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WIREs Dev Biol
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Cell‐intrinsic timing in animal development

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Abstract In certain instances we can witness cells controlling the sequence of their behaviors as they divide and differentiate. Striking examples occur in the nervous systems of animals where the order of differentiated cell types can be traced to internal changes in their progenitors. Elucidating the molecular mechanisms underlying such cell fate succession has been of interest for its role in generating cell type diversity and proper tissue structure. Another well‐studied instance of developmental timing occurs in the larva of the nematode Caenorhabditis elegans, where the heterochronic gene pathway controls the succession of a variety of developmental events. In each case, the identification of molecules involved and the elucidation of their regulatory relationships is ongoing, but some important factors and dynamics have been revealed. In particular, certain homologs of worm heterochronic factors have been shown to work in neural development, alerting us to possible connections among these systems and the possibility of universal components of timing mechanisms. These connections also cause us to consider whether cell‐intrinsic timing is more widespread, regardless of whether multiple differentiated cell types are produced in any particular order. This article is categorized under: Establishment of Spatial and Temporal Patterns > Regulation of Size, Proportion, and Timing Gene Expression and Transcriptional Hierarchies > Gene Networks and Genomics Gene Expression and Transcriptional Hierarchies > Regulatory RNA
Temporal identity in Drosophila neurogenesis. Top: Drosophila neuroblasts divide asymmetrically to produce distinct neural progeny marked by the expression of four transcription factors: Hunchback (Hb), Kruppel (Kr), POU domain protein (Pdm), and Castor (Cas). Bottom: The protein levels of each of the four transcription factors rise and fall in turn within the neuroblast lineage.
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The developmental timing mechanism of Caenorhabditis elegans. Top: A genetic representation of the dynamic regulation that leads to the stage‐specific cell behaviors in the epidermis (numbered circles). At the end of larval development, the terminal differentiation factor encoded by lin‐29 is expressed. MicroRNAs act cooperatively and sequentially to repress four protein regulators whose levels change in a stage‐specific manner. Some of the protein regulators influence the accumulation or action of the microRNAs. Bottom: All four of the proteins are expressed at the start of larval development but are repressed by the microRNAs, which accumulate over time.
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Heterochronic mutants of Caenorhabditis elegans. A typical epidermal cell lineage through the four larval stages (L1–L4) is shown next to colored circles to represent the stage‐specific cell lineage pattern. Three horizontal lines at the end of the L4 stage indicates terminal differentiation of the epidermis. To the right are shown the patterns of temporal defects in heterochronic mutants.
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Timing in the vertebrate retina. Top: Retinal neural progenitors change in competence over time, losing the ability to produce earlier‐born neural cell types and gaining the ability to produce later‐born types. Bottom: Loss of Ikaros causes a deficiency of early‐born cell types Loss of microRNAs causes an over‐production of some early‐born cell types and a deficiency of later‐born cell types.
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Timing in vertebrate neural development. In diverse locations throughout the vertebrate nervous system, a common pool of neural progenitors gives rise sequentially to different types of neurons and different types of glia. Right: Deletion of microRNA function (by deleting their processing enzyme Dicer) causes skipping of later‐born neuron types, but not early‐born types nor glia.
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Temporal identity mutants in Drosophila. The temporal identify factors help specify neural types and control the sequence of temporal identity factor expression. Top: The normal expression of the factors. Middle: Loss of Kruppel (Kr) causes fewer mature neurons, either because the fate was skipped or the cell died. Bottom: Constitutive expression (CE) of Kruppel causes supernumary neurons of the Kruppel‐expressing type.
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Gene Expression and Transcriptional Hierarchies > Gene Networks and Genomics
Gene Expression and Transcriptional Hierarchies > Regulatory RNA
Establishment of Spatial and Temporal Patterns > Regulation of Size, Proportion, and Timing