Waves and patterning in developmental biology: vertebrate segmentation and feather bud formation as case studies

Baker, Ruth E.; Schnell, Santiago; Maini, Philip K.

doi:10.1387/ijdb.072493rb

Cited by 33 publications

(30 citation statements)

References 102 publications

(147 reference statements)

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“…There is mounting evidence for the validity of Turing-based models to explain pattern evolution in several diverse biological systems, including feather bud arrangements (Baker et al, 2009), hair follicle spacing (Maini et al, 2006;Sick et al, 2006), palatal rugae distribution (Economou et al, 2012), tongue papilla patterning (Zhou et al, 2006), digit patterning (Raspopovic et al, 2014) and zebrafish mesodermal pigmentation (Eom et al, 2012;Kondo and Miura, 2010), and it is interesting that Bmp ligands Development (2016Development ( ) 143, 427-436 doi:10.1242 appear to act as Turing inhibitors in several of these systems (Garfinkel et al, 2004;Harris et al, 2005;Mou et al, 2011). In the intestine, we have seen that several different Bmp ligands are expressed by clusters (Bmp2, 4, 5, 7) and functional assays indicate that high concentrations of all of these Bmps act to inhibit the formation of clusters (Fig.…”

Section: Discussionmentioning

confidence: 99%

Villification in the mouse: Bmp signals control intestinal villus patterning

et al. 2015

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In the intestine, finger-like villi provide abundant surface area for nutrient absorption. During murine villus development, epithelial Hedgehog (Hh) signals promote aggregation of subepithelial mesenchymal clusters that drive villus emergence. Clusters arise first dorsally and proximally and spread over the entire intestine within 24 h, but the mechanism driving this pattern in the murine intestine is unknown. In chick, the driver of cluster pattern is tensile force from developing smooth muscle, which generates deep longitudinal epithelial folds that locally concentrate the Hh signal, promoting localized expression of cluster genes. By contrast, we show that in mouse, muscle-induced epithelial folding does not occur and artificial deformation of the epithelium does not determine the pattern of clusters or villi. In intestinal explants, modulation of Bmp signaling alters the spatial distribution of clusters and changes the pattern of emerging villi. Increasing Bmp signaling abolishes cluster formation, whereas inhibiting Bmp signaling leads to merged clusters. These dynamic changes in cluster pattern are faithfully simulated by a mathematical model of a Turing field in which an inhibitor of Bmp signaling acts as the Turing activator. In vivo, genetic interruption of Bmp signal reception in either epithelium or mesenchyme reveals that Bmp signaling in Hh-responsive mesenchymal cells controls cluster pattern. Thus, unlike in chick, the murine villus patterning system is independent of muscle-induced epithelial deformation. Rather, a complex cocktail of Bmps and Bmp signal modulators secreted from mesenchymal clusters determines the pattern of villi in a manner that mimics the spread of a self-organizing Turing field.

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Section: Discussionmentioning

confidence: 99%

Villification in the mouse: Bmp signals control intestinal villus patterning

et al. 2015

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“…During cluster patterning, evidence suggests that Bmp ligands act as the Turing inhibitor while modifiers of Bmp signaling, such as twisted gastrulation (Twsg1), may comprise the Turing activator (Walton et al, 2016). Thus, intestinal mesenchymal cluster patterning can be added to a growing list of biological systems that behave in accord with the Turing model, including: patterning of digits (Raspopovic et al, 2014), chick feather buds (Baker et al, 2009), hair follicles (Maini et al, 2006;Sick et al, 2006), zebrafish mesodermal pigment (Eom et al, 2012) and tongue papillae (Zhou et al, 2006). In summary, murine villus development occurs through rapid conversion of a thick pseudostratified epithelial tube into a regular field of patterned villus domes, a process initiated by epithelially secreted Hh ligands.…”

Section: Villus Formation and Patterning In The Mousementioning

confidence: 99%

Generation of intestinal surface: an absorbing tale

et al. 2016

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The vertebrate small intestine requires an enormous surface area to effectively absorb nutrients from food. Morphological adaptations required to establish this extensive surface include generation of an extremely long tube and convolution of the absorptive surface of the tube into villi and microvilli. In this Review, we discuss recent findings regarding the morphogenetic and molecular processes required for intestinal tube elongation and surface convolution, examine shared and unique aspects of these processes in different species, relate these processes to known human maladies that compromise absorptive function and highlight important questions for future research.

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“…The mathematical formulation is preferable due to the clear advantage of yielding analytical analyses. Moreover, biological interactions and processes are often nonlinear, and this is where intuitive, verbal reasoning may let us down; whereas mathematical methods allow us to analyse diverse biological processes (Baker et al 2009). …”

Section: Animal Growth Modelsmentioning

confidence: 99%

An Analytical Model of Animal Growth

Stass¹

2017

ESJ

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The purpose of this study was to explain some aspects of ontogenetic growth in pigs by analysing the relationships between variables that are significant to the development of animals. The novelty of the study is a new modelling approach to the growth problem, with the attention that has been paid to both a new set of variables, and an analytical discrete-continuous hybrid model, innovative for the field. This is a first species-specific hybrid model for animal growth formulated in discrete-time difference equation technique. The efficiency of the model is not only due to the modelling technique but also due to a set of relevant variables, especially a feed conversion coefficient, which provides a link between macro and micro physiological scales. The model is based on functional relationships between relevant variables acquired from experimental data analyses, and field observations. The concept explains some aspects of growth in pigs from 30 kg to 600 kg, which is considered the maximum individual weight for a boar, and further growth up to a species maximum weight. The model predicts that boar can reach their maximum individual weight of 600 kg when 6,40 years old and are required to consume 62,51 kg of feed to put on the last kilogram. The phenotypes that can attain their maximum individual weight go through bifurcation of the growth trajectory, a transform in the growth mode. After bifurcation, the smallest number of the phenotypes go on the growth trajectory that leads to a set of species maximum weights of over 1205 kg, and the greatest number of phenotypes continue to live until aged 24,90 years, provided their maximum weights do not change. The study includes growth rate equations, identifies species maximum weight phenotypes, and produces insight into pig longevity. The results suggest that species maximum weight growth trajectories are phenotype-dependant. A modified discrete-time difference equation technique combined with standard continuum methods is an appropriate formalism to model ontogenetic growth in animals.

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Waves and patterning in developmental biology: vertebrate segmentation and feather bud formation as case studies

Cited by 33 publications

References 102 publications

Villification in the mouse: Bmp signals control intestinal villus patterning

Villification in the mouse: Bmp signals control intestinal villus patterning

Generation of intestinal surface: an absorbing tale

An Analytical Model of Animal Growth

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