Multi-layered epigenetic mechanisms contribute to transcriptional memory in T lymphocytes

BMC Immunology

Volumn 16, Issue 1, 2015, Pages

  Dunn, Jennifer ^a   McCuaig, Robert ^a   Tu, Wen Juan ^a   Hardy, Kristine ^a   Rao, Sudha ^a  

^a UNIVERSITY OF CANBERRA   (Australia)

Author keywords

Epigenetics; Histone variant exchange; Memory T cells; PKC theta; Post translational modification; Transcriptional memory; Yeast

Indexed keywords

HISTONE; PROTEIN KINASE; TRANSCRIPTION FACTOR; CHROMATIN;

ADAPTIVE IMMUNITY; ANTIGEN SPECIFICITY; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; COMPARATIVE STUDY; EPIGENETICS; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; HEALTH CARE PLANNING; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; IMMUNOLOGICAL MEMORY; MEMORY T LYMPHOCYTE; NONHUMAN; PROMOTER REGION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TRANSCRIPTIONAL MEMORY; YEAST; ANIMAL; CHROMATIN; GENETIC EPIGENESIS; GENETICS; METABOLISM; T LYMPHOCYTE;

ANIMALS; CHROMATIN; EPIGENESIS, GENETIC; HISTONES; HUMANS; IMMUNOLOGIC MEMORY; T-LYMPHOCYTES; TRANSCRIPTION, GENETIC;

EID: 84928804690     PISSN: None     EISSN: 14712172     Source Type: Journal    
DOI: 10.1186/s12865-015-0089-9     Document Type: Article

References (87)

1. Zediak VP, Wherry EJ, Berger SL. The contribution of epigenetic memory to immunologic memory. Curr Opin Genet Dev. 2011;21(2):154-9.
2. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature. 1999;401(6754):708-12.
3. Weng NP, Araki Y, Subedi K. The molecular basis of the memory T cell response: differential gene expression and its epigenetic regulation. Nat Rev Immunol. 2012;12(4):306-15.
4. Hammarlund E, Lewis MW, Hansen SG, Strelow LI, Nelson JA, Sexton GJ, et al. Duration of antiviral immunity after smallpox vaccination. Nat Med. 2003;9(9):1131-7.
5. Kundu S, Horn PJ, Peterson CL. SWI/SNF is required for transcriptional memory at the yeast GAL gene cluster. Genes Dev. 2007;21(8):997-1004.
6. Goldberg AD, Allis CD, Bernstein E. Epigenetics: a landscape takes shape. Cell. 2007;128(4):635-8.
7. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet. 2003;33(Suppl):245-54.
8. Kouzarides T. Chromatin modifications and their functions. Cell. 2007;128(4):693-705.
9. Strahl BD, Allis CD. The language of covalent histone modifications. Nature. 2000;403:41-5.
10. Barksi A, Cuddapah S, Cui K, Ron TY, Schones DE, Wang Z, et al. High-resolution profiling of histone methylations in the human genome. Cell. 2007;129(4):823-37.
11. Northdrop JK, Thomas RM, Wells AD, Shen H. Epigenetic remodeling of the IL-2 and IFN-gamma loci in memory CD8 T cells is influenced by CD4 T cells. J Immunol. 2006;177(2):1062-9.
12. Northdrop JK, Wells AD, Shen H. Cutting edge: chromatin remodeling as a molecular basis for the enhanced functionality of memory CD8 T cells. J Immunol. 2008;181(2):865-8.
13. + T-cell response. Blood. 2006;108(10):3363-70.
14. H2 lymphocytes. Nat Immunol. 2002;4(1):78-86.
15. Yamashita M, Shinnakasu R, Nigo Y, Kimura M, Hasegawa A, Taniguchi M, et al. Interleukin (IL)-4-independent maintenance of histone modification of the IL-4 gene loci in memory Th2 cells. J Biol Chem. 2004;279(38):39454-64.
16. Araki Y, Wang Z, Zang C, Wood III WH, Schones D, Cui K, et al. Genome-wide analysis of histone methylation reveals chromatin state-based regulation of gene transcription and function of memory CD8+ T cells. Immunity. 2009;30(6):912-25.
17. Yamashita M, Hirahara K, Shinnakasu R, Hosokawa H, Norikane S, Kimura MY, et al. Crucial role of MLL for the maintenance of memory T helper type 2 cell responses. Immunity. 2006;24(5):611-22.
18. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell. 2006;125(2):315-26.
19. Cui K, Zang C, Roh TY, Schones DE, Childs RW, Peng W, et al. Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell Stem Cell. 2009;4(1):80-93.
20. Seit-Nebi A, Cheng W, Xu H, Han J. MLK4 has negative effect on TLR4 signaling. Cell Mol Immunol. 2012;9(1):27-33.
21. + T cell differentiation. Immunity. 2014;41(5):853-65.
22. Kornberg RD, Lorch Y. Interplay between chromatin structure and transcription. Curr Opin Cell Biol. 1995;7(3):371-5.
23. Luger K, Madar AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature. 1997;389:251-60.
24. Li B, Carey M, Workman JL. The role of chromatin during transcription. Cell. 2007;128:707-19.
25. Weber CM, Henikoff S. Histone variants: dynamic punctuation in transcription. Genes Dev. 2014;28(7):672-82.
26. Jin C, Felsenfeld G. Nucleosome stability mediated by histone variants H3.3 and H2A.Z. Genes Dev. 2007;21(12):1519-29.
27. Chen P, Zhao J, Wang Y, Wang M, Long H, Liang D, et al. H3.3 actively marks enhancers and primes gene transcription via opening higher-ordered chromatin. Genes Dev. 2013;27(19):2109-24.
28. Loyola A, Bonaldi T, Roche D, Imhof A, Almouzni G. PTMs on H3 variants before chromatin assembly potentiate their epigenetic state. Mol Cell. 2006;24(2):309-16.
29. Zhang H, Roberts DN, Cairns BR. Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss. Cell. 2005;123(2):219-31.
30. Raisner RM, Hartley PD, Meneghini MD, Bao MZ, Liu CL, Schreiber SL, et al. Histone variant H2A.Z marks the 5' ends of both active and inactive genes in euchromatin. Cell. 2005;123(2):233-48.
31. Sutcliffe EL, Parish IA, He YQ, Juelich T, Tierney ML, Rangasamy D, et al. Dyamic histone variant exchange accompanies gene induction in T cells. Mol Cell Biol. 2009;29(7):1972-86.
32. Gévry N, Chan HM, Laflamme L, Livingston DM, Gaudreau L. p21 transcription is regulated by differential localization of H2A.Z. Genes Dev. 2007;21(15):1869-81.
33. Morillo-Huesca M, Clemente-Ruiz M, Andújar E, Prado F. The SWR1 histone replacement complex causes genetic instability and genome-wide transcription misregulation in the absence of H2A.Z. PLoS One. 2010;5(8):e12143.
34. Jin C, Zang C, Wei G, Cui K, Peng W, Zhao K, et al. H3.3/H2A.Z double variant-containing nucleosomes mark 'nucleosome-free regions' of active promoters and other regulatory regions. Nat Genet. 2009;41(8):941-5.
35. Goldberg AD, Banaszynski LA, Noh KM, Lewis PW, Elsaesser SJ, Stadler S, et al. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell. 2010;140(5):678-91.
36. McKittrick E, Gafken PR, Ahmad K, Henikoff S. Histone H3.3 is enriched in covalent modifications associated with active transcription. Proc Natl Acad Sci U S A. 2004;101(6):1525-30.
37. Wong MM, Byun JS, Sacta M, Jin Q, Baek SJ, Gardner K. Promoter-bound p300 complexes facilitate post-mitotic transmission of transcriptional memory. PLoS One. 2014;9(6):e99989.
38. Chen P, Wang Y, Li G. Dynamics of histone variant H3.3 and its coregulation with H2A.Z at enhancers and promoters. Nucleus. 2014;5(1):21-7.
39. Santenard A, Ziegler-Birling C, Koch M, Tora L, Bannister AJ, Torres-Padilla ME. Heterochromatin formation in the mouse embryo requires critical residues of the histone variant H3.3. Nat Cell Biol. 2010;12(9):853-62.
40. Wong LH, McGhie JD, Sim M, Anderson MA, Ahn S, Hannan RD, et al. ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res. 2010:20(3):351-60.
41. Suto RK, Clarkson MJ, Tremethick DJ, Luger K. Crystal structure of a nucleosome core particle containing the variant histone H2A.Z. Nat Struct Biol. 2000;7(12):1121-4.
42. Bruce K, Myers FA, Mantouvalou E, Lefevre P, Greaves I, Bonifer C, et al. The replacement histone H2A.Z in a hyperacetylated form is feature of active genes in chicken. Nucleic Acids Res. 2005;33(17):5633-9.
43. Sarcinella E, Zuzarte PC, Lau PN, Draker R, Cheung P. Monoubiquitylation of H2A.Z distinguishes its association with euchromatin or facultative heterochromatin. Mol Cell Biol. 2007;27(18):6457-68.
44. Henikoff S. Labile H3.3+H2A.Z nucleosomes mark 'nucleosome-free regions'. Nat Genet. 2009;41(8):865-6.
45. Henikoff S, Henikoff JG, Sakai A, Loeb GB, Ahmad K. Genome-wide profiling of salt fractions maps physical properties of chromatin. Genome Res. 2009;19(3):460-9.
46. Braunschweig U, Hogan GJ, Pagie L, van Steensel B. Histone H1 binding is inhibited by histone variant H3.3. EMBO J. 2009;28(23):3635-45.
47. Ng RK, Gurdon JB. Epigenetic memory of an active gene state depends on histone H3.3 incorporation into chromatin in the absence of transcription. Nat Cell Biol. 2008;10(1):102-9.
48. Brickner DG, Cajigas I, Fondufe-Mittendorf Y, Ahmed S, Lee PC, Widom J, et al. H2A.Z-mediated localization of genes at the nuclear periphery confers epigenetic memory of previous transcriptional state. PLoS Biol. 2007;5(4):e81.
49. Chow CM, Georgiou A, Szutorisz H, Maia e Silva A, Pombo A, Barahona I, et al. Variant histone H3.3 marks promoters of transcriptionally active genes during mammalian cell division. EMBO Rep. 2005;6(4):354-60.
50. Zovik IB, Paulukaitis BS, Day JJ, Etikala DM, Sweatt JD. Histone H2A.Z subunit exchange controls consolidation of recent and remote memory. Nature. 2014;515(7528):582-6.
51. Nekrasov M, Soboleva TA, Jack C, Tremethick DJ. Histone variant selectivity at the transcription start site: H2A.Z or H2A.Lap1. Nucleus. 2013;4(6):431-8.
52. Soboleva TA, Nekrasov M, Ryan DP, Tremethick DJ. Histone variants at the transcription start-site. Trends Genet. 2014;30(5):199-209.
53. Luk E, Vu ND, Patteson K, Mizuguchi G, Wu WH, Ranjan A, et al. Chz1, a nuclear chaperone for histone H2AZ. Mol Cell. 2007;25(3):357-68.
54. Obri A, Ouararhni K, Papin C, Diebold ML, Padmanabhan K, Marek M, et al. ANP32E is a histone chaperone that removes H2A.Z from chromatin. Nature. 2014;505(7485):648-53.
55. Hong J, Feng H, Wang F, Ranjan A, Chen J, Jiang J, et al. The catalytic subunit of the SWR1 remodeler is a histone chaperone for the H2A.Z-H2B dimer. Mol Cell. 2014;53(3):498-505.
56. Keenan C, Long A, Kelleher D. Protein kinase C and T cell function. Biochim Biophys Acta. 1997;1358(2):113-26.
57. Baier G, Telford D, Giampa L, Coggeshall KM, Baier-Bitterlich G, Isakov N, et al. Molecular cloning and characterization of PKC theta, a novel member of the protein kinase C (PKC) gene family expressed predominantly in hematopoietic cells. J Biol Chem. 1993;268(7):4997-5004.
58. Sun Z, Arendt CW, Ellmeier W, Schaeffer EM, Sunshine MJ, Gandhi L, et al. PKC-theta is required for TCR-induced NF-kappaB activation in mature but not immature T lymphocytes. Nature. 2000;404(6776):402-7.
59. Anderson K, Fitzgerald M, Dupont M, Wang T, Paz N, Dorsch M, et al. Mice deficient in PKC theta demonstrate impaired in vivo T cell activation and protection from T cell-mediated inflammatory diseases. Autoimmunity. 2006;39(6):469-78.
60. Barouch-Bentov R, Lemmens EE, Hu J, Janssen EM, Droin NM, Song J, et al. Protein kinase C-theta is an early survival factor required for differentiation of effector CD8+ T cells. J Immunol. 2005;175(8):5126-34.
61. Sutcliffe EL, Bunting KL, He YQ, Li J, Phetsouphanh C, Seddiki N, et al. Chromatin-associated protein kinase C-Θ regulates an inducible gene expression program and microRNAs in human T lymphocytes. Mol Cell. 2011;41(6):704-19.
62. I controls demethylation at histone H3K4. Nature. 2010;464(7289):792-6.
63. Pascual-Ahuir A, Struhl K, Proft M. Genome-wide location analysis of the stress-activated MAP kinase Hog1 in yeast. Methods. 2006;40(3):272-8.
64. Pokholok DK, Zeitlinger J, Hannett NM, Reynolds DB, Young RA. Activated signal transduction kinases frequently occupy target genes. Science. 2006;313(5786):533-6.
65. Cui W, Liu Y, Weinstein JS, Craft J, Kaech SM. An interleukin-21-interleukin-10-STAT3 pathway is critical for functional maturation of memory CD8+ T cells. Immunity. 2011;35(5):792-805.
66. Siegel AM, Heimall J, Freeman AF, Hsu AP, Brittain E, Brenchley JM, et al. A critical role for STAT3 transcription factor signaling in the development and maintenance of human T cell memory. Immunity. 2011;35(5):806-18.
67. Jeannet G, Boudousquié C, Gardiol N, Kang J, Huelsken J, Held W. Essential role of the Wnt pathway effector Tcf-1 for the establishment of functional CD8 T cell memory. Proc Natl Acad Sci U S A. 2010;107(21):9777-82.
68. Zhou X, Xue HH. Cutting edge: generation of memory precursors and functional memory CD8+ T cells depends on T cell factor-1 and lymphoid enhancer-binding-1. J Immunol. 2012;189(6):2722-6.
69. Rao RR, Li Q, Odunsi K, Shrikant PA. The mTOR kinase determines effector versus memory CD8+ T cell fate by regulating the expression of transcription factors T-bet and Eomesodermin. Immunity. 2010;32(1):67-78.
70. + T cell differentiation. Immunity. 2012;36(3):374-87.
71. Oestreich KJ, Mohn SE, Weinmann AS. Molecular mechanisms that control the expression and activity of Bcl-6 in TH1 cells to regulate flexibility with a TFH-like gene profile. Nat Immunol. 2012;13(4):405-11.
72. Macintyre AN, Finlay D, Preston G, Sinclair LV, Waugh CM, Tamas P, et al. Protein kinase B controls transcriptional proteins that direct cytotoxic T cell fate but is dispensable for T cell metabolism. Immunity. 2011;34(2):224-36.
73. + T cells. Proc Natl Acad Sci U S A. 2007;104(17):7175-80.
74. Lai W, Yu M, Huang MN, Okoye F, Keegan AD, Farber DL. Transcriptional control of rapid recall by memory CD4 T cells. J Immunol. 2011;187(1):133-40.
75. Kersh EN, Kaech SM, Onami TM, Moran M, Wherry EJ, Miceli MC, et al. TCR signal transduction in antigen-specific memory CD8 T cells. J Immunol. 2003;170(11):5455-63.
76. Kalland ME, Oberprieler NG, Vang T, Taskén K, Torgersen KM. T cell-signaling network analysis reveals distinct differences between CD28 and CD2 costimulation responses in various subsets and in the MAPK pathway between resting and activated regulatory T cells. J Immunol. 2011;187(10):5233-45.
77. Chandok MR, Okoye FI, Ndejembi MP, Farber DL. A biochemical signature for the rapid recall of memory CD4 T cells. J Immunol. 2007;179(6):3689-98.
78. Tan-Wong SM, Wijayatilake HD, Proudfoot NJ. Gene loops function to maintain transcriptional memory through interaction with the nuclear pore complex. Genes Dev. 2009;23(22):2610-24.
79. Ansari A, Hampsey M. A role for CPF 3'-end processing machinery in RNAP II-dependent gene looping. Genes Dev. 2005;19(24):2969-78.
80. Flintoft L. Transcriptional memory remodelled. Nat Rev Genet. 2007;8:323.
81. Zacharioudakis I, Gligoris T, Tzamarias D. A yeast catabolic enzyme controls transcriptional memory. Curr Biol. 2007;17(23):2041-6.
82. Light WH, Brickner JH. Nuclear pore proteins regulate chromatin structure and transcriptional memory by a conserved mechanism. Nucleus. 2013;4(5):357-60.
83. Light WH, Brickner DG, Brand VR, Brickner JH. Interaction of a DNA zip code with the nuclear pore complex promotes H2A.Z incorporation and INO1 transcriptional memory. Mol Cell. 2010;40(1):112-25.
84. Light WH, Freaney J, Sood V, Thompson A, D'Urso A, Curt MH, et al. A conserved role for human Nup98 in altering chromatin structure and promoting epigenetic transcriptional memory. PLoS Biol. 2013;11(3):e1001524.
85. Lake RJ, Tsai PF, Choi I, Won KJ, Fan HY. RBPJ, the major transcriptional effect of notch signaling, remains associated with chromatin throughout mitosis, suggesting a role in mitotic bookmarking. PLoS Genet. 2014;10(3):e1004204.
86. Araki K, Turner AP, Shaffer VO, Gangappa S, Keller SA, Bachmann MF, et al. mTOR regulates memory CD8 T cell differentiation. Nature. 2009;460(7251):108-12.
87. Ashe A, Sapetschnig A, Weick EM, Mitchell J, Bagijn MP, Cording AC, et al. piRNAs can trigger a multigenerational epigenetic memory in the germline of C. elegans. Cell. 2012;150(1):88-99.