Mechanics of neural tube morphogenesis

Moon, Lauren D.; Xiong, Fengzhu

doi:10.1016/j.semcdb.2021.09.009

Cited by 20 publications

(17 citation statements)

References 204 publications

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Section: Resultsmentioning

confidence: 99%

“…These data show that a higher level of tissue tension impairs the ability of the neural folds to meet and potentially prevents tube closure on the dorsal midline. The increased tension is likely transmitted to the neural epithelium via the non-neural ectoderm, which is known to play a mechanical role in neural tube closure in different systems (Karzbrun et al, 2021;Moon and Xiong, 2021;Morita et al, 2012;Nikolopoulou et al, 2019;Smith and Schoenwolf, 1997). Indeed, some of the sandwiched embryos show a permanently open posterior neural tube despite developing a normal tail fold (Figure 3H), resulting in a phenotype that resembles mammalian Neural Tube Defects (NTDs) such as spina bifida (Wallingford et al, 2013).…”

Section: Vm Mechanics Affect Development Of the Early Embryomentioning

confidence: 99%

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Downregulation of Extraembryonic Tension Controls Body Axis Formation in Avian Embryos

Kunz

Wang

Chan

et al. 2021

Preprint

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Embryonic 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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Section: Resultsmentioning

confidence: 99%

Section: Vm Mechanics Affect Development Of the Early Embryomentioning

confidence: 99%

Downregulation of Extraembryonic Tension Controls Body Axis Formation in Avian Embryos

Kunz

Wang

Chan

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…On the other hand, the mechanical cues can guide cell behaviors and cell fates through mechanotransduction during embryonic development 36 , 41 ; thus, the technique can help understand the interaction between biochemical signaling and biomechanical cues. In addition, the closure of the neural tube is physically driven by both the generated force and the mechanical resistance of the tissue 10 , 12 , 42 . The in situ quantification of the mechanical properties can help decouple the roles of the force and the tissue mechanics and thus allow better elucidation of the biomechanical interactions.…”

Section: Discussionmentioning

confidence: 99%

Time-lapse mechanical imaging of neural tube closure in live embryo using Brillouin microscopy

Handler

Scarcelli

Zhang

2023

Sci Rep

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Neural tube closure (NTC) is a complex process of embryonic development involving molecular, cellular, and biomechanical mechanisms. While the genetic factors and biochemical signaling have been extensively investigated, the role of tissue biomechanics remains mostly unexplored due to the lack of tools. Here, we developed an optical modality that can conduct time-lapse mechanical imaging of neural plate tissue as the embryo is experiencing neurulation. This technique is based on the combination of a confocal Brillouin microscope and a modified ex ovo culturing of chick embryo with an on-stage incubator. With this technique, for the first time, we captured the mechanical evolution of the neural plate tissue with live embryos. Specifically, we observed the continuous increase in tissue modulus of the neural plate during NTC for ex ovo cultured embryos, which is consistent with the data of in ovo culture as well as previous studies. Beyond that, we found that the increase in tissue modulus was highly correlated with the tissue thickening and bending. We foresee this non-contact and label-free technique opening new opportunities to understand the biomechanical mechanisms in embryonic development.

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“…On the other hand, the mechanical cues can guide cell behaviors and cell fates through mechanotransduction during embryonic development (Miller and Davidson, 2013; Davis and Tapon, 2019); thus, the technique can also help understand the interaction between biochemical signaling and biomechanical cues. In addition, the closure of the neural tube is physically driven by both the generated force and the mechanical resistance of the tissue (Zhou et al, 2015; Galea et al, 2017; Moon and Xiong, 2021). The in-situ quantification of the mechanical properties can help decouple the roles of the force and the tissue mechanics thus allow better elucidation of the biomechanical interaction.…”

Section: Discussionmentioning

confidence: 99%

Time-lapse mechanical imaging of neural tube closure in live embryo using Brillouin microscopy

Handler

Scarcelli

Zhang

2022

Preprint

View full text Add to dashboard Cite

Neural tube closure (NTC) is a complex process of embryonic development involving molecular, cellular, and biomechanical mechanisms. While the genetic factors and biochemical signaling have been extensively investigated, the role of tissue biomechanics remains mostly unexplored due to the lack of tools. Here, we developed a new optical modality that can conduct time-lapse mechanical imaging of neural plate tissue as the embryo is experiencing neurulation. This technique is based on the combination of a confocal Brillouin microscope and an on-stage incubator for the modified ex ovo culturing of chick embryo. With this technique, for the first time, we captured the mechanical evolution of the neural plate tissue with live embryos. Specifically, we observed the continuous stiffening of the neural plate during NTC for ex ovo cultured embryos, which is consistent with the data of in ovo culture as well as previous studies. Beyond that, we found the tissue stiffening was highly correlated with the tissue thickening and bending. We foresee this non-contact and label-free technique can open new opportunities to understand the biomechanical mechanisms in development.

show abstract

Mechanics of neural tube morphogenesis

Cited by 20 publications

References 204 publications

Downregulation of Extraembryonic Tension Controls Body Axis Formation in Avian Embryos

Downregulation of Extraembryonic Tension Controls Body Axis Formation in Avian Embryos

Time-lapse mechanical imaging of neural tube closure in live embryo using Brillouin microscopy

Time-lapse mechanical imaging of neural tube closure in live embryo using Brillouin microscopy

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