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Abstract:

The segmentation clock is an oscillating genetic network thought to govern the rhythmic and sequential subdivision of the elongating body axis of the vertebrate embryo into somites: the precursors of the segmented vertebral column. Understanding how the rhythmic signal arises, how it achieves precision and how it patterns the embryo remain challenging issues. Recent work has provided evidence of how the period of the segmentation clock is regulated and how this affects the anatomy of the embryo. The ongoing development of realtime clock reporters and mathematical models promise novel insight into the dynamic behavior of the clock. © 2012. Published by The Company of Biologists Ltd.

Registro:

Documento: Artículo
Título:Patterning embryos with oscillations: Structure, function and dynamics of the vertebrate segmentation clock
Autor:Oates, A.C.; Morelli, L.G.; Ares, S.
Filiación:Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, 01307 Dresden, Germany
CONICET, Departamento de Fisica, FCEyN, UBA, Pabellón I, Ciudad Universitaria, Buenos Aires, Argentina
Max Planck Institute for the Physics of Complex Systems, Nöthnitzer Strasse 38, 01187 Dresden, Germany
Grupo Interdisciplinar de Sistemas Complejos (GISC), Spain
Logic of Genomic Systems Laboratory, Centro Nacional de Biotechnología - CSIC, Calle Darwin 3, 28049 Madrid, Spain
Palabras clave:Gradient; Modeling; Negative feedback; Oscillator; Signaling; Somitogenesis; Notch receptor; Wnt protein; anatomy; biological rhythm; cell cycle arrest; cell synchronization; embryo segmentation; gene expression; gene mutation; mathematical model; molecular dynamics; molecular genetics; molecular mechanics; nonhuman; oscillation; periodicity; priority journal; review; signal transduction; somite; steady state; Animals; Biological Clocks; Biological Evolution; Body Patterning; CLOCK Proteins; Embryonic Development; Gene Expression Regulation, Developmental; Models, Theoretical; Receptors, Notch; Receptors, Opioid, delta; Signal Transduction; Somites; Vertebrates; Wnt Proteins; Vertebrata
Año:2012
Volumen:139
Número:4
Página de inicio:625
Página de fin:639
DOI: http://dx.doi.org/10.1242/dev.063735
Título revista:Development
Título revista abreviado:Development (Cambridge)
ISSN:09501991
CODEN:DEVPE
CAS:CLOCK Proteins, 2.3.1.48; Receptors, Notch; Receptors, Opioid, delta; Wnt Proteins
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_09501991_v139_n4_p625_Oates

Referencias:

  • Al-Mutairi, M.S., Cadalbert, L.C., McGachy, H.A., Shweash, M., Schroeder, J., Kurnik, M., Sloss, C.M., Plevin, R., MAP kinase phosphatase-2 plays a critical role in response to infection by Leishmania mexicana (2010) PLoS Pathog, 6, p. 1001192
  • Aoyama, H., Asamoto, K., The developmental fate of the rostral/caudal half of a somite for vertebra and rib formation: Experimental confirmation of the resegmentation theory using chick-quail chimeras (2000) Mech. Dev, 99, pp. 71-82
  • Aulehla, A., Johnson, R.L., Dynamic expression of lunatic fringe suggests a link between notch signaling and an autonomous cellular oscillator driving somite segmentation (1999) Dev. Biol, 207, pp. 49-61
  • Aulehla, A., Pourquié, O., Signaling gradients during paraxial mesoderm development (2010) Cold Spring Harb. Perspect. Biol, 2, p. 000869
  • Aulehla, A., Wehrle, C., Brand-Saberi, B., Kemler, R., Gossler, A., Kanzler, B., Herrmann, B.G., Wnt3a plays a major role in the segmentation clock controlling somitogenesis (2003) Dev. Cell, 4, pp. 395-406
  • Aulehla, A., Wiegraebe, W., Baubet, V., Wahl, M.B., Deng, C., Taketo, M., Lewandoski, M., Pourquié, O., A beta-catenin gradient links the clock and wavefront systems in mouse embryo segmentation (2008) Nat. Cell Biol, 10, pp. 186-193
  • Bessho, Y., Sakata, R., Komatsu, S., Shiota, K., Yamada, S., Kageyama, R., Dynamic expression and essential functions of Hes7 in somite segmentation (2001) Genes Dev, 15, pp. 2642-2647
  • Bessho, Y., Hirata, H., Masamizu, Y., Kageyama, R., Periodic repression by the bHLH factor Hes7 is an essential mechanism for the somite segmentation clock (2003) Genes Dev, 17, pp. 1451-1456
  • Carver, E.A., Jiang, R., Lan, Y., Oram, K.F., Gridley, T., The mouse snail gene encodes a key regulator of the epithelial-mesenchymal transition (2001) Mol. Cell. Biol, 21, pp. 8184-8188
  • Chen, J., Kang, L., Zhang, N., Negative feedback loop formed by Lunatic fringe and Hes7 controls their oscillatory expression during somitogenesis (2005) Genesis, 43, pp. 196-204
  • Chipman, A.D., Akam, M., The segmentation cascade in the centipede Strigamia maritima: Involvement of the Notch pathway and pair-rule gene homologues (2008) Dev. Biol, 319, pp. 160-169
  • Christ, B., Scaal, M., Formation and differentiation of avian somite derivatives (2008) Adv. Exp. Med. Biol, 638, pp. 1-41
  • Conlon, R.A., Reaume, A.G., Rossant, J., Notch1 is required for the coordinate segmentation of somites (1995) Development, 121, pp. 1533-1545
  • Cooke, J., The problem of periodic patterns in embryos (1981) Philos. Trans. R. Soc. Lond, 295, pp. 509-524
  • 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
  • Dahmann, C., Oates, A.C., Brand, M., Boundary formation and maintenance in tissue development (2011) Nat. Rev. Genet, 12, pp. 43-55
  • Dale, J.K., Maroto, M., Dequeant, M.L., Malapert, P., McGrew, M., Pourquié, O., Periodic notch inhibition by lunatic fringe underlies the chick segmentation clock (2003) Nature, 421, pp. 275-278
  • Dale, J.K., Malapert, P., Chal, J., Vilhais-Neto, G., Maroto, M., Johnson, T., Jayasinghe, S., Pourquié, O., Oscillations of the snail genes in the presomitic mesoderm coordinate segmental patterning and morphogenesis in vertebrate somitogenesis (2006) Dev. Cell, 10, pp. 355-366
  • Damen, W.G., Evolutionary conservation and divergence of the segmentation process in arthropods (2007) Dev. Dyn, 236, pp. 1379-1391
  • Dequeant, 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
  • del Diez, C.R., Olivera-Martinez, I., Goriely, A., Gale, E., Maden, M., Storey, K., Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension (2003) Neuron, 40, pp. 65-79
  • Dubrulle, J., fgf8 mRNA decay establishes a gradient that couples axial elongation to patterning in the vertebrate embryo (2004) Nature, 427, pp. 419-422
  • 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
  • Dunwoodie, S.L., Clements, M., Sparrow, D.B., Sa, X., Conlon, R.A., Beddington, R.S., Axial skeletal defects caused by mutation in the spondylocostal dysplasia/pudgy gene Dll3 are associated with disruption of the segmentation clock within the presomitic mesoderm (2002) Development, 129, pp. 1795-1806
  • Elmasri, H., Winkler, C., Liedtke, D., Sasado, T., Morinaga, C., Suwa, H., Niwa, K., Yasuoka, A., Mutations affecting somite formation in the Medaka (Oryzias latipes) (2004) Mech. Dev, 121, pp. 659-671
  • Evrard, Y.A., Lun, Y., Aulehla, A., Gan, L., Johnson, R.L., Lunatic fringe is an essential mediator of somite segmentation and patterning (1998) Nature, 394, pp. 377-381
  • Ferjentsik, Z., Hayashi, S., Dale, J.K., Bessho, Y., Herreman, A., de Strooper, B., del Monte, G., Maroto, M., Notch is a critical component of the mouse somitogenesis oscillator and is essential for the formation of the somites (2009) PLoS Genet, 5, p. 1000662
  • Forsberg, H., Crozet, F., Brown, N.A., Waves of mouse Lunatic fringe expression, in four-hour cycles at two-hour intervals, precede somite boundary formation (1998) Curr. Biol, 8, pp. 1027-1030
  • Gibb, S., Zagorska, A., Melton, K., Tenin, G., Vacca, I., Trainor, P., Maroto, M., Dale, J.K., Interfering with Wnt signalling alters the periodicity of the segmentation clock (2009) Dev. Biol, 330, pp. 21-31
  • 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
  • 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
  • Henry, C.A., Urban, M.K., Dill, K.K., Merlie, J.P., Page, M.F., Kimmel, C.B., Amacher, S.L., Two linked hairy/Enhancer of split-related zebrafish genes, her1 and her7, function together to refine alternating somite boundaries (2002) Development, 129, pp. 3693-3704
  • Herrgen, L., Ares, S., Morelli, L.G., Schröter, C., Jülicher, F., Oates, A.C., Intercellular coupling regulates the period of the segmentation clock (2010) Curr. Biol, 20, pp. 1244-1253
  • 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
  • Hirata, H., Bessho, Y., Kokubu, H., Masamizu, Y., Yamada, S., Lewis, J., Kageyama, R., Instability of Hes7 protein is crucial for the somite segmentation clock (2004) Nat. Genet, 36, pp. 750-754
  • Hogenesch, J.B., Ueda, H.R., Understanding systems-level properties: Timely stories from the study of clocks (2011) Nat. Rev. Genet, 12, pp. 407-416
  • 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 Dev, 14, pp. 1678-1690
  • Holley, S.A., Julich, D., Rauch, G.J., Geisler, R., 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
  • de Hrabe, A.M., McIntyre II, J., Gossler, A., Maintenance of somite borders in mice requires the Delta homologue DII1 (1997) Nature, 386, pp. 717-721
  • Huang, R., Zhi, Q., Brand-Saberi, B., Christ, B., New experimental evidence for somite resegmentation (2000) Anat. Embryol, 202, pp. 195-200
  • Huppert, S.S., Ilagan, M.X., de Strooper, B., Kopan, R., Analysis of Notch function in presomitic mesoderm suggests a gamma-secretaseindependent role for presenilins in somite differentiation (2005) Dev. Cell, 8, pp. 677-688
  • Ishimatsu, K., Takamatsu, A., Takeda, H., Emergence of traveling waves in the zebrafish segmentation clock (2010) Development, 137, pp. 1595-1599
  • 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
  • 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
  • Jouve, C., Iimura, T., Pourquié, O., Onset of the segmentation clock in the chick embryo: Evidence for oscillations in the somite precursors in the primitive streak (2002) Development, 129, pp. 1107-1117
  • Julich, D., Hwee, L.C., Round, J., Nicolaije, C., Schroeder, J., Davies, A., Geisler, R., Holley, S.A., 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
  • Kim, W., Matsui, T., Yamao, M., Ishibashi, M., Tamada, K., Takumi, T., Kohno, K., Sakumura, Y., The period of the somite segmentation clock is sensitive to Notch activity (2011) Mol. Biol. Cell, 22, pp. 3541-3549
  • Krol, A., Roellig, D., Dequeant, M.L., Tassy, O., Glynn, E., Hattem, G., Mushegian, A., Pourquié, O., Evolutionary plasticity of segmentation clock networks (2011) Development, 138, pp. 2783-2792
  • Kuramoto, Y., (1984) Chemical Oscillations, Waves and Turbulence, , Berlin, Germany: Springer Verlag
  • Lai, E.C., Notch signaling: Control of cell communication and cell fate (2004) Development, 131, pp. 965-973
  • Lewis, J., Autoinhibition with transcriptional delay: A simple mechanism for the zebrafish somitogenesis oscillator (2003) Curr. Biol, 13, pp. 1398-1408
  • Li, Y., Fenger, U., Niehrs, C., Pollet, N., Cyclic expression of esr9 gene in Xenopus presomitic mesoderm (2003) Differentiation, 71, pp. 83-89
  • Macdonald, B.T., Adamska, M., Meisler, M.H., Hypomorphic expression of Dkk1 in the doubleridge mouse: Dose dependence and compensatory interactions with Lrp6 (2004) Development, 131, pp. 2543-2552
  • 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
  • Maroto, M., Dale, J.K., Dequeant, M.L., Petit, A.C., Pourquié, O., Synchronised cycling gene oscillations in presomitic mesoderm cells require cellcell contact (2005) Int. J. Dev. Biol, 49, pp. 309-315
  • Maruhashi, M., van de Putte, T., Huylebroeck, D., Kondoh, H., Higashi, Y., Involvement of SIP1 in positioning of somite boundaries in the mouse embryo (2005) Dev. Dyn, 234, pp. 332-338
  • 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
  • McGrew, M.J., Dale, J.K., Fraboulet, S., Pourquié, O., The lunatic fringe gene is a target of the molecular clock linked to somite segmentation in avian embryos (1998) Curr. Biol, 8, pp. 979-982
  • Meinhardt, H., (1982) Models of Biological Pattern Formation, , London, UK: Academic Press
  • Monk, N.A., Oscillatory expression of Hes1, p53, and NF-kappaB driven by transcriptional time delays (2003) Curr. Biol, 13, pp. 1409-1413
  • 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
  • Moreno, T.A., Kintner, C., Regulation of segmental patterning by retinoic acid signaling during Xenopus somitogenesis (2004) Dev. Cell, 6, pp. 205-218
  • Morimoto, M., Takahashi, Y., Endo, M., Saga, Y., The Mesp2 transcription factor establishes segmental borders by suppressing Notch activity (2005) Nature, 435, pp. 354-359
  • 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) Dev. Cell, 13, pp. 298-304
  • Niwa, Y., Shimojo, H., Isomura, A., Gonzalez, A., Miyachi, H., Kageyama, R., Different types of oscillations in Notch and Fgf signaling regulate the spatiotemporal periodicity of somitogenesis (2011) Genes Dev, 25, pp. 1115-1120
  • Novak, B., Tyson, J.J., Design principles of biochemical oscillators (2008) Nat. Rev. Mol. Cell Biol, 9, pp. 981-991
  • 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
  • Oates, A.C., Gorfinkiel, N., Gonzalez-Gaitan, M., Heisenberg, C.P., Quantitative approaches in developmental biology (2009) Nat. Rev. Genet, 10, pp. 517-530
  • Oginuma, M., Takahashi, Y., Kitajima, S., Kiso, M., Kanno, J., Kimura, A., Saga, Y., The oscillation of Notch activation, but not its boundary, is required for somite border formation and rostral-caudal patterning within a somite (2010) Development, 137, pp. 1515-1522
  • Ohtsuka, T., Ishibashi, M., Gradwohl, G., Nakanishi, S., Guillemot, F., Kageyama, R., Hes1 and Hes5 as notch effectors in mammalian neuronal differentiation (1999) EMBO J, 18, pp. 2196-2207
  • Olivera-Martinez, I., Storey, K.G., Wnt signals provide a timing mechanism for the FGF-retinoid differentiation switch during vertebrate body axis extension (2007) Development, 134, pp. 2125-2135
  • Oswald, A., Oates, A.C., Control of endogenous gene expression timing by introns (2011) Genome Biol, 12, p. 107
  • 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
  • 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
  • Pearson, M., Elsdale, T., Somitogenesis In Amphibian Embryos. I. Experimental Evidence For An Interaction Between Two Temporal Factors In the Specification of Somite Pattern (1979) J. Embryol. Exp. Morphol, 51, pp. 27-50
  • Pourquié, O., Tam, P.P., A nomenclature for prospective somites and phases of cyclic gene expression in the presomitic mesoderm. Dev (2001) Cell, 1, pp. 619-620
  • Resende, T.P., Ferreira, M., Teillet, M.A., Tavares, A.T., Andrade, R.P., Palmeirim, I., Sonic hedgehog in temporal control of somite formation (2010) Proc. Natl. Acad. Sci. USA, 107, pp. 12907-12912
  • Richardson, M.K., Allen, S.P., Wright, G.M., Raynaud, A., Hanken, J., Somite number and vertebrate evolution (1998) Development, 125, pp. 151-160
  • 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
  • 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
  • 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
  • Schröter, C., Oates, A.C., Segment number and axial identity in a segmentation clock period mutant (2010) Curr. Biol, 20, pp. 1254-1258
  • Schröter, C., Herrgen, L., Cardona, A., Brouhard, G.J., Feldman, B., Oates, A.C., Dynamics of zebrafish somitogenesis (2008) Dev. Dyn, 237, pp. 545-
  • Shankaran, H., Wiley, H.S., Oscillatory dynamics of the extracellular signal-regulated kinase pathway (2010) Curr. Opin. Genet. Dev, 20, pp. 650-655
  • Shankaran, S.S., Sieger, D., Schroter, C., Czepe, C., Pauly, M.C., Laplante, M.A., Becker, T.S., Gajewski, M., Completing the set of h/E(spl) cyclic genes in zebrafish: Her12 and her15 reveal novel modes of expression and contribute to the segmentation clock (2007) Dev. Biol, 304, pp. 615-632
  • Shen, J., Bronson, R.T., Chen, D.F., Xia, W., Selkoe, D.J., Tonegawa, S., Skeletal and CNS defects in Presenilin-1-deficient mice (1997) Cell, 89, pp. 629-639
  • Shifley, E.T., Vanhorn, K.M., Perez-Balaguer, A., Franklin, J.D., Weinstein, M., Cole, S.E., Oscillatory lunatic fringe activity is crucial for segmentation of the anterior but not posterior skeleton (2008) Development, 135, pp. 899-908
  • Sieger, D., Ackermann, B., Winkler, C., Tautz, D., Gajewski, M., Her1 and her13.2 are jointly required for somitic border specification along the entire axis of the fish embryo (2006) Dev. Biol, 293, pp. 242-251
  • Sirbu, I.O., Duester, G., Retinoic-acid signalling in node ectoderm and posterior neural plate directs left-right patterning of somitic mesoderm (2006) Nat. Cell Biol, 8, pp. 271-277
  • Stauber, M., Sachidanandan, C., Morgenstern, C., Ish-Horowicz, D., Differential axial requirements for lunatic fringe and Hes7 transcription during mouse somitogenesis (2009) PLoS ONE, 4, p. 7996
  • Suriben, R., Fisher, D.A., Cheyette, B.N., Dact1 presomitic mesoderm expression oscillates in phase with Axin2 in the somitogenesis clock of mice (2006) Dev. Dyn, 235, pp. 3177-3183
  • Suriben, R., Kivimae, S., Fisher, D.A., Moon, R.T., Cheyette, B.N., Posterior malformations in Dact1 mutant mice arise through misregulated Vangl2 at the primitive streak (2009) Nat. Genet, 41, pp. 977-985
  • Takashima, Y., Ohtsuka, T., Gonzalez, A., Miyachi, H., Kageyama, R., Intronic delay is essential for oscillatory expression in the segmentation clock (2011) Proc. Natl. Acad. Sci. USA, 108, pp. 3300-3305
  • Tenin, G., Wright, D., Ferjentsik, Z., Bone, R., McGrew, M.J., Maroto, M., The chick somitogenesis oscillator is arrested before all paraxial mesoderm is segmented into somites (2010) BMC Dev. Biol, 10, p. 24
  • 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
  • Vermot, J., Gallego, L.J., Fraulob, V., Niederreither, K., Chambon, P., Dolle, P., Retinoic acid controls the bilateral symmetry of somite formation in the mouse embryo (2005) Science, 308, pp. 563-566
  • Wartlick, O., Kicheva, A., Gonzalez-Gaitan, M., Morphogen gradient formation (2009) Cold Spring Harb. Perspect. Biol, 1, p. 001255
  • Watanabe, T., Takahashi, Y., Tissue morphogenesis coupled with cell shape changes (2010) Curr. Opin. Genet. Dev, 20, pp. 443-447
  • Wilson, V., Olivera-Martinez, I., Storey, K.G., Stem cells, signals and vertebrate body axis extension (2009) Development, 136, pp. 1591-1604
  • Winfree, A.T., Biological rhythms and the behavior of populations of coupled oscillators (1967) J. Theor. Biol, 16, pp. 15-42
  • Wong, P.C., Zheng, H., Chen, H., Becher, M.W., Sirinathsinghji, D.J., Trumbauer, M.E., Chen, H.Y., Sisodia, S.S., Presenilin 1 is required for Notch1 and DII1 expression in the paraxial mesoderm (1997) Nature, 387, pp. 288-292
  • Wright, D., Ferjentsik, Z., Chong, S.W., Qiu, X., Jiang, Y.J., Malapert, P., Pourquié, O., Franco, C., Cyclic Nrarp mRNA expression is regulated by the somitic oscillator but Nrarp protein levels do not oscillate (2009) Dev. Dyn, 238, pp. 3043-3055
  • Yao, Y., Li, W., Wu, J., Germann, U.A., Su, M.S., Kuida, K., Boucher, D.M., Extracellular signal-regulated kinase 2 is necessary for mesoderm differentiation (2003) Proc. Natl. Acad. Sci. USA, 100, pp. 12759-12764
  • Yu, H.M., Jerchow, B., Sheu, T.J., Liu, B., Costantini, F., Puzas, J.E., Birchmeier, W., Hsu, W., The role of Axin2 in calvarial morphogenesis and craniosynostosis (2005) Development, 132, pp. 1995-2005
  • Zhang, N., Gridley, T., Defects in somite formation in lunatic fringedeficient mice (1998) Nature, 394, pp. 374-377
  • Zhao, X., Duester, G., Effect of retinoic acid signaling on Wnt/betacatenin and FGF signaling during body axis extension (2009) Gene Expr. Patt, 9, pp. 430-435

Citas:

---------- APA ----------
Oates, A.C., Morelli, L.G. & Ares, S. (2012) . Patterning embryos with oscillations: Structure, function and dynamics of the vertebrate segmentation clock. Development, 139(4), 625-639.
http://dx.doi.org/10.1242/dev.063735
---------- CHICAGO ----------
Oates, A.C., Morelli, L.G., Ares, S. "Patterning embryos with oscillations: Structure, function and dynamics of the vertebrate segmentation clock" . Development 139, no. 4 (2012) : 625-639.
http://dx.doi.org/10.1242/dev.063735
---------- MLA ----------
Oates, A.C., Morelli, L.G., Ares, S. "Patterning embryos with oscillations: Structure, function and dynamics of the vertebrate segmentation clock" . Development, vol. 139, no. 4, 2012, pp. 625-639.
http://dx.doi.org/10.1242/dev.063735
---------- VANCOUVER ----------
Oates, A.C., Morelli, L.G., Ares, S. Patterning embryos with oscillations: Structure, function and dynamics of the vertebrate segmentation clock. Development (Cambridge). 2012;139(4):625-639.
http://dx.doi.org/10.1242/dev.063735