The Helix-Loop-Helix Protein ID2 Governs NK Cell Fate by Tuning Their Sensitivity to Interleukin-15

Immunity

Volumn 44, Issue 1, 2016, Pages 103-115

  Delconte, Rebecca B ^a,b   Shi, Wei ^a,b   Sathe, Priyanka ^a,b   Ushiki, Takashi ^a,b   Seillet, Cyril ^a,b   Minnich, Martina ^c   Kolesnik, Tatiana B ^a,b   Rankin, Lucille C ^a,b   Mielke, Lisa A ^a,b   Zhang, Jian Guo ^a,b   Busslinger, Meinrad ^c   Smyth, Mark J ^d,e   Hutchinson, Dana S ^f   Nutt, Stephen L ^a,b   Nicholson, Sandra E ^a,b   Alexander, Warren S ^a,b   Corcoran, Lynn M ^a,b   Vivier, Eric ^g,h   Belz, Gabrielle T ^a   Carotta, Sebastian ^a,i   Huntington, Nicholas D ^a   more..

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^d QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^e UNIVERSITY OF QUEENSLAND   (Australia)

^f MONASH UNIVERSITY   (Australia)

^g AIX MARSEILLE UNIVERSITY   (France)

^h ASSISTANCE PUBLIQUE HÔPITAUX DE MARSEILLE   (France)

ⁱ Boehringer Ingelheim RCV   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

HELIX LOOP HELIX PROTEIN; INHIBITOR OF DIFFERENTIATION 2; INTERLEUKIN 15; INTERLEUKIN 15 RECEPTOR; IDB2 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FATE; CELL MATURATION; CONTROLLED STUDY; GENE; GENE TARGETING; HOMEOSTASIS; ID2 GENE; MOUSE; NATURAL KILLER CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RECEPTOR UPREGULATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SOCS3 GENE; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; CYTOLOGY; FEMALE; FLOW CYTOMETRY; IMMUNOLOGY; MALE; METABOLISM; MUTANT MOUSE STRAIN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; FEMALE; FLOW CYTOMETRY; INHIBITOR OF DIFFERENTIATION PROTEIN 2; INTERLEUKIN-15; KILLER CELLS, NATURAL; MALE; MICE; MICE, MUTANT STRAINS; RECEPTORS, INTERLEUKIN-15; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS;

EID: 84958841305     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2015.12.007     Document Type: Article

References (52)

1. Alexander W.S., Starr R., Fenner J.E., Scott C.L., Handman E., Sprigg N.S., Corbin J.E., Cornish A.L., Darwiche R., Owczarek C.M., et al. SOCS1 is a critical inhibitor of interferon gamma signaling and prevents the potentially fatal neonatal actions of this cytokine. Cell 1999, 98:597-608.
2. Bezman N.A., Kim C.C., Sun J.C., Min-Oo G., Hendricks D.W., Kamimura Y., Best J.A., Goldrath A.W., Lanier L.L. Molecular definition of the identity and activation of natural killer cells. Nat. Immunol. 2012, 13:1000-1009. Immunological Genome Project Consortium.
3. Boos M.D., Yokota Y., Eberl G., Kee B.L. Mature natural killer cell and lymphoid tissue-inducing cell development requires Id2-mediated suppression of E protein activity. J. Exp. Med. 2007, 204:1119-1130.
4. Boyman O., Kovar M., Rubinstein M.P., Surh C.D., Sprent J. Selective stimulation of T cell subsets with antibody-cytokine immune complexes. Science 2006, 311:1924-1927.
5. Carotta S., Dakic A., D'Amico A., Pang S.H., Greig K.T., Nutt S.L., Wu L. The transcription factor PU.1 controls dendritic cell development and Flt3 cytokine receptor expression in a dose-dependent manner. Immunity 2010, 32:628-641.
6. Carotta S., Pang S.H., Nutt S.L., Belz G.T. Identification of the earliest NK-cell precursor in the mouse BM. Blood 2011, 117:5449-5452.
7. Carson W.E., Giri J.G., Lindemann M.J., Linett M.L., Ahdieh M., Paxton R., Anderson D., Eisenmann J., Grabstein K., Caligiuri M.A. Interleukin (IL) 15 is a novel cytokine that activates human natural killer cells via components of the IL-2 receptor. J. Exp. Med. 1994, 180:1395-1403.
8. Constantinides M.G., McDonald B.D., Verhoef P.A., Bendelac A. A committed precursor to innate lymphoid cells. Nature 2014, 508:397-401.
9. Croker B.A., Krebs D.L., Zhang J.G., Wormald S., Willson T.A., Stanley E.G., Robb L., Greenhalgh C.J., Förster I., Clausen B.E., et al. SOCS3 negatively regulates IL-6 signaling in vivo. Nat. Immunol. 2003, 4:540-545.
10. de Boer J., Williams A., Skavdis G., Harker N., Coles M., Tolaini M., Norton T., Williams K., Roderick K., Potocnik A.J., Kioussis D. Transgenic mice with hematopoietic and lymphoid specific expression of Cre. Eur. J. Immunol. 2003, 33:314-325.
11. Ephrussi A., Church G.M., Tonegawa S., Gilbert W. B lineage--specific interactions of an immunoglobulin enhancer with cellular factors in vivo. Science 1985, 227:134-140.
12. Firth M.A., Madera S., Beaulieu A.M., Gasteiger G., Castillo E.F., Schluns K.S., Kubo M., Rothman P.B., Vivier E., Sun J.C. Nfil3-independent lineage maintenance and antiviral response of natural killer cells. J. Exp. Med. 2013, 210:2981-2990.
13. Gascoyne D.M., Long E., Veiga-Fernandes H., de Boer J., Williams O., Seddon B., Coles M., Kioussis D., Brady H.J. The basic leucine zipper transcription factor E4BP4 is essential for natural killer cell development. Nat. Immunol. 2009, 10:1118-1124.
14. Geiger T.L., Abt M.C., Gasteiger G., Firth M.A., O'Connor M.H., Geary C.D., O'Sullivan T.E., van den Brink M.R., Pamer E.G., Hanash A.M., Sun J.C. Nfil3 is crucial for development of innate lymphoid cells and host protection against intestinal pathogens. J. Exp. Med. 2014, 211:1723-1731.
15. Gilfillan S., Chan C.J., Cella M., Haynes N.M., Rapaport A.S., Boles K.S., Andrews D.M., Smyth M.J., Colonna M. DNAM-1 promotes activation of cytotoxic lymphocytes by nonprofessional antigen-presenting cells and tumors. J. Exp. Med. 2008, 205:2965-2973.
16. Glaser S.P., Lee E.F., Trounson E., Bouillet P., Wei A., Fairlie W.D., Izon D.J., Zuber J., Rappaport A.R., Herold M.J., et al. Anti-apoptotic Mcl-1 is essential for the development and sustained growth of acute myeloid leukemia. Genes Dev. 2012, 26:120-125.
17. Guo X., Liang Y., Zhang Y., Lasorella A., Kee B.L., Fu Y.X. Innate lymphoid cells control early colonization resistance against intestinal pathogens through ID2-dependent regulation of the microbiota. Immunity 2015, 42:731-743.
18. Held W., Kunz B., Lowin-Kropf B., van de Wetering M., Clevers H. Clonal acquisition of the Ly49A NK cell receptor is dependent on the trans-acting factor TCF-1. Immunity 1999, 11:433-442.
19. Henthorn P., Kiledjian M., Kadesch T. Two distinct transcription factors that bind the immunoglobulin enhancer microE5/kappa 2 motif. Science 1990, 247:467-470.
20. Herold M.J., Stuchbery R., Mérino D., Willson T., Strasser A., Hildeman D., Bouillet P. Impact of conditional deletion of the pro-apoptotic BCL-2 family member BIM in mice. Cell Death Dis. 2014, 5:e1446.
21. Holmes M.L., Huntington N.D., Thong R.P., Brady J., Hayakawa Y., Andoniou C.E., Fleming P., Shi W., Smyth G.K., Degli-Esposti M.A., et al. Peripheral natural killer cell maturation depends on the transcription factor Aiolos. EMBO J. 2014, 33:2721-2734.
22. Hoyler T., Klose C.S., Souabni A., Turqueti-Neves A., Pfeifer D., Rawlins E.L., Voehringer D., Busslinger M., Diefenbach A. The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells. Immunity 2012, 37:634-648.
23. Huntington N.D., Puthalakath H., Gunn P., Naik E., Michalak E.M., Smyth M.J., Tabarias H., Degli-Esposti M.A., Dewson G., Willis S.N., et al. Interleukin 15-mediated survival of natural killer cells is determined by interactions among Bim, Noxa and Mcl-1. Nat. Immunol. 2007, 8:856-863.
24. Huntington N.D., Tabarias H., Fairfax K., Brady J., Hayakawa Y., Degli-Esposti M.A., Smyth M.J., Tarlinton D.M., Nutt S.L. NK cell maturation and peripheral homeostasis is associated with KLRG1 up-regulation. J. Immunol. 2007, 178:4764-4770.
25. Huntington N.D., Vosshenrich C.A., Di Santo J.P. Developmental pathways that generate natural-killer-cell diversity in mice and humans. Nat. Rev. Immunol. 2007, 7:703-714.
26. Jackson J.T., Hu Y., Liu R., Masson F., D'Amico A., Carotta S., Xin A., Camilleri M.J., Mount A.M., Kallies A., et al. Id2 expression delineates differential checkpoints in the genetic program of CD8α+ and CD103+ dendritic cell lineages. EMBO J. 2011, 30:2690-2704.
27. Kennedy M.K., Glaccum M., Brown S.N., Butz E.A., Viney J.L., Embers M., Matsuki N., Charrier K., Sedger L., Willis C.R., 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.
28. Klose C.S., Diefenbach A. Transcription factors controlling innate lymphoid cell fate decisions. Curr. Top. Microbiol. Immunol. 2014, 381:215-255.
29. Kühn R., Schwenk F., Aguet M., Rajewsky K. Inducible gene targeting in mice. Science 1995, 269:1427-1429.
30. Lin Y.Y., Jones-Mason M.E., Inoue M., Lasorella A., Iavarone A., Li Q.J., Shinohara M.L., Zhuang Y. Transcriptional regulator Id2 is required for the CD4 T cell immune response in the development of experimental autoimmune encephalomyelitis. J. Immunol. 2012, 189:1400-1405.
31. Lodolce J.P., Boone D.L., Chai S., Swain R.E., Dassopoulos T., Trettin S., Ma A. IL-15 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation. Immunity 1998, 9:669-676.
32. Ma A., Koka R., Burkett P. Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annu. Rev. Immunol. 2006, 24:657-679.
33. Marçais A., Cherfils-Vicini J., Viant C., Degouve S., Viel S., Fenis A., Rabilloud J., Mayol K., Tavares A., Bienvenu J., et al. The metabolic checkpoint kinase mTOR is essential for IL-15 signaling during the development and activation of NK cells. Nat. Immunol. 2014, 15:749-757.
34. Masson F., Minnich M., Olshansky M., Bilic I., Mount A.M., Kallies A., Speed T.P., Busslinger M., Nutt S.L., Belz G.T. Id2-mediated inhibition of E2A represses memory CD8+ T cell differentiation. J. Immunol. 2013, 190:4585-4594.
35. Masson F., Ghisi M., Groom J.R., Kallies A., Seillet C., Johnstone R.W., Nutt S.L., Belz G.T. Id2 represses E2A-mediated activation of IL-10 expression in T cells. Blood 2014, 123:3420-3428.
36. Monticelli L.A., Yang Y., Knell J., D'Cruz L.M., Cannarile M.A., Engel I., Kronenberg M., Goldrath A.W. Transcriptional regulator Id2 controls survival of hepatic NKT cells. Proc. Natl. Acad. Sci. USA 2009, 106:19461-19466.
37. Murre C. Helix-loop-helix proteins and lymphocyte development. Nat. Immunol. 2005, 6:1079-1086.
38. Murre C., McCaw P.S., Baltimore D. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell 1989, 56:777-783.
39. Narni-Mancinelli E., Chaix J., Fenis A., Kerdiles Y.M., Yessaad N., Reynders A., Gregoire C., Luche H., Ugolini S., Tomasello E., et al. Fate mapping analysis of lymphoid cells expressing the NKp46 cell surface receptor. Proc. Natl. Acad. Sci. USA 2011, 108:18324-18329.
40. Prlic M., Blazar B.R., Farrar M.A., Jameson S.C. In vivo survival and homeostatic proliferation of natural killer cells. J. Exp. Med. 2003, 197:967-976.
41. Prlic M., Kamimura D., Bevan M.J. Rapid generation of a functional NK-cell compartment. Blood 2007, 110:2024-2026.
42. Quong M.W., Romanow W.J., Murre C. E protein function in lymphocyte development. Annu. Rev. Immunol. 2002, 20:301-322.
43. Sathe P., Delconte R.B., Souza-Fonseca-Guimaraes F., Seillet C., Chopin M., Vandenberg C.J., Rankin L.C., Mielke L.A., Vikstrom I., Kolesnik T.B., et al. Innate immunodeficiency following genetic ablation of Mcl1 in natural killer cells. Nat. Commun. 2014, 5:4539.
44. Seillet C., Huntington N.D., Gangatirkar P., Axelsson E., Minnich M., Brady H.J., Busslinger M., Smyth M.J., Belz G.T., Carotta S. Differential requirement for Nfil3 during NK cell development. J. Immunol. 2014, 192:2667-2676.
45. Seillet C., Rankin L.C., Groom J.R., Mielke L.A., Tellier J., Chopin M., Huntington N.D., Belz G.T., Carotta S. Nfil3 is required for the development of all innate lymphoid cell subsets. J. Exp. Med. 2014, 211:1733-1740.
46. Vikstrom I., Carotta S., Lüthje K., Peperzak V., Jost P.J., Glaser S., Busslinger M., Bouillet P., Strasser A., Nutt S.L., Tarlinton D.M. Mcl-1 is essential for germinal center formation and B cell memory. Science 2010, 330:1095-1099.
47. Wormald S., Zhang J.G., Krebs D.L., Mielke L.A., Silver J., Alexander W.S., Speed T.P., Nicola N.A., Hilton D.J. The comparative roles of suppressor of cytokine signaling-1 and -3 in the inhibition and desensitization of cytokine signaling. J. Biol. Chem. 2006, 281:11135-11143.
48. Xu W., Domingues R.G., Fonseca-Pereira D., Ferreira M., Ribeiro H., Lopez-Lastra S., Motomura Y., Moreira-Santos L., Bihl F., Braud V., et al. NFIL3 orchestrates the emergence of common helper innate lymphoid cell precursors. Cell Rep. 2015, 10:2043-2054.
49. Yang M., Li D., Chang Z., Yang Z., Tian Z., Dong Z. PDK1 orchestrates early NK cell development through induction of E4BP4 expression and maintenance of IL-15 responsiveness. J. Exp. Med. 2015, 212:253-265.
50. Yokota Y., Mansouri A., Mori S., Sugawara S., Adachi S., Nishikawa S., Gruss P. Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2. Nature 1999, 397:702-706.
51. Yu X., Wang Y., Deng M., Li Y., Ruhn K.A., Zhang C.C., Hooper L.V. The basic leucine zipper transcription factor NFIL3 directs the development of a common innate lymphoid cell precursor. eLife 2014, 3:3.
52. Zheng X., Wang Y., Wei H., Ling B., Sun R., Tian Z. Bcl-xL is associated with the anti-apoptotic effect of IL-15 on the survival of CD56(dim) natural killer cells. Mol. Immunol. 2008, 45:2559-2569.