The development of adult innate lymphoid cells

Current Opinion in Immunology

Volumn 39, Issue , 2016, Pages 114-120

  Yang, Qi ^a,b   Bhandoola, Avinash ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PATTERN RECOGNITION RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PLZF; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ADULT ANIMAL; BONE MARROW; CELL FATE; CELL MATURATION; COMMON HELPER INNATE LYMPHOID CELL PROGENITOR; EXPERIMENTAL MOUSE; GENE; HUMAN; LYMPHOCYTE FUNCTION; LYMPHOID CELL; NATURAL KILLER CELL; NONHUMAN; RECOMBINATION ACTIVATING GENE; REVIEW; STEM CELL; T LYMPHOCYTE; ANIMAL; CYTOLOGY; IMMUNOLOGY; INNATE IMMUNITY; LYMPHOID PROGENITOR CELL; PHYSIOLOGY;

ANIMALS; HUMANS; IMMUNITY, INNATE; KILLER CELLS, NATURAL; LYMPHOID PROGENITOR CELLS; T-LYMPHOCYTES;

EID: 84957592868     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2016.01.006     Document Type: Review

References (87)

1. Eberl G., Di Santo J.P., Vivier E. The brave new world of innate lymphoid cells. Nat Immunol 2015, 16:1-5.
2. De Obaldia M.E., Bhandoola A. Transcriptional regulation of innate and adaptive lymphocyte lineages. Annu Rev Immunol 2015, 33:607-642.
3. Artis D., Spits H. The biology of innate lymphoid cells. Nature 2015, 517:293-301.
4. Yang Q., Jeremiah Bell J., Bhandoola A. T-cell lineage determination. Immunol Rev 2010, 238:12-22.
5. Spits H., Artis D., Colonna M., Diefenbach A., Di Santo J.P., Eberl G., Koyasu S., Locksley R.M., McKenzie A.N., Mebius R.E., et al. Innate lymphoid cells - a proposal for uniform nomenclature. Nat Rev Immunol 2012, 13:145-149.
6. Wong S.H., Walker J.A., Jolin H.E., Drynan L.F., Hams E., Camelo A., Barlow J.L., Neill D.R., Panova V., Koch U., et al. Transcription factor RORalpha is critical for nuocyte development. Nat Immunol 2012.
7. Yang Q., Saenz S.A., Zlotoff D.A., Artis D., Bhandoola A. Cutting edge: natural helper cells derive from lymphoid progenitors. J Immunol 2011, 187:5505-5509.
8. Possot C., Schmutz S., Chea S., Boucontet L., Louise A., Cumano A., Golub R. Notch signaling is necessary for adult, but not fetal, development of RORgammat(+) innate lymphoid cells. Nat Immunol 2011, 12:949-958.
9. Constantinides M.G., Gudjonson H., McDonald B.D., Ishizuka I.E., Verhoef P.A., Dinner A.R., Bendelac A. PLZF expression maps the early stages of ILC1 lineage development. Proc Natl Acad Sci U S A 2015, 112:5123-5128.
10. Constantinides M.G., McDonald B.D., Verhoef P.A., Bendelac A. A committed precursor to innate lymphoid cells. Nature 2014, 508:397-401.
11. Klose C.S., Flach M., Mohle L., Rogell L., Hoyler T., Ebert K., Fabiunke C., Pfeifer D., Sexl V., Fonseca-Pereira D., et al. Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell 2014, 157:340-356.
12. Rosmaraki E.E., Douagi I., Roth C., Colucci F., Cumano A., Di Santo J.P. Identification of committed NK cell progenitors in adult murine bone marrow. Eur J Immunol 2001, 31:1900-1909.
13. 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.
14. Halim T.Y., MacLaren A., Romanish M.T., Gold M.J., McNagny K.M., Takei F. Retinoic-acid-receptor-related orphan nuclear receptor alpha is required for natural helper cell development and allergic inflammation. Immunity 2012, 37:463-474.
15. 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:e04406.
16. Cherrier M., Sawa S., Eberl G. Notch, Id2, and RORgammat sequentially orchestrate the fetal development of lymphoid tissue inducer cells. J Exp Med 2012, 209:729-740.
17. Yang Q., Li F., Harly C., Xing S., Ye L., Xia X., Wang H., Wang X., Yu S., Zhou X., et al. TCF-1 upregulation identifies early innate lymphoid progenitors in the bone marrow. Nat Immunol 2015.
18. Paclik D., Stehle C., Lahmann A., Hutloff A., Romagnani C. ICOS regulates the pool of group 2 innate lymphoid cells under homeostatic and inflammatory conditions in mice. Eur J Immunol 2015.
19. Maazi H., Patel N., Sankaranarayanan I., Suzuki Y., Rigas D., Soroosh P., Freeman G.J., Sharpe A.H., Akbari O. ICOS:ICOS-ligand interaction is required for type 2 innate lymphoid cell function, homeostasis, and induction of airway hyperreactivity. Immunity 2015, 42:538-551.
20. Kamachi F., Isshiki T., Harada N., Akiba H., Miyake S. ICOS promotes group 2 innate lymphoid cell activation in lungs. Biochem Biophys Res Commun 2015, 463:739-745.
21. Wang X.F., Lei Y., Chen M., Chen C.B., Ren H., Shi T.D. PD-1/PDL1 and CD28/CD80 pathways modulate natural killer T cell function to inhibit hepatitis B virus replication. J Viral Hepat 2013, 20(Suppl. 1):27-39.
22. Terme M., Ullrich E., Aymeric L., Meinhardt K., Desbois M., Delahaye N., Viaud S., Ryffel B., Yagita H., Kaplanski G., et al. IL-18 induces PD-1-dependent immunosuppression in cancer. Cancer Res 2012, 71:5393-5399.
23. Benson D.M., Bakan C.E., Mishra A., Hofmeister C.C., Efebera Y., Becknell B., Baiocchi R.A., Zhang J., Yu J., Smith M.K., et al. The PD-1/PD-L1 axis modulates the natural killer cell versus multiple myeloma effect: a therapeutic target for CT-011, a novel monoclonal anti-PD-1 antibody. Blood 2010, 116:2286-2294.
24. 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.
25. Steinke F.C., Yu S., Zhou X., He B., Yang W., Zhou B., Kawamoto H., Zhu J., Tan K., Xue H.H. TCF-1 and LEF-1 act upstream of Th-POK to promote the CD4(+) T cell fate and interact with Runx3 to silence Cd4 in CD8(+) T cells. Nat Immunol 2014, 15:646-656.
26. Yu S., Zhou X., Steinke F.C., Liu C., Chen S.C., Zagorodna O., Jing X., Yokota Y., Meyerholz D.K., Mullighan C.G., et al. The TCF-1 and LEF-1 transcription factors have cooperative and opposing roles in T cell development and malignancy. Immunity 2012, 37:813-826.
27. Weber B.N., Chi A.W., Chavez A., Yashiro-Ohtani Y., Yang Q., Shestova O., Bhandoola A. A critical role for TCF-1 in T-lineage specification and differentiation. Nature 2011, 476:63-68.
28. Wang R., Xie H., Huang Z., Ma J., Fang X., Ding Y., Sun Z. T cell factor 1 regulates thymocyte survival via a RORgammat-dependent pathway. J Immunol 2011, 187:5964-5973.
29. Germar K., Dose M., Konstantinou T., Zhang J., Wang H., Lobry C., Arnett K.L., Blacklow S.C., Aifantis I., Aster J.C., et al. T-cell factor 1 is a gatekeeper for T-cell specification in response to Notch signaling. Proc Natl Acad Sci U S A 2011, 108:20060-20065.
30. Yang Q., Monticelli L.A., Saenz S.A., Chi A.W., Sonnenberg G.F., Tang J., De Obaldia M.E., Bailis W., Bryson J.L., Toscano K., et al. T cell factor 1 is required for group 2 innate lymphoid cell generation. Immunity 2013, 38:694-704.
31. Mielke L.A., Groom J.R., Rankin L.C., Seillet C., Masson F., Putoczki T., Belz G.T. TCF-1 controls ILC2 and NKp46+RORgammat+ innate lymphocyte differentiation and protection in intestinal inflammation. J Immunol 2013, 191:4383-4391.
32. Yagi R., Zhong C., Northrup D.L., Yu F., Bouladoux N., Spencer S., Hu G., Barron L., Sharma S., Nakayama T., et al. The transcription factor GATA3 is critical for the development of all IL-7Ralpha-expressing innate lymphoid cells. Immunity 2014, 40:378-388.
33. Serafini N., Klein Wolterink R.G., Satoh-Takayama N., Xu W., Vosshenrich C.A., Hendriks R.W., Di Santo J.P. Gata3 drives development of RORgammat+ group 3 innate lymphoid cells. J Exp Med 2014, 211:199-208.
34. Klein Wolterink R.G., Serafini N., van Nimwegen M., Vosshenrich C.A., de Bruijn M.J., Fonseca Pereira D., Veiga Fernandes H., Hendriks R.W., Di Santo J.P. Essential, dose-dependent role for the transcription factor Gata3 in the development of IL-5+ and IL-13+ type 2 innate lymphoid cells. Proc Natl Acad Sci U S A 2013, 110:10240-10245.
35. Mjosberg J., Bernink J., Golebski K., Karrich J.J., Peters C.P., Blom B., te Velde A.A., Fokkens W.J., van Drunen C.M., Spits H. The transcription factor GATA3 is essential for the function of human type 2 innate lymphoid cells. Immunity 2012, 37:649-659.
36. Samson S.I., Richard O., Tavian M., Ranson T., Vosshenrich C.A., Colucci F., Buer J., Grosveld F., Godin I., Di Santo J.P. GATA-3 promotes maturation, IFN-gamma production, and liver-specific homing of NK cells. Immunity 2003, 19:701-711.
37. Barton K., Muthusamy N., Fischer C., Ting C.N., Walunas T.L., Lanier L.L., Leiden J.M. The Ets-1 transcription factor is required for the development of natural killer cells in mice. Immunity 1998, 9:555-563.
38. Fathman J.W., Bhattacharya D., Inlay M.A., Seita J., Karsunky H., Weissman I.L. Identification of the earliest natural killer cell-committed progenitor in murine bone marrow. Blood 2011, 118:5439-5447.
39. Ramirez K., Chandler K.J., Spaulding C., Zandi S., Sigvardsson M., Graves B.J., Kee B.L. Gene deregulation and chronic activation in natural killer cells deficient in the transcription factor ETS1. Immunity 2012, 36:921-932.
40. Doherty T.A., Khorram N., Chang J.E., Kim H.K., Rosenthal P., Croft M., Broide D.H. STAT6 regulates natural helper cell proliferation during lung inflammation initiated by Alternaria. Am J Physiol Lung Cell Mol Physiol 2012, 303:L577-L588.
41. Li P., Burke S., Wang J., Chen X., Ortiz M., Lee S.C., Lu D., Campos L., Goulding D., Ng B.L., et al. Reprogramming of T cells to natural killer-like cells upon Bcl11b deletion. Science 2010, 329:85-89.
42. Li L., Leid M., Rothenberg E.V. An early T cell lineage commitment checkpoint dependent on the transcription factor Bcl11b. Science 2010, 329:89-93.
43. Ikawa T., Hirose S., Masuda K., Kakugawa K., Satoh R., Shibano-Satoh A., Kominami R., Katsura Y., Kawamoto H. An essential developmental checkpoint for production of the T cell lineage. Science 2010, 329:93-96.
44. Califano D., Cho J.J., Uddin M.N., Lorentsen K.J., Yang Q., Bhandoola A., Li H., Avram D. Transcription factor Bcl11b controls identity and function of mature type 2 innate lymphoid cells. Immunity 2015, 43:354-368.
45. Zhong C., Zhu J. Bcl11b drives the birth of ILC2 innate lymphocytes. J Exp Med 2015, 212:828.
46. Yu Y., Wang C., Clare S., Wang J., Lee S.C., Brandt C., Burke S., Lu L., He D., Jenkins N.A., et al. The transcription factor Bcl11b is specifically expressed in group 2 innate lymphoid cells and is essential for their development. J Exp Med 2015, 212:865-874.
47. Walker J.A., Oliphant C.J., Englezakis A., Yu Y., Clare S., Rodewald H.R., Belz G., Liu P., Fallon P.G., McKenzie A.N. Bcl11b is essential for group 2 innate lymphoid cell development. J Exp Med 2015, 212:875-882.
48. Xu L., Cao Y., Xie Z., Huang Q., Bai Q., Yang X., He R., Hao Y., Wang H., Zhao T., et al. The transcription factor TCF-1 initiates the differentiation of TFH cells during acute viral infection. Nat Immunol 2015, 16:991-999.
49. Steinke F.C., Xue H.H. From inception to output, Tcf1 and Lef1 safeguard development of T cells and innate immune cells. Immunol Res 2015, 59:45-55.
50. Choi Y.S., Gullicksrud J.A., Xing S., Zeng Z., Shan Q., Li F., Love P.E., Peng W., Xue H.H., Crotty S. LEF-1 and TCF-1 orchestrate TFH differentiation by regulating differentiation circuits upstream of the transcriptional repressor Bcl6. Nat Immunol 2015, 16:980-990.
51. Vivier E., Nunes J.A., Vely F. Natural killer cell signaling pathways. Science 2004, 306:1517-1519.
52. Lanier L.L. Natural killer cell receptor signaling. Curr Opin Immunol 2003, 15:308-314.
53. De Obaldia M.E., Bell J.J., Bhandoola A. Early T-cell progenitors are the major granulocyte precursors in the adult mouse thymus. Blood 2013, 121:64-71.
54. 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.
55. 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.
56. 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., et al. Nfil3 is crucial for development of innate lymphoid cells and host protection against intestinal pathogens. J Exp Med 2014, 211:1723-1731.
57. Male V., Nisoli I., Kostrzewski T., Allan D.S., Carlyle J.R., Lord G.M., Wack A., Brady H.J. 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.
58. Moro K., Yamada T., Tanabe M., Takeuchi T., Ikawa T., Kawamoto H., Furusawa J., Ohtani M., Fujii H., Koyasu S. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature 2010, 463:540-544.
59. 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.
60. Morrow M.A., Mayer E.W., Perez C.A., Adlam M., Siu G. Overexpression of the Helix-Loop-Helix protein Id2 blocks T cell development at multiple stages. Mol Immunol 1999, 36:491-503.
61. 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.
62. Seehus C.R., Aliahmad P., de la Torre B., Iliev I.D., Spurka L., Funari V.A., Kaye J. The development of innate lymphoid cells requires TOX-dependent generation of a common innate lymphoid cell progenitor. Nat Immunol 2015, 16:599-608.
63. Aliahmad P., de la Torre B., Kaye J. Shared dependence on the DNA-binding factor TOX for the development of lymphoid tissue-inducer cell and NK cell lineages. Nat Immunol 2010, 11:945-952.
64. Aliahmad P., Kaye J. Development of all CD4 T lineages requires nuclear factor TOX. J Exp Med 2008, 205:245-256.
65. Welner R.S., Esplin B.L., Garrett K.P., Pelayo R., Luche H., Fehling H.J., Kincade P.W. Asynchronous RAG-1 expression during B lymphopoiesis. J Immunol 2009, 183:7768-7777.
66. Igarashi H., Gregory S.C., Yokota T., Sakaguchi N., Kincade P.W. Transcription from the RAG1 locus marks the earliest lymphocyte progenitors in bone marrow. Immunity 2002, 17:117-130.
67. Karo J.M., Schatz D.G., Sun J.C. The RAG recombinase dictates functional heterogeneity and cellular fitness in natural killer cells. Cell 2014, 159:94-107.
68. Ji Y., Resch W., Corbett E., Yamane A., Casellas R., Schatz D.G. The in vivo pattern of binding of RAG1 and RAG2 to antigen receptor loci. Cell 2010, 141:419-431.
69. Sun J.C., Beilke J.N., Lanier L.L. Adaptive immune features of natural killer cells. Nature 2009, 457:557-561.
70. O'Leary J.G., Goodarzi M., Drayton D.L., von Andrian U.H. T cell- and B cell-independent adaptive immunity mediated by natural killer cells. Nat Immunol 2006, 7:507-516.
71. Montaldo E., Teixeira-Alves L.G., Glatzer T., Durek P., Stervbo U., Hamann W., Babic M., Paclik D., Stolzel K., Grone J., et al. Human RORgammat(+)CD34(+) cells are lineage-specified progenitors of group 3 RORgammat(+) innate lymphoid cells. Immunity 2014, 41:988-1000.
72. Esplin B.L., Shimazu T., Welner R.S., Garrett K.P., Nie L., Zhang Q., Humphrey M.B., Yang Q., Borghesi L.A., Kincade P.W. Chronic exposure to a TLR ligand injures hematopoietic stem cells. J Immunol 2010, 186:5367-5375.
73. Welner R.S., Pelayo R., Nagai Y., Garrett K.P., Wuest T.R., Carr D.J., Borghesi L.A., Farrar M.A., Kincade P.W. Lymphoid precursors are directed to produce dendritic cells as a result of TLR9 ligation during herpes infection. Blood 2008, 112:3753-3761.
74. Nagai Y., Garrett K.P., Ohta S., Bahrun U., Kouro T., Akira S., Takatsu K., Kincade P.W. Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment. Immunity 2006, 24:801-812.
75. Spencer S.P., Wilhelm C., Yang Q., Hall J.A., Bouladoux N., Boyd A., Nutman T.B., Urban J.F., Wang J., Ramalingam T.R., et al. Adaptation of innate lymphoid cells to a micronutrient deficiency promotes type 2 barrier immunity. Science 2014, 343:432-437.
76. van de Pavert S.A., Ferreira M., Domingues R.G., Ribeiro H., Molenaar R., Moreira-Santos L., Almeida F.F., Ibiza S., Barbosa I., Goverse G., et al. Maternal retinoids control type 3 innate lymphoid cells and set the offspring immunity. Nature 2014, 508:123-127.
77. Qiu J., Heller J.J., Guo X., Chen Z.M., Fish K., Fu Y.X., Zhou L. The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells. Immunity 2012, 36:92-104.
78. Lee J.S., Cella M., McDonald K.G., Garlanda C., Kennedy G.D., Nukaya M., Mantovani A., Kopan R., Bradfield C.A., Newberry R.D., et al. AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch. Nat Immunol 2011, 13:144-151.
79. Kiss E.A., Vonarbourg C., Kopfmann S., Hobeika E., Finke D., Esser C., Diefenbach A. Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science 2011, 334:1561-1565.
80. Reynders A., Yessaad N., Vu Manh T.P., Dalod M., Fenis A., Aubry C., Nikitas G., Escaliere B., Renauld J.C., Dussurget O., et al. Identity, regulation and in vivo function of gut NKp46+RORgammat+ and NKp46+RORgammat- lymphoid cells. EMBO J 2011, 30:2934-2947.
81. Crellin N.K., Trifari S., Kaplan C.D., Cupedo T., Spits H. Human NKp44+IL-22+ cells and LTi-like cells constitute a stable RORC+ lineage distinct from conventional natural killer cells. J Exp Med 2010, 207:281-290.
82. Luci C., Reynders A., Ivanov I.I., Cognet C., Chiche L., Chasson L., Hardwigsen J., Anguiano E., Banchereau J., Chaussabel D., et al. Influence of the transcription factor RORgammat on the development of NKp46+ cell populations in gut and skin. Nat Immunol 2009, 10:75-82.
83. Cella M., Fuchs A., Vermi W., Facchetti F., Otero K., Lennerz J.K., Doherty J.M., Mills J.C., Colonna M. A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature 2009, 457:722-725.
84. Satoh-Takayama N., Vosshenrich C.A., Lesjean-Pottier S., Sawa S., Lochner M., Rattis F., Mention J.J., Thiam K., Cerf-Bensussan N., Mandelboim O., et al. Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity 2008, 29:958-970.
85. Kim H.Y., Lee H.J., Chang Y.J., Pichavant M., Shore S.A., Fitzgerald K.A., Iwakura Y., Israel E., Bolger K., Faul J., et al. Interleukin-17-producing innate lymphoid cells and the NLRP3 inflammasome facilitate obesity-associated airway hyperreactivity. Nat Med 2014, 20:54-61.
86. Dudakov J.A., Hanash A.M., Jenq R.R., Young L.F., Ghosh A., Singer N.V., West M.L., Smith O.M., Holland A.M., Tsai J.J., et al. Interleukin-22 drives endogenous thymic regeneration in mice. Science 2012, 336:91-95.
87. Vosshenrich C.A., Garcia-Ojeda M.E., Samson-Villeger S.I., Pasqualetto V., Enault L., Richard-Le Goff O., Corcuff E., Guy-Grand D., Rocha B., Cumano A., et al. A thymic pathway of mouse natural killer cell development characterized by expression of GATA-3 and CD127. Nat Immunol 2006, 7:1217-1224.