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Abstract:

Cell movement and intercellular signaling occur simultaneously to organize morphogenesis during embryonic development. Cell movement can cause relative positional changes between neighboring cells. When intercellular signals are local such cell mixing may affect signaling, changing the flow of information in developing tissues. Little is known about the effect of cell mixing on intercellular signaling in collective cellular behaviors and methods to quantify its impact are lacking. Here we discuss how to determine the impact of cell mixing on cell signaling drawing an example from vertebrate embryogenesis: the segmentation clock, a collective rhythm of interacting genetic oscillators. We argue that comparing cell mixing and signaling timescales is key to determining the influence of mixing. A signaling timescale can be estimated by combining theoretical models with cell signaling perturbation experiments. A mixing timescale can be obtained by analysis of cell trajectories from live imaging. After comparing cell movement analyses in different experimental settings, we highlight challenges in quantifying cell mixing from embryonic timelapse experiments, especially a reference frame problem due to embryonic motions and shape changes. We propose statistical observables characterizing cell mixing that do not depend on the choice of reference frames. Finally, we consider situations in which both cell mixing and signaling involve multiple timescales, precluding a direct comparison between single characteristic timescales. In such situations, physical models based on observables of cell mixing and signaling can simulate the flow of information in tissues and reveal the impact of observed cell mixing on signaling. © 2017 Japanese Society of Developmental Biologists

Registro:

Documento: Artículo
Título:Determining the impact of cell mixing on signaling during development
Autor:Uriu, K.; Morelli, L.G.
Filiación:Graduate School of Natural Science and Technology, Kanazawa University, Kakuma-machi, Kanazawa, 920-1192, Japan
Instituto de Investigación en Biomedicina de Buenos Aires (IBioBA) – CONICET – Partner Institute of the Max Planck Society, Godoy Cruz 2390, Buenos Aires, C1425FQD, Argentina
Department of Systemic Cell Biology, Max Planck Institute for Molecular Physiology, Otto-Hahn-Str. 11, Dortmund, 44227, Germany
Departamento de Física, FCEyN, UBA, Pabellon 1, Ciudad Universitaria, Buenos Aires, 1428, Argentina
Palabras clave:cell movement; coupled oscillators; Delta-Notch signal; mean squared displacement; synchronization; cell culture; cell mixing; cell motion; cell tracking; embryo development; nonhuman; oscillator; quantitative analysis; Review; signal transduction; theoretical study; zebra fish; animal; biological rhythm; embryo development; human; physiology; signal transduction; theoretical model; Animals; Biological Clocks; Embryonic Development; Humans; Models, Theoretical; Signal Transduction
Año:2017
Volumen:59
Número:5
Página de inicio:351
Página de fin:368
DOI: http://dx.doi.org/10.1111/dgd.12366
Título revista:Development Growth and Differentiation
Título revista abreviado:Dev. Growth Differ.
ISSN:00121592
CODEN:DGDFA
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00121592_v59_n5_p351_Uriu

Referencias:

  • Al-Kofahi, Y., Lassoued, W., Lee, W., Roysam, B., Improved automatic detection and segmentation of cell nuclei in histopathology images (2010) IEEE Trans. Biomed. Eng., 57, pp. 841-852
  • Amat, F., Lemon, W., Mossing, D.P., McDole, K., Wan, Y., Branson, K., Myers, E.W., Keller, P.J., Fast, accurate reconstruction of cell lineages from large-scale fluorescence microscopy data (2014) Nat. Methods, 11, pp. 951-958
  • Angelini, T.E., Hannezo, E., Trepat, X., Marquez, M., Fredberg, J.J., Weitz, D.A., Glass-like dynamics of collective cell migration (2011) Proc. Natl Acad. Sci. USA, 108, pp. 4714-4719
  • Annila, T., Lihavainen, E., Marques, I.J., Williams, D.R., Yli-Harja, O., Ribeiro, A., ZebIAT, an image analysis tool for registering zebrafish embryos and quantifying cancer metastasis (2013) BMC Bioinformatics, 14, p. S5
  • Arboleda-Estudillo, Y., Krieg, M., Stuhmer, J., Licata, N.A., Muller, D.J., Heisenberg, C.P., Movement directionality in collective migration of germ layer progenitors (2010) Curr. Biol., 20, pp. 161-169
  • Ares, S., Morelli, L.G., Jorg, D.J., Oates, A.C., Julicher, F., Collective modes of coupled phase oscillators with delayed coupling (2012) Phys. Rev. Lett., 108, p. 204101
  • Aulehla, A., Wiegraebe, W., Baubet, V., Wahl, M.B., Deng, C., Taketo, M., Lewandoski, M., Pourquie, O., A beta-catenin gradient links the clock and wavefront systems in mouse embryo segmentation (2008) Nat. Cell Biol., 10, pp. 186-193
  • Bajard, L., Morelli, L.G., Ares, S., Pecreaux, J., Julicher, F., Oates, A.C., Wnt-regulated dynamics of positional information in zebrafish somitogenesis (2014) Development, 141, pp. 1381-1391
  • Benazeraf, B., Francois, P., Baker, R.E., Denans, N., Little, C.D., Pourquie, O., A random cell motility gradient downstream of FGF controls elongation of an amniote embryo (2010) Nature, 466, pp. 248-252
  • Bhavna, R., Uriu, K., Valentin, G., Tinevez, J.Y., Oates, A.C., Object segmentation and ground truth in 3D embryonic imaging (2016) PLoS One, 11
  • Buscarino, A., Fortuna, L., Frasca, M., Rizzo, A., Dynamical network interactions in distributed control of robots (2006) Chaos, 16, p. 15116
  • Chen, C., Liu, S., Shi, X.Q., Chate, H., Wu, Y., Weak synchronization and large-scale collective oscillation in dense bacterial suspensions (2017) Nature, 542, pp. 210-214
  • Delaune, E.A., Francois, P., Shih, N.P., Amacher, S.L., Single-cell-resolution imaging of the impact of Notch signaling and mitosis on segmentation clock dynamics (2012) Dev. Cell, 23, pp. 995-1005
  • Delfini, M.C., Dubrulle, J., Malapert, P., Chal, J., Pourquie, O., Control of the segmentation process by graded MAPK/ERK activation in the chick embryo (2005) Proc. Natl Acad. Sci. USA, 102, pp. 11343-11348
  • Dequeant, M.L., Glynn, E., Gaudenz, K., Wahl, M., Chen, J., Mushegian, A., Pourquie, O., A complex oscillating network of signaling genes underlies the mouse segmentation clock (2006) Science, 314, pp. 1595-1598
  • Dieterich, P., Klages, R., Preuss, R., Schwab, A., Anomalous dynamics of cell migration (2008) Proc. Natl Acad. Sci. USA, 105, pp. 459-463
  • Dray, N., Lawton, A., Nandi, A., Julich, D., Emonet, T., Holley, S.A., Cell-fibronectin interactions propel vertebrate trunk elongation via tissue mechanics (2013) Curr. Biol., 23, pp. 1335-1341
  • Faure, E., Savy, T., Rizzi, B., Melani, C., Stasova, O., Fabreges, D., Spir, R., Bourgine, P., A workflow to process 3D+time microscopy images of developing organisms and reconstruct their cell lineage (2016) Nat. Commun., 7, p. 8674
  • Feynman, R.P., Leighton, R.B., Sands, M., (1963) The Feynman Lectures on Physics, 1. , Addison-Wesley, Massachussetts
  • Frasca, M., Buscarino, A., Rizzo, A., Fortuna, L., Boccaletti, S., Synchronization of moving chaotic agents (2008) Phys. Rev. Lett., 100, p. 44102
  • Friedl, P., Gilmour, D., Collective cell migration in morphogenesis, regeneration and cancer (2009) Nat. Rev. Mol. Cell Biol., 10, pp. 445-457
  • Fujiwara, N., Kurths, J., Diaz-Guilera, A., Synchronization in networks of mobile oscillators (2011) Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 83, p. 25101
  • Gail, M.H., Boone, C.W., The locomotion of mouse fibroblasts in tissue culture (1970) Biophys. J., 10, pp. 980-993
  • Garcia, S., Hannezo, E., Elgeti, J., Joanny, J.F., Silberzan, P., Gov, N.S., Physics of active jamming during collective cellular motion in a monolayer (2015) Proc. Natl Acad. Sci. USA, 112, pp. 15314-15319
  • Gardiner, C., (2009) Stochastic Methods, , 4th edn, Springer-Verlag, Berlin
  • Gomez, C., Ozbudak, E.M., Wunderlich, J., Baumann, D., Lewis, J., Pourquie, O., Control of segment number in vertebrate embryos (2008) Nature, 454, pp. 335-339
  • Haga, H., Irahara, C., Kobayashi, R., Nakagaki, T., Kawabata, K., Collective movement of epithelial cells on a collagen gel substrate (2005) Biophys. J., 88, pp. 2250-2256
  • Hanisch, A., Holder, M.V., Choorapoikayil, S., Gajewski, M., Ozbudak, E.M., Lewis, J., The elongation rate of RNA polymerase II in zebrafish and its significance in the somite segmentation clock (2013) Development, 140, pp. 444-453
  • Herrgen, L., Ares, S., Morelli, L.G., Schroter, C., Julicher, F., Oates, A.C., Intercellular coupling regulates the period of the segmentation clock (2010) Curr. Biol., 20, pp. 1244-1253
  • Hester, S.D., Belmonte, J.M., Gens, J.S., Clendenon, S.G., Glazier, J.A., A multi-cell, multi-scale model of vertebrate segmentation and somite formation (2011) PLoS Comput. Biol., 7
  • 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
  • Hubaud, A., Pourquie, O., Signalling dynamics in vertebrate segmentation (2014) Nat. Rev. Mol. Cell Biol., 15, pp. 709-721
  • 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
  • Jörg, D.J., Morelli, L.G., Soroldoni, D., Oates, A.C., Jülicher, F., Continuum theory of gene expression waves during vertebrate segmentation (2015) New J. Phys., 17, p. 93042
  • Kageyama, R., Niwa, Y., Isomura, A., Gonzalez, A., Harima, Y., Oscillatory gene expression and somitogenesis (2012) Wiley Interdiscip. Rev. Dev. Biol., 1, pp. 629-641
  • Keller, P.J., Schmidt, A.D., Wittbrodt, J., Stelzer, E.H., Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy (2008) Science, 322, pp. 1065-1069
  • Krol, A.J., Roellig, D., Dequeant, M.L., Tassy, O., Glynn, E., Hattem, G., Mushegian, A., Pourquie, O., Evolutionary plasticity of segmentation clock networks (2011) Development, 138, pp. 2783-2792
  • Kuramoto, Y., (1984) Chemical Oscillations, Waves, and Turbulence, , Springer-Verlag, Berlin
  • Lawton, A.K., Nandi, A., Stulberg, M.J., Dray, N., Sneddon, M.W., Pontius, W., Emonet, T., Holley, S.A., Regulated tissue fluidity steers zebrafish body elongation (2013) Development, 140, pp. 573-582
  • Levis, D., Pagonabarraga, I., Díaz-Guilera, A., Synchronization in dynamical networks of locally coupled self-propelled oscillators (2017) Phys. Rev. X, 7, p. 11028
  • Lewis, J., Autoinhibition with transcriptional delay: a simple mechanism for the zebrafish somitogenesis oscillator (2003) Curr. Biol., 13, pp. 1398-1408
  • Li, G., Liu, T., Nie, J., Guo, L., Malicki, J., Mara, A., Holley, S.A., Wong, S.T., Detection of blob objects in microscopic zebrafish images based on gradient vector diffusion (2007) Cytometry A, 71, pp. 835-845
  • Li, L., Cox, E.C., Flyvbjerg, H., ‘Dicty dynamics’: Dictyostelium motility as persistent random motion (2011) Phys. Biol., 8, p. 46006
  • Liao, B.K., Jorg, D.J., Oates, A.C., Faster embryonic segmentation through elevated Delta-Notch signalling (2016) Nat. Commun., 7, p. 11861
  • Liu, C., Weaver, D.R., Strogatz, S.H., Reppert, S.M., Cellular construction of a circadian clock: period determination in the suprachiasmatic nuclei (1997) Cell, 91, pp. 855-860
  • Liu, Y.J., Le Berre, M., Lautenschlaeger, F., Maiuri, P., Callan-Jones, A., Heuze, M., Takaki, T., Piel, M., Confinement and low adhesion induce fast amoeboid migration of slow mesenchymal cells (2015) Cell, 160, pp. 659-672
  • Maiuri, P., Rupprecht, J.F., Wieser, S., Ruprecht, V., Benichou, O., Carpi, N., Coppey, M., Voituriez, R., Actin flows mediate a universal coupling between cell speed and cell persistence (2015) Cell, 161, pp. 374-386
  • Manning, A.J., Kimelman, D., Tbx16 and Msgn1 are required to establish directional cell migration of zebrafish mesodermal progenitors (2015) Dev. Biol., 406, pp. 172-185
  • Mara, A., Schroeder, J., Chalouni, C., Holley, S.A., Priming, initiation and synchronization of the segmentation clock by deltaD and deltaC (2007) Nat. Cell Biol., 9, pp. 523-530
  • Marchetti, M.C., Joanny, J.F., Ramaswamy, S., Liverpool, T.B., Prost, J., Rao, M., Simha, R.A., Hydrodynamics of soft active matter (2013) Rev. Mod. Phys., 85, pp. 1143-1189
  • Marshall, W.F., Straight, A., Marko, J.F., Swedlow, J., Dernburg, A., Belmont, A., Murray, A.W., Sedat, J.W., Interphase chromosomes undergo constrained diffusional motion in living cells (1997) Curr. Biol., 7, pp. 930-939
  • 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
  • Morelli, L.G., Ares, S., Herrgen, L., Schroter, C., Julicher, F., Oates, A.C., Delayed coupling theory of vertebrate segmentation (2009) HFSP J., 3, pp. 55-66
  • Morishita, Y., Kuroiwa, A., Suzuki, T., Quantitative analysis of tissue deformation dynamics reveals three characteristic growth modes and globally aligned anisotropic tissue deformation during chick limb development (2015) Development, 142, pp. 1672-1683
  • Nnetu, K.D., Knorr, M., Strehle, D., Zink, M., Käs, J.A., Directed persistent motion maintains sheet integrity during multi-cellular spreading and migration (2012) Soft Matter, 8, p. 6913
  • Norden, C., Young, S., Link, B.A., Harris, W.A., Actomyosin is the main driver of interkinetic nuclear migration in the retina (2009) Cell, 138, pp. 1195-1208
  • Oates, A.C., Morelli, L.G., Ares, S., Patterning embryos with oscillations: structure, function and dynamics of the vertebrate segmentation clock (2012) Development, 139, pp. 625-639
  • Oginuma, M., Moncuquet, P., Xiong, F., Karoly, E., Chal, J., Guevorkian, K., Pourquie, O., A gradient of glycolytic activity coordinates FGF and Wnt signaling during elongation of the body axis in amniote embryos (2017) Dev. Cell, 40, pp. 342-353. , e310
  • Ozbudak, E.M., Lewis, J., Notch signalling synchronizes the zebrafish segmentation clock but is not needed to create somite boundaries (2008) PLoS Genet., 4
  • Peruani, F., Morelli, L.G., Self-propelled particles with fluctuating speed and direction of motion in two dimensions (2007) Phys. Rev. Lett., 99, p. 10602
  • Peruani, F., Deutsch, A., Bar, M., Nonequilibrium clustering of self-propelled rods (2006) Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 74, p. 30904
  • Peruani, F., Nicola, E.M., Morelli, L.G., Mobility induces global synchronization of oscillators in periodic extended systems (2010) New J. Phys., 12, p. 93029
  • Pikovsky, A., Rosenblum, M., Kurths, J., (2001) Synchronization: A Universal Concept in Nonlinear Sciences, , Cambridge University Press, New York
  • Pourquie, O., Vertebrate segmentation: from cyclic gene networks to scoliosis (2011) Cell, 145, pp. 650-663
  • Qu, L., Long, F., Liu, X., Kim, S., Myers, E., Peng, H., Simultaneous recognition and segmentation of cells: application in C. elegans (2011) Bioinformatics, 27, pp. 2895-2902
  • Qu, L., Long, F., Peng, H., 3-D Registration of Biological Images and Models: Registration of microscopic images and its uses in segmentation and annotation (2015) IEEE Signal Process. Mag., 32, pp. 70-77
  • Rafelski, S.M., Keller, L.C., Alberts, J.B., Marshall, W.F., Apparent diffusive motion of centrin foci in living cells: implications for diffusion-based motion in centriole duplication (2011) Phys. Biol., 8, p. 26010
  • Ramaswamy, S., The mechanics and statistics of active matter (2010) Annu. Rev. Condens. Matter Phys., 1, pp. 323-345
  • 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
  • Rieu, J.P., Upadhyaya, A., Glazier, J.A., Ouchi, N.B., Sawada, Y., Diffusion and deformations of single hydra cells in cellular aggregates (2000) Biophys. J., 79, pp. 1903-1914
  • Rorth, P., Collective cell migration (2009) Annu. Rev. Cell Dev. Biol., 25, pp. 407-429
  • Saga, Y., The mechanism of somite formation in mice (2012) Curr. Opin. Genet. Dev., 22, pp. 331-338
  • 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
  • Sbalzarini, I.F., Koumoutsakos, P., Feature point tracking and trajectory analysis for video imaging in cell biology (2005) J. Struct. Biol., 151, pp. 182-195
  • 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 Biol., 10
  • Selmeczi, D., Mosler, S., Hagedorn, P.H., Larsen, N.B., Flyvbjerg, H., Cell motility as persistent random motion: theories from experiments (2005) Biophys. J., 89, pp. 912-931
  • Sepulveda, N., Petitjean, L., Cochet, O., Grasland-Mongrain, E., Silberzan, P., Hakim, V., Collective cell motion in an epithelial sheet can be quantitatively described by a stochastic interacting particle model (2013) PLoS Comput. Biol., 9
  • Shih, N.P., Francois, P., Delaune, E.A., Amacher, S.L., Dynamics of the slowing segmentation clock reveal alternating two-segment periodicity (2015) Development, 142, pp. 1785-1793
  • Shimojo, H., Isomura, A., Ohtsuka, T., Kori, H., Miyachi, H., Kageyama, R., Oscillatory control of Delta-like1 in cell interactions regulates dynamic gene expression and tissue morphogenesis (2016) Genes Dev., 30, pp. 102-116
  • Skufca, J.D., Bollt, E.M., Communication and synchronization in disconnected networks with dynamic topology: moving neighborhood networks (2004) Math. Biosci. Eng., 1, pp. 1-13
  • Soroldoni, D., Jorg, D.J., Morelli, L.G., Richmond, D.L., Schindelin, J., Julicher, F., Oates, A.C., Genetic oscillations. 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., Anderson, 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
  • Stegmaier, J., Otte, J.C., Kobitski, A., Fast segmentation of stained nuclei in terabyte-scale, time resolved 3D microscopy image stacks (2014) PLoS One, 9
  • Stegmaier, J., Amat, F., Lemon, W.C., McDole, K., Wan, Y., Teodoro, G., Mikut, R., Keller, P.J., Real-time three-dimensional cell segmentation in large-scale microscopy data of developing embryos (2016) Dev. Cell, 36, pp. 225-240
  • Steventon, B., Duarte, F., Lagadec, R., Mazan, S., Nicolas, J.F., Hirsinger, E., Species-specific contribution of volumetric growth and tissue convergence to posterior body elongation in vertebrates (2016) Development, 143, pp. 1732-1741
  • Szabo, B., Szollosi, G.J., Gonci, B., Juranyi, Z., Selmeczi, D., Vicsek, T., Phase transition in the collective migration of tissue cells: experiment and model (2006) Phys. Rev. E, 74, p. 61908
  • Szabo, A., Unnep, R., Mehes, E., Twal, W.O., Argraves, W.S., Cao, Y., Czirok, A., Collective cell motion in endothelial monolayers (2010) Phys. Biol., 7, p. 46007
  • Takagi, H., Sato, M.J., Yanagida, T., Ueda, M., Functional analysis of spontaneous cell movement under different physiological conditions (2008) PLoS One, 3
  • Tambe, D.T., Hardin, C.C., Angelini, T.E., Rajendran, K., Park, C.Y., Serra-Picamal, X., Zhou, E.H., Trepat, X., Collective cell guidance by cooperative intercellular forces (2011) Nat. Mater., 10, pp. 469-475
  • Upadhyaya, A., Rieu, J.P., Glazier, J.A., Sawada, Y., Anomalous diffusion and non-Gaussian velocity distribution of Hydra cells in cellular aggregates (2001) Phys. A, 293, pp. 549-558
  • Uriu, K., Genetic oscillators in development (2016) Dev. Growth Differ., 58, pp. 16-30
  • Uriu, K., Morelli, L.G., Collective cell movement promotes synchronization of coupled genetic oscillators (2014) Biophys. J., 107, pp. 514-526
  • Uriu, K., Morishita, Y., Iwasa, Y., Random cell movement promotes synchronization of the segmentation clock (2010) Proc. Natl Acad. Sci. USA, 107, pp. 4979-4984
  • Uriu, K., Ares, S., Oates, A.C., Morelli, L.G., Optimal cellular mobility for synchronization arising from the gradual recovery of intercellular interactions (2012) Phys. Biol., 9, p. 36006
  • Uriu, K., Ares, S., Oates, A.C., Morelli, L.G., Dynamics of mobile coupled phase oscillators (2013) Phys. Rev. E, 87, p. 32911
  • Uriu, K., Morelli, L.G., Oates, A.C., Interplay between intercellular signaling and cell movement in development (2014) Semin. Cell Dev. Biol., 35, pp. 66-72
  • Vedel, S., Tay, S., Johnston, D.M., Bruus, H., Quake, S.R., Migration of cells in a social context (2013) Proc. Natl Acad. Sci. USA, 110, pp. 129-134
  • Vedula, S.R., Leong, M.C., Lai, T.L., Hersen, P., Kabla, A.J., Lim, C.T., Ladoux, B., Emerging modes of collective cell migration induced by geometrical constraints (2012) Proc. Natl Acad. Sci. USA, 109, pp. 12974-12979
  • Vestergaard, C.L., Pedersen, J.N., Mortensen, K.I., Flyvbjerg, H., Estimation of motility parameters from trajectory data (2015) Eur. Phys. J., 224, pp. 1151-1168
  • Vicsek, T., Zafeiris, A., Collective motion (2012) Phys. Rep., 517, pp. 71-140
  • Vicsek, T., Czirok, A., Ben-Jacob, E., Cohen, I.I., Shochet, O., Novel type of phase transition in a system of self-driven particles (1995) Phys. Rev. Lett., 75, pp. 1226-1229
  • Wang, P., Gonzalez, M.C., Hidalgo, C.A., Barabasi, A.L., Understanding the spreading patterns of mobile phone viruses (2009) Science, 324, pp. 1071-1076
  • Webb, A.B., Oates, A.C., Timing by rhythms: daily clocks and developmental rulers (2016) Dev. Growth Differ., 58, pp. 43-58
  • Webb, A.B., Lengyel, I.M., Jorg, D.J., Valentin, G., Julicher, F., Morelli, L.G., Oates, A.C., Persistence, period and precision of autonomous cellular oscillators from the zebrafish segmentation clock (2016) Elife, 5
  • Wright, G.J., Giudicelli, F., Soza-Ried, C., Hanisch, A., Ariza-Mcnaughton, L., Lewis, J., DeltaC and DeltaD interact as Notch ligands in the zebrafish segmentation clock (2011) Development, 138, pp. 2947-2956
  • Wu, P.H., Giri, A., Sun, S.X., Wirtz, D., Three-dimensional cell migration does not follow a random walk (2014) Proc. Natl Acad. Sci. USA, 111, pp. 3949-3954
  • Xiong, F., Tentner, A.R., Huang, P., Gelas, A., Mosaliganti, K.R., Souhait, L., Rannou, N., Megason, S.G., Specified neural progenitors sort to form sharp domains after noisy Shh signaling (2013) Cell, 153, pp. 550-561
  • Yabe, T., Takada, S., Molecular mechanism for cyclic generation of somites: lessons from mice and zebrafish (2016) Dev. Growth Differ., 58, pp. 31-42
  • Yamaguchi, Y., Suzuki, T., Mizoro, Y., Kori, H., Okada, K., Chen, Y., Fustin, J.M., Okamura, H., Mice genetically deficient in vasopressin V1a and V1b receptors are resistant to jet lag (2013) Science, 342, pp. 85-90
  • Zhou, C., Kurths, J., Noise-sustained and controlled synchronization of stirred excitable media by external forcing (2005) New J. Phys., 7, p. 18

Citas:

---------- APA ----------
Uriu, K. & Morelli, L.G. (2017) . Determining the impact of cell mixing on signaling during development. Development Growth and Differentiation, 59(5), 351-368.
http://dx.doi.org/10.1111/dgd.12366
---------- CHICAGO ----------
Uriu, K., Morelli, L.G. "Determining the impact of cell mixing on signaling during development" . Development Growth and Differentiation 59, no. 5 (2017) : 351-368.
http://dx.doi.org/10.1111/dgd.12366
---------- MLA ----------
Uriu, K., Morelli, L.G. "Determining the impact of cell mixing on signaling during development" . Development Growth and Differentiation, vol. 59, no. 5, 2017, pp. 351-368.
http://dx.doi.org/10.1111/dgd.12366
---------- VANCOUVER ----------
Uriu, K., Morelli, L.G. Determining the impact of cell mixing on signaling during development. Dev. Growth Differ. 2017;59(5):351-368.
http://dx.doi.org/10.1111/dgd.12366