1932

Abstract

Cell identity and function largely rely on the programming of transcriptomes during development and differentiation. Signature gene expression programs are orchestrated by regulatory circuits consisting of acting promoters and enhancers, which respond to a plethora of cues via the action of transcription factors. In turn, transcription factors direct epigenetic modifications to revise chromatin landscapes, and drive contacts between distal promoter-enhancer combinations. In immune cells, regulatory circuits for effector genes are especially complex and flexible, utilizing distinct sets of transcription factors and enhancers, depending on the cues each cell type receives during an infection, after sensing cellular damage, or upon encountering a tumor. Here, we review major players in the coordination of gene regulatory programs within innate and adaptive immune cells, as well as integrative omics approaches that can be leveraged to decipher their underlying circuitry.

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2022-04-26
2024-06-16
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Literature Cited

  1. 1. 
    Sartorelli V, Lauberth SM. 2020. Enhancer RNAs are an important regulatory layer of the epigenome. Nat. Struct. Mol. Biol. 27:6521–28
    [Google Scholar]
  2. 2. 
    Dunham I, Kundaje A, Aldred SF, Collins PJ, Davis CA et al. 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489:741457–74
    [Google Scholar]
  3. 3. 
    Chaudhri VK, Dienger-Stambaugh K, Wu Z, Shrestha M, Singh H. 2020. Charting the cis-regulome of activated B cells by coupling structural and functional genomics. Nat. Immunol. 21:2210–20
    [Google Scholar]
  4. 4. 
    Holliday R, Pugh JE. 1975. DNA modification mechanisms and gene activity during development. Science 187:4173226–32
    [Google Scholar]
  5. 5. 
    Riggs AD. 1975. X inactivation, differentiation, and DNA methylation. Cytogenet. Genome Res. 14:19–25
    [Google Scholar]
  6. 6. 
    Strahl BD, Allis CD. 2000. The language of covalent histone modifications. Nature 403:676541–45
    [Google Scholar]
  7. 7. 
    Rothbart SB, Strahl BD. 2014. Interpreting the language of histone and DNA modifications. Biochem. Biophys. Acta Gene Reg. Mech. 1839:8627–43
    [Google Scholar]
  8. 8. 
    Jenuwein T, Allis CD. 2001. Translating the histone code. Science 293:55321074–80
    [Google Scholar]
  9. 9. 
    Myers FA, Evans DR, Clayton AL, Thorne AW, Crane-Robinson C. 2001. Targeted and extended acetylation of histones H4 and H3 at active and inactive genes in chicken embryo erythrocytes. J. Biol. Chem. 276:2320197–205
    [Google Scholar]
  10. 10. 
    Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW et al. 2010. Histone H3K27ac separates active from poised enhancers and predicts developmental state. PNAS 107:5021931–36
    [Google Scholar]
  11. 11. 
    Raisner R, Kharbanda S, Jin L, Jeng E, Chan E et al. 2018. Enhancer activity requires CBP/P300 bromodomain-dependent histone H3K27 acetylation. Cell Rep 24:71722–29
    [Google Scholar]
  12. 12. 
    Ng HH, Ciccone DN, Morshead KB, Oettinger MA, Struhl K. 2003. Lysine-79 of histone H3 is hypomethylated at silenced loci in yeast and mammalian cells: a potential mechanism for position-effect variegation. PNAS 100:41820–25
    [Google Scholar]
  13. 13. 
    Liang G, Lin JCY, Wei V, Yoo C, Cheng JC et al. 2004. Distinct localization of histone H3 acetylation and H3-K4 methylation to the transcription start sites in the human genome. PNAS 101:197357–62
    [Google Scholar]
  14. 14. 
    Barrera LO, Li Z, Smith AD, Arden KC, Cavenee WK et al. 2008. Genome-wide mapping and analysis of active promoters in mouse embryonic stem cells and adult organs. Genome Res 18:146–59
    [Google Scholar]
  15. 15. 
    Yoshida H, Lareau CA, Ramirez RN, Rose SA, Maier B et al. 2019. The cis-regulatory atlas of the mouse immune system. Cell 176:4897–912.e20
    [Google Scholar]
  16. 16. 
    Abascal F, Acosta R, Addleman NJ, Adrian J, Afzal V et al. 2020. Expanded encyclopaedias of DNA elements in the human and mouse genomes. Nature 583:7818699–710
    [Google Scholar]
  17. 17. 
    Collins PL, Cella M, Porter SI, Li S, Gurewitz GL et al. 2019. Gene regulatory programs conferring phenotypic identities to human NK cells. Cell 176:1–2348–60.e12
    [Google Scholar]
  18. 18. 
    Koues OI, Collins PL, Cella M, Robinette ML, Porter SI et al. 2016. Distinct gene regulatory pathways for human innate versus adaptive lymphoid cells. Cell 165:51134–46
    [Google Scholar]
  19. 19. 
    Brind'Amour J, Liu S, Hudson M, Chen C, Karimi MM, Lorincz MC. 2015. An ultra-low-input native ChIP-seq protocol for genome-wide profiling of rare cell populations. Nat. Commun. 6:6033
    [Google Scholar]
  20. 20. 
    Skene PJ, Henikoff JG, Henikoff S. 2018. Targeted in situ genome-wide profiling with high efficiency for low cell numbers. Nat. Protoc. 13:51006–19
    [Google Scholar]
  21. 21. 
    Rao SSP, Huntley MH, Durand NC, Stamenova EK, Bochkov ID et al. 2014. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159:71665–80
    [Google Scholar]
  22. 22. 
    Kempfer R, Pombo A. 2020. Methods for mapping 3D chromosome architecture. Nat. Rev. Genet. 21:4207–26
    [Google Scholar]
  23. 23. 
    Roels J, Kuchmiy A, De Decker M, Strubbe S, Lavaert M et al. 2020. Distinct and temporary-restricted epigenetic mechanisms regulate human αβ and γδ T cell development. Nat. Immunol. 21:101280–92
    [Google Scholar]
  24. 24. 
    Johnson JL, Georgakilas G, Petrovic J, Kurachi M, Cai S et al. 2018. Lineage-determining transcription factor TCF-1 initiates the epigenetic identity of T cells. Immunity 48:2243–57.e10
    [Google Scholar]
  25. 25. 
    Ungerbäck J, Hosokawa H, Wang X, Strid T, Williams BA et al. 2018. Pioneering, chromatin remodeling, and epigenetic constraint in early T-cell gene regulation by SPI1 (PU.1). Genome Res 28:101508–19
    [Google Scholar]
  26. 26. 
    Majumder K, Koues OI, Chan EAW, Kyle KE, Horowitz JE et al. 2015. Lineage-specific compaction of Tcrb requires a chromatin barrier to protect the function of a long-range tethering element. J. Exp. Med. 212:1107–20
    [Google Scholar]
  27. 27. 
    Gopalakrishnan S, Majumder K, Predeus A, Huang Y, Koues OI et al. 2013. Unifying model for molecular determinants of the preselection Vβ repertoire. PNAS 110:34E3206–15
    [Google Scholar]
  28. 28. 
    Martinez GJ, Pereira RM, Äijö T, Kim EY, Marangoni F et al. 2015. The transcription factor NFAT promotes exhaustion of activated CD8+ T cells. Immunity 42:2265–78
    [Google Scholar]
  29. 29. 
    Nutt SL, Kee BL. 2007. The transcriptional regulation of B cell lineage commitment. Immunity 26:6715–25
    [Google Scholar]
  30. 30. 
    Hart GT, Hogquist KA, Jameson SC. 2012. Krüppel-like factors in lymphocyte biology. J. Immunol. 188:2521–26
    [Google Scholar]
  31. 31. 
    Igarashi K, Ochiai K, Itoh-Nakadai A, Muto A. 2014. Orchestration of plasma cell differentiation by Bach2 and its gene regulatory network. Immunol. Rev. 261:1116–25
    [Google Scholar]
  32. 32. 
    Laidlaw BJ, Duan L, Xu Y, Vazquez SE, Cyster JG. 2020. The transcription factor Hhex cooperates with the corepressor Tle3 to promote memory B cell development. Nat. Immunol. 21:91082–93
    [Google Scholar]
  33. 33. 
    Ochiai K, Maienschein-Cline M, Simonetti G, Chen J, Rosenthal R et al. 2013. Transcriptional regulation of germinal center B and plasma cell fates by dynamical control of IRF4. Immunity 38:5918–29
    [Google Scholar]
  34. 34. 
    Sciammas R, Shaffer AL, Schatz JH, Zhao H, Staudt LM, Singh H. 2006. Graded expression of interferon regulatory factor-4 coordinates isotype switching with plasma cell differentiation. Immunity 25:2225–36
    [Google Scholar]
  35. 35. 
    Crotty S, Johnston RJ, Schoenberger SP. 2010. Effectors and memories: Bcl-6 and Blimp-1 in T and B lymphocyte differentiation. Nat. Immunol. 11:2114–20
    [Google Scholar]
  36. 36. 
    Choi J, Crotty S. 2021. Bcl6-mediated transcriptional regulation of follicular helper T cells (TFH). Trends Immunol 42:4336–49
    [Google Scholar]
  37. 37. 
    Roy K, Mitchell S, Liu Y, Ohta S, Lin Y-S et al. 2019. A regulatory circuit controlling the dynamics of NFκB cRel transitions B cells from proliferation to plasma cell differentiation. Immunity 50:3616–28.e6
    [Google Scholar]
  38. 38. 
    Patterson DG, Kania AK, Zuo Z, Scharer CD, Boss JM. 2021. Epigenetic gene regulation in plasma cells. Immunol. Rev. 303:18–22
    [Google Scholar]
  39. 39. 
    Manakkat Vijay GK, Singh H 2021. Cell fate dynamics and genomic programming of plasma cell precursors. Immunol. Rev. 303:162–71
    [Google Scholar]
  40. 40. 
    Trezise S, Nutt SL. 2021. The gene regulatory network controlling plasma cell function. Immunol. Rev. 303:123–34
    [Google Scholar]
  41. 41. 
    Arnold CD, Gerlach D, Stelzer C, Boryń ŁM, Rath M, Stark A. 2013. Genome-wide quantitative enhancer activity maps identified by STARR-seq. Science 339:61231074–77
    [Google Scholar]
  42. 42. 
    Barwick BG, Scharer CD, Bally APR, Boss JM. 2016. Plasma cell differentiation is coupled to division-dependent DNA hypomethylation and gene regulation. Nat. Immunol. 17:101216–25
    [Google Scholar]
  43. 43. 
    Scharer CD, Barwick BG, Guo M, Bally APR, Boss JM. 2018. Plasma cell differentiation is controlled by multiple cell division-coupled epigenetic programs. Nat. Commun. 9:11698
    [Google Scholar]
  44. 44. 
    Fujii K, Tanaka S, Hasegawa T, Narazaki M, Kumanogoh A et al. 2020. Tet DNA demethylase is required for plasma cell differentiation by controlling expression levels of IRF4. Int. Immunol. 32:10683–90
    [Google Scholar]
  45. 45. 
    Dominguez PM, Ghamlouch H, Rosikiewicz W, Kumar P, Béguelin W et al. 2018. TET2 deficiency causes germinal center hyperplasia, impairs plasma cell differentiation, and promotes B-cell lymphomagenesis. Cancer Discov 8:121633–53
    [Google Scholar]
  46. 46. 
    Lio CWJ, Shukla V, Samaniego-Castruita D, González-Avalos E, Chakraborty A et al. 2019. TET enzymes augment activation-induced deaminase (AID) expression via 5-hydroxymethylcytosine modifications at the Aicda superenhancer. Sci. Immunol. 4:34eaau7523
    [Google Scholar]
  47. 47. 
    Onodera A, González-Avalos E, Lio C-WJ, Georges RO, Bellacosa A et al. 2021. Roles of TET and TDG in DNA demethylation in proliferating and non-proliferating immune cells. Genome Biol 22:1186
    [Google Scholar]
  48. 48. 
    Johnston RJ, Poholek AC, DiToro D, Yusuf I, Eto D et al. 2009. Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation. Science 325:59431006–10
    [Google Scholar]
  49. 49. 
    Yu D, Rao S, Tsai LM, Lee SK, He Y et al. 2009. The transcriptional repressor Bcl-6 directs T follicular helper cell lineage commitment. Immunity 31:3457–68
    [Google Scholar]
  50. 50. 
    Nurieva RI, Chung Y, Martinez GJ, Yang XO, Tanaka S et al. 2009. Bcl6 mediates the development of T follicular helper cells. Science 325:59431001–5
    [Google Scholar]
  51. 51. 
    Choi J, Diao H, Faliti CE, Truong J, Rossi M et al. 2020. Bcl-6 is the nexus transcription factor of T follicular helper cells via repressor-of-repressor circuits. Nat. Immunol. 21:7777–89
    [Google Scholar]
  52. 52. 
    Moriyama S, Takahashi N, Green JA, Hori S, Kubo M et al. 2014. Sphingosine-1-phosphate receptor 2 is critical for follicular helper T cell retention in germinal centers. J. Exp. Med. 211:71297–305
    [Google Scholar]
  53. 53. 
    Fu G, Guy CS, Chapman NM, Palacios G, Wei J et al. 2021. Metabolic control of TFH cells and humoral immunity by phosphatidylethanolamine. Nature 595:7869724–29
    [Google Scholar]
  54. 54. 
    Weisel FJ, Mullett SJ, Elsner RA, Menk AV, Trivedi N et al. 2020. Germinal center B cells selectively oxidize fatty acids for energy while conducting minimal glycolysis. Nat. Immunol. 21:3331–42
    [Google Scholar]
  55. 55. 
    Oestreich KJ, Read KA, Gilbertson SE, Hough KP, McDonald PW et al. 2014. Bcl-6 directly represses the gene program of the glycolysis pathway. Nat. Immunol. 15:10957–64
    [Google Scholar]
  56. 56. 
    Lemonnier F, Couronné L, Parrens M, Jaïs JP, Travert M et al. 2012. Recurrent TET2 mutations in peripheral T-cell lymphomas correlate with TFH-like features and adverse clinical parameters. Blood 120:71466–69
    [Google Scholar]
  57. 57. 
    Barwick BG, Scharer CD, Martinez RJ, Price MJ, Wein AN et al. 2018. B cell activation and plasma cell differentiation are inhibited by de novo DNA methylation. Nat. Commun. 9:11900
    [Google Scholar]
  58. 58. 
    Sage PT, Sharpe AH. 2016. T follicular regulatory cells. Immunol. Rev. 271:1246–59
    [Google Scholar]
  59. 59. 
    Kennedy DE, Okoreeh MK, Maienschein-Cline M, Ai J, Veselits M et al. 2020. Novel specialized cell state and spatial compartments within the germinal center. Nat. Immunol. 21:6660–70
    [Google Scholar]
  60. 60. 
    Victora GD, Schwickert TA, Fooksman DR, Kamphorst AO, Meyer-Hermann M et al. 2010. Germinal center dynamics revealed by multiphoton microscopy with a photoactivatable fluorescent reporter. Cell 143:4592–605
    [Google Scholar]
  61. 61. 
    Danilova N. 2012. The evolution of adaptive immunity. Adv. Exp. Med. Biol. 738:218–35
    [Google Scholar]
  62. 62. 
    Netea MG, Joosten LAB, Latz E, Mills KHG, Natoli G et al. 2016. Trained immunity: a program of innate immune memory in health and disease. Science 352:6284aaf1098
    [Google Scholar]
  63. 63. 
    Naik S, Larsen SB, Gomez NC, Alaverdyan K, Sendoel A et al. 2017. Inflammatory memory sensitizes skin epithelial stem cells to tissue damage. Nature 550:7677475–80
    [Google Scholar]
  64. 64. 
    Kleinnijenhuis J, Quintin J, Preijers F, Joosten LAB, Jacobs C et al. 2014. BCG-induced trained immunity in NK cells: role for non-specific protection to infection. Clin. Immunol. 155:2213–19
    [Google Scholar]
  65. 65. 
    Divangahi M, Aaby P, Khader SA, Barreiro LB, Bekkering S et al. 2021. Trained immunity, tolerance, priming and differentiation: distinct immunological processes. Nat. Immunol. 22:12–6 Erratum. 2021. Nat. Immunol. 22:928
    [Google Scholar]
  66. 66. 
    Netea MG, van der Meer JWM. 2017. Trained immunity: an ancient way of remembering. Cell Host Microbe 21:3297–300
    [Google Scholar]
  67. 67. 
    Arts RJW, Moorlag SJCFM, Novakovic B, Li Y, Wang SY et al. 2018. BCG vaccination protects against experimental viral infection in humans through the induction of cytokines associated with trained immunity. Cell Host Microbe 23:189–100.e5
    [Google Scholar]
  68. 68. 
    Schnack L, Sohrabi Y, Lagache SMM, Kahles F, Bruemmer D et al. 2019. Mechanisms of trained innate immunity in oxLDL primed human coronary smooth muscle cells. Front. Immunol. 10:13
    [Google Scholar]
  69. 69. 
    Schrum JE, Crabtree JN, Dobbs KR, Kiritsy MC, Reed GW et al. 2018. Cutting edge: Plasmodium falciparum induces trained innate immunity. J. Immunol. 200:41243–48
    [Google Scholar]
  70. 70. 
    Christ A, Günther P, Lauterbach MAR, Duewell P, Biswas D et al. 2018. Western diet triggers NLRP3-dependent innate immune reprogramming. Cell 172:1–2162–75.e14
    [Google Scholar]
  71. 71. 
    You M, Chen L, Zhang D, Zhao P, Chen Z et al. 2021. Single-cell epigenomic landscape of peripheral immune cells reveals establishment of trained immunity in individuals convalescing from COVID-19. Nat. Cell Biol. 23:6620–30
    [Google Scholar]
  72. 72. 
    Fang TC, Schaefer U, Mecklenbrauker I, Stienen A, Dewell S et al. 2012. Histone H3 lysine 9 di-methylation as an epigenetic signature of the interferon response. J. Exp. Med. 209:4661–69
    [Google Scholar]
  73. 73. 
    De Santa F, Totaro MG, Prosperini E, Notarbartolo S, Testa G, Natoli G. 2007. The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of Polycomb-mediated gene silencing. Cell 130:61083–94
    [Google Scholar]
  74. 74. 
    Saeed S, Quintin J, Kerstens HHD, Rao NA, Aghajanirefah A et al. 2014. Epigenetic programming of monocyte-to-macrophage differentiation and trained innate immunity. Science 345:62041251086
    [Google Scholar]
  75. 75. 
    Buffen K, Oosting M, Quintin J, Ng A, Kleinnijenhuis J et al. 2014. Autophagy controls BCG-induced trained immunity and the response to intravesical BCG therapy for bladder cancer. PLOS Pathog 10:10e1004485
    [Google Scholar]
  76. 76. 
    Fanucchi S, Fok ET, Dalla E, Shibayama Y, Börner K et al. 2019. Immune genes are primed for robust transcription by proximal long noncoding RNAs located in nuclear compartments. Nat. Genet. 51:1138–50
    [Google Scholar]
  77. 77. 
    Quintin J, Saeed S, Martens JHA, Giamarellos-Bourboulis EJ, Ifrim DC et al. 2012. Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes. Cell Host Microbe 12:2223–32
    [Google Scholar]
  78. 78. 
    Kleinnijenhuis J, Quintin J, Preijers F, Joosten LAB, Ifrim DC et al. 2012. Bacille Calmette-Guérin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes. PNAS 109:4317537–42
    [Google Scholar]
  79. 79. 
    Kaufmann E, Sanz J, Dunn JL, Khan N, Mendonça LE et al. 2018. BCG educates hematopoietic stem cells to generate protective innate immunity against tuberculosis. Cell 172:1–2176–90.e19
    [Google Scholar]
  80. 80. 
    Mitroulis I, Ruppova K, Wang B, Chen LS, Grzybek M et al. 2018. Modulation of myelopoiesis progenitors is an integral component of trained immunity. Cell 172:1–2147–61.e12
    [Google Scholar]
  81. 81. 
    Cirovic B, de Bree LCJ, Groh L, Blok BA, Chan J et al. 2020. BCG vaccination in humans elicits trained immunity via the hematopoietic progenitor compartment. Cell Host Microbe 28:2322–34.e5
    [Google Scholar]
  82. 82. 
    de Laval B, Maurizio J, Kandalla PK, Brisou G, Simonnet L et al. 2020. C/EBPβ-dependent epigenetic memory induces trained immunity in hematopoietic stem cells. Cell Stem Cell 26:5657–74.e8
    [Google Scholar]
  83. 83. 
    Cheng SC, Quintin J, Cramer RA, Shepardson KM, Saeed S et al. 2014. MTOR- and HIF-1α-mediated aerobic glycolysis as metabolic basis for trained immunity. Science 345:62041250684
    [Google Scholar]
  84. 84. 
    Arts RJW, Novakovic B, ter Horst R, Carvalho A, Bekkering S et al. 2016. Glutaminolysis and fumarate accumulation integrate immunometabolic and epigenetic programs in trained immunity. Cell Metab 24:6807–19
    [Google Scholar]
  85. 85. 
    Fan H, Cook JA 2004. Molecular mechanism of endotoxin tolerance. J. Endotoxin Res. 10:271–84
    [Google Scholar]
  86. 86. 
    West MA, Heagy W. 2002. Endotoxin tolerance: A review. Crit. Care Med. 30:1 SupplS64–73
    [Google Scholar]
  87. 87. 
    DiNardo AR, Netea MG, Musher DM. 2021. Postinfectious epigenetic immune modifications—a double-edged sword. N. Engl. J. Med. 384:3261–70
    [Google Scholar]
  88. 88. 
    Novakovic B, Habibi E, Wang SY, Arts RJW, Davar R et al. 2016. β-Glucan reverses the epigenetic state of LPS-induced immunological tolerance. Cell 167:51354–68.e14
    [Google Scholar]
  89. 89. 
    Wei G, Wei L, Zhu J, Zang C, Hu-Li J et al. 2009. Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 30:1155–67
    [Google Scholar]
  90. 90. 
    Hawkins RD, Larjo A, Tripathi SK, Wagner U, Luu Y et al. 2013. Global chromatin state analysis reveals lineage-specific enhancers during the initiation of human T helper 1 and T helper 2 cell polarization. Immunity 38:61271–84
    [Google Scholar]
  91. 91. 
    Vahedi G, Takahashi H, Nakayamada S, Sun HW, Sartorelli V et al. 2012. STATs shape the active enhancer landscape of T cell populations. Cell 151:5981–93
    [Google Scholar]
  92. 92. 
    Dong C. 2021. Cytokine regulation and function in T cells. Annu. Rev. Immunol. 39:51–76
    [Google Scholar]
  93. 93. 
    Bando JK, Gilfillan S, Di Luccia B, Fachi JL, Sécca C et al. 2020. ILC2s are the predominant source of intestinal ILC-derived IL-10. J. Exp. Med. 217:2e20191520
    [Google Scholar]
  94. 94. 
    Vivier E, Artis D, Colonna M, Diefenbach A, Di Santo JP et al. 2018. Innate lymphoid cells: 10 years on. Cell 174:51054–66
    [Google Scholar]
  95. 95. 
    Shih HY, Sciumè G, Mikami Y, Guo L, Sun HW et al. 2016. Developmental acquisition of regulomes underlies innate lymphoid cell functionality. Cell 165:51120–33
    [Google Scholar]
  96. 96. 
    Bielecki P, Riesenfeld SJ, Hütter JC, Torlai Triglia E, Kowalczyk MS et al. 2021. Skin-resident innate lymphoid cells converge on a pathogenic effector state. Nature 592:7852128–32
    [Google Scholar]
  97. 97. 
    Tortola L, Jacobs A, Pohlmeier L, Obermair FJ, Ampenberger F et al. 2020. High-dimensional T helper cell profiling reveals a broad diversity of stably committed effector states and uncovers interlineage relationships. Immunity 53:3597–613.e6
    [Google Scholar]
  98. 98. 
    Harbour SN, Maynard CL, Zindl CL, Schoeb TR, Weaver CT. 2015. Th17 cells give rise to Th1 cells that are required for the pathogenesis of colitis. PNAS 112:227061–66
    [Google Scholar]
  99. 99. 
    Lee YK, Turner H, Maynard CL, Oliver JR, Chen D et al. 2009. Late developmental plasticity in the T helper 17 lineage. Immunity 30:192–107
    [Google Scholar]
  100. 100. 
    Hirota K, Duarte JH, Veldhoen M, Hornsby E, Li Y et al. 2011. Fate mapping of IL-17-producing T cells in inflammatory responses. Nat. Immunol. 12:3255–63
    [Google Scholar]
  101. 101. 
    Nussbaum K, Burkhard SH, Ohs I, Mair F, Klose CSN et al. 2017. Tissue microenvironment dictates the fate and tumor-suppressive function of type 3 ILCs. J. Exp. Med. 214:82331–47
    [Google Scholar]
  102. 102. 
    Mazzoni A, Maggi L, Liotta F, Cosmi L, Annunziato F 2019. Biological and clinical significance of T helper 17 cell plasticity. Immunology 158:4287–95
    [Google Scholar]
  103. 103. 
    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 38:4769–81
    [Google Scholar]
  104. 104. 
    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. 14:3221–29
    [Google Scholar]
  105. 105. 
    Uhlig HH, McKenzie BS, Hue S, Thompson C, Joyce-Shaikh B et al. 2006. Differential activity of IL-12 and IL-23 in mucosal and systemic innate immune pathology. Immunity 25:2309–18
    [Google Scholar]
  106. 106. 
    Muraoka WT, Korchagina AA, Xia Q, Shein SA, Jing X et al. 2021. Campylobacter infection promotes IFNγ-dependent intestinal pathology via ILC3 to ILC1 conversion. Mucosal Immunol 14:3703–16
    [Google Scholar]
  107. 107. 
    Vahedi G, Kanno Y, Furumoto Y, Jiang K, Parker SCJ et al. 2015. Super-enhancers delineate disease-associated regulatory nodes in T cells. Nature 520:7548558–62
    [Google Scholar]
  108. 108. 
    Cella M, Gamini R, Sécca C, Collins PL, Zhao S et al. 2019. Subsets of ILC3−ILC1-like cells generate a diversity spectrum of innate lymphoid cells in human mucosal tissues. Nat. Immunol. 20:8980–91 Erratum. 2019. Nat. Immunol. 20(10):1405
    [Google Scholar]
  109. 109. 
    Mazzurana L, Forkel M, Rao A, Van Acker A, Kokkinou E et al. 2019. Suppression of Aiolos and Ikaros expression by lenalidomide reduces human ILC3−ILC1/NK cell transdifferentiation. Eur. J. Immunol. 49:91344–55
    [Google Scholar]
  110. 110. 
    Chea S, Perchet T, Petit M, Verrier T, Guy-Grand D et al. 2016. Notch signaling in group 3 innate lymphoid cells modulates their plasticity. Sci. Signal. 9:426ra45
    [Google Scholar]
  111. 111. 
    Pokrovskii M, Hall JA, Ochayon DE, Yi R, Chaimowitz NS et al. 2019. Characterization of transcriptional regulatory networks that promote and restrict identities and functions of intestinal innate lymphoid cells. Immunity 51:1185–97.e6
    [Google Scholar]
  112. 112. 
    Parker ME, Barrera A, Wheaton JD, Zuberbuehler MK, Allan DSJ et al. 2020. c-Maf regulates the plasticity of group 3 innate lymphoid cells by restraining the type 1 program. J. Exp. Med. 217:1e20191030
    [Google Scholar]
  113. 113. 
    Tizian C, Lahmann A, Hölsken O, Cosovanu C, Kofoed-Branzk M et al. 2020. c-Maf restrains T-bet-driven programming of CCR6-negative group 3 innate lymphoid cells. eLife 9:e52549 Erratum. 2020. eLife 9:e56774
    [Google Scholar]
  114. 114. 
    Xu J, Yang Y, Qiu G, Lal G, Wu Z et al. 2009. c-Maf regulates IL-10 expression during Th17 polarization. J. Immunol. 182:106226–36
    [Google Scholar]
  115. 115. 
    Meyer zu Horste G, Wu C, Wang C, Cong L, Pawlak M et al. 2016. RBPJ controls development of pathogenic Th17 cells by regulating IL-23 receptor expression. Cell Rep 16:2392–404
    [Google Scholar]
  116. 116. 
    Russ BE, Olshanksy M, Smallwood HS, Li J, Denton AE et al. 2014. Distinct epigenetic signatures delineate transcriptional programs during virus-specific CD8+ T cell differentiation. Immunity 41:5853–65
    [Google Scholar]
  117. 117. 
    Yukawa M, Jagannathan S, Vallabh S, Kartashov AV, Chen X et al. 2020. AP-1 activity induced by co-stimulation is required for chromatin opening during T cell activation. J. Exp. Med. 217:1e20182009
    [Google Scholar]
  118. 118. 
    Bevington SL, Cauchy P, Piper J, Bertrand E, Lalli N et al. 2016. Inducible chromatin priming is associated with the establishment of immunological memory in T cells. EMBO J 35:5515–35
    [Google Scholar]
  119. 119. 
    van der Veeken J, Zhong Y, Sharma R, Mazutis L, Dao P et al. 2019. Natural genetic variation reveals key features of epigenetic and transcriptional memory in virus-specific CD8 T cells. Immunity 50:51202–17.e7
    [Google Scholar]
  120. 120. 
    Istaces N, Splittgerber M, Lima Silva V, Nguyen M, Thomas S et al. 2019. EOMES interacts with RUNX3 and BRG1 to promote innate memory cell formation through epigenetic reprogramming. Nat. Commun. 10:13306
    [Google Scholar]
  121. 121. 
    Levanon D, Negreanu V, Lotem J, Bone KR, Brenner O et al. 2014. Transcription factor Runx3 regulates interleukin-15-dependent natural killer cell activation. Mol. Cell. Biol. 34:61158–69
    [Google Scholar]
  122. 122. 
    Wang D, Diao H, Getzler AJ, Rogal W, Frederick MA et al. 2018. The transcription factor Runx3 establishes chromatin accessibility of cis-regulatory landscapes that drive memory cytotoxic T lymphocyte formation. Immunity 48:4659–74.e6
    [Google Scholar]
  123. 123. 
    Holmes TD, Pandey RV, Helm EY, Schlums H, Han H et al. 2021. The transcription factor Bcl11b promotes both canonical and adaptive NK cell differentiation. Sci. Immunol. 6:57eabc9801
    [Google Scholar]
  124. 124. 
    McFarland AP, Yalin A, Wang SY, Cortez VS, Landsberger T et al. 2021. Multi-tissue single-cell analysis deconstructs the complex programs of mouse natural killer and type 1 innate lymphoid cells in tissues and circulation. Immunity 54:61320–37
    [Google Scholar]
  125. 125. 
    Zook EC, Li ZY, Xu Y, de Pooter RF, Verykokakis M et al. 2018. Transcription factor ID2 prevents E proteins from enforcing a naïve T lymphocyte gene program during NK cell development. Sci. Immunol. 3:22eaao2139
    [Google Scholar]
  126. 126. 
    Wu JQ, Seay M, Schulz VP, Hariharan M, Tuck D et al. 2012. Tcf7 is an important regulator of the switch of self-renewal and differentiation in a multipotential hematopoietic cell line. PLOS Genet 8:3e1002565
    [Google Scholar]
  127. 127. 
    Lin WHW, Nish SA, Yen B, Chen YH, Adams WC et al. 2016. CD8+ T lymphocyte self-renewal during effector cell determination. Cell Rep 17:71773–82
    [Google Scholar]
  128. 128. 
    Li ZY, Morman RE, Hegermiller E, Sun M, Bartom ET et al. 2021. The transcriptional repressor ID2 supports natural killer cell maturation by controlling TCF1 amplitude. J. Exp. Med. 218:6e20202032
    [Google Scholar]
  129. 129. 
    Yu S, Zhou X, Steinke FC, Liu C, Chen SC et al. 2012. The TCF-1 and LEF-1 transcription factors have cooperative and opposing roles in T cell development and malignancy. Immunity 37:5813–26
    [Google Scholar]
  130. 130. 
    Xing S, Li F, Zeng Z, Zhao Y, Yu S et al. 2016. Tcf1 and Lef1 transcription factors establish CD8+ T cell identity through intrinsic HDAC activity. Nat. Immunol. 17:6695–703
    [Google Scholar]
  131. 131. 
    Wu T, Shin HM, Moseman EA, Ji Y, Huang B et al. 2015. TCF1 is required for the T follicular helper cell response to viral infection. Cell Rep 12:122099–110
    [Google Scholar]
  132. 132. 
    Omilusik KD, Best JA, Yu B, Goossens S, Weidemann A et al. 2015. Transcriptional repressor ZEB2 promotes terminal differentiation of CD8+ effector and memory T cell populations during infection. J. Exp. Med. 212:122027–39
    [Google Scholar]
  133. 133. 
    Pace L, Goudot C, Zueva E, Gueguen P, Burgdorf N et al. 2018. The epigenetic control of stemness in CD8+ T cell fate commitment. Science 359:6372177–86
    [Google Scholar]
  134. 134. 
    Danilo M, Chennupati V, Silva JG, Siegert S, Held W 2018. Suppression of Tcf1 by inflammatory cytokines facilitates effector CD8 T cell differentiation. Cell Rep 22:82107–17
    [Google Scholar]
  135. 135. 
    Shao P, Li F, Wang J, Chen X, Liu C, Xue H-H 2019. Cutting edge: Tcf1 instructs T follicular helper cell differentiation by repressing Blimp1 in response to acute viral infection. J. Immunol. 203:4801–6
    [Google Scholar]
  136. 136. 
    Sun JC, Beilke JN, Lanier LL. 2009. Adaptive immune features of natural killer cells. Nature 457:7229557–61
    [Google Scholar]
  137. 137. 
    Lopez-Vergès S, Milush JM, Schwartz BS, Pando MJ, Jarjoura J et al. 2011. Expansion of a unique CD57+NKG2Chi natural killer cell subset during acute human cytomegalovirus infection. PNAS 108:3614725–32
    [Google Scholar]
  138. 138. 
    Wiedemann GM, Santosa EK, Grassmann S, Sheppard S, Le Luduec JB et al. 2021. Deconvoluting global cytokine signaling networks in natural killer cells. Nat. Immunol. 22:5627–38
    [Google Scholar]
  139. 139. 
    Sciumè G, Mikami Y, Jankovic D, Nagashima H, Villarino AV et al. 2020. Rapid enhancer remodeling and transcription factor repurposing enable high magnitude gene induction upon acute activation of NK cells. Immunity 53:4745–58.e4
    [Google Scholar]
  140. 140. 
    Lau CM, Adams NM, Geary CD, Weizman O, Rapp M et al. 2018. Epigenetic control of innate and adaptive immune memory. Nat. Immunol. 19:9963–72
    [Google Scholar]
  141. 141. 
    Sun JC, Madera S, Bezman NA, Beilke JN, Kaplan MH, Lanier LL. 2012. Proinflammatory cytokine signaling required for the generation of natural killer cell memory. J. Exp. Med. 209:5947–54
    [Google Scholar]
  142. 142. 
    Beaulieu AM, Zawislak CL, Nakayama T, Sun JC 2014. The transcription factor Zbtb32 controls the proliferative burst of virus-specific natural killer cells responding to infection. Nat. Immunol. 15:6546–53
    [Google Scholar]
  143. 143. 
    Rapp M, Lau CM, Adams NM, Weizman O, O'Sullivan TE et al. 2017. Core-binding factor and Runx transcription factors promote adaptive natural killer cell responses. Sci. Immunol. 2:18eaan3796
    [Google Scholar]
  144. 144. 
    Adams NM, Lau CM, Fan X, Rapp M, Geary CD et al. 2018. Transcription factor IRF8 orchestrates the adaptive natural killer cell response. Immunity 48:61172–82.e6
    [Google Scholar]
  145. 145. 
    Intlekofer AM, Takemoto N, Wherry EJ, Longworth SA, Northrup JT et al. 2005. Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat. Immunol. 6:121236–44
    [Google Scholar]
  146. 146. 
    Shin HM, Kapoor VN, Kim G, Li P, Kim HR et al. 2017. Transient expression of ZBTB32 in anti-viral CD8+ T cells limits the magnitude of the effector response and the generation of memory. PLOS Pathog 13:8e1006544
    [Google Scholar]
  147. 147. 
    Colonna M. 2018. Innate lymphoid cells: diversity, plasticity, and unique functions in immunity. Immunity 48:61104–17
    [Google Scholar]
  148. 148. 
    Verbist KC, Cole CJ, Field MB, Klonowski KD. 2011. A role for IL-15 in the migration of effector CD8 T cells to the lung airways following influenza infection. J. Immunol. 186:1174–82
    [Google Scholar]
  149. 149. 
    Mackay LK, Minnich M, Kragten NAM, Liao Y, Nota B et al. 2016. Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes. Science 352:6284459–63
    [Google Scholar]
  150. 150. 
    Behr FM, Kragten NAM, Wesselink TH, Nota B, Van Lier RAW et al. 2019. Blimp-1 rather than Hobit drives the formation of tissue-resident memory CD8+ T cells in the lungs. Front. Immunol. 10:400
    [Google Scholar]
  151. 151. 
    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 552:7684253–57
    [Google Scholar]
  152. 152. 
    Youngblood B, Hale JS, Kissick HT, Ahn E, Xu X et al. 2017. Effector CD8 T cells dedifferentiate into long-lived memory cells. Nature 552:7685404–9
    [Google Scholar]
  153. 153. 
    Akondy RS, Fitch M, Edupuganti S, Yang S, Kissick HT et al. 2017. Origin and differentiation of human memory CD8 T cells after vaccination. Nature 552:7685362–67
    [Google Scholar]
  154. 154. 
    Abdel-Hakeem MS, Manne S, Beltra J-C, Stelekati E, Chen Z et al. 2021. Epigenetic scarring of exhausted T cells hinders memory differentiation upon eliminating chronic antigenic stimulation. Nat. Immunol. 22:81008–19
    [Google Scholar]
  155. 155. 
    Ghoneim HE, Fan Y, Moustaki A, Abdelsamed HA, Dash P et al. 2017. De novo epigenetic programs inhibit PD-1 blockade-mediated T cell rejuvenation. Cell 170:1142–57.e19
    [Google Scholar]
  156. 156. 
    Scott-Browne JP, López-Moyado IF, Trifari S, Wong V, Chavez L et al. 2016. Dynamic changes in chromatin accessibility occur in CD8+ T cells responding to viral infection. Immunity 45:61327–40
    [Google Scholar]
  157. 157. 
    Mognol GP, Spreafico R, Wong V, Scott-Browne JP, Togher S et al. 2017. Exhaustion-associated regulatory regions in CD8+ tumor-infiltrating T cells. PNAS 114:13E2776–85
    [Google Scholar]
  158. 158. 
    Doering TA, Crawford A, Angelosanto JM, Paley MA, Ziegler CG, Wherry EJ. 2012. Network analysis reveals centrally connected genes and pathways involved in CD8+ T cell exhaustion versus memory. Immunity 37:61130–44
    [Google Scholar]
  159. 159. 
    Sen DR, Kaminski J, Barnitz RA, Kurachi M, Gerdemann U et al. 2016. The epigenetic landscape of T cell exhaustion. Science 354:63161165–69
    [Google Scholar]
  160. 160. 
    Pauken KE, Sammons MA, Odorizzi PM, Manne S, Godec J et al. 2016. Epigenetic stability of exhausted T cells limits durability of reinvigoration by PD-1 blockade. Science 354:1160–65
    [Google Scholar]
  161. 161. 
    Beltra JC, Manne S, Abdel-Hakeem MS, Kurachi M, Giles JR et al. 2020. Developmental relationships of four exhausted CD8+ T cell subsets reveals underlying transcriptional and epigenetic landscape control mechanisms. Immunity 52:5825–41.e8
    [Google Scholar]
  162. 162. 
    Hudson WH, Gensheimer J, Hashimoto M, Wieland A, Valanparambil RM et al. 2019. Proliferating transitory T cells with an effector-like transcriptional signature emerge from PD-1+ stem-like CD8+ T cells during chronic infection. Immunity 51:1043–58.e4
    [Google Scholar]
  163. 163. 
    Chen Y, Zander RA, Wu X, Schauder DM, Kasmani MY et al. 2021. BATF regulates progenitor to cytolytic effector CD8+ T cell transition during chronic viral infection. Nat. Immunol. 22:996–1007
    [Google Scholar]
  164. 164. 
    Page N, Lemeille S, Vincenti I, Klimek B, Mariotte A et al. 2021. Persistence of self-reactive CD8+ T cells in the CNS requires TOX-dependent chromatin remodeling. Nat. Commun. 12:11009
    [Google Scholar]
  165. 165. 
    Paley MA, Kroy DC, Odorizzi PM, Johnnidis JB, Dolfi DV et al. 2012. Progenitor and terminal subsets of CD8+ T cells cooperate to contain chronic viral infection. Science 338:61111220–25
    [Google Scholar]
  166. 166. 
    Zhou X, Yu S, Zhao DM, Harty JT, Badovinac VP, Xue HH. 2010. Differentiation and persistence of memory CD8+ T cells depend on T cell factor 1. Immunity 33:2229–40
    [Google Scholar]
  167. 167. 
    Pearce EL, Mullen AC, Martins GA, Krawczyk CM, Hutchins AS et al. 2003. Control of effector CD8+ T cell function by the transcription factor Eomesodermin. Science 302:56471041–43
    [Google Scholar]
  168. 168. 
    Joshi NS, Cui W, Chandele A, Lee HK, Urso DR et al. 2007. Inflammation directs memory precursor and short-lived effector CD8+ T cell fates via the graded expression of T-bet transcription factor. Immunity 27:2281–95
    [Google Scholar]
  169. 169. 
    Mann TH, Kaech SM. 2019. Tick-TOX, it's time for T cell exhaustion. Nat. Immunol. 20:91092–94
    [Google Scholar]
  170. 170. 
    Man K, Gabriel SS, Liao Y, Gloury R, Preston S et al. 2017. Transcription factor IRF4 promotes CD8+ T cell exhaustion and limits the development of memory-like T cells during chronic infection. Immunity 47:61129–41.e5
    [Google Scholar]
  171. 171. 
    Quigley M, Pereyra F, Nilsson B, Porichis F, Fonseca C et al. 2010. Transcriptional analysis of HIV-specific CD8+ T cells shows that PD-1 inhibits T cell function by upregulating BATF. Nat. Med. 16:101147–51
    [Google Scholar]
  172. 172. 
    Utzschneider DT, Charmoy M, Chennupati V, Pousse L, Ferreira DP et al. 2016. T cell factor 1-expressing memory-like CD8+ T cells sustain the immune response to chronic viral infections. Immunity 45:2415–27
    [Google Scholar]
  173. 173. 
    Im SJ, Hashimoto M, Gerner MY, Lee J, Kissick HT et al. 2016. Defining CD8+ T cells that provide the proliferative burst after PD-1 therapy. Nature 537:7620417–21
    [Google Scholar]
  174. 174. 
    Singer M, Wang C, Cong L, Marjanovic ND, Kowalczyk MS et al. 2016. A distinct gene module for dysfunction uncoupled from activation in tumor-infiltrating T cells. Cell 166:61500–11.e9
    [Google Scholar]
  175. 175. 
    Scott AC, Dündar F, Zumbo P, Chandran SS, Klebanoff CA et al. 2019. TOX is a critical regulator of tumour-specific T cell differentiation. Nature 571:7764270–74
    [Google Scholar]
  176. 176. 
    Alfei F, Kanev K, Hofmann M, Wu M, Ghoneim HE et al. 2019. TOX reinforces the phenotype and longevity of exhausted T cells in chronic viral infection. Nature 571:7764265–69
    [Google Scholar]
  177. 177. 
    Khan O, Giles JR, McDonald S, Manne S, Ngiow SF et al. 2019. TOX transcriptionally and epigenetically programs CD8+ T cell exhaustion. Nature 571:7764211–18
    [Google Scholar]
  178. 178. 
    Chen J, López-Moyado IF, Seo H, Lio CWJ, Hempleman LJ et al. 2019. NR4A transcription factors limit CAR T cell function in solid tumours. Nature 567:7749530–34
    [Google Scholar]
  179. 179. 
    Seo H, Chen J, González-Avalos E, Samaniego-Castruita D, Das A et al. 2019. TOX and TOX2 transcription factors cooperate with NR4A transcription factors to impose CD8+ T cell exhaustion. PNAS 116:2512410–15
    [Google Scholar]
  180. 180. 
    Yao C, Lou G, Sun HW, Zhu Z, Sun Y et al. 2021. BACH2 enforces the transcriptional and epigenetic programs of stem-like CD8+ T cells. Nat. Immunol. 22:3370–80
    [Google Scholar]
  181. 181. 
    Merino A, Zhang B, Dougherty P, Luo X, Wang J et al. 2019. Chronic stimulation drives human NK cell dysfunction and epigenetic reprograming. J. Clin. Investig. 129:93770–85
    [Google Scholar]
  182. 182. 
    Ebihara T, Taniuchi I. 2019. Exhausted-like group 2 innate lymphoid cells in chronic allergic inflammation. Trends Immunol 40:121095–104
    [Google Scholar]
  183. 183. 
    Platonova S, Cherfils-Vicini J, Damotte D, Crozet L, Vieillard V et al. 2011. Profound coordinated alterations of intratumoral NK cell phenotype and function in lung carcinoma. Cancer Res 71:165412–22
    [Google Scholar]
  184. 184. 
    Youngblood B, Oestreich KJ, Ha SJ, Duraiswamy J, Akondy RS et al. 2011. Chronic virus infection enforces demethylation of the locus that encodes PD-1 in antigen-specific CD8+ T cells. Immunity 35:3400–12
    [Google Scholar]
  185. 185. 
    Kiner E, Willie E, Vijaykumar B, Chowdhary K, Schmutz H et al. 2021. Gut CD4+ T cell phenotypes are a continuum molded by microbes, not by TH archetypes. Nat. Immunol. 22:2216–28
    [Google Scholar]
  186. 186. 
    Tibbitt CA, Stark JM, Martens L, Ma J, Mold JE et al. 2019. Single-cell RNA sequencing of the T helper cell response to house dust mites defines a distinct gene expression signature in airway Th2 cells. Immunity 51:1169–84.e5
    [Google Scholar]
  187. 187. 
    Mimitou EP, Cheng A, Montalbano A, Hao S, Stoeckius M et al. 2019. Multiplexed detection of proteins, transcriptomes, clonotypes and CRISPR perturbations in single cells. Nat. Methods 16:5409–12
    [Google Scholar]
  188. 188. 
    Efremova M, Vento-Tormo R, Park JE, Teichmann SA, James KR. 2020. Immunology in the era of single-cell technologies. Annu. Rev. Immunol. 38:727–57
    [Google Scholar]
  189. 189. 
    Mezger A, Klemm S, Mann I, Brower K, Mir A et al. 2018. High-throughput chromatin accessibility profiling at single-cell resolution. Nat. Commun. 9:13647
    [Google Scholar]
  190. 190. 
    Kaya-Okur HS, Wu SJ, Codomo CA, Pledger ES, Bryson TD et al. 2019. CUT&Tag for efficient epigenomic profiling of small samples and single cells. Nat. Commun. 10:11930
    [Google Scholar]
  191. 191. 
    Pierce SE, Granja JM, Greenleaf WJ. 2021. High-throughput single-cell chromatin accessibility CRISPR screens enable unbiased identification of regulatory networks in cancer. Nat. Commun. 12:12969
    [Google Scholar]
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