Making sense in biology: an appreciation of Julian Lewis

Lander, Arthur D.

doi:10.1186/s12915-014-0057-5

Cited by 4 publications

(4 citation statements)

References 6 publications

(6 reference statements)

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“…Because the her7;hes6 double mutant is segmented normally in most cases, we assume that her1 is sufficient to drive the cellular oscillators in the PSM. In appreciation of Julian Lewis, we show that his simple initial her1 model is still remarkably powerful (Lewis, 2003;Lander, 2014). It is the key which we use to understand the principles governing the travelling wave that controls the rhythmicity of the vertebrate segmentation.…”

Section: A Reduced Mechanistic Model Recapitulates Travelling Waves Imentioning

confidence: 91%

Travelling waves in somitogenesis: Collective cellular properties emerge from time-delayed juxtacrine oscillation coupling

Tomka

Iber

Boareto

2018

Progress in Biophysics and Molecular Biology

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The sculpturing of the vertebrate body plan into segments begins with the sequential formation of somites in the presomitic mesoderm (PSM). The rhythmicity of this process is controlled by travelling waves of gene expression. These kinetic waves emerge from coupled cellular oscillators and sweep across the PSM. In zebrafish, the oscillations are driven by autorepression of her genes and are synchronized via Notch signalling. Mathematical modelling has played an important role in explaining how collective properties emerge from the molecular interactions. Increasingly more quantitative experimental data permits the validation of those mathematical models, yet leads to increasingly more complex model formulations that hamper an intuitive understanding of the underlying mechanisms. Here, we review previous efforts, and design a mechanistic model of the her1 oscillator, which represents the experimentally viable her7;hes6 double mutant. This genetically simplified system is ideally suited to conceptually recapitulate oscillatory entrainment and travelling wave formation, and to highlight open questions. It shows that three key parameters, the autorepression delay, the juxtacrine coupling delay, and the coupling strength, are sufficient to understand the emergence of the collective period, the collective amplitude, and the synchronization of neighbouring Her1 oscillators. Moreover, two spatiotemporal time delay gradients, in the autorepression and in the juxtacrine signalling, are required to explain the collective oscillatory dynamics and synchrony of PSM cells. The highlighted developmental principles likely apply more generally to other developmental processes, including neurogenesis and angiogenesis.

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Section: A Reduced Mechanistic Model Recapitulates Travelling Waves Imentioning

confidence: 91%

Travelling waves in somitogenesis: Collective cellular properties emerge from time-delayed juxtacrine oscillation coupling

Tomka

Iber

Boareto

2018

Progress in Biophysics and Molecular Biology

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“…Modelling temporal and spatial variations in biological systems is essential for understanding their dynamic responses to external perturbations and/or endogenous developmental processes (Rantalainen et al, 2008 [ 24 ]; Lander, 2014 [ 25 ]). In the presented study we applied PCA, and OPLS regression to analyze spatial patterns in the data (which are also temporal patterns, as the spatial progression from cambial initials to mature phloem and xylem reflect chronological developmental sequences).…”

Section: Methodsmentioning

confidence: 99%

Quantitative proteomics reveals protein profiles underlying major transitions in aspen wood development

et al. 2016

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BackgroundWood development is of outstanding interest both to basic research and industry due to the associated cellulose and lignin biomass production. Efforts to elucidate wood formation (which is essential for numerous aspects of both pure and applied plant science) have been made using transcriptomic analyses and/or low-resolution sampling. However, transcriptomic data do not correlate perfectly with levels of expressed proteins due to effects of post-translational modifications and variations in turnover rates. In addition, high-resolution analysis is needed to characterize key transitions. In order to identify protein profiles across the developmental region of wood formation, an in-depth and tissue specific sampling was performed.ResultsWe examined protein profiles, using an ultra-performance liquid chromatography/quadrupole time of flight mass spectrometry system, in high-resolution tangential sections spanning all wood development zones in Populus tremula from undifferentiated cambium to mature phloem and xylem, including cell expansion and cell death zones. In total, we analyzed 482 sections, 20–160 μm thick, from four 47-year-old trees growing wild in Sweden. We obtained high quality expression profiles for 3,082 proteins exhibiting consistency across the replicates, considering that the trees were growing in an uncontrolled environment. A combination of Principal Component Analysis (PCA), Orthogonal Projections to Latent Structures (OPLS) modeling and an enhanced stepwise linear modeling approach identified several major transitions in global protein expression profiles, pinpointing (for example) locations of the cambial division leading to phloem and xylem cells, and secondary cell wall formation zones. We also identified key proteins and associated pathways underlying these developmental landmarks. For example, many of the lignocellulosic related proteins were upregulated in the expansion to the early developmental xylem zone, and for laccases with a rapid decrease in early xylem zones. We observed upregulation of two forms of xylem cysteine protease (Potri.002G005700.1 and Potri.005G256000.2; Pt-XCP2.1) in early xylem and their downregulation in late maturing xylem. Our data also show that Pt-KOR1.3 (Potri.003G151700.2) exhibits an expression pattern that supports the hypothesis put forward in previous studies that this is a key xyloglucanase involved in cellulose biosynthesis in primary cell walls and reduction of cellulose crystallinity in secondary walls.ConclusionOur novel multivariate approach highlights important processes and provides confirmatory insights into the molecular foundations of wood development.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2458-z) contains supplementary material, which is available to authorized users.

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“…Because this mutant is segmented normally in most cases (Schröter et al, 2012), we assume that her1 is sufficient to drive the cellular oscillators in the PSM. In appreciation of Julian Lewis, we show that his simple initial her1 model is still remarkably powerful (Lewis, 2003; Lander, 2014). It is the key, which we use to understand the principles governing the travelling wave that controls the rhythmicity of the vertebrate segmentation.…”

Section: Discussionmentioning

confidence: 84%

Travelling waves in somitogenesis: collective cellular properties emerge from time-delayed juxtacrine oscillation coupling

Tomka

Iber

Boareto

2018

Preprint

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Making sense in biology: an appreciation of Julian Lewis

Cited by 4 publications

References 6 publications

Travelling waves in somitogenesis: Collective cellular properties emerge from time-delayed juxtacrine oscillation coupling

Travelling waves in somitogenesis: Collective cellular properties emerge from time-delayed juxtacrine oscillation coupling

Quantitative proteomics reveals protein profiles underlying major transitions in aspen wood development

Travelling waves in somitogenesis: collective cellular properties emerge from time-delayed juxtacrine oscillation coupling

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