-
Seminars in Cell & Developmental Biology May 2023Recent advances in pluripotent stem cell culture allow researchers to generate not only most embryonic cell types, but also morphologies of many embryonic structures,... (Review)
Review
Recent advances in pluripotent stem cell culture allow researchers to generate not only most embryonic cell types, but also morphologies of many embryonic structures, entirely in vitro. This recreation of embryonic form from naïve cells, known as synthetic morphogenesis, has important implications for both developmental biology and regenerative medicine. However, the capacity of stem cell-based models to recapitulate the morphogenetic cell behaviors that shape natural embryos remains unclear. In this review, we explore several examples of synthetic morphogenesis, with a focus on models of gastrulation and surrounding stages. By varying cell types, source species, and culture conditions, researchers have recreated aspects of primitive streak formation, emergence and elongation of the primary embryonic axis, neural tube closure, and more. Here, we describe cell behaviors within in vitro/ex vivo systems that mimic in vivo morphogenesis and highlight opportunities for more complete models of early development.
Topics: Gastrulation; Morphogenesis
PubMed: 35817656
DOI: 10.1016/j.semcdb.2022.07.002 -
Nature Communications Aug 2022Cranial neural crest cells are an evolutionary innovation of vertebrates for craniofacial development and function, yet the mechanisms that govern the cell fate...
Cranial neural crest cells are an evolutionary innovation of vertebrates for craniofacial development and function, yet the mechanisms that govern the cell fate decisions of postmigratory cranial neural crest cells remain largely unknown. Using the mouse molar as a model, we perform single-cell transcriptome profiling to interrogate the cell fate diversification of postmigratory cranial neural crest cells. We reveal the landscape of transcriptional heterogeneity and define the specific cellular domains during the progression of cranial neural crest cell-derived dental lineage diversification, and find that each domain makes a specific contribution to distinct molar mesenchymal tissues. Furthermore, IGF signaling-mediated cell-cell interaction between the cellular domains highlights the pivotal role of autonomous regulation of the dental mesenchyme. Importantly, we reveal cell-type-specific gene regulatory networks in the dental mesenchyme and show that Foxp4 is indispensable for the differentiation of periodontal ligament. Our single-cell atlas provides comprehensive mechanistic insight into the cell fate diversification process of the cranial neural crest cell-derived odontogenic populations.
Topics: Animals; Cell Differentiation; Gene Expression Regulation, Developmental; Mesoderm; Mice; Morphogenesis; Neural Crest; Odontogenesis; Signal Transduction
PubMed: 35974052
DOI: 10.1038/s41467-022-32490-y -
Biochemical Society Transactions Jun 2020The development of natural tissues, organs and bodies depends on mechanisms of patterning and of morphogenesis, typically (but not invariably) in that order, and often... (Review)
Review
The development of natural tissues, organs and bodies depends on mechanisms of patterning and of morphogenesis, typically (but not invariably) in that order, and often several times at different final scales. Using synthetic biology to engineer patterning and morphogenesis will both enhance our basic understanding of how development works, and provide important technologies for advanced tissue engineering. Focusing on mammalian systems built to date, this review describes patterning systems, both contact-mediated and reaction-diffusion, and morphogenetic effectors. It also describes early attempts to connect the two to create self-organizing physical form. The review goes on to consider how these self-organized systems might be modified to increase the complexity and scale of the order they produce, and outlines some possible directions for future research and development.
Topics: Animals; Body Patterning; Cell Differentiation; Humans; Morphogenesis; Organoids; Receptors, Notch; Signal Transduction; Synthetic Biology; Tissue Engineering
PubMed: 32510150
DOI: 10.1042/BST20200013 -
Philosophical Transactions of the Royal... Oct 2020
Topics: Animals; Morphogenesis; Plant Development
PubMed: 32829677
DOI: 10.1098/rstb.2019.0549 -
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 -
Developmental Cell Jun 2019Self-organization is pervasive in development, from symmetry breaking in the early embryo to tissue patterning and morphogenesis. For a few model systems, the underlying... (Review)
Review
Self-organization is pervasive in development, from symmetry breaking in the early embryo to tissue patterning and morphogenesis. For a few model systems, the underlying molecular and cellular processes are now sufficiently characterized that mathematical models can be confronted with experiments, to explore the dynamics of pattern formation. Here, we review selected systems, ranging from cyanobacteria to mammals, where different forms of cell-cell communication, acting alone or together with positional cues, drive the patterning of cell fates, highlighting the insights that even very simple models can provide as well as the challenges on the path to a predictive understanding of development.
Topics: Animals; Body Patterning; Cell Communication; Cell Differentiation; Mammals; Models, Biological; Morphogenesis
PubMed: 31163171
DOI: 10.1016/j.devcel.2019.05.019 -
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 -
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 -
Current Topics in Developmental Biology 2021As multi-cellular organisms evolved from small clusters of cells to complex metazoans, biological tubes became essential for life. Tubes are typically thought of as... (Review)
Review
As multi-cellular organisms evolved from small clusters of cells to complex metazoans, biological tubes became essential for life. Tubes are typically thought of as mainly playing a role in transport, with the hollow space (lumen) acting as a conduit to distribute nutrients and waste, or for gas exchange. However, biological tubes also provide a platform for physiological, mechanical, and structural functions. Indeed, tubulogenesis is often a critical aspect of morphogenesis and organogenesis. C. elegans is made up of tubes that provide structural support and protection (the epidermis), perform the mechanical and enzymatic processes of digestion (the buccal cavity, pharynx, intestine, and rectum), transport fluids for osmoregulation (the excretory system), and execute the functions necessary for reproduction (the germline, spermatheca, uterus and vulva). Here we review our current understanding of the genetic regulation, molecular processes, and physical forces involved in tubulogenesis and morphogenesis of the epidermal, digestive and excretory systems in C. elegans.
Topics: Animals; Caenorhabditis elegans; Female; Morphogenesis; Organogenesis
PubMed: 33992152
DOI: 10.1016/bs.ctdb.2020.12.012 -
Developmental Biology Aug 2022Myriads forces are at play during morphogenesis. Their concerted activity shapes individual cells, tissues and the whole embryo, representing the most awe-inspiring... (Review)
Review
Myriads forces are at play during morphogenesis. Their concerted activity shapes individual cells, tissues and the whole embryo, representing the most awe-inspiring marvel of developmental biology. In spite of their prevalence, the potential instructive role of cell mechanics in fate determination and patterning has remained long neglected, in part due to the difficulties in translating the physical world of cells in molecular terms. The recent discovery of the principles of mechanotransduction, of how these impact on gene expression, is however starting to change this scenario, making mechanotransduction finally amenable to experimental dissection through genetics, molecular and bioengineering approaches. Here we review this emerging field, and a series of discoveries that potently bring back cell mechanics at the centerstage of vertebrate developmental biology. We discuss the role of actomyosin contractility as integrating platform between morphogens, lateral inhibition and mechanosignaling. We also review data indicating that supracellular pulling forces, coupled with solid-to-fluid changes in the material contexture of embryonic fields, may act as overarching mechanical "organizers". The evidence also indicates that a continuum of forces is what ultimately locks "self-organizing" movements with cell fate, from the earliest pre-implantation decisions to the fine details of organogenesis. Notably, similar mechanisms are reawakened in organoids and in adult tissues during regeneration. Developmental biology has been correctly depicted, but recently often forgotten, as the "mother" of all biological disciplines. Investigations in developmental mechanics may revamp interest, and have a broad impact in the fields of regenerative medicine, stem cells and cancer biology.
Topics: Actomyosin; Animals; Embryonic Development; Mechanotransduction, Cellular; Morphogenesis; Organogenesis; Vertebrates
PubMed: 35580730
DOI: 10.1016/j.ydbio.2022.05.005