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Untwisting the Caenorhabditis elegans embryo.

Christensen RP, Bokinsky A, Santella A, Wu Y, Marquina-Solis J, Guo M, Kovacevic I, Kumar A, Winter PW, Tashakkori N, McCreedy E, Liu H, McAuliffe M, Mohler W, Colón-Ramos DA, Bao Z, Shroff H - Elife (2015)

Bottom Line: However, studies of single cell development have largely been conducted in fixed or pre-twitching live embryos, because of technical difficulties associated with embryo movement in late embryogenesis.The detailed positional information we obtained enabled us to develop a composite model showing movement of these cells and neurites in an 'average' worm embryo.The untwisting and cell tracking capabilities of our method provide a foundation on which to catalog C. elegans neurodevelopment, allowing interrogation of developmental events in previously inaccessible periods of embryogenesis.

View Article: PubMed Central - PubMed

Affiliation: Section on High Resolution Optical Imaging, National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, United States.

ABSTRACT
The nematode Caenorhabditis elegans possesses a simple embryonic nervous system with few enough neurons that the growth of each cell could be followed to provide a systems-level view of development. However, studies of single cell development have largely been conducted in fixed or pre-twitching live embryos, because of technical difficulties associated with embryo movement in late embryogenesis. We present open-source untwisting and annotation software (http://mipav.cit.nih.gov/plugin_jws/mipav_worm_plugin.php) that allows the investigation of neurodevelopmental events in late embryogenesis and apply it to track the 3D positions of seam cell nuclei, neurons, and neurites in multiple elongating embryos. We also provide a tutorial describing how to use the software (Supplementary file 1) and a detailed description of the untwisting algorithm (Appendix). The detailed positional information we obtained enabled us to develop a composite model showing movement of these cells and neurites in an 'average' worm embryo. The untwisting and cell tracking capabilities of our method provide a foundation on which to catalog C. elegans neurodevelopment, allowing interrogation of developmental events in previously inaccessible periods of embryogenesis.

No MeSH data available.


Related in: MedlinePlus

Temporal alignment of embryo data.Data from two embryos are shown before (top) and after (bottom) temporal alignment. The data derived from embryo 4 was shifted 5 timepoints to the right, following the procedure described in 'Materials and methods'. Data shown are the z positions from the right V3 seam cell nucleus. Only a portion of the data, at early timepoints, is shown to highlight the shifting procedure.DOI:http://dx.doi.org/10.7554/eLife.10070.017
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fig4s1: Temporal alignment of embryo data.Data from two embryos are shown before (top) and after (bottom) temporal alignment. The data derived from embryo 4 was shifted 5 timepoints to the right, following the procedure described in 'Materials and methods'. Data shown are the z positions from the right V3 seam cell nucleus. Only a portion of the data, at early timepoints, is shown to highlight the shifting procedure.DOI:http://dx.doi.org/10.7554/eLife.10070.017

Mentions: The strong qualitative similarities in seam cell nuclear trajectories among the five embryos we inspected led us to investigate whether data from different embryos could be combined to yield a composite model of development representing growth in an 'average' embryo. Initial examination of the axial (nose-to-tail) seam cell nuclear trajectories from different embryos suggested a high degree of stereotypy; except for a relative shift in time, the trajectories displayed very similar shapes (Figure 4A). We thus shifted the axial data in time until the trajectories from multiple embryos overlaid (Figure 4B, Figure 4—figure supplement 1). We determined the amount of shift by using a three parameter logistic function to fit the raw axial displacement data (Figure 4—figure supplement 2, Tables 1, 2, Materials and methods), overlaying the data from various embryos until the inflection points in each curve were identical.10.7554/eLife.10070.016Figure 4.Alignment of data from different embryos.


Untwisting the Caenorhabditis elegans embryo.

Christensen RP, Bokinsky A, Santella A, Wu Y, Marquina-Solis J, Guo M, Kovacevic I, Kumar A, Winter PW, Tashakkori N, McCreedy E, Liu H, McAuliffe M, Mohler W, Colón-Ramos DA, Bao Z, Shroff H - Elife (2015)

Temporal alignment of embryo data.Data from two embryos are shown before (top) and after (bottom) temporal alignment. The data derived from embryo 4 was shifted 5 timepoints to the right, following the procedure described in 'Materials and methods'. Data shown are the z positions from the right V3 seam cell nucleus. Only a portion of the data, at early timepoints, is shown to highlight the shifting procedure.DOI:http://dx.doi.org/10.7554/eLife.10070.017
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4764590&req=5

fig4s1: Temporal alignment of embryo data.Data from two embryos are shown before (top) and after (bottom) temporal alignment. The data derived from embryo 4 was shifted 5 timepoints to the right, following the procedure described in 'Materials and methods'. Data shown are the z positions from the right V3 seam cell nucleus. Only a portion of the data, at early timepoints, is shown to highlight the shifting procedure.DOI:http://dx.doi.org/10.7554/eLife.10070.017
Mentions: The strong qualitative similarities in seam cell nuclear trajectories among the five embryos we inspected led us to investigate whether data from different embryos could be combined to yield a composite model of development representing growth in an 'average' embryo. Initial examination of the axial (nose-to-tail) seam cell nuclear trajectories from different embryos suggested a high degree of stereotypy; except for a relative shift in time, the trajectories displayed very similar shapes (Figure 4A). We thus shifted the axial data in time until the trajectories from multiple embryos overlaid (Figure 4B, Figure 4—figure supplement 1). We determined the amount of shift by using a three parameter logistic function to fit the raw axial displacement data (Figure 4—figure supplement 2, Tables 1, 2, Materials and methods), overlaying the data from various embryos until the inflection points in each curve were identical.10.7554/eLife.10070.016Figure 4.Alignment of data from different embryos.

Bottom Line: However, studies of single cell development have largely been conducted in fixed or pre-twitching live embryos, because of technical difficulties associated with embryo movement in late embryogenesis.The detailed positional information we obtained enabled us to develop a composite model showing movement of these cells and neurites in an 'average' worm embryo.The untwisting and cell tracking capabilities of our method provide a foundation on which to catalog C. elegans neurodevelopment, allowing interrogation of developmental events in previously inaccessible periods of embryogenesis.

View Article: PubMed Central - PubMed

Affiliation: Section on High Resolution Optical Imaging, National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, United States.

ABSTRACT
The nematode Caenorhabditis elegans possesses a simple embryonic nervous system with few enough neurons that the growth of each cell could be followed to provide a systems-level view of development. However, studies of single cell development have largely been conducted in fixed or pre-twitching live embryos, because of technical difficulties associated with embryo movement in late embryogenesis. We present open-source untwisting and annotation software (http://mipav.cit.nih.gov/plugin_jws/mipav_worm_plugin.php) that allows the investigation of neurodevelopmental events in late embryogenesis and apply it to track the 3D positions of seam cell nuclei, neurons, and neurites in multiple elongating embryos. We also provide a tutorial describing how to use the software (Supplementary file 1) and a detailed description of the untwisting algorithm (Appendix). The detailed positional information we obtained enabled us to develop a composite model showing movement of these cells and neurites in an 'average' worm embryo. The untwisting and cell tracking capabilities of our method provide a foundation on which to catalog C. elegans neurodevelopment, allowing interrogation of developmental events in previously inaccessible periods of embryogenesis.

No MeSH data available.


Related in: MedlinePlus