Epigenetic control of innate and adaptive immune memory

Nature Immunology

Volumn 19, Issue 9, 2018, Pages 963-972

  Lau, Colleen M ^a   Adams, Nicholas M ^a   Geary, Clair D ^a   Weizman, Orr El ^a   Rapp, Moritz ^a   Pritykin, Yuri ^a   Leslie, Christina S ^a   Sun, Joseph C ^a,b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; ALPHA INTERFERON; CISH PROTEIN; DNA METHYLTRANSFERASE 3A; GAMMA INTERFERON; GAMMA INTERFERON RECEPTOR 1; IFNG PROTEIN; INTERFERON REGULATORY FACTOR 9; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 18; INTERLEUKIN 2; KLRG1 PROTEIN; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN; STAT PROTEIN; STAT1 PROTEIN; STAT2 PROTEIN; STAT4 PROTEIN; STAT6 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR T BET; UNCLASSIFIED DRUG; ZBTB32 PROTEIN;

ADAPTIVE IMMUNITY; ARTICLE; CD8+ T LYMPHOCYTE; CELL FATE; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; ENHANCER REGION; EPIGENETICS; GENE EXPRESSION; GENE LOCUS; GENETIC REGULATION; IMMUNOLOGICAL MEMORY; INFECTION; INNATE IMMUNITY; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RNA SEQUENCE; SIGNAL TRANSDUCTION; ANIMAL; ANTIGEN MEDIATED CLONAL SELECTION; C57BL MOUSE; CELL CULTURE; GENE EXPRESSION PROFILING; GENETIC EPIGENESIS; GENETICS; HERPES VIRUS INFECTION; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MUROMEGALOVIRUS; PHYSIOLOGY;

ADAPTIVE IMMUNITY; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CHROMATIN; CLONAL SELECTION, ANTIGEN-MEDIATED; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; HERPESVIRIDAE INFECTIONS; IMMUNITY, INNATE; IMMUNOLOGIC MEMORY; KILLER CELLS, NATURAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUROMEGALOVIRUS; STAT1 TRANSCRIPTION FACTOR; STAT4 TRANSCRIPTION FACTOR;

EID: 85048593874     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/s41590-018-0176-1     Document Type: Article

References (60)

1. + T cells. Nat. Rev. Immunol. 11, 645–657 (2011).
2. Vivier, E. et al. Innate or adaptive immunity? The example of natural killer cells. Science 331, 44–49 (2011).
3. Arase, H., Mocarski, E. S., Campbell, A. E., Hill, A. B. & Lanier, L. L. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 296, 1323–1326 (2002).
4. Smith, H. R. et al. Recognition of a virus-encoded ligand by a natural killer cell activation receptor. Proc. Natl Acad. Sci. USA 99, 8826–8831 (2002).
5. Dokun, A. O. et al. Specific and nonspecific NK cell activation during virus infection. Nat. Immunol. 2, 951–956 (2001).
6. Daniels, K. A. et al. Murine cytomegalovirus is regulated by a discrete subset of natural killer cells reactive with monoclonal antibody to Ly49H. J. Exp. Med. 194, 29–44 (2001).
7. Sun, J. C., Beilke, J. N. & Lanier, L. L. Adaptive immune features of natural killer cells. Nature 457, 557–561 (2009).
8. Bezman, N. A. et al. Molecular definition of the identity and activation of natural killer cells. Nat. Immunol. 13, 1000–1009 (2012).
9. Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y. & Greenleaf, W. J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10, 1213–1218 (2013).
10. Kaech, S. M., Hemby, S., Kersh, E. & Ahmed, R. Molecular and functional profiling of memory CD8 T cell differentiation. Cell 111, 837–851 (2002).
11. Madera, S. et al. Type I IFN promotes NK cell expansion during viral infection by protecting NK cells against fratricide. J. Exp. Med. 213, 225–233 (2016).
12. Tassi, I. et al. NK cell-activating receptors require PKC-theta for sustained signaling, transcriptional activation, and IFN-gamma secretion. Blood 112, 4109–4116 (2008).
13. Brand, A. et al. LDHA-associated lactic acid production blunts tumor immunosurveillance by T and NK Cells. Cell Metab. 24, 657–671 (2016).
14. Freund-Brown, J. et al. Cutting edge: murine NK cells degranulate and retain cytotoxic function without store-operated calcium entry. J. Immunol. 199, 1973–1978 (2017).
15. Andrews, D. M., Scalzo, A. A., Yokoyama, W. M., Smyth, M. J. & Degli-Esposti, M. A. Functional interactions between dendritic cells and NK cells during viral infection. Nat. Immunol. 4, 175–181 (2003).
16. Sun, J. C. et al. Proinflammatory cytokine signaling required for the generation of natural killer cell memory. J. Exp. Med. 209, 947–954 (2012).
17. García-Sastre, A. & Biron, C. A. Type 1 interferons and the virus-host relationship: a lesson in détente. Science 312, 879–882 (2006).
18. Rapp, M. et al. Core-binding factor β and Runx transcription factors promote adaptive natural killer cell responses. Sci. Immunol. 2, eaan3796 (2017).
19. Nguyen, K. B. et al. Interferon alpha/beta-mediated inhibition and promotion of interferon gamma: STAT1 resolves a paradox. Nat. Immunol. 1, 70–76 (2000).
20. Gil, M. P. et al. Regulating type 1 IFN effects in CD8 T cells during viral infections: changing STAT4 and STAT1 expression for function. Blood 120, 3718–3728 (2012).
21. Madera, S. & Sun, J. C. Cutting edge: stage-specific requirement of IL-18 for antiviral NK cell expansion. J. Immunol. 194, 1408–1412 (2015).
22. Pauken, K. E. et al. Epigenetic stability of exhausted T cells limits durability of reinvigoration by PD-1 blockade. Science 354, 1160–1165 (2016).
23. Sen, D. R. et al. The epigenetic landscape of T cell exhaustion. Science 354, 1165–1169 (2016).
24. + T cells responding to viral infection. Immunity 45, 1327–1340 (2016).
25. + T cell differentiation. Nat. Immunol. 18, 573–582 (2017).
26. Ghoneim, H. E. et al. De novo epigenetic programs inhibit PD-1 blockade-mediated T cell rejuvenation. Cell 170, 142–157.e19 (2017).
27. Philip, M. et al. Chromatin states define tumour-specific T cell dysfunction and reprogramming. Nature 545, 452–456 (2017).
28. Zhou, X. et al. Differentiation and persistence of memory CD8(+) T cells depend on T cell factor 1. Immunity 33, 229–240 (2010).
29. Dominguez, C. X. et al. The transcription factors ZEB2 and T-bet cooperate to program cytotoxic T cell terminal differentiation in response to LCMV viral infection. J. Exp. Med. 212, 2041–2056 (2015).
30. Omilusik, K. D. et al. Transcriptional repressor ZEB2 promotes terminal differentiation of CD8+ effector and memory T cell populations during infection. J. Exp. Med. 212, 2027–2039 (2015).
31. Roychoudhuri, R. et al. BACH2 regulates CD8(+) T cell differentiation by controlling access of AP-1 factors to enhancers. Nat. Immunol. 17, 851–860 (2016).
32. Smith-Garvin, J. E., Koretzky, G. A. & Jordan, M. S. T cell activation. Annu. Rev. Immunol. 27, 591–619 (2009).
33. González, A. J., Setty, M. & Leslie, C. S. Early enhancer establishment and regulatory locus complexity shape transcriptional programs in hematopoietic differentiation. Nat. Genet. 47, 1249–1259 (2015).
34. Shih, H. Y. et al. Developmental acquisition of regulomes underlies innate lymphoid cell functionality. Cell 165, 1120–1133 (2016).
35. Corces, M. R. et al. Lineage-specific and single-cell chromatin accessibility charts human hematopoiesis and leukemia evolution. Nat. Genet. 48, 1193–1203 (2016).
36. Weber, B. N. et al. A critical role for TCF-1 in T-lineage specification and differentiation. Nature 476, 63–68 (2011).
37. Germar, K. et al. T-cell factor 1 is a gatekeeper for T-cell specification in response to Notch signaling. Proc. Natl Acad. Sci. USA 108, 20060–20065 (2011).
38. Xing, S. et al. Tcf1 and Lef1 transcription factors establish CD8(+) T cell identity through intrinsic HDAC activity. Nat. Immunol. 17, 695–703 (2016).
39. Yang, Q. et al. TCF-1 upregulation identifies early innate lymphoid progenitors in the bone marrow. Nat. Immunol. 16, 1044–1050 (2015).
40. Jeevan-Raj, B. et al. The transcription factor Tcf1 contributes to normal NK cell development and function by limiting the expression of granzymes. Cell Rep. 20, 613–626 (2017).
41. Johnson, J. L. et al. Lineage-determining transcription factor TCF-1 initiates the epigenetic identity of T cells. Immunity 48, 243–257.e10 (2018).
42. O’Shea, J. J. et al. The JAK-STAT pathway: impact on human disease and therapeutic intervention. Annu. Rev. Med. 66, 311–328 (2015).
43. Villarino, A. V., Kanno, Y. & O’Shea, J. J. Mechanisms and consequences of Jak-STAT signaling in the immune system. Nat. Immunol. 18, 374–384 (2017).
44. Hartman, S. E. et al. Global changes in STAT target selection and transcription regulation upon interferon treatments. Genes Dev. 19, 2953–2968 (2005).
45. Kaplan, M. H., Sun, Y. L., Hoey, T. & Grusby, M. J. Impaired IL-12 responses and enhanced development of Th2 cells in Stat4-deficient mice. Nature 382, 174–177 (1996).
46. Meraz, M. A. et al. Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 84, 431–442 (1996).
47. Fodil-Cornu, N. et al. Ly49h-deficient C57BL/6 mice: a new mouse cytomegalovirus-susceptible model remains resistant to unrelated pathogens controlled by the NK gene complex. J. Immunol. 181, 6394–6405 (2008).
48. Zheng, Y. et al. Genome-wide analysis of Foxp3 target genes in developing and mature regulatory T cells. Nature 445, 936–940 (2007).
49. Beaulieu, A. M., Zawislak, C. L., Nakayama, T. & Sun, J. C. The transcription factor Zbtb32 controls the proliferative burst of virus-specific natural killer cells responding to infection. Nat. Immunol. 15, 546–553 (2014).
50. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
51. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
52. Lawrence, M. et al. Software for computing and annotating genomic ranges. PLOS Comput. Biol. 9, e1003118 (2013).
53. Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
54. Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
55. Li, Q. H., Brown, J. B., Huang, H. Y. & Bickel, P. J. Measuring reproducibility of high-throughput experiments. Ann. Appl. Stat. 5, 1752–1779 (2011).
56. Zhu, L. J. et al. ChIPpeakAnno: a Bioconductor package to annotate ChIP-seq and ChIP-chip data. BMC Bioinforma. 11, 237 (2010).
57. McLean, C. Y. et al. GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28, 495–501 (2010).
58. Bray, N. L., Pimentel, H., Melsted, P. & Pachter, L. Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34, 525–527 (2016).
59. Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576–589 (2010).
60. Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).