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Seminars in Cell & Developmental Biology Nov 2022Lumens, liquid-filled cavities surrounded by polarized tissue cells, are elementary units involved in the morphogenesis of organs. Theoretical modeling and computations,... (Review)
Review
Lumens, liquid-filled cavities surrounded by polarized tissue cells, are elementary units involved in the morphogenesis of organs. Theoretical modeling and computations, which can integrate various factors involved in biophysics of morphogenesis of cell assembly and lumens, may play significant roles to elucidate the mechanisms in formation of such complex tissue with lumens. However, up to present, it has not been documented well what computational approaches or frameworks can be applied for this purpose and how we can choose the appropriate approach for each problem. In this review, we report some typical lumen morphologies and basic mechanisms for the development of lumens, focusing on three keywords - mechanics, hydraulics and geometry - while outlining pros and cons of the current main computational strategies. We also describe brief guidance of readouts, i.e., what we should measure in experiments to make the comparison with the model's assumptions and predictions.
Topics: Cell Polarity; Morphogenesis
PubMed: 35773151
DOI: 10.1016/j.semcdb.2022.05.021 -
Seminars in Cell & Developmental Biology Oct 2022The blastocoel is a fluid-filled cavity characteristic of animal embryos at the blastula stage. Its emergence is commonly described as the result of cleavage patterning,... (Review)
Review
The blastocoel is a fluid-filled cavity characteristic of animal embryos at the blastula stage. Its emergence is commonly described as the result of cleavage patterning, but this historical view conceals a large diversity of mechanisms and overlooks many unsolved questions from a biophysics perspective. In this review, we describe generic mechanisms for blastocoel morphogenesis, rooted in biological literature and simple physical principles. We propose novel directions of study and emphasize the importance to study blastocoel morphogenesis as an evolutionary and physical continuum.
Topics: Animals; Biophysics; Blastocyst; Morphogenesis
PubMed: 34756494
DOI: 10.1016/j.semcdb.2021.10.005 -
Nature Methods Nov 2023
Topics: Models, Biological; Morphogenesis
PubMed: 37935984
DOI: 10.1038/s41592-023-02075-8 -
Cells Jan 2022Early limb bud development has been of considerable interest for the study of embryological development and especially morphogenesis. The focus has long been on... (Review)
Review
Early limb bud development has been of considerable interest for the study of embryological development and especially morphogenesis. The focus has long been on biochemical signalling and less on cell biomechanics and mechanobiology. However, their importance cannot be understated since tissue shape changes are ultimately controlled by active forces and bulk tissue rheological properties that in turn depend on cell-cell interactions as well as extracellular matrix composition. Moreover, the feedback between gene regulation and the biomechanical environment is still poorly understood. In recent years, novel experimental techniques and computational models have reinvigorated research on this biomechanical and mechanobiological side of embryological development. In this review, we consider three stages of early limb development, namely: outgrowth, elongation, and condensation. For each of these stages, we summarize basic biological regulation and examine the role of cellular and tissue mechanics in the morphogenetic process.
Topics: Biomechanical Phenomena; Embryonic Development; Limb Buds; Morphogenesis; Signal Transduction
PubMed: 35159230
DOI: 10.3390/cells11030420 -
Seminars in Cell & Developmental Biology Dec 2021Morphogenesis drives the formation of functional living shapes. Gene expression patterns and signaling pathways define the body plans of the animal and control the... (Review)
Review
Morphogenesis drives the formation of functional living shapes. Gene expression patterns and signaling pathways define the body plans of the animal and control the morphogenetic processes shaping the embryonic tissues. During embryogenesis, a tissue can undergo composite morphogenesis resulting from multiple concomitant shape changes. While previous studies have unraveled the mechanisms that drive simple morphogenetic processes, how a tissue can undergo multiple and simultaneous changes in shape is still not known and not much explored. In this chapter, we focus on the process of concomitant tissue folding and extension that is vital for the animal since it is key for embryo gastrulation and neurulation. Recent pioneering studies focus on this problem highlighting the roles of different spatially coordinated cell mechanisms or of the synergy between different patterns of gene expression to drive composite morphogenesis.
Topics: Animals; Embryonic Development; Morphogenesis
PubMed: 34172395
DOI: 10.1016/j.semcdb.2021.06.007 -
Molecular Plant Jul 2022Plants produce a rich diversity of biological forms, and the diversity of leaves is especially notable. Mechanisms of leaf morphogenesis have been studied in the past... (Review)
Review
Plants produce a rich diversity of biological forms, and the diversity of leaves is especially notable. Mechanisms of leaf morphogenesis have been studied in the past two decades, with a growing focus on the interactive roles of mechanics in recent years. Growth of plant organs involves feedback by mechanical stress: growth induces stress, and stress affects growth and morphogenesis. Although much attention has been given to potential stress-sensing mechanisms and cellular responses, the mechanical principles guiding morphogenesis have not been well understood. Here we synthesize the overarching roles of mechanics and mechanical stress in multilevel and multiple stages of leaf morphogenesis, encompassing leaf primordium initiation, phyllotaxis and venation patterning, and the establishment of complex mature leaf shapes. Moreover, the roles of mechanics at multiscale levels, from subcellular cytoskeletal molecules to single cells to tissues at the organ scale, are articulated. By highlighting the role of mechanical buckling in the formation of three-dimensional leaf shapes, this review integrates the perspectives of mechanics and biology to provide broader insights into the mechanobiology of leaf morphogenesis.
Topics: Morphogenesis; Organogenesis, Plant; Plant Leaves; Plants; Stress, Mechanical
PubMed: 35662674
DOI: 10.1016/j.molp.2022.05.015 -
Development, Growth & Differentiation Jun 2023We review several mathematical models and concepts in developmental biology that have been established over the last decade. (1) Feedback vertex set: Ascidian embryos... (Review)
Review
We review several mathematical models and concepts in developmental biology that have been established over the last decade. (1) Feedback vertex set: Ascidian embryos contain cells of seven types, and cell fate is controlled by ~100 interacting genes. The "feedback vertex set" of the directed graph of the gene regulatory network consists of a small number of genes. By experimentally manipulating them, we can differentiate cells into any cell type. (2) Tissue deformation: Describing morphological changes in tissues and relating them to gene expression and other cellular processes is key in understanding morphogenesis. Expansion and anisotropy of the tissue are described by a "deformation tensor" at each location. A study on chick limb bud formation revealed that both the volume growth rate and anisotropy in deformation differed significantly between locations and stages. (3) Mechanobiology: Forces operating on each cell may alter cell shape and gene expression, which may subsequently exert forces on their surroundings. Measurements of force, tissue shape, and gene expression help us understand autonomous tissue deformation. (4) Adaptive design of development: An optimal growth schedule in fluctuating environments explains the growth response to starvation in Drosophila larvae. Adaptive placement of morphogen sources makes development robust to noises.
Topics: Animals; Morphogenesis; Cell Differentiation; Organogenesis; Drosophila; Models, Biological
PubMed: 37190873
DOI: 10.1111/dgd.12856 -
Philosophical Transactions of the Royal... Oct 2020Cell intercalation is a key topological transformation driving tissue morphogenesis, homeostasis and diseases such as cancer cell invasion. In recent years, much work... (Review)
Review
Cell intercalation is a key topological transformation driving tissue morphogenesis, homeostasis and diseases such as cancer cell invasion. In recent years, much work has been undertaken to better elucidate the fundamental mechanisms controlling intercalation. Cells often use protrusions to propel themselves in between cell neighbours, resulting in topology changes. Nevertheless, in simple epithelial tissues, formed by a single layer of densely packed prism-shaped cells, topology change takes place in an astonishing fashion: cells exchange neighbours medio-laterally by conserving their apical-basal architecture and by maintaining an intact epithelial layer. Medio-lateral cell intercalation in simple epithelia is thus an exemplary case of both robustness and plasticity. Interestingly, in simple epithelia, cells use a combinatory set of mechanisms to ensure a topological transformation at the apical and basal sides. This article is part of the discussion meeting issue 'Contemporary morphogenesis'.
Topics: Animals; Drosophila; Embryo, Nonmammalian; Epithelial Cells; Gastrulation; Morphogenesis
PubMed: 32829682
DOI: 10.1098/rstb.2019.0552 -
Integrative and Comparative Biology Dec 2023While the modern framework of evolutionary development (evo-devo) has been decidedly genetic, historic analyses have also considered the importance of mechanics in the... (Review)
Review
While the modern framework of evolutionary development (evo-devo) has been decidedly genetic, historic analyses have also considered the importance of mechanics in the evolution of form. With the aid of recent technological advancements in both quantifying and perturbing changes in the molecular and mechanical effectors of organismal shape, how molecular and genetic cues regulate the biophysical aspects of morphogenesis is becoming increasingly well studied. As a result, this is an opportune time to consider how the tissue-scale mechanics that underlie morphogenesis are acted upon through evolution to establish morphological diversity. Such a focus will enable a field of evo-devo mechanobiology that will serve to better elucidate the opaque relations between genes and forms by articulating intermediary physical mechanisms. Here, we review how the evolution of shape is measured and related to genetics, how recent strides have been made in the dissection of developmental tissue mechanics, and how we expect these areas to coalesce in evo-devo studies in the future.
Topics: Animals; Biological Evolution; Developmental Biology; Morphogenesis
PubMed: 37193661
DOI: 10.1093/icb/icad033 -
Annual Review of Cell and Developmental... Oct 2021Morphogenesis is one of the most remarkable examples of biological pattern formation. Despite substantial progress in the field, we still do not understand the... (Review)
Review
Morphogenesis is one of the most remarkable examples of biological pattern formation. Despite substantial progress in the field, we still do not understand the organizational principles responsible for the robust convergence of the morphogenesis process across scales to form viable organisms under variable conditions. Achieving large-scale coordination requires feedback between mechanical and biochemical processes, spanning all levels of organization and relating the emerging patterns with the mechanisms driving their formation. In this review, we highlight the role of mechanics in the patterning process, emphasizing the active and synergistic manner in which mechanical processes participate in developmental patterning rather than merely following a program set by biochemical signals. We discuss the value of applying a coarse-grained approach that considers the large-scale dynamics and feedback and complements the reductionist approach focused on molecular detail. A central challenge in this approach is identifying relevant coarse-grained variables and developing effective theories that can serve as a basis for an integrated framework toward understanding this remarkable pattern-formation process.
Topics: Animals; Morphogenesis
PubMed: 34242058
DOI: 10.1146/annurev-cellbio-120319-030931