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Herrgen, L.; Ares, S.; Morelli, L.G.; Schröter, C.; Jülicher, F.; Oates, A.C. "Intercellular coupling regulates the period of the segmentation clock" (2010) Current Biology. 20(14):1254-1258
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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.

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, Ciudad Universitaria, Pabellón I, 1428 Buenos Aires, Argentina
Idioma: Inglés
Palabras clave:DEVBIO; Danio rerio; Ixodida; Vertebrata
Año:2010
Volumen:20
Número:14
Página de inicio:1254
Página de fin:1258
DOI: http://dx.doi.org/10.1016/j.cub.2010.05.071
Título revista:Current Biology
Título revista abreviado:Curr. Biol.
ISSN:09609822
CODEN:CUBLE
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_09609822_v20_n14_p1254_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. USA, 103, pp. 1313-1318
  • 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. USA, 105, pp. 11212-11217
  • 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 (2007) PLoS Comput. Biol., 3, p. 32
  • Tiedemann, H.B., Schneltzer, E., Zeiser, S., Rubio-Aliaga, I., Wurst, W., Beckers, J., Przemeck, G.K., Hrabé De Angelis, M., Cell-based simulation of dynamic expression patterns in the presomitic mesoderm (2007) J. Theor. Biol., 248, pp. 120-129
  • Cooke, J., Zeeman, E.C., A clock and wavefront model for control of the number of repeated structures during animal morphogenesis (1976) J. Theor. Biol., 58, pp. 455-476
  • Cooke, J., The problem of periodic patterns in embryos (1981) Philos. Trans. R. Soc. Lond. B Biol. Sci., 295, pp. 509-524
  • Gomez, C., Ozbudak, E.M., Wunderlich, J., Baumann, D., Lewis, J., Pourquié, O., Control of segment number in vertebrate embryos (2008) Nature, 454, pp. 335-339
  • Herrgen, L., Schröter, C., Bajard, L., Oates, A.C., Multiple embryo time-lapse imaging of zebrafish development (2009) Methods Mol. Biol., 546, pp. 243-254
  • Jülich, D., Hwee Lim, C., Round, J., Nicolaije, C., Schroeder, J., Davies, A., Geisler, R., Holley, Beamter/deltaC and the role of Notch ligands in the zebrafish somite segmentation, hindbrain neurogenesis and hypochord differentiation (2005) Dev. Biol., 286, pp. 391-404. , Tübingen 2000 Screen Consortium S.A
  • Van Eeden, F.J., Granato, M., Schach, U., Brand, M., Furutani-Seiki, M., Haffter, P., Hammerschmidt, M., Kane, D.A., Mutations affecting somite formation and patterning in the zebrafish, Danio rerio (1996) Development, 123, pp. 153-164
  • 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
  • Oates, A.C., Mueller, C., Ho, R.K., Cooperative function of deltaC and her7 in anterior segment formation (2005) Dev. Biol., 280, pp. 133-149
  • Jiang, Y.J., Brand, M., Heisenberg, C.P., Beuchle, D., Furutani-Seiki, M., Kelsh, R.N., Warga, R.M., Hammerschmidt, M., Mutations affecting neurogenesis and brain morphology in the zebrafish, Danio rerio (1996) Development, 123, pp. 205-216
  • Dequéant, M.L., Pourquié, O., Segmental patterning of the vertebrate embryonic axis (2008) Nat. Rev. Genet., 9, pp. 370-382
  • Sawada, A., Fritz, A., Jiang, Y.J., Yamamoto, A., Yamasu, K., Kuroiwa, A., Saga, Y., Takeda, H., Zebrafish Mesp family genes, mesp-a and mesp-b are segmentally expressed in the presomitic mesoderm, and Mesp-b confers the anterior identity to the developing somites (2000) Development, 127, pp. 1691-1702
  • Konopka, R.J., Benzer, S., Clock mutants of Drosophila melanogaster (1971) Proc. Natl. Acad. Sci. USA, 68, pp. 2112-2116
  • Bruce, V.G., Mutants of the biological clock in Chlamydomonas reinhardi (1972) Genetics, 70, pp. 537-548
  • Feldman, J.F., Hoyle, M.N., Isolation of circadian clock mutants of Neurospora crassa (1973) Genetics, 75, pp. 605-613
  • Vitaterna, M.H., King, D.P., Chang, A.M., Kornhauser, J.M., Lowrey, P.L., McDonald, J.D., Dove, W.F., Takahashi, J.S., Mutagenesis and mapping of a mouse gene, Clock, essential for circadian behavior (1994) Science, 264, pp. 719-725
  • Momiji, H., Monk, N.A., Oscillatory Notch-pathway activity in a delay model of neuronal differentiation (2009) Phys. Rev. e Stat. Nonlin. Soft Matter Phys., 80, p. 021930
  • Shimizu, K., Chiba, S., Hosoya, N., Kumano, K., Saito, T., Kurokawa, M., Kanda, Y., Hirai, H., Binding of Delta1, Jagged1, and Jagged2 to Notch2 rapidly induces cleavage, nuclear translocation, and hyperphosphorylation of Notch2 (2000) Mol. Cell. Biol., 20, pp. 6913-6922
  • Itoh, M., Kim, C.H., Palardy, G., Oda, T., Jiang, Y.J., Maust, D., Yeo, S.Y., Ariza-Mcnaughton, L., Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta (2003) Dev. Cell, 4, pp. 67-82
  • Goldbeter, A., Pourquié, O., Modeling the segmentation clock as a network of coupled oscillations in the Notch, Wnt and FGF signaling pathways (2008) J. Theor. Biol., 252, pp. 574-585
  • González, A., Kageyama, R., Hopf bifurcation in the presomitic mesoderm during the mouse segmentation (2009) J. Theor. Biol., 259, pp. 176-189
  • Uriu, K., Morishita, Y., Iwasa, Y., Synchronized oscillation of the segmentation clock gene in vertebrate development (2010) J. Math. Biol., 61, pp. 207-229
  • Aton, S.J., Colwell, C.S., Harmar, A.J., Waschek, J., Herzog, E.D., Vasoactive intestinal polypeptide mediates circadian rhythmicity and synchrony in mammalian clock neurons (2005) Nat. Neurosci., 8, pp. 476-483
  • Renn, S.C., Park, J.H., Rosbash, M., Hall, J.C., Taghert, P.H., A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila (1999) Cell, 99, pp. 791-802
  • Shimojo, H., Ohtsuka, T., Kageyama, R., Oscillations in notch signaling regulate maintenance of neural progenitors (2008) Neuron, 58, pp. 52-64
  • Plikus, M.V., Chuong, C.M., Complex hair cycle domain patterns and regenerative hair waves in living rodents (2008) J. Invest. Dermatol., 128, pp. 1071-1080
  • Westerfield, M., (2000) The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio Rerio), , 4th Edition University of Oregon Press Eugene, OR
  • Holley, S.A., Geisler, R., Nüsslein-Volhard, C., Control of her1 expression during zebrafish somitogenesis by a delta-dependent oscillator and an independent wave-front activity (2000) Genes Dev., 14, pp. 1678-1690
  • Holley, S.A., Jülich, D., Rauch, G.J., Geisler, R., Nüsslein-Volhard, C., Her1 and the notch pathway function within the oscillator mechanism that regulates zebrafish somitogenesis (2002) Development, 129, pp. 1175-1183
  • Brand, M., Heisenberg, C.P., Jiang, Y.J., Beuchle, D., Lun, K., Furutani-Seiki, M., Granato, M., Kane, D.A., Mutations in zebrafish genes affecting the formation of the boundary between midbrain and hindbrain (1996) Development, 123, pp. 179-190
  • Heisenberg, C.P., Brand, M., Jiang, Y.J., Warga, R.M., Beuchle, D., Van Eeden, F.J., Furutani-Seiki, M., Hammerschmidt, M., Genes involved in forebrain development in the zebrafish, Danio rerio (1996) Development, 123, pp. 191-203
  • Grandel, H., Lun, K., Rauch, G.J., Rhinn, M., Piotrowski, T., Houart, C., Sordino, P., Geisler, R., Retinoic acid signalling in the zebrafish embryo is necessary during pre-segmentation stages to pattern the anterior-posterior axis of the CNS and to induce a pectoral fin bud (2002) Development, 129, pp. 2851-2865
  • Zhang, C., Li, Q., Lim, C.H., Qiu, X., Jiang, Y.J., The characterization of zebrafish antimorphic mib alleles reveals that Mib and Mind bomb-2 (Mib2) function redundantly (2007) Dev. Biol., 305, pp. 14-27

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), 1254-1258.
http://dx.doi.org/10.1016/j.cub.2010.05.071
---------- 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) : 1254-1258.
http://dx.doi.org/10.1016/j.cub.2010.05.071
---------- 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. 1254-1258.
http://dx.doi.org/10.1016/j.cub.2010.05.071
---------- 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):1254-1258.
http://dx.doi.org/10.1016/j.cub.2010.05.071