Transcriptional memory

Transcriptional memory is a biological phenomenon, initially discovered in yeast[1], during which cells primed with a particular cue show increased rates of gene expression after re-stimulation at a later time. This event was shown to take place: in yeast during growth in galactose[1][2] and inositol starvation[3]; plants during environmental stress[4][5][6]; in mammalian cells during LPS[7] and interferon[8][9][10] induction. Prior work has shown that certain characteristics of chromatin may contribute to the poised transcriptional state that allows for faster re-induction. These include: activity of specific transcription factors[11][12][13], retention of RNA polymerase II at the promoters of poised genes[9], activity of chromatin remodeling complexes[2], propagation of H3K4me2[8][13] and H3K36me3[10] histone modifications, occupancy of the H3.3 histone variant[10], as well as binding of nuclear pore components[9][14].

Principle of transcriptional memory. A pulse of an inducer (priming) results in expression of target genes, which subsides upon withdrawal. During a window of no induction (window of memory), some genes maintain a poised but transcriptionally silent state that results in a stronger gene activation upon a second challenge.

References
  1. Acar, Murat; Becskei, Attila; van Oudenaarden, Alexander (2005-05-12). "Enhancement of cellular memory by reducing stochastic transitions". Nature. 435 (7039): 228–232. Bibcode:2005Natur.435..228A. doi:10.1038/nature03524. ISSN 1476-4687. PMID 15889097.
  2. Kundu, Sharmistha; Horn, Peter J.; Peterson, Craig L. (2007-04-15). "SWI/SNF is required for transcriptional memory at the yeast GAL gene cluster". Genes & Development. 21 (8): 997–1004. doi:10.1101/gad.1506607. ISSN 0890-9369. PMC 1847716. PMID 17438002.
  3. Brickner, Donna Garvey; Cajigas, Ivelisse; Fondufe-Mittendorf, Yvonne; Ahmed, Sara; Lee, Pei-Chih; Widom, Jonathan; Brickner, Jason H (April 2007). "H2A.Z-Mediated Localization of Genes at the Nuclear Periphery Confers Epigenetic Memory of Previous Transcriptional State". PLOS Biology. 5 (4): e81. doi:10.1371/journal.pbio.0050081. ISSN 1544-9173. PMC 1828143. PMID 17373856.
  4. Ding, Yong; Fromm, Michael; Avramova, Zoya (January 2012). "Multiple exposures to drought 'train' transcriptional responses in Arabidopsis". Nature Communications. 3 (1): 740. Bibcode:2012NatCo...3..740D. doi:10.1038/ncomms1732. ISSN 2041-1723. PMID 22415831.
  5. Ding, Yong; Liu, Ning; Virlouvet, Laetitia; Riethoven, Jean-Jack; Fromm, Michael; Avramova, Zoya (2013). "Four distinct types of dehydration stress memory genes in Arabidopsis thaliana". BMC Plant Biology. 13 (1): 229. doi:10.1186/1471-2229-13-229. ISSN 1471-2229. PMC 3879431. PMID 24377444.
  6. Sani, Emanuela; Herzyk, Pawel; Perrella, Giorgio; Colot, Vincent; Amtmann, Anna (June 2013). "Hyperosmotic priming of Arabidopsis seedlings establishes a long-term somatic memory accompanied by specific changes of the epigenome". Genome Biology. 14 (6): R59. doi:10.1186/gb-2013-14-6-r59. ISSN 1474-760X. PMC 3707022. PMID 23767915.
  7. Foster, Simmie L.; Hargreaves, Diana C.; Medzhitov, Ruslan (2007-05-30). "Gene-specific control of inflammation by TLR-induced chromatin modifications". Nature. 447 (7147): 972–978. Bibcode:2007Natur.447..972F. doi:10.1038/nature05836. ISSN 0028-0836. PMID 17538624.
  8. Gialitakis, M.; Arampatzi, P.; Makatounakis, T.; Papamatheakis, J. (2010-04-15). "Gamma Interferon-Dependent Transcriptional Memory via Relocalization of a Gene Locus to PML Nuclear Bodies". Molecular and Cellular Biology. 30 (8): 2046–2056. doi:10.1128/MCB.00906-09. ISSN 0270-7306. PMC 2849471. PMID 20123968.
  9. Light, William H.; Freaney, Jonathan; Sood, Varun; Thompson, Abbey; D'Urso, Agustina; Horvath, Curt M.; Brickner, Jason H. (2013-03-26). Misteli, Tom (ed.). "A Conserved Role for Human Nup98 in Altering Chromatin Structure and Promoting Epigenetic Transcriptional Memory". PLOS Biology. 11 (3): e1001524. doi:10.1371/journal.pbio.1001524. ISSN 1545-7885. PMC 3608542. PMID 23555195.
  10. Kamada, Rui; Yang, Wenjing; Zhang, Yubo; Patel, Mira C.; Yang, Yanqin; Ouda, Ryota; Dey, Anup; Wakabayashi, Yoshiyuki; Sakaguchi, Kazuyasu (2018-09-10). "Interferon stimulation creates chromatin marks and establishes transcriptional memory". Proceedings of the National Academy of Sciences. 115 (39): E9162–E9171. doi:10.1073/pnas.1720930115. ISSN 0027-8424. PMC 6166839. PMID 30201712.
  11. D'Urso, Agustina; Takahashi, Yoh-Hei; Xiong, Bin; Marone, Jessica; Coukos, Robert; Randise-Hinchliff, Carlo; Wang, Ji-Ping; Shilatifard, Ali; Brickner, Jason H. (23 June 2016). "Set1/COMPASS and Mediator are repurposed to promote epigenetic transcriptional memory". eLife. 5. doi:10.7554/eLife.16691. ISSN 2050-084X. PMC 4951200. PMID 27336723.
  12. Sood, Varun; Cajigas, Ivelisse; D'Urso, Agustina; Light, William H.; Brickner, Jason H. (August 2017). "Epigenetic Transcriptional Memory of GAL Genes Depends on Growth in Glucose and the Tup1 Transcription Factor in Saccharomyces cerevisiae". Genetics. 206 (4): 1895–1907. doi:10.1534/genetics.117.201632. ISSN 1943-2631. PMC 5560796. PMID 28607146.
  13. Lämke, Jörn; Brzezinka, Krzysztof; Altmann, Simone; Bäurle, Isabel (2016-01-18). "A hit-and-run heat shock factor governs sustained histone methylation and transcriptional stress memory". The EMBO Journal. 35 (2): 162–175. doi:10.15252/embj.201592593. ISSN 1460-2075. PMC 4718455. PMID 26657708.
  14. Pascual-Garcia, Pau; Debo, Brian; Aleman, Jennifer R.; Talamas, Jessica A.; Lan, Yemin; Nguyen, Nha H.; Won, Kyoung J.; Capelson, Maya (2017-04-06). "Metazoan Nuclear Pores Provide a Scaffold for Poised Genes and Mediate Induced Enhancer-Promoter Contacts". Molecular Cell. 66 (1): 63–76.e6. doi:10.1016/j.molcel.2017.02.020. ISSN 1097-4164. PMID 28366641.


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