Segment-Specific Adhesion as a Driver of Convergent Extension

Vroomans, Renske M. A.; Hogeweg, Paulien; Tusscher, Kirsten H. W. J. ten

doi:10.1371/journal.pcbi.1004092

“…The assumption that this extension should not affect the relative proportions in A and P compartment size requires future experimental validation. In addition, our finding that elevated tension along compartment boundaries does not affect compartment sizes may be contrasted with theoretical and experimental studies showing how differential line tension, either at compartment boundaries or across tissues, may drive convergent extension [ 52 , 53 ]. A key conceptual difference between the present work and these studies is the assumption of a fixed, or free, boundary to the tissue.…”

Section: Discussionmentioning

confidence: 60%

Capabilities and Limitations of Tissue Size Control through Passive Mechanical Forces

Kursawe

¹

,

Brodskiy

²

,

Zartman

³

et al. 2015

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Embryogenesis is an extraordinarily robust process, exhibiting the ability to control tissue size and repair patterning defects in the face of environmental and genetic perturbations. The size and shape of a developing tissue is a function of the number and size of its constituent cells as well as their geometric packing. How these cellular properties are coordinated at the tissue level to ensure developmental robustness remains a mystery; understanding this process requires studying multiple concurrent processes that make up morphogenesis, including the spatial patterning of cell fates and apoptosis, as well as cell intercalations. In this work, we develop a computational model that aims to understand aspects of the robust pattern repair mechanisms of the Drosophila embryonic epidermal tissues. Size control in this system has previously been shown to rely on the regulation of apoptosis rather than proliferation; however, to date little work has been done to understand the role of cellular mechanics in this process. We employ a vertex model of an embryonic segment to test hypotheses about the emergence of this size control. Comparing the model to previously published data across wild type and genetic perturbations, we show that passive mechanical forces suffice to explain the observed size control in the posterior (P) compartment of a segment. However, observed asymmetries in cell death frequencies across the segment are demonstrated to require patterning of cellular properties in the model. Finally, we show that distinct forms of mechanical regulation in the model may be distinguished by differences in cell shapes in the P compartment, as quantified through experimentally accessible summary statistics, as well as by the tissue recoil after laser ablation experiments.

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“…In addition, our finding that elevated tension along compartment boundaries does not affect compartment sizes may be contrasted with theoretical and experimental studies showing how differential line tension, either at compartment boundaries or across tissues, may drive convergent extension [52,53]. A key conceptual difference between the present work and these studies is the assumption of a fixed, or free, boundary to the tissue.…”

Section: Drosophilamentioning

confidence: 55%

Capabilities and Limitations of Tissue Size Control Through Passive Mechanical Forces

Kursawe

¹

,

Brodskiy

²

,

Zartman

³

et al. 2015

Preprint

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Embryogenesis is an extraordinarily robust process, exhibiting the ability to control tissue size and repair patterning defects in the face of environmental and genetic perturbations. The size and shape of a developing tissue is a function of the number and size of its constituent cells as well as their geometric packing. How these cellular properties are coordinated at the tissue level to ensure developmental robustness remains a mystery; understanding this process requires studying multiple concurrent processes that make up morphogenesis, including the spatial patterning of cell fates and apoptosis, as well as cell intercalations. In this work, we develop a computational model that aims to understand aspects of the robust pattern repair mechanisms of the Drosophila embryonic epidermal tissues. Size control in this system has previously been shown to rely on the regulation of apoptosis rather than proliferation; however, to date little work has been done to understand the role of cellular mechanics in this process. We employ a vertex model of an embryonic segment to test hypotheses about the emergence of this size control. Comparing the model to previously published data across wild type and genetic perturbations, we show that passive mechanical forces suffice to explain the observed size control in the posterior (P) compartment of a segment. However, observed asymmetries in cell death frequencies across the segment are demonstrated to require patterning of cellular properties in the model. Finally, we show that distinct forms of mechanical regulation in the model may be distinguished by differences in cell shapes in the P compartment, as quantified through experimentally accessible summary statistics, as well as by the tissue recoil after laser ablation experiments. Author SummaryDeveloping embryos are able to grow organs of the correct size even in the face of significant external perturbations. Such robust size control is achieved via tissue-level coordination of cell growth, proliferation, death and rearrangement, through mechanisms that are not well understood. Here, we employ computational modelling to test hypotheses of size control in the developing fruit fly. Segments in the surface tissues of the fruit fly embryo PLOS Computational Biology |

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“…Both asymmetric external forces on a tissue ( passive CE ) and asymmetric forces generated by the cells within a tissue ( active CE ) can lead to CE ( Fig 1 ) [ 10 ]. Hypothesized mechanisms for CE include anisotropic cell edge/actin contraction [ 11 , 12 ], anisotropic cell adhesion and elongation [ 13 , 14 ], cell shape extension/retraction [ 11 , 15 ], combinations of a constraining boundary with undirected cell elongation [ 16 ] or with directed leading edge protrusion [ 17 ], and increased cell adhesion within tissue segments [ 18 ] (see Supplemental Material for a more detailed discussion of previous models). Existing models of CE, however, neglect the experimentally observed prevalence of filopodial extension parallel to the direction of tissue convergence [ 3 , 9 , 19 – 24 ], which could produce anisotropic traction forces between cells or between cells and the extracellular matrix [ 25 – 28 ].…”

Section: Introductionmentioning

confidence: 99%

Filopodial-Tension Model of Convergent-Extension of Tissues

Belmonte

¹

,

Swat

²

,

Glazier

³

2016

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In convergent-extension (CE), a planar-polarized epithelial tissue elongates (extends) in-plane in one direction while shortening (converging) in the perpendicular in-plane direction, with the cells both elongating and intercalating along the converging axis. CE occurs during the development of most multicellular organisms. Current CE models assume cell or tissue asymmetry, but neglect the preferential filopodial activity along the convergent axis observed in many tissues. We propose a cell-based CE model based on asymmetric filopodial tension forces between cells and investigate how cell-level filopodial interactions drive tissue-level CE. The final tissue geometry depends on the balance between external rounding forces and cell-intercalation traction. Filopodial-tension CE is robust to relatively high levels of planar cell polarity misalignment and to the presence of non-active cells. Addition of a simple mechanical feedback between cells fully rescues and even improves CE of tissues with high levels of polarity misalignments. Our model extends easily to three dimensions, with either one converging and two extending axes, or two converging and one extending axes, producing distinct tissue morphologies, as observed in vivo.

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Segment-Specific Adhesion as a Driver of Convergent Extension

Cited by 34 publications

References 38 publications

Capabilities and Limitations of Tissue Size Control through Passive Mechanical Forces

Capabilities and Limitations of Tissue Size Control through Passive Mechanical Forces

Capabilities and Limitations of Tissue Size Control Through Passive Mechanical Forces

Filopodial-Tension Model of Convergent-Extension of Tissues

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