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Cited by 181T-cell and B-cell ImmunologyImmune responses and vaccinationsImmune cells in cancer

Tissue-resident immune cells in humans

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Gray, Joshua I., Farber, Donna L.·2022·Annual Review of Immunology
DOI 10.1146/annurev-immunol-093019-112809PMC PMC11194112
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Abstract

Tissue-resident immune cells span both myeloid and lymphoid cell lineages, have been found in multiple human tissues, and play integral roles at all stages of the immune response, from maintaining homeostasis to responding to infectious challenges to resolution of inflammation to tissue repair. In humans, studying immune cells and responses in tissues is challenging, although recent advances in sampling and high-dimensional profiling have provided new insights into the ontogeny, maintenance, and functional role of tissue-resident immune cells. Each tissue contains a specific complement of resident immune cells. Moreover, resident immune cells for each lineage share core properties, along with tissue-specific adaptations. Here we propose a five-point checklist for defining resident immune cell types in humans and describe the currently known features of resident immune cells, their mechanisms of development, and their putative functional roles within various human organs. We also consider these aspects of resident immune cells in the context of future studies and therapeutics.

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  1. [1]Worbs T, Hammerschmidt SI, Förster R. 2017. Dendritic cell migration in health and disease. Nat. Rev. Immunol 17(1):30–48 [DOI] [PubMed] [Google Scholar]
  2. [3]Turner DL,Farber DL. 2014. Mucosal resident memory CD4 T cells in protection and immunopathology. Front. Immunol 5:331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. [4]Weisel NM, Weisel FJ, Farber DL, Borghesi LA, Shen Y, et al. 2020. Comprehensive analyses of B-cell compartments across the human body reveal novel subsets and a gut-resident memory phenotype. Blood 136:2774–85 [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. [5]Kumar BV, Ma W, Miron M, Granot T, Guyer RS, et al. 2017. Human tissue-resident memory T cells are defined by core transcriptional and functional signatures in lymphoid and mucosal sites. Cell Rep. 20:2921–34 [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. [6]Szabo PA, Levitin HM, Miron M, Snyder ME, Senda T, et al. 2019. Single-cell transcriptomics of human T cells reveals tissue and activation signatures in health and disease. Nat. Commun 10:4706. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. [7]Szabo PA, Miron M, Farber DL. 2019. Location, location, location: tissue resident memory T cells in mice and humans. Sci. Immunol 4:eaas9673 [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. [9]Weisberg SP,Carpenter DJ,Chait M,Dogra P,Gartrell-Corrado RD, et al. 2019. Tissue-resident memory T cells mediate immune homeostasis in the human pancreas through the PD-1/PD-L1 pathway. Cell Rep. 29:3916–32.e5 [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. [10]Weisberg SP,Ural BB,Farber DL. 2021. Tissue-specific immunity for a changing world. Cell 184:1517–29 [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. [11]Masopust D, Soerens AG. 2019. Tissue-resident T cells and other resident leukocytes. Annu. Rev. Immunol 37:521–46 [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. [13]Teichmann LL, Kashgarian M, Weaver CT, Roers A, Muller W, Shlomchik MJ. 2012. B cell-derived IL-10 does not regulate spontaneous systemic autoimmunity in MRL. Faslpr mice. J. Immunol 188:678–85 [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. [14]Teijaro JR, Turner D, Pham Q, Wherry EJ, Lefrancois L, Farber DL. 2011. Cutting edge: tissueretentive lung memory CD4 T cells mediate optimal protection to respiratory virus infection. J. Immunol 187:5510–14 [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. [16]Mackay LK, Kallies A. 2017. Transcriptional regulation of tissue-resident lymphocytes. Trends Immunol. 38:94–103 [DOI] [PubMed] [Google Scholar]
  13. [17]Mackay LK, Minnich M, Kragten NA, Liao Y, Nota B, et al. 2016. Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes. Science 352:459–63 [DOI] [PubMed] [Google Scholar]
  14. [18]Milner JJ, Toma C, Yu B, Zhang K, Omilusik K, et al. 2017. Runx3 programs CD8+ T cell residency in non-lymphoid tissues and tumours. Nature 552:253–57 [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. [19]Zundler S, Becker E, Spocinska M, Slawik M, Parga-Vidal L, et al. 2019. Hobit- and Blimp-1-driven CD4+ tissue-resident memory T cells control chronic intestinal inflammation. Nat. Immunol 20:288–300 [DOI] [PubMed] [Google Scholar]
  16. [20]Ginhoux F, Guilliams M. 2016. Tissue-resident macrophage ontogeny and homeostasis. Immunity 44:439–49 [DOI] [PubMed] [Google Scholar]
  17. [21]Carpenter DJ, Granot T, Matsuoka N, Senda T, Kumar BV, et al. 2018. Human immunology studies using organ donors: impact of clinical variations on immune parameters in tissues and circulation. Am. J. Transplant 18:74–88 [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. [22]Poon MML,Farber DL. 2020. The whole body as the system in systems immunology. iScience 23:101509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. [23]Farber DL. 2021. Tissues, not blood, are where immune cells act. Nature 593:506–9 [DOI] [PubMed] [Google Scholar]
  20. [24]Vieira Braga FA, Kar G, Berg M, Carpaij OA, Polanski K, et al. 2019. A cellular census of human lungs identifies novel cell states in health and in asthma. Nat. Med 25:1153–63 [DOI] [PubMed] [Google Scholar]
  21. [25]Vantourout P, Hayday A. 2013. Six-of-the-best: unique contributions of γδ T cells to immunology. Nat. Rev. Immunol 13:88–100 [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. [26]Provine NM, Klenerman P. 2020. MAIT cells in health and disease. Annu. Rev. Immunol 38:203–28 [DOI] [PubMed] [Google Scholar]
  23. [27]Blériot C,Chakarov S,Ginhoux F. 2020. Determinants of resident tissue macrophage identity and function. Immunity 52(6):957–70 [DOI] [PubMed] [Google Scholar]
  24. [28]Cox N, Pokrovskii M, Vicario R, Geissmann F. 2021. Origins, biology, and diseases of tissue macrophages. Annu. Rev. Immunol 39:313–44 [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. [30]Evren E, Ringqvist E, Tripathi KP, Sleiers N, Rives IC, et al. 2021. Distinct developmental pathways from blood monocytes generate human lung macrophage diversity. Immunity 54:259–75.e7 [DOI] [PubMed] [Google Scholar]
  26. [31]Ruiz-Alcaraz AJ, Carmona-Martinez V, Tristan-Manzano M, Machado-Linde F, Sanchez-Ferrer ML,et al. 2018. Characterization of human peritoneal monocyte/macrophage subsets in homeostasis: phenotype, GATA6, phagocytic/oxidative activities and cytokines expression. Sci. Rep 8:12794. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. [32]Bujko A, Atlasy N, Landsverk OJB, Richter L, Yaqub S, et al. 2018. Transcriptional and functional profiling defines human small intestinal macrophage subsets. J. Exp. Med 215:441–58 [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. [33]Byrne AJ, Powell JE, O’Sullivan BJ, Ogger PP, Hoffland A, et al. 2020. Dynamics of human monocytes and airway macrophages during healthy aging and after transplant. J. Exp. Med 217:e20191236. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. [34]MacParland SA, Liu JC, Ma XZ, Innes BT, Bartczak AM, et al. 2018. Single cell RNA sequencing of human liver reveals distinct intrahepatic macrophage populations. Nat. Commun 9:4383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. [35]Szabo PA, Dogra P, Gray JI, Wells SB, Connors TJ, et al. 2021. Longitudinal profiling of respiratory and systemic immune responses reveals myeloid cell-driven lung inflammation in severe COVID-19. Immunity 54:797–814.e6 [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. [36]Yu YR, Hotten DF, Malakhau Y, Volker E, Ghio AJ, et al. 2016. Flow cytometric analysis of myeloid cells in human blood, bronchoalveolar lavage, and lung tissues. Am. J. Respir. Cell Mol. Biol 54:13–24 [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. [37]Wu X, Hollingshead N, Roberto J, Knupp A, Kenerson H, et al. 2020. Human liver macrophage subsets defined by CD32. Front. Immunol 11:2108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. [38]MacParland SA, Liu JC, Ma XZ, Innes BT, Bartczak AM, et al. 2018. Single cell RNA sequencing of human liver reveals distinct intrahepatic macrophage populations. Nat. Commun 9:4383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. [39]Davies LC, Taylor PR. 2015. Tissue-resident macrophages: then and now. Immunology 144:541–48 [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. [40]Szabo PA, Dogra P, Gray JI, Wells SB, Connors TJ, et al. 2021. Longitudinal profiling of respiratory and systemic immune responses reveals myeloid cell-driven lung inflammation in severe COVID-19. Immunity 54:797–814.e6 [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. [41]Gosselin D, Skola D, Coufal NG, Holtman IR, Schlachetzki JCM, et al. 2017. An environmentdependent transcriptional network specifies human microglia identity. Science 356:1248–59 [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. [43]Schmidt SV, Krebs W, Ulas T, Xue J, Babler K, et al. 2016. The transcriptional regulator network of human inflammatory macrophages is defined by open chromatin. Cell Res. 26:151–70 [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. [44]Trizzino M, Zucco A, Deliard S, Wang F, Barbieri E, et al. 2021. EGR1 is a gatekeeper of inflammatory enhancers in human macrophages. Sci. Adv 7:eaaz8836 [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. [45]Bian Z,Gong Y,Huang T,Lee CZW,Bian L,et al. 2020. Deciphering human macrophage development at single-cell resolution. Nature 582:571–76 [DOI] [PubMed] [Google Scholar]
  40. [46]Rosas M, Davies LC, Giles PJ, Liao CT, Kharfan B, et al. 2014. The transcription factor Gata6 links tissue macrophage phenotype and proliferative renewal. Science 344:645–48 [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. [47]Schneider C, Nobs SP, Kurrer M, Rehrauer H, Thiele C, Kopf M. 2014. Induction of the nuclear receptor PPAR-γ 3 by the cytokine GM-CSF is critical for the differentiation of fetal monocytes into alveolar macrophages. Nat. Immunol 15:1026–37 [DOI] [PubMed] [Google Scholar]
  42. [48]van de Laar L, Saelens W, De Prijck S, Martens L, Scott CL, et al. 2016. Yolk sac macrophages, fetal liver, and adult monocytes can colonize an empty niche and develop into functional tissue-resident macrophages. Immunity 44:755–68 [DOI] [PubMed] [Google Scholar]
  43. [49]Sallusto F, Lenig D, Förster R, Lipp M, Lanzavecchia A. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 402:34–38 [DOI] [PubMed] [Google Scholar]
  44. [50]Gordon CL, Miron M, Thome JJ, Matsuoka N, Weiner J, et al. 2017. Tissue reservoirs of antiviral T cell immunity in persistent human CMV infection. J. Exp. Med 214:651–67 [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. [52]Thome JJ, Yudanin N, Ohmura Y, Kubota M, Grinshpun B, et al. 2014. Spatial map of human T cell compartmentalization and maintenance over decades of life. Cell 159:814–28 [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. [53]Matloubian M, Lo CG, Cinamon G, Lesneski MJ, Xu Y, et al. 2004. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 427:355–60 [DOI] [PubMed] [Google Scholar]
  47. [54]Hombrink P, Helbig C, Backer RA, Piet B, Oja AE, et al. 2016. Programs for the persistence, vigilance and control of human CD8+ lung-resident memory T cells. Nat. Immunol 17:1467–78 [DOI] [PubMed] [Google Scholar]
  48. [55]Weinreich MA, Takada K, Skon C, Reiner SL, Jameson SC, Hogquist KA. 2009. KLF2 transcriptionfactor deficiency in T cells results in unrestrained cytokine production and upregulation of bystander chemokine receptors. Immunity 31:122–30 [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. [56]Klicznik MM, Morawski PA, Höllbacher B, Varkhande SR, Motley SJ, et al. 2019. Human CD4+CD103+ cutaneous resident memory T cells are found in the circulation of healthy individuals. Sci. Immunol 4(37):eaav8995 [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. [57]Oja AE,Piet B,Helbig C,Stark R,Van Der Zwan D,et al. 2018. Trigger-happy resident memory CD4+ T cells inhabit the human lungs. Mucosal Immunol. 11:654–67 [DOI] [PubMed] [Google Scholar]
  51. [58]FitzPatrick MEB, Provine NM, Garner LC, Powell K, Amini A, et al. 2021. Human intestinal tissue-resident memory T cells comprise transcriptionally and functionally distinct subsets. Cell Rep. 34:108661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. [59]Hunter S, Willcox CR, Davey MS, Kasatskaya SA, Jeffery HC, et al. 2018. Human liver infiltrating γδ T cells are composed of clonally expanded circulating and tissue-resident populations. J. Hepatol 69:654–65 [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. [60]McCully ML, Ladell K, Andrews R, Jones RE, Miners KL, et al. 2018. CCR8 expression defines tissue-resident memory T cells in human skin. J. Immunol 200:1639–50 [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. [61]Terpstra ML, Remmerswaal EBM, van der Bom-Baylon ND, Sinnige MJ, Kers J, et al. 2020. Tissue-resident mucosal-associated invariant T (MAIT) cells in the human kidney represent a functionally distinct subset. Eur. J. Immunol 50:1783–97 [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. [62]Kumar BV, Ma W, Miron M, Granot T, Guyer RS, et al. 2017. Human tissue-resident memory T cells are defined by core transcriptional and functional signatures in lymphoid and mucosal sites. Cell Rep. 20:2921–34 [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. [63]Szabo PA, Levitin HM, Miron M, Snyder ME, Senda T, et al. 2019. Single-cell transcriptomics of human T cells reveals tissue and activation signatures in health and disease. Nat. Commun 10:4706. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. [65]Miron M, Kumar BV, Meng W, Granot T, Carpenter DJ, et al. 2018. Human lymph nodes maintain TCF-1hi memory T cells with high functional potential and clonal diversity throughout life. J.Immunol 201:2132–40 [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. [66]Day C, Patel R, Guillen C, Wardlaw AJ. 2009. The chemokine CXCL16 is highly and constitutively expressed by human bronchial epithelial cells. Exp. Lung Res 35:272–83 [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. [67]Pallett LJ, Davies J, Colbeck EJ, Robertson F, Hansi N, et al. 2017. IL-2high tissue-resident T cells in the human liver: sentinels for hepatotropic infection. J. Exp. Med 214:1567–80 [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. [68]Kumar BV, Kratchmarov R, Miron M, Carpenter DJ, Senda T, et al. 2018. Functional heterogeneity of human tissue-resident memory T cells based on dye efflux capacities. JCI Insight 3:e123568. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. [69]Dogra P, Rancan C, Ma W, Toth M, Senda T, et al. 2020. Tissue determinants of human NK cell development, function, and residence. Cell 180:749–63.e13 [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. [70]Marquardt N, Kekalainen E, Chen P, Lourda M, Wilson JN, et al. 2019. Unique transcriptional and protein-expression signature in human lung tissue-resident NK cells. Nat. Commun 10:3841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. [71]Zhao J, Zhang S, Liu Y, He X, Qu M, et al. 2020. Single-cell RNA sequencing reveals the heterogeneity of liver-resident immune cells in human. Cell Discov. 6:22. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. [72]Brownlie D, Scharenberg M, Mold JE, Hard J, Kekalainen E, et al. 2021. Expansions of adaptive-like NK cells with a tissue-resident phenotype in human lung and blood. PNAS 118:e2016580118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. [73]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-gamma-producing cells. Immunity 38:769–81 [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. [74]Yudanin NA, Schmitz F, Flamar AL, Thome JJC, Tait Wojno E, et al. 2019. Spatial and temporal mapping of human innate lymphoid cells reveals elements of tissue specificity. Immunity 50:505–19.e4 [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. [75]Bar-Ephraim YE, Cornelissen F, Papazian N, Konijn T, Hoogenboezem RM, et al. 2017. Cross-tissue transcriptomic analysis of human secondary lymphoid organ-residing ILC3s reveals a quiescent state in the absence of inflammation. Cell Rep. 21:823–33 [DOI] [PubMed] [Google Scholar]
  68. [76]Bar-Ephraim YE, Koning JJ, Burniol Ruiz E, Konijn T, Mourits VP, et al. 2019. CD62L is a functional and phenotypic marker for circulating innate lymphoid cell precursors. J. Immunol 202:171–82 [DOI] [PubMed] [Google Scholar]
  69. [77]Lim AI, Li Y, Lopez-Lastra S, Stadhouders R, Paul F, et al. 2017. Systemic human ILC precursors provide a substrate for tissue ILC differentiation. Cell 168:1086–100.e10 [DOI] [PubMed] [Google Scholar]
  70. [78]Mjosberg JM, Trifari S, Crellin NK, Peters CP, van Drunen CM, et al. 2011. Human IL-25- and IL-33-responsive type 2 innate lymphoid cells are defined by expression of CRTH2 and CD161. Nat.Immunol 12:1055–62 [DOI] [PubMed] [Google Scholar]
  71. [79]Simoni Y, Fehlings M, Kloverpris HN, McGovern N, Koo SL, et al. 2017. Human innate lymphoid cell subsets possess tissue-type based heterogeneity in phenotype and frequency. Immunity 46:148–61 [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. [80]Bjorklund AK, Forkel M, Picelli S, Konya V, Theorell J, et al. 2016. The heterogeneity of human CD127+ innate lymphoid cells revealed by single-cell RNA sequencing. Nat. Immunol 17:451–60 [DOI] [PubMed] [Google Scholar]
  73. [81]Hoorweg K, Peters CP, Cornelissen F, Aparicio-Domingo P, Papazian N, et al. 2012. Functional differences between human NKp44− and NKp44+ RORC+ innate lymphoid cells. Front. Immunol 3:72. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. [84]Gherardini J, Uchida Y, Hardman JA, Chéret J, Mace K, et al. 2020. Tissue-resident macrophages can be generated de novo in adult human skin from resident progenitor cells during substance P-mediated neurogenic inflammation ex vivo. PLOS ONE 15:e0227817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. [85]Hsu AP, Sampaio EP, Khan J, Calvo KR, Lemieux JE, et al. 2011. Mutations in GATA2 are associated with the autosomal dominant and sporadic monocytopenia and mycobacterial infection (MonoMAC) syndrome. Blood 118:2653–55 [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. [86]Vinh DC, Patel SY, Uzel G, Anderson VL, Freeman AF, et al. 2010. Autosomal dominant and sporadic monocytopenia with susceptibility to mycobacteria, fungi, papillomaviruses, and myelodysplasia. Blood 115:1519–29 [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. [87]Eguíluz-Gracia I, Lawaetz Schultz HH, Sikkeland LIB, Danilova E, Holm AM, et al. 2016. Long-term persistence of human donor alveolar macrophages in lung transplant recipients. Thorax 71:1006–11 [DOI] [PubMed] [Google Scholar]
  78. [88]Kamada N, Hisamatsu T, Honda H, Kobayashi T, Chinen H, et al. 2009. Human CD14+ macrophages in intestinal lamina propria exhibit potent antigen-presenting ability. J. Immunol 183:1724–31 [DOI] [PubMed] [Google Scholar]
  79. [89]Ráki M, Tollefsen S, Molberg Ø, Lundin KEA, Sollid LM, Jahnsen FL. 2006. A unique dendritic cell subset accumulates in the celiac lesion and efficiently activates gluten-reactive T cells. Gastroenterology 131:428–38 [DOI] [PubMed] [Google Scholar]
  80. [93]Wang X, Rao H, Zhao J, Wee A, Li X, et al. 2020. STING expression in monocyte-derived macrophages is associated with the progression of liver inflammation and fibrosis in patients with nonalcoholic fatty liver disease. Lab. Investig 100:542–52 [DOI] [PubMed] [Google Scholar]
  81. [94]Jardine L, Cytlak U, Gunawan M, Reynolds G, Green K, et al. 2020. Donor monocyte-derived macrophages promote human acute graft-versus-host disease. J. Clin. Investig 130:4574–86 [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. [95]Keophiphath M, Rouault C, Divoux A, Clement K, Lacasa D. 2010. CCL5 promotes macrophage recruitment and survival in human adipose tissue. Arterioscler. Thromb. Vasc. Biol 30:39–45 [DOI] [PubMed] [Google Scholar]
  83. [96]Goodman T,Lefrancois L. 1989. Intraepithelial lymphocytes: Anatomical site, not T cell receptor form, dictates phenotype and function. J. Exp. Med 170:1569–81 [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. [97]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 [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. [98]Havran WL, Allison JP. 1990. Origin of Thy-1+ dendritic epidermal cells of adult mice from fetal thymic precursors. Nature 344:68–70 [DOI] [PubMed] [Google Scholar]
  86. [99]Itohara S, Farr AG, Lafaille JJ, Bonneville M, Takagaki Y, et al. 1990. Homing of a γδ thymocyte subset with homogeneous T-cell receptors to mucosal epithelia. Nature 343:754–57 [DOI] [PubMed] [Google Scholar]
  87. [100]Carding SR, Kyes S, Jenkinson EJ, Kingston R, Bottomly K, et al. 1990. Developmentally regulated fetal thymic and extrathymic T-cell receptor γδ gene expression. Genes Dev. 4:1304–15 [DOI] [PubMed] [Google Scholar]
  88. [101]Haas JD, Ravens S, Düber S, Sandrock I, Oberdörfer L, et al. 2012. Development of interleukin-17-producing γδ T cells is restricted to a functional embryonic wave. Immunity 37:48–59 [DOI] [PubMed] [Google Scholar]
  89. [102]McVay LD, Carding SR. 1996. Extrathymic origin of human gamma delta T cells during fetal development. J. Immunol 157(7):2873–82 [PubMed] [Google Scholar]
  90. [103]McVay LD, Carding SR, Bottomly K, Hayday AC. 1991. Regulated expression and structure of T cell receptor γ/δ transcripts in human thymic ontogeny. EMBO J. 10:83–91 [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. [106]Deusch K, Lüling F, Reich K, Classen M, Wagner H, Pfeffer K. 1991. A major fraction of human intraepithelial lymphocytes simultaneously expresses the γ/δ T cell receptor, the CD8 accessory molecule and preferentially uses the Vδ1 gene segment. Eur. J. Immunol 21:1053–59 [DOI] [PubMed] [Google Scholar]
  92. [107]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 [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. [108]Ullrich R, Schieferdecker HL, Ziegler K, Riecken EO, Zeitz M. 1990. γδ T cells in the human intestine express surface markers of activation and are preferentially located in the epithelium. Cell. Immunol 128:619–27 [DOI] [PubMed] [Google Scholar]
  94. [109]Stras SF, Werner L, Toothaker JM, Olaloye OO, Oldham AL, et al. 2019. Maturation of the human intestinal immune system occurs early in fetal development. Dev. Cell 51:357–73.e5 [DOI] [PubMed] [Google Scholar]
  95. [110]Schreurs R, Baumdick ME, Sagebiel AF, Kaufmann M, Mokry M, et al. 2019. Human fetal TNF-α-cytokine-producing CD4+ effector memory T cells promote intestinal development and mediate inflammation early in life. Immunity 50:462–76.e8 [DOI] [PubMed] [Google Scholar]
  96. [111]Li N, van Unen V, Abdelaal T, Guo N, Kasatskaya SA, et al. 2019. Memory CD4+ T cells are generated in the human fetal intestine. Nat. Immunol 20:301–12 [DOI] [PMC free article] [PubMed] [Google Scholar]
  97. [114]Connors TJ, Baird JS, Yopes MC, Zens KD, Pethe K, et al. 2018. Developmental regulation of effector and resident memory T cell generation during pediatric viral respiratory tract infection. J. Immunol 201:432–39 [DOI] [PMC free article] [PubMed] [Google Scholar]
  98. [115]Bourdely P, Anselmi G, Vaivode K, Ramos RN, Missolo-Koussou Y, et al. 2020. Transcriptional and functional analysis of CD1c+ human dendritic cells identifies a CD163+ subset priming CD8+CD103+ T cells. Immunity 53:335–52.e8 [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. [116]Zhang N, Bevan MJ. 2013. Transforming growth factor-beta signaling controls the formation and maintenance of gut-resident memory T cells by regulating migration and retention. Immunity 39:687–96 [DOI] [PMC free article] [PubMed] [Google Scholar]
  100. [117]Pizzolla A, Nguyen TH, Sant S, Jaffar J, Loudovaris T, et al. 2018. Influenza-specific lung-resident memory T cells are proliferative and polyfunctional and maintain diverse TCR profiles. J. Clin. Investig 128:721–33 [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. [118]Turner DL, Bickham KL, Thome JJ, Kim CY, D’Ovidio F, et al. 2014. Lung niches for the generation and maintenance of tissue-resident memory T cells. Mucosal Immunol. 7:501–10 [DOI] [PMC free article] [PubMed] [Google Scholar]
  102. [119]Poon MML, Byington E, Meng W, Kubota M, Matsumoto R, et al. 2021. Heterogeneity of human anti-viral immunity shaped by virus, tissue, age, and sex. Cell Rep. 37(9):110071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  103. [120]Poon MML, Rybkina K, Kato Y, Kubota M, Matsumoto R, et al. 2021. SARS-CoV-2 infection generatest issue-localized immunological memory in humans. Sci. Immunol 6(65):eabl9105 [DOI] [PMC free article] [PubMed] [Google Scholar]
  104. [121]Hegazy AN, West NR, Stubbington MJT, Wendt E, Suijker KIM, et al. 2017. Circulating and tissue-resident CD4+ T cells with reactivity to intestinal microbiota are abundant in healthy individuals and function is altered during inflammation. Gastroenterology 153:1320–37.e16 [DOI] [PMC free article] [PubMed] [Google Scholar]
  105. [122]Djenidi F, Adam J, Goubar A, Durgeau A, Meurice G, et al. 2015. CD8+CD103+ tumor-infiltrating lymphocytes are tumor-specific tissue-resident memory T cells and a prognostic factor for survival in lung cancer patients. J. Immunol 194:3475–86 [DOI] [PubMed] [Google Scholar]
  106. [123]Okła K, Farber DL, Zou W. 2021. Tissue-resident memory T cells in tumor immunity and immunotherapy. J. Exp. Med 218:e20201605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  107. [124]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 [DOI] [PMC free article] [PubMed] [Google Scholar]
  108. [125]Miron M, Meng W, Rosenfeld AM, Dvorkin S, Poon MML, et al. 2021. Maintenance of the human memory T cell repertoire by subset and tissue site. Genome Med. 13:100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  109. [126]Morris SE, Farber DL, Yates AJ. 2019. Tissue-resident memory T cells in mice and humans: towards a quantitative ecology. J. Immunol 203:2561–69 [DOI] [PMC free article] [PubMed] [Google Scholar]
  110. [127]Snyder ME, Finlayson MO, Connors TJ, Dogra P, Senda T, et al. 2019. Generation and persistence of human tissue-resident memory T cells in lung transplantation. Sci. Immunol 4:eaav5581 [DOI] [PMC free article] [PubMed] [Google Scholar]
  111. [128]Bartolome-Casado R, Landsverk OJB, Chauhan SK, Richter L, Phung D, et al. 2019. Resident memory CD8 T cells persist for years in human small intestine. J. Exp. Med 216:2412–26 [DOI] [PMC free article] [PubMed] [Google Scholar]
  112. [129]Bartolomé-Casado R, Landsverk OJB, Chauhan SK, Sætre F, Hagen KT, et al. 2021. CD4+ T cells persist for years in the human small intestine and display a TH1 cytokine profile. Mucosal Immunol. 14(2):402–10 [DOI] [PubMed] [Google Scholar]
  113. [130]Zuber J, Shonts B, Lau SP, Obradovic A, Fu J, et al. 2016. Bidirectional intragraft alloreactivity drives the repopulation of human intestinal allografts and correlates with clinical outcome. Sci. Immunol 1:eaah3732 [DOI] [PMC free article] [PubMed] [Google Scholar]
  114. [131]Hombrink P, Helbig C, Backer RA, Piet B, Oja AE, et al. 2016. Programs for the persistence, vigilance and control of human CD8+ lung-resident memory T cells. Nat. Immunol 17:1467–78 [DOI] [PubMed] [Google Scholar]
  115. [132]Vieira Braga FA, Hertoghs KM, Kragten NA, Doody GM, Barnes NA, et al. 2015. Blimp-1 homolog Hobit identifies effector-type lymphocytes in humans. Eur. J. Immunol 45:2945–58 [DOI] [PubMed] [Google Scholar]
  116. [133]Huntington ND, Alves NL, Legrand N, Lim A, Strick-Marchand H, et al. 2011. IL-15 transpresentation promotes both human T-cell reconstitution and T-cell-dependent antibody responses in vivo. PNAS 108:6217–22 [DOI] [PMC free article] [PubMed] [Google Scholar]
  117. [134]Nozad Charoudeh H, Tang Y, Cheng M, Cilio CM, Jacobsen SE, Sitnicka E. 2010. Identification of an NK/T cell-restricted progenitor in adult bone marrow contributing to bone marrow- and thymicdependent NK cells. Blood 116:183–92 [DOI] [PubMed] [Google Scholar]
  118. [135]Yu J, Freud AG, Caligiuri MA. 2013. Location and cellular stages of natural killer cell development. Trends Immunol. 34:573–82 [DOI] [PMC free article] [PubMed] [Google Scholar]
  119. [136]Cuff AO, Robertson FP, Stegmann KA, Pallett LJ, Maini MK, et al. 2016. Eomeshi NK cells in human liver are long-lived and do not recirculate but can be replenished from the circulation. J. Immunol 197:4283–91 [DOI] [PMC free article] [PubMed] [Google Scholar]
  120. [137]Lunemann S, Martrus G, Goebels H, Kautz T, Langeneckert A, et al. 2017. Hobit expression by a subset of human liver-resident CD56bright natural killer cells. Sci. Rep 7:6676. [DOI] [PMC free article] [PubMed] [Google Scholar]
  121. [138]Melsen JE, Lugthart G, Vervat C, Kielbasa SM, van der Zeeuw SAJ, et al. 2018. Human bone marrowresident natural killer cells have a unique transcriptional profile and resemble resident memory CD8+ T cells. Front. Immunol 9:1829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  122. [139]Scoville SD, Mundy-Bosse BL, Zhang MH, Chen L, Zhang X, et al. 2016. A progenitor cell expressing transcription factor RORγt generates all human innate lymphoid cell subsets. Immunity 44:1140–50 [DOI] [PMC free article] [PubMed] [Google Scholar]
  123. [140]Vivier E, Artis D, Colonna M, Diefenbach A, Di Santo JP, et al. 2018. Innate lymphoid cells: 10 years on. Cell 174:1054–66 [DOI] [PubMed] [Google Scholar]
  124. [141]Mjosberg J, Bernink J, Golebski K, Karrich JJ, Peters CP, et al. 2012. The transcription factor GATA3 is essential for the function of human type 2 innate lymphoid cells. Immunity 37:649–59 [DOI] [PubMed] [Google Scholar]
  125. [142]Orecchioni M, Ghosheh Y, Pramod AB, Ley K. 2019. Macrophage polarization: different gene signatures in M1 (LPS+) vs. classically and M2 (LPS−) vs. alternatively activated macrophages. Front. Immunol 10:1084. [DOI] [PMC free article] [PubMed] [Google Scholar]
  126. [143]Bissonnette EY, Lauzon-Joset JF, Debley JS, Ziegler SF. 2020. Cross-talk between alveolar macrophages and lung epithelial cells is essential to maintain lung homeostasis. Front. Immunol 11:583042. [DOI] [PMC free article] [PubMed] [Google Scholar]
  127. [144]Balhara J, Gounni AS. 2012. The alveolar macrophages in asthma: a double-edged sword. Mucosal Immunol. 5:605–9 [DOI] [PubMed] [Google Scholar]
  128. [145]Berenson CS, Kruzel RL, Eberhardt E, Sethi S. 2013. Phagocytic dysfunction of human alveolar macrophages and severity of chronic obstructive pulmonary disease. J. Infect. Dis 208:2036–45 [DOI] [PMC free article] [PubMed] [Google Scholar]
  129. [146]Mathias LJ, Khong SML, Spyroglou L, Payne NL, Siatskas C, et al. 2013. Alveolar macrophages are critical for the inhibition of allergic asthma by mesenchymal stromal cells. J. Immunol 191:5914–24 [DOI] [PubMed] [Google Scholar]
  130. [147]Vlahos R, Bozinovski S. 2014. Role of alveolar macrophages in chronic obstructive pulmonary disease. Front. Immunol 5:435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  131. [148]Trapnell BC, Nakata K, Bonella F, Campo I, Griese M, et al. 2019. Pulmonary alveolar proteinosis. Nat. Rev. Dis. Primers 5:16. [DOI] [PubMed] [Google Scholar]
  132. [149]Bivona JJ, Crymble HM, Guigni BA, Stapleton RD, Files DC, et al. 2021. Macrophages augment the skeletal muscle proinflammatory response through TNFα following LPS-induced acute lung injury. FASEB J. 35:e21462. [DOI] [PMC free article] [PubMed] [Google Scholar]
  133. [150]Drummond RA, Swamydas M, Oikonomou V, Zhai B, Dambuza IM, et al. 2019. CARD9 + microglia promote antifungal immunity via IL-1β- and CXCL1-mediated neutrophil recruitment. Nat. Immunol 20:559–70 [DOI] [PMC free article] [PubMed] [Google Scholar]
  134. [151]Larsson BM, Larsson K, Malmberg P, Palmberg L. 1999. Gram positive bacteria induce IL-6 and IL-8 production in human alveolar macrophages and epithelial cells. Inflammation 23:217–30 [DOI] [PubMed] [Google Scholar]
  135. [152]Bujko A, Atlasy N, Landsverk OJB, Richter L, Yaqub S, et al. 2018. Transcriptional and functional profiling defines human small intestinal macrophage subsets. J. Exp. Med 215:441–58 [DOI] [PMC free article] [PubMed] [Google Scholar]
  136. [153]Melms JC, Biermann J, Huang H, Wang Y, Nair A, et al. 2021. A molecular single-cell lung atlas of lethal COVID-19. Nature 595:114–19 [DOI] [PMC free article] [PubMed] [Google Scholar]
  137. [154]Arnold CE, Gordon P, Barker RN, Wilson HM. 2015. The activation status of human macrophages presenting antigen determines the efficiency of Th17 responses. Immunobiology 220:10–19 [DOI] [PubMed] [Google Scholar]
  138. [155]Muntjewerff EM, Meesters LD, van den Bogaart G. 2020. Antigen cross-presentation by macrophages. Front. Immunol 11:1276. [DOI] [PMC free article] [PubMed] [Google Scholar]
  139. [156]Tang-Huau TL, Gueguen P, Goudot C, Durand M, Bohec M, et al. 2018. Human in vivo-generated monocyte-derived dendritic cells and macrophages cross-present antigens through a vacuolar pathway. Nat. Commun 9:2570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  140. [157]Dijkgraaf FE, Matos TR, Hoogenboezem M, Toebes M, Vredevoogd DW, et al. 2019. Tissue patrol by resident memory CD8+ T cells in human skin. Nat. Immunol 20:756–64 [DOI] [PubMed] [Google Scholar]
  141. [158]Snyder ME, Sembrat J, Noda K, Myerburg MM, Craig A, et al. 2021. Human lung-resident macrophages colocalize with and provide costimulation to PD1hi tissue-resident memory T cells. Am. J. Respir. Crit. Care Med 203:1230–44 [DOI] [PMC free article] [PubMed] [Google Scholar]
  142. [159]Rao A, Strauss O, Kokkinou E, Bruchard M, Tripathi KP, et al. 2020. Cytokines regulate the antigen-presenting characteristics of human circulating and tissue-resident intestinal ILCs. Nat. Commun 11:2049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  143. [160]Tu Z, Bozorgzadeh A, Pierce RH, Kurtis J, Crispe IN, Orloff MS. 2008. TLR-dependent cross talk between human Kupffer cells and NK cells. J. Exp. Med 205:233–44 [DOI] [PMC free article] [PubMed] [Google Scholar]
  144. [161]Pallett LJ, Davies J, Colbeck EJ, Robertson F, Hansi N, et al. 2017. IL-2high tissue-resident T cells in the human liver: sentinels for hepatotropic infection. J. Exp. Med 214:1567–80 [DOI] [PMC free article] [PubMed] [Google Scholar]
  145. [162]Jozwik A, Habibi MS, Paras A, Zhu J, Guvenel A, et al. 2016. RSV-specific airway resident memory CD8+ T cells and differential disease severity after experimental human infection. Nat. Commun 6:10224. Erratum. 2015. Nat. Commun. 7:11011 [DOI] [PMC free article] [PubMed] [Google Scholar]
  146. [163]Hernández-Castañeda MA, Happ K, Cattalani F, Wallimann A, Blanchard M, et al. 2020. γδ T cells kill Plasmodium falciparum in a granzyme- and granulysin-dependent mechanism during the late blood stage. J. Immunol 204:1798–809 [DOI] [PMC free article] [PubMed] [Google Scholar]
  147. [164]Couzi L, Pitard V, Sicard X, Garrigue I, Hawchar O, et al. 2012. Antibody-dependent anticytomegalovirus activity of human γδ T cells expressing CD16 (FcγRIIIa). Blood 119:1418–27 [DOI] [PubMed] [Google Scholar]
  148. [165]Li H, Xiang Z, Feng T, Li J, Liu Y, et al. 2013. Human Vγ9Vδ2-T cells efficiently kill influenza virusinfected lung alveolar epithelial cells. Cell. Mol. Immunol 10:159–64 [DOI] [PMC free article] [PubMed] [Google Scholar]
  149. [166]Vandereyken M, James OJ, Swamy M. 2020. Mechanisms of activation of innate-like intraepithelial T lymphocytes. Cell. Immunol 13:721–31 [DOI] [PMC free article] [PubMed] [Google Scholar]
  150. [167]Scharenberg M, Vangeti S, Kekalainen E, Bergman P, Al-Ameri M, et al. 2019. Influenza A virus infection induces hyperresponsiveness in human lung tissue-resident and peripheral blood NK cells. Front. Immunol 10:1116. [DOI] [PMC free article] [PubMed] [Google Scholar]
  151. [168]Blumenthal RL, Campbell DE, Hwang P, DeKruyff RH, Frankel LR, Umetsu DT. 2001. Human alveolar macrophages induce functional inactivation in antigen-specific CD4 T cells. J. Allergy Clin. Immunol 107:258–64 [DOI] [PubMed] [Google Scholar]
  152. [169]Coleman MM, Ruane D, Moran B, Dunne PJ, Keane J, Mills KHG. 2013. Alveolar macrophages contribute to respiratory tolerance by inducing FoxP3 expression in naive T cells. Am. J. Respir. Cell Mol. Biol 48:773–80 [DOI] [PubMed] [Google Scholar]
  153. [170]Grunwell JR, Yeligar SM, Stephenson S, Ping XD, Gauthier TW, et al. 2018. TGF-β1 suppresses the type I IFN response and induces mitochondrial dysfunction in alveolar macrophages. J. Immunol 200:2115–28 [DOI] [PMC free article] [PubMed] [Google Scholar]
  154. [171]Roth MD, Golub SH. 1993. Human pulmonary macrophages utilize prostaglandins and transforming growth factor β1 to suppress lymphocyte activation. J. Leukoc. Biol 53:366–71 [DOI] [PubMed] [Google Scholar]
  155. [173]Allard B, Panariti A, Martin JG. 2018. Alveolar macrophages in the resolution of inflammation, tissue repair, and tolerance to infection. Front. Immunol 9:1777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  156. [174]Mahida RY, Scott A, Parekh D, Lugg ST, Hardy RS, et al. 2021. Acute Respiratory Distress Syndrome is associated with impaired alveolar macrophage efferocytosis. Eur. Respir. J 58(3):2100829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  157. [175]Bajpai G, Schneider C, Wong N, Bredemeyer A, Hulsmans M, et al. 2018. The human heart contains distinct macrophage subsets with divergent origins and functions. Nat. Med 24:1234–45 [DOI] [PMC free article] [PubMed] [Google Scholar]
  158. [176]Dalby E, Christensen SM, Wang J, Hamidzadeh K, Chandrasekaran P, et al. 2020. Immune complex–driven generation of human macrophages with anti-inflammatory and growth-promoting activity. J. Immunol 205:102–12 [DOI] [PMC free article] [PubMed] [Google Scholar]
  159. [177]Kasikara C, Schilperoort M, Gerlach B, Xue C, Wang X, et al. 2021. Deficiency of macrophage PHACTR1 impairs efferocytosis and promotes atherosclerotic plaque necrosis. J. Clin. Investig 131:e145275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  160. [178]Soares L, Tsavaler L, Rivas A, Engleman E. 1998. V7 (CD101) ligation inhibits TCR/CD3-induced IL-2 production by blocking Ca2+ flux and nuclear factor of activated T cell nuclear translocation. J. Immunol 161: 209–17 [PubMed] [Google Scholar]
  161. [179]Smolders J, Heutinck KM, Fransen NL, Remmerswaal EBM, Hombrink P, et al. 2018. Tissue-resident memory T cells populate the human brain. Nat. Commun 9(1):4593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  162. [180]Watad A, Rowe H, Russell T, Zhou Q, Anderson LK, et al. 2020. Normal human enthesis harbours conventional CD4+ and CD8+ T cells with regulatory features and inducible IL-17A and TNF expression. Ann. Rheumat. Dis 79:1044–54 [DOI] [PMC free article] [PubMed] [Google Scholar]
  163. [181]Lam AJ, MacDonald KN, Pesenacker AM, Juvet SC, Morishita KA, et al. 2019. Innate control of tissuereparative human regulatory T cells. J. Immunol 202:2195–209 [DOI] [PubMed] [Google Scholar]
  164. [182]Casetti R,Agrati C,Wallace M,Sacchi A,Martini F,et al. 2009. Cutting edge: TGF-β1 and IL-15 induce FOXP3 + γδ regulatory T cells in the presence of antigen stimulation. J. Immunol 183:3574–77 [DOI] [PubMed] [Google Scholar]
  165. [183]Kouakanou L, Peters C, Sun Q, Floess S, Bhat J, et al. 2020. Vitamin C supports conversion of human γδ T cells into FOXP3-expressing regulatory cells by epigenetic regulation. Sci. Rep 10:6550. [DOI] [PMC free article] [PubMed] [Google Scholar]
  166. [184]Kühl AA, Pawlowski NN, Grollich K, Blessenohl M, Westermann J, et al. 2009. Human peripheral γδ T cells possess regulatory potential. Immunology 128:580–88 [DOI] [PMC free article] [PubMed] [Google Scholar]
  167. [185]Krishnan S, Prise IE, Wemyss K, Schenck LP, Bridgeman HM, et al. 2018. Amphiregulin-producing γδ T cells are vital for safeguarding oral barrier immune homeostasis. PNAS 115:10738–43 [DOI] [PMC free article] [PubMed] [Google Scholar]
  168. [186]Fazio J, Quabius ES, Müller A, Adam-Klages S, Wesch D, et al. 2013. Vδ2 T cell deficiency in granulomatosis with polyangiitis (Wegener’s granulomatosis). Clin. Immunol 149:65–72 [DOI] [PubMed] [Google Scholar]
  169. [187]Cerboni C, Zingoni A, Cippitelli M, Piccoli M, Frati L, Santoni A. 2007. 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 110:606–15 [DOI] [PubMed] [Google Scholar]
  170. [188]Rabinovich BA, Li J, Shannon J, Hurren R, Chalupny J, et al. 2003. Activated, but not resting, T cells can be recognized and killed by syngeneic NK cells. J. Immunol 170:3572–6 [DOI] [PubMed] [Google Scholar]
  171. [189]Nielsen N, Odum N, Urso B, Lanier LL, Spee P. 2012. Cytotoxicity of CD56bright NK cells towards autologous activated CD4+ T cells is mediated through NKG2D, LFA-1 and TRAIL and dampened via CD94/NKG2A. PLOS ONE 7:e31959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  172. [190]Fasbender F, Widera A, Hengstler JG, Watzl C. 2016. Natural killer cells and liver fibrosis. Front. Immunol 7:19. [DOI] [PMC free article] [PubMed] [Google Scholar]

Cited by

Sorted by citations

Authors
Gray, J. I., & Farber, D. L.
Affiliations
  • Columbia University Irving Medical Center (US)
  • Department of Microbiology and Immunology, Columbia University Irving Medical Center, New York, USA;
Venue
Annual Review of Immunology
Publisher
Annual Reviews
Published
2022-04-26
Volume
40
Issue
1
Pages
195-220
ISSN
  • 0732-0582 (ISSN-L)
  • 1545-3278
DOI
10.1146/annurev-immunol-093019-112809
PMC
PMC11194112
OpenAlex
W4206764390
Cited by
181
References
19
Citations by year
2026: 40 · 2025: 55 · 2024: 44 · 2023: 28 · 2022: 14
FWCI
3.70
Type
journal article
Language
en
Open access
Locations
  • Annual Review of Immunology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institute of Allergy and Infectious Diseases (P01AI106697, U19AI128949)
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
  • Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
  • Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
Keywords
tissue-resident immune cells, myeloid cells, lymphoid cells, immune homeostasis, inflammation resolution, tissue repair, immune cell development, human tissue, immune cell classification
MeSH terms
Animals, Homeostasis, Humans, Immunity, Innate, Inflammation, Lymphocytes, Cell Lineage

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