, L. Chiche, L. Chasson, J. Hardwigsen, E. Anguiano, J. Banchereau, D. Chaussabel, et al. 2009. Influence of the transcription factor RORγt on the development of NKp46+ cell populations in gut and skin. Nat. Immunol. 10:75-82. http://dx.doi.org/10.1038/ni.1681
30. Male, V., I. Nisoli, T. Kostrzewski, D.S. Allan, J.R. Carlyle, G.M. Lord, A. Wack, and H.J. Brady. 2014. The transcription factor E4bp4/Nfil3 controls commitment to the NK lineage and directly regulates Eomes and Id2 expression. J. Exp. Med. 211:635-642. http://dx.doi.org/10.1084/jem.20132398
31. + innate lymphocyte differentiation and protection in intestinal inflammation. J. Immunol. 191:4383-4391. http://dx.doi.org/10.4049/jimmunol.1301228
32. Mjosberg, J., J. Bernink, K. Golebski, J.J. Karrich, C.P. Peters, B. Blom, A.A. te Velde, W.J. Fokkens, C.M. van Drunen, and H. Spits. 2012. The transcription factor GATA3 is essential for the function of human type 2 innate lymphoid cells. Immunity. 37:649-659. http://dx.doi.org/10.1016/j.immuni.2012.08.015
33. Molofsky, A.B., J.C. Nussbaum, H.E. Liang, S.J. Van Dyken, L.E. Cheng, A. Mohapatra, A. Chawla, and R.M. Locksley. 2013. Innate lymphoid type 2 cells sustain visceral adipose tissue eosinophils and alternatively activated macrophages. J. Exp. Med. 210:535-549. http://dx.doi.org/10.1084/jem.20121964
34. + lymphoid cells. Nature. 463:540-544. http://dx.doi.org/10.1038/nature08636
35. + T cells. Nat. Immunol. 12:450-459. http://dx.doi.org/10.1038/ni.2020
36. 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
37. Nussbaum, J.C., S.J. Van Dyken, J. von Moltke, L.E. Cheng, A. Mohapatra, A.B. Molofsky, E.E. Thornton, M.F. Krummel, A. Chawla, H.E. Liang, and R.M. Locksley. 2013. Type 2 innate lymphoid cells control eosinophil homeostasis. Nature. 502:245-248. http://dx.doi.org/10.1038/nature12526
38. + innate lymphoid cells. Nat. Immunol. 12:949-958. http://dx.doi.org/10.1038/ni.2105
39. Qiu, J., J.J. Heller, X. Guo, Z.M. Chen, K. Fish, Y.X. Fu, and L. Zhou. 2012. The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells. Immunity. 36:92-104. http://dx.doi.org/10.1016/j.immuni.2011.11.011
40. Rankin, L.C., J.R. Groom, M. Chopin, M.J. Herold, J.A. Walker, L.A. Mielke, A.N. McKenzie, S. Carotta, S.L. Nutt, and G.T. Belz. 2013. The transcription factor T-bet is essential for the development of NKp46+ innate lymphocytes via the Notch pathway. Nat. Immunol. 14:389-395. http://dx.doi.org/10.1038/ni.2545
41. Rupnik, M., M.H. Wilcox, and D.N. Gerding. 2009. Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat. Rev. Microbiol. 7:526-536. http://dx.doi.org/10.1038/nrmicro2164
42. + cells. Nat. Immunol. 10:83-91. http://dx.doi.org/10.1038/ni.1684
43. Satoh-Takayama, N., C.A. Vosshenrich, S. Lesjean-Pottier, S. Sawa, M. Lochner, F. Rattis, J.J. Mention, K. Thiam, N. Cerf-Bensussan, O. Mandelboim, et al. 2008. Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity. 29:958-970. http://dx.doi.org/10.1016/j.immuni.2008.11.001
44. Satoh-Takayama, N., S. Lesjean-Pottier, P. Vieira, S. Sawa, G. Eberl, C.A. Vosshenrich, and J.P. Di Santo. 2010. IL-7 and IL-15 independently program the differentiation of intestinal CD3?NKp46+ cell subsets from Id2-dependent precursors. J. Exp. Med. 207:273-280. http://dx.doi.org/10.1084/jem.20092029
45. + innate lymphoid cells. Science. 330:665-669. http://dx.doi.org/10.1126/science.1194597
46. Sciume, G., K. Hirahara, H. Takahashi, A. Laurence, A.V. Villarino, K.L. Singleton, S.P. Spencer, C. Wilhelm, A.C. Poholek, G. Vahedi, et al. 2012. Distinct requirements for T-bet in gut innate lymphoid cells. J. Exp. Med. 209:2331-2338. http://dx.doi.org/10.1084/jem.20122097
47. + group 3 innate lymphoid cells. J. Exp. Med. 211:199-208. http://dx.doi.org/10.1084/jem.20131038
48. + lymphoid tissue-inducer cells promote innate immunity in the gut. Immunity. 34:122-134. http://dx.doi.org/10.1016/j.immuni.2010.12.009
49. Sonnenberg, G.F., L.A. Monticelli, T. Alenghat, T.C. Fung, N.A. Hutnick, J. Kunisawa, N. Shibata, S. Grunberg, R. Sinha, A.M. Zahm, et al. 2012. Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria. Science. 336:1321-1325. http://dx.doi.org/10.1126/science.1222551
50. Sonnenberg, G.F., J. Mjosberg, H. Spits, and D. Artis. 2013. SnapShot: innate lymphoid cells. Immunity. 39:622-622: e1. http://dx.doi.org/10.1016/j.immuni.2013.08.021
51. Spits, H., and T. Cupedo. 2012. Innate lymphoid cells: emerging insights in development, lineage relationships, and function. Annu. Rev. Immunol. 30:647-675. http://dx.doi.org/10.1146/annurev-immunol-020711-075053
52. Spits, H., and J.P. Di Santo. 2011. The expanding family of innate lymphoid cells: regulators and effectors of immunity and tissue remodeling. Nat. Immunol. 12:21-27. http://dx.doi.org/10.1038/ni.1962
53. Spits, H., D. Artis, M. Colonna, A. Diefenbach, J.P. Di Santo, G. Eberl, S. Koyasu, R.M. Locksley, A.N. McKenzie, R.E. Mebius, et al. 2013. Innate lymphoid cells-a proposal for uniform nomenclature. Nat. Rev. Immunol. 13:145-149. http://dx.doi.org/10.1038/nri3365
54. Spooner, C.J., J. Lesch, D. Yan, A.A. Khan, A. Abbas, V. Ramirez-Carrozzi, M. Zhou, R. Soriano, J. Eastham-Anderson, L. Diehl, et al. 2013. Specification of type 2 innate lymphocytes by the transcriptional determinant Gfi1. Nat. Immunol. 14:1229-1236. http://dx.doi.org/10.1038/ni.2743
55. 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
56. Ubeda, C., L. Lipuma, A. Gobourne, A. Viale, I. Leiner, M. Equinda, R. Khanin, and E.G. Pamer. 2012. Familial transmission rather than defective innate immunity shapes the distinct intestinal microbiota of TLR-deficient mice. J. Exp. Med. 209:1445-1456. http://dx.doi.org/10.1084/jem.20120504
57. Veldhoen, M., K. Hirota, A.M. Westendorf, J. Buer, L. Dumoutier, J.C. Renauld, and B. Stockinger. 2008. The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature. 453:106-109. http://dx.doi.org/10.1038/nature06881
58. Walker, J.A., J.L. Barlow, and A.N. McKenzie. 2013. Innate lymphoid cells-how did we miss them? Nat. Rev. Immunol. 13:75-87. http://dx.doi.org/10.1038/nri3349
59. Wong, S.H., J.A. Walker, H.E. Jolin, L.F. Drynan, E. Hams, A. Camelo, J.L. Barlow, D.R. Neill, V. Panova, U. Koch, et al. 2012. Transcription factor RORα is critical for nuocyte development. Nat. Immunol. 13:229-236. http://dx.doi.org/10.1038/ni.2208
60. Yang, Q., S.A. Saenz, D.A. Zlotoff, D. Artis, and A. Bhandoola. 2011. Cutting edge: Natural helper cells derive from lymphoid progenitors. J. Immunol. 187:5505-5509. http://dx.doi.org/10.4049/jimmunol.1102039
61. Yang, Q., L.A. Monticelli, S.A. Saenz, A.W. Chi, G.F. Sonnenberg, J. Tang, M.E. De Obaldia, W. Bailis, J.L. Bryson, K. Toscano, et al. 2013. T cell factor 1 is required for group 2 innate lymphoid cell generation. Immunity. 38:694-704. http://dx.doi.org/10.1016/j.immuni.2012.12.003
62. Yokota, Y., A. Mansouri, S. Mori, S. Sugawara, S. Adachi, S. Nishikawa, and P. Gruss. 1999. Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2. Nature. 397:702-706. http://dx.doi.org/10.1038/17812
63. Yu, X., D. Rollins, K.A. Ruhn, J.J. Stubblefield, C.B. Green, M. Kashiwada, P.B. Rothman, J.S. Takahashi, and L.V. Hooper. 2013. TH17 cell differentiation is regulated by the circadian clock. Science. 342:727-730. http://dx.doi.org/10.1126/science.1243884
64. Zhang, W., J. Zhang, M. Kornuc, K. Kwan, R. Frank, and S.D. Nimer. 1995. Molecular cloning and characterization of NF-IL3A, a transcriptional activator of the human interleukin-3 promoter. Mol. Cell. Biol. 15:6055-6063.