Control of Hoxd genes' collinearity during early limb development
Open accessAbstract
Hoxd genes are essential for limb growth and patterning. They are activated following a complex transcriptional regulation, leading to expression domains that are collinear in both space and time. To understand the mechanism(s) underlying collinearity, we produced and analyzed a set of mouse strains containing systematic deletions and duplications within the HoxD cluster. We show that two waves of transcriptional activation, controlled by different mechanisms, generate the observed developmental expression patterns. The first wave is time-dependent, involves the action of opposite regulatory modules, and is essential for the growth and polarity of the limb up to the forearm. The second phase involves a different regulation and is required for the morphogenesis of digits. We propose that these two phases reflect the different phylogenetic histories of proximal versus distal limb structures and discuss the biological relevance of these collinear patterns, particularly for the origin of the anterior-to-posterior limb polarity.
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A second phase of hoxd expression is controlled by distant enhancers 200 kb from the 5' end, required to pattern the autopod region where digits form.
“A second phase of hoxd expression is controlled by other complex distant enhancers located 200kb away from the 5' end of the cluster, which are required to pattern the autopod region of the tetrapod limb where the digits form (Tarchini and Duboule, 2006).”
From Evolution of Gene Regulatory Networks Controlling Body Plan Development (2011) · cites this paper as Tarchini and Duboule, 2006
The Introduction describes a global enhancer region centromeric to the 5′ end of the HoxD cluster that controls expression in digits, and “Two Waves of Hoxd Gene Expression Occur during Forelimb Bud Development” identifies a second wave in the presumptive digit territory. Our copy does not give the claimed 200 kb distance or establish that the enhancers are required to pattern the autopod, rather than to regulate Hoxd expression there. Page numbers are unavailable in the indexed copy. (LLM, conf=0.84)
Experimental — accuracy not yet measuredThe GCR is responsible for graded expression of the five posterior hox genes across the A/P dimension of the autopod.
“This “global control region” (GCR) is responsible for a graded expression of the five posterior hox genes across the A/P dimension of the autopod.”
From Evolution of Gene Regulatory Networks Controlling Body Plan Development (2011) · cites this paper as Tarchini and Duboule, 2006
The ‘Two Waves of Hoxd Gene Expression’ section says the GCR drives expression of five contiguous genes in the presumptive digit domain, which becomes the autopod. The Introduction attributes their anterior–posterior expression asymmetry to the posterior location of Shh signaling; its description of a progressive decrease concerns transcriptional efficiency across the genes, not a GCR-driven gradient across the autopod. Page numbers are unavailable in our copy. (LLM, conf=0.86)
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Chromatin topology and the timing of enhancer function at the HoxD locus
Rodríguez-Carballo, E., Lopez‐Delisle, L., Willemin, A., Beccari, L. L., Gitto, S., Mascrez, B., & Duboule, D. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2015083117 · Cited by 53 · see citing works
Self-citationOn the Formation of Digits and Joints during Limb Development
Hiscock, T. W., Tschopp, P., & Tabin, C. J. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.04.021 · Cited by 57 · see citing works
Atypical relaxation of structural constraints in Hox gene clusters of the green anole lizardPreprint
Di‐Poï, N., Montoya‐Burgos, J. I., & Duboule, D. (2009) · Genome Research · doi:10.1101/gr.087932.108 · Cited by 55 · see citing works
Self-citationChromatin Architectures and Hox Gene Collinearity
Noordermeer, D., & Duboule, D. (2013) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-416027-9.00004-8 · Cited by 54 · see citing works
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Tschopp, P., & Duboule, D. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2010.12.034 · Cited by 53 · see citing works
Self-citationDistinct Roles and Regulations for Hoxd Genes in Metanephric Kidney Development
Di‐Poï, N., Zákány, J., & Duboule, D. (2007) · PLoS Genetics · doi:10.1371/journal.pgen.0030232 · Cited by 51 · see citing works
Self-citationTheoretical and experimental approaches to understand morphogen gradients
Ibañes, M., & Belmonte, J. C. I. (2008) · Molecular Systems Biology · doi:10.1038/msb.2008.14 · Cited by 53 · see citing works
Altered transmission of HOX and apoptotic SNPs identify a potential common pathway for clubfoot
Ester, A. R., Weymouth, K. S., Burt, A., Wise, C. A., Scott, A., Gurnett, C. A., Dobbs, M. B., Blanton, S. H., & Hecht, J. T. (2009) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.33130 · Cited by 52 · see citing works
Tsai, L., Liao, H., Chen, Y., Fang, J., & Chen, C. (2009) · Clinical Genetics · doi:10.1111/j.1399-0004.2008.01147.x · Cited by 50 · see citing works
Huang, B., Trofka, A., Furusawa, A., Norrie, J. L., Rabinowitz, A. H., Vokes, S. A., Taketo, M. M., Zákány, J., & Mackem, S. (2016) · Nature Communications · doi:10.1038/ncomms12903 · Cited by 50 · see citing works
Chapter 6 Global Control Regions and Regulatory Landscapes in Vertebrate Development and Evolution
Spitz, F., & Duboule, D. (2008) · Advances in genetics · doi:10.1016/s0065-2660(07)00006-5 · Cited by 50 · see citing works
Self-citationHoxd and Gli3 interactions modulate digit number in the amniote limb
Sheth, R., Bastida, M. F., & Ros, M. A. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.07.023 · Cited by 47 · see citing works
Interactions between HOXD and Gli3 genes control the limb apical ectodermal ridge via Fgf10
Zákány, J., Zacchetti, G., & Duboule, D. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.03.517 · Cited by 46 · see citing works
Self-citationFerrier, D. E. K. (2016) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2016.00036 · Cited by 46 · see citing works
Anatomic Demarcation of Cells: Genes to Patterns
Chang, H. Y. (2009) · Science · doi:10.1126/science.1175686 · Cited by 45 · see citing works
Ectopic nuclear reorganisation driven by a Hoxb1 transgene transposed into Hoxd
Morey, C., Silva, N. D., Kmita, M., Duboule, D., & Bickmore, W. A. (2008) · Journal of Cell Science · doi:10.1242/jcs.023234 · Cited by 43 · see citing works
Self-citationThe Molecular Regulation of Vertebrate Limb Patterning
Butterfield, N. C., McGlinn, E., & Wicking, C. (2010) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(10)90009-4 · Cited by 42 · see citing works
Brault, V., Pereira, P. L., Duchon, A., & Hérault, Y. (2006) · PLoS Genetics · doi:10.1371/journal.pgen.0020086 · Cited by 42 · see citing works
Integration of the transcriptional networks regulating limb morphogenesis
Rabinowitz, A. H., & Vokes, S. A. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.05.035 · Cited by 40 · see citing works
Insights from sharks: Evolutionary and developmental models of fin development
Cole, N. J., & Currie, P. D. (2007) · Developmental Dynamics · doi:10.1002/dvdy.21268 · Cited by 40 · see citing works
“Self‐regulation,” a new facet of Hox genes' function
Sheth, R., Bastida, M. F., Kmita, M., & Ros, M. A. (2013) · Developmental Dynamics · doi:10.1002/dvdy.24019 · Cited by 40 · see citing works
Sarcopterygian fin ontogeny elucidates the origin of hands with digits
Woltering, J. M., Irisarri, I., Ericsson, R., Joss, J. M. P., Sordino, P., & Meyer, A. (2020) · Science Advances · doi:10.1126/sciadv.abc3510 · Cited by 40 · see citing works
Sonic hedgehog is not a limb morphogen but acts as a trigger to specify all digits in mice
Zhu, J., Patel, R., Trofka, A., Harfe, B. D., & Mackem, S. (2022) · Developmental Cell · doi:10.1016/j.devcel.2022.07.016 · Cited by 40 · see citing works
Characterization of Xenopus digits and regenerated limbs of the froglet
Satoh, A., Endo, T., Abe, M., Yakushiji‐Kaminatsui, N., Ohgo, S., Tamura, K., & Ide, H. (2006) · Developmental Dynamics · doi:10.1002/dvdy.20985 · Cited by 40 · see citing works
Tanaka, M. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.03.007 · Cited by 40 · see citing works
Xu, M., Zhao, G., Lv, X., Liu, G., Wang, L. Y., Hao, D., Wang, J., Liu, D., & Liang, C. (2014) · Molecular and Cellular Biology · doi:10.1128/mcb.00567-14 · Cited by 39 · see citing works
Hox genes regulation in vertebrates
Soshnikova, N. V. (2013) · Developmental Dynamics · doi:10.1002/dvdy.24014 · Cited by 38 · see citing works
New frontiers in the evolution of fin development
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An examination of the Chiropteran HoxD locus from an evolutionary perspective
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Gradients, waves and timers, an overview of limb patterning models
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The origins, scaling and loss of tetrapod digits
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- Authors
- Tarchini, B., & Duboule, D.
- Affiliations
- University of Geneva (CH)
- Corresponding author
- Duboule, Denis
- Venue
- Developmental Cell
- Publisher
- Elsevier BV
- Published
- 2006-01
- Volume
- 10
- Issue
- 1
- Pages
- 93-103
- ISSN
- 1534-5807 (ISSN-L)
- OpenAlex
- W2127678679
- Cited by
- 222
- References
- 35
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 7 · 2023: 6 · 2022: 5 · 2021: 13 · 2020: 10 · 2019: 8 · 2018: 10 · 2017: 12 · 2016: 13 · 2015: 6 · 2014: 13 · 2013: 13 · 2012: 12
- FWCI
- 8.85
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 2754 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Developmental Cell (publishedVersion)
- PubMed (publishedVersion)
- Archive ouverte UNIGE (University of Geneva) (publishedVersion, other-oa)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
- Funders
- National Center of Competence in Research Quantum Science and Technology
- Canton de Genève
- Louis-Jeantet Foundation
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Developmental Biology › Congenital limb and hand anomalies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- Hoxd genes, HoxD cluster, multicollinearity, limb development, transcriptional regulation, gene deletion, mouse mutants
- MeSH terms
- Age Factors, Animals, DNA-Binding Proteins, Embryo, Mammalian, Extremities, Genes, Homeobox, Mice, Transgenic, Models, Biological, Nuclear Proteins, Gene Deletion, In Situ Hybridization, Homeodomain Proteins, Gene Expression Regulation, Developmental, Body Patterning, Mice
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