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Biology subjects

Ryan, A. Q.

Publications and source records attributed to Ryan, A. Q..

4 recordsLinked to original sources

SpinePy enables automated 3D spatiotemporal quantification of multicellular in vitro systems

Organoids and stem-cell-based embryo models such as gastruloids are powerful systems to quantitatively study morphogenesis and patterning. This requires 3D analysis in reference frames that emerge dynamically over development, but are less stereotypical than in vivo. Meaningful statistical comparison and interpretation of biological and physical quantities in space and time -- such as signaling activity, gene expression or cell flows -- depend on proper quantification in these internal and dynamic coordinate systems, especially in in vitro systems that naturally exhibit larger variation. Here, we present a computational framework, packaged as a modular Python toolkit termed SpinePy, that identifies the emergent primary body axis ("spine") of individual gastruloids and constructs a local, dynamic coordinate system aligned to their morphology. SpinePy enables 3D quantification relative to evolving axes and statistical comparisons of morphodynamics, patterning, and densities across structures with varying geometries. We validate and benchmark SpinePy using both synthetic and experimental gastruloid data, providing practical insights into method performance. Using this framework, we generate 3D patterning maps from gastruloids formed with different initial cell numbers (N0). This reveals distinct patterning classes that are better explained by gastruloid volumes than by N0. While demonstrated in gastruloids, SpinePy is broadly applicable to any multicellular system where analysis relative to evolving internal axes is needed, advancing quantitative and comparative spatial biology.

developmental biology↗

Timely neurogenesis enables increased nuclear packing order during neuronal lamination

The coordination of cell proliferation, migration, and differentiation is crucial for organogenesis in many tissues, including the central nervous system and other organs that arise from pseudostratified epithelia (PSE). PSE feature densely packed elongated epithelial cells, with nuclei positioned along the apicobasal cell axis in a cell cycle-dependent manner. Also, PSE serve as organ precursors in diverse developmental contexts across evolution. While the role of nuclear movements in PSE has been extensively studied, less is known about whether and how their nuclear packing arrangements and changes of packing state influence tissue morphogenesis. To address this, we analyzed nuclear shapes, sizes and neighborhood statistics by segmenting nuclei in 3D and over development in zebrafish retinal neuroepithelia (RNE). We find that in PSE nuclei exhibit orientational, nematic-like order but remain positionally disordered. This pattern is conserved in other, less packed, neuroepithelia, like the hindbrain, suggesting that nematic-like order is a hallmark of pseudostratification. Our analysis during retinal development also revealed that nuclear packing density increases, approaching theoretical packing limits for disordered monodisperse ellipsoids at stages when the tissue transitions to a laminated neuronal structure. As neurogenesis progresses, nuclear shapes are remodeled, enabling the RNE to shift to a crystalline, ordered structure, while maintaining orientational alignment. Failure to initiate neurogenesis results in severe tissue deformations due to increased buckling instability. Our results thus show an instance where nuclear shape and nuclear positioning and their changes are essential for proper retinal morphogenesis, a phenomenon most likely also found in other tissue arrangements.

developmental biology↗

Tissue scale properties of the extracellular matrix regulates nuclear shape, organisation and fate in the embryonic midline sutures

Balancing self-renewal and differentiation is a key feature of every stem cell niche and one that is tuned by mechanical interactions of cells with their neighbors and surrounding extracellular matrix. The fibrous stem cell niches that develop as sutures between skull bones must balance the complex extracellular environment that emerges to define them with self-renewal and bone production. Here, we address the role for physical stimuli in suture development by probing the relationship between nuclear shape, organization and gene expression in response to a developing collagen network in embryonic midline sutures. This work complements genetic approaches used to study sutures and provides the first quantitative analyses of physical structure in these sutures. By combining multiple imaging modalities with novel shape description, in addition to network analysis methods, we find the early emergence of a complex extracellular collagen network to have an important role in regulating morphogenesis and cell fate. We show that disrupted collagen crosslinking can alter ECM organization of midline sutures as well as stimulate expression of bone differentiation markers. Further, our findings suggest that in vivo, skeletal tissues can uncouple the response of the nuclear lamina from collagen mediated tissue stiffening seen in vitro. Our findings highlight a crucial relationship between the cellular microenvironment, tissue stiffness and geometry with gene expression in normal development and maintenance of progenitor fate in embryonic sutures.

developmental biology↗

Lumen expansion facilitates epiblast-primitive endoderm fate specification in the mouse blastocyst formation.

Mouse blastocyst formation involves lumen formation and cell fate specification. While many studies have investigated how the blastocyst cell lineages are specified through genetics and signaling, studies into the potential role of the fluid lumen have yet to be conducted. We discover that blastocyst fluid emerges by secretion of cytoplasmic vesicles to intercellular space in addition to trans-epithelial flow. We observe that the beginning of epiblast and primitive endoderm spatial segregation directly follows lumen coalescence. Notably, we show that perturbing lumen expansion by pharmacological and biophysical means impair the specification and spatial segregation of primitive endoderm cells within the blastocyst. Combined, our results suggest that blastocyst lumen expansion plays a critical role in guiding cell fate specification and positioning. As epithelial tissues typically form lumina, lumen expansion may provide a general mechanism of cell fate control in many tissues.

developmental biology↗