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Abstract:

In vertebrate development, the sequential and rhythmic segmentation of the body axis is regulated by a "segmentation clock". This clock is comprised of a population of coordinated oscillating cells that together produce rhythmic gene expression patterns in the embryo. Whether individual cells autonomously maintain oscillations, or whether oscillations depend on signals from neighboring cells is unknown. Using a transgenic zebrafish reporter line for the cyclic transcription factor Her1, we recorded single tailbud cells in vitro. We demonstrate that individual cells can behave as autonomous cellular oscillators. We described the observed variability in cell behavior using a theory of generic oscillators with correlated noise. Single cells have longer periods and lower precision than the tissue, highlighting the role of collective processes in the segmentation clock. Our work reveals a population of cells from the zebrafish segmentation clock that behave as self-sustained, autonomous oscillators with distinctive noisy dynamics. © Webb et al.

Registro:

Documento: Artículo
Título:Persistence, period and precision of autonomous cellular oscillators from the zebrafish segmentation clock
Autor:Webb, A.B.; Lengyel, I.M.; Jörg, D.J.; Valentin, G.; Jülicher, F.; Morelli, L.G.; Oates, A.C.
Filiación:MRC-National Institute for Medical Research, London, United Kingdom
Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
Departamento de Física, FCEyN UBA and IFIBA, CONICET, Buenos Aires, Argentina
Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
Department of Cell and Developmental Biology, University College London, London, United Kingdom
The Francis Crick Institute, Mill Hill Laboratory, London, United Kingdom
Genoway, Lyon, France
Instituto de, Investigación en Biomedicina de Buenos Aires (IBioBA), CONICET - Partner Institute of the Max Planck Society, Buenos Aires, Argentina
Palabras clave:animal cell; Article; circadian rhythm; embryo segmentation; gene expression assay; immunocytochemistry; nonhuman; oscillation; zebra fish; animal; biological rhythm; biosynthesis; cell culture; cell function; embryology; gene expression profiling; gene fusion; physiology; reporter gene; transgenic animal; basic helix loop helix transcription factor; her1 protein, zebrafish; zebrafish protein; Animals; Animals, Genetically Modified; Artificial Gene Fusion; Basic Helix-Loop-Helix Transcription Factors; Biological Clocks; Cell Physiological Phenomena; Cells, Cultured; Gene Expression Profiling; Genes, Reporter; Zebrafish; Zebrafish Proteins
Año:2016
Volumen:5
Número:FEBRUARY2016
DOI: http://dx.doi.org/10.7554/eLife.08438
Título revista:eLife
Título revista abreviado:eLife
ISSN:2050084X
CAS:Basic Helix-Loop-Helix Transcription Factors; her1 protein, zebrafish; Zebrafish Proteins
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_2050084X_v5_nFEBRUARY2016_p_Webb

Referencias:

  • Albeck, J.G., Mills, G.B., Brugge, J.S., Frequency-modulated pulses of ERK activity transmit quantitative proliferation signals (2013) Molecular Cell, 49, pp. 249-261
  • Aoki, K., Kumagai, Y., Sakurai, A., Komatsu, N., Fujita, Y., Shionyu, C., Matsuda, M., Stochastic ERK activation induced by noise and cell-to-cell propagation regulates cell density-dependent proliferation (2013) Molecular Cell, 52, pp. 529-540
  • Ay, A., Holland, J., Sperlea, A., Devakanmalai, G.S., Knierer, S., Sangervasi, S., Stevenson, A., Ozbudak, E.M., Spatial gradients of protein-level time delays set the pace of the traveling segmentation clock waves (2014) Development, 141, pp. 4158-4167
  • Barral, J., Dierkes, K., Lindner, B., Julicher, F., Martin, P., Coupling a sensory hair-cell bundle to cyber clones enhances nonlinear amplification (2010) Proceedings of the National Academy of Sciences of the United States of America, 107, pp. 8079-8084
  • Chang, H.H., Hemberg, M., Barahona, M., Ingber, D.E., Huang, S., Transcriptome-wide noise controls lineage choice in mammalian progenitor cells (2008) Nature, 453, pp. 544-547
  • Cooke, J., Zeeman, E.C., A clock and wavefront model for control of the number of repeated structures during animal morphogenesis (1976) Journal of Theoretical Biology, 58, pp. 455-476
  • Danino, T., Mondragón-Palomino, O., Tsimring, L., Hasty, J., A synchronized quorum of genetic clocks (2010) Nature, 463, pp. 326-330
  • Delaune, E.A., François, P., Shih, N.P., Amacher, S.L., Single-cell-resolution imaging of the impact of notch signaling and mitosis on segmentation clock dynamics (2012) Developmental Cell, 23, pp. 995-1005
  • Dequéant, M.-L., Glynn, E., Gaudenz, K., Wahl, M., Chen, J., Mushegian, A., Pourquié, O., A complex oscillating network of signaling genes underlies the mouse segmentation clock (2006) Science, 314, pp. 1595-1598
  • Diz-Muñoz, A., Krieg, M., Bergert, M., Ibarlucea-Benitez, I., Muller, D.J., Paluch, E., Heisenberg, C.-P., Control of directed cell migration in vivo by membrane-to-cortex attachment (2010) Plos Biology, 8, pp. e1000544
  • Dubrulle, J., McGrew, M.J., Pourquié, O., FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal hox gene activation (2001) Cell, 106, pp. 219-232
  • Garcia-Ojalvo, J., Elowitz, M.B., Strogatz, S.H., Modeling a synthetic multicellular clock: Repressilators coupled by quorum sensing (2004) Proceedings of the National Academy of Sciences of the United States of America, 101, pp. 10955-10960
  • Giudicelli, F., Ozbudak, E.M., Wright, G.J., Lewis, J., Setting the tempo in development: An investigation of the zebrafish somite clock mechanism (2007) Plos Biology, 5, pp. e150
  • Goldbeter, A., Pourquié, O., Modeling the segmentation clock as a network of coupled oscillations in the notch, wnt and FGF signaling pathways (2008) Journal of Theoretical Biology, 252, pp. 574-585
  • Gonze, D., Bernard, S., Waltermann, C., Kramer, A., Herzel, H., Spontaneous synchronization of coupled circadian oscillators (2005) Biophysical Journal, 89, pp. 120-129
  • Gregor, T., Fujimoto, K., Masaki, N., Sawai, S., The onset of collective behavior in social amoebae (2010) Science, 328, pp. 1021-1025
  • Herrgen, L., Ares, S., Morelli, L.G., Schroter, C., Julicher, F., Oates, A.C., Intercellular coupling regulates the period of the segmentation clock (2010) Current Biology, 20, pp. 1244-1253
  • Herzog, E.D., Aton, S.J., Numano, R., Sakaki, Y., Tei, H., Temporal precision in the mammalian circadian system: A reliable clock from less reliable neurons (2004) Journal of Biological Rhythms, 19, pp. 35-46
  • Hirata, H., Yoshiura, S., Ohtsuka, T., Bessho, Y., Harada, T., Yoshikawa, K., Kageyama, R., Oscillatory expression of the bHLH factor Hes1 regulated by a negative feedback loop (2002) Science, 298, pp. 840-843
  • Holley, S.A., Geisler, R., Nusslein-Volhard, C., Control of her1 expression during zebrafish somitogenesis by a delta-dependent oscillator and an independent wave-front activity (2000) Genes & Development, 14, pp. 1678-1690
  • Holley, S.A., Julich, D., Rauch, G.-J., Geisler, R., Nusslein-Volhard, C., Her1 and the notch pathway function within the oscillator mechanism that regulates zebrafish somitogenesis (2002) Development, 129, pp. 1175-1183
  • Horikawa, K., Ishimatsu, K., Yoshimoto, E., Kondo, S., Takeda, H., Noise-resistant and synchronized oscillation of the segmentation clock (2006) Nature, 441, pp. 719-723
  • Huang, S., Non-genetic heterogeneity of cells in development: More than just noise (2009) Development, 136, pp. 3853-3862
  • Huang, H., Lindgren, A., Wu, X., Liu, N.-A., Lin, S., High-throughput screening for bioactive molecules using primary cell culture of transgenic zebrafish embryos (2012) Cell Reports, 2, pp. 695-704
  • Imayoshi, I., Isomura, A., Harima, Y., Kawaguchi, K., Kori, H., Miyachi, H., Fujiwara, T., Kageyama, R., Oscillatory control of factors determining multipotency and fate in mouse neural progenitors (2013) Science, 342, pp. 1203-1208
  • Ishimatsu, K., Takamatsu, A., Takeda, H., Emergence of traveling waves in the zebrafish segmentation clock (2010) Development, 137, pp. 1595-1599
  • Jiang, Y.J., Aerne, B.L., Smithers, L., Haddon, C., Ish-Horowicz, D., Lewis, J., Notch signalling and the synchronization of the somite segmentation clock (2000) Nature, 408, pp. 475-479
  • Krol, A.J., Roellig, D., Dequéant, M.-L., Tassy, O., Glynn, E., Hattem, G., Mushegian, A., Pourquié, O., Evolutionary plasticity of segmentation clock networks (2011) Development, 138, pp. 2783-2792
  • Langenberg, T., Brand, M., Cooper, M.S., Imaging brain development and organogenesis in zebrafish using immobilized embryonic explants (2003) Developmental Dynamics, 228, pp. 464-474
  • Lauschke, V.M., Tsiairis, C.D., François, P., Aulehla, A., Scaling of embryonic patterning based on phase-gradient encoding (2012) Nature, 493, pp. 101-105
  • Leise, T.L., Wang, C.W., Gitis, P.J., Welsh, D.K., Persistent cell-autonomous circadian oscillations in fibroblasts revealed by six-week single-cell imaging of PER2::LUC bioluminescence (2012) Plos One, 7, pp. e33334-e33334
  • Lewis, J., Autoinhibition with transcriptional delay (2003) Current Biology, 13, pp. 1398-1408
  • Maroto, M., Dale, J.K., Dequéant, M.-L., Petit, A.-C., Pourquié, O., Synchronised cycling gene oscillations in presomitic mesoderm cells require cell-cell contact (2005) The International Journal of Developmental Biology, 49, pp. 309-315
  • Martin, B.L., Kimelman, D., Brachyury establishes the embryonic mesodermal progenitor niche (2010) Genes & Development, 24, pp. 2778-2783
  • Martin, B.L., Kimelman, D., Canonical wnt signaling dynamically controls multiple stem cell fate decisions during vertebrate body formation (2012) Developmental Cell, 22, pp. 223-232
  • Masamizu, Y., Ohtsuka, T., Takashima, Y., Nagahara, H., Takenaka, Y., Yoshikawa, K., Okamura, H., Kageyama, R., Real-time imaging of the somite segmentation clock: Revelation of unstable oscillators in the individual presomitic mesoderm cells (2006) Proceedings of the National Academy of Sciences of the United States of America, 103, pp. 1313-1318
  • Matsuda, M., Koga, M., Woltjen, K., Nishida, E., Ebisuya, M., Synthetic lateral inhibition governs cell-type bifurcation with robust ratios (2015) Nature Communications, 6, p. 6195
  • Maître, J.-L., Berthoumieux, H., Krens, S., Salbreux, G., Julicher, F., Paluch, E., Heisenberg, C.-P., Adhesion functions in cell sorting by mechanically coupling the cortices of adhering cells (2012) Science, 338, pp. 253-256
  • Meinhardt, H., Hierarchical inductions of cell states: A model for segmentation in drosophila (1986) Journal of Cell Science, 1986, pp. 357-381
  • Meinhardt, H.H., Gierer, A.A., Pattern formation by local self-activation and lateral inhibition (2000) Bioessays, 22, pp. 753-760
  • Monk, N.A.M., Oscillatory expression of Hes1, p53, and NF-kB driven by transcriptional time delays (2003) Current Biology, 13, pp. 1409-1413
  • Morelli, L., Julicher, F., Precision of genetic oscillators and clocks (2007) Physical Review Letters, 98, pp. 1-4
  • Morelli, L.G., Ares, S., Herrgen, L., Schroter, C., Julicher, F., Oates, A.C., Delayed coupling theory of vertebrate segmentation (2009) HFSP Journal, 3, pp. 55-66
  • Niwa, Y., Masamizu, Y., Liu, T., Nakayama, R., Deng, C.X., Kageyama, R., The initiation and propagation of Hes7 oscillation are cooperatively regulated by fgf and notch signaling in the somite segmentation clock (2007) Developmental Cell, 13, pp. 298-304
  • Oates, A.C., Ho, R.K., Hairy/E(Spl)-related (her) genes are central components of the segmentation oscillator and display redundancy with the Delta/Notch signaling pathway in the formation of anterior segmental boundaries in the zebrafish (2002) Development, 129, pp. 2929-2946
  • Palmeirim, I., Henrique, D., Ish-Horowicz, D., Pourquie, O., Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesis (1997) Cell, 91, pp. 639-648
  • Palmeirim, I., Dubrulle, J., Henrique, D., Ish-Horowicz, D., Pourquié, O., Uncoupling segmentation and somitogenesis in the chick presomitic mesoderm (1998) Developmental Genetics, 23, pp. 77-85
  • Riedel-Kruse, I.H., Muller, C., Oates, A.C., Synchrony dynamics during initiation, failure, and rescue of the segmentation clock (2007) Science, 317, pp. 1911-1915
  • Ruprecht, V., Wieser, S., Callan-Jones, A., Smutny, M., Morita, H., Sako, K., Barone, V., Heisenberg, C.-P., Cortical contractility triggers a stochastic switch to fast amoeboid cell motility (2015) Cell, 160, pp. 673-685
  • Sawada, A., Shinya, M., Jiang, Y.J., Kawakami, A., Kuroiwa, A., Takeda, H., Fgf/MAPK signalling is a crucial positional cue in somite boundary formation (2001) Development, 128, pp. 4873-4880
  • Schroter, C., Herrgen, L., Cardona, A., Brouhard, G.J., Feldman, B., Oates, A.C., Dynamics of zebrafish somitogenesis (2008) Developmental Dynamics, 237, pp. 545-553
  • Schroter, C., Ares, S., Morelli, L.G., Isakova, A., Hens, K., Soroldoni, D., Gajewski, M., Oates, A.C., Topology and dynamics of the zebrafish segmentation clock core circuit (2012) Plos Biology, 10, pp. e1001364
  • Shih, N.P., Francois, P., Delaune, E., Amacher, S.L., Dynamics of the slowing segmentation clock reveal alternating two-segment periodicity (2015) Development, 142, pp. 1785-1793
  • Sigal, A., Milo, R., Cohen, A., Geva-Zatorsky, N., Klein, Y., Liron, Y., Rosenfeld, N., Alon, U., Variability and memory of protein levels in human cells (2006) Nature, 444, pp. 643-646
  • Soroldoni, D., Jorg, D.J., Morelli, L.G., Richmond, D.L., Schindelin, J., Julicher, F., Oates, A.C., A doppler effect in embryonic pattern formation (2014) Science, 345, pp. 222-225
  • Sprinzak, D., Lakhanpal, A., Lebon, L., Santat, L.A., Fontes, M.E., Erson, G.A., Garcia-Ojalvo, J., Elowitz, M.B., Cis- interactions between notch and delta generate mutually exclusive signalling states (2010) Nature, 465, pp. 86-90
  • Strogatz, S.H., (1994) Nonlinear Dynamics and Chaos
  • Suel, G.M., Garcia-Ojalvo, J., Liberman, L.M., Elowitz, M.B., An excitable gene regulatory circuit induces transient cellular differentiation (2006) Nature, 440, pp. 545-550
  • Trofka, A., Schwendinger-Schreck, J., Brend, T., Pontius, W., Emonet, T., Holley, S.A., The Her7 node modulates the network topology of the zebrafish segmentation clock via sequestration of the Hes6 hub (2012) Development, 18
  • Uriu, K., Morishita, Y., Iwasa, Y., Traveling wave formation in vertebrate segmentation (2009) Journal of Theoretical Biology, 257, pp. 385-396
  • Verdugo, A., Rand, R., Hopf bifurcation in a DDE model of gene expression (2008) Communications in Nonlinear Science and Numerical Simulation, 13, pp. 235-242
  • Verdugo, A., Rand, R., Center manifold analysis of a DDE model of gene expression (2008) Communications in Nonlinear Science and Numerical Simulation, 13, pp. 1112-1120
  • Webb, A.B., Angelo, N., Huettner, J.E., Herzog, E.D., Takahashi, I.J.S., Intrinsic, nondeterministic circadian rhythm generation in identified mammalian neurons (2009) Proceedings of the National Academy of Sciences of the United States of America, 106, pp. 16493-16498
  • Webb, A.B., Soroldoni, D., Oswald, A., Schindelin, J., Oates, A.C., Generation of dispersed presomitic mesoderm cell cultures for imaging of the zebrafish segmentation clock in single cells (2014) Journal of Visualized Experiments, pp. 1-8
  • Welsh, D.K., Logothetis, D.E., Meister, M., Reppert, S.M., Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms (1995) Neuron, 14, pp. 697-706
  • Westerfield, M., (2000) The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio Rerio), , 4th edition Eugene: University of Oregon Press
  • Wu, X.P., Eshete, M., Bifurcation analysis for a model of gene expression with delays (2011) Communications in Nonlinear Science and Numerical Simulation, 16, pp. 1073-1088
  • Xu, C., Tabebordbar, M., Iovino, S., Ciarlo, C., Liu, J., Castiglioni, A., Price, E., Zon, L.I., A zebrafish embryo culture system defines factors that promote vertebrate myogenesis across species (2013) Cell, 155, pp. 909-921

Citas:

---------- APA ----------
Webb, A.B., Lengyel, I.M., Jörg, D.J., Valentin, G., Jülicher, F., Morelli, L.G. & Oates, A.C. (2016) . Persistence, period and precision of autonomous cellular oscillators from the zebrafish segmentation clock. eLife, 5(FEBRUARY2016).
http://dx.doi.org/10.7554/eLife.08438
---------- CHICAGO ----------
Webb, A.B., Lengyel, I.M., Jörg, D.J., Valentin, G., Jülicher, F., Morelli, L.G., et al. "Persistence, period and precision of autonomous cellular oscillators from the zebrafish segmentation clock" . eLife 5, no. FEBRUARY2016 (2016).
http://dx.doi.org/10.7554/eLife.08438
---------- MLA ----------
Webb, A.B., Lengyel, I.M., Jörg, D.J., Valentin, G., Jülicher, F., Morelli, L.G., et al. "Persistence, period and precision of autonomous cellular oscillators from the zebrafish segmentation clock" . eLife, vol. 5, no. FEBRUARY2016, 2016.
http://dx.doi.org/10.7554/eLife.08438
---------- VANCOUVER ----------
Webb, A.B., Lengyel, I.M., Jörg, D.J., Valentin, G., Jülicher, F., Morelli, L.G., et al. Persistence, period and precision of autonomous cellular oscillators from the zebrafish segmentation clock. eLife. 2016;5(FEBRUARY2016).
http://dx.doi.org/10.7554/eLife.08438