Mechanical control of tissue shape and morphogenetic flows during vertebrate body axis elongation

AbstractShaping embryonic tissues into their functional morphologies requires cells to control the physical state of the tissue in space and time. While regional variations in cellular forces or cell proliferation have been typically assumed to be the main physical factors controlling tissue morphogenesis, recent experiments have revealed that spatial variations in the tissue physical (fluid/solid) state play a key role in shaping embryonic tissues. Here we theoretically study how the regional control of fluid and solid tissue states guides morphogenetic flows to shape the extending vertebrate body axis. Our results show that both the existence of a fluid-to-solid tissue transition along the anteroposterior axis and the tissue surface tension determine the shape of the tissue and its ability to elongate unidirectionally, with large tissue tensions preventing unidirectional elongation and promoting blob-like tissue expansions. We predict both the tissue morphogenetic flows and stresses that enable unidirectional axis elongation. Our results show the existence of a sharp transition in the structure of morphogenetic flows, from a flow with no vortices to a flow with two counter-rotating vortices, caused by a transition in the number and location of topological defects in the flow field. Finally, comparing the theoretical predictions to quantitative measurements of both tissue flows and shape during zebrafish body axis elongation, we show that the observed morphogenetic events can be explained by the existence of a fluid-to-solid tissue transition along the anteroposterior axis. These results highlight the role of spatiotemporally-controlled fluid-to-solid transitions in the tissue state as a physical mechanism of embryonic morphogenesis.

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Mechanical control of tissue shape and morphogenetic flows during vertebrate body axis elongation

10.1101/2020.06.17.157586 ◽

2020 ◽

Author(s):

Samhita P. Banavar ◽

Emmet K. Carn ◽

Payam Rowghanian ◽

Georgina Stooke-Vaughan ◽

Sangwoo Kim ◽

...

Keyword(s):

Topological Defects ◽

Body Axis ◽

Physical Factors ◽

Anteroposterior Axis ◽

Solid Tissue ◽

Embryonic Tissues ◽

Quantitative Measurements ◽

Theoretical Predictions ◽

Axis Elongation ◽

Mere Existence

ABSTRACTShaping embryonic tissues into their functional morphologies requires cells to control the physical state of the tissue in space and time. While regional variations in cellular forces or cell proliferation have been typically assumed to be the main physical factors controlling tissue morphogenesis, recent experiments have revealed that spatial variations in the tissue physical (fluid/solid) state play a key role in shaping embryonic tissues. Here we theoretically study how the regional control of fluid and solid tissue states guides morphogenetic flows to shape the extending vertebrate body axis. Our results show that both the existence of a fluid-to-solid tissue transition along the anteroposterior axis and the tissue surface tension determine the shape of the tissue and its ability to elongate unidirectionally, with large tissue tensions preventing unidirectional elongation and promoting blob-like tissue expansions. We predict both the tissue morphogenetic flows and stresses that enable unidirectional axis elongation. Our results show the existence of a sharp transition in the structure of morphogenetic flows, from a flow with no vortices to a flow with two counter-rotating vortices, caused by a transition in the number and location of topological defects in the flow field. Finally, comparing the theoretical predictions to quantitative measurements of both tissue flows and shape during zebrafish body axis elongation, we show that the observed morphogenetic events can be explained by the mere existence of a fluid-to-solid tissue transition along the anteroposterior axis. These results highlight the role of spatiotemporally-controlled fluid-to-solid transitions in the tissue state as a physical mechanism of embryonic morphogenesis.

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Faculty Opinions recommendation of Loss of FGF-dependent mesoderm identity and rise of endogenous retinoid signalling determine cessation of body axis elongation.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.717964057.793465738 ◽

2012 ◽

Author(s):

Anna-Katerina Hadjantonakis ◽

Anna Ferrer-Vaquer

Keyword(s):

Body Axis ◽

Axis Elongation

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A fluid-to-solid jamming transition underlies vertebrate body axis elongation

Nature ◽

10.1038/s41586-018-0479-2 ◽

2018 ◽

Vol 561 (7723) ◽

pp. 401-405 ◽

Cited By ~ 151

Author(s):

Alessandro Mongera ◽

Payam Rowghanian ◽

Hannah J. Gustafson ◽

Elijah Shelton ◽

David A. Kealhofer ◽

...

Keyword(s):

Body Axis ◽

Jamming Transition ◽

Axis Elongation

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How do signaling and transcription factors regulate both axis elongation and Hox gene expression along the anteroposterior axis?

Development Growth & Differentiation ◽

10.1111/dgd.12682 ◽

2020 ◽

Vol 62 (5) ◽

pp. 363-375 ◽

Cited By ~ 1

Author(s):

Seiji Saito ◽

Takayuki Suzuki

Keyword(s):

Gene Expression ◽

Transcription Factors ◽

Hox Gene ◽

Anteroposterior Axis ◽

Axis Elongation

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Notochord vacuoles are lysosome-related organelles that function in axis and spine morphogenesis

The Journal of Cell Biology ◽

10.1083/jcb.201212095 ◽

2013 ◽

Vol 200 (5) ◽

pp. 667-679 ◽

Cited By ~ 86

Author(s):

Kathryn Ellis ◽

Jennifer Bagwell ◽

Michel Bagnat

Keyword(s):

Embryonic Development ◽

Early Development ◽

Molecular Mechanisms ◽

Body Axis ◽

Endosomal Trafficking ◽

Vertebrate Development ◽

Axis Elongation ◽

Lysosome Related Organelles ◽

Spine Morphogenesis

The notochord plays critical structural and signaling roles during vertebrate development. At the center of the vertebrate notochord is a large fluid-filled organelle, the notochord vacuole. Although these highly conserved intracellular structures have been described for decades, little is known about the molecular mechanisms involved in their biogenesis and maintenance. Here we show that zebrafish notochord vacuoles are specialized lysosome-related organelles whose formation and maintenance requires late endosomal trafficking regulated by the vacuole-specific Rab32a and H+-ATPase–dependent acidification. We establish that notochord vacuoles are required for body axis elongation during embryonic development and identify a novel role in spine morphogenesis. Thus, the vertebrate notochord plays important structural roles beyond early development.

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Downregulation of Extraembryonic Tension Controls Body Axis Formation in Avian Embryos

10.1101/2021.02.24.432525 ◽

2021 ◽

Author(s):

Daniele Kunz ◽

Anfu Wang ◽

Chon U Chan ◽

Robyn H. Pritchard ◽

Wenyu Wang ◽

...

Keyword(s):

Structural Analysis ◽

Outer Layer ◽

Shape Change ◽

Body Axis ◽

Vitelline Membrane ◽

Axis Formation ◽

Extraembryonic Tissue ◽

Avian Embryos ◽

Embryonic Tissues ◽

Tissue Tension

AbstractEmbryonic tissues undergoing shape change draw mechanical input from extraembryonic substrates. In avian eggs, the early blastoderm disk is under the tension of the vitelline membrane (VM). Here we report that chicken VM characteristically downregulates tension and stiffness to facilitate stage-specific embryo morphogenesis. While early relaxation of the VM impairs blastoderm expansion, maintaining VM tension in later stages resists the convergence of the posterior body causing stalled elongation, open neural tube, and axis rupture. Biochemical and structural analysis shows that VM weakening follows the reduction of its outer-layer glycoprotein fibers, which is caused by an increasing albumen pH due to CO2 release from the egg. Our results identify a previously unrecognized mechanism of body axis defects through mis-regulation of extraembryonic tissue tension.

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Faculty Opinions recommendation of A fluid-to-solid jamming transition underlies vertebrate body axis elongation.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.733952420.793550659 ◽

2018 ◽

Author(s):

Brian Stramer

Keyword(s):

Body Axis ◽

Jamming Transition ◽

Axis Elongation

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Integer topological defects organize stresses driving tissue morphogenesis

10.1101/2020.06.02.129262 ◽

2020 ◽

Cited By ~ 1

Author(s):

Pau Guillamat ◽

Carles Blanch-Mercader ◽

Karsten Kruse ◽

Aurélien Roux

Keyword(s):

Topological Defects ◽

Self Organization ◽

Tissue Architecture ◽

Tissue Morphogenesis ◽

Compressive Stresses ◽

Cellular Forces ◽

Stress Patterns

AbstractTissues acquire their function and shape via differentiation and morphogenesis. Both processes are driven by coordinating cellular forces and shapes at the tissue scale, but general principles governing this interplay remain to be discovered. Here, we report that self-organization of myoblasts around integer topological defects, namely spirals and asters, triggers localized differentiation and, when differentiation is inhibited, drives the growth of cylindrical multicellular protrusions. Both localized differentiation and growth require specific stress patterns. By analyzing the experimental velocity and orientation profiles through active gel theory, we show that integer topological defects can concentrate compressive stresses, which we measure by using deformable pillars. Altogether, we envision topological defects as mechanical organizational centers that control differentiation and morphogenesis to establish tissue architecture.

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