Activation and Function of Innate Lymphoid Cells

  • Walter Gottlieb Land


Efferent innate immune responses include the function of innate lymphoid cells, a previously unappreciated cell type of the innate immune system that has been characterized in mice and humans and found to influence the induction, regulation, and resolution of inflammation, fundamentally. There is considerable phenotypic and functional heterogeneity in the mature family of innate lymphoid cells, and broadly three groups have been defined based upon shared expression of surface markers, transcription factors, and effector cytokine production. Various immunological functions of innate lymphoid cells have been described, and increasing numbers of studies have implicated these cells in inflammatory disorders. Within group 1 of this category of cells, natural killer cells play an outstanding role and are the by far most frequently investigated cell type. Activation and subsequent responses of innate lymphoid cells, in particular, natural killer cells, to infective, sterile, or tumoral cellular stress scenarios are induced and regulated—directly or indirectly—by MAMPs and/or DAMPs which are sensed by numerous pattern recognition molecules. These receptors are expressed on their cell surface and, following the recognition process, can instigate, promote, or suppress effector cell functions. Notably, disease association studies in defined patient populations have identified significant alterations in innate lymphoid cell responses, indicating a potential role for these cell populations in human health and disease.


  1. 1.
    Ebbo M, Crinier A, Vély F, Vivier E. Innate lymphoid cells: major players in inflammatory diseases. Nat Rev Immunol. 2017;17(11):665–78. Available from: CrossRefGoogle Scholar
  2. 2.
    Sonnenberg GF, Artis D. Innate lymphoid cells in the initiation, regulation and resolution of inflammation. Nat Med. 2015;21:698–708. Available from: CrossRefPubMedCentralGoogle Scholar
  3. 3.
    Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol. 2008;9:503–10. Available from: CrossRefGoogle Scholar
  4. 4.
    Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, et al. Innate or adaptive immunity? The example of natural killer cells. Science. 2011;331:44–9. Available from: CrossRefPubMedCentralGoogle Scholar
  5. 5.
    Raulet DH, Gasser S, Gowen BG, Deng W, Jung H. Regulation of ligands for the NKG2D activating receptor. Annu Rev Immunol. 2013;31:413–41. Available from: CrossRefPubMedCentralGoogle Scholar
  6. 6.
    Lanier LL. NKG2D receptor and its ligands in host defense. Cancer Immunol Res. 2015;3:575–82. Available from: CrossRefPubMedCentralGoogle Scholar
  7. 7.
    Carapito R, Bahram S. Genetics, genomics, and evolutionary biology of NKG2D ligands. Immunol Rev. 2015;267:88–116. Available from: CrossRefGoogle Scholar
  8. 8.
    Carapito R, Aouadi I, Ilias W, Bahram S. Natural killer group 2, member D/NKG2D ligands in hematopoietic cell transplantation. Front Immunol. 2017;8:368. Available from: CrossRefPubMedCentralGoogle Scholar
  9. 9.
    Quatrini L, Molfetta R, Zitti B, Peruzzi G, Fionda C, Capuano C, et al. Ubiquitin-dependent endocytosis of NKG2D-DAP10 receptor complexes activates signaling and functions in human NK cells. Sci Signal. 2015;8:ra108. Available from: CrossRefGoogle Scholar
  10. 10.
    Rojas JM, Spada R, Sanz-Ortega L, Morillas L, Mejías R, Mulens-Arias V, et al. PI3K p85 β regulatory subunit deficiency does not affect NK cell differentiation and increases NKG2D-mediated activation. J Leukoc Biol. 2016;100:1285–96. Available from: CrossRefGoogle Scholar
  11. 11.
    Karimi MA, Aguilar OA, Zou B, Bachmann MH, Carlyle JR, Baldwin CL, et al. A truncated human NKG2D splice isoform negatively regulates NKG2D-mediated function. J Immunol. 2014;193:2764–71. Available from: CrossRefPubMedCentralGoogle Scholar
  12. 12.
    Ferlazzo G, Morandi B. Cross-talks between natural killer cells and distinct subsets of dendritic cells. Front Immunol. 2014;5:159. Available from: CrossRefPubMedCentralGoogle Scholar
  13. 13.
    Thomas R, Yang X. NK-DC crosstalk in immunity to microbial infection. J Immunol Res. 2016;2016:1–7. Available from: CrossRefGoogle Scholar
  14. 14.
    Parisi L, Bassani B, Tremolati M, Gini E, Farronato G, Bruno A. Natural killer cells in the orchestration of chronic inflammatory diseases. J Immunol Res. 2017;2017:1–13. Available from: CrossRefGoogle Scholar
  15. 15.
    Waggoner SN, Reighard SD, Gyurova IE, Cranert SA, Mahl SE, Karmele EP, et al. Roles of natural killer cells in antiviral immunity. Curr Opin Virol. 2016;16:15–23. Available from: CrossRefGoogle Scholar
  16. 16.
    Iannello A, Thompson TW, Ardolino M, Marcus A, Raulet DH. Immunosurveillance and immunotherapy of tumors by innate immune cells. Curr Opin Immunol. 2016;38:52–8. Available from: CrossRefGoogle Scholar
  17. 17.
    Schmidt S, Ullrich E, Bochennek K, Zimmermann S-Y, Lehrnbecher T. Role of natural killer cells in antibacterial immunity. Expert Rev Hematol. 2016;9:1119–27. Available from: CrossRefGoogle Scholar
  18. 18.
    Marcus A, Gowen BG, Thompson TW, Iannello A, Ardolino M, Deng W, et al. Recognition of tumors by the innate immune system and natural killer cells. Adv Immunol. 2014;122:91–128. Available from: CrossRefPubMedCentralGoogle Scholar
  19. 19.
    Leal FE, Premeaux TA, Abdel-Mohsen M, Ndhlovu LC. Role of natural killer cells in HIV-associated malignancies. Front Immunol. 2017;8:315. Available from: CrossRefPubMedCentralGoogle Scholar
  20. 20.
    Iannello A, Raulet DH. Immune surveillance of unhealthy cells by natural killer cells. Cold Spring Harb Symp Quant Biol. 2013;78:249–57. Available from: CrossRefPubMedCentralGoogle Scholar
  21. 21.
    Screpanti V, Wallin RPA, Grandien A, Ljunggren H-G. Impact of FASL-induced apoptosis in the elimination of tumor cells by NK cells. Mol Immunol. 2005;42:495–9. Available from: CrossRefGoogle Scholar
  22. 22.
    Smyth MJ, Cretney E, Kelly JM, Westwood JA, Street SEA, Yagita H, et al. Activation of NK cell cytotoxicity. Mol Immunol. 2005;42:501–10. Available from: CrossRefGoogle Scholar
  23. 23.
    Topham NJ, Hewitt EW. Natural killer cell cytotoxicity: how do they pull the trigger? Immunology. 2009;128:7–15. Available from: CrossRefPubMedCentralGoogle Scholar
  24. 24.
    de Saint Basile G, Ménasché G, Fischer A. Molecular mechanisms of biogenesis and exocytosis of cytotoxic granules. Nat Rev Immunol. 2010;10:568–79. Available from: CrossRefGoogle Scholar
  25. 25.
    Caulfield AJ, Lathem WW. Disruption of fas-fas ligand signaling, apoptosis, and innate immunity by bacterial pathogens. PLoS Pathog. 2014;10:e1004252. Available from: CrossRefPubMedCentralGoogle Scholar
  26. 26.
    Martinez-Lostao L, Anel A, Pardo J. How do cytotoxic lymphocytes kill cancer cells? Clin Cancer Res. 2015;21:5047–56. Available from: CrossRefGoogle Scholar
  27. 27.
    Zhu Y, Huang B, Shi J, Zhu Y, Huang B, Shi J. Fas ligand and lytic granule differentially control cytotoxic dynamics of Natural Killer cell against cancer target. Oncotarget. 2016;5:2–4. Available from: Google Scholar
  28. 28.
    Lettau M, Kabelitz D, Janssen O. Lysosome-related effector vesicles in T lymphocytes and NK cells. Scand J Immunol. 2015;82:235–43. Available from: CrossRefGoogle Scholar
  29. 29.
    Jong AY, Wu C-H, Li J, Sun J, Fabbri M, Wayne AS, et al. Large-scale isolation and cytotoxicity of extracellular vesicles derived from activated human natural killer cells. J Extracell Vesicles. 2017;6:1294368. Available from: CrossRefPubMedCentralGoogle Scholar
  30. 30.
    Han J, Pluhackova K, Böckmann RA. The multifaceted role of SNARE proteins in membrane fusion. Front Physiol. 2017;8:5. Available from: CrossRefPubMedCentralGoogle Scholar
  31. 31.
    D’Orlando O, Zhao F, Kasper B, Orinska Z, Müller J, Hermans-Borgmeyer I, et al. Syntaxin 11 is required for NK and CD8 + T-cell cytotoxicity and neutrophil degranulation. Eur J Immunol. 2013;43:194–208. Available from: CrossRefGoogle Scholar
  32. 32.
    Voskoboinik I, Smyth MJ, Trapani JA. Perforin-mediated target-cell death and immune homeostasis. Nat Rev Immunol. 2006;6:940–52. Available from: CrossRefGoogle Scholar
  33. 33.
    Hoves S, Trapani JA, Voskoboinik I. The battlefield of perforin/granzyme cell death pathways. J Leukoc Biol. 2010;87:237–43. Available from: CrossRefGoogle Scholar
  34. 34.
    Djeu JY, Jiang K, Wei S. A view to a kill: signals triggering cytotoxicity. Clin Cancer Res. 2002;8:636–40. Available from: PubMedGoogle Scholar
  35. 35.
    Orange JS, Ballas ZK. Natural killer cells in human health and disease. Clin Immunol. 2006;118:1–10. Available from: CrossRefGoogle Scholar
  36. 36.
    Campbell KS, Hasegawa J. Natural killer cell biology: an update and future directions. J Allergy Clin Immunol. 2013;132:536–44. Available from: CrossRefPubMedCentralGoogle Scholar
  37. 37.
    Almeida CR, Caires HR, Vasconcelos DP, Barbosa MA. NAP-2 secreted by human NK cells can stimulate mesenchymal stem/stromal cell recruitment. Stem Cell Rep. 2016;6:466–73. Available from: CrossRefGoogle Scholar
  38. 38.
    Cerwenka A, Lanier LL. Natural killer cell memory in infection, inflammation and cancer. Nat Rev Immunol. 2016;16:112–23. Available from: CrossRefGoogle Scholar
  39. 39.
    Gabrielli S, Ortolani C, del Zotto G, Luchetti F, Canonico B, Buccella F, et al. The memories of NK cells: innate-adaptive immune intrinsic crosstalk. J Immunol Res. 2016;2016:1–14. Available from: CrossRefGoogle Scholar
  40. 40.
    Champsaur M, Lanier LL. Effect of NKG2D ligand expression on host immune responses. Immunol Rev. 2010;235:267–85. Available from: CrossRefPubMedCentralGoogle Scholar
  41. 41.
    Lodoen MB, Lanier LL. Viral modulation of NK cell immunity. Nat Rev Microbiol. 2005;3:59–69. Available from: CrossRefGoogle Scholar
  42. 42.
    Tokuyama M, Lorin C, Delebecque F, Jung H, Raulet DH, Coscoy L. Expression of the RAE-1 family of stimulatory NK-cell ligands requires activation of the PI3K pathway during viral infection and transformation. PLoS Pathog. 2011;7:e1002265. Available from: CrossRefPubMedCentralGoogle Scholar
  43. 43.
    Pignoloni B, Fionda C, Dell’Oste V, Luganini A, Cippitelli M, Zingoni A, et al. Distinct roles for human cytomegalovirus immediate early proteins IE1 and IE2 in the transcriptional regulation of MICA and PVR/CD155 expression. J Immunol. 2016;197:4066–78. Available from: CrossRefGoogle Scholar
  44. 44.
    Lam VC, Lanier LL. NK cells in host responses to viral infections. Curr Opin Immunol. 2017;44:43–51. Available from: CrossRefGoogle Scholar
  45. 45.
    Rölle A, Pollmann J, Ewen E-M, Le VTK, Halenius A, Hengel H, et al. IL-12-producing monocytes and HLA-E control HCMV-driven NKG2C+ NK cell expansion. J Clin Invest. 2014;124:5305–16. Available from: CrossRefPubMedCentralGoogle Scholar
  46. 46.
    Liu LL, Landskron J, Ask EH, Enqvist M, Sohlberg E, Traherne JA, et al. Critical role of CD2 costimulation in adaptive natural killer cell responses revealed in NKG2C-deficient humans. Cell Rep. 2016;15:1088–99. Available from: CrossRefPubMedCentralGoogle Scholar
  47. 47.
    Rölle A, Brodin P. Immune adaptation to environmental influence: the case of NK cells and HCMV. Trends Immunol. 2016;37:233–43. Available from: CrossRefGoogle Scholar
  48. 48.
    Jost S, Tomezsko PJ, Rands K, Toth I, Lichterfeld M, Gandhi RT, et al. CD4+ T-cell help enhances NK cell function following therapeutic HIV-1 vaccination. J Virol. 2014;88:8349–54. Available from: CrossRefPubMedCentralGoogle Scholar
  49. 49.
    Werner JM, Serti E, Chepa-Lotrea X, Stoltzfus J, Ahlenstiel G, Noureddin M, et al. Ribavirin improves the IFN-γ response of natural killer cells to IFN-based therapy of hepatitis C virus infection. Hepatology. 2014;60:1160–9. Available from: CrossRefPubMedCentralGoogle Scholar
  50. 50.
    van Beek JJP, Wimmers F, Hato SV, de Vries IJM, Sköld AE. Dendritic cell cross talk with innate and innate-like effector cells in antitumor immunity: implications for DC vaccination. Crit Rev Immunol. 2014;34:517–36. Available from: CrossRefGoogle Scholar
  51. 51.
    Zhou Z, Yu X, Zhang J, Tian Z, Zhang C. TLR7/8 agonists promote NK-DC cross-talk to enhance NK cell anti-tumor effects in hepatocellular carcinoma. Cancer Lett. 2015;369:298–306. Available from: CrossRefGoogle Scholar
  52. 52.
    Tallerico R, Garofalo C, Carbone E. A new biological feature of natural killer cells: the recognition of solid tumor-derived cancer stem cells. Front Immunol. 2016;7:179. Available from: CrossRefPubMedCentralGoogle Scholar
  53. 53.
    Sagiv A, Burton DGA, Moshayev Z, Vadai E, Wensveen F, Ben-Dor S, et al. NKG2D ligands mediate immunosurveillance of senescent cells. Aging (Albany NY). 2016;8:328–44. Available from: CrossRefGoogle Scholar
  54. 54.
    Chuprin A, Gal H, Biron-Shental T, Biran A, Amiel A, Rozenblatt S, et al. Cell fusion induced by ERVWE1 or measles virus causes cellular senescence. Genes Dev. 2013;27:2356–66. Available from: CrossRefPubMedCentralGoogle Scholar
  55. 55.
    Burton DGA, Krizhanovsky V. Physiological and pathological consequences of cellular senescence. Cell Mol Life Sci. 2014;71:4373–86. Available from: CrossRefPubMedCentralGoogle Scholar
  56. 56.
    Muñoz-Espín D, Serrano M. Cellular senescence: from physiology to pathology. Nat Rev Mol Cell Biol. 2014;15:482–96. Available from: CrossRefGoogle Scholar
  57. 57.
    Campisi J. Aging, cellular senescence, and cancer. Annu Rev Physiol. 2013;75:685–705. Available from: CrossRefGoogle Scholar
  58. 58.
    Ovadya Y, Krizhanovsky V. Senescent cells: SASPected drivers of age-related pathologies. Biogerontology. 2014;15:627–42. Available from: CrossRefGoogle Scholar
  59. 59.
    Krizhanovsky V, Yon M, Dickins RA, Hearn S, Simon J, Miething C, et al. Senescence of activated stellate cells limits liver fibrosis. Cell. 2008;134:657–67. Available from: CrossRefPubMedCentralGoogle Scholar
  60. 60.
    Sagiv A, Biran A, Yon M, Simon J, Lowe SW, Krizhanovsky V. Granule exocytosis mediates immune surveillance of senescent cells. Oncogene. 2013;32:1971–7. Available from: CrossRefGoogle Scholar
  61. 61.
    Ernst WA, Thoma-Uszynski S, Teitelbaum R, Ko C, Hanson DA, Clayberger C, et al. Granulysin, a T cell product, kills bacteria by altering membrane permeability. J Immunol. 2000;165:7102–8. Available from: CrossRefGoogle Scholar
  62. 62.
    Lu C-C, Wu T-S, Hsu Y-J, Chang C-J, Lin C-S, Chia J-H, et al. NK cells kill mycobacteria directly by releasing perforin and granulysin. J Leukoc Biol. 2014;96:1119–29. Available from: CrossRefGoogle Scholar
  63. 63.
    Gonzales CM, Williams CB, Calderon VE, Huante MB, Moen ST, Popov VL, et al. Antibacterial role for natural killer cells in host defense to Bacillus anthracis. Infect Immun. 2012;80:234–42. Available from: CrossRefPubMedCentralGoogle Scholar
  64. 64.
    Agerberth B, Charo J, Werr J, Olsson B, Idali F, Lindbom L, et al. The human antimicrobial and chemotactic peptides LL-37 and alpha-defensins are expressed by specific lymphocyte and monocyte populations. Blood. 2000;96:3086–93. Available from: PubMedGoogle Scholar
  65. 65.
    Schuster IS, Coudert JD, Andoniou CE, Degli-Esposti MA. “Natural regulators”: NK cells as modulators of T cell immunity. Front Immunol. 2016;7:235. Available from: CrossRefPubMedCentralGoogle Scholar
  66. 66.
    Agaugue S, Marcenaro E, Ferranti B, Moretta L, Moretta A. Human natural killer cells exposed to IL-2, IL-12, IL-18, or IL-4 differently modulate priming of naive T cells by monocyte-derived dendritic cells. Blood. 2008;112:1776–83. Available from: CrossRefGoogle Scholar
  67. 67.
    Moretta L, Ferlazzo G, Bottino C, Vitale M, Pende D, Mingari MC, et al. Effector and regulatory events during natural killer-dendritic cell interactions. Immunol Rev. 2006;214:219–28. Available from: CrossRefGoogle Scholar
  68. 68.
    Vitale M, Della Chiesa M, Carlomagno S, Pende D, Aricò M, Moretta L, et al. NK-dependent DC maturation is mediated by TNFalpha and IFNgamma released upon engagement of the NKp30 triggering receptor. Blood. 2005;106:566–71. Available from: CrossRefGoogle Scholar
  69. 69.
    Zingoni A, Sornasse T, Cocks BG, Tanaka Y, Santoni A, Lanier LL. Cross-talk between activated human NK cells and CD4+ T cells via OX40-OX40 ligand interactions. J Immunol. 2004;173:3716–24. Available from: CrossRefGoogle Scholar
  70. 70.
    Krebs P, Barnes MJ, Lampe K, Whitley K, Bahjat KS, Beutler B, et al. NK-cell-mediated killing of target cells triggers robust antigen-specific T-cell-mediated and humoral responses. Blood. 2009;113:6593–602. Available from: CrossRefPubMedCentralGoogle Scholar
  71. 71.
    Rabinovich BA, Li J, Shannon J, Hurren R, Chalupny J, Cosman D, et al. Activated, but not resting, T cells can be recognized and killed by syngeneic NK cells. J Immunol. 2003;170:3572–6. Available from: CrossRefGoogle Scholar
  72. 72.
    Cerboni C, Zingoni A, Cippitelli M, Piccoli M, Frati L, Santoni A. Antigen-activated human T lymphocytes express cell-surface NKG2D ligands via an ATM/ATR-dependent mechanism and become susceptible to autologous NK-cell lysis. Blood. 2007;110:606–15. Available from: CrossRefGoogle Scholar
  73. 73.
    Nielsen N, Ødum N, Ursø B, Lanier LL, Spee P. Cytotoxicity of CD56(bright) NK cells towards autologous activated CD4+ T cells is mediated through NKG2D, LFA-1 and TRAIL and dampened via CD94/NKG2A. PLoS One. 2012;7:e31959. Available from: CrossRefPubMedCentralGoogle Scholar
  74. 74.
    Lee S-H, Kim K-S, Fodil-Cornu N, Vidal SM, Biron CA. Activating receptors promote NK cell expansion for maintenance, IL-10 production, and CD8 T cell regulation during viral infection. J Exp Med. 2009;206:2235–51. Available from: CrossRefPubMedCentralGoogle Scholar
  75. 75.
    Perona-Wright G, Mohrs K, Szaba FM, Kummer LW, Madan R, Karp CL, et al. Systemic but not local infections elicit immunosuppressive IL-10 production by natural killer cells. Cell Host Microbe. 2009;6:503–12. Available from: CrossRefPubMedCentralGoogle Scholar
  76. 76.
    Sun JC, Beilke JN, Lanier LL. Adaptive immune features of natural killer cells. Nature. 2009;457:557–61. Available from: CrossRefPubMedCentralGoogle Scholar
  77. 77.
    Sun JC, Beilke JN, Lanier LL. Immune memory redefined: characterizing the longevity of natural killer cells. Immunol Rev. 2010;236:83–94. Available from: CrossRefPubMedCentralGoogle Scholar
  78. 78.
    Kyaw T, Tipping P, Toh B-H, Bobik A. Killer cells in atherosclerosis. Eur J Pharmacol. 2017;816:67–75. Available from: CrossRefGoogle Scholar
  79. 79.
    Groh V, Bruhl A, El-Gabalawy H, Nelson JL, Spies T. Stimulation of T cell autoreactivity by anomalous expression of NKG2D and its MIC ligands in rheumatoid arthritis. Proc Natl Acad Sci U S A. 2003;100:9452–7. Available from: CrossRefPubMedCentralGoogle Scholar
  80. 80.
    Allez M, Tieng V, Nakazawa A, Treton X, Pacault V, Dulphy N, et al. CD4+NKG2D+ T cells in Crohn’s disease mediate inflammatory and cytotoxic responses through MICA interactions. Gastroenterology. 2007;132:2346–58. Available from: CrossRefGoogle Scholar
  81. 81.
    Popko K, Górska E. The role of natural killer cells in pathogenesis of autoimmune diseases. Cent J Immunol. 2015;40:470–6. Available from: CrossRefGoogle Scholar
  82. 82.
    Spits H, Artis D, Colonna M, Diefenbach A, Di Santo JP, Eberl G, et al. Innate lymphoid cells—a proposal for uniform nomenclature. Nat Rev Immunol. 2013;13:145–9. Available from: CrossRefGoogle Scholar
  83. 83.
    Sonnenberg GF, Mjösberg J, Spits H, Artis D. SnapShot: innate lymphoid cells. Immunity. 2013;39:622–622.e1. Available from: CrossRefGoogle Scholar
  84. 84.
    Walker JA, Barlow JL, McKenzie ANJ. Innate lymphoid cells—how did we miss them? Nat Rev Immunol. 2013;13:75–87. Available from: CrossRefGoogle Scholar
  85. 85.
    Artis D, Spits H. The biology of innate lymphoid cells. Nature. 2015;517:293–301. Available from: CrossRefGoogle Scholar
  86. 86.
    Klose CSN, Artis D. Innate lymphoid cells as regulators of immunity, inflammation and tissue homeostasis. Nat Immunol. 2016;17:765–74. Available from: CrossRefGoogle Scholar
  87. 87.
    Lai D-M, Shu Q, Fan J. The origin and role of innate lymphoid cells in the lung. Mil Med Res. 2016;3:25. Available from: CrossRefPubMedCentralGoogle Scholar
  88. 88.
    Tait Wojno ED, Artis D. Emerging concepts and future challenges in innate lymphoid cell biology. J Exp Med. 2016;213:2229–48. Available from: CrossRefPubMedCentralGoogle Scholar
  89. 89.
    Withers DR. Innate lymphoid cell regulation of adaptive immunity. Immunology. 2016;149:123–30. Available from: CrossRefPubMedCentralGoogle Scholar
  90. 90.
    Narni-Mancinelli E, Gauthier L, Baratin M, Guia S, Fenis A, Deghmane A-E, et al. Complement factor P is a ligand for the natural killer cell-activating receptor NKp46. Sci. Immunol. 2017;2:eaam9628. Available from: CrossRefPubMedCentralGoogle Scholar
  91. 91.
    Fuchs A. ILC1s in tissue inflammation and infection. Front Immunol. 2016;7:104. Available from: CrossRefPubMedCentralGoogle Scholar
  92. 92.
    Saez de Guinoa J, Jimeno R, Farhadi N, Jervis PJ, Cox LR, Besra GS, et al. CD1d-mediated activation of group 3 innate lymphoid cells drives IL-22 production. EMBO Rep. 2017;18:39–47. Available from: CrossRefGoogle Scholar
  93. 93.
    Halim TYF, Steer CA, Mathä L, Gold MJ, Martinez-Gonzalez I, McNagny KM, et al. Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation. Immunity. 2014;40:425–35. Available from: CrossRefPubMedCentralGoogle Scholar
  94. 94.
    Wang W, Erbe AK, DeSantes KB, Sondel PM. Donor selection for ex vivo-expanded natural killer cells as adoptive cancer immunotherapy. Future Oncol. 2017;13:1043–7. Available from: CrossRefGoogle Scholar
  95. 95.
    Perry JSA, Han S, Xu Q, Herman ML, Kennedy LB, Csako G, et al. Inhibition of LTi cell development by CD25 blockade is associated with decreased intrathecal inflammation in multiple sclerosis. Sci Transl Med. 2012;4:145ra106. Available from: CrossRefGoogle Scholar
  96. 96.
    Preiningerova JL, Vachova M. Daclizumab high-yield process in the treatment of relapsing-remitting multiple sclerosis. Ther Adv Neurol Disord. 2017;10:67–75. Available from: CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.University of StrasbourgMolecular ImmunoRheumatology, Laboratory of Excellence TransplantexStrasbourgFrance

Personalised recommendations