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Abstract:

Background: Coupled biological oscillators can tick with the same period. How this collective period is established is a key question in understanding biological clocks. We explore this question in the segmentation clock, a population of coupled cellular oscillators in the vertebrate embryo that sets the rhythm of somitogenesis, the morphological segmentation of the body axis. The oscillating cells of the zebrafish segmentation clock are thought to possess noisy autonomous periods, which are synchronized by intercellular coupling through the Delta-Notch pathway. Here we ask whether Delta-Notch coupling additionally influences the collective period of the segmentation clock. Results: Using multiple-embryo time-lapse microscopy, we show that disruption of Delta-Notch intercellular coupling increases the period of zebrafish somitogenesis. Embryonic segment length and the spatial wavelength of oscillating gene expression also increase correspondingly, indicating an increase in the segmentation clock's period. Using a theory based on phase oscillators in which the collective period self-organizes because of time delays in coupling, we estimate the cell-autonomous period, the coupling strength, and the coupling delay from our data. Further supporting the role of coupling delays in the clock, we predict and experimentally confirm an instability resulting from decreased coupling delay time. Conclusions: Synchronization of cells by Delta-Notch coupling regulates the collective period of the segmentation clock. Our identification of the first segmentation clock period mutants is a critical step toward a molecular understanding of temporal control in this system. We propose that collective control of period via delayed coupling may be a general feature of biological clocks. © 2010 Elsevier Ltd. All rights reserved.

Registro:

Documento: Artículo
Título:Intercellular coupling regulates the period of the segmentation clock
Autor:Herrgen, L.; Ares, S.; Morelli, L.G.; Schröter, C.; Jülicher, F.; Oates, A.C.
Filiación:Max Planck Institute for Molecular Cell Biology and Genetics, Pfotenhauerstraße 108, 01307 Dresden, Germany
Max Planck Institute for the Physics of Complex Systems, Nöthnitzer Straße 38, 01187 Dresden, Germany
Departamento de Fisica, FCEyN, UBA, Pabellón i, Ciudad Universitaria, 1428 Buenos Aires, Argentina
Palabras clave:DEVBIO; membrane protein; Notch receptor; protein; signal peptide; animal; article; biological model; biological rhythm; computer simulation; fluorescence microscopy; gene expression regulation; metabolism; morphogenesis; physiology; prenatal development; signal transduction; somite; time; zebra fish; Animals; Biological Clocks; Body Patterning; Computer Simulation; Gene Expression Regulation, Developmental; Intracellular Signaling Peptides and Proteins; Membrane Proteins; Microscopy, Fluorescence; Models, Biological; Receptors, Notch; Signal Transduction; Somites; Time Factors; Zebrafish; Danio rerio; Ixodida; Vertebrata; Danio rerio; Ixodida; Vertebrata
Año:2010
Volumen:20
Número:14
Página de inicio:1244
Página de fin:1253
DOI: http://dx.doi.org/10.1016/j.cub.2010.06.034
Título revista:Current Biology
Título revista abreviado:Curr. Biol.
ISSN:09609822
CODEN:CUBLE
CAS:protein, 67254-75-5; Intracellular Signaling Peptides and Proteins; Membrane Proteins; Receptors, Notch; delta protein
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_09609822_v20_n14_p1244_Herrgen.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_09609822_v20_n14_p1244_Herrgen

Referencias:

  • Winfree, A.T., Biological rhythms and the behavior of populations of coupled oscillators (1967) J. Theor. Biol., 16, pp. 15-42
  • Kuramoto, Y., (1984) Chemical Oscillations, Waves and Turbulence, , Springer Verlag Berlin
  • Taylor, A.F., Tinsley, M.R., Wang, F., Huang, Z., Showalter, K., Dynamical quorum sensing and synchronization in large populations of chemical oscillators (2009) Science, 323, pp. 614-617
  • Walker, T.J., Acoustic synchrony: Two mechanisms in the snowy tree cricket (1969) Science, 166, pp. 891-894
  • Buck, J., Synchronous rhythmic flashing of fireflies. II (1988) Q. Rev. Biol., 63, pp. 265-289
  • Schuster, H.P., Wagner, G., Mutual entrainment of two limit cycle oscillators with time delayed coupling (1989) Progress of Theoretical Physics, 81, pp. 939-945
  • Yeung, S., Strogatz, S., Time delay in the Kuramoto model of coupled oscillators (1999) Phys. Rev. Lett., 82, pp. 648-651
  • Wünsche, H.J., Bauer, S., Kreissl, J., Ushakov, O., Korneyev, N., Henneberger, F., Wille, E., Fischer, I., Synchronization of delay-coupled oscillators: A study of semiconductor lasers (2005) Phys. Rev. Lett., 94, p. 163901
  • Lewis, J., Autoinhibition with transcriptional delay: A simple mechanism for the zebrafish somitogenesis oscillator (2003) Curr. Biol., 13, pp. 1398-1408
  • 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
  • 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) Proc. Natl. Acad. Sci., 103, pp. 1313-1318. , USA
  • Palmeirim, I., Henrique, D., Ish-Horowicz, D., Pourquié, O., Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesis (1997) Cell, 91, pp. 639-648
  • Riedel-Kruse, I.H., Müller, C., Oates, A.C., Synchrony dynamics during initiation, failure, and rescue of the segmentation clock (2007) Science, 317, pp. 1911-1915
  • Schröter, C., Herrgen, L., Cardona, A., Brouhard, G.J., Feldman, B., Oates, A.C., Dynamics of zebrafish somitogenesis (2008) Dev. Dyn., 237, pp. 545-553
  • 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
  • Ozbudak, E.M., Lewis, J., Notch signalling synchronizes the zebrafish segmentation clock but is not needed to create somite boundaries (2008) PLoS Genet., 4, p. 15
  • 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 Biol., 5, p. 150
  • Heuss, S.F., Ndiaye-Lobry, D., Six, E.M., Israël, A., Logeat, F., The intracellular region of Notch ligands Dll1 and Dll3 regulates their trafficking and signaling activity (2008) Proc. Natl. Acad. Sci., 105, pp. 11212-11217. , USA
  • Leier, A., Marquez-Lago, T.T., Burrage, K., Generalized binomial tau-leap method for biochemical kinetics incorporating both delay and intrinsic noise (2008) J. Chem. Phys., 128, p. 205107
  • Morelli, L.G., Ares, S., Herrgen, L., Schröter, C., Jülicher, F., Oates, A.C., Delayed coupling theory of vertebrate segmentation (2009) HFSP J., 3, pp. 55-66
  • Kaern, M., Menzinger, M., Hunding, A., Segmentation and somitogenesis derived from phase dynamics in growing oscillatory media (2000) J. Theor. Biol., 207, pp. 473-493
  • Jaeger, J., Goodwin, B.C., A cellular oscillator model for periodic pattern formation (2001) J. Theor. Biol., 213, pp. 171-181
  • Uriu, K., Morishita, Y., Iwasa, Y., Traveling wave formation in vertebrate segmentation (2009) J. Theor. Biol., 257, pp. 385-396
  • Cinquin, O., Repressor dimerization in the zebrafish somitogenesis clock PLoS Comput. Biol., 3

Citas:

---------- APA ----------
Herrgen, L., Ares, S., Morelli, L.G., Schröter, C., Jülicher, F. & Oates, A.C. (2010) . Intercellular coupling regulates the period of the segmentation clock. Current Biology, 20(14), 1244-1253.
http://dx.doi.org/10.1016/j.cub.2010.06.034
---------- CHICAGO ----------
Herrgen, L., Ares, S., Morelli, L.G., Schröter, C., Jülicher, F., Oates, A.C. "Intercellular coupling regulates the period of the segmentation clock" . Current Biology 20, no. 14 (2010) : 1244-1253.
http://dx.doi.org/10.1016/j.cub.2010.06.034
---------- MLA ----------
Herrgen, L., Ares, S., Morelli, L.G., Schröter, C., Jülicher, F., Oates, A.C. "Intercellular coupling regulates the period of the segmentation clock" . Current Biology, vol. 20, no. 14, 2010, pp. 1244-1253.
http://dx.doi.org/10.1016/j.cub.2010.06.034
---------- VANCOUVER ----------
Herrgen, L., Ares, S., Morelli, L.G., Schröter, C., Jülicher, F., Oates, A.C. Intercellular coupling regulates the period of the segmentation clock. Curr. Biol. 2010;20(14):1244-1253.
http://dx.doi.org/10.1016/j.cub.2010.06.034