Gene regulation in the immediate-early response process

Bahrami, Shahram; Drabløs, Finn

doi:10.1016/j.jbior.2016.05.001

Cited by 465Genomics and Chromatin DynamicsProtein Kinase Regulation and GTPase SignalingGene Regulatory Network Analysis

Gene regulation in the immediate-early response process

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Bahrami, Shahram, Drabløs, Finn·2016·Advances in Biological Regulation

DOI 10.1016/j.jbior.2016.05.001

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Abstract

Immediate-early genes (IEGs) can be activated and transcribed within minutes after stimulation, without the need for de novo protein synthesis, and they are stimulated in response to both cell-extrinsic and cell-intrinsic signals. Extracellular signals are transduced from the cell surface, through receptors activating a chain of proteins in the cell, in particular extracellular-signal-regulated kinases (ERKs), mitogen-activated protein kinases (MAPKs) and members of the RhoA-actin pathway. These communicate through a signaling cascade by adding phosphate groups to neighboring proteins, and this will eventually activate and translocate TFs to the nucleus and thereby induce gene expression. The gene activation also involves proximal and distal enhancers that interact with promoters to simulate gene expression. The immediate-early genes have essential biological roles, in particular in stress response, like the immune system, and in differentiation. Therefore they also have important roles in various diseases, including cancer development. In this paper we summarize some recent advances on key aspects of the activation and regulation of immediate-early genes.

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Teif, V. B., & Rippe, K. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp610 · Cited by 99 · see citing works
Mitogen-induced recruitment of ERK and MSK to SRE promoter complexes by ternary complex factor Elk-1
Zhang, H.-M., Li, L., Papadopoulou, N., Hodgson, G., Evans, E., Galbraith, M., Dear, M., Vougier, S., Saxton, J., & Shaw, P. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn099 · Cited by 95 · cited 1× · see citing works
“ELK1 leads to recruitment of MSKs to the promoter and thereby H3S10 phosphorylation (Zhang et al., 2008).”
Background
Myocardin Sumoylation Transactivates Cardiogenic Genes in Pluripotent 10T1/2 Fibroblasts
Wang, J., Li, A., Wang, Z.-G., Feng, X., Olson, E., & Schwartz, R. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.01160-06 · Cited by 90 · cited 1× · see citing works
“Phosphorylation of MKL1 inhibits its activity, while SUMO-modification of MKL1 and myocardin has the opposite effect (Nakagawa and Kuzumaki, 2005; Wang et al., 2007).”
Background
Complexity in Transcription Control at the Activation Domain–Mediator Interface
Balamotis, M. A., Pennella, M. A., Stevens, J. L., Wasylyk, B., Belmont, A. S., & Berk, A. J. (2009) · Science Signaling · doi:10.1126/scisignal.1164302 · Cited by 84 · cited 1× · see citing works
“Multiple pathways may be activated in parallel for a given signal (Bebien et al., 2003).”
Background
The Serum Response Factor and a Putative Novel Transcription Factor Regulate Expression of the Immediate-Early Gene Arc/Arg3.1 in Cultured Cortical Neurons
Pintchovski, S. A., Peebles, C., Kim, H. J., Verdin, E., & Finkbeiner, S. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5575-08.2009 · Cited by 80 · cited 1× · see citing works
“In other signaling situations, SRF can co-operate with other co-regulatory factors such as members of the MRTF (myocardin-related transcription factor) family, and thereby affect the regulation of FOS expression (Cen et al., 2003; Knoll and Nordheim, 2009; Posern and Treisman, 2006).”
Background
Single-round of antigen receptor signaling programs naïve B cells to receive T cell help
Damdinsuren, B., Zhang, Y.-Q., Khalil, A., Wood, W., Becker, K., Shlomchik, M., & Sen, R. (2010) · Immunity · doi:10.1016/j.immuni.2010.02.013 · Cited by 73 · see citing works
Specific Interaction of Egr1 and c/EBPβ Leads to the Transcriptional Activation of the Human Low Density Lipoprotein Receptor Gene*
Zhang, F., Lin, M.-H., Abidi, P., Thiel, G., & Liu, J.-W. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m305564200 · Cited by 73
Role of ERK signaling in activity-dependent modifications of histone proteins
Ciccarelli, A., & Giustetto, M. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.01.039 · Cited by 70 · see citing works
Comparison of MAPK specificity across the ETS transcription factor family identifies a high-affinity ERK interaction required for ERG function in prostate cells
Selvaraj, N., Kedage, V., & Hollenhorst, P. C. (2015) · Cell Communication and Signaling · doi:10.1186/s12964-015-0089-7 · Cited by 69 · see citing works
Activation and Repression of Cellular Immediate Early Genes by Serum Response Factor Cofactors*
Lee, S.-M., Vasishtha, M., & Prywes, R. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.108878 · Cited by 68 · see citing works
Physical interaction between p53 and primary response gene Egr-1.
Liu, J., Grogan, L., Nau, M., Allegra, C. J., Chu, E., & Wright, J. J. (2001) · International Journal of Oncology · doi:10.3892/ijo.18.4.863 · Cited by 66 · see citing works
H3S28 phosphorylation is a hallmark of the transcriptional response to cellular stressPreprint
Sawicka, A., Hartl, D., Goiser, M., Pusch, O., Stocsits, R. R., Tamir, I., Mechtler, K., & Seiser, C. (2014) · Genome Research · doi:10.1101/gr.176255.114 · Cited by 66 · see citing works
Histone H3 phosphorylation, immediate-early gene expression, and the nucleosomal response: a historical perspective1This article is part of Special Issue entitled Asilomar Chromatin and has undergone the Journal’s usual peer review process.
Healy, S., Khan, P., He, S., & Davie, J. (2012) · Biochemistry and Cell Biology · doi:10.1139/o11-092 · Cited by 66 · cited 3× · see citing works
“…signal, such as growth factors (e.g. platelet-derived growth factor (PDGF) and epidermal growth factor (EGF)), mitogens and phorbol esters, immunological and neurological signals, developmental, and stress (e.g. UV, toxins) (Herschman, 1991; Morgan and Curran, 1991; O'Donnell et al., 2012).”
Background
Angiotensin II–Stimulated Signaling Through G Proteins and β-Arrestin
Shenoy, S. K., & Lefkowitz, R. (2005) · Science's STKE · doi:10.1126/stke.3112005cm14 · Cited by 65
Immediate-early gene induction by the stresses anisomycin and arsenite in human osteosarcoma cells involves MAPK cascade signaling to Elk-1, CREB and SRF
Bebien, M., Salinas, S., Bécamel, C., Richard, V., Linares, L. K., & Hipskind, R. (2003) · Oncogene · doi:10.1038/sj.onc.1206334 · Cited by 65 · see citing works
Transcriptional Dynamics Reveal Critical Roles for Non-coding RNAs in the Immediate-Early Response
Aitken, S., Magi, S., Alhendi, A. M. N., Itoh, M., Kawaji, H., Lassmann, T., Daub, C. O., Arner, E., Carninci, P., Forrest, A. R. R., et al. (2015) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004217 · Cited by 62 · cited 2× · see citing works
“After stimulation of IEG expression the production of these microRNAs is blocked, but then comes quickly back to normal levels (Aitken et al., 2015; Avraham et al., 2010).”
Background
Dynamic bookmarking of primary response genes by p300 and RNA polymerase II complexes
Byun, J. S., Wong, M., Cui, W., Idelman, G., Li, Q., Siervi, A. D., Bilke, S., Haggerty, C. M., Player, A. N., Wang, Y. H., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0905469106 · Cited by 61 · cited 3× · see citing works
“The importance of the control of MKL1 activation by TCFs or other factors is clear in megakaryoblastic leukemia, where MKL1 is fused to the RBM15 protein and activated due to constitutive nuclear localization (Cen et al., 2003; Guettler et al., 2008).”
Background
Convergence of the SUMO and MAPK pathways on the ETS-domain transcription factor Elk-1.
Yang, S.-H., & Sharrocks, A. (2006) · Biochemical Society Symposium · doi:10.1042/bss0730121 · Cited by 49 · cited 2× · see citing works
“The TCF component is a receptor of this signal, being a direct MAPK phosphorylation target (Selvaraj et al., 2015; Shaw and Saxton, 2003; Yang and Sharrocks, 2006).”
Background
The Immediate Early Gene Product EGR1 and Polycomb Group Proteins Interact in Epigenetic Programming during Chondrogenesis
Spaapen, F., van den Akker, G., Caron, M. M. J., Prickaerts, P., Rofel, C., Dahlmans, V. E. H., Surtel, D. A., Paulis, Y. W. J., Schweizer, F., Welting, T. J. M., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0058083 · Cited by 49 · see citing works
Regulation of Egr-1 by association with the proteasome component C8.
Bae, M., Jeong, C.-H., Kim, S.-H., Bae, M., Jeong, J.-W., Ahn, M., Bae, S., Kim, N., Kim, C., Kim, K., et al. (2002) · Biochimica et Biophysica Acta · doi:10.1016/s0167-4889(02)00310-5 · Cited by 45 · cited 2× · see citing works
“…and non-DNA-binding domains (Bahrami et al., 2015), it has interaction with CEBPB, PSMA3 and P53 and is involved in the regulation of cell growth and differentiation in response to signals such as mitogens, growth factors, and stress stimuli (Bae et al., 2002; Liu et al., 2001; Zhang et al., 2003).”
Background
Regulation of lymphocyte fate by Ras/ERK signals
Yasuda, T., & Kurosaki, T. (2008) · Cell Cycle · doi:10.4161/cc.7.23.7103 · Cited by 42 · cited 1× · see citing works
“…in mammalian cells, including ERK (extracellular signal regulated kinase), RSK (p90 ribosomal S6 kinase), JNK (c-Jun N-terminal kinase), p38, and ERK5 (extracellular signal regulated kinase-5, also called Big MAP kinase-1 (BMK1)) (Raman et al., 2007; Yang et al., 2003; Yasuda and Kurosaki, 2008).”
Background
Fos family protein degradation by the proteasome.
Gomard, T., Jariel-Encontre, I., Basbous, J., Bossis, G., Mocquet-Torcy, G., & Piechaczyk, M. (2008) · Biochemical Society Transactions · doi:10.1042/bst0360858 · Cited by 40 · cited 2×
“For example, expression of the FOS gene peaks 30e60min after stimulation, and returns to basal expression after 90min (Greenberg and Ziff, 1984).”
Background
Transcriptional activity of megakaryoblastic leukemia 1 (MKL1) is repressed by SUMO modification
Nakagawa, K., & Kuzumaki, N. (2005) · Genes to Cells · doi:10.1111/j.1365-2443.2005.00880.x · Cited by 39 · see citing works
Dynamic Acetylation of All Lysine 4–Methylated Histone H3 in the Mouse Nucleus: Analysis at c-fos and c-jun
Hazzalin, C. A., & Mahadevan, L. C. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030393 · Cited by 35 · see citing works
Cascades of transcriptional induction during human lymphocyte activation.
Ellisen, L., Palmer, R., Maki, R., Truong, V., Tamayo, P., Oliner, J., & Haber, D. A. (2001) · European Journal of Cell Biology · doi:10.1078/0171-9335-00162 · Cited by 35 · cited 1× · see citing works
“They have been found within or close to almost 40% of all promoters of mammalian genes (Deaton and Bird, 2011; Fatemi et al., 2005).”
Background
High Degree of Overlap between Responses to a Virus and to the House Dust Mite Allergen in Airway Epithelial Cells
Golebski, K., Luiten, S., van Egmond, D., Groot, E. J. J. D., Röschmann, K., Fokkens, W. J., & van Drunen, C. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087768 · Cited by 34 · see citing works
The Response of Secondary Genes to Lipopolysaccharides in Macrophages Depends on Histone Deacetylase and Phosphorylation of C/EBPβ
Serrat, N., Sebastián, C., Pereira-Lopes, S., Valverde-Estrella, L., Lloberas, J., & Celada, A. (2014) · Journal of Immunology · doi:10.4049/jimmunol.1203500 · Cited by 34 · cited 1× · see citing works
“The TCF component is a receptor of this signal, being a direct MAPK phosphorylation target (Selvaraj et al., 2015; Shaw and Saxton, 2003; Yang and Sharrocks, 2006).”
Background
Preparing the First Responders: Building the Inflammatory Transcriptome from the Ground Up
Rogatsky, I., & Adelman, K. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.03.038 · Cited by 33 · see citing works
Invasion is a genetic program regulated by transcription factors.
Ozanne, B., Spence, H., Mcgarry, L., & Hennigan, R. (2006) · Current Opinion in Genetics and Development · doi:10.1016/j.gde.2005.12.012 · Cited by 33 · cited 1× · see citing works
“This transcription factor plays an important role during both normal development and disease states such as cancer (Ozanne et al., 2006).”
Background
Chromatin states reveal functional associations for globally defined transcription start sites in four human cell lines
Rye, M. B., Sandve, G. K., Daub, C. O., Kawaji, H., Carninci, P., Forrest, A. R. R., & Drabløs, F. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-120 · Cited by 31 · see citing works
Self-citation
The Essential Function for Serum Response Factor in T-Cell Development Reflects Its Specific Coupling to Extracellular Signal-Regulated Kinase Signaling
Mylona, A., Nicolas, R., Maurice, D., Sargent, M., Tuil, D., Daegelen, D., Treisman, R., & Costello, P. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.01058-10 · Cited by 27 · cited 1× · see citing works
“Phosphorylation of MKL1 inhibits its activity, while SUMO-modification of MKL1 and myocardin has the opposite effect (Nakagawa and Kuzumaki, 2005; Wang et al., 2007).”
Background
Role of human transcription elongation factor DSIF in the suppression of senescence and apoptosis
Komori, T., Inukai, N., Yamada, T., Yamaguchi, Y., & Handa, H. (2009) · Genes to Cells · doi:10.1111/j.1365-2443.2008.01273.x · Cited by 27 · see citing works
Lessons on transcriptional control from the serum response network
Galbraith, M., & Espinosa, J. M. (2011) · Current Opinion in Genetics and Development · doi:10.1016/j.gde.2011.01.011 · Cited by 26 · see citing works
The actin/MKL1 signalling pathway influences cell growth and gene expression through large-scale chromatin reorganization and histone post-translational modifications.
Flouriot, G., Huet, G., Demay, F., Pakdel, F., Boujrad, N., & Michel, D. (2014) · Biochemical Journal · doi:10.1042/bj20131240 · Cited by 25 · cited 1× · see citing works
“They will also initiate changes in post-translational modifications of histones, leading to changes in the chromatin structure (Ciccarelli and Giustetto, 2014; Flouriot et al., 2014; Sawicka et al., 2014).”
Background
Negative elongation factor NELF controls transcription of immediate early genes in a stimulus-specific manner.
Fujita, T., Piuz, I., & Schlegel, W. (2009) · Experimental Cell Research · doi:10.1016/j.yexcr.2008.10.032 · Cited by 25 · see citing works
Response network analysis of differential gene expression in human epithelial lung cells during avian influenza infections
Tatebe, K., Zeytun, A., Ribeiro, R., Hoffmann, R., Harrod, K., & Forst, C. (2010) · BMC Bioinformatics · doi:10.1186/1471-2105-11-170 · Cited by 22 · cited 1× · see citing works
“Chromatin remodeling allows proteins of the regulatory transcription machinery access to condensed genomic DNA, and thereby control of gene expression (Teif and Rippe, 2009).”
Background
The role of mitogen‐ and stress‐activated protein kinase 1 and 2 in chronic skin inflammation in mice
Bertelsen, T., Iversen, L., Riis, J. L., Arthur, J. S., Bibby, B., Kragballe, K., & Johansen, C. (2011) · Experimental Dermatology · doi:10.1111/j.1600-0625.2010.01153.x · Cited by 21 · cited 1×
“Also RNA polymerase II is accumulated and “poised” at the proximal promoter region of IEGs (Byun et al., 2009; Tullai et al., 2007).”
Background
Poly(ADP-Ribosyl)ation Is Required to Modulate Chromatin Changes at c-MYC Promoter during Emergence from Quiescence
Mostocotto, C., Carbone, M., Battistelli, C., Ciotti, A., Amati, P., & Maione, R. (2014) · PLoS ONE · doi:10.1371/journal.pone.0102575 · Cited by 13 · cited 2×
“Depending on the kind of cell type and the duration of signaling, the biological outcome may be different (Murphy and Blenis, 2006).”
Background
HDAC inhibitors prevent the induction of the immediate‐early gene FOSL1, but do not alter the nucleosome response
Khan, D. H., & Davie, J. (2013) · FEBS Letters · doi:10.1016/j.febslet.2013.03.029 · Cited by 10 · see citing works
A property-based analysis of human transcription factors
Bahrami, S., Ehsani, R., & Drabløs, F. (2015) · BMC Research Notes · doi:10.1186/s13104-015-1039-6 · Cited by 10 · see citing works
Self-citation
Transcriptional activation of immediate-early genes c-fos, c-jun, and Egr-1 in response to anisomycin treatment of cells transformed by the E1A and cHa-ras oncogenes
Kukushkin, A., Svetlikova, S., & Pospelov, V. (2005) · Molecular Biology · doi:10.1007/s11008-005-0010-3 · Cited by 4

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5 of the 109 references couldn’t be matched to a known paper.

Sorted by citations

Loss of a mammalian circular RNA locus causes miRNA deregulation and affects brain function
Piwecka, M., Glažar, P., Hernandez-Miranda, L. R., Memczak, S., Wolf, S. A., Rybak-Wolf, A., Filipchyk, A., Klironomos, F., Cerda Jara, C. A., Fenske, P., et al. (2017) · Science · doi:10.1126/science.aam8526 · Cited by 1,210 · see citing works
The Role of Early Growth Response 1 (EGR1) in Brain Plasticity and Neuropsychiatric Disorders
Duclot, F., & Kabbaj, M. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00035 · Cited by 359 · see citing works
“In this perspective, it appears crucial to better understand how the organism reacts to environmental stimuli and provide a coordinated and adapted response.”
BackgroundInfluential
Immediate Early Genes, Memory and Psychiatric Disorders: Focus on c-Fos, Egr1 and Arc
Gallo, F. T., Katche, C., Morici, J. F., Medina, J. H., & Weisstaub, N. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00079 · Cited by 339 · see citing works
“…to a variety of cellular stimuli Frontiers in Behavioral Neuroscience | www.frontiersin.org 2 April 2018 | Volume 12 | Article 79 (Hughes and Dragunow, 1995; Kaczmarek and Chaudhuri, 1997; Herdegen and Leah, 1998; Pinaud et al., 2005; Terleph and Tremere, 2006; Bahrami and Drabløs, 2016).”
Background
Single-cell transcriptomic atlas of the human retina identifies cell types associated with age-related macular degeneration
Menon, M., Mohammadi, S., Davila-Velderrain, J., Goods, B. A., Cadwell, T. D., Xing, Y., Stemmer-Rachamimov, A., Shalek, A. K., Love, J. C., Kellis, M., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12780-8 · Cited by 331 · see citing works
The RNA modification N6-methyladenosine as a novel regulator of the immune system
Shulman, Z., & Stern‐Ginossar, N. (2020) · Nature Immunology · doi:10.1038/s41590-020-0650-4 · Cited by 429 · see citing works
Heterogeneity of human bone marrow and blood natural killer cells defined by single-cell transcriptome
Yang, C., Siebert, J., Burns, R., Gerbec, Z. J., Bonacci, B. B., Rymaszewski, A. L., Rau, M. J., Riese, M. J., Rao, S., Carlson, K.-S., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-11947-7 · Cited by 298 · see citing works
The neuroscience of positive emotions and affect: Implications for cultivating happiness and wellbeing
Alexander, R., Aragón, O. R., Bookwala, J., Cherbuin, N., Gatt, J. M., Kahrilas, I. J., Kästner, N., Lawrence, A. B., Lowe, L. J., Morrison, R., et al. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.12.002 · Cited by 329 · see citing works
“…in linking physical exercise to positive affect (Burgdorf et al., 2016; Torres-Aleman, 2010), and it is also known that immediate early genes (IEG; Bahrami and Drabl ø s, 2016) which can be rapidly induced by the sensory experience of enrichment (Brown et al., 2018) have roles in both…”
Single-cell atlas of colonic CD8+ T cells in ulcerative colitis
Corridoni, D., Antanaviciute, A., Gupta, T., Fawkner-Corbett, D., Aulicino, A., Jagielowicz, M., Parikh, K., Repapi, E., Taylor, S. L., Ishikawa, D., et al. (2020) · Nature Medicine · doi:10.1038/s41591-020-1003-4 · Cited by 252 · see citing works
Single cell chromatin accessibility reveals pancreatic islet cell type- and state-specific regulatory programs of diabetes risk
Chiou, J., Zeng, C., Cheng, Z., Han, J. Y., Schlichting, M., Huang, S., Wang, J., Sui, Y., Deogaygay, A., Okino, M.-L., et al. (2019) · doi:10.1101/693671 · Cited by 189 · see citing works
A genetic map of the mouse dorsal vagal complex and its role in obesity
Ludwig, M. Q., Cheng, W., Gordian, D., Lee, J., Paulsen, S. J., Hansen, S. N., Egerod, K. L., Barkholt, P., Rhodes, C. J., Secher, A., et al. (2021) · Nature Metabolism · doi:10.1038/s42255-021-00363-1 · Cited by 186 · see citing works
Regulation of the RNAPII Pool Is Integral to the DNA Damage Response
Vidaković, A. T., Mitter, R., Kelly, G. P., Neumann, M., Harreman, M. T., Rodríguez‐Martínez, M., Herlihy, A. E., Weems, J. C., Boeing, S., Encheva, V., et al. (2020) · Cell · doi:10.1016/j.cell.2020.02.009 · Cited by 209 · see citing works
“Dominant among these are the so-called immediate-early genes (IEGs), which are rapidly but transiently upregulated following a variety of stimuli, such as growth factors, hormones or cellular stress (Bahrami and Drabløs, 2016).”
Enhancer hijacking activates oncogenic transcription factor NR4A3 in acinic cell carcinomas of the salivary glands
Haller, F., Bieg, M., Will, R. D., Körner, C., Weichenhan, D., Bott, A., Ishaque, N., Lutsik, P., Moskalev, E. A., Mueller, S. K., et al. (2019) · Nature Communications · doi:10.1038/s41467-018-08069-x · Cited by 207 · see citing works
Acoel genome reveals the regulatory landscape of whole-body regeneration
Gehrke, A. R., Neverett, E. R., Luo, Y., Brandt, A., Ricci, L., Hulett, R. E., Gompers, A. D., Ruby, J. G., Rokhsar, D. S., Reddien, P. W., et al. (2019) · Science · doi:10.1126/science.aau6173 · Cited by 172 · see citing works
The midnolin-proteasome pathway catches proteins for ubiquitination-independent degradation
Gu, X., Nardone, C., Kamitaki, N., Mao, A., Elledge, S. J., & Greenberg, M. E. (2023) · Science · doi:10.1126/science.adh5021 · Cited by 153 · see citing works
“The IEG mRNAs ac-cumulateto a high level, andoncethese mRNAs are translated, the IEG proteins undergo rapid decay ( 5 ).”
Background
Engram-specific transcriptome profiling of contextual memory consolidation
Rao‐Ruiz, P., Couey, J. J., Marcelo, I. M., Bouwkamp, C. G., Slump, D. E., Matos, M. R., van der Loo, R. J., Martins, G. J., van den Hout, M. C. G. N., van IJcken, W. F. J., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09960-x · Cited by 146 · see citing works
Current knowledge on the acute regulation of steroidogenesis
Selvaraj, V., Stocco, D. M., & Clark, B. J. (2018) · Biology of Reproduction · doi:10.1093/biolre/ioy102 · Cited by 118 · see citing works
Characterization of the Giardia intestinalis secretome during interaction with human intestinal epithelial cells: The impact on host cells
Ma'ayeh, S., Liu, J.-Y., Peirasmaki, D., Hörnaeus, K., Lind, S. B., Grabherr, M., Bergquist, J., & Svärd, S. (2017) · PLoS Neglected Tropical Diseases · doi:10.1371/journal.pntd.0006120 · Cited by 116 · see citing works
Early Growth Response Gene-2 Is Essential for M1 and M2 Macrophage Activation and Plasticity by Modulation of the Transcription Factor CEBPβ
Veremeyko, T., Yung, A. W. Y., Anthony, D. C., Strekalova, T. V., & Ponomarev, E. D. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02515 · Cited by 105 · see citing works
“The most studied gene from Egr family is Egr1, while the function of Egr2 is less studied (47, 48).”
Background
Mechanisms of African swine fever virus pathogenesis and immune evasion inferred from gene expression changes in infected swine macrophages
Zhu, J. J., Ramanathan, P., Bishop, E., O'Donnell, V., Gladue, D., & Borca, M. (2019) · PLoS ONE · doi:10.1371/journal.pone.0223955 · Cited by 100 · see citing works
“EGRs, FOS and JUN are immediate early response genes which expression can be rapidly induced without requiring de novo protein synthesis during viral infection [40, 65].”
Background
Olfactory sensory neurons mediate ultrarapid antiviral immune responses in a TrkA-dependent manner
Sepahi, A., Kraus, A., Casadei, E., Johnston, C. A., Galindo-Villegas, J., Kelly, C., García-Moreno, D., Muñoz, P., Mulero, V., Huertas, M., et al. (2019) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1900083116 · Cited by 83 · see citing works
Gut dysbiosis impairs hippocampal plasticity and behaviors by remodeling serum metabolome
Liu, G., Yu, Q., Tan, B., Ke, X., Zhang, C., Li, H., Zhang, T.-M., & Lu, Y.-M. (2022) · Gut microbes · doi:10.1080/19490976.2022.2104089 · Cited by 79 · see citing works
“They are believed to be crucial for synaptic plasticity, hippocampal memory, and long-term changes in mood.(59) Decreased hippocampal IEGs expression by infusion of antisense oligonucleotide has been reported to impair learning and memory.”
Background
Chromatin Remodeling and Immediate Early Gene Activation by SLFN11 in Response to Replication Stress
Murai, J., Zhang, H.-L., Pongor, L., Tang, S.-W., Jo, U., Moribe, F., Ma, Y., Tomita, M., & Pommier, Y. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.02.117 · Cited by 71 · see citing works
“As IEGs are generally short in length (Bahrami and Drabløs, 2016), we next considered the gene length.”
BackgroundInfluential
Determinants of renal cell carcinoma invasion and metastatic competence
Kim, K., Zhou, Q.-B., Christie, A., Stevens, C., Ma, Y., Onabolu, O., Chintalapati, S., McKenzie, T., Tcheuyap, V., Woolford, L., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25918-4 · Cited by 69 · see citing works
The collateral activity of RfxCas13d can induce lethality in a RfxCas13d knock-in mouse model
Li, Y.-F., Xu, J., Guo, X.-F., Li, Z.-W., Cao, L., Liu, S.-D., Guo, Y., Wang, G., Luo, Y., Zhang, Z., et al. (2023) · Genome Biology · doi:10.1186/s13059-023-02860-w · Cited by 68 · see citing works
“IEGs are activated transiently and rapidly in response to various cellular stimuli and several pathways have been reported to regulate the activation of IEGs, such as the RhoA-actin and the ERK, JNK, and p38 MAPK pathways [42].”
Background
Neural Stimulation and Molecular Mechanisms of Plasticity and Regeneration: A Review
Hogan, M., Hamilton, G. F., & Horner, P. J. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00271 · Cited by 74 · see citing works
“Recently, it was demonstrated that some IEGs exhibit control mechanisms that are not directly dependent on neural activity (Okuno, 2011; Bahrami and Drabløs, 2016).”
Background
Lipoxins Regulate the Early Growth Response–1 Network and Reverse Diabetic Kidney Disease
Brennan, E. P., Mohan, M., McClelland, A., Tikellis, C., Ziemann, M., Kaspi, A., Gray, S. P., Pickering, R. J., Tan, S. M., Shah, S. T. A., et al. (2018) · Journal of the American Society of Nephrology · doi:10.1681/asn.2017101112 · Cited by 71 · see citing works
NR4A1 regulates expression of immediate early genes, suppressing replication stress in cancer
Guo, H.-S., Golczer, G., Wittner, B., Langenbucher, A., Zachariah, M. A., Dubash, T. D., Hong, X., Comaills, V., Burr, R., Ebright, R., et al. (2021) · Molecules and Cells · doi:10.1016/j.molcel.2021.09.016 · Cited by 63 · see citing works
Insulin‐like growth factor 1 signaling in tenocytes is required for adult tendon growth
Disser, N. P., Sugg, K., Talarek, J. R., Sarver, D. C., Rourke, B. J., & Mendias, C. (2019) · The FASEB Journal · doi:10.1096/fj.201901503r · Cited by 62 · see citing works
Transcription factor Fra-2 and its emerging role in matrix deposition, proliferation and inflammation in chronic lung diseases.
Birnhuber, A., Biasin, V., Schnoegl, D., Marsh, L., & Kwapiszewska, G. (2019) · Cellular Signalling · doi:10.1016/j.cellsig.2019.109408 · Cited by 61 · see citing works
Sequential enhancer state remodelling defines human germline competence and specification
Tang, W. W. C., Castillo-Venzor, A., Gruhn, W. H., Kobayashi, T., Penfold, C. A., Morgan, M., Sun, D., Irie, N., & Surani, M. (2022) · Nature Cell Biology · doi:10.1038/s41556-022-00878-z · Cited by 59 · see citing works
Psychedelic-Induced Neural Plasticity: A Comprehensive Review and a Discussion of Clinical Implications
Weiss, F., Magnesa, A., Gambini, M., Gurrieri, R., Annuzzi, E., Elefante, C., Perugi, G., & Marazziti, D. (2025) · Brain Sciences · doi:10.3390/brainsci15020117 · Cited by 67 · see citing works
“Gene expression studies (Tables 1–4) show that these compounds can induce the expression of IEGs (e.g., c-Fos and egr1 ), which are known to be involved in cell growth, differentiation and adaptation, not only in neurons, but in putatively every nucleated cytotype [120].”
Temporal unsnarling of brain’s acute neuroinflammatory transcriptional profiles reveals panendothelitis as the earliest event preceding microgliosis
Kodali, M. C., Chen, H., & Liao, F. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-00955-5 · Cited by 60 · see citing works
“responses and are transcribed within minutes of cellextrinsic signals without the need for de-novo protein synthesis [34, 42].”
Background
Contribution of Neuroepigenetics to Huntington’s Disease
Francelle, L., Lotz, C., Outeiro, T. F., Brouillet, E., & Mérienne, K. (2017) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2017.00017 · Cited by 69 · see citing works
“The Ras/MAPK/MSK1 signaling pathway is another pathway, where transcriptional and epigenetic responses are coordinated through phosphorylation events targeting transcription factors and histones (e.g., ELK1 and H3 at serine 10, respectively) (Brami-Cherrier et al., 2009; Bahrami and Drablos, 2016).”
Background
HTLV-1: Regulating the Balance Between Proviral Latency and Reactivation
Kulkarni, A., & Bangham, C. R. M. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.00449 · Cited by 56 · see citing works
“TATA boxes are frequently observed in promoters of cellular genes which are highly regulated and responsive to stress and extracellular signals (Basehoar et al., 2004; Bahrami and Drablos, 2016).”
Background
Analysis of sea star larval regeneration reveals conserved processes of whole-body regeneration across the metazoa
Cary, G., Wolff, A., Zueva, O. R., Pattinato, J., & Hinman, V. (2017) · BMC Biology · doi:10.1186/s12915-019-0633-9 · Cited by 56 · see citing works
Defining the identity and the niches of epithelial stem cells with highly pleiotropic multilineage potency in the human thymus
Ragazzini, R., Boeing, S., Zanieri, L., Green, M. J., D’Agostino, G., Bartolović, K., Água-Doce, A., Greco, M., Watson, S. A., Batsivari, A., et al. (2023) · Developmental Cell · doi:10.1016/j.devcel.2023.08.017 · Cited by 54 · see citing works
“When we determined the marker genes of this cluster, we identiﬁed a group of immediate-early genes (IEGs) (i.e., JUN, FOS, ATF3 —so-called AP-1 family genes—and EGR1 ), associated with rapid responses to regulatory signals, such as immune responses or cellular stress 44 (Figure S1G).”
Background
Microfluidics for Peptidomics, Proteomics, and Cell Analysis
Vitorino, R. M. P., Guedes, S. D. M., da Costa, J. P., & Kašička, V. (2021) · Nanomaterials · doi:10.3390/nano11051118 · Cited by 64 · see citing works
“In contrast, biological processes characterized by rapid responses to stimulation, those requiring steady and rapid delivery of the stimulant, or those requiring rapid lysis of cells were amenable to transverse delivery of the stimulant [199,202].”
Background
Characterizing the landscape of gene expression variance in humans
Wolf, S. W., Melo, D., Garske, K., Pallares, L. F., Lea, A., & Ayroles, J. (2023) · bioRxiv · doi:10.1101/2022.11.15.516646 · Cited by 49
FGF Signalling in the Self-Renewal of Colon Cancer Organoids
Otte, J., Dizdar, L., Behrens, B., Goering, W., Knoefel, W. T., Wruck, W., Stoecklein, N. H., & Adjaye, J. (2019) · Scientific Reports · doi:10.1038/s41598-019-53907-7 · Cited by 53 · see citing works
Roles of TP53 in determining therapeutic sensitivity, growth, cellular senescence, invasion and metastasis
McCubrey, J. A., Lertpiriyapong, K., Fitzgerald, T. L., Martelli, A. M., Cocco, L., Rakus, D., Gizak, A., Libra, M., Cervello, M., Montalto, G., et al. (2016) · Advances in Biological Regulation · doi:10.1016/j.jbior.2016.10.001 · Cited by 52 · see citing works
What happens at the lesion does not stay at the lesion: Transcription-coupled nucleotide excision repair and the effects of DNA damage on transcription in cis and trans
Geijer, M. E., & Marteijn, J. A. F. (2018) · DNA repair · doi:10.1016/j.dnarep.2018.08.007 · Cited by 60 · see citing works
“IEGs are in general short genes and their expression can be rapidly induced following cellular stress [130].”
Background
Lectins as mitosis stimulating factors: Briefly reviewed
de Carvalho, E. V. M. M., de Oliveira, W. F., Coelho, L. C. B. B., & Correia, M. T. D. S. (2018) · Life Sciences · doi:10.1016/j.lfs.2018.06.003 · Cited by 48 · see citing works
Evolution in chronic cold: varied loss of cellular response to heat in Antarctic notothenioid fish
Bilyk, K. T., Vargas‐Chacoff, L., & Cheng, C. ‐. C. (2018) · BMC Evolutionary Biology · doi:10.1186/s12862-018-1254-6 · Cited by 49 · see citing works
When mRNA translation meets decay
Bicknell, A. A., & Ricci, E. P. (2017) · Biochemical Society Transactions · doi:10.1042/bst20160243 · Cited by 55 · see citing works
Degrons: defining the rules of protein degradation
Zhang, Z., Mena, E. L., Timms, R. T., Koren, I., & Elledge, S. J. (2025) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-025-00870-z · Cited by 57 · see citing works
A mechanism for oxidative damage repair at gene regulatory elements
Ray, S., Abugable, A. A., Parker, J., Liversidge, K., Palminha, N. M., Liao, C., Acosta-Martin, A. E., Souza, C. S., Jurga, M., Sudbery, I., et al. (2022) · Nature · doi:10.1038/s41586-022-05217-8 · Cited by 44 · see citing works
Topoisomerase IIα represses transcription by enforcing promoter-proximal pausing
Herrero-Ruíz, A., Martínez-García, P. M., Terrón-Bautista, J., Millán-Zambrano, G., Lieberman, J., Jimeno-González, S., & Cortés-Ledesma, F. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108977 · Cited by 44 · see citing works
Endogenous retroviruses drive lineage-specific regulatory evolution across primate and rodent placentae.
Sun, M.-A., Wolf, G., Wang, Y., Senft, A. D., Ralls, S., Jin, J.-P., Dunn-Fletcher, C. E., Muglia, L., & Macfarlan, T. (2021) · Molecular biology and evolution · doi:10.1093/molbev/msab223 · Cited by 43 · see citing works
Single-cell RNA sequencing of the retina in a model of retinitis pigmentosa reveals early responses to degeneration in rods and cones
Karademir, D., Todorova, V., Ebner, L. J. A., Samardzija, M., & Grimm, C. (2022) · BMC Biology · doi:10.1186/s12915-022-01280-9 · Cited by 50 · see citing works
“Many are transcription factors that orchestrate cellular responses by regulating downstream targets before they are rapidly inactivated [71].”
Background
Molecular tissue changes in early myocardial ischemia: from pathophysiology to the identification of new diagnostic markers
Aljakna, A., Fracasso, T., & Sabatasso, S. (2018) · Zeitschrift für Rechtsmedizin · doi:10.1007/s00414-017-1750-z · Cited by 42
Production of rAAV by plasmid transfection induces antiviral and inflammatory responses in suspension HEK293 cells
Chung, C.-H., Murphy, C. M., Wingate, V., Pavlicek, J. W., Nakashima, R., Wei, W., Mccarty, D., Rabinowitz, J., & Barton, E. (2023) · Molecular Therapy: Methods & Clinical Development · doi:10.1016/j.omtm.2023.01.002 · Cited by 41 · see citing works
“transient up-regulation of immediate-early genes including EGR1 and FOS/JUN gene families, as well as DUSPs that properly control the MAPK activation.(27,28) The up-regulation of the DUSPs is a negative feedback mechanism to prevent sustained MAPK activation, and several DUSPs have been implicated in down-regulating t…”
Background
Loss of RNF40 Decreases NF-&kgr;B Activity in Colorectal Cancer Cells and Reduces Colitis Burden in Mice
Kosinsky, R., Chua, R., Qui, M., Saul, D., Mehlich, D., Ströbel, P., Schildhaus, H., Wegwitz, F., Faubion, W., & Johnsen, S. (2018) · Journal of Crohn's & Colitis · doi:10.1093/ecco-jcc/jjy165 · Cited by 41 · see citing works
Multiscale modeling of tumor growth and angiogenesis: Evaluation of tumor-targeted therapy
Nivlouei, S. J., Soltani, M., Carvalho, J., Travasso, R. D. M., Salimpour, M. R., & Shirani, E. (2021) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1009081 · Cited by 42 · see citing works
“Fos MSK And RSK [80,81] Myc ERK 1/2 Or ß-Catenin [82,83]”
Background
Dense time-course gene expression profiling of the Drosophila melanogaster innate immune response
Schlamp, F., Delbare, S., Early, A. M., Wells, M. T., Basu, S., & Clark, A. G. (2021) · BMC Genomics · doi:10.1186/s12864-021-07593-3 · Cited by 54 · see citing works
Regulation of stress signaling pathways by protein lipoxidation
Patinen, T., Adinolfi, S., Cortés, C., Härkönen, J., Deen, A. J., & Levonen, A. (2019) · Redox Biology · doi:10.1016/j.redox.2019.101114 · Cited by 39 · see citing works
“as immediate early response 5 (IER5) [97] and multiple heat shock proteins (chaperones) that have various different functions.”
BackgroundInfluential
Histone H2A monoubiquitylation and p38-MAPKs regulate immediate-early gene-like reactivation of latent retrovirus HTLV-1.
Kulkarni, A., Taylor, G., Klose, R. J., Schofield, C., & Bangham, C. (2018) · JCI Insight · doi:10.1172/jci.insight.123196 · Cited by 39 · see citing works
“Most cellular IEG promoters exhibit a balance between the transcriptionally activating histone epigenetic mark H3K4me3 and the repressive H3K27me3 mark (18) and are therefore termed bivalent promoters.”
BackgroundInfluential
Regulation of Latency in the Human T Cell Leukemia Virus, HTLV-1
Bangham, C. R. M., Miura, M., Kulkarni, A., & Matsuoka, M. (2019) · Annual Review of Virology · doi:10.1146/annurev-virology-092818-015501 · Cited by 41 · see citing works
“It is the balance between these counteracting epigenetic marks that decides the activity of the promoter (70).”
Background
The adhesion-GPCR BAI1 shapes dendritic arbors via Bcr-mediated RhoA activation causing late growth arrest
Duman, J. G., Mulherkar, S. A., Tu, Y.-K., Erikson, K., Tzeng, C. P., Mavratsas, V. C., Ho, T. S., & Tolias, K. F. (2019) · eLife · doi:10.7554/elife.47566 · Cited by 32 · see citing works
“What are the steps that connect BAI1/RhoA to growth arrest? Is it due to the effects of RhoA-regulated kinases on the actin and/or microtubule cytoskeleton? This might seem to be the most likely, yet Rho-GTPases also regulate gene expression (Bahrami and Drabløs, 2016) and there are high levels of RhoA in neuronal som…”
Background
Dissecting Neuronal Activation on a Brain-Wide Scale With Immediate Early Genes
Franceschini, A., Costantini, I., Pavone, F. S., & Silvestri, L. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.569517 · Cited by 41 · see citing works
“…(also known as ZiF268), are a class of genes that is activated transiently and rapidly in response to a wide variety of cellular stimuli (Hunt et al., 1988; Sagar et al., 1988; Kaczmarek and Nikolajew, 1990; Hughes et al., 1992; Pinaud, 2004; Terleph and Tremere, 2006; Bahrami and Drabløs, 2016).”
Background
Social defeat stress in adult mice causes alterations in gene expression, alternative splicing, and the epigenetic landscape of H3K4me3 in the prefrontal cortex: An impact of early-life stress
Reshetnikov, V. V., Kisaretova, P. E., Ershov, N., Merkulova, T. I., & Bondar, N. P. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110068 · Cited by 40 · see citing works
Previous Early-life Stress Modifies Acute Corticosterone-induced Synaptic Plasticity in the Medial Prefrontal Cortex of Adolescent Rats
Majcher‐Maślanka, I., Solarz, A., Wędzony, K., & Chocyk, A. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.03.038 · Cited by 35 · see citing works
Mitogen‐activated protein kinase‐activated protein kinase‐2 (MK2) and its role in cell survival, inflammatory signaling, and migration in promoting cancer
Morgan, D., Berggren, K. L., Spiess, C., Smith, H. M., Tejwani, A., Weir, S. J., Lominska, C. E., Thomas, S. M., & Gan, G. N. (2021) · Molecular Carcinogenesis · doi:10.1002/mc.23348 · Cited by 42 · see citing works
“Many of these genes are transcription factors themselves and they activate genes involved in changes to the cell cycle, cell growth, cell differentiation, apoptosis, and the immune response.(134,135) Heidenreich et al.”
Background
Towards Novel Treatments for Schizophrenia: Molecular and Behavioural Signatures of the Psychotropic Agent SEP-363856
Begni, V., Sanson, A., Luoni, A., Sensini, F., Grayson, B., Munni, S., Neill, J., & Riva, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22084119 · Cited by 36 · see citing works
“The 60 min time period was chosen based on previous studies, and since immediate-early genes are rapidly induced [7,52].”
Method
Initiated by CREB: Resolving Gene Regulatory Programs in Learning and Memory
Kaldun, J. C., & Sprecher, S. G. (2019) · BioEssays · doi:10.1002/bies.201900045 · Cited by 49 · see citing works
The effects of cardiac stretch on atrial fibroblasts: analysis of the evidence and potential role in atrial fibrillation
Li, X., García-Elías, A., Benito, B., & Nattel, S. (2021) · Cardiovascular Research · doi:10.1093/cvr/cvab035 · Cited by 39 · see citing works
“Activation of G proteins and kinases activates ERK2 and JNK1 and leads to the phosphorylation of the early response genes c-Jun, c-Fos, and Fra-1.”
Background
Responses of the Differentiated Intestinal Epithelial Cell Line Caco-2 to Infection With the Giardia intestinalis GS Isolate
Ma'ayeh, S., Knörr, L., Sköld, K., Garnham, A., Ansell, B., Jex, A., & Svärd, S. (2018) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2018.00244 · Cited by 35 · see citing works
“Control Primary Response Genes Primary response genes, which include immediate early and delayed genes, play pivotal roles in a wide range of biological processes including differentiation, proliferation, survival, stress, innate and adaptive immune responses, and glucose metabolism (Fowler et al., 2011; Bahrami and D…”
Background
RNA polymerase II pausing in development: orchestrating transcription
Abuhashem, A., Garg, V., & Hadjantonakis, A. (2022) · Open Biology · doi:10.1098/rsob.210220 · Cited by 36 · see citing works
“This mechanism of gene regulation seems plausible given that many transcriptional responses occur within minutes of signal induction [112,113].”
Background
Immediate early genes in social insects: a tool to identify brain regions involved in complex behaviors and molecular processes underlying neuroplasticity
Sommerlandt, F. M. J., Brockmann, A., Rössler, W., & Spaethe, J. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2948-z · Cited by 33 · see citing works
Multivariate Control of Transcript to Protein Variability in Single Mammalian Cells
Popovic, D., Koch, B., Kueblbeck, M., Ellenberg, J., & Pelkmans, L. (2018) · Cell Systems · doi:10.1016/j.cels.2018.09.001 · Cited by 33 · see citing works
IER2-induced senescence drives melanoma invasion through osteopontin
Kyjacová, L., Saup, R., Rönsch, K., Wallbaum, S., Dukowic-Schulze, S., Foss, A., Scherer, S. D., Rothley, M., Neeb, A., Grau, N., et al. (2021) · Oncogene · doi:10.1038/s41388-021-02027-6 · Cited by 32 · see citing works
Sphingosine 1‐phosphate but not Fingolimod protects neurons against excitotoxic cell death by inducing neurotrophic gene expression in astrocytes
Tran, C. L., Heng, B., Teo, J. D., Humphrey, S. J., Qi, Y., Couttas, T. A., Stefen, H., Brettle, M., Fath, T., Guillemin, G., et al. (2019) · Journal of Neurochemistry · doi:10.1111/jnc.14917 · Cited by 32 · see citing works
“Similarly, only JTE significantly reduced JUN phosphorylation at S63 in both U251 cells and primary astrocytes (Figure 5c,d).”
BackgroundMethodInfluential
Chemically induced herbicide tolerance in rice by the safener metcamifen is associated with a phased stress response
Brazier-Hicks, M., Howell, A., Cohn, J., Hawkes, T., Hall, G., Mcindoe, E., & Edwards, R. (2019) · Journal of Experimental Botany · doi:10.1093/jxb/erz438 · Cited by 32
“do not require protein synthesis and so their expression is not affected by translational inhibitors (Bahrami and Drabløs, 2016).”
Background
Targeting nuclear receptor NR4A1–dependent adipocyte progenitor quiescence promotes metabolic adaptation to obesity
Zhang, Y., Alexander Joel Federation, Kim, S., O’Keefe, J., Lun, M., Xiang, D., Brown, J. D., & Steinhauser, M. L. (2018) · Journal of Clinical Investigation · doi:10.1172/jci98353 · Cited by 41 · see citing works
Environmental perturbations lead to extensive directional shifts in RNA processing
Richards, A. L., Watza, D., Findley, A. S., Alazizi, A., Wen, X., Pai, A. A., Piqué-Regi, R., & Luca, F. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006995 · Cited by 31 · see citing works
Visual learning in a virtual reality environment upregulates immediate early gene expression in the mushroom bodies of honey bees
Geng, H., Lafon, G., Avarguès-Weber, A., Buatois, A., Massou, I., & Giurfa, M. (2022) · Communications Biology · doi:10.1038/s42003-022-03075-8 · Cited by 29 · see citing works
Pubertal adversity alters chromatin dynamics and stress circuitry in the pregnant brain
Morrison, K. E., Cole, A. B., Kane, P. J., Meadows, V. E., Thompson, S. M., & Bale, T. L. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0634-y · Cited by 23 · see citing works
Intravenous Infusion of Mesenchymal Stem Cells Alters Motor Cortex Gene Expression in a Rat Model of Acute Spinal Cord Injury
Oshigiri, T., Sasaki, T., Sasaki, M., Kataoka-Sasaki, Y., Nakazaki, M., Oka, S., Morita, T., Hirota, R., Yoshimoto, M., Yamashita, T., et al. (2019) · Journal of Neurotrauma · doi:10.1089/neu.2018.5793 · Cited by 28 · see citing works
Transcriptional and metabolomic characterization of spontaneous metabolic cycles in Mytilus californianus under subtidal conditions.
Gracey, A., & Connor, K. M. (2016) · Marine Genomics · doi:10.1016/j.margen.2016.07.004 · Cited by 28 · see citing works
“…are broadly classified as early genes (Reinke et al., 2013), a class of genes that are activated and transcribed within minutes of various stimuli (Bahrami and Drablos, 2016), 2 apoptosis-inhibiting baculoviral inhibitor of apoptosis (IAP) repeat-containing proteins (BIRC2, BIRC7), and 2 isoforms…”
Background
Direction of epithelial folding defines impact of mechanical forces on epithelial state.
Błoński, S., Aureille, J., Badawi, S., Zaremba, D., Pernet, L., Grichine, A., Fraboulet, S., Korczyk, P., Recho, P., Guilluy, C., et al. (2021) · Developmental Cell · doi:10.1016/j.devcel.2021.11.008 · Cited by 27 · see citing works
Palmitate differentially regulates Spexin, and its receptors Galr2 and Galr3, in GnRH neurons through mechanisms involving PKC, MAPKs, and TLR4.
Wang, L., Tran, A., Lee, J. L., & Belsham, D. (2020) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2020.110991 · Cited by 27 · see citing works
Regulation of Cell Cycle Entry and Exit: A Single Cell Perspective
Coller, H. A. (2020) · Comprehensive physiology · doi:10.1002/j.2040-4603.2020.tb00110.x · Cited by 5 · see citing works
“The transcription factor Myc is also induced as an immediate early gene (18).”
Maternal Exposure to Dietary Selenium Causes Dopaminergic Hyperfunction and Cognitive Impairment in Zebrafish Offspring
Naderi, M., Ferrari, M. C. O., Chivers, D. P., & Niyogi, S. (2018) · Environmental Science & Technology · doi:10.1021/acs.est.8b04768 · Cited by 32 · see citing works
Social support rescues acute stress-induced cognitive impairments by modulating ERK1/2 phosphorylation in adolescent mice
Kim, J., Ko, M. J., Gonzales, E. L., Kang, R. J., Kim, D. G., Kim, Y., Seung, H., Oh, H. A., Eun, P. H., & Shin, C. Y. (2018) · Scientific Reports · doi:10.1038/s41598-018-30524-4 · Cited by 28 · see citing works
Engineered D2R Variants Reveal the Balanced and Biased Contributions of G-Protein and β-Arrestin to Dopamine-Dependent Functions
Rose, S. J., Pack, T., Peterson, S. M., Payne, K., Borrelli, E., & Caron, M. (2018) · Neuropsychopharmacology · doi:10.1038/npp.2017.254 · Cited by 27
Peripheral neuronal activation shapes the microbiome and alters gut physiology
Griffiths, J. A., Yoo, B. B., Thuy-Boun, P. S., Cantu, V., Weldon, K. C., Challis, C., Sweredoski, M. J., Chan, K. Y., Thron, T., Sharon, G., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.113953 · Cited by 37 · see citing works
Cryopreservation of microglia enables single-cell RNA sequencing with minimal effects on disease-related gene expression patterns
Morsey, B., Niu, M., Dyavar, S. R., Fletcher, C. V., Lamberty, B. G., Emanuel, K., Fangmeier, A., & Fox, H. S. (2021) · iScience · doi:10.1016/j.isci.2021.102357 · Cited by 25 · see citing works
Feeling the force from within – new tools and insights into nuclear mechanotransduction
Morival, J. L. P., Hazelwood, A., & Lammerding, J. (2025) · Journal of Cell Science · doi:10.1242/jcs.263615 · Cited by 26 · see citing works
The Fra-1: Novel role in regulating extensive immune cell states and affecting inflammatory diseases
He, Y., Zhou, H., Chen, L., Wang, Y., Xie, W., Xu, Z., Xiong, Y., Feng, Y., Liu, G.-Y., Li, X., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.954744 · Cited by 31 · see citing works
“In cells, AP-1 family members, including Fra-1, belong to immediate early cell genes (48).”
Background
An Adaptive Role for DNA Double-Strand Breaks in Hippocampus-Dependent Learning and Memory
Boutros, S. W., Unni, V. K., & Raber, J. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23158352 · Cited by 29 · see citing works
“Expression of IEGs is cleared relatively quickly, returning to baseline levels within 2–3 h following stimulation [11].”
Background
Genome-Wide Identification, Transcript Profiling and Bioinformatic Analyses of GRAS Transcription Factor Genes in Rice
Dutta, M., Saha, A., Moin, M., & Kirti, P. (2021) · Frontiers in Plant Science · doi:10.3389/fpls.2021.777285 · Cited by 25
β-adrenergic signaling triggers enteric glial reactivity and acute enteric gliosis during surgery
Leven, P., Schneider, R., Schneider, L., Mallesh, S., Berghe, P. V., Sasse, P., Kalff, J. C., & Wehner, S. (2023) · Journal of Neuroinflammation · doi:10.1186/s12974-023-02937-0 · Cited by 24 · see citing works
“Regarding gliosis, we detected an upregulation of Ier5l and Ifrd1 , two genes of the “immediate-early gene” group that regulate cell growth and immune function [57] and include other factors., e.g., Fos , Egr1/2 , Nr4a1/2 , Jun , Atf3, and Fosl , all strongly induced upon IM.”
Background
Rapid Transcriptional Reprogramming Associated With Heat Stress-Induced Unfolded Protein Response in Developing Brassica napus Anthers
Lohani, N., Singh, M. B., & Bhalla, P. (2022) · Frontiers in Plant Science · doi:10.3389/fpls.2022.905674 · Cited by 24
Acute thermal stress elicits interactions between gene expression and alternative splicing in a fish of conservation concern
Thorstensen, M., Turko, A., Heath, D., Jeffries, K., & Pitcher, T. (2022) · bioRxiv · doi:10.1101/2022.02.20.481219 · Cited by 24
“The panel of early response genes represents a positive control of genes we expected would change in expression if the thermal and handling stressors were reflected in a transcriptomic response (Bahrami and Drabløs, 2016; Fowler et al., 2011; Jeffries et al., 2018; Sopinka et al., 2016).”
Blue Light-Induced Gene Expression Alterations in Cultured Neurons Are the Result of Phototoxic Interactions with Neuronal Culture Media
Duke, C. G., Savell, K. E., Tuscher, J., Phillips, R. A., & Day, J. (2019) · eNeuro · doi:10.1523/eneuro.0386-19.2019 · Cited by 24 · see citing works
Glucocorticoids delay RAF-induced senescence promoted by EGR1
Carvalho, C., L'hôte, V., Courbeyrette, R., Kratassiouk, G., Pinna, G., Cintrat, J., Denby-Wilkes, C., Derbois, C., Olaso, R., Deleuze, J., et al. (2019) · Journal of Cell Science · doi:10.1242/jcs.230748 · Cited by 24 · see citing works
“ERK1/2 activates EGR1 transcription by phosphorylating the ELK1 subunit of the SRF transcription factor (Bahrami and Drabløs, 2016).”
Method
Expression of immediate early genes in brain reward circuitries: Differential regulation by psychostimulant and opioid drugs
Bisagno, V., & Cadet, J. L. (2018) · Neurochemistry International · doi:10.1016/j.neuint.2018.12.004 · Cited by 26 · see citing works
Synsepalum dulcificum extracts exhibit cytotoxic activity on human colorectal cancer cells and upregulate c-fos and c-jun early apoptotic gene expression
Seong, J., Oyong, G., & Cabrera, E. (2018) · doi:10.4103/2221-1691.227999 · Cited by 24
“On the other hand, Shyu et al. assumed that upregulation of c-fos and c-jun transcripts and following apoptosis may be due to the subsequent AP-1 formation and its involvement in mitogen-activated protein kinase pathway or sensitization of the cancer cells to the tumor necrosis factor-related apoptosis-inducing ligand…”
BackgroundInfluential
Commonalities and Differences in the Substrates Underlying Consolidation of First- and Second-Order Conditioned Fear
Lay, B. P. P., Westbrook, R. F., Glanzman, D., & Holmes, N. M. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.2966-17.2018 · Cited by 24 · see citing works
“In rodent models, early phases of protein synthesis have been identified with activation of immediate early genes, such as Arc, and through this activation, polymerization of the major cytoskeletal protein, actin (Steward et al., 2014; Bahrami and Drabløs, 2016).”
A bioinformatics approach for identifying potential molecular mechanisms and key genes involved in COVID-19 associated cardiac remodeling
Ceylan, H. (2021) · Gene Reports · doi:10.1016/j.genrep.2021.101246 · Cited by 23 · see citing works
“Immediate early genes (IEGs) are rapidly and transiently activated genes in response to diverse molecular and cellular events (Bahrami and Drabl ø s, 2016).”
A new synthetic antitumor naphthoquinone induces ROS-mediated apoptosis with activation of the JNK and p38 signaling pathways.
de Almeida, P. D., Jobim, G. D. S. B., Ferreira, C. C. D. S., Bernardes, L. R., Dias, R. B., Sales, C. B. S., Valverde, L. D. F., Rocha, C., Soares, M., Bezerra, D., et al. (2021) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2021.109444 · Cited by 23 · see citing works
“FOS gene is related to immediate response and quickly expressed [28], while MAX gene is capable of forming homodimers and heterodimers with family members, which include MAD, MXL1, and MYC, these transcriptionally active dimer can promote cell proliferation as well as apoptosis [29].”
Background

Authors: Bahrami, S., & Drabløs, F.
Affiliations: Norwegian University of Science and Technology (NO)
Corresponding author: Drabløs, Finn
ORCID: Bahrami, Shahram
Drabløs, Finn
Venue: Advances in Biological Regulation
Publisher: Elsevier BV
Published: 2016-09
Volume: 62
Pages: 37-49
ISSN: 2212-4926 (ISSN-L)
DOI: 10.1016/j.jbior.2016.05.001
OpenAlex: W2349918789
Cited by: 465
References: 109
Citations by year: 2026: 49 · 2025: 50 · 2024: 40 · 2023: 50 · 2022: 65 · 2021: 64 · 2020: 42 · 2019: 44 · 2018: 36 · 2017: 20 · 2016: 5
FWCI: 3.17
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by-nc-nd/4.0/ (vor)
Locations: Advances in Biological Regulation (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
Funders: Helse Midt-Norge
Norges Teknisk-Naturvitenskapelige Universitet
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
Keywords: immediate early genes, gene expression regulation, transcription factor activation, MAPK signaling, ERK, signal transduction, enhancers, promoter regulation, stress response, immune response, cell differentiation, cancer
MeSH terms: Actins, Animals, Cell Differentiation, Cell Nucleus, Eukaryotic Cells, Gene Expression Regulation, Humans, Phosphorylation, Promoter Regions, Genetic, Transcription Factors, Signal Transduction, Genes, Immediate-Early, rhoA GTP-Binding Protein, Mitogen-Activated Protein Kinases, Extracellular Signal-Regulated MAP Kinases

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Gene regulation in the immediate-early response process

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