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5 Janelia Publications

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    10/02/18 | Integrin-mediated attachment of the blastoderm to the vitelline envelope impacts gastrulation of insects.
    Muenster S, Jain A, Mietke A, Pavlopoulos A, Grill SW, Tomancak P
    bioRxiv. 2018 Oct 2:. doi: 10.1101/421701

    During gastrulation, physical forces reshape the simple embryonic tissue to form a complex body plan of multicellular organisms. These forces often cause large-scale asymmetric movements of the embryonic tissue. In many embryos, the tissue undergoing gastrulation movements is surrounded by a rigid protective shell. While it is well recognized that gastrulation movements depend on forces generated by tissue-intrinsic contractility, it is not known if interactions between the tissue and the protective shell provide additional forces that impact gastrulation. Here we show that a particular part of the blastoderm tissue of the red flour beetle Tribolium castaneum tightly adheres in a temporally coordinated manner to the vitelline envelope surrounding the embryo. This attachment generates an additional force that counteracts the tissue-intrinsic contractile forces to create asymmetric tissue movements. Furthermore, this localized attachment is mediated by a specific integrin, and its knock-down leads to a gastrulation phenotype consistent with complete loss of attachment. Moreover, analysis of another integrin in the fruit fly Drosophila melanogaster suggests that gastrulation in this organism also relies on adhesion between the blastoderm and the vitelline. Together, our findings reveal a conserved mechanism whereby the spatiotemporal pattern of tissue adhesion to the vitelline envelope provides controllable counter-forces that shape gastrulation movements in insects.

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    03/29/18 | Multi-view light-sheet imaging and tracking with the MaMuT software reveals the cell lineage of a direct developing arthropod limb.
    Wolff C, Tinevez J, Pietzsch T, Stamataki E, Harich B, Guignard L, Preibisch S, Shorte S, Keller PJ, Tomancak P, Pavlopoulos A
    eLife. 2018 Mar 29:. doi: 10.7554/eLife.34410

    During development, coordinated cell behaviors orchestrate tissue and organ morphogenesis. Detailed descriptions of cell lineages and behaviors provide a powerful framework to elucidate the mechanisms of morphogenesis. To study the cellular basis of limb development, we imaged transgenic fluorescently-labeled embryos from the crustacean Parhyale hawaiensis with multi-view light-sheet microscopy at high spatiotemporal resolution over several days of embryogenesis. The cell lineage of outgrowing thoracic limbs was reconstructed at single-cell resolution with new software called Massive Multi-view Tracker (MaMuT). In silico clonal analyses suggested that the early limb primordium becomes subdivided into anterior-posterior and dorsal-ventral compartments whose boundaries intersect at the distal tip of the growing limb. Limb-bud formation is associated with spatial modulation of cell proliferation, while limb elongation is also driven by preferential orientation of cell divisions along the proximal-distal growth axis. Cellular reconstructions were predictive of the expression patterns of limb development genes including the BMP morphogen Decapentaplegic.

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    11/16/16 | The genome of the crustacean Parhyale hawaiensis: a model for animal development, regeneration, immunity and lignocellulose digestion.
    Kao D, Lai AG, Stamataki E, Rosic S, Konstantinides N, Jarvis E, Di Donfrancesco A, Pouchkina-Stantcheva N, Semon M, Grillo M, Bruce H, Kumar S, Siwanowicz I, Le A, Lemire A, Extavour C, Browne W, Wolff C, Averof M, et al
    eLife. 2016 Nov 16;5:e20062. doi: 10.7554/eLife.20062

    Parhyale hawaiensis is a blossoming model system for studies of developmental mechanisms and more recently adult regeneration. We have sequenced the genome allowing annotation of all key signaling pathways, small non-coding RNAs and transcription factors that will enhance ongoing functional studies. Parhayle is a member of the Malacostraca, which includes crustacean food crop species. We analysed the immunity related genes of Parhyale as an important comparative system for these species, where immunity related aquaculture problems have increased as farming has intensified. We also find that Parhyale and other species within Multicrustacea contain the enzyme sets necessary to perform lignocellulose digestion (wood eating), suggesting this ability may predate the diversification of this lineage. Our data provide an essential resource for further development of the Parhyale model. The first Malacostracan genome sequence will underpin ongoing comparative work in important food crop species and research investigating lignocellulose as energy source.

    Publication first appeared in BioRxiv on August 2, 2016. http://dx.doi.org/10.1101/065789

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    07/28/16 | Non-insect crustacean models in developmental genetics including an encomium to Parhyale hawaiensis.
    Stamataki E, Pavlopoulos A
    Current Opinion in Genetics & Development. 2016 Jul 28;39:149-156. doi: 10.1016/j.gde.2016.07.004

    The impressive diversity of body plans, lifestyles and segmental specializations exhibited by crustaceans (barnacles, copepods, shrimps, crabs, lobsters and their kin) provides great material to address longstanding questions in evolutionary developmental biology. Recent advances in forward and reverse genetics and in imaging approaches applied in the amphipod Parhyale hawaiensis and other emerging crustacean model species have made it possible to probe the molecular and cellular basis of crustacean diversity. A number of biological and technical qualities like the slow tempo and holoblastic cleavage mode, the stereotypy of many cellular processes, the functional and morphological diversity of limbs along the body axis, and the availability of various experimental manipulations, have made Parhyale a powerful system to study normal development and regeneration.

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    05/18/16 | Toll genes have an ancestral role in axis elongation.
    Benton MA, Pechmann M, Frey N, Stappert D, Conrads KH, Chen Y, Stamataki E, Pavlopoulos A, Roth S
    Current Biology : CB. 2016 May 18;26(12):1609-15. doi: 10.1016/j.cub.2016.04.055

    One of the key morphogenetic processes used during development is the controlled intercalation of cells between their neighbors. This process has been co-opted into a range of developmental events, and it also underlies an event that occurs in each major group of bilaterians: elongation of the embryo along the anterior-posterior axis [1]. In Drosophila, a novel component of this process was recently discovered by Paré et al., who showed that three Toll genes function together to drive cell intercalation during germband extension [2]. This finding raises the question of whether this role of Toll genes is an evolutionary novelty of flies or a general mechanism of embryonic morphogenesis. Here we show that the Toll gene function in axis elongation is, in fact, widely conserved among arthropods. First, we functionally demonstrate that two Toll genes are required for cell intercalation in the beetle Tribolium castaneum. We then show that these genes belong to a previously undescribed Toll subfamily and that members of this subfamily exhibit striped expression (as seen in Tribolium and previously reported in Drosophila [3-5]) in embryos of six other arthropod species spanning the entire phylum. Last, we show that two of these Toll genes are required for normal morphogenesis during anterior-posterior embryo elongation in the spider Parasteatoda tepidariorum, a member of the most basally branching arthropod lineage. From our findings, we hypothesize that Toll genes had a morphogenetic function in embryo elongation in the last common ancestor of all arthropods, which existed over 550 million years ago.

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