Transcription factors: from enhancer binding to developmental control

Spitz, François; Furlong, Eileen E. M.

doi:10.1038/nrg3207

Cited by 2,227Genomics and Chromatin DynamicsDevelopmental Biology and Gene RegulationGene Regulatory Network Analysis

Transcription factors: from enhancer binding to developmental control

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Spitz, François, Furlong, Eileen E. M.·2012·Nature Reviews Genetics

DOI 10.1038/nrg3207

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Abstract

Developmental progression is driven by specific spatiotemporal domains of gene expression, which give rise to stereotypically patterned embryos even in the presence of environmental and genetic variation. Views of how transcription factors regulate gene expression are changing owing to recent genome-wide studies of transcription factor binding and RNA expression. Such studies reveal patterns that, at first glance, seem to contrast with the robustness of the developmental processes they encode. Here, we review our current knowledge of transcription factor function from genomic and genetic studies and discuss how different strategies, including extensive cooperative regulation (both direct and indirect), progressive priming of regulatory elements, and the integration of activities from multiple enhancers, confer specificity and robustness to transcriptional regulation during development.

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Transcription factors modulate the expression of multiple downstream targets in intricately coordinated and co-regulated pathways.
“Transcription factors by nature modulate the expression of multiple downstream targets in intricately coordinated and co‐regulated pathways [12, 14].”
From Targeting Microglial Transcriptional Reprogramming as a Therapy Strategy for Alzheimer's Disease (2026) · cites this paper as [14]
Endogenous enhancers contain binding sites for 5-6 transcription factors on average.
“On average, endogenous enhancers contain binding sites for 5–6 TFs1”
From Single-molecule states link transcription factor binding to gene expression (2024) · cites this paper as [1]
TF sequence motifs alone are poorly predictive, as only a small fraction of potential TF binding sites in the genome are typically bound in a cell type where the TF is expressed.
“TF sequence motifs alone are poorly predictive, as only a small fraction of potential TF binding sites in the genome are typically bound in a cell type where the TF is expressed68.”
From Towards a comprehensive catalogue of validated and target-linked human enhancers (2020) · cites this paper as [68]
Enhancers interact with their cognate promoters in 3D space and can be latent, primed, or active.
“They interact with their cognate promoters in 3D space, and can be latent, primed, or active68,69.”
From Towards a comprehensive catalogue of validated and target-linked human enhancers (2020) · cites this paper as [68]
The presence of a motif for an expressed TF does not mean that it is bound, and even if it is, not all binding is functional.
“Furthermore, the presence of a motif for an expressed TF does not mean that it is bound, and even if it is, not all binding is functional68.”
From Towards a comprehensive catalogue of validated and target-linked human enhancers (2020) · cites this paper as [68]

Our present understanding is that enhancers are bound by cell-type-specific TFs, associated with open chromatin, and flanked by histones carrying H3K27ac and/or H3K4me1 modifications.
“Our present understanding is that enhancers are bound by cell-type-specific TFs, are associated with regions of open chromatin, and are flanked by histones carrying H3K27ac and/or H3K4me1 modifications.”
From Towards a comprehensive catalogue of validated and target-linked human enhancers (2020) · cites this paper as [68]
At the DNA level, enhancers represent clusters of binding sites for sequence-specific transcription factors.
“At the DNA level, enhancers represent clusters of binding sites for sequence-specific transcription factors (TFs) (Fig. 1A) (reviewed in [29, 30]).”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [30]
Pioneer factors often must recruit additional non-pioneer sequence-specific transcription factors for efficient enhancer activation.
“Often, pioneer factors must recruit additional non-pioneer sequence-specific TFs for efficient enhancer activation [30, 31].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [30]
The TF collective model proposes that a set of the same transcription factors binds to multiple enhancers but an individual enhancer does not necessarily have the full set of transcription factor binding sites.
“An intermediate model for enhancer grammar known as the “TF collective” proposes that a set of the same TFs binds to multiple enhancers but an individual enhancer does not necessarily have the full set of TF binding sites [30, 91].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [30]
Many enhancers operate via binding with transcription factors to facilitate contact with promoters.
“Many enhancers operate via binding with transcription factors (TFs) to facilitate contact with promoters61.”
From Variant-to-function mapping of late-onset Alzheimer’s disease GWAS signals in human microglial cell models implicates RTFDC1 at the CASS4 locus (2024) · cites this paper as [61]
Transcription factors can bind directly to enhancer elements to modulate target gene expression.
“Since TFs can bind directly to enhancer elements to modulate target gene expression9, measuring their abundance provides critical insight into how these proteins drive gene regulatory states.”
From NEAT-seq: simultaneous profiling of intra-nuclear proteins, chromatin accessibility and gene expression in single cells (2022) · cites this paper as [9]

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Defining transcriptional networks through integrative modeling of mRNA expression and transcription factor binding data
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How different eukaryotic transcriptional activators can cooperate promiscuously
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Gene regulatory logic of dopamine neuron differentiation
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Genome-wide protein–DNA binding dynamics suggest a molecular clutch for transcription factor function
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Temporal Coordination of Gene Networks by Zelda in the Early Drosophila Embryo
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Finding distal regulatory elements in the human genome
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A Temporal Map of Transcription Factor Activity: Mef2 Directly Regulates Target Genes at All Stages of Muscle Development
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Different core promoters possess distinct regulatory activities in the Drosophila embryoPreprint
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Multiple enhancers ensure precision of gap gene-expression patterns in the Drosophila embryo
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Epigenetic switch involved in activation of pioneer factor FOXA1-dependent enhancersPreprint
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A functional screen for sonic hedgehog regulatory elements across a 1 Mb interval identifies long-range ventral forebrain enhancers
Jeong, Y., El-Jaick, K. B., Roessler, E., Muenke, M., & Epstein, D. J. (2006) · Development · doi:10.1242/dev.02239 · Cited by 227 · see citing works
Program-Specific Distribution of a Transcription Factor Dependent on Partner Transcription Factor and MAPK Signaling
Zeitlinger, J., Simon, I., Harbison, C. T., Hannett, N. M., Volkert, T. L., Fink, G. R., & Young, R. A. (2003) · Cell · doi:10.1016/s0092-8674(03)00301-5 · Cited by 224 · see citing works
The role of chromatin accessibility in directing the widespread, overlapping patterns of Drosophila transcription factor binding
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Nucleosome Core Displacement in Vitro via a Metastable Transcription Factor-Nucleosome Complex
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Cell signaling can direct either binary or graded transcriptional responses
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Genomic regulatory blocks underlie extensive microsynteny conservation in insectsPreprint
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Quantitative and predictive model of transcriptional control of the Drosophila melanogaster even skipped gene
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Transcriptional and Nontranscriptional Functions of E2F1 in Response to DNA Damage
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Transcriptional competence and the active marking of tissue-specific enhancers by defined transcription factors in embryonic and induced pluripotent stem cellsPreprint
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Noncooperative Interactions between Transcription Factors and Clustered DNA Binding Sites Enable Graded Transcriptional Responses to Environmental Inputs
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Collaborative Competition Mechanism for Gene Activation In Vivo
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Control of a Genetic Regulatory Network by a Selector Gene
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Computational Models for Neurogenic Gene Expression in the Drosophila Embryo
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Promoter-proximal tethering elements regulate enhancer-promoter specificity in the Drosophila Antennapedia complex
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Direct Response to Notch Activation: Signaling Crosstalk and Incoherent Logic
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Duplications Involving a Conserved Regulatory Element Downstream of BMP2 Are Associated with Brachydactyly Type A2
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Quantitative Models of the Mechanisms That Control Genome-Wide Patterns of Transcription Factor Binding during Early Drosophila Development
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Deletion of long-range regulatory elements upstream of SOX9 causes campomelic dysplasia
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Large-scale analysis of the regulatory architecture of the mouse genome with a transposon-associated sensor
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Structural Rules and Complex Regulatory Circuitry Constrain Expression of a Notch- and EGFR-Regulated Eye Enhancer
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Immunity Regulatory DNAs Share Common Organizational Features in Drosophila
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Opposing Functions of the ETS Factor Family Define Shh Spatial Expression in Limb Buds and Underlie Polydactyly
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The transcription factor Pax5 regulates its target genes by recruiting chromatin‐modifying proteins in committed B cells
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Mouse limb deformity mutations disrupt a global control region within the large regulatory landscape required for Gremlin expressionPreprint
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Multilineage Priming of Enhancer Repertoires Precedes Commitment to the B and Myeloid Cell Lineages in Hematopoietic Progenitors
Mercer, E. M., Lin, Y. C., Benner, C. W., Jhunjhunwala, S., Dutkowski, J., Flores, M., Sigvardsson, M., Ideker, T. E., Glass, C. K., & Murre, C. (2011) · Immunity · doi:10.1016/j.immuni.2011.06.013 · Cited by 139 · see citing works
Shadow enhancers: Frequently asked questions about distributed cis‐regulatory information and enhancer redundancy
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Whole-genome comparison of Leu3 binding in vitro and in vivo reveals the importance of nucleosome occupancy in target site selectionPreprint
Liu, X., Lee, C., Granek, J. A., Clarke, N. D., & Lieb, J. D. (2006) · Genome Research · doi:10.1101/gr.5655606 · Cited by 132 · see citing works
Two distinct auto-regulatory loops operate at the PU.1 locus in B cells and myeloid cells
Leddin, M., Perrod, C., Hoogenkamp, M., Ghani, S., Assi, S., Heinz, S., Wilson, N. K., Follows, G., Schönheit, J., Vockentanz, L., et al. (2011) · Blood · doi:10.1182/blood-2010-08-302976 · Cited by 131 · see citing works
Functional Architecture and Evolution of Transcriptional Elements That Drive Gene Coexpression
Brown, C. D., Johnson, D. S., & Sidow, A. (2007) · Science · doi:10.1126/science.1145893 · Cited by 124 · see citing works
Early chromatin unfolding by RUNX1: a molecular explanation for differential requirements during specification versus maintenance of the hematopoietic gene expression program
Hoogenkamp, M., Lichtinger, M., Krysinska, H., Lancrin, C., Clarke, D., Williamson, A., Mazzarella, L., Ingram, R., Jorgensen, H., Fisher, A., et al. (2009) · Blood · doi:10.1182/blood-2008-11-191890 · Cited by 121 · see citing works
Information display by transcriptional enhancers
Kulkarni, M. M., & Arnosti, D. N. (2003) · Development · doi:10.1242/dev.00890 · Cited by 118 · see citing works
A microduplication of the long range SHH limb regulator (ZRS) is associated with triphalangeal thumb-polysyndactyly syndrome
Klopocki, E., Ott, C.-E., Benatar, N., Ullmann, R., Mundlos, S., & Lehmann, K. (2008) · Journal of Medical Genetics · doi:10.1136/jmg.2007.055699 · Cited by 118 · see citing works
Genome-wide discovery of human heart enhancersPreprint
Narlikar, L., Sakabe, N. J., Blanski, A. A., Arimura, F. E., Westlund, J. M., Nóbrega, M. A., & Ovcharenko, I. (2010) · Genome Research · doi:10.1101/gr.098657.109 · Cited by 117 · see citing works
Duplications of noncoding elements 5′ of SOX9 are associated with brachydactyly-anonychia
Kurth, I., Klopocki, E., Stricker, S., van Oosterwijk, J. G., Vanek, S., Altmann, J., Santos, H. G., van Harssel, J. J. T., de Ravel, T. J. L., Wilkie, A. O. M., et al. (2009) · Nature Genetics · doi:10.1038/ng0809-862 · Cited by 116 · see citing works
Bicoid cooperative DNA binding is critical for embryonic patterning in Drosophila
Lebrecht, D., Foehr, M. L., Smith, E., Lopes, F. J. P., Vanario‐Alonso, C. E., Reinitz, J., Burz, D. S., & Hanes, S. D. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506462102 · Cited by 115 · see citing works
Pioneer factor interactions and unmethylated CpG dinucleotides mark silent tissue-specific enhancers in embryonic stem cells
Xu, J., Pope, S. D., Jazirehi, A. R., Attema, J. L., Papathanasiou, P., Watts, J. A., Zaret, K. S., Weissman, I. L., & Smale, S. T. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704579104 · Cited by 114 · see citing works
Uncovering cis-regulatory sequence requirements for context-specific transcription factor bindingPreprint
Yáñez-Cuna, J. O., Dinh, H. Q., Kvon, E. Z., Shlyueva, D., & Stark, A. (2012) · Genome Research · doi:10.1101/gr.132811.111 · Cited by 113 · see citing works
Transgenic analysis of Hoxd gene regulation during digit development
Gonzalez, F., Duboule, D., & Spitz, F. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.03.020 · Cited by 107 · see citing works
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Non‐DNA‐binding cofactors enhance DNA‐binding specificity of a transcriptional regulatory complex
Siggers, T., Duyzend, M., Reddy, J., Khan, S., & Bulyk, M. L. (2011) · Molecular Systems Biology · doi:10.1038/msb.2011.89 · Cited by 107 · see citing works
Genome-wide ChIP-Seq reveals a dramatic shift in the binding of the transcription factor erythroid Kruppel-like factor during erythrocyte differentiation
Pilon, A. M., Ajay, S. S., Kumar, S. A., Steiner, L. A., Cherukuri, P. F., Wincovitch, S., Anderson, S. M., Mullikin, J. C., Gallagher, P. G., Hardison, R. C., et al. (2011) · Blood · doi:10.1182/blood-2011-05-355107 · Cited by 104 · see citing works
hairy mediates dominant repression in the Drosophila embryo
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A Two-Step, PU.1-Dependent Mechanism for Developmentally Regulated Chromatin Remodeling and Transcription of the c-fms Gene
Krysinska, H., Hoogenkamp, M., Ingram, R., Wilson, N., Tagoh, H., Laslo, P., Singh, H., & Bonifer, C. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.01915-06 · Cited by 102 · see citing works
A chromatin-mediated mechanism for specification of conditional transcription factor targets
Buck, M. J., & Lieb, J. D. (2006) · Nature Genetics · doi:10.1038/ng1917 · Cited by 96 · see citing works
Adventitious changes in long-range gene expression caused by polymorphic structural variation and promoter competition
Lower, K. M., Hughes, J. R., De Gobbi, M., Henderson, S., Viprakasit, V., Fisher, C., Goriely, A., Ayyub, H., Sloane-Stanley, J., Vernimmen, D., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0909331106 · Cited by 92 · see citing works
Temporal ChIP-on-chip reveals Biniou as a universal regulator of the visceral muscle transcriptional networkPreprint
Jakobsen, J. S., Braun, M. M., Astorga, J., Gustafson, E. H., Sandmann, T., Karzynski, M., Carlsson, P., & Furlong, E. E. M. (2007) · Genes & Development · doi:10.1101/gad.437607 · Cited by 91 · see citing works
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A Systematic Analysis of Tinman Function Reveals Eya and JAK-STAT Signaling as Essential Regulators of Muscle Development
Liu, Y.-H., Jakobsen, J. S., Valentin, G., Amarantos, I., Gilmour, D. T., & Furlong, E. E. M. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.01.006 · Cited by 90 · see citing works
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Epigenetic Priming of a Pre-B Cell-Specific Enhancer through Binding of Sox2 and Foxd3 at the ESC Stage
Liber, D., Domaschenz, R., Holmqvist, P.-H., Mazzarella, L., Georgiou, A., Leleu, M., Fisher, A. G., Labosky, P. A., & Dillon, N. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.05.020 · Cited by 90 · see citing works
Nucleosome Disruption by Transcription Factor Binding in Yeast
Morse, R. H. (1993) · Science · doi:10.1126/science.8248805 · Cited by 89 · see citing works
Disperse versus Compact Elements for the Regulation ofruntStripes inDrosophila
Klingler, M., Soong, J., Butler, B., et al. (1996) · Developmental Biology · doi:10.1006/dbio.1996.0146 · Cited by 86 · see citing works
A comparison of in vivo and in vitro DNA‐binding specificities suggests a new model for homeoprotein DNA binding in Drosophila embryos
Carr, A., & Biggin, M. D. (1999) · The EMBO Journal · doi:10.1093/emboj/18.6.1598 · Cited by 84 · see citing works
Comparison of ABF1 and RAP1 in Chromatin Opening and Transactivator Potentiation in the Budding Yeast Saccharomyces cerevisiae
Yarragudi, A., Miyake, T., Li, R., & Morse, R. H. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.20.9152-9164.2004 · Cited by 84 · see citing works
Complexity and organization of DNA-protein interactions in the 5′-regulatory region of an endoderm-specific marker gene in the sea urchin embryo
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Design flexibility in cis-regulatory control of gene expression: Synthetic and comparative evidence
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Consequences of Eukaryotic Enhancer Architecture for Gene Expression Dynamics, Development, and Fitness
Ludwig, M. Z., Manu, Kittler, R., White, K. P., & Kreitman, M. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002364 · Cited by 73 · see citing works
Epigenetic silencing of the c‐fms locus during B‐lymphopoiesis occurs in discrete steps and is reversible
Tagoh, H., Schebesta, A., Lefevre, P., Wilson, N. K., Hume, D. A., Busslinger, M., & Bonifer, C. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600421 · Cited by 72 · see citing works
Bystander gene activation by a locus control region
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Structure and regulation of a complex locus: the cut gene of Drosophila.
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The complex transcription regulatory landscape of our genome: control in three dimensions
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Detection and characterization of silencers and enhancer-blockers in the greater CFTR locusPreprint
Petrykowska, H. M., Vockley, C. M., & Elnitski, L. L. (2008) · Genome Research · doi:10.1101/gr.073817.107 · Cited by 62 · see citing works
Study of FoxA Pioneer Factor at Silent Genes Reveals Rfx-Repressed Enhancer at Cdx2 and a Potential Indicator of Esophageal Adenocarcinoma Development
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Nuclear integration of positive Dpp signals, antagonistic Wg inputs and mesodermal competence factors duringDrosophilavisceral mesoderm induction
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Multiple modes of dorsal‐bHLH transcriptional synergy in the Drosophila embryo.
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Two Chromatin Remodeling Activities Cooperate during Activation of Hormone Responsive Promoters
Vicent, G. P., Zaurin, R., Nacht, A. S., Li, A., Font-Mateu, J., Le Dily, F., Vermeulen, M., Mann, M., & Beato, M. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000567 · Cited by 55 · see citing works
Conservation of enhancer location in divergent insects
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Epistatic relationships reveal the functional organization of yeast transcription factors
Zheng, J., Benschop, J. J., Shales, M., Kemmeren, P., Greenblatt, J., Cagney, G., Holstege, F. C. P., Li, H., & Krogan, N. J. (2010) · Molecular Systems Biology · doi:10.1038/msb.2010.77 · Cited by 52 · see citing works
Combinatorial activation and concentration-dependent repression of the Drosophila even skipped stripe 3+7 enhancer
Struffi, P., Corado, M., Kaplan, L., Yu, D., Rushlow, C. A., & Small, S. (2011) · Development · doi:10.1242/dev.065987 · Cited by 48 · see citing works
Dynamic CRM occupancy reflects a temporal map of developmental progression
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Predicting functionality of protein–DNA interactions by integrating diverse evidence
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Multiple modular promoter elements drive gradedbrinkerexpression in response to the Dpp morphogen gradient
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Conserved enhancer and silencer elements responsible for differential Adh transcription in Drosophila cell lines.
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Non-additive interactions involving two distinct elements mediate sloppy-paired regulation by pair-rule transcription factors
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Combinatorial patterning mechanisms in the Drosophila embryo
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Long-range regulation is a major driving force in maintaining genome integrity
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The bicoid and dorsal morphogens use a similar strategy to make stripes in the Drosophila embryo
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Use of a Drosophila genome‐wide conserved sequence database to identify functionally related cis‐regulatory enhancers
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Accessibility of transcriptionally inactive genes is specifically reduced at homeoprotein-DNA binding sites in Drosophila
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Master Transcription Factors and Mediator Establish Super-Enhancers at Key Cell Identity Genes
Whyte, W. A., Orlando, D. A., Hnisz, D., Abraham, B. J., Lin, C. Y., Kagey, M. H., Rahl, P. B., Lee, T. I., & Young, R. A. (2013) · Cell · doi:10.1016/j.cell.2013.03.035 · Cited by 4,143 · see citing works
Super-enhancers in the control of cell identity and disease
Hnisz, D., Abraham, B. J., Lee, T. I., Lau, A., Saint-André, V., Sigova, A. A., Hoke, H. A., & Young, R. A. (2013) · Cell · doi:10.1016/j.cell.2013.09.053 · Cited by 3,662 · see citing works
The Human Transcription Factors
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Authors: Spitz, F., & Furlong, E. E. M.
Affiliations: European Molecular Biology Laboratory (DE)
Corresponding author: Spitz, François
Furlong, Eileen E. M.
ORCID: Spitz, François
Furlong, Eileen E. M.
Venue: Nature Reviews Genetics
Publisher: Springer Science and Business Media LLC
Published: 2012-08-07
Volume: 13
Issue: 9
Pages: 613-626
ISSN: 1471-0056 (ISSN-L)
1471-0064
DOI: 10.1038/nrg3207
OpenAlex: W2045362835
Semantic Scholar: 915d392561047b606dfce4c293d44be3f1a8508a
Cited by: 2,227
References: 161
Citations by year: 2026: 165 · 2025: 200 · 2024: 221 · 2023: 185 · 2022: 208 · 2021: 186 · 2020: 172 · 2019: 159 · 2018: 154 · 2017: 122 · 2016: 148 · 2015: 114 · 2014: 104 · 2013: 85 · 2012: 2
FWCI: 8.71
Type: journal article
Language: en
Open access: green
zenodo.org
Licence: other-oa
www.springer.com/tdm (tdm)
Locations: Nature Reviews Genetics (publishedVersion)
PubMed (publishedVersion)
Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, other-oa)
Funders: European Commission
Deutsche Forschungsgemeinschaft
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
Keywords: transcription factors, enhancers, developmental gene regulation, enhancer binding, developmental robustness, cooperative regulation, spatiotemporal gene expression, embryonic patterning, transcription factor binding sites
MeSH terms: Animals, Chromatin, Enhancer Elements, Genetic, Humans, Promoter Regions, Genetic, Transcription Factors, Transcription, Genetic, Gene Expression Regulation, Developmental, Mice, Rats

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Transcription factors: from enhancer binding to developmental control

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Integrity signals

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