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3. Single-cell transcriptional dynamics in a living vertebrate

Author

Eck, Elizabeth, primary, Moretti, Bruno, additional, Schlomann, Brandon H, additional, Bragantini, Jordão, additional, Lange, Merlin, additional, Zhao, Xiang, additional, VijayKumar, Shruthi, additional, Valentin, Guillaume, additional, Loureiro, Cristina, additional, Soroldoni, Daniele, additional, Royer, Loic Alain, additional, Oates, Andrew C., additional, and Garcia, Hernan H, additional

Published
2024
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4. Nonlinearity arising from noncooperative transcription factor binding enhances negative feedback and promotes genetic oscillations

Author

Lengyel, Iván M., Soroldoni, Daniele, Oates, Andrew C., and Morelli, Luis G.

Subjects
Nonlinear Sciences - Adaptation and Self-Organizing Systems, Physics - Biological Physics, Quantitative Biology - Molecular Networks
Abstract

We study the effects of multiple binding sites in the promoter of a genetic oscillator. We evaluate the regulatory function of a promoter with multiple binding sites in the absence of cooperative binding, and consider different hypotheses for how the number of bound repressors affects transcription rate. Effective Hill exponents of the resulting regulatory functions reveal an increase in the nonlinearity of the feedback with the number of binding sites. We identify optimal configurations that maximize the nonlinearity of the feedback. We use a generic model of a biochemical oscillator to show that this increased nonlinearity is reflected in enhanced oscillations, with larger amplitudes over wider oscillatory ranges. Although the study is motivated by genetic oscillations in the zebrafish segmentation clock, our findings may reveal a general principle for gene regulation., Comment: 11 pages, 8 figures

Published
2014
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9. The roles of Groucho/Tle in left-right asymmetry and Kupffer's vesicle organogenesis

Author

Bajoghli, Baubak, Aghaallaei, Narges, Soroldoni, Daniele, and Czerny, Thomas

Subjects
Developmental biology, Biological sciences
Abstract

Byline: Baubak Bajoghli, Narges Aghaallaei, Daniele Soroldoni, Thomas Czerny Keywords: Medaka; Groucho; Lefty; Nodal; Lrd; Left-right asymmetry; Heart; Wnt signaling; Kupffer's vesicle Abstract: The heart is the first organ to form and function in the vertebrate embryo. Furthermore, differences between the left and right sides of the embryo become first detectable during cardiac development. We observed strong cardiac laterality phenotypes in medaka embryos by manipulating Groucho protein activity. The phenotypes produced by misexpressing Tle4 and the dominant-negative Aes reveal a general effect of these corepressor proteins on left-right (LR) development. With the help of an inducible expression system, we were able to define temporally different phases for these effects. In an early phase during gastrulation, Groucho proteins regulate Brachyury expression in the dorsal forerunner cells, which later gives rise to the Kupffer's vesicle (KV). The interference of endogenous Groucho proteins by misexpression of Aes leads to KVs of reduced size, whereas overexpression of Tle4 results in enlarged KVs. The expression level of the cilia marker Lrd was also affected both positively and negatively from these treatments. In the late phase during somitogenesis, Groucho proteins regulate the asymmetric activities of Nodal and Lefty genes. Altering canonical Wnt signaling produced similar results in late embryos, however, this did not affect KV morphogenesis or Lrd expression in early embryos. Therefore, changes in Kupffer's vesicle morphogenesis and the laterality of visceral organs following alterations in Groucho corepressor levels demonstrate two distinct phases in which Groucho proteins help establish LR asymmetry in medaka fish. Author Affiliation: Institute of Animal Breeding and Genetics, University of Veterinary Medicine, Veterinarplatz 1, A-1210 Vienna, Austria Article History: Received 23 December 2005; Revised 6 November 2006; Accepted 14 November 2006

Published
2007

13. Topology and dynamics of the zebrafish segmentation clock core circuit

Author

Schröter, Christian, Ares, Saúl, Morelli, Luis G., Isakova, Alina, Hens, Korneel, Soroldoni, Daniele, Gajewski, Martin, Jülicher, Frank, Maerkl, Sebastian J., Deplancke, Bart, Oates, Andrew C., and University of Zurich

Subjects
core circuit, Transcription, Genetic, protein antibody, Biochemistry, Substrate Specificity, purl.org/becyt/ford/1 [https], somitogenesis, SX00 SystemsX.ch, 2400 General Immunology and Microbiology, zebra fish, Protein Interaction Mapping, Molecular Cell Biology, Basic Helix-Loop-Helix Transcription Factors, Protein Interaction Maps, SX05 DynamiX, Biology (General), segmentation clock, Promoter Regions, Genetic, Mathematical Computing, Zebrafish, embryonic structures, Feedback, Physiological, her7 gene, messenger RNA, Protein Stability, molecular clock, Gene Expression Regulation, Developmental, 2800 General Neuroscience, protein function, unclassified drug, Phenotype, Somites, messenger RNA synthesis, transcription factor Her1, Synopsis, transcription factor Her6, transcription regulation, transcription factor Her7, Dimerization, her1 gene, CIENCIAS NATURALES Y EXACTAS, SX20 Research, Technology and Development Projects, QH301-705.5, homodimer, transcription factor Her6 antibody, Otras Ciencias Biológicas, animal experiment, embryo, 1100 General Agricultural and Biological Sciences, Molecular dynamics, protein DNA binding, Models, Biological, Article, animal tissue, Ciencias Biológicas, Model Organisms, Biological Clocks, 1300 General Biochemistry, Genetics and Molecular Biology, Two-Hybrid System Techniques, Genetics, Animals, controlled study, mutant, RNA, Messenger, gene, purl.org/becyt/ford/1.6 [https], her6 gene, Biology, Body Patterning, Vertebrata, Danio rerio, nonhuman, embryo segmentation, genetic network, embryo development, Zebrafish Proteins, Repressor Proteins, basic helix loop helix transcription factor, 570 Life sciences, biology, Prediction, Mathematics, Transcription Factors, Developmental Biology
Abstract

During vertebrate embryogenesis, the rhythmic and sequential segmentation of the body axis is regulated by an oscillating genetic network termed the segmentation clock. We describe a new dynamic model for the core pace-making circuit of the zebrafish segmentation clock based on a systematic biochemical investigation of the network's topology and precise measurements of somitogenesis dynamics in novel genetic mutants. We show that the core pace-making circuit consists of two distinct negative feedback loops, one with Her1 homodimers and the other with Her7:Hes6 heterodimers, operating in parallel. To explain the observed single and double mutant phenotypes of her1, her7, and hes6 mutant embryos in our dynamic model, we postulate that the availability and effective stability of the dimers with DNA binding activity is controlled in a "dimer cloud" that contains all possible dimeric combinations between the three factors. This feature of our model predicts that Hes6 protein levels should oscillate despite constant hes6 mRNA production, which we confirm experimentally using novel Hes6 antibodies. The control of the circuit's dynamics by a population of dimers with and without DNA binding activity is a new principle for the segmentation clock and may be relevant to other biological clocks and transcriptional regulatory networks. © 2012 Schröter et al. Fil: Schroter, Christian. University of Cambridge; Estados Unidos Fil: Ares, Saúl. Max Planck Institute For The Physics Of Complex Systems; Alemania Fil: Morelli, Luis Guillermo. Universidad de Buenos Aires; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Física de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Física de Buenos Aires; Argentina Fil: Isakova, Alina. Ecole Polytechnique Federale de Lausanne; Francia Fil: Hens, Korneel. Ecole Polytechnique Federale de Lausanne; Francia Fil: Soroldoni, Daniele. Max Planck Institute Of Molecular Cell Biology And Genetics; Alemania Fil: Gajewski, Martin. Universitat zu Köln; Alemania Fil: Jülicher, Frank. Max Planck Institute For The Physics Of Complex Systems; Alemania Fil: Maerkl, Sebastian J.. Ecole Polytechnique Federale de Lausanne; Francia Fil: Deplancke, Bart. Ecole Polytechnique Federale de Lausanne; Francia Fil: Oates, Andrew C.. Max Planck Institute Of Molecular Cell Biology And Genetics; Alemania

Published
2016
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14. Continuum theory of gene expression waves during vertebrate segmentation

Author

Jörg, David J, Morelli, Luis Guillermo, Soroldoni, Daniele, Oates, Andrew C., and Jülicher, Frank

Subjects
Paper, EMBRYONIC DEVELOPMENT, 05.45.Xt, BIOLOGICAL PHYSICS, Ciencias Físicas, morphogenesis, purl.org/becyt/ford/1.3 [https], 87.18.Hf, 82.39.Rt, coupled oscillators, purl.org/becyt/ford/1 [https], Astronomía, pattern formation, 87.17.Pq, PATTERNING, GENE EXPRESSION WAVES, CIENCIAS NATURALES Y EXACTAS
Abstract

The segmentation of the vertebrate body plan during embryonic development is a rhythmic and sequential process governed by genetic oscillations. These genetic oscillations give rise to traveling waves of gene expression in the segmenting tissue. Here we present a minimal continuum theory of vertebrate segmentation that captures the key principles governing the dynamic patterns of gene expression including the effects of shortening of the oscillating tissue. We show that our theory can quantitatively account for the key features of segmentation observed in zebrafish, in particular the shape of the wave patterns, the period of segmentation and the segment length as a function of time. Fil: Jörg, David J. Max Planck Institute for the Physics of Complex Systems; Alemania Fil: Morelli, Luis Guillermo. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Física de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Física de Buenos Aires; Argentina Fil: Soroldoni, Daniele. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Física de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Física de Buenos Aires; Argentina Fil: Oates, Andrew C.. Francis Crick Institute, Mill Hill Laboratory; Alemania Fil: Jülicher, Frank. Max Planck Institute for the Physics of Complex Systems; Alemania

Published
2015
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20. Topology and Dynamics of the Zebrafish Segmentation Clock Core Circuit

Author

Schröter, Christian, Ares, Saúl, Morelli, Luis G, Isakova, Alina, Hens, Korneel, Soroldoni, Daniele, Gajewski, Martin, Jülicher, Frank, Maerkl, Sebastian J, Deplancke, Bart, Oates, Andrew C, Schröter, Christian, Ares, Saúl, Morelli, Luis G, Isakova, Alina, Hens, Korneel, Soroldoni, Daniele, Gajewski, Martin, Jülicher, Frank, Maerkl, Sebastian J, Deplancke, Bart, and Oates, Andrew C

Abstract

During vertebrate embryogenesis, the rhythmic and sequential segmentation of the body axis is regulated by an oscillating genetic network termed the segmentation clock. We describe a new dynamic model for the core pace-making circuit of the zebrafish segmentation clock based on a systematic biochemical investigation of the network’s topology and precise measurements of somitogenesis dynamics in novel genetic mutants. We show that the core pace-making circuit consists of two distinct negative feedback loops, one with Her1 homodimers and the other with Her7:Hes6 heterodimers, operating in parallel. To explain the observed single and double mutant phenotypes of her1, her7, and hes6 mutant embryos in our dynamic model, we postulate that the availability and effective stability of the dimers with DNA binding activity is controlled in a "dimer cloud" that contains all possible dimeric combinations between the three factors. This feature of our model predicts that Hes6 protein levels should oscillate despite constant hes6 mRNA production, which we confirm experimentally using novel Hes6 antibodies. The control of the circuit’s dynamics by a population of dimers with and without DNA binding activity is a new principle for the segmentation clock and may be relevant to other biological clocks and transcriptional regulatory networks.

Published
2012

21. Topology and Dynamics of the Zebrafish Segmentation Clock Core Circuit

Author

Schröter, Christian, primary, Ares, Saúl, additional, Morelli, Luis G., additional, Isakova, Alina, additional, Hens, Korneel, additional, Soroldoni, Daniele, additional, Gajewski, Martin, additional, Jülicher, Frank, additional, Maerkl, Sebastian J., additional, Deplancke, Bart, additional, and Oates, Andrew C., additional

Published
2012
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25. Single-cell transcriptional dynamics in a living vertebrate.

Author

Eck E, Moretti B, Schlomann BH, Bragantini J, Lange M, Zhao X, VijayKumar S, Valentin G, Loureiro C, Soroldoni D, Royer LA, Oates AC, and Garcia HG

Abstract

The ability to quantify transcriptional dynamics in individual cells via live imaging has revolutionized our understanding of gene regulation. However, such measurements are lacking in the context of vertebrate embryos. We addressed this deficit by applying MS2-MCP mRNA labeling to the quantification of transcription in zebrafish, a model vertebrate. We developed a platform of transgenic organisms, light sheet fluorescence microscopy, and optimized image analysis that enables visualization and quantification of MS2 reporters. We used these tools to obtain the first single-cell, real-time measurements of transcriptional dynamics of the segmentation clock. Our measurements challenge the traditional view of smooth clock oscillations and instead suggest a model of discrete transcriptional bursts that are organized in space and time. Together, these results highlight how measuring single-cell transcriptional activity can reveal unexpected features of gene regulation and how this data can fuel the dialogue between theory and experiment.

Published
2024
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26. Simple and efficient transgenesis with meganuclease constructs in zebrafish.

Author

Soroldoni D, Hogan BM, and Oates AC

Subjects
Animals, DNA genetics, DNA metabolism, Deoxyribonucleases, Type II Site-Specific administration & dosage, Deoxyribonucleases, Type II Site-Specific metabolism, Female, Genes, Reporter, Genetic Engineering methods, Germ-Line Mutation, Green Fluorescent Proteins, Male, Microinjections, Saccharomyces cerevisiae Proteins administration & dosage, Saccharomyces cerevisiae Proteins metabolism, Zebrafish embryology, Zebrafish metabolism, Deoxyribonucleases, Type II Site-Specific genetics, Gene Transfer Techniques, Saccharomyces cerevisiae Proteins genetics, Zebrafish genetics
Abstract

In the past, microinjection of plasmid DNA into early embryos represented the state of the art to generate transgenic zebrafish. However, this approach suffers significant drawbacks (mosaic distribution of the injected transgene, late transgene integration at high copy numbers, low transgenesis frequency), making the generation of transgenic lines a laborious task. Coinjection of I-SceI meganuclease with a reporter construct flanked by I-SceI sites overcomes these problems by earlier transgene integration into the host genome. Here, we provide an optimized protocol for I-SceI meganuclease-mediated transgenesis in zebrafish. This simple protocol provides a reliable method to transiently test tissue-specific reporter expression of meganuclease constructs in injected embryos (F0). Furthermore, it substantially facilitates the generation of multiple stable transgenic lines increasing transgenesis frequencies up to 45%, compared with 5% without I-SceI. The reliable reporter activity in F0 and the improved transgenesis frequency make this protocol a powerful tool for use in gain- and loss-of-function, cell tracing, and cell labeling experiments.

Published
2009
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