X-ray phase-contrast in vivo microtomography probes new aspects of Xenopus gastrulation

Julian Moosmann, Alexey Ershov, Venera Altapova, Tilo Baumbach, Maneeshi S. Prasad, Carole Labonne, Xianghui Xiao, Jubin Kashef, Ralf Hofmann

    Research output: Contribution to journalArticle

    54 Citations (Scopus)

    Abstract

    An ambitious goal in biology is to understand the behaviour of cells during development by imaging-in vivo and with subcellular resolution-changes of the embryonic structure. Important morphogenetic movements occur throughout embryogenesis, but in particular during gastrulation when a series of dramatic, coordinated cell movements drives the reorganization of a simple ball or sheet of cells into a complex multi-layered organism. In Xenopus laevis, the South African clawed frog and also in zebrafish, cell and tissue movements have been studied in explants, in fixed embryos, in vivo using fluorescence microscopy or microscopic magnetic resonance imaging. None of these methods allows cell behaviours to be observed with micrometre-scale resolution throughout the optically opaque, living embryo over developmental time. Here we use non-invasive in vivo, time-lapse X-ray microtomography, based on single-distance phase contrast and combined with motion analysis, to examine the course of embryonic development. We demonstrate that this powerful four-dimensional imaging technique provides high-resolution views of gastrulation processes in wild-type X. laevis embryos, including vegetal endoderm rotation, archenteron formation, changes in the volumes of cavities within the porous interstitial tissue between archenteron and blastocoel, migration/confrontation of mesendoderm and closure of the blastopore. Differential flow analysis separates collective from relative cell motion to assign propulsion mechanisms. Moreover, digitally determined volume balances confirm that early archenteron inflation occurs through the uptake of external water. A transient ectodermal ridge, formed in association with the confrontation of ventral and head mesendoderm on the blastocoel roof, is identified. When combined with perturbation experiments to investigate molecular and biomechanical underpinnings of morphogenesis, our technique should help to advance our understanding of the fundamentals of development.

    Original languageEnglish
    Pages (from-to)374-377
    Number of pages4
    JournalNature
    Volume497
    Issue number7449
    DOIs
    Publication statusPublished - 16 May 2013

    Fingerprint

    Gastrula
    Gastrulation
    Xenopus
    Embryonic Structures
    X-Rays
    Xenopus laevis
    Embryonic Development
    Cell Movement
    X-Ray Microtomography
    Endoderm
    Economic Inflation
    Zebrafish
    Morphogenesis
    Fluorescence Microscopy
    Anura
    Head
    Magnetic Resonance Imaging
    Water

    ASJC Scopus subject areas

    • General

    Cite this

    Moosmann, J., Ershov, A., Altapova, V., Baumbach, T., Prasad, M. S., Labonne, C., ... Hofmann, R. (2013). X-ray phase-contrast in vivo microtomography probes new aspects of Xenopus gastrulation. Nature, 497(7449), 374-377. https://doi.org/10.1038/nature12116

    X-ray phase-contrast in vivo microtomography probes new aspects of Xenopus gastrulation. / Moosmann, Julian; Ershov, Alexey; Altapova, Venera; Baumbach, Tilo; Prasad, Maneeshi S.; Labonne, Carole; Xiao, Xianghui; Kashef, Jubin; Hofmann, Ralf.

    In: Nature, Vol. 497, No. 7449, 16.05.2013, p. 374-377.

    Research output: Contribution to journalArticle

    Moosmann, J, Ershov, A, Altapova, V, Baumbach, T, Prasad, MS, Labonne, C, Xiao, X, Kashef, J & Hofmann, R 2013, 'X-ray phase-contrast in vivo microtomography probes new aspects of Xenopus gastrulation', Nature, vol. 497, no. 7449, pp. 374-377. https://doi.org/10.1038/nature12116
    Moosmann J, Ershov A, Altapova V, Baumbach T, Prasad MS, Labonne C et al. X-ray phase-contrast in vivo microtomography probes new aspects of Xenopus gastrulation. Nature. 2013 May 16;497(7449):374-377. https://doi.org/10.1038/nature12116
    Moosmann, Julian ; Ershov, Alexey ; Altapova, Venera ; Baumbach, Tilo ; Prasad, Maneeshi S. ; Labonne, Carole ; Xiao, Xianghui ; Kashef, Jubin ; Hofmann, Ralf. / X-ray phase-contrast in vivo microtomography probes new aspects of Xenopus gastrulation. In: Nature. 2013 ; Vol. 497, No. 7449. pp. 374-377.
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