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Annual Review of Immunology

Volume 38, 2020

Innate Lymphocyte Mechanisms in Skin Diseases

Abstract

Innate lymphocyte populations are emerging as key effectors in tissue homeostasis, microbial defense, and inflammatory skin disease. The cells are evolutionarily ancient and carry conserved principles of function, which can be achieved through shared or unique specific mechanisms. Recent technological and treatment advances have provided insight into heterogeneity within and between individuals and species. Similar pathways can extend through to adaptive lymphocytes, which softens the margins with innate lymphocyte populations and allows investigation of nonredundant pathways of immunity and inflammation that might be amenable to therapeutic intervention. Here, we review advances in understanding of innate lymphocyte biology with a focus on skin disease and the roles of commensal and pathogen responses and tissue homeostasis.

Keyword(s): innate, lymphocytes, skin
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/content/journals/10.1146/annurev-immunol-082919-093554
2020-04-26
2024-04-23
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Literature Cited

  1. 1. 
    Hayday AC, Vantourout P. 2020. The innate biologies of adaptive antigen receptors. Annu. Rev. Immunol 38:487–510
     [Google Scholar]
  2. 2. 
    Fallon PG, Ballantyne SJ, Mangan NE, Barlow JL, Dasvarma A et al. 2006. Identification of an interleukin (IL)-25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion. J. Exp. Med. 203:1105–16
     [Google Scholar]
  3. 3. 
    Cherrier DE, Serafini N, Di Santo JP 2018. Innate lymphoid cell development: a T cell perspective. Immunity 48:1091–103
     [Google Scholar]
  4. 4. 
    Vivier E, Artis D, Colonna M, Diefenbach A, Di Santo JP et al. 2018. Innate lymphoid cells: 10 years on. Cell 174:1054–66
     [Google Scholar]
  5. 5. 
    Spits H, Artis D, Colonna M, Diefenbach A, Di Santo JP et al. 2013. Innate lymphoid cells—a proposal for uniform nomenclature. Nat. Rev. Immunol. 13:145–49
     [Google Scholar]
  6. 6. 
    Gasteiger G, Fan X, Dikiy S, Lee SY, Rudensky AY 2015. Tissue residency of innate lymphoid cells in lymphoid and nonlymphoid organs. Science 350:981–85
     [Google Scholar]
  7. 7. 
    Kim BS. 2015. Innate lymphoid cells in the skin. J. Investig. Dermatol. 135:673–78
     [Google Scholar]
  8. 8. 
    Bruggen MC, Bauer WM, Reininger B, Clim E, Captarencu C et al. 2016. In situ mapping of innate lymphoid cells in human skin: evidence for remarkable differences between normal and inflamed skin. J. Investig. Dermatol. 136:2396–405
     [Google Scholar]
  9. 9. 
    Satoh-Takayama N, Vosshenrich CA, Lesjean-Pottier S, Sawa S, Lochner M et al. 2008. Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity 29:958–70
     [Google Scholar]
  10. 10. 
    Glatzer T, Killig M, Meisig J, Ommert I, Luetke-Eversloh M et al. 2013. RORγ+ innate lymphoid cells acquire a proinflammatory program upon engagement of the activating receptor NKp44. Immunity 38:1223–35
     [Google Scholar]
  11. 11. 
    Salimi M, Xue L, Jolin H, Hardman C, Cousins DJ et al. 2016. Group 2 innate lymphoid cells express functional NKp30 receptor inducing type 2 cytokine production. J. Immunol. 196:45–54
     [Google Scholar]
  12. 12. 
    Lee JS, Cella M, McDonald KG, Garlanda C, Kennedy GD et al. 2011. AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch. Nat. Immunol. 13:144–51
     [Google Scholar]
  13. 13. 
    Qiu J, Heller JJ, Guo X, Chen ZM, Fish K et al. 2012. The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells. Immunity 36:92–104
     [Google Scholar]
  14. 14. 
    Stockinger B, Hirota K, Duarte J, Veldhoen M 2011. External influences on the immune system via activation of the aryl hydrocarbon receptor. Semin. Immunol. 23:99–105
     [Google Scholar]
  15. 15. 
    Crellin NK, Trifari S, Kaplan CD, Satoh-Takayama N, Di Santo JP, Spits H 2010. Regulation of cytokine secretion in human CD127+ LTi-like innate lymphoid cells by Toll-like receptor 2. Immunity 33:752–64
     [Google Scholar]
  16. 16. 
    Marafini I, Monteleone I, Di Fusco D, Cupi ML, Paoluzi OA et al. 2015. TNF-α producing innate lymphoid cells (ILCs) are increased in active celiac disease and contribute to promote intestinal atrophy in mice. PLOS ONE 10:e0126291
     [Google Scholar]
  17. 17. 
    Xu H, Wang X, Lackner AA, Veazey RS 2015. Type 3 innate lymphoid cell depletion is mediated by TLRs in lymphoid tissues of simian immunodeficiency virus-infected macaques. FASEB J 29:5072–80
     [Google Scholar]
  18. 18. 
    Mjosberg J, Spits H. 2016. Human innate lymphoid cells. J. Allergy Clin. Immunol. 138:1265–76
     [Google Scholar]
  19. 19. 
    Hardman CS, Chen YL, Salimi M, Jarrett R, Johnson D et al. 2017. CD1a presentation of endogenous antigens by group 2 innate lymphoid cells. Sci. Immunol. 2:eaan5918
     [Google Scholar]
  20. 20. 
    Gil ML, Gozalbo D. 2009. Role of Toll-like receptors in systemic Candida albicans infections. Front. Biosci. 14:570–82
     [Google Scholar]
  21. 21. 
    Vu AT, Baba T, Chen X, Le TA, Kinoshita H et al. 2010. Staphylococcus aureus membrane and diacylated lipopeptide induce thymic stromal lymphopoietin in keratinocytes through the Toll-like receptor 2-Toll-like receptor 6 pathway. J. Allergy Clin. Immunol. 126:985–93.e3
     [Google Scholar]
  22. 22. 
    Hvid M, Vestergaard C, Kemp K, Christensen GB, Deleuran B, Deleuran M 2011. IL-25 in atopic dermatitis: a possible link between inflammation and skin barrier dysfunction?. J. Invest. Dermatol. 131:150–57
     [Google Scholar]
  23. 23. 
    Tohyama M, Shirakara Y, Yamasaki K, Sayama K, Hashimoto K 2001. Differentiated keratinocytes are responsible for TNF-α regulated production of macrophage inflammatory protein 3α/CCL20, a potent chemokine for Langerhans cells. J. Dermatol. Sci. 27:130–39
     [Google Scholar]
  24. 24. 
    Yang J, Hu S, Zhao L, Kaplan DH, Perdew GH, Xiong N 2016. Selective programming of CCR10+ innate lymphoid cells in skin-draining lymph nodes for cutaneous homeostatic regulation. Nat. Immunol. 17:48–56
     [Google Scholar]
  25. 25. 
    Kobayashi T, Voisin B, Kim DY, Kennedy EA, Jo JH et al. 2019. Homeostatic control of sebaceous glands by innate lymphoid cells regulates commensal bacteria equilibrium. Cell 176:982–97.e16
     [Google Scholar]
  26. 26. 
    Nussbaum JC, Van Dyken SJ, von Moltke J, Cheng LE, Mohapatra A et al. 2013. Type 2 innate lymphoid cells control eosinophil homeostasis. Nature 502:245–48
     [Google Scholar]
  27. 27. 
    Cardoso V, Chesne J, Ribeiro H, Garcia-Cassani B, Carvalho T et al. 2017. Neuronal regulation of type 2 innate lymphoid cells via neuromedin U. Nature 549:277–81
     [Google Scholar]
  28. 28. 
    Ibiza S, Garcia-Cassani B, Ribeiro H, Carvalho T, Almeida L et al. 2016. Glial-cell-derived neuroregulators control type 3 innate lymphoid cells and gut defence. Nature 535:440–43
     [Google Scholar]
  29. 29. 
    Moriyama S, Brestoff JR, Flamar AL, Moeller JB, Klose CSN et al. 2018. β2-adrenergic receptor-mediated negative regulation of group 2 innate lymphoid cell responses. Science 359:1056–61
     [Google Scholar]
  30. 30. 
    Riol-Blanco L, Ordovas-Montanes J, Perro M, Naval E, Thiriot A et al. 2014. Nociceptive sensory neurons drive interleukin-23-mediated psoriasiform skin inflammation. Nature 510:157–61
     [Google Scholar]
  31. 31. 
    Oetjen LK, Mack MR, Feng J, Whelan TM, Niu H et al. 2017. Sensory neurons co-opt classical immune signaling pathways to mediate chronic itch. Cell 171:217–28.e13
     [Google Scholar]
  32. 32. 
    Halim TY, Steer CA, Matha L, Gold MJ, Martinez-Gonzalez I et al. 2014. Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation. Immunity 40:425–35
     [Google Scholar]
  33. 33. 
    Mirchandani AS, Besnard AG, Yip E, Scott C, Bain CC et al. 2014. Type 2 innate lymphoid cells drive CD4+ Th2 cell responses. J. Immunol. 192:2442–48
     [Google Scholar]
  34. 34. 
    Oliphant CJ, Hwang YY, Walker JA, Salimi M, Wong SH et al. 2014. MHCII-mediated dialog between group 2 innate lymphoid cells and CD4+ T cells potentiates type 2 immunity and promotes parasitic helminth expulsion. Immunity 41:283–95
     [Google Scholar]
  35. 35. 
    Drake LY, Iijima K, Kita H 2014. Group 2 innate lymphoid cells and CD4+ T cells cooperate to mediate type 2 immune response in mice. Allergy 69:1300–7
     [Google Scholar]
  36. 36. 
    Halim TY, Hwang YY, Scanlon ST, Zaghouani H, Garbi N et al. 2016. Group 2 innate lymphoid cells license dendritic cells to potentiate memory TH2 cell responses. Nat. Immunol. 17:57–64
     [Google Scholar]
  37. 37. 
    Hepworth MR, Monticelli LA, Fung TC, Ziegler CG, Grunberg S et al. 2013. Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria. Nature 498:113–17
     [Google Scholar]
  38. 38. 
    von Burg N, Chappaz S, Baerenwaldt A, Horvath E, Bose Dasgupta S et al. 2014. Activated group 3 innate lymphoid cells promote T-cell-mediated immune responses. PNAS 111:12835–40
     [Google Scholar]
  39. 39. 
    Saez de Guinoa J, Jimeno R, Farhadi N, Jervis PJ, Cox LR et al. 2017. CD1d-mediated activation of group 3 innate lymphoid cells drives IL-22 production. EMBO Rep 18:39–47
     [Google Scholar]
  40. 40. 
    Gour N, Smole U, Yong HM, Lewkowich IP, Yao N et al. 2018. C3a is required for ILC2 function in allergic airway inflammation. Mucosal. Immunol. 11:1653–62
     [Google Scholar]
  41. 41. 
    Kim BS, Wang K, Siracusa MC, Saenz SA, Brestoff JR et al. 2014. Basophils promote innate lymphoid cell responses in inflamed skin. J. Immunol. 193:3717–25
     [Google Scholar]
  42. 42. 
    Motomura Y, Morita H, Moro K, Nakae S, Artis D et al. 2014. Basophil-derived interleukin-4 controls the function of natural helper cells, a member of ILC2s, in lung inflammation. Immunity 40:758–71
     [Google Scholar]
  43. 43. 
    Barnig C, Cernadas M, Dutile S, Liu X, Perrella MA et al. 2013. Lipoxin A4 regulates natural killer cell and type 2 innate lymphoid cell activation in asthma. Sci. Transl. Med. 5:174ra26
     [Google Scholar]
  44. 44. 
    Roediger B, Kyle R, Yip KH, Sumaria N, Guy TV et al. 2013. Cutaneous immunosurveillance and regulation of inflammation by group 2 innate lymphoid cells. Nat. Immunol. 14:564–73
     [Google Scholar]
  45. 45. 
    Xue L, Salimi M, Panse I, Mjosberg JM, McKenzie AN et al. 2014. Prostaglandin D2 activates group 2 innate lymphoid cells through chemoattractant receptor-homologous molecule expressed on TH2 cells. J. Allergy Clin. Immunol. 133:1184–94
     [Google Scholar]
  46. 46. 
    Salimi M, Stoger L, Liu W, Go S, Pavord I et al. 2017. Cysteinyl leukotriene E4 activates human group 2 innate lymphoid cells and enhances the effect of prostaglandin D2 and epithelial cytokines. J. Allergy Clin. Immunol. 140:1090–100.e11
     [Google Scholar]
  47. 47. 
    Lefrancais E, Duval A, Mirey E, Roga S, Espinosa E et al. 2014. Central domain of IL-33 is cleaved by mast cell proteases for potent activation of group-2 innate lymphoid cells. PNAS 111:15502–7
     [Google Scholar]
  48. 48. 
    Shih HY, Sciume G, Mikami Y, Guo L, Sun HW et al. 2016. Developmental acquisition of regulomes underlies innate lymphoid cell functionality. Cell 165:1120–33
     [Google Scholar]
  49. 49. 
    Salimi M, Barlow JL, Saunders SP, Xue L, Gutowska-Owsiak D et al. 2013. A role for IL-25 and IL-33-driven type-2 innate lymphoid cells in atopic dermatitis. J. Exp. Med. 210:2939–50
     [Google Scholar]
  50. 50. 
    Victor AR, Nalin AP, Dong W, McClory S, Wei M et al. 2017. IL-18 drives ILC3 proliferation and promotes IL-22 production via NF-κB. J. Immunol. 199:2333–42
     [Google Scholar]
  51. 51. 
    Gladiator A, Wangler N, Trautwein-Weidner K, LeibundGut-Landmann S 2013. Cutting edge: IL-17-secreting innate lymphoid cells are essential for host defense against fungal infection. J. Immunol. 190:521–25
     [Google Scholar]
  52. 52. 
    Li Z, Hodgkinson T, Gothard EJ, Boroumand S, Lamb R et al. 2016. Epidermal Notch1 recruits RORγ+ group 3 innate lymphoid cells to orchestrate normal skin repair. Nat. Commun. 7:11394
     [Google Scholar]
  53. 53. 
    Rak GD, Osborne LC, Siracusa MC, Kim BS, Wang K et al. 2016. IL-33-dependent group 2 innate lymphoid cells promote cutaneous wound healing. J. Investig. Dermatol. 136:487–96
     [Google Scholar]
  54. 54. 
    Teunissen MBM, Munneke JM, Bernink JH, Spuls PI, Res PCM et al. 2014. Composition of innate lymphoid cell subsets in the human skin: enrichment of NCR+ ILC3 in lesional skin and blood of psoriasis patients. J. Investig. Dermatol. 134:2351–60
     [Google Scholar]
  55. 55. 
    Villanova F, Flutter B, Tosi I, Grys K, Sreeneebus H et al. 2014. Characterization of innate lymphoid cells in human skin and blood demonstrates increase of NKp44+ ILC3 in psoriasis. J. Investig. Dermatol. 134:984–91
     [Google Scholar]
  56. 56. 
    Fuchs A, Vermi W, Lee JS, Lonardi S, Gilfillan S et al. 2013. Intraepithelial type 1 innate lymphoid cells are a unique subset of IL-12- and IL-15-responsive IFN-γ-producing cells. Immunity 38:769–81
     [Google Scholar]
  57. 57. 
    Klose CS, Kiss EA, Schwierzeck V, Ebert K, Hoyler T et al. 2013. A T-bet gradient controls the fate and function of CCR6-RORγt+ innate lymphoid cells. Nature 494:261–65
     [Google Scholar]
  58. 58. 
    Bernink JH, Peters CP, Munneke M, te Velde AA, Meijer SL et al. 2013. Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat. Immunol. 14:221–29
     [Google Scholar]
  59. 59. 
    Rankin LC, Groom JR, Chopin M, Herold MJ, Walker JA et al. 2013. The transcription factor T-bet is essential for the development of NKp46+ innate lymphocytes via the Notch pathway. Nat. Immunol. 14:389–95
     [Google Scholar]
  60. 60. 
    Vonarbourg C, Mortha A, Bui VL, Hernandez PP, Kiss EA et al. 2010. Regulated expression of nuclear receptor RORγt confers distinct functional fates to NK cell receptor-expressing RORγt+ innate lymphocytes. Immunity 33:736–51
     [Google Scholar]
  61. 61. 
    Wang X, Peng H, Cong J, Wang X, Lian Z et al. 2018. Memory formation and long-term maintenance of IL-7Rα+ ILC1s via a lymph node-liver axis. Nat. Commun. 9:4854
     [Google Scholar]
  62. 62. 
    Carbone T, Nasorri F, Pennino D, Eyerich K, Foerster S et al. 2010. CD56highCD16−CD62L− NK cells accumulate in allergic contact dermatitis and contribute to the expression of allergic responses. J. Immunol. 184:1102–10
     [Google Scholar]
  63. 63. 
    Vosshenrich CA, Garcia-Ojeda ME, Samson-Villeger SI, Pasqualetto V, Enault L et al. 2006. A thymic pathway of mouse natural killer cell development characterized by expression of GATA-3 and CD127. Nat. Immunol. 7:1217–24
     [Google Scholar]
  64. 64. 
    Imai Y, Yasuda K, Sakaguchi Y, Haneda T, Mizutani H et al. 2013. Skin-specific expression of IL-33 activates group 2 innate lymphoid cells and elicits atopic dermatitis-like inflammation in mice. PNAS 110:13921–26
     [Google Scholar]
  65. 65. 
    Kim BS, Siracusa MC, Saenz SA, Noti M, Monticelli LA et al. 2013. TSLP elicits IL-33-independent innate lymphoid cell responses to promote skin inflammation. Sci. Transl. Med. 5:170ra16
     [Google Scholar]
  66. 66. 
    Ricardo-Gonzalez RR, Van Dyken SJ, Schneider C, Lee J, Nussbaum JC et al. 2018. Tissue signals imprint ILC2 identity with anticipatory function. Nat. Immunol. 19:1093–99
     [Google Scholar]
  67. 67. 
    Konishi H, Tsutsui H, Murakami T, Yumikura-Futatsugi S, Yamanaka K et al. 2002. IL-18 contributes to the spontaneous development of atopic dermatitis-like inflammatory skin lesion independently of IgE/stat6 under specific pathogen-free conditions. PNAS 99:11340–45
     [Google Scholar]
  68. 68. 
    Zedan K, Rasheed Z, Farouk Y, Alzolibani AA, Bin Saif G et al. 2015. Immunoglobulin E, interleukin-18 and interleukin-12 in patients with atopic dermatitis: correlation with disease activity. J. Clin. Diagn. Res. 9:WC01–5
     [Google Scholar]
  69. 69. 
    Ferreira MA, Vonk JM, Baurecht H, Marenholz I, Tian C et al. 2017. Shared genetic origin of asthma, hay fever and eczema elucidates allergic disease biology. Nat. Genet. 49:1752–57
     [Google Scholar]
  70. 70. 
    Palmer CN, Irvine AD, Terron-Kwiatkowski A, Zhao Y, Liao H et al. 2006. Common loss-of-function variants of the epidermal barrier protein filaggrin are a major predisposing factor for atopic dermatitis. Nat. Genet. 38:441–46
     [Google Scholar]
  71. 71. 
    Trautmann A, Altznauer F, Akdis M, Simon HU, Disch R et al. 2001. The differential fate of cadherins during T-cell-induced keratinocyte apoptosis leads to spongiosis in eczematous dermatitis. J. Investig. Dermatol. 117:927–34
     [Google Scholar]
  72. 72. 
    Pantelyushin S, Haak S, Ingold B, Kulig P, Heppner FL et al. 2012. RORγt+ innate lymphocytes and γδ T cells initiate psoriasiform plaque formation in mice. J. Clin. Investig. 122:2252–56
     [Google Scholar]
  73. 73. 
    Dyring-Andersen B, Geisler C, Agerbeck C, Lauritsen JP, Gudjonsdottir SD et al. 2014. Increased number and frequency of group 3 innate lymphoid cells in nonlesional psoriatic skin. Br. J. Dermatol. 170:609–16
     [Google Scholar]
  74. 74. 
    Czarnowicki T, Gonzalez J, Shemer A, Malajian D, Xu H et al. 2015. Severe atopic dermatitis is characterized by selective expansion of circulating TH2/TC2 and TH22/TC22, but not TH17/TC17, cells within the skin-homing T-cell population. J. Allergy Clin. Immunol. 136:104–15.e7
     [Google Scholar]
  75. 75. 
    Zheng Y, Danilenko DM, Valdez P, Kasman I, Eastham-Anderson J et al. 2007. Interleukin-22, a TH17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 445:648–51
     [Google Scholar]
  76. 76. 
    Gaggero S, Bruschi M, Petretto A, Parodi M, Zotto GD et al. 2018. Nidogen-1 is a novel extracellular ligand for the NKp44 activating receptor. Oncoimmunology 7:e1470730
     [Google Scholar]
  77. 77. 
    Luci C, Reynders A, Ivanov II, Cognet C, Chiche L et al. 2009. Influence of the transcription factor RORγt on the development of NKp46+ cell populations in gut and skin. Nat. Immunol. 10:75–82
     [Google Scholar]
  78. 78. 
    Carrega P, Ferlazzo G. 2012. Natural killer cell distribution and trafficking in human tissues. Front. Immunol. 3:347
     [Google Scholar]
  79. 79. 
    Mace EM, Orange JS. 2019. Emerging insights into human health and NK cell biology from the study of NK cell deficiencies. Immunol. Rev. 287:202–25
     [Google Scholar]
  80. 80. 
    Ebert LM, Meuter S, Moser B 2006. Homing and function of human skin γδ T cells and NK cells: relevance for tumor surveillance. J. Immunol. 176:4331–36
     [Google Scholar]
  81. 81. 
    Placek K, Schultze JL, Netea MG 2019. Immune memory characteristics of innate lymphoid cells. Curr. Opin. Infect. Dis. 32:196–203
     [Google Scholar]
  82. 82. 
    Netea MG, Schlitzer A, Placek K, Joosten LAB, Schultze JL 2019. Innate and adaptive immune memory: an evolutionary continuum in the host's response to pathogens. Cell Host Microbe 25:13–26
     [Google Scholar]
  83. 83. 
    Nikzad R, Angelo LS, Aviles-Padilla K, Le DT, Singh VK et al. 2019. Human natural killer cells mediate adaptive immunity to viral antigens. Sci. Immunol. 4:eaat8116
     [Google Scholar]
  84. 84. 
    Kawakami Y, Tomimori Y, Yumoto K, Hasegawa S, Ando T et al. 2009. Inhibition of NK cell activity by IL-17 allows vaccinia virus to induce severe skin lesions in a mouse model of eczema vaccinatum. J. Exp. Med. 206:1219–25
     [Google Scholar]
  85. 85. 
    Buentke E, Heffler LC, Wilson JL, Wallin RP, Lofman C et al. 2002. Natural killer and dendritic cell contact in lesional atopic dermatitis skin—Malassezia-influenced cell interaction. J. Investig. Dermatol. 119:850–57
     [Google Scholar]
  86. 86. 
    Katsuta M, Takigawa Y, Kimishima M, Inaoka M, Takahashi R, Shiohara T 2006. NK cells and γδ+ T cells are phenotypically and functionally defective due to preferential apoptosis in patients with atopic dermatitis. J. Immunol. 176:7736–44
     [Google Scholar]
  87. 87. 
    Aktas E, Akdis M, Bilgic S, Disch R, Falk CS et al. 2005. Different natural killer (NK) receptor expression and immunoglobulin E (IgE) regulation by NK1 and NK2 cells. Clin. Exp. Immunol. 140:301–9
     [Google Scholar]
  88. 88. 
    Hall TJ, Rycroft R, Brostoff J 1985. Decreased natural killer cell activity in atopic eczema. Immunology 56:337–44
     [Google Scholar]
  89. 89. 
    Lever RS, Lesko MJ, MacKie RM, Parrott DM 1985. Natural killer cell activity in atopic dermatitis: a sequential study. Clin. Allergy 15:479–86
     [Google Scholar]
  90. 90. 
    Shimada Y, Sato S, Hasegawa M, Tedder TF, Takehara K 1999. Elevated serum L-selectin levels and abnormal regulation of L-selectin expression on leukocytes in atopic dermatitis: Soluble L-selectin levels indicate disease severity. J. Allergy Clin. Immunol. 104:163–68
     [Google Scholar]
  91. 91. 
    Dunphy S, Gardiner CM. 2011. NK cells and psoriasis. J. Biomed. Biotechnol. 2011:248317
     [Google Scholar]
  92. 92. 
    Batista MD, Ho EL, Kuebler PJ, Milush JM, Lanier LL et al. 2013. Skewed distribution of natural killer cells in psoriasis skin lesions. Exp. Dermatol. 22:64–66
     [Google Scholar]
  93. 93. 
    Ottaviani C, Nasorri F, Bedini C, de Pita O, Girolomoni G, Cavani A 2006. CD56brightCD16− NK cells accumulate in psoriatic skin in response to CXCL10 and CCL5 and exacerbate skin inflammation. Eur. J. Immunol. 36:118–28
     [Google Scholar]
  94. 94. 
    Bjorkstrom NK, Ljunggren HG, Michaelsson J 2016. Emerging insights into natural killer cells in human peripheral tissues. Nat. Rev. Immunol. 16:310–20
     [Google Scholar]
  95. 95. 
    Parolini S, Santoro A, Marcenaro E, Luini W, Massardi L et al. 2007. The role of chemerin in the colocalization of NK and dendritic cell subsets into inflamed tissues. Blood 109:3625–32
     [Google Scholar]
  96. 96. 
    Vermi W, Riboldi E, Wittamer V, Gentili F, Luini W et al. 2005. Role of ChemR23 in directing the migration of myeloid and plasmacytoid dendritic cells to lymphoid organs and inflamed skin. J. Exp. Med. 201:509–15
     [Google Scholar]
  97. 97. 
    Wittamer V, Franssen JD, Vulcano M, Mirjolet JF, Le Poul E et al. 2003. Specific recruitment of antigen-presenting cells by chemerin, a novel processed ligand from human inflammatory fluids. J. Exp. Med. 198:977–85
     [Google Scholar]
  98. 98. 
    Albanesi C, Scarponi C, Pallotta S, Daniele R, Bosisio D et al. 2009. Chemerin expression marks early psoriatic skin lesions and correlates with plasmacytoid dendritic cell recruitment. J. Exp. Med. 206:249–58
     [Google Scholar]
  99. 99. 
    Cavani A, De Pita O, Girolomoni G 2007. New aspects of the molecular basis of contact allergy. Curr. Opin. Allergy Clin. Immunol. 7:404–8
     [Google Scholar]
  100. 100. 
    van den Boorn JG, Jakobs C, Hagen C, Renn M, Luiten RM et al. 2016. Inflammasome-dependent induction of adaptive NK cell memory. Immunity 44:1406–21
     [Google Scholar]
  101. 101. 
    Malhotra N, Leyva-Castillo JM, Jadhav U, Barreiro O, Kam C et al. 2018. RORα-expressing T regulatory cells restrain allergic skin inflammation. Sci. Immunol. 3:eaao6923
     [Google Scholar]
  102. 102. 
    Provine NM, Klenerman P. 2020. MAIT cells in health and disease. Annu. Rev. Immunol. 38:203–28
     [Google Scholar]
  103. 103. 
    Porcelli S, Yockey CE, Brenner MB, Balk SP 1993. Analysis of T-cell antigen receptor (TCR) expression by human peripheral blood CD4−8− α/β T-cells demonstrates preferential use of several V β genes and an invariant TCR α chain. J. Exp. Med. 178:1–16
     [Google Scholar]
  104. 104. 
    Treiner E, Duban L, Bahram S, Radosavljevic M, Wanner V et al. 2003. Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature 422:164–69
     [Google Scholar]
  105. 105. 
    Kumar V, Ahmad A. 2018. Role of MAIT cells in the immunopathogenesis of inflammatory diseases: new players in old game. Int. Rev. Immunol. 37:90–110
     [Google Scholar]
  106. 106. 
    Gibbs A, Leeansyah E, Introini A, Paquin-Proulx D, Hasselrot K et al. 2017. MAIT cells reside in the female genital mucosa and are biased towards IL-17 and IL-22 production in response to bacterial stimulation. Mucosal. Immunol. 10:35–45
     [Google Scholar]
  107. 107. 
    Teunissen MBM, Yeremenko NG, Baeten DLP, Chielie S, Spuls PI et al. 2014. The IL-17A-producing CD8+ T-cell population in psoriatic lesional skin comprises mucosa-associated invariant T cells and conventional T cells. J. Investig. Dermatol. 134:2898–907
     [Google Scholar]
  108. 108. 
    Li J, Reantragoon R, Kostenko L, Corbett AJ, Varigos G, Carbone FR 2017. The frequency of mucosal-associated invariant T cells is selectively increased in dermatitis herpetiformis. Australas. J. Dermatol. 58:200–4
     [Google Scholar]
  109. 109. 
    Billerbeck E, Kang YH, Walker L, Lockstone H, Grafmueller S et al. 2010. Analysis of CD161 expression on human CD8+ T cells defines a distinct functional subset with tissue-homing properties. PNAS 107:3006–11
     [Google Scholar]
  110. 110. 
    Johnston A, Gudjonsson JE. 2014. Psoriasis and the MAITing game: a role for IL-17A+ invariant TCR CD8+ T cells in psoriasis. ? J. Investig. Dermatol. 134:2864–66
     [Google Scholar]
  111. 111. 
    Mortezavi M, Ritchlin C. 2015. Immunologic advances reveal new therapeutic targets in psoriasis and psoriatic arthritis. Discov. Med. 20:169–75
     [Google Scholar]
  112. 112. 
    Barral DC, Brenner MB. 2007. CD1 antigen presentation: how it works. Nat. Rev. Immunol. 7:929–41
     [Google Scholar]
  113. 113. 
    Chancellor A, Tocheva AS, Cave-Ayland C, Tezera L, White A et al. 2017. CD1b-restricted GEM T cell responses are modulated by Mycobacterium tuberculosis mycolic acid meromycolate chains. PNAS 114:E10956–64
     [Google Scholar]
  114. 114. 
    Gras S, Van Rhijn I, Shahine A, Cheng TY, Bhati M et al. 2016. T cell receptor recognition of CD1b presenting a mycobacterial glycolipid. Nat. Commun. 7:13257
     [Google Scholar]
  115. 115. 
    de Jong A, Cheng TY, Huang S, Gras S, Birkinshaw RW et al. 2014. CD1a-autoreactive T cells recognize natural skin oils that function as headless antigens. Nat. Immunol. 15:177–85
     [Google Scholar]
  116. 116. 
    Kobayashi C, Shiina T, Tokioka A, Hattori Y, Komori T et al. 2012. GM-CSF-independent CD1a expression in epidermal Langerhans cells: evidence from human CD1A genome-transgenic mice. J. Investig. Dermatol. 132:241–44
     [Google Scholar]
  117. 117. 
    Birkinshaw RW, Pellicci DG, Cheng TY, Keller AN, Sandoval-Romero M et al. 2015. αβ T cell antigen receptor recognition of CD1a presenting self lipid ligands. Nat. Immunol. 16:258–66
     [Google Scholar]
  118. 118. 
    Li D, Wang L, Yu L, Freundt EC, Jin B et al. 2009. Ig-like transcript 4 inhibits lipid antigen presentation through direct CD1d interaction. J. Immunol. 182:1033–40
     [Google Scholar]
  119. 119. 
    Sugita M, van der Wel N, Rogers RA, Peters PJ, Brenner MB 2000. CD1c molecules broadly survey the endocytic system. PNAS 97:8445–50
     [Google Scholar]
  120. 120. 
    Sugita M, Grant EP, van Donselaar E, Hsu VW, Rogers RA et al. 1999. Separate pathways for antigen presentation by CD1 molecules. Immunity 11:743–52
     [Google Scholar]
  121. 121. 
    de Jong A, Peña-Cruz V, Cheng T-Y, Clark RA, Van Rhijn I, Moody DB 2010. CD1a-autoreactive T cells are a normal component of the human αβ T cell repertoire. Nat. Immunol. 11:1102–9
     [Google Scholar]
  122. 122. 
    de Lalla C, Lepore M, Piccolo FM, Rinaldi A, Scelfo A et al. 2011. High-frequency and adaptive-like dynamics of human CD1 self-reactive T cells. Eur. J. Immunol. 41:602–10
     [Google Scholar]
  123. 123. 
    Wun KS, Reijneveld JF, Cheng T-Y, Ladell K, Uldrich AP et al. 2018. T cell autoreactivity directed toward CD1c itself rather than toward carried self lipids. Nat. Immunol. 19:397–406
     [Google Scholar]
  124. 124. 
    Cerny D, Thi Le DH, The TD, Zuest R, Kg S et al. 2016. Complete human CD1a deficiency on Langerhans cells due to a rare point mutation in the coding sequence. J. Allergy Clin. Immunol. 138:1709–12.e11
     [Google Scholar]
  125. 125. 
    Seshadri C, Shenoy M, Wells RD, Hensley-McBain T, Andersen-Nissen E et al. 2013. Human CD1a deficiency is common and genetically regulated. J. Immunol. 191:1586–93
     [Google Scholar]
  126. 126. 
    Jarrett R, Salio M, Lloyd-Lavery A, Subramaniam S, Bourgeois E et al. 2016. Filaggrin inhibits generation of CD1a neolipid antigens by house dust mite-derived phospholipase. Sci. Transl. Med. 8:325ra18
     [Google Scholar]
  127. 127. 
    Bourgeois EA, Subramaniam S, Cheng TY, De Jong A, Layre E et al. 2015. Bee venom processes human skin lipids for presentation by CD1a. J. Exp. Med. 212:149–63
     [Google Scholar]
  128. 128. 
    Subramaniam S, Aslam A, Misbah SA, Salio M, Cerundolo V et al. 2016. Elevated and cross-responsive CD1a-reactive T cells in bee and wasp venom allergic individuals. Eur. J. Immunol. 46:242–52
     [Google Scholar]
  129. 129. 
    Kim JH, Hu Y, Yongqing T, Kim J, Hughes VA et al. 2016. CD1a on Langerhans cells controls inflammatory skin disease. Nat. Immunol. 17:1159–66
     [Google Scholar]
  130. 130. 
    Agea E, Russano A, Bistoni O, Mannucci R, Nicoletti I et al. 2005. Human CD1-restricted T cell recognition of lipids from pollens. J. Exp. Med. 202:295–308
     [Google Scholar]
  131. 131. 
    Betts RJ, Perkovic A, Mahapatra S, Del Bufalo A, Camara K et al. 2017. Contact sensitizers trigger human CD1-autoreactive T-cell responses. Eur. J. Immunol. 47:1171–80
     [Google Scholar]
  132. 132. 
    Kuo IH, Yoshida T, De Benedetto A, Beck LA 2013. The cutaneous innate immune response in patients with atopic dermatitis. J. Allergy Clin. Immunol. 131:266–78
     [Google Scholar]
  133. 133. 
    Belkaid Y, Tamoutounour S. 2016. The influence of skin microorganisms on cutaneous immunity. Nat. Rev. Immunol. 16:353–66
     [Google Scholar]
  134. 134. 
    Naik S, Bouladoux N, Wilhelm C, Molloy MJ, Salcedo R et al. 2012. Compartmentalized control of skin immunity by resident commensals. Science 337:1115–19
     [Google Scholar]
  135. 135. 
    Nascimento CR, Freire-de-Lima CG, da Silva de Oliveira A, Rumjanek FD, Rumjanek VM 2011. The short chain fatty acid sodium butyrate regulates the induction of CD1a in developing dendritic cells. Immunobiology 216:275–84
     [Google Scholar]
  136. 136. 
    De Libero G, Moran AP, Gober H-J, Rossy E, Shamshiev A et al. 2005. Bacterial infections promote T cell recognition of self-glycolipids. Immunity 22:763–72
     [Google Scholar]
  137. 137. 
    Hunger RE, Sieling PA, Ochoa MT, Sugaya M, Burdick AE et al. 2004. Langerhans cells utilize CD1a and langerin to efficiently present nonpeptide antigens to T cells. J. Clin. Investig. 113:701–8
     [Google Scholar]
  138. 138. 
    Young DC, Kasmar A, Moraski G, Cheng T-Y, Walz AJ et al. 2009. Synthesis of dideoxymycobactin antigens presented by CD1a reveals T cell fine specificity for natural lipopeptide structures. J. Biol. Chem. 284:25087–96
     [Google Scholar]
  139. 139. 
    Gros E, Bussmann C, Bieber T, Förster I, Novak N 2009. Expression of chemokines and chemokine receptors in lesional and nonlesional upper skin of patients with atopic dermatitis. J. Allergy Clin. Immunol. 124:753–60.e1
     [Google Scholar]
  140. 140. 
    Taylor RS, Baadsgaard O, Hammerberg C, Cooper KD 1991. Hyperstimulatory CD1a+CD1b+CD36+ Langerhans cells are responsible for increased autologous T lymphocyte reactivity to lesional epidermal cells of patients with atopic dermatitis. J. Immunol. 147:3794–802
     [Google Scholar]
  141. 141. 
    Lind SM, Kuylenstierna C, Moll M, Jordö ED, Winqvist O et al. 2009. IL-18 skews the invariant NKT-cell population via autoreactive activation in atopic eczema. Eur. J. Immunol. 39:2293–301
     [Google Scholar]
  142. 142. 
    Goubier A, Vocanson M, Macari C, Poyet G, Herbelin A et al. 2013. Invariant NKT cells suppress CD8+ T-cell–mediated allergic contact dermatitis independently of regulatory CD4+ T cells. J. Investig. Dermatol. 133:980–87
     [Google Scholar]
  143. 143. 
    Cheung KL, Jarrett R, Subramaniam S, Salimi M, Gutowska-Owsiak D et al. 2016. Psoriatic T cells recognize neolipid antigens generated by mast cell phospholipase delivered by exosomes and presented by CD1a. J. Exp. Med. 213:2399–412
     [Google Scholar]
  144. 144. 
    Bagchi S, He Y, Zhang H, Cao L, Rhijn IV et al. 2017. CD1b-autoreactive T cells contribute to hyperlipidemia-induced skin inflammation in mice. J. Clin. Investig. 127:2339–52
     [Google Scholar]
  145. 145. 
    Bagchi S, Genardi S, Wang C-R 2018. Linking CD1-restricted T cells with autoimmunity and dyslipidemia: Lipid levels matter. Front. Immunol. 9:1616
     [Google Scholar]
  146. 146. 
    Zhao Y, Fishelevich R, Petrali JP, Zheng L, Anatolievna MA et al. 2008. Activation of keratinocyte protein kinase Cζ in psoriasis plaques. J. Investig. Dermatol. 128:2190–97
     [Google Scholar]
  147. 147. 
    Bonish B, Jullien D, Dutronc Y, Huang BB, Modlin R et al. 2000. Overexpression of CD1d by keratinocytes in psoriasis and CD1d-dependent IFN-γ production by NK-T cells. J. Immunol. 165:4076–85
     [Google Scholar]
  148. 148. 
    Nickoloff BJ, Bonish B, Huang BB, Porcelli SA 2000. Characterization of a T cell line bearing natural killer receptors and capable of creating psoriasis in a SCID mouse model system. J. Dermatol. Sci. 24:212–25
     [Google Scholar]
  149. 149. 
    Moodycliffe AM, Nghiem D, Clydesdale G, Ullrich SE 2000. Immune suppression and skin cancer development: regulation by NKT cells. Nat. Immunol. 1:521–25
     [Google Scholar]
  150. 150. 
    Shevchuk Z, Filip A, Shevchuk V, Kashuba E 2014. Number of Langerhans cells is decreased in premalignant keratosis and skin cancers. Exp. Oncol. 36:34–37
     [Google Scholar]
  151. 151. 
    Gerlini G, Tun-Kyi A, Dudli C, Burg G, Pimpinelli N, Nestle FO 2004. Metastatic melanoma secreted IL-10 down-regulates CD1 molecules on dendritic cells in metastatic tumor lesions. Am. J. Pathol. 165:1853–63
     [Google Scholar]
  152. 152. 
    Berthier-Vergnes O, Gaucherand M, Peguet-Navarro J, Plouet J, Pageaux JF et al. 2001. Human melanoma cells inhibit the earliest differentiation steps of human Langerhans cell precursors but failed to affect the functional maturation of epidermal Langerhans cells. Br. J. Cancer 85:1944–51
     [Google Scholar]
  153. 153. 
    Eisenthal A, Polyvkin N, Bramante-Schreiber L, Misonznik F, Hassner A, Lifschitz-Mercer B 2001. Expression of dendritic cells in ovarian tumors correlates with clinical outcome in patients with ovarian cancer. Hum. Pathol. 32:803–7
     [Google Scholar]
  154. 154. 
    Goldman SA, Baker E, Weyant RJ, Clarke MR, Myers JN, Lotze MT 1998. Peritumoral CD1a-positive dendritic cells are associated with improved survival in patients with tongue carcinoma. Arch. Otolaryngol. Head Neck Surg. 124:641–46
     [Google Scholar]
  155. 155. 
    Tahir SM, Cheng O, Shaulov A, Koezuka Y, Bubley GJ et al. 2001. Loss of IFN-γ production by invariant NK T cells in advanced cancer. J. Immunol. 167:4046–50
     [Google Scholar]
  156. 156. 
    Dhodapkar MV, Geller MD, Chang DH, Shimizu K, Fujii S-I et al. 2003. A reversible defect in natural killer T cell function characterizes the progression of premalignant to malignant multiple myeloma. J. Exp. Med. 197:1667–76
     [Google Scholar]
  157. 157. 
    Yanagisawa K, Seino K-I, Ishikawa Y, Nozue M, Todoroki T, Fukao K 2002. Impaired proliferative response of Vα24 NKT cells from cancer patients against α-galactosylceramide. J. Immunol. 168:6494–99
     [Google Scholar]
  158. 158. 
    Taniguchi M, Tashiro T, Dashtsoodol N, Hongo N, Watarai H 2010. The specialized iNKT cell system recognizes glycolipid antigens and bridges the innate and acquired immune systems with potential applications for cancer therapy. Int. Immunol. 22:1–6
     [Google Scholar]
  159. 159. 
    Cui J, Shin T, Kawano T, Sato H, Kondo E et al. 1997. Requirement for Vα14 NKT cells in IL-12-mediated rejection of tumors. Science 278:1623–26
     [Google Scholar]
  160. 160. 
    Crowe NY, Coquet JM, Berzins SP, Kyparissoudis K, Keating R et al. 2005. Differential antitumor immunity mediated by NKT cell subsets in vivo. J. Exp. Med. 202:1279–88
     [Google Scholar]
  161. 161. 
    Wolf BJ, Choi JE, Exley MA 2018. Novel approaches to exploiting invariant NKT cells in cancer immunotherapy. Front. Immunol. 9:384
     [Google Scholar]
  162. 162. 
    García P, Llano M, de Heredia AB, Willberg CB, Caparrós E et al. 2002. Human T cell receptor-mediated recognition of HLA-E. Eur. J. Immunol. 32:936–44
     [Google Scholar]
  163. 163. 
    Braud VM, Allan DS, O'Callaghan CA, Soderstrom K, D'Andrea A et al. 1998. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391:795–99
     [Google Scholar]
  164. 164. 
    Harriff MJ, Wolfe LM, Swarbrick G, Null M, Cansler ME et al. 2017. HLA-E presents glycopeptides from the Mycobacterium tuberculosis protein MPT32 to human CD8+ T cells. Sci. Rep. 7:4622
     [Google Scholar]
  165. 165. 
    Zeng X, Chen H, Gupta R, Paz-Altschul O, Bowcock AM, Liao W 2013. Deletion of the activating NKG2C receptor and a functional polymorphism in its ligand HLA-E in psoriasis susceptibility. Exp. Dermatol. 22:679–81
     [Google Scholar]
  166. 166. 
    Valés-Gómez M, Reyburn HT, Erskine RA, López-Botet M, Strominger JL 1999. Kinetics and peptide dependency of the binding of the inhibitory NK receptor CD94/NKG2-A and the activating receptor CD94/NKG2-C to HLA-E. EMBO J 18:4250–60
     [Google Scholar]
  167. 167. 
    Morel E, Escamochero S, Cabañas R, Díaz R, Fiandor A, Bellón T 2010. CD94/NKG2C is a killer effector molecule in patients with Stevens-Johnson syndrome and toxic epidermal necrolysis. J. Allergy Clin. Immunol. 125:703–10.e8
     [Google Scholar]
  168. 168. 
    Michaëlsson J, Teixeira de Matos C, Achour A, Lanier LL, Kärre K, Söderström K 2002. A signal peptide derived from hsp60 binds HLA-E and interferes with CD94/NKG2A recognition. J. Exp. Med. 196:1403–14
     [Google Scholar]
  169. 169. 
    Seung NR, Park EJ, Kim CW, Kim KH, Kim KJ et al. 2007. Comparison of expression of heat-shock protein 60, Toll-like receptors 2 and 4, and T-cell receptor γδ in plaque and guttate psoriasis. J. Cutaneous Pathol. 34:903–11
     [Google Scholar]
  170. 170. 
    Tremante E, Ginebri A, Lo Monaco E, Benassi B, Frascione P et al. 2014. A melanoma immune response signature including Human Leukocyte Antigen-E. Pigment Cell Melanoma Res 27:103–12
     [Google Scholar]
  171. 171. 
    Derré L, Corvaisier M, Charreau B, Moreau A, Godefroy E et al. 2006. Expression and release of HLA-E by melanoma cells and melanocytes: potential impact on the response of cytotoxic effector cells. J. Immunol. 177:3100–7
     [Google Scholar]
  172. 172. 
    Lo Monaco E, Tremante E, Cerboni C, Melucci E, Sibilio L et al. 2011. Human leukocyte antigen E contributes to protect tumor cells from lysis by natural killer cells. Neoplasia 13:822–30
     [Google Scholar]
  173. 173. 
    Wang X, Cui Y, Luo G, Wang Q, Hu J et al. 2012. Activated mouse CD4+Foxp3− T cells facilitate melanoma metastasis via Qa-1-dependent suppression of NK-cell cytotoxicity. Cell Res 22:1696–706
     [Google Scholar]
  174. 174. 
    Oliveira CC, van Veelen PA, Querido B, de Ru A, Sluijter M et al. 2010. The nonpolymorphic MHC Qa-1b mediates CD8+ T cell surveillance of antigen-processing defects. J. Exp. Med. 207:207–21
     [Google Scholar]
  175. 175. 
    Lampen MH, Hassan C, Sluijter M, Geluk A, Dijkman K et al. 2013. Alternative peptide repertoire of HLA-E reveals a binding motif that is strikingly similar to HLA-A2. Mol. Immunol. 53:126–31
     [Google Scholar]
  176. 176. 
    Kamiya T, Seow SV, Wong D, Robinson M, Campana D 2019. Blocking expression of inhibitory receptor NKG2A overcomes tumor resistance to NK cells. J. Clin. Investig. 129:2094–106
     [Google Scholar]
  177. 177. 
    Andre P, Denis C, Soulas C, Bourbon-Caillet C, Lopez J et al. 2018. Anti-NKG2A mAb is a checkpoint inhibitor that promotes anti-tumor immunity by unleashing both T and NK cells. Cell 175:1731–43.e13
     [Google Scholar]
  178. 178. 
    van Montfoort N, Borst L, Korrer MJ, Sluijter M, Marijt KA et al. 2018. NKG2A blockade potentiates CD8 T cell immunity induced by cancer vaccines. Cell 175:1744–55.e15
     [Google Scholar]
  179. 179. 
    Garman RD, Doherty PJ, Raulet DH 1986. Diversity, rearrangement, and expression of murine T cell gamma genes. Cell 45:733–42
     [Google Scholar]
  180. 180. 
    Cai Y, Xue F, Fleming C, Yang J, Ding C et al. 2014. Differential developmental requirement and peripheral regulation for dermal Vγ4 and Vγ6T17 cells in health and inflammation. Nat. Commun. 5:3986
     [Google Scholar]
  181. 181. 
    Xiong N, Raulet DH. 2007. Development and selection of γδ T cells. Immunol. Rev. 215:15–31
     [Google Scholar]
  182. 182. 
    Havran WL, Allison JP. 1988. Developmentally ordered appearance of thymocytes expressing different T-cell antigen receptors. Nature 335:443–45
     [Google Scholar]
  183. 183. 
    Gentek R, Ghigo C, Hoeffel G, Jorquera A, Msallam R et al. 2018. Epidermal γδ T cells originate from yolk sac hematopoiesis and clonally self-renew in the adult. J. Exp. Med. 215:2994–3005
     [Google Scholar]
  184. 184. 
    Girardi M. 2001. Regulation of cutaneous malignancy by γζ T cells. Science 294:605–9
     [Google Scholar]
  185. 185. 
    Havran W, Chien Y, Allison J 1991. Recognition of self antigens by skin-derived T cells with invariant gamma delta antigen receptors. Science 252:1430–32
     [Google Scholar]
  186. 186. 
    Sharp LL, Jameson JM, Cauvi G, Havran WL 2005. Dendritic epidermal T cells regulate skin homeostasis through local production of insulin-like growth factor 1. Nat. Immunol. 6:73–79
     [Google Scholar]
  187. 187. 
    MacLeod AS, Hemmers S, Garijo O, Chabod M, Mowen K et al. 2013. Dendritic epidermal T cells regulate skin antimicrobial barrier function. J. Clin. Investig. 123:4364–74
     [Google Scholar]
  188. 188. 
    Bos JD, Teunissen MB, Cairo I, Krieg SR, Kapsenberg ML et al. 1990. T-cell receptor γδ bearing cells in normal human skin. J. Investig. Dermatol. 94:37–42
     [Google Scholar]
  189. 189. 
    Fujita M, Miyachi Y, Nakata K, Imamura S 1993. γδ T-cell receptor-positive cells in human skin. I. Incidence and V-region gene expression in granulomatous skin lesions. J. Am. Acad. Dermatol. 28:46–50
     [Google Scholar]
  190. 190. 
    Toulon A, Breton L, Taylor KR, Tenenhaus M, Bhavsar D et al. 2009. A role for human skin-resident T cells in wound healing. J. Exp. Med. 206:743–50
     [Google Scholar]
  191. 191. 
    Matos TR, O'Malley JT, Lowry EL, Hamm D, Kirsch IR et al. 2017. Clinically resolved psoriatic lesions contain psoriasis-specific IL-17-producing αβ T cell clones. J. Clin. Investig. 127:4031–41
     [Google Scholar]
  192. 192. 
    Holtmeier W, Pfänder M, Hennemann A, Caspary WF, Zollner TM, Kaufmann R 2001. The TCR δ repertoire in normal human skin is restricted and distinct from the TCR δ repertoire in the peripheral blood. J. Investig. Dermatol. 116:275–80
     [Google Scholar]
  193. 193. 
    Vavassori S, Kumar A, Wan GS, Ramanjaneyulu GS, Cavallari M et al. 2013. Butyrophilin 3A1 binds phosphorylated antigens and stimulates human γδ T cells. Nat. Immunol. 14:908–16
     [Google Scholar]
  194. 194. 
    Alexander AAZ, Maniar A, Cummings J-S, Hebbeler AM, Schulze DH et al. 2008. Isopentenyl pyrophosphate-activated CD56+ γδ T lymphocytes display potent antitumor activity toward human squamous cell carcinoma. Clin. Cancer Res. 14:4232–40
     [Google Scholar]
  195. 195. 
    Vantourout P, Laing A, Woodward MJ, Zlatareva I, Apolonia L et al. 2018. Heteromeric interactions regulate butyrophilin (BTN) and BTN-like molecules governing γδ T cell biology. PNAS 115:1039–44
     [Google Scholar]
  196. 196. 
    Harly C, Guillaume Y, Nedellec S, Peigne C-M, Monkkonen H et al. 2012. Key implication of CD277/butyrophilin-3 (BTN3A) in cellular stress sensing by a major human T-cell subset. Blood 120:2269–79
     [Google Scholar]
  197. 197. 
    Di Marco Barros R, Roberts NA, Dart RJ, Vantourout P, Jandke A et al. 2016. Epithelia use butyrophilin-like molecules to shape organ-specific γδ T cell compartments. Cell 167:203–18.e17
     [Google Scholar]
  198. 198. 
    Barbee SD, Woodward MJ, Turchinovich G, Mention J-J, Lewis JM et al. 2011. Skint-1 is a highly specific, unique selecting component for epidermal T cells. PNAS 108:3330–35
     [Google Scholar]
  199. 199. 
    Alejenef A, Pachnio A, Halawi M, Christmas SE, Moss PAH, Khan N 2014. Cytomegalovirus drives Vδ2neg γδ T cell inflation in many healthy virus carriers with increasing age. Clin. Exp. Immunol. 176:418–28
     [Google Scholar]
  200. 200. 
    Davey MS, Willcox CR, Joyce SP, Ladell K, Kasatskaya SA et al. 2017. Clonal selection in the human Vδ1 T cell repertoire indicates γδ TCR-dependent adaptive immune surveillance. Nat. Commun. 8:14760
     [Google Scholar]
  201. 201. 
    Willcox CR, Pitard V, Netzer S, Couzi L, Salim M et al. 2012. Cytomegalovirus and tumor stress surveillance by binding of a human γδ T cell antigen receptor to endothelial protein C receptor. Nat. Immunol. 13:872–79
     [Google Scholar]
  202. 202. 
    Xue M, Campbell D, Sambrook PN, Fukudome K, Jackson CJ 2005. Endothelial protein C receptor and protease-activated receptor-1 mediate induction of a wound-healing phenotype in human keratinocytes by activated protein C. J. Investig. Dermatol. 125:1279–85
     [Google Scholar]
  203. 203. 
    Xu B, Pizarro JC, Holmes MA, McBeth C, Groh V et al. 2011. Crystal structure of a γδ T-cell receptor specific for the human MHC class I homolog MICA. PNAS 108:2414–19
     [Google Scholar]
  204. 204. 
    Jinushi M, Takehara T, Tatsumi T, Kanto T, Groh V et al. 2003. Expression and role of MICA and MICB in human hepatocellular carcinomas and their regulation by retinoic acid. Int. J. Cancer 104:354–61
     [Google Scholar]
  205. 205. 
    Melandri D, Zlatareva I, Chaleil RAG, Dart RJ, Chancellor A et al. 2018. The γδTCR combines innate immunity with adaptive immunity by utilizing spatially distinct regions for agonist selection and antigen responsiveness. Nat. Immunol. 19:1352–65
     [Google Scholar]
  206. 206. 
    Cairo C, Arabito E, Landi F, Casati A, Brunetti E et al. 2005. Analysis of circulating γδ+ T cells in children affected by IgE-associated and non-IgE-associated allergic atopic eczema/dermatitis syndrome. Clin. Exp. Immunol. 141:116–21
     [Google Scholar]
  207. 207. 
    Mann ER, McCarthy NE, Peake STC, Milestone AN, Al-Hassi HO et al. 2012. Skin- and gut-homing molecules on human circulating γδ T cells and their dysregulation in inflammatory bowel disease. Clin. Exp. Immunol. 170:122–30
     [Google Scholar]
  208. 208. 
    Strid J, Sobolev O, Zafirova B, Polic B, Hayday A 2011. The intraepithelial T cell response to NKG2D-ligands links lymphoid stress surveillance to atopy. Science 334:1293–97
     [Google Scholar]
  209. 209. 
    Jiang X, Park CO, Geddes Sweeney J, Yoo MJ, Gaide O, Kupper TS 2017. Dermal γδ T cells do not freely re-circulate out of skin and produce IL-17 to promote neutrophil infiltration during primary contact hypersensitivity. PLOS ONE 12:e0169397
     [Google Scholar]
  210. 210. 
    O'Brien RL, Born WK. 2015. Dermal γδ T cells—What have we learned. ? Cell. Immunol. 296:62–69
     [Google Scholar]
  211. 211. 
    Sumaria N, Roediger B, Ng LG, Qin J, Pinto R et al. 2011. Cutaneous immunosurveillance by self-renewing dermal γδ T cells. J. Exp. Med. 208:505–18
     [Google Scholar]
  212. 212. 
    Gray EE, Suzuki K, Cyster JG 2011. Cutting edge: identification of a motile IL-17-producing γδ T cell population in the dermis. J. Immunol. 186:6091–95
     [Google Scholar]
  213. 213. 
    van der Fits L, Mourits S, Voerman JS, Kant M, Boon L et al. 2009. Imiquimod-induced psoriasis-like skin inflammation in mice is mediated via the IL-23/IL-17 axis. J. Immunol. 182:5836–45
     [Google Scholar]
  214. 214. 
    Han Y, Mora J, Huard A, da Silva P, Wiechmann S et al. 2019. IL-38 ameliorates skin inflammation and limits IL-17 production from γδ T cells. Cell Rep 27:835–46.e5
     [Google Scholar]
  215. 215. 
    Cai Y, Shen X, Ding C, Qi C, Li K et al. 2011. Pivotal role of dermal IL-17-producing γδ T cells in skin inflammation. Immunity 35:596–610
     [Google Scholar]
  216. 216. 
    Laggner U, Di Meglio P, Perera GK, Hundhausen C, Lacy KE et al. 2011. Identification of a novel proinflammatory human skin-homing Vγ9Vδ2 T cell subset with a potential role in psoriasis. J. Immunol. 187:2783–93
     [Google Scholar]
  217. 217. 
    Gober H-J, Kistowska M, Angman L, Jenö P, Mori L, De Libero G 2003. Human T cell receptor γδ cells recognize endogenous mevalonate metabolites in tumor cells. J. Exp. Med. 197:163–68
     [Google Scholar]
  218. 218. 
    Petrini I, Pacini S, Galimberti S, Taddei MR, Romanini A, Petrini M 2011. Impaired function of gamma-delta lymphocytes in melanoma patients. Eur. J. Clin. Investig. 41:1186–94
     [Google Scholar]
  219. 219. 
    Campillo JA, Martinez-Escribano JA, Minguela A, Lopez-Alvarez R, Marin LA et al. 2007. Increased number of cytotoxic CD3+ CD28− γδ T cells in peripheral blood of patients with cutaneous malignant melanoma. Dermatology 214:283–88
     [Google Scholar]
  220. 220. 
    Lafont V, Sanchez F, Laprevotte E, Michaud H-A, Gros L et al. 2014. Plasticity of γδ T cells: impact on the anti-tumor response. Front. Immunol. 5:622
     [Google Scholar]
  221. 221. 
    Kong HH, Oh J, Deming C, Conlan S, Grice EA et al. 2012. Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res 22:850–59
     [Google Scholar]
  222. 222. 
    Leung DY, Travers JB, Giorno R, Norris DA, Skinner R et al. 1995. Evidence for a streptococcal superantigen-driven process in acute guttate psoriasis. J. Clin. Investig. 96:2106–12
     [Google Scholar]
  223. 223. 
    Strickland I, Hauk PJ, Trumble AE, Picker LJ, Leung DY 1999. Evidence for superantigen involvement in skin homing of T cells in atopic dermatitis. J. Investig. Dermatol. 112:249–53
     [Google Scholar]
  224. 224. 
    Macias ES, Pereira FA, Rietkerk W, Safai B 2011. Superantigens in dermatology. J. Am. Acad. Dermatol. 64:455–72
     [Google Scholar]
  225. 225. 
    Commons RJ, Smeesters PR, Proft T, Fraser JD, Robins-Browne R, Curtis N 2014. Streptococcal superantigens: categorization and clinical associations. Trends. Mol. Med. 20:48–62
     [Google Scholar]
  226. 226. 
    Kawakami K, Yamamoto N, Kinjo Y, Miyagi K, Nakasone C et al. 2003. Critical role of Vα14+ natural killer T cells in the innate phase of host protection against Streptococcus pneumoniae infection. Eur. J. Immunol. 33:3322–30
     [Google Scholar]
  227. 227. 
    Sada-Ovalle I, Chiba A, Gonzales A, Brenner MB, Behar SM 2008. Innate invariant NKT cells recognize Mycobacterium tuberculosis-infected macrophages, produce interferon-γ, and kill intracellular bacteria. PLOS Pathog 4:e1000239
     [Google Scholar]
  228. 228. 
    Kee SJ, Kwon YS, Park YW, Cho YN, Lee SJ et al. 2012. Dysfunction of natural killer T cells in patients with active Mycobacterium tuberculosis infection. Infect. Immun. 80:2100–8
     [Google Scholar]
  229. 229. 
    Snyder-Cappione JE, Nixon DF, Loo CP, Chapman JM, Meiklejohn DA et al. 2007. Individuals with pulmonary tuberculosis have lower levels of circulating CD1d-restricted NKT cells. J. Infect. Dis. 195:1361–64
     [Google Scholar]
  230. 230. 
    Wu C, Li Z, Fu X, Yu S, Lao S, Yang B 2015. Antigen-specific human NKT cells from tuberculosis patients produce IL-21 to help B cells for the production of immunoglobulins. Oncotarget 6:28633–45
     [Google Scholar]
  231. 231. 
    Zhao Y, Lin L, Xiao Z, Li M, Wu X et al. 2018. Protective role of γδ T cells in different pathogen infections and its potential clinical application. J. Immunol. Res. 2018:5081634
     [Google Scholar]
  232. 232. 
    Naik S, Bouladoux N, Linehan JL, Han SJ, Harrison OJ et al. 2015. Commensal-dendritic-cell interaction specifies a unique protective skin immune signature. Nature 520:104–8
     [Google Scholar]
  233. 233. 
    Ridaura VK, Bouladoux N, Claesen J, Chen YE, Byrd AL et al. 2018. Contextual control of skin immunity and inflammation by Corynebacterium. J. Exp. Med 215:785–99
     [Google Scholar]
  234. 234. 
    Jameson J, Ugarte K, Chen N, Yachi P, Fuchs E et al. 2002. A role for skin γδ T cells in wound repair. Science 296:747–49
     [Google Scholar]
  235. 235. 
    Molne L, Corthay A, Holmdahl R, Tarkowski A 2003. Role of γ/δ T cell receptor-expressing lymphocytes in cutaneous infection caused by Staphylococcus aureus. Clin. Exp. Immunol 132:209–15
     [Google Scholar]
  236. 236. 
    Cho JS, Pietras EM, Garcia NC, Ramos RI, Farzam DM et al. 2010. IL-17 is essential for host defense against cutaneous Staphylococcus aureus infection in mice. J. Clin. Investig. 120:1762–73
     [Google Scholar]
  237. 237. 
    Canesso MCC, Vieira AT, Castro TBR, Schirmer BGA, Cisalpino D et al. 2014. Skin wound healing is accelerated and scarless in the absence of commensal microbiota. J. Immunol. 193:5171–80
     [Google Scholar]
  238. 238. 
    Grice EA, Kong HH, Conlan S, Deming CB, Davis J et al. 2009. Topographical and temporal diversity of the human skin microbiome. Science 324:1190–92
     [Google Scholar]
  239. 239. 
    Belheouane M, Gupta Y, Kunzel S, Ibrahim S, Baines JF 2017. Improved detection of gene-microbe interactions in the mouse skin microbiota using high-resolution QTL mapping of 16S rRNA transcripts. Microbiome 5:59
     [Google Scholar]
  240. 240. 
    Hayday AC. 2009. γδ T cells and the lymphoid stress-surveillance response. Immunity 31:184–96
     [Google Scholar]
  241. 241. 
    Cua DJ, Tato CM. 2010. Innate IL-17-producing cells: the sentinels of the immune system. Nat. Rev. Immunol. 10:479–89
     [Google Scholar]
  242. 242. 
    Eberl M, Hintz M, Reichenberg A, Kollas AK, Wiesner J, Jomaa H 2003. Microbial isoprenoid biosynthesis and human γδ T cell activation. FEBS Lett 544:4–10
     [Google Scholar]
  243. 243. 
    Xu S, Han Y, Xu X, Bao Y, Zhang M, Cao X 2010. IL-17A-producing γδT cells promote CTL responses against Listeria monocytogenes infection by enhancing dendritic cell cross-presentation. J. Immunol. 185:5879–87
     [Google Scholar]
  244. 244. 
    Romagnoli PA, Sheridan BS, Pham QM, Lefrancois L, Khanna KM 2016. IL-17A-producing resident memory γδ T cells orchestrate the innate immune response to secondary oral Listeria monocytogenes infection. PNAS 113:8502–7
     [Google Scholar]
  245. 245. 
    Wong EB, Ndung'u T, Kasprowicz VO 2017. The role of mucosal-associated invariant T cells in infectious diseases. Immunology 150:45–54
     [Google Scholar]
  246. 246. 
    Martin E, Treiner E, Duban L, Guerri L, Laude H et al. 2009. Stepwise development of MAIT cells in mouse and human. PLOS Biol 7:e54
     [Google Scholar]
  247. 247. 
    Gold MC, McLaren JE, Reistetter JA, Smyk-Pearson S, Ladell K et al. 2014. MR1-restricted MAIT cells display ligand discrimination and pathogen selectivity through distinct T cell receptor usage. J. Exp. Med. 211:1601–10
     [Google Scholar]
  248. 248. 
    Paus R, Eichmuller S, Hofmann U, Czarnetzki BM, Robinson P 1994. Expression of classical and nonclassical MHC class I antigens in murine hair follicles. Br. J. Dermatol. 131:177–83
     [Google Scholar]
  249. 249. 
    Ruckert R, Hofmann U, van der Veen C, Bulfone-Paus S, Paus R 1998. MHC class I expression in murine skin: developmentally controlled and strikingly restricted intraepithelial expression during hair follicle morphogenesis and cycling, and response to cytokine treatment in vivo. J. Investig. Dermatol. 111:25–30
     [Google Scholar]
  250. 250. 
    Bian Y, Shang S, Siddiqui S, Zhao J, Joosten SA et al. 2017. MHC Ib molecule Qa-1 presents Mycobacterium tuberculosis peptide antigens to CD8+ T cells and contributes to protection against infection. PLOS Pathog 13:e1006384
     [Google Scholar]
  251. 251. 
    Shang S, Siddiqui S, Bian Y, Zhao J, Wang CR 2016. Nonclassical MHC Ib-restricted CD8+ T cells recognize Mycobacterium tuberculosis-derived protein antigens and contribute to protection against infection. PLOS Pathog 12:e1005688
     [Google Scholar]
  252. 252. 
    Rodgers JR, Cook RG. 2005. MHC class Ib molecules bridge innate and acquired immunity. Nat. Rev. Immunol. 5:459–71
     [Google Scholar]
  253. 253. 
    Aractingi S, Briand N, Le Danff C, Viguier M, Bachelez H et al. 2001. HLA-G and NK receptor are expressed in psoriatic skin: a possible pathway for regulating infiltrating T cells?. Am. J. Pathol. 159:71–77
     [Google Scholar]
  254. 254. 
    Morandi F, Rizzo R, Fainardi E, Rouas-Freiss N, Pistoia V 2016. Recent advances in our understanding of HLA-G biology: lessons from a wide spectrum of human diseases. J. Immunol. Res. 2016:4326495
     [Google Scholar]
  255. 255. 
    Murdaca G, Contini P, Negrini S, Ciprandi G, Puppo F 2016. Immunoregulatory role of HLA-G in allergic diseases. J. Immunol. Res. 2016:6865758
     [Google Scholar]
  256. 256. 
    Urosevic M. 2002. HLA-G protein up-regulation in primary cutaneous lymphomas is associated with interleukin-10 expression in large cell T-cell lymphomas and indolent B-cell lymphomas. Blood 99:609–17
     [Google Scholar]
  257. 257. 
    Cardili RN, Alves TG, Freitas JC, Soares CP, Mendes-Junior CT et al. 2010. Expression of human leucocyte antigen-G primarily targets affected skin of patients with psoriasis. Br. J. Dermatol. 163:769–75
     [Google Scholar]
  258. 258. 
    Linehan JL, Harrison OJ, Han SJ, Byrd AL, Vujkovic-Cvijin I et al. 2018. Non-classical immunity controls microbiota impact on skin immunity and tissue repair. Cell 172:784–96.e18
     [Google Scholar]
  259. 259. 
    Andrews DM, Sullivan LC, Baschuk N, Chan CJ, Berry R et al. 2012. Recognition of the nonclassical MHC class I molecule H2-M3 by the receptor Ly49A regulates the licensing and activation of NK cells. Nat. Immunol. 13:1171–77
     [Google Scholar]
  260. 260. 
    Legoux F, Salou M, Lantz O 2017. Unconventional or preset alpha beta T cells: evolutionarily conserved tissue-resident T cells recognizing nonpeptidic ligands. Annu. Rev. Cell Dev. Biol. 33:511–35
     [Google Scholar]
  261. 261. 
    Gallo RL, Nakatsuji T. 2011. Microbial symbiosis with the innate immune defense system of the skin. J. Investig. Dermatol. 131:1974–80
     [Google Scholar]
  262. 262. 
    Grice EA, Snitkin ES, Yockey LJ, Bermudez DM, NISC Comp. Seq. Program, et al. 2010. Longitudinal shift in diabetic wound microbiota correlates with prolonged skin defense response. PNAS 107:14799–804
     [Google Scholar]
  263. 263. 
    Martin JM, Zenilman JM, Lazarus GS 2010. Molecular microbiology: new dimensions for cutaneous biology and wound healing. J. Investig. Dermatol. 130:38–48
     [Google Scholar]
  264. 264. 
    Schierle CF, De la Garza M, Mustoe TA, Galiano RD 2009. Staphylococcal biofilms impair wound healing by delaying reepithelialization in a murine cutaneous wound model. Wound Repair Regen 17:354–59
     [Google Scholar]
  265. 265. 
    Iwase T, Uehara Y, Shinji H, Tajima A, Seo H et al. 2010. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 465:346–49
     [Google Scholar]
  266. 266. 
    Nakatsuji T, Chen TH, Narala S, Chun KA, Two AM et al. 2017. Antimicrobials from human skin commensal bacteria protect against Staphylococcus aureus and are deficient in atopic dermatitis. Sci. Transl. Med. 9:eaah4680
     [Google Scholar]
  267. 267. 
    Zipperer A, Konnerth MC, Laux C, Berscheid A, Janek D et al. 2016. Human commensals producing a novel antibiotic impair pathogen colonization. Nature 535:511–16
     [Google Scholar]
  268. 268. 
    Wanke I, Steffen H, Christ C, Krismer B, Gotz F et al. 2011. Skin commensals amplify the innate immune response to pathogens by activation of distinct signaling pathways. J. Investig. Dermatol. 131:382–90
     [Google Scholar]
  269. 269. 
    Geoghegan JA, Irvine AD, Foster TJ 2018. Staphylococcus aureus and atopic dermatitis: a complex and evolving relationship. Trends Microbiol 26:484–97
     [Google Scholar]
  270. 270. 
    Masenga J, Garbe C, Wagner J, Orfanos CE 1990. Staphylococcus aureus in atopic dermatitis and in nonatopic dermatitis. Int. J. Dermatol. 29:579–82
     [Google Scholar]
  271. 271. 
    Simpson EL, Villarreal M, Jepson B, Rafaels N, David G et al. 2018. Patients with atopic dermatitis colonized with Staphylococcus aureus have a distinct phenotype and endotype. J. Invest. Dermatol. 138:2224–33
     [Google Scholar]
  272. 272. 
    Weisenseel P, Laumbacher B, Besgen P, Ludolph-Hauser D, Herzinger T et al. 2002. Streptococcal infection distinguishes different types of psoriasis. J. Med. Genet. 39:767–68
     [Google Scholar]
  273. 273. 
    Telfer NR, Chalmers RJ, Whale K, Colman G 1992. The role of streptococcal infection in the initiation of guttate psoriasis. Arch. Dermatol. 128:39–42
     [Google Scholar]
  274. 274. 
    Zeeuwen PL, de Jongh GJ, Rodijk-Olthuis D, Kamsteeg M, Verhoosel RM et al. 2008. Genetically programmed differences in epidermal host defense between psoriasis and atopic dermatitis patients. PLOS ONE 3:e2301
     [Google Scholar]
  275. 275. 
    Kwon S, Choi JY, Shin JW, Huh CH, Park KC et al. 2019. Changes in lesional and non-lesional skin microbiome during treatment of atopic dermatitis. Acta Derm. Venereol. 99:284–90
     [Google Scholar]
  276. 276. 
    Shi B, Leung DYM, Taylor PA, Li H 2018. Methicillin-resistant Staphylococcus aureus colonization is associated with decreased skin commensal bacteria in atopic dermatitis. J. Invest. Dermatol. 138:1668–71
     [Google Scholar]
  277. 277. 
    Byrd AL, Deming C, Cassidy SKB, Harrison OJ, Ng WI et al. 2017. Staphylococcus aureus and Staphylococcus epidermidis strain diversity underlying pediatric atopic dermatitis. Sci. Transl. Med. 9:eaal4651
     [Google Scholar]
  278. 278. 
    Schwarz A, Bruhs A, Schwarz T 2017. The short-chain fatty acid sodium butyrate functions as a regulator of the skin immune system. J. Investig. Dermatol. 137:855–64
     [Google Scholar]
  279. 279. 
    Beck DB, Aksentijevich I. 2019. Biochemistry of autoinflammatory diseases: catalyzing monogenic disease. Front. Immunol. 10:101
     [Google Scholar]
  280. 280. 
    Martinez-Quiles N, Goldbach-Mansky R. 2018. Updates on autoinflammatory diseases. Curr. Opin. Immunol. 55:97–105
     [Google Scholar]
  281. 281. 
    Milner JD. 2020. Primary atopic disorders. Annu. Rev. Immunol 38:785–808
     [Google Scholar]
  282. 282. 
    Lazear HM, Nice TJ, Diamond MS 2015. Interferon-λ: immune functions at barrier surfaces and beyond. Immunity 43:15–28
     [Google Scholar]
  283. 283. 
    Wolk K, Witte K, Witte E, Raftery M, Kokolakis G et al. 2013. IL-29 is produced by TH17 cells and mediates the cutaneous antiviral competence in psoriasis. Sci. Transl. Med. 5:204ra129
     [Google Scholar]
  284. 284. 
    Li Y, Cheng H, Zuo XB, Sheng YJ, Zhou FS et al. 2013. Association analyses identifying two common susceptibility loci shared by psoriasis and systemic lupus erythematosus in the Chinese Han population. J. Med. Genet. 50:812–18
     [Google Scholar]
  285. 285. 
    Strange A, Capon F, Spencer CC, Knight J, Weale ME et al. 2010. A genome-wide association study identifies new psoriasis susceptibility loci and an interaction between HLA-C and ERAP1. Nat. Genet. 42:985–90
     [Google Scholar]
  286. 286. 
    Dand N, Mucha S, Tsoi LC, Mahil SK, Stuart PE et al. 2017. Exome-wide association study reveals novel psoriasis susceptibility locus at TNFSF15 and rare protective alleles in genes contributing to type I IFN signalling. Hum. Mol. Genet. 26:4301–13
     [Google Scholar]
  287. 287. 
    Reich K, Huffmeier U, Konig IR, Lascorz J, Lohmann J et al. 2007. TNF polymorphisms in psoriasis: association of psoriatic arthritis with the promoter polymorphism TNF*-857 independent of the PSORS1 risk allele. Arthritis Rheum 56:2056–64
     [Google Scholar]
  288. 288. 
    Jarosz-Griffiths HH, Holbrook J, Lara-Reyna S, McDermott MF 2019. TNF receptor signalling in autoinflammatory diseases. Int. Immunol. 31:639–48
     [Google Scholar]
  289. 289. 
    De Simone C, Farina M, Maiorino A, Fanali C, Perino F et al. 2015. TNF-alpha gene polymorphisms can help to predict response to etanercept in psoriatic patients. J. Eur. Acad. Dermatol. Venereol. 29:1786–90
     [Google Scholar]
  290. 290. 
    Gurung P, Kanneganti TD. 2016. Autoinflammatory skin disorders: the inflammasomme in focus. Trends. Mol. Med. 22:545–64
     [Google Scholar]
  291. 291. 
    Watanabe H, Gaide O, Petrilli V, Martinon F, Contassot E et al. 2007. Activation of the IL-1β-processing inflammasome is involved in contact hypersensitivity. J. Invest. Dermatol. 127:1956–63
     [Google Scholar]
  292. 292. 
    Ekman AK, Verma D, Fredrikson M, Bivik C, Enerback C 2014. Genetic variations of NLRP1: susceptibility in psoriasis. Br. J. Dermatol. 171:1517–20
     [Google Scholar]
  293. 293. 
    Jordan CT, Cao L, Roberson ED, Pierson KC, Yang CF et al. 2012. PSORS2 is due to mutations in CARD14. Am. J. Hum. Genet. 90:784–95
     [Google Scholar]
  294. 294. 
    Marrakchi S, Guigue P, Renshaw BR, Puel A, Pei XY et al. 2011. Interleukin-36-receptor antagonist deficiency and generalized pustular psoriasis. N. Engl. J. Med. 365:620–28
     [Google Scholar]
  295. 295. 
    Onoufriadis A, Simpson MA, Pink AE, Di Meglio P, Smith CH et al. 2011. Mutations in IL36RN/IL1F5 are associated with the severe episodic inflammatory skin disease known as generalized pustular psoriasis. Am. J. Hum. Genet. 89:432–37
     [Google Scholar]
  296. 296. 
    Capon F. 2013. IL36RN mutations in generalized pustular psoriasis: just the tip of the iceberg?. J. Investig. Dermatol. 133:2503–4
     [Google Scholar]
  297. 297. 
    Hussain S, Berki DM, Choon SE, Burden AD, Allen MH et al. 2015. IL36RN mutations define a severe autoinflammatory phenotype of generalized pustular psoriasis. J. Allergy Clin. Immunol. 135:1067–70.e9
     [Google Scholar]
  298. 298. 
    Setta-Kaffetzi N, Navarini AA, Patel VM, Pullabhatla V, Pink AE et al. 2013. Rare pathogenic variants in IL36RN underlie a spectrum of psoriasis-associated pustular phenotypes. J. Investig. Dermatol. 133:1366–69
     [Google Scholar]
  299. 299. 
    Rossi-Semerano L, Piram M, Chiaverini C, De Ricaud D, Smahi A, Kone-Paut I 2013. First clinical description of an infant with interleukin-36-receptor antagonist deficiency successfully treated with anakinra. Pediatrics 132:e1043–47
     [Google Scholar]
  300. 300. 
    D'Erme AM, Wilsmann-Theis D, Wagenpfeil J, Holzel M, Ferring-Schmitt S et al. 2015. IL-36γ (IL-1F9) is a biomarker for psoriasis skin lesions. J. Investig. Dermatol. 135:1025–32
     [Google Scholar]
  301. 301. 
    Nestle FO, Conrad C, Tun-Kyi A, Homey B, Gombert M et al. 2005. Plasmacytoid predendritic cells initiate psoriasis through interferon-α production. J. Exp. Med. 202:135–43
     [Google Scholar]
  302. 302. 
    van der Fits L, van der Wel LI, Laman JD, Prens EP, Verschuren MC 2004. In psoriasis lesional skin the type I interferon signaling pathway is activated, whereas interferon-α sensitivity is unaltered. J. Investig. Dermatol. 122:51–60
     [Google Scholar]
  303. 303. 
    Bhalerao J, Bowcock AM. 1998. The genetics of psoriasis: a complex disorder of the skin and immune system. Hum. Mol. Genet. 7:1537–45
     [Google Scholar]
  304. 304. 
    Duerr CU, McCarthy CD, Mindt BC, Rubio M, Meli AP et al. 2016. Type I interferon restricts type 2 immunopathology through the regulation of group 2 innate lymphoid cells. Nat. Immunol. 17:65–75
     [Google Scholar]
  305. 305. 
    Kloverpris HN, Kazer SW, Mjosberg J, Mabuka JM, Wellmann A et al. 2016. Innate lymphoid cells are depleted irreversibly during acute HIV-1 infection in the absence of viral suppression. Immunity 44:391–405
     [Google Scholar]
  306. 306. 
    Sandling JK, Garnier S, Sigurdsson S, Wang C, Nordmark G et al. 2011. A candidate gene study of the type I interferon pathway implicates IKBKE and IL8 as risk loci for SLE. Eur. J. Hum. Genet. 19:479–84
     [Google Scholar]
  307. 307. 
    Gui J, Gober M, Yang X, Katlinski KV, Marshall CM et al. 2016. Therapeutic elimination of the type 1 interferon receptor for treating psoriatic skin inflammation. J. Investig. Dermatol. 136:1990–2002
     [Google Scholar]
  308. 308. 
    Crow MK, Olferiev M, Kirou KA 2015. Targeting of type I interferon in systemic autoimmune diseases. Transl. Res. 165:296–305
     [Google Scholar]
  309. 309. 
    Furie R, Werth VP, Merola JF, Stevenson L, Reynolds TL et al. 2019. Monoclonal antibody targeting BDCA2 ameliorates skin lesions in systemic lupus erythematosus. J. Clin. Investig. 129:1359–71
     [Google Scholar]
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Innate Lymphocyte Mechanisms in Skin Diseases
Annual Review of Immunology 38, 171 (2020); https://doi.org/10.1146/annurev-immunol-082919-093554
/content/journals/10.1146/annurev-immunol-082919-093554
/content/journals/10.1146/annurev-immunol-082919-093554
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