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Elongated Cells Drive Morphogenesis in a Surface-Wrapped Finite-Element Model of Germband Retraction.
Biophys J 2019; 117(1):157-169BJ

Abstract

During Drosophila embryogenesis, the germband first extends to curl around the posterior end of the embryo and then retracts back; however, retraction is not simply the reversal of extension. At a tissue level, extension is coincident with ventral furrow formation, and at a cellular level, extension occurs via convergent cell neighbor exchanges in the germband, whereas retraction involves only changes in cell shape. To understand how cell shapes, tissue organization, and cellular forces drive germband retraction, we investigate this process using a whole-embryo, surface-wrapped cellular finite-element model. This model represents two key epithelial tissues-amnioserosa and germband-as adjacent sheets of two-dimensional cellular finite elements that are wrapped around an ellipsoidal three-dimensional approximation of an embryo. The model reproduces the detailed kinematics of in vivo retraction by fitting just one free model parameter, the tension along germband cell interfaces; all other cellular forces are constrained to follow ratios inferred from experimental observations. With no additional parameter adjustments, the model also reproduces quantitative assessments of mechanical stress using laser dissection and failures of retraction when amnioserosa cells are removed via mutations or microsurgery. Surprisingly, retraction in the model is robust to changes in cellular force values but is critically dependent on starting from a configuration with highly elongated amnioserosa cells. Their extreme cellular elongation is established during the prior process of germband extension and is then used to drive retraction. The amnioserosa is the one tissue whose cellular morphogenesis is reversed from germband extension to retraction, and this reversal coordinates the forces needed to retract the germband back to its pre-extension position and shape. In this case, cellular force strengths are less important than the carefully established cell shapes that direct them. VIDEO

ABSTRACT

.

Authors+Show Affiliations

Department of Physics & Astronomy, Vanderbilt University, Nashville, Tennessee.Department of Civil & Environmental Engineering, University of Waterloo, Waterloo, Ontario, Canada.Department of Physics & Astronomy, Vanderbilt University, Nashville, Tennessee.Department of Physics, Stetson University, DeLand, Florida.Department of Physics & Astronomy, Vanderbilt University, Nashville, Tennessee.Department of Civil & Environmental Engineering, University of Waterloo, Waterloo, Ontario, Canada.Department of Physics & Astronomy, Vanderbilt University, Nashville, Tennessee; Department of Biological Sciences, Vanderbilt University, Nashville, Tennessee. Electronic address: shane.hutson@vanderbilt.edu.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

31229244

Citation

McCleery, W Tyler, et al. "Elongated Cells Drive Morphogenesis in a Surface-Wrapped Finite-Element Model of Germband Retraction." Biophysical Journal, vol. 117, no. 1, 2019, pp. 157-169.
McCleery WT, Veldhuis J, Bennett ME, et al. Elongated Cells Drive Morphogenesis in a Surface-Wrapped Finite-Element Model of Germband Retraction. Biophys J. 2019;117(1):157-169.
McCleery, W. T., Veldhuis, J., Bennett, M. E., Lynch, H. E., Ma, X., Brodland, G. W., & Hutson, M. S. (2019). Elongated Cells Drive Morphogenesis in a Surface-Wrapped Finite-Element Model of Germband Retraction. Biophysical Journal, 117(1), pp. 157-169. doi:10.1016/j.bpj.2019.05.023.
McCleery WT, et al. Elongated Cells Drive Morphogenesis in a Surface-Wrapped Finite-Element Model of Germband Retraction. Biophys J. 2019 Jul 9;117(1):157-169. PubMed PMID: 31229244.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Elongated Cells Drive Morphogenesis in a Surface-Wrapped Finite-Element Model of Germband Retraction. AU - McCleery,W Tyler, AU - Veldhuis,Jim, AU - Bennett,Monica E, AU - Lynch,Holley E, AU - Ma,Xiaoyan, AU - Brodland,G Wayne, AU - Hutson,M Shane, Y1 - 2019/06/05/ PY - 2016/07/18/received PY - 2019/05/13/revised PY - 2019/05/20/accepted PY - 2020/07/09/pmc-release PY - 2019/6/24/pubmed PY - 2019/6/24/medline PY - 2019/6/24/entrez SP - 157 EP - 169 JF - Biophysical journal JO - Biophys. J. VL - 117 IS - 1 N2 - During Drosophila embryogenesis, the germband first extends to curl around the posterior end of the embryo and then retracts back; however, retraction is not simply the reversal of extension. At a tissue level, extension is coincident with ventral furrow formation, and at a cellular level, extension occurs via convergent cell neighbor exchanges in the germband, whereas retraction involves only changes in cell shape. To understand how cell shapes, tissue organization, and cellular forces drive germband retraction, we investigate this process using a whole-embryo, surface-wrapped cellular finite-element model. This model represents two key epithelial tissues-amnioserosa and germband-as adjacent sheets of two-dimensional cellular finite elements that are wrapped around an ellipsoidal three-dimensional approximation of an embryo. The model reproduces the detailed kinematics of in vivo retraction by fitting just one free model parameter, the tension along germband cell interfaces; all other cellular forces are constrained to follow ratios inferred from experimental observations. With no additional parameter adjustments, the model also reproduces quantitative assessments of mechanical stress using laser dissection and failures of retraction when amnioserosa cells are removed via mutations or microsurgery. Surprisingly, retraction in the model is robust to changes in cellular force values but is critically dependent on starting from a configuration with highly elongated amnioserosa cells. Their extreme cellular elongation is established during the prior process of germband extension and is then used to drive retraction. The amnioserosa is the one tissue whose cellular morphogenesis is reversed from germband extension to retraction, and this reversal coordinates the forces needed to retract the germband back to its pre-extension position and shape. In this case, cellular force strengths are less important than the carefully established cell shapes that direct them. VIDEO ABSTRACT. SN - 1542-0086 UR - https://www.unboundmedicine.com/medline/citation/31229244/Elongated_Cells_Drive_Morphogenesis_in_a_Surface-Wrapped_Finite-Element_Model_of_Germband_Retraction L2 - https://linkinghub.elsevier.com/retrieve/pii/S0006-3495(19)30443-6 DB - PRIME DP - Unbound Medicine ER -