Cell biology of embryonic migration - PubMed (original) (raw)
Review
Cell biology of embryonic migration
Satoshi Kurosaka et al. Birth Defects Res C Embryo Today. 2008 Jun.
Abstract
Cell migration is an evolutionarily conserved mechanism that underlies the development and functioning of uni- and multicellular organisms and takes place in normal and pathogenic processes, including various events of embryogenesis, wound healing, immune response, cancer metastases, and angiogenesis. Despite the differences in the cell types that take part in different migratory events, it is believed that all of these migrations occur by similar molecular mechanisms, whose major components have been functionally conserved in evolution and whose perturbation leads to severe developmental defects. These mechanisms involve intricate cytoskeleton-based molecular machines that can sense the environment, respond to signals, and modulate the entire cell behavior. A big question that has concerned the researchers for decades relates to the coordination of cell migration in situ and its relation to the intracellular aspects of the cell migratory mechanisms. Traditionally, this question has been addressed by researchers that considered the intra- and extracellular mechanisms driving migration in separate sets of studies. As more data accumulate researchers are now able to integrate all of the available information and consider the intracellular mechanisms of cell migration in the context of the developing organisms that contain additional levels of complexity provided by extracellular regulation. This review provides a broad summary of the existing and emerging data in the cell and developmental biology fields regarding cell migration during development.
(c) 2008 Wiley-Liss, Inc.
Figures
Figure 1. Cell migration
A schematic representation of a generic cell of mesenchymal morphology migrating directionally along a two-dimensional substrate. Polarization, mediated by signaling molecules, defines the leading and the trailing edge of the cell and the direction of migration. Lamella, lamellipodia, and filopodia are responsible for the activity and directionality of the leading edge, whose protrusion is mediated by the branched actin network. A cell attaches to the substrate via dynamic focal adhesions. Actin filaments in the cytoplasm to the rear of the lamella form stress fibers that transmit the myosin-mediated tractional forces to propel the cell movement and regulate the trailing edge retraction via actomyosin contractility. See the explanation in the text for further details.
Figure 2. Migration of different cell types is driven by the same mechanisms
Top left, immunofluorescence image of a migrating fibroblast stained with rhodamine-phalloidin to visualize actin filaments. Top right, closeup electron microscopy image of a platinum replica of the leading edge cytoskeletal network of a migrating fibroblast, similar to that shown on the left. Bottom left, immunofluorescence image of neurite outgrowth and closeup image of a neuronal growth cone (boxed) illustrates the migration events during neuritogenesis and the laying down of the nervous system. Bottom right, close-up electron microscopy image of a platinum replica of the leading edge cytoskeletal network in a neuronal growth cone, similar to that shown on the left. Despite morphological differences, variations in the amount of filopodia and the relative density of the actin cytoskeleton, the major structural features of the leading edge, are similar in both cell types. Images in the top panels, bottom right panel, and the close-up of the neuronal growth cone in the bottom left panel courtesy of Dr. T. M. Svitkina (University of Pennsylvania). Bars, 2 µm for immunofluorescence images and 200 nm for the electron micrographs.
Figure 3. Timing of the major migratory events in mouse embryogenesis in relation to the embryo growth
Letters and numbers on the top denote days postcoitum. 1mm scale bar of the same size is shown next to each embryo to enable the direct size comparison. Boxed image showed an enlargement of the gastrula shown above. The major migratory events corresponding to those shown in Table 1 are written for the appropriate stages underneath. Images and sizes are adapted from Kaufman (1992) and have been used as the basis for the calculation of migration distances shown in Table 1.
Figure 4. Pathways of neural crest migration, neuritogenesis, and angiogenesis during mouse development
Neural crest cells (left) generally migrate from the back area of the embryo, originating from different somite regions at different embryonic stages as listed in Table 1. Large green arrows in the head area denote cranial neural crest, blue arrow – cardiac neural crest, black – vagal neural crest, orange arrow – sacral neural crest, and thin red arrows – trunk neural crest. Neurites and blood vessels sprout from the structures laid out during earlier stages of development and reach to all the areas of the mature organism along the pathways illustrated on the right hand image. Illustrations were prepared by O. Karengina based on an image of a mouse embryo at E13.5.
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