Interactions between innate and adaptive lymphocytes

Nature Reviews Immunology

Volumn 14, Issue 9, 2014, Pages 631-639

  Gasteiger, Georg ^a,b   Rudensky, Alexander Y ^c  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 18; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 25; INTERLEUKIN 33; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 7; STAT5 PROTEIN; THYMIC STROMAL LYMPHOPOIETIN;

ADAPTIVE IMMUNITY; CELL DIFFERENTIATION; CELL INTERACTION; CYTOKINE PRODUCTION; HELPER CELL; IMMUNE RESPONSE; INFLAMMATION; INNATE IMMUNITY; LYMPHOCYTE; LYMPHOID CELL; MOLECULAR MECHANICS; NATURAL KILLER CELL; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; CELL COMMUNICATION; HUMAN; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; REGULATORY T LYMPHOCYTE; ANTIGEN SPECIFICITY; AUTOIMMUNITY; CELL EXPANSION; CELL FUNCTION; CELL PROLIFERATION; CYTOTOXICITY; HELMINTHIASIS; INNATE LYMPHOID CELL; INTRAABDOMINAL FAT; LYMPHOCYTE SUBPOPULATION; MEMORY T LYMPHOCYTE; NONHUMAN; SENSOR; SKIN ALLERGY; T LYMPHOCYTE ACTIVATION;

ADAPTIVE IMMUNITY; CELL COMMUNICATION; CYTOKINES; HUMANS; IMMUNITY, INNATE; INFLAMMATION; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; T-LYMPHOCYTES, HELPER-INDUCER; T-LYMPHOCYTES, REGULATORY;

EID: 84906938693     PISSN: 14741733     EISSN: 14741741     Source Type: Journal    
DOI: 10.1038/nri3726     Document Type: Review

References (88)

1. Sanos, S. L. & Diefenbach, A. Innate lymphoid cells: from border protection to the initiation of inflammatory diseases. Immunol. Cell Biol. 91, 215-224 (2013).
2. Spits, H. et al. Innate lymphoid cells-a proposal for uniform nomenclature. Nature Rev. Immunol. 13, 145-149 (2013).
3. Walker, J. A., Barlow, J. L. & McKenzie, A. N. Innate lymphoid cells-how did we miss them? Nature Rev. Immunol. 13, 75-87 (2013).
4. Kirchberger, S. et al. Innate lymphoid cells sustain colon cancer through production of interleukin-22 in a mouse model. J. Exp. Med. 210, 917-931 (2013).
5. Fuchs, A. et al. 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 (2013).
6. Roediger, B. et al. Cutaneous immunosurveillance and regulation of inflammation by group 2 innate lymphoid cells. Nature Immunol. 14, 564-573 (2013).
7. Molofsky, A. B. et al. Innate lymphoid type 2 cells sustain visceral adipose tissue eosinophils and alternatively activated macrophages. J. Exp. Med. 210, 535-549 (2013).
8. Sitrin, J., Ring, A., Garcia, K. C., Benoist, C. & Mathis, D. Regulatory T cells control NK cells in an insulitic lesion by depriving them of IL-2. J. Exp. Med. 210, 1153-1165 (2013).
9. Hams, E. et al. IL-25 and type 2 innate lymphoid cells induce pulmonary fibrosis. Proc. Natl Acad. Sci. USA 111, 367-372 (2014).
10. McHedlidze, T. et al. Interleukin-33-dependent innate lymphoid cells mediate hepatic fibrosis. Immunity 39, 357-371 (2013).
11. Chang, Y. J. et al. Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity. Nature Immunol. 12, 631-638 (2011).
12. Halim, T. Y. et al. Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation. Immunity 40, 425-435 (2014).
13. Wilhelm, C. et al. An IL-9 fate reporter demonstrates the induction of an innate IL-9 response in lung inflammation. Nature Immunol. 12, 1071-1077 (2011).
14. Feuerer, M., Shen, Y., Littman, D. R., Benoist, C. & Mathis, D. How punctual ablation of regulatory T cells unleashes an autoimmune lesion within the pancreatic islets. Immunity 31, 654-664 (2009).
15. Lee, J. S. et al. AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch. Nature Immunol. 13, 144-151 (2012).
16. Monticelli, L. A. et al. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nature Immunol. 12, 1045-1054 (2011).
17. Swain, S. L., McKinstry, K. K. & Strutt, T. M. Expanding roles for CD4+ T cells in immunity to viruses. Nature Rev. Immunol. 12, 136-148 (2012).
18. Hepworth, M. R. et al. Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria. Nature 498, 113-117 (2013).
19. Waggoner, S. N., Cornberg, M., Selin, L. K. & Welsh, R. M. Natural killer cells act as rheostats modulating antiviral T cells. Nature 481, 394-398 (2012).
20. Qiu, J. et al. Group 3 innate lymphoid cells inhibit T-cell-mediated intestinal inflammation through aryl hydrocarbon receptor signaling and regulation of microflora. Immunity 39, 386-399 (2013).
21. Lang, P. A. et al. Natural killer cell activation enhances immune pathology and promotes chronic infection by limiting CD8+ T-cell immunity. Proc. Natl Acad. Sci. USA 109, 1210-1215 (2012).
22. Gorski, S. A., Hahn, Y. S. & Braciale, T. J. Group 2 innate lymphoid cell production of IL-5 is regulated by NKT cells during influenza virus infection. PLoS Pathog. 9, e1003615 (2013).
23. Magri, G. et al. Innate lymphoid cells integrate stromal and immunological signals to enhance antibody production by splenic marginal zone B cells. Nature Immunol. 15, 354-364 (2014).
24. Crome, S. Q., Lang, P. A., Lang, K. S. & Ohashi, P. S. Natural killer cells regulate diverse T cell responses. Trends Immunol. 34, 342-349 (2013).
25. Strowig, T. et al. Tonsilar NK cells restrict B cell transformation by the Epstein-Barr virus via IFN-.. PLoS Pathog. 4, e27 (2008).
26. Fehniger, T. A. et al. CD56bright natural killer cells are present in human lymph nodes and are activated by T cell-derived IL-2: a potential new link between adaptive and innate immunity. Blood 101, 3052-3057 (2003). (Pubitemid 36857995)
27. Luther, C., Warner, K. & Takei, F. Unique progenitors in mouse lymph node develop into CD127+ NK cells: thymus-dependent and thymus-independent pathways. Blood 117, 4012-4021 (2011).
28. Vosshenrich, C. A. et al. A thymic pathway of mouse natural killer cell development characterized by expression of GATA-3 and CD127. Nature Immunol. 7, 1217-1224 (2006). (Pubitemid 44594318)
29. Mirchandani, A. S. et al. Type 2 innate lymphoid cells drive CD4+ Th2 cell responses. J. Immunol. 192, 2442-2448 (2014).
30. Neill, D. R. et al. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464, 1367-1370 (2010).
31. Sutton, C. E. et al. Interleukin-1 and IL-23 induce innate IL-17 production from .d T cells, amplifying Th17 responses and autoimmunity. Immunity 31, 331-341 (2009).
32. Cui, Y. et al. Major role of .d T cells in the generation of IL-17+ uveitogenic T cells. J. Immunol. 183, 560-567 (2009).
33. Mortha, A. et al. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science 343, 1249288 (2014).
34. Withers, D. R. et al. Cutting edge: lymphoid tissue inducer cells maintain memory CD4 T cells within secondary lymphoid tissue. J. Immunol. 189, 2094-2098 (2012).
35. Aloisi, F. & Pujol-Borrell, R. Lymphoid neogenesis in chronic inflammatory diseases. Nature Rev. Immunol. 6, 205-217 (2006). (Pubitemid 43290990)
36. Peppa, D. et al. Up-regulation of a death receptor renders antiviral T cells susceptible to NK cell-mediated deletion. J. Exp. Med. 210, 99-114 (2013).
37. Gasteiger, G., Hemmers, S., Bos, P. D., Sun, J. C. & Rudensky, A. Y. IL-2-dependent adaptive control of NK cell homeostasis. J. Exp. Med. 210, 1179-1187 (2013).
38. Bevan, M. J. Helping the CD8+ T-cell response. Nature Rev. Immunol. 4, 595-602 (2004).
39. Soudja, S. M. et al. Memory-T-cell-derived interferon-. instructs potent innate cell activation for protective immunity. Immunity 40, 974-988 (2014).
40. Josefowicz, S. Z., Lu, L. F. & Rudensky, A. Y. Regulatory T cells: mechanisms of differentiation and function. Annu. Rev. Immunol. 30, 531-564 (2012).
41. Ghiringhelli, F. et al. CD4+CD25+ regulatory T cells inhibit natural killer cell functions in a transforming growth factor-ß-dependent manner. J. Exp. Med. 202, 1075-1085 (2005). (Pubitemid 41464501)
42. Smyth, M. J. et al. CD4+CD25+ T regulatory cells suppress NK cell-mediated immunotherapy of cancer. J. Immunol. 176, 1582-1587 (2006). (Pubitemid 43134302)
43. Ni, J., Miller, M., Stojanovic, A., Garbi, N. & Cerwenka, A. Sustained effector function of IL-12/15/18-preactivated NK cells against established tumors. J. Exp. Med. 209, 2351-2365 (2012).
44. Maury, S. et al. CD4+CD25+ regulatory T cell depletion improves the graft-versus-tumor effect of donor lymphocytes after allogeneic hematopoietic stem cell transplantation. Sci. Transl Med. 2, 41ra52 (2010).
45. Barao, I. et al. Suppression of natural killer cellmediated bone marrow cell rejection by CD4+CD25+ regulatory T cells. Proc. Natl Acad. Sci. USA 103, 5460-5465 (2006).
46. Bihl, F. et al. Primed antigen-specific CD4+ T cells are required for NK cell activation in vivo upon Leishmania major infection. J. Immunol. 185, 2174-2181 (2010).
47. Sungur, C. M. et al. Murine natural killer cell licensing and regulation by T regulatory cells in viral responses. Proc. Natl Acad. Sci. USA 110, 7401-7406 (2013).
48. Lee, S. H., Fragoso, M. F. & Biron, C. A. Cutting edge: a novel mechanism bridging innate and adaptive immunity: IL-12 induction of CD25 to form highaffinity IL-2 receptors on NK cells. J. Immunol. 189, 2712-2716 (2012).
49. Terme, M. et al. Regulatory T cells control dendritic cell/NK cell cross-talk in lymph nodes at the steady state by inhibiting CD4+ self-reactive T cells. J. Immunol. 180, 4679-4686 (2008).
50. Su, H. C. et al. IL-2-dependent NK cell responses discovered in virus-infected beta 2-microglobulindeficient mice. J. Immunol. 153, 5674-5681 (1994).
51. Henney, C. S., Kuribayashi, K., Kern, D. E. & Gillis, S. Interleukin-2 augments natural killer cell activity. Nature 291, 335-338 (1981). (Pubitemid 11083437)
52. Horowitz, A., Behrens, R. H., Okell, L., Fooks, A. R. & Riley, E. M. NK cells as effectors of acquired immune responses: effector CD4+ T cell-dependent activation of NK cells following vaccination. J. Immunol. 185, 2808-2818 (2010).
53. Horowitz, A. et al. Cross-talk between T cells and NK cells generates rapid effector responses to Plasmodium falciparum-infected erythrocytes. J. Immunol. 184, 6043-6052 (2010).
54. Pandiyan, P., Zheng, L., Ishihara, S., Reed, J. & Lenardo, M. J. CD4+CD25+Foxp3+ regulatory T cells induce cytokine deprivation-mediated apoptosis of effector CD4+ T cells. Nature Immunol. 8, 1353-1362 (2007). (Pubitemid 350131172)
55. Fehniger, T. A. et al. Acquisition of murine NK cell cytotoxicity requires the translation of a pre-existing pool of granzyme B and perforin mRNAs. Immunity 26, 798-811 (2007). (Pubitemid 46907665)
56. Gasteiger, G. et al. IL-2-dependent tuning of NK cell sensitivity for target cells is controlled by regulatory T cells. J. Exp. Med. 210, 1167-1178 (2013).
57. Long, S. A. et al. Rapamycin/IL-2 combination therapy in patients with type 1 diabetes augments Tregs yet transiently impairs ß-cell function. Diabetes 61, 2340-2348 (2012).
58. Daussy, C. 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. 211, 563-577 (2014).
59. Klose, C. S. et al. Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell 157, 340-356 (2014).
60. Caligiuri, M. A. et al. Selective modulation of human natural killer cells in vivo after prolonged infusion of low dose recombinant interleukin 2. J. Clin. Invest. 91, 123-132 (1993). (Pubitemid 23037263)
61. Ito, S. et al. Ultra-low dose interleukin-2 promotes immune-modulating function of regulatory T cells and natural killer cells in healthy volunteers. Mol. Ther. 22, 1388-1395 (2014).
62. Dalbeth, N. & Callan, M. F. A subset of natural killer cells is greatly expanded within inflamed joints. Arthritis Rheum. 46, 1763-1772 (2002). (Pubitemid 34774507)
63. Bauernhofer, T., Kuss, I., Henderson, B., Baum, A. S. & Whiteside, T. L. Preferential apoptosis of CD56dim natural killer cell subset in patients with cancer. Eur. J. Immunol. 33, 119-124 (2003). (Pubitemid 36157649)
64. Schierloh, P. et al. Increased susceptibility to apoptosis of CD56dimCD16+ NK cells induces the enrichment of IFN-.-producing CD56bright cells in tuberculous pleurisy. J. Immunol. 175, 6852-6860 (2005). (Pubitemid 41598930)
65. Klose, C. S. et al. A T-bet gradient controls the fate and function of CCR6-ROR.t+ innate lymphoid cells. Nature 494, 261-265 (2013).
66. Sojka, D. K. et al. Tissue-resident natural killer (NK) cells are cell lineages distinct from thymic and conventional splenic NK cells. eLife 3, e01659 (2014).
67. Guo, L., Junttila, I. S. & Paul, W. E. Cytokine-induced cytokine production by conventional and innate lymphoid cells. Trends Immunol. 33, 598-606 (2012).
68. Mjosberg, J. et al. The transcription factor GATA3 is essential for the function of human type 2 innate lymphoid cells. Immunity 37, 649-659 (2012).
69. Cipolletta, D. et al. PPAR-. is a major driver of the accumulation and phenotype of adipose tissue Treg cells. Nature 486, 549-553 (2012).
70. Busse, D. et al. Competing feedback loops shape IL-2 signaling between helper and regulatory T lymphocytes in cellular microenvironments. Proc. Natl Acad. Sci. USA 107, 3058-3063 (2010).
71. Hofer, T., Krichevsky, O. & Altan-Bonnet, G. Competition for IL-2 between regulatory and effector T cells to chisel immune responses. Frontiers Immunol. 3, 268 (2012).
72. Scharton, T. M. & Scott, P. Natural killer cells are a source of interferon-. that drives differentiation of CD4+ T cell subsets and induces early resistance to Leishmania major in mice. J. Exp. Med. 178, 567-577 (1993). (Pubitemid 23218205)
73. Xu, W. & Di Santo, J. P. Taming the beast within: regulation of innate lymphoid cell homeostasis and function. J. Immunol. 191, 4489-4496 (2013).
74. Gebhardt, T., Mueller, S. N., Heath, W. R. & Carbone, F. R. Peripheral tissue surveillance and residency by memory T cells. Trends Immunol. 34, 27-32 (2013).
75. Shin, H. & Iwasaki, A. Tissue-resident memory T cells. Immunol. Rev. 255, 165-181 (2013).
76. Vezys, V. et al. Memory CD8 T-cell compartment grows in size with immunological experience. Nature 457, 196-199 (2009).
77. Welsh, R. M. & Selin, L. K. Attrition of memory CD8 T cells. Nature 459, E3-E4 (2009).
78. Huster, K. M. et al. Cutting edge: memory CD8 T cell compartment grows in size with immunological experience but nevertheless can lose function. J. Immunol. 183, 6898-6902 (2009).
79. Schenkel, J. M., Fraser, K. A., Vezys, V. & Masopust, D. Sensing and alarm function of resident memory CD8+ T cells. Nature Immunol. 14, 509-513 (2013).
80. Burzyn, D. et al. A special population of regulatory T cells potentiates muscle repair. Cell 155, 1282-1295 (2013).
81. Elliott, J. M. & Yokoyama, W. M. Unifying concepts of MHC-dependent natural killer cell education. Trends Immunol. 32, 364-372 (2011).
82. Gordon, S. M. et al. The transcription factors T-bet and Eomes control key checkpoints of natural killer cell maturation. Immunity 36, 55-67 (2012).
83. Peng, H. et al. Liver-resident NK cells confer adaptive immunity in skin-contact inflammation. J. Clin. Invest. 123, 1444-1456 (2013).
84. Constantinides, M. G., McDonald, B. D., Verhoef, P. A. & Bendelac, A. A committed precursor to innate lymphoid cells. Nature 508, 397-401 (2014).
85. Fathman, J. W. et al. Identification of the earliest natural killer cell-committed progenitor in murine bone marrow. Blood 118, 5439-5447 (2011).
86. Oliphant, C. J. et al. MHCII-mediated dialog between group 2 innate lymphoid cells and CD4+ T cells potentiates type 2 immunity and promotes parasitic helminth expulsion. Immunity http://dx.doi.org/10.1016/j.immuni.2014. 06.016 (2014).
87. Chan, C. W. et al. Interferon-producing killer dendritic cells provide a link between innate and adaptive immunity. Nature Med. 12, 207-213 (2006). (Pubitemid 43214747)
88. Taieb, J. et al. A novel dendritic cell subset involved in tumor immunosurveillance. Nature Med. 12, 214-219 (2006).-baba