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Remembering foods and foes: emerging principles of transcriptional memory

Cell Death & Differentiation (2023)Cite this article

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Abstract

Transcriptional memory is characterized by a primed cellular state, induced by an external stimulus that results in an altered expression of primed genes upon re-exposure to the inducing signal. Intriguingly, the primed state is heritably maintained across somatic cell divisions even after the initial stimulus and target gene transcription cease. This phenomenon is widely observed across various organisms and appears to enable cells to retain a memory of external signals, thereby adapting to environmental changes. Signals range from nutrient supplies (food) to a variety of stress signals, including exposure to pathogens (foes), leading to long-term memory such as in the case of trained immunity in plants and mammals. Here, we review these priming phenomena and our current understanding of transcriptional memory. We consider different mechanistic models for how memory can work and discuss existing evidence for potential carriers of memory. Key molecular signatures include: the poising of RNA polymerase II machinery, maintenance of histone marks, as well as alterations in nuclear positioning and long-range chromatin interactions. Finally, we discuss the potential adaptive roles of transcriptional memory in the organismal response to its environment from nutrient sensing to trained immunity.

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Fig. 1: Definition of transcriptional memory.
Fig. 2: Possible trans-acting factors that contribute to transcriptional memory.
Fig. 3: Possible cis-acting factors that contribute to transcriptional memory.
Fig. 4: Common elements implicated in transcriptional memory.

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References

  1. Brickner DG, Cajigas I, Fondufe-Mittendorf Y, Ahmed S, Lee P-C, 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:e81.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Kamada R, Yang W, Zhang Y, Patel MC, Yang Y, Ouda R, et al. Interferon stimulation creates chromatin marks and establishes transcriptional memory. Proc Natl Acad Sci USA. 2018;115:E9162–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Siwek W, Tehrani SSH, Mata JF, Jansen LET. Activation of clustered IFNγ target genes drives cohesin-controlled transcriptional memory. Mol Cell. 2020;80:396–409.e6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bheda P. Metabolic transcriptional memory. Mol Metab. 2020;38:100955.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. 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;40:112–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Sood V, Cajigas I, D’Urso A, Light WH, Brickner JH. Epigenetic transcriptional memory of GAL genes depends on growth in glucose and the Tup1 transcription factor in Saccharomyces cerevisiae. Genetics. 2017;206:1895–907.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Pascual-Garcia P, Debo B, Aleman JR, Talamas JA, Lan Y, Nguyen NH, et al. Metazoan nuclear pores provide a scaffold for poised genes and mediate induced enhancer-promoter contacts. Mol Cell. 2017;66:63–76.e6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Heard E, Martienssen RA. Transgenerational epigenetic inheritance: myths and mechanisms. Cell. 2014;157:95–109.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Durrant WE, Dong X. Systemic acquired resistance. Annu Rev Phytopathol. 2004;42:185–209.

    Article  CAS  PubMed  Google Scholar 

  10. Ding Y, Fromm M, Avramova Z. Multiple exposures to drought ‘train’ transcriptional responses in Arabidopsis. Nat Commun. 2012;3:1–9.

    Article  Google Scholar 

  11. Song J, Angel A, Howard M, Dean C. Vernalization—a cold-induced epigenetic switch. J Cell Sci. 2012;125:3723–31.

    CAS  PubMed  Google Scholar 

  12. Lämke J, Brzezinka K, Altmann S, Bäurle I. A hit-and-run heat shock factor governs sustained histone methylation and transcriptional stress memory. EMBO J. 2016;35:162–75.

    Article  PubMed  Google Scholar 

  13. Naik S, Larsen SB, Gomez NC, Alaverdyan K, Sendoel A, Yuan S, et al. Inflammatory memory sensitizes skin epithelial stem cells to tissue damage. Nature. 2017;550:475–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Sohn C, Lee A, Qiao Y, Loupasakis K, Ivashkiv LB, Kalliolias GD. Prolonged tumor necrosis factor α primes fibroblast-like synoviocytes in a gene-specific manner by altering chromatin. Arthritis Rheumatol. 2015;67:86–95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Gialitakis M, Arampatzi P, Makatounakis T, Papamatheakis J. Gamma interferon-dependent transcriptional memory via relocalization of a gene locus to PML nuclear bodies. Mol Cell Biol. 2010;30:2046–56.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Light WH, Freaney J, Sood V, Thompson A, D’Urso A, Horvath CM, et al. A conserved role for human Nup98 in altering chromatin structure and promoting epigenetic transcriptional memory. PLoS Biol. 2013;11:e1001524.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Ostuni R, Piccolo V, Barozzi I, Polletti S, Termanini A, Bonifacio S, et al. Latent enhancers activated by stimulation in differentiated cells. Cell. 2013;152:157–71.

    Article  CAS  PubMed  Google Scholar 

  18. Netea MG, Quintin J, van der Meer JWM. Trained immunity: a memory for innate host defense. Cell Host Microbe. 2011;9:355–61.

    Article  CAS  PubMed  Google Scholar 

  19. Netea MG, Joosten LAB, Latz E, Mills KHG, Natoli G, Stunnenberg HG, et al. Trained immunity: a program of innate immune memory in health and disease. Science. 2016;352:aaf1098.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Foster SL, Hargreaves DC, Medzhitov R. Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature. 2007;447:972–8.

    Article  CAS  PubMed  Google Scholar 

  21. Novakovic B, Habibi E, Wang S-Y, Arts RJW, Davar R, Megchelenbrink W, et al. β-Glucan reverses the epigenetic state of LPS-induced immunological tolerance. Cell. 2016;167:1354–68.e14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Divangahi M, Aaby P, Khader SA, Barreiro LB, Bekkering S, Chavakis T, et al. Trained immunity, tolerance, priming and differentiation: distinct immunological processes. Nat Immunol. 2020;22:2–6.

    Article  Google Scholar 

  23. Natoli G, Ostuni R. Adaptation and memory in immune responses. Nat Immunol. 2019;20:783–92.

    Article  CAS  PubMed  Google Scholar 

  24. Seeley JJ, Ghosh S. Molecular mechanisms of innate memory and tolerance to LPS. J Leukoc Biol. 2017;101:107–19.

    Article  CAS  PubMed  Google Scholar 

  25. Schuettengruber B, Bourbon HM, Di Croce L, Cavalli G. Genome regulation by polycomb and trithorax: 70 years and counting. Cell. 2017;171:34–57.

    Article  CAS  PubMed  Google Scholar 

  26. Yu JR, Lee CH, Oksuz O, Stafford JM, Reinberg D. PRC2 is high maintenance. Genes Dev. 2019;33:903–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Margueron R, Reinberg D. Chromatin structure and the inheritance of epigenetic information. Nat Rev Genet. 2010;11:285–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Reinberg D, Vales LD. Chromatin domains rich in inheritance only certain histone posttranslational modifications qualify as being epigenetic. Science. 2018;361:33–4.

    Article  CAS  PubMed  Google Scholar 

  29. Zacharioudakis I, Gligoris T, Tzamarias D. A yeast catabolic enzyme controls transcriptional memory. Curr Biol. 2007;17:2041–6.

    Article  CAS  PubMed  Google Scholar 

  30. Ptashne M, Gann A. Genes and Signals. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2002.

  31. Ptashne M. Principles of a switch. Nat Chem Biol. 2011;7:484–7.

    Article  CAS  PubMed  Google Scholar 

  32. Ptashne M. Epigenetics: core misconcept. Proc Natl Acad Sci USA. 2013;110:7101–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. D’Urso A, Takahashi Y-H, Xiong B, Marone J, Coukos R, Randise-Hinchliff C, et al. Set1/COMPASS and Mediator are repurposed to promote epigenetic transcriptional memory. eLife 2016;5:e16691.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Sump B, Brickner DG, D’Urso A, Kim SH, Brickner JH. Mitotically heritable, RNA polymerase II-independent H3K4 dimethylation stimulates INO1 transcriptional memory. eLife. 2022;11:e77646.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Liu N, Avramova Z. Molecular mechanism of the priming by jasmonic acid of specific dehydration stress response genes in Arabidopsis. Epigenetics Chromatin. 2016;9:1–23.

    Article  Google Scholar 

  36. Larsen SB, Cowley CJ, Sajjath SM, Barrows D, Yang Y, Carroll TS, et al. Establishment, maintenance, and recall of inflammatory memory. Cell Stem Cell. 2021;28:1758–74.e8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Ghisletti S, Barozzi I, Mietton F, Polletti S, De Santa F, Venturini E, et al. Identification and characterization of enhancers controlling the inflammatory gene expression program in macrophages. Immunity. 2010;32:317–28.

    Article  CAS  PubMed  Google Scholar 

  38. Ivashkiv LB. Epigenetic regulation of macrophage polarization and function. Trends Immunol. 2013;34:216–23.

    Article  CAS  PubMed  Google Scholar 

  39. Tehrani SS, Mikulski P, Abdul-Zani I, Mata JF, Siwek W, Jansen LE. STAT1 is required to establish but not maintain interferon-γ-induced transcriptional memory. EMBO J. 2023;42:e112259.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Palozola KC, Lerner J, Zaret KS. A changing paradigm of transcriptional memory propagation through mitosis. Nat Rev Mol Cell Biol. 2019;20:55–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Zhao Z, Zhang Z, Li J, Dong Q, Xiong J, Li Y, et al. Sustained tnf-α stimulation leads to transcriptional memory that greatly enhances signal sensitivity and robustness. eLife. 2020;9:1–27.

    Article  Google Scholar 

  42. Li B, Zeis P, Alekseenko A, Lin G, Tekkedil MM, Steinmetz LM, et al. Differential regulation of mRNA stability modulates transcriptional memory and facilitates environmental adaptation. Nat Commun. 2023;14:910.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Oamen HP, Lau Y, Caudron F. Prion-like proteins as epigenetic devices of stress adaptation. Exp Cell Res. 2020;396:112262.

    Article  CAS  PubMed  Google Scholar 

  44. Harvey ZH, Chakravarty AK, Futia RA, Jarosz DF. A prion epigenetic switch establishes an active chromatin state. Cell. 2020;180:928–40.e14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. D’Urso A, Brickner JH. Epigenetic transcriptional memory. Curr Genet. 2017;63:435–9.

    Article  PubMed  Google Scholar 

  46. Bheda P, Aguilar-Gómez D, Becker NB, Becker J, Stavrou E, Kukhtevich I et al. Single-cell tracing dissects regulation of maintenance and inheritance of transcriptional reinduction memory. Mol Cell. 2020;78:915–25.

    Article  CAS  PubMed  Google Scholar 

  47. Pascual-Garcia P, Little SC, Capelson M. Nup98-dependent transcriptional memory is established independently of transcription. eLife. 2022;11:e63404.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Gómez-Rodríguez M, Jansen LET. Basic properties of epigenetic systems: lessons from the centromere. Curr Opin Genet Dev. 2013;23:219–27.

    Article  PubMed  Google Scholar 

  49. Miller T, Krogan NJ, Dover J, Erdjument-Bromage H, Tempst P, Johnston M, et al. COMPASS: a complex of proteins associated with a trithorax-related SET domain protein. Proc Natl Acad Sci. 2001;98:12902–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Quintin J, Saeed S, Martens JHA, Giamarellos-Bourboulis EJ, Ifrim DC, Logie C, et al. Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes. Cell Host Microbe. 2012;12:223–32.

    Article  CAS  PubMed  Google Scholar 

  51. Rasid O, Chevalier C, Camarasa TM-N, Fitting C, Cavaillon J-M, Hamon MA. H3K4me1 supports memory-like NK cells induced by systemic inflammation. Cell Rep. 2019;29:3933–45.e3.

    Article  CAS  PubMed  Google Scholar 

  52. Qiu J, Xu B, Ye D, Ren D, Wang S, Benci JL, et al. Cancer cells resistant to immune checkpoint blockade acquire interferon-associated epigenetic memory to sustain T cell dysfunction. Nat Cancer. 2023;4:43–61.

    CAS  PubMed  Google Scholar 

  53. Halley JE, Kaplan T, Wang AY, Kobor MS, Rine J. Roles for H2A.Z and its acetylation in GAL1 transcription and gene induction, but Not GAL1-transcriptional memory. PLOS Biol. 2010;8:e1000401.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Brzezinka K, Altmann S, Czesnick H, Nicolas P, Gorka M, Benke E, et al. Arabidopsis FORGETTER1 mediates stress-induced chromatin memory through nucleosome remodeling. eLife 2016;5:e17061.

    Article  Google Scholar 

  55. Jeronimo C, Robert F. The mediator complex: at the nexus of RNA polymerase II transcription. Trends Cell Biol. 2017;27:765–83.

    Article  CAS  PubMed  Google Scholar 

  56. Allen BL, Taatjes DJ. The Mediator complex: a central integrator of transcription. Nat Rev Mol Cell Biol. 2015;16:155–66.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Andrau J-C, van de Pasch L, Lijnzaad P, Bijma T, Koerkamp MG, van de Peppel J, et al. Genome-wide location of the coactivator mediator: binding without activation and transient Cdk8 interaction on DNA. Mol Cell. 2006;22:179–92.

    Article  CAS  PubMed  Google Scholar 

  58. Luyties O, Taatjes DJ. The Mediator kinase module: an interface between cell signaling and transcription. Trends Biochem Sci. 2022;47:314–27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Osman S, Mohammad E, Lidschreiber M, Stuetzer A, Bazsó FL, Maier KC, et al. The Cdk8 kinase module regulates interaction of the mediator complex with RNA polymerase II. J Biol Chem. 2021;296:100734.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Rawlings JS, Rosler KM, Harrison DA. The JAK/STAT signaling pathway. J Cell Sci. 2004;117:1281–3.

    Article  CAS  PubMed  Google Scholar 

  61. Bancerek J, Poss ZC, Steinparzer I, Sedlyarov V, Pfaffenwimmer T, Mikulic I, et al. CDK8 kinase phosphorylates transcription factor STAT1 to selectively regulate the interferon response. Immunity. 2013;38:250–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Du J, Johnson LM, Jacobsen SE, Patel DJ. DNA methylation pathways and their crosstalk with histone methylation. Nat Rev Mol Cell Biol. 2015;16:519–32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Law JA, Jacobsen SE. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet. 2010;11:204–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Seaborne RA, Strauss J, Cocks M, Shepherd S, O’Brien TD, van Someren KA, et al. Human skeletal muscle possesses an epigenetic memory of hypertrophy. Sci Rep. 2018;8:1898.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Turner DC, Seaborne RA, Sharples AP. Comparative transcriptome and methylome analysis in human skeletal muscle anabolism, hypertrophy and epigenetic memory. Sci Rep. 2019;9:4251.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Luna E, Bruce TJA, Roberts MR, Flors V, Ton J. Next-generation systemic acquired resistance. Plant Physiol. 2012;158:844–53.

    Article  CAS  PubMed  Google Scholar 

  67. Iurlaro M, von Meyenn F, Reik W. DNA methylation homeostasis in human and mouse development. Curr Opin Genet Dev. 2017;43:101–9.

    Article  CAS  PubMed  Google Scholar 

  68. Iberg-Badeaux A, Collombet S, Laurent B, van Oevelen C, Chin K-K, Thieffry D, et al. A transcription factor pulse can prime chromatin for heritable transcriptional memory. Mol Cell Biol. 2017;37:e00372-16.

    Article  PubMed  PubMed Central  Google Scholar 

  69. Guan Q, Haroon S, Bravo DG, Will JL, Gasch AP. Cellular memory of acquired stress resistance in Saccharomyces cerevisiae. Genetics. 2012;192:495–505.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Casolari JM, Brown CR, Komili S, West J, Hieronymus H, Silver PA. Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization. Cell. 2004;117:427–39.

    Article  CAS  PubMed  Google Scholar 

  71. Sood V, Brickner JH. Nuclear pore interactions with the genome. Curr Opin Genet Dev. 2014;25:43–9.

    Article  CAS  PubMed  Google Scholar 

  72. Fanucchi S, Fok ET, Dalla E, Shibayama Y, Börner K, Chang EY, et al. Immune genes are primed for robust transcription by proximal long noncoding RNAs located in nuclear compartments. Nat Genet. 2019;51:138–50.

    Article  CAS  PubMed  Google Scholar 

  73. Zee BM, Levin RS, DiMaggio PA, Garcia BA. Global turnover of histone post-translational modifications and variants in human cells. Epigenetics Chromatin. 2010;3:22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Alabert C, Barth TK, Reverón-Gómez N, Sidoli S, Schmidt A, Jensen ON, et al. Two distinct modes for propagation of histone PTMs across the cell cycle. Genes Dev. 2015;29:585–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Reverón-Gómez N, González-Aguilera C, Stewart-Morgan KR, Petryk N, Flury V, Graziano S, et al. Accurate recycling of parental histones reproduces the histone modification landscape during DNA replication. Mol Cell. 2018;72:239–49.e5.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Crump NT, Milne TA. Why are so many MLL lysine methyltransferases required for normal mammalian development? Cell Mol Life Sci. 2019;76:2885–98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Ding Y, Fromm M, Avramova Z. Multiple exposures to drought ‘train’ transcriptional responses in Arabidopsis. Nat Commun. 2012;3:740.

    Article  PubMed  Google Scholar 

  78. Colditz GA, Brewer TF, Berkey CS, Wilson ME, Burdick E, Fineberg HV, et al. Efficacy of BCG vaccine in the prevention of tuberculosis: meta-analysis of the published literature. JAMA. 1994;271:698–702.

    Article  CAS  PubMed  Google Scholar 

  79. Fox AE, Evans GL, Turner FJ, Schwartz BS, Blaustein A. Stimulation of nonspecific resistance to infection by a crude cell wall preparation from Mycobacterium phlei. J Bacteriol. 1966;92:1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Metawea B, El-Nashar AR, Kamel I, Kassem W, Shamloul R. Application of viable bacille Calmette-Guérin topically as a potential therapeutic modality in condylomata acuminata: a placebo-controlled study. Urology. 2005;65:247–50.

    Article  PubMed  Google Scholar 

  81. Qiao Y, Giannopoulou EG, Chan CH, Park S-H, Gong S, Chen J, et al. Synergistic activation of inflammatory cytokine genes by interferon-γ-induced chromatin remodeling and toll-like receptor signaling. Immunity. 2013;39:454–69.

    Article  CAS  PubMed  Google Scholar 

  82. Kleinnijenhuis J, Quintin J, Preijers F, Joosten LAB, Ifrim DC, Saeed S, et al. Bacille Calmette-Guerin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes. Proc Natl Acad Sci. 2012;109:17537–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Lau CM, Adams NM, Geary CD, Weizman O-E, Rapp M, Pritykin Y, et al. Epigenetic control of innate and adaptive immune memory. Nat Immunol. 2018;19:963–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Verma D, Parasa VR, Raffetseder J, Martis M, Mehta RB, Netea M, et al. Anti-mycobacterial activity correlates with altered DNA methylation pattern in immune cells from BCG-vaccinated subjects. Sci Rep. 2017;7:12305.

    Article  PubMed  PubMed Central  Google Scholar 

  85. Netea MG, Domínguez-Andrés J, Barreiro LB, Chavakis T, Divangahi M, Fuchs E, et al. Defining trained immunity and its role in health and disease. Nat Rev Immunol. 2020;20:375–88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Ivashkiv LB. IFNγ: signalling, epigenetics and roles in immunity, metabolism, disease and cancer immunotherapy. Nat Rev Immunol. 2018;18:545–58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Kaufmann E, Sanz J, Dunn JL, Khan N, Mendonça LE, Pacis A, et al. BCG educates hematopoietic stem cells to generate protective innate immunity against tuberculosis. Cell. 2018;172:176–90.e19.

    Article  CAS  PubMed  Google Scholar 

  88. Sun JC, Beilke JN, Lanier LL. Adaptive immune features of natural killer cells. Nature. 2009;457:557–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

Funding

Work in our lab is supported by a Senior Wellcome Research Fellowship 210645/Z/18/Z to LETJ. SSHT was supported by Fundação para a Ciência e a Tecnologia (FCT) doctoral fellowship PD/BD/128438/2017. PM is the recipient of a Pump-Priming award from the Goodger and Schorstein Scholarships Trust Fund (0011194). PM and SSHT were supported by the Wellcome SRF. AK is a Clarendon Scholar supported by the Hill Foundation.

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  1. Department of Biochemistry, University of Oxford, OX1 3QU, Oxford, UK

    Sahar S. H. Tehrani, Anna Kogan, Pawel Mikulski & Lars E. T. Jansen

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SSHT conceived and wrote the initial draft. AK wrote additional sections and designed the figures. PM wrote additional sections and helped direct the writing of the manuscript. LETJ helped design figures and wrote the final version. All authors were involved in literature searches, updating and proofreading the manuscript.

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Correspondence to Pawel Mikulski or Lars E. T. Jansen.

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Tehrani, S.S.H., Kogan, A., Mikulski, P. et al. Remembering foods and foes: emerging principles of transcriptional memory. Cell Death Differ (2023). https://doi.org/10.1038/s41418-023-01200-6

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