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Enhanced Snapshot: the Segmentation Clock

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Enhanced Snapshot: the Segmentation Clock SnapShot: The Segmentation Clock Daniela Roellig,1 Luis G. Morelli,1 Saúl Ares,2 Frank Jülicher,2 and Andrew C. Oates1 1Max Planck Institute of Molecular Cell Biology and Genetics, Dresden 01307, Germany 2Max Planck Institute for the Physics of Complex Systems, Dresden 01187, Germany The vertebral column is a conserved anatomical structure that defines the vertebrate phylum. This periodic or segmental pattern is established early in development when the vertebral precursors, the somites, are rhythmically produced from presomitic mesoderm (PSM) (Movie 1). Somites give rise to vertebrae, ribs, and skeletal muscles and lay the scaffolding for other segmented structures like spinal nerves and vertebral arteries. The PSM is initially produced during gastrulation and forms two rods of mesenchymal tissue on either side of the midline. A combination of proliferation and convergent extension constantly supplies new cells to the PSM as the embryo elongates. The rhythmic formation of somites from PSM is conserved across all vertebrates and follows a species-specific period, ranging from about 25 min in zebrafish, 90 min in chicken, 120 min in mouse, and 4–5 hr in humans. This embryonic rhythm is regulated by a multicellular genetic oscillator termed the segmentation clock. A Clock and Wavefront at the Heart of the Segmentation Clock The clock and wavefront model of somitogenesis was originally proposed by Cooke and Zeeman in 1976. In this model, the clock is a population of cellular oscillators, which are coordinated across the PSM. An arrest wavefront in the anterior PSM moves posteriorly and stops clock oscillations as it passes. The length of a segment is the distance traveled by the arrest front in one cycle of the clock. Thus, the rhythm of the clock is written into the periodic anatomy of the developing vertebrate embryo (Movie 2). In all vertebrates examined, the activity of the oscillators causes anteriorly traveling waves of cyclic gene expression that terminate at the position of a future somite boundary (Movie 3). These anteriorly traveling waves of gene expression may be caused by the gradual slowing down of the cellular oscillators and should not be confused with the posteriorly traveling arrest wavefront. The position and movement of the wavefront is regulated by gradients of signaling molecules that span the PSM along the anteroposterior (A/P) axis. Single-Cell Oscillators and Multicellular Synchronization Individual mouse PSM cells in culture show persistent cyclic gene oscillation. A simple model for the molecular circuitry of a cell-autonomous oscillator proposes a delayed nega- tive feedback loop of transcriptional repression. In mouse and zebrafish, dimeric Hes/Her bHLH proteins periodically repress their own transcription, and a Hes gene mutant in zebrafish alters the period of segmentation. Whether this feedback loop is sufficient for autonomous oscillations and how the period is regulated remain unknown. When PSM cells are not synchronized, coherent somite boundaries do not form. In the zebrafish, cell-cell synchronization occurs by Delta-Notch intercellular signaling, and this may also be the case in chick and mouse. A molecular regulatory model proposes that cyclic expression of ligands and modifiers of the Notch receptor, under the control of Hes/ Her periodic repression, cause periodic activation of Notch signaling activity in neighboring cells. This leads to the synchronization of Hes/Her gene expression between these cells. Loss of Notch signaling alters the period of segmentation in zebrafish. The Wavefront and Thresholds of Signaling Gradients Gradients of signals provide positional information along the A/P axis that defines the maturation state of the PSM cells. Mesodermal progenitors in the tail bud mature as they move anteriorly and become segmentally determined in the anterior PSM. Opposing gradients of Fgf/Wnt and retinoic acid (RA) control the movement of the wavefront along the PSM, defining a threshold where the oscillations of cyclic genes are arrested. For example, elevated levels of Wnt-responsive β-catenin expand the domain of oscillating gene expression anteriorly. A transient change of Fgf signaling levels can shift the position of the wavefront and thereby alter segment length. The molecular mechanisms by which these gradients slow and stop the clock are not known. RA is found in the anterior PSM and segmented region, and although its loss causes asymmetry, its precise role in somitogenesis is still unclear. Converting the Oscillations into Segments and then Somites As best studied in the mouse, cells passing the arrest front in the clock phase with a high level of Notch signaling turn on Mesp gene expression, defining the segment length. Subsequently, Mesp expression is restricted to the prospective anterior somite compartment as a polarity marker via interactions with Ripply repressors. Somite morphogenesis occurs at the anterior end of the PSM as a mesenchymal-to-epithelial transition of boundary cells. Mesp expression controls EphA4 expression, cell adhesion, and cell shape changes that form the epithelial boundary of the somite. Species-Specific Gene Regulatory Networks Total somite number is tightly controlled for each species but varies widely between species. For example, zebrafish has about 31 segments, whereas chick and mouse have 55 and 65, respectively, and snakes have several hundred segments. Segment number is controlled by altering the ratio of clock period and wavefront velocity, as well as the total time of embryonic outgrowth during which segmentation occurs. Oscillations of genes in the Notch, Fgf, and Wnt signaling pathways have been observed in different vertebrate species. Nevertheless, conservation of the individual cyclic genes within these pathways is very limited. The function of most of these cyclic genes, and whether their oscillations are required for segmentation, is still unclear. Overlap between all three species is limited to cyclic Hes/Her orthologs, suggesting that these genes are the core of a conserved oscillatory mechanism. REFERENCES Aulehla, A., Wehrle, C., Brand-Saberi, B., Kemler, R., Gossler, A., Kanzler, B., and Herrmann, B.G. (2003). Wnt3a plays a major role in the segmentation clock controlling somitogen- esis. Dev. Cell 4, 395–406. Cooke, J., and Zeeman, E.C. (1976). A clock and wavefront model for control of the number of repeated structures during animal morphogenesis. J. Theor. Biol. 58, 455–476. Dubrulle, J., McGrew, M.J., and Pourquié, O. (2001). FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activa- tion. Cell 106, 219–232. Gomez, C., Ozbudak, E.M., Wunderlich, J., Baumann, D., Lewis, J., and Pourquié, O. (2008). Control of segment number in vertebrate embryos. Nature 454, 335–339. Herrgen, L., Ares, S., Morelli, L.G., Schröter, C., Jülicher, F., and Oates, A.C. (2010). Intercellular coupling regulates the period of the segmentation clock. Curr. Biol. 20, 1244–1253. Horikawa, K., Ishimatsu, K., Yoshimoto, E., Kondo, S., and Takeda, H. (2006). Noise-resistant and synchronized oscillation of the segmentation clock. Nature 441, 719–723. Krol, A.J., Roellig, D., Dequeant, M.-L., Tassy, O., Glynn, E., Hattem, G., Mushegian, A., Oates, A.C., and Pourquie, O. (2011). Evolutionary plasticity of segmentation clock networks. Development, in press. Lewis, J. (2003). Autoinhibition with transcriptional delay: a simple mechanism for the zebrafish somitogenesis oscillator. Curr. Biol. 13, 1398–1408. Masamizu, Y., Ohtsuka, T., Takashima, Y., Nagahara, H., Takenaka, Y., Yoshikawa, K., Okamura, H., and Kageyama, R. (2006). Real-time imaging of the somite segmentation clock: revelation of unstable oscillators in the individual presomitic mesoderm cells. Proc. Natl. Acad. Sci. USA 103, 1313–1318. Palmeirim, I., Henrique, D., Ish-Horowicz, D., and Pourquié, O. (1997). Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesis. Cell 91, 639–648. Riedel-Kruse, I.H., Müller, C., and Oates, A.C. (2007). Synchrony dynamics during initiation, failure, and rescue of the segmentation clock. Science 317, 1911–1915. Schröter, C., and Oates, A.C. (2010). Segment number and axial identity in a segmentation clock period mutant. Curr. Biol. 20, 1254–1258. 800.e1 Cell 145, May 27, 2011 ©2011 Elsevier Inc. DOI10.1016/j.cell.2011.05.007.
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