Transcriptional memory
Biological phenomenon
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.
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 allowing 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] Moreover, locally bound cohesin was shown to inhibit establishment of transcriptional memory in human cells during interferon gamma stimulation.[ 15]
References
^ a b 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 . S2CID 4429383 .
^ a b 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 .
^ 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 .
^ 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 .
^ 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 .
^ 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 .
^ 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 . S2CID 4426398 .
^ a b 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 .
^ a b c 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 .
^ a b c 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. Bibcode :2018PNAS..115E9162K . doi :10.1073/pnas.1720930115 . ISSN 0027-8424 . PMC 6166839 . PMID 30201712 .
^ 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 .
^ 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 .
^ a b 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 .
^ 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 . PMC 7439321 . PMID 28366641 .
^ Siwek, Wojciech; Tehrani, Sahar S.H.; Mata, João F.; Jansen, Lars E.T. (November 2020). "Activation of Clustered IFNγ Target Genes Drives Cohesin-Controlled Transcriptional Memory" . Molecular Cell . 80 (3): 396–409.e6. doi :10.1016/j.molcel.2020.10.005 . ISSN 1097-2765 . PMC 7657446 . PMID 33108759 . S2CID 225100808 .