ILC2 memory: Recollection of previous activation

Immunological Reviews

Volumn 283, Issue 1, 2018, Pages 41-53

  Martinez Gonzalez, Itziar ^a,b   Ghaedi, Maryam ^a,b   Steer, Catherine A ^a,b   Mathä, Laura ^a,b   Vivier, Eric ^c,d   Takei, Fumio ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b BRITISH COLUMBIA CANCER AGENCY   (Canada)

^c CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^d INNATE PHARMA   (France)

Author keywords

allergic diseases; ILC2s; immunological memory; neonates

Indexed keywords

ALLERGIC ASTHMA; CELL ACTIVATION; CELL MATURATION; CELLULAR IMMUNITY; HUMAN; IMMUNOLOGICAL MEMORY; IMMUNOPATHOGENESIS; LUNG; LYMPHOID CELL; MEMORY CELL; NEWBORN PERIOD; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY TRACT INFLAMMATION; REVIEW; SKIN; SMALL INTESTINE; AGE; ANIMAL; ASTHMA; CELL DIFFERENTIATION; CYTOLOGY; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE SUBPOPULATION; METABOLISM;

AGE FACTORS; ANIMALS; ASTHMA; CELL DIFFERENTIATION; HUMANS; IMMUNITY, INNATE; IMMUNOLOGIC MEMORY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE SUBSETS;

EID: 85045647724     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12643     Document Type: Review

References (74)

1. Nabekura T, Lanier LL. Tracking the fate of antigen-specific versus cytokine-activated natural killer cells after cytomegalovirus infection. J Exp Med. 2016;213:2745-2758.
2. Martinez-Gonzalez I, Matha L, Steer CA, Ghaedi M, Poon GF, Takei F. Allergen-experienced group 2 innate lymphoid cells acquire memory-like properties and enhance allergic lung inflammation. Immunity. 2016;45:198-208.
3. Netea MG, van der Meer JW. Trained immunity: An ancient way of remembering. Cell Host Microbe. 2017;21:297-300.
4. Naik S, Larsen SB, Gomez NC, et al. Inflammatory memory sensitizes skin epithelial stem cells to tissue damage. Nature. 2017;550:475-480.
5. Ebbo M, Crinier A, Vely F, Vivier E. Innate lymphoid cells: Major players in inflammatory diseases. Nat Rev Immunol. 2017;17:665-678.
6. Jamieson AM, Diefenbach A, McMahon CW, Xiong N, Carlyle JR, Raulet DH. The role of the NKG2D immunoreceptor in immune cell activation and natural killing. Immunity. 2002;17:19-29.
7. Seillet C, Belz GT, Huntington ND. Development, homeostasis, and heterogeneity of NK cells and ILC1. Curr Top Microbiol Immunol. 2016;395:37-61.
8. Bernink JH, Krabbendam L, Germar K, et al. Interleukin-12 and -23 control plasticity of CD127(+) group 1 and group 3 innate lymphoid cells in the intestinal lamina propria. Immunity. 2015;43:146-160.
9. von Moltke J, Ji M, Liang HE, Locksley RM. Tuft-cell-derived IL-25 regulates an intestinal ILC2-epithelial response circuit. Nature. 2016;529:221-225.
10. Kitajima M, Ziegler SF. Cutting edge: Identification of the thymic stromal lymphopoietin-responsive dendritic cell subset critical for initiation of type 2 contact hypersensitivity. J Immunol. 2013;191:4903-4907.
11. Halim TY, Krauss RH, Sun AC, Takei F. Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergen-induced airway inflammation. Immunity. 2012;36:451-463.
12. Huang Y, Guo L, Qiu J, et al. IL-25-responsive, lineage-negative KLRG1(hi) cells are multipotential ‘inflammatory’ type 2 innate lymphoid cells. Nat Immunol. 2015;16:161-169.
13. Kim BS, Siracusa MC, Saenz SA, et al. TSLP elicits IL-33-independent innate lymphoid cell responses to promote skin inflammation. Sci Transl Med. 2013;5:170ra116.
14. O'Sullivan TE, Sun JC, Lanier LL. Natural killer cell memory. Immunity. 2015;43:634-645.
15. Cooper MA, Elliott JM, Keyel PA, Yang L, Carrero JA, Yokoyama WM. Cytokine-induced memory-like natural killer cells. Proc Natl Acad Sci USA. 2009;106:1915-1919.
16. Kleinnijenhuis J, Quintin J, Preijers F, et al. Bacille Calmette-Guerin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes. Proc Natl Acad Sci USA. 2012;109:17537-17542.
17. Martinez-Gonzalez I, Matha L, Steer CA, Takei F. Immunological memory of group 2 innate lymphoid cells. Trends Immunol. 2017;38:423-431.
18. Halim TY, Steer CA, Matha L, et al. Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation. Immunity. 2014;40:425-435.
19. Klose CSN, Mahlakoiv T, Moeller JB, et al. The neuropeptide neuromedin U stimulates innate lymphoid cells and type 2 inflammation. Nature. 2017;549:282-286.
20. Karo JM, Sun JC. Novel molecular mechanism for generating NK-cell fitness and memory. Eur J Immunol. Jul 2015;45:1906-1915.
21. Ghaedi M, Steer CA, Martinez-Gonzalez I, Halim TY, Abraham N, Takei F. Common-lymphoid-progenitor-independent pathways of innate and T lymphocyte development. Cell Rep. 2016;15:471-480.
22. Leong JW, Chase JM, Romee R, et al. Preactivation with IL-12, IL-15, and IL-18 induces CD25 and a functional high-affinity IL-2 receptor on human cytokine-induced memory-like natural killer cells. Biol Blood Marrow Transplant. 2014;20:463-473.
23. Gasteiger G, Fan X, Dikiy S, Lee SY, Rudensky AY. Tissue residency of innate lymphoid cells in lymphoid and nonlymphoid organs. Science. 2015;350:981-985.
24. Paust S, Gill HS, Wang BZ, 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.
25. Salimi M, Barlow JL, Saunders SP, et al. A role for IL-25 and IL-33-driven type-2 innate lymphoid cells in atopic dermatitis. J Exp Med. 2013;210:2939-2950.
26. Wohlfahrt T, Usherenko S, Englbrecht M, et al. Type 2 innate lymphoid cell counts are increased in patients with systemic sclerosis and correlate with the extent of fibrosis. Ann Rheum Dis. 2016;75:623-626.
27. Terasaki S, Nakanuma Y, Hoso M, et al. Three cases of primary biliary cirrhosis associated with bronchial asthma. J Gastroenterol. 1995;30:667-671.
28. Yang Q, Li F, Harly C, et al. TCF-1 upregulation identifies early innate lymphoid progenitors in the bone marrow. Nat Immunol. 2015;16:1044-1050.
29. Tanriver Y, Diefenbach A. Transcription factors controlling development and function of innate lymphoid cells. Int Immunol. 2014;26:119-128.
30. Klose CS, Flach M, Mohle L, et al. Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell. 2014;157:340-356.
31. Constantinides MG, McDonald BD, Verhoef PA, Bendelac A. A committed precursor to innate lymphoid cells. Nature. 2014;508:397-401.
32. Halim TY, MacLaren A, Romanish MT, Gold MJ, McNagny KM, 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.
33. Saluzzo S, Gorki AD, Rana BMJ, et al. First-breath-induced type 2 pathways shape the lung immune environment. Cell Rep. 2017;18:1893-1905.
34. Steer CA, Martinez-Gonzalez I, Ghaedi M, Allinger P, Matha L, Takei F. Group 2 innate lymphoid cell activation in the neonatal lung drives type 2 immunity and allergen sensitization. J Allergy Clin Immunol. 2017;140:593-595 e593.
35. de Kleer IM, Kool M, de Bruijn MJ, et al. Perinatal activation of the interleukin-33 pathway promotes type 2 immunity in the developing lung. Immunity. 2016;45:1285-1298.
36. Netea MG, Joosten LA, Latz E, et al. Trained immunity: A program of innate immune memory in health and disease. Science. 2016;352:aaf1098.
37. Morita H, Arae K, Unno H, et al. An interleukin-33-mast cell-interleukin-2 axis suppresses papain-induced allergic inflammation by promoting regulatory T cell numbers. Immunity. 2015;43:175-186.
38. Bartemes KR, Kephart GM, Fox SJ, Kita H. Enhanced innate type 2 immune response in peripheral blood from patients with asthma. J Allergy Clin Immunol. 2014;134:671-678 e674.
39. Smith SG, Chen R, Kjarsgaard M, et al. Increased numbers of activated group 2 innate lymphoid cells in the airways of patients with severe asthma and persistent airway eosinophilia. J Allergy Clin Immunol. 2016;137:75-86 e78.
40. Salazar F, Ghaemmaghami AM. Allergen recognition by innate immune cells: Critical role of dendritic and epithelial cells. Front Immunol. 2013;4:356.
41. Motomura Y, Morita H, Moro K, et al. Basophil-derived interleukin-4 controls the function of natural helper cells, a member of ILC2s, in lung inflammation. Immunity. 2014;40:758-771.
42. Doherty TA, Khorram N, Lund S, Mehta AK, Croft M, Broide DH. Lung type 2 innate lymphoid cells express cysteinyl leukotriene receptor 1, which regulates TH2 cytokine production. J Allergy Clin Immunol. 2013;132:205-213.
43. Rigas D, Lewis G, Aron JL, et al. Type 2 innate lymphoid cell suppression by regulatory T cells attenuates airway hyperreactivity and requires inducible T-cell costimulator-inducible T-cell costimulator ligand interaction. J Allergy Clin Immunol. 2017;139:1468-1477 e1462.
44. Martinez-Gonzalez I, Steer CA, Takei F. Lung ILC2s link innate and adaptive responses in allergic inflammation. Trends Immunol. 2015;36:189-195.
45. Oliphant CJ, Hwang YY, Walker JA, 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. 2014;41:283-295.
46. Lambrecht BN, Hammad H. The immunology of asthma. Nat Immunol. 2015;16:45-56.
47. Busse WW, Holgate S, Kerwin E, et al. Randomized, double-blind, placebo-controlled study of brodalumab, a human anti-IL-17 receptor monoclonal antibody, in moderate to severe asthma. Am J Respir Crit Care Med. 2013;188:1294-1302.
48. Wakashin H, Hirose K, Maezawa Y, et al. IL-23 and Th17 cells enhance Th2-cell-mediated eosinophilic airway inflammation in mice. Am J Respir Crit Care Med. 2008;178:1023-1032.
49. Kim HY, Lee HJ, Chang YJ, et al. Interleukin-17-producing innate lymphoid cells and the NLRP3 inflammasome facilitate obesity-associated airway hyperreactivity. Nat Med. 2014;20:54-61.
50. Everaere L, Ait-Yahia S, Molendi-Coste O, et al. Innate lymphoid cells contribute to allergic airway disease exacerbation by obesity. J Allergy Clin Immunol. 2016;138:1309-1318 e1311.
51. Calderon MA, Cox L, Casale TB, Moingeon P, Demoly P. Multiple-allergen and single-allergen immunotherapy strategies in polysensitized patients: Looking at the published evidence. J Allergy Clin Immunol. 2012;129:929-934.
52. Unutmaz D, Pileri P, Abrignani S. Antigen-independent activation of naive and memory resting T cells by a cytokine combination. J Exp Med. 1994;180:1159-1164.
53. Christianson CA, Goplen NP, Zafar I, et al. Persistence of asthma requires multiple feedback circuits involving type 2 innate lymphoid cells and IL-33. J Allergy Clin Immunol. 2015;136:59-68 e14.
54. Denning DW, O'Driscoll BR, Hogaboam CM, Bowyer P, Niven RM. The link between fungi and severe asthma: A summary of the evidence. The European Respiratory Journal. 2006;27:615-626.
55. Kouzaki H, Iijima K, Kobayashi T, O'Grady SM, Kita H. The danger signal, extracellular ATP, is a sensor for an airborne allergen and triggers IL-33 release and innate Th2-type responses. J Immunol. 2011;186:4375-4387.
56. Van Dyken SJ, Garcia D, Porter P, et al. Fungal chitin from asthma-associated home environments induces eosinophilic lung infiltration. J Immunol. 2011;187:2261-2267.
57. Kabata H, Moro K, Fukunaga K, et al. Thymic stromal lymphopoietin induces corticosteroid resistance in natural helper cells during airway inflammation. Nat Commun. 2013;4:2675.
58. Lloyd CM, Saglani S. Development of allergic immunity in early life. Immunol Rev. 2017;278:101-115.
59. Saravia J, You D, Shrestha B, et al. Respiratory syncytial virus disease is mediated by age-variable IL-33. PLoS Pathog. 2015;11:e1005217.
60. Monticelli LA, Sonnenberg GF, Abt MC, et al. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat Immunol. 2011;12:1045-1054.
61. Monticelli LA, Osborne LC, Noti M, Tran SV, Zaiss DM, Artis D. IL-33 promotes an innate immune pathway of intestinal tissue protection dependent on amphiregulin-EGFR interactions. Proc Natl Acad Sci USA. 2015;112:10762-10767.
62. Beale J, Jayaraman A, Jackson DJ, et al. Rhinovirus-induced IL-25 in asthma exacerbation drives type 2 immunity and allergic pulmonary inflammation. Sci Transl Med. 2014;6:256ra134.
63. DeKruyff RH, Yu S, Kim HY, Umetsu DT. Innate immunity in the lung regulates the development of asthma. Immunol Rev. 2014;260:235-248.
64. Crellin NK, Trifari S, Kaplan CD, Satoh-Takayama N, Di Santo JP, Spits H. Regulation of cytokine secretion in human CD127(+) LTi-like innate lymphoid cells by Toll-like receptor 2. Immunity. 2010;33:752-764.
65. Yang Q, Ge MQ, Kokalari B, et al. Group 2 innate lymphoid cells mediate ozone-induced airway inflammation and hyperresponsiveness in mice. J Allergy Clin Immunol. 2016;137:571-578.
66. Bal SM, Bernink JH, Nagasawa M, et al. IL-1beta, IL-4 and IL-12 control the fate of group 2 innate lymphoid cells in human airway inflammation in the lungs. Nat Immunol. 2016;17:636-645.
67. Silver JS, Kearley J, Copenhaver AM, et al. Inflammatory triggers associated with exacerbations of COPD orchestrate plasticity of group 2 innate lymphoid cells in the lungs. Nat Immunol. 2016;17:626-635.
68. Ohne Y, Silver JS, Thompson-Snipes L, et al. IL-1 is a critical regulator of group 2 innate lymphoid cell function and plasticity. Nat Immunol. 2016;17:646-655.
69. Mathews JA, Krishnamoorthy N, Kasahara DI, et al. IL-33 drives augmented responses to ozone in obese mice. Environ Health Perspect. 2017;125:246-253.
70. Hams E, Armstrong ME, Barlow JL, et al. IL-25 and type 2 innate lymphoid cells induce pulmonary fibrosis. Proc Natl Acad Sci USA. 2014;111:367-372.
71. Li D, Guabiraba R, Besnard AG, et al. IL-33 promotes ST2-dependent lung fibrosis by the induction of alternatively activated macrophages and innate lymphoid cells in mice. J Allergy Clin Immunol. 2014;134:1422-1432 e11.
72. Luetke-Eversloh M, Hammer Q, Durek P, et al. Human cytomegalovirus drives epigenetic imprinting of the IFNG locus in NKG2Chi natural killer cells. PLoS Pathog. 2014;10:e1004441.
73. Saeed S, Quintin J, Kerstens HH, et al. Epigenetic programming of monocyte-to-macrophage differentiation and trained innate immunity. Science. 2014;345:1251086.
74. Mjosberg JM, Trifari S, Crellin NK, et al. Human IL-25- and IL-33-responsive type 2 innate lymphoid cells are defined by expression of CRTH2 and CD161. Nat Immunol. 2011;12:1055-1062.