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Quantitative analysis of tissue deformation dynamics reveals three characteristic growth modes and globally aligned anisotropic tissue deformation during chick limb development.

Morishita Y, Kuroiwa A, Suzuki T - Development (2015)

Bottom Line: We also found anisotropic tissue deformation along the proximal-distal axis.Morphogenetic simulation and experimental studies suggested that this directional tissue elongation, and not local growth, has the greatest impact on limb shaping.Our study marks a pivotal point for multi-scale system understanding in vertebrate development.

View Article: PubMed Central - PubMed

Affiliation: Laboratory for Developmental Morphogeometry, RIKEN Quantitative Biology Center, Kobe 650-0047, Japan RIKEN Center for Developmental Biology, Kobe 650-0047, Japan yoshihiro.morishita@riken.jp suzuki.takayuki@j.mbox.nagoya-u.ac.jp.

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Tissue-level characterization of deformation dynamics. Global organ deformation is defined by map ϕ (A), and local tissue deformation is defined by the deformation gradient tensor F (B). Tissue growth rate and deformation anisotropy are two key characteristics. (C-E) Examples of local tissue deformation, with different values for deformation anisotropy, identical tissue growth rate and identical deformation anisotropy, respectively. (F) Cell trajectory or velocity in a growing tissue appears different, depending on the position of the camera, even if tissue deformation dynamics are identical. Here, the case of spatially uniform growth is shown. (G) Possible scenarios for deformation dynamics at each stage (artificially generated by computer simulations). For each stage, different deformation dynamics, producing the same morphology, are possible. The heat maps indicate spatial patterns of tissue growth rate (left) and deformation anisotropy (right). Black arrows represent the orientation of the principal stretch at each position [see the higher magnification view in case (2-b) for an example]. In case (1-a), the morphology in the middle panel is achieved by distally biased volume growth and anisotropy of tissue deformation along the proximo-distal axis. In case (1-b), spatially uniform volume growth and proximally biased anisotropic tissue deformation generate the same morphology, and in case (1-c), the same morphology is also realized by a more complex deformation pattern with posteriorly biased tissue growth. The deformation dynamics can change with developmental stage [cases (2-a) and (2-b)].
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DEV109728F1: Tissue-level characterization of deformation dynamics. Global organ deformation is defined by map ϕ (A), and local tissue deformation is defined by the deformation gradient tensor F (B). Tissue growth rate and deformation anisotropy are two key characteristics. (C-E) Examples of local tissue deformation, with different values for deformation anisotropy, identical tissue growth rate and identical deformation anisotropy, respectively. (F) Cell trajectory or velocity in a growing tissue appears different, depending on the position of the camera, even if tissue deformation dynamics are identical. Here, the case of spatially uniform growth is shown. (G) Possible scenarios for deformation dynamics at each stage (artificially generated by computer simulations). For each stage, different deformation dynamics, producing the same morphology, are possible. The heat maps indicate spatial patterns of tissue growth rate (left) and deformation anisotropy (right). Black arrows represent the orientation of the principal stretch at each position [see the higher magnification view in case (2-b) for an example]. In case (1-a), the morphology in the middle panel is achieved by distally biased volume growth and anisotropy of tissue deformation along the proximo-distal axis. In case (1-b), spatially uniform volume growth and proximally biased anisotropic tissue deformation generate the same morphology, and in case (1-c), the same morphology is also realized by a more complex deformation pattern with posteriorly biased tissue growth. The deformation dynamics can change with developmental stage [cases (2-a) and (2-b)].

Mentions: In characterizing the macroscopic deformation patterns of tissues that are composed of a large number of cells, it is useful to regard them as continuums, by neglecting or averaging out the variability in the shapes and sizes of individual cells. In the case of the chick limb bud, there are millions of cells, and thus the continuum approach is appropriate. When an organ is regarded as a continuum, its deformation is mathematically described as a map (Bonet and Wood, 2008), i.e. the relationship between the spatial coordinates of each unit of tissue or landmark (e.g. small populations of cells) before and after deformation (Fig. 1A; Materials and Methods). Such a positional relationship, of course, might to some extent be different between embryos. The map we refer to here is an average over multiple embryos; smaller variability in tissue deformation between embryos from the average map indicates that the morphogenetic process is more robust and deterministic.Fig. 1.


Quantitative analysis of tissue deformation dynamics reveals three characteristic growth modes and globally aligned anisotropic tissue deformation during chick limb development.

Morishita Y, Kuroiwa A, Suzuki T - Development (2015)

Tissue-level characterization of deformation dynamics. Global organ deformation is defined by map ϕ (A), and local tissue deformation is defined by the deformation gradient tensor F (B). Tissue growth rate and deformation anisotropy are two key characteristics. (C-E) Examples of local tissue deformation, with different values for deformation anisotropy, identical tissue growth rate and identical deformation anisotropy, respectively. (F) Cell trajectory or velocity in a growing tissue appears different, depending on the position of the camera, even if tissue deformation dynamics are identical. Here, the case of spatially uniform growth is shown. (G) Possible scenarios for deformation dynamics at each stage (artificially generated by computer simulations). For each stage, different deformation dynamics, producing the same morphology, are possible. The heat maps indicate spatial patterns of tissue growth rate (left) and deformation anisotropy (right). Black arrows represent the orientation of the principal stretch at each position [see the higher magnification view in case (2-b) for an example]. In case (1-a), the morphology in the middle panel is achieved by distally biased volume growth and anisotropy of tissue deformation along the proximo-distal axis. In case (1-b), spatially uniform volume growth and proximally biased anisotropic tissue deformation generate the same morphology, and in case (1-c), the same morphology is also realized by a more complex deformation pattern with posteriorly biased tissue growth. The deformation dynamics can change with developmental stage [cases (2-a) and (2-b)].
© Copyright Policy - open-access
Related In: Results  -  Collection

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DEV109728F1: Tissue-level characterization of deformation dynamics. Global organ deformation is defined by map ϕ (A), and local tissue deformation is defined by the deformation gradient tensor F (B). Tissue growth rate and deformation anisotropy are two key characteristics. (C-E) Examples of local tissue deformation, with different values for deformation anisotropy, identical tissue growth rate and identical deformation anisotropy, respectively. (F) Cell trajectory or velocity in a growing tissue appears different, depending on the position of the camera, even if tissue deformation dynamics are identical. Here, the case of spatially uniform growth is shown. (G) Possible scenarios for deformation dynamics at each stage (artificially generated by computer simulations). For each stage, different deformation dynamics, producing the same morphology, are possible. The heat maps indicate spatial patterns of tissue growth rate (left) and deformation anisotropy (right). Black arrows represent the orientation of the principal stretch at each position [see the higher magnification view in case (2-b) for an example]. In case (1-a), the morphology in the middle panel is achieved by distally biased volume growth and anisotropy of tissue deformation along the proximo-distal axis. In case (1-b), spatially uniform volume growth and proximally biased anisotropic tissue deformation generate the same morphology, and in case (1-c), the same morphology is also realized by a more complex deformation pattern with posteriorly biased tissue growth. The deformation dynamics can change with developmental stage [cases (2-a) and (2-b)].
Mentions: In characterizing the macroscopic deformation patterns of tissues that are composed of a large number of cells, it is useful to regard them as continuums, by neglecting or averaging out the variability in the shapes and sizes of individual cells. In the case of the chick limb bud, there are millions of cells, and thus the continuum approach is appropriate. When an organ is regarded as a continuum, its deformation is mathematically described as a map (Bonet and Wood, 2008), i.e. the relationship between the spatial coordinates of each unit of tissue or landmark (e.g. small populations of cells) before and after deformation (Fig. 1A; Materials and Methods). Such a positional relationship, of course, might to some extent be different between embryos. The map we refer to here is an average over multiple embryos; smaller variability in tissue deformation between embryos from the average map indicates that the morphogenetic process is more robust and deterministic.Fig. 1.

Bottom Line: We also found anisotropic tissue deformation along the proximal-distal axis.Morphogenetic simulation and experimental studies suggested that this directional tissue elongation, and not local growth, has the greatest impact on limb shaping.Our study marks a pivotal point for multi-scale system understanding in vertebrate development.

View Article: PubMed Central - PubMed

Affiliation: Laboratory for Developmental Morphogeometry, RIKEN Quantitative Biology Center, Kobe 650-0047, Japan RIKEN Center for Developmental Biology, Kobe 650-0047, Japan yoshihiro.morishita@riken.jp suzuki.takayuki@j.mbox.nagoya-u.ac.jp.

Show MeSH
Related in: MedlinePlus