Compartment (development)

In developmental biology, compartments are fields of cells of distinct cell lineage, cell affinity, and genetic identity. In a developing organ, all cells within a compartment possess similar affinities, and so intermingle with each other. However, cells in neighbouring compartments have different cell affinity values and so never mix, thereby restricting the movement of cells to within compartments. Much cell proliferation may follow the appearance of compartments during development, hence this affinity-based subdivision has the effect of forcing cell lineages to stay within compartment boundaries.

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Compartments in Insects

Compartments were first discovered in the epidermis of the insects Oncopeltus fasciatus and Drosophila melanogaster (see Crick and Lawrence, 1975). The insect epidermis is subdivided into only two compartment types: Anterior (A) and Posterior (P), which are alternated along the antero-posterior (A-P) axis, so the compartments stay distinct. An insect segment is made of a pair of A and P compartments. Genetically, compartments arise during embryogenesis because the gene engrailed (en) is switched on in 14 stripes (Kornberg et al., 1985). The Engrailed protein, a transcription factor, functions to specify the identity of the P compartments, its absence from a cell conferring A identity (Morata and Lawrence, 1975). A and P compartments remain present throughout fly development; most adult structures, including all appendages, are comprised of A and P compartments, the boundaries of which are inherited from the embryo (reviewed in Lawrence and Struhl, 1996).

The generation of compartments has important consequences for multiple aspect of insect development, since en does more than simply specify posterior identity. For example, in the embryonic and adult abdomen, as well as in the wing and leg imaginal discs, en activates transcription of the hedgehog gene (hh, Tabata et al., 1992). hh encodes a diffusible protein, which is released from its source cell and moves into the extracellular environment, where it meets other target cells. On reaching a cell, Hh protein binds to its receptor Patched (Ptc, Ingham et al., 1991), which (via several intermediary proteins) transduces the Hh signal to the nucleus, causing the activation of Hh target genes. Since en-expressing cells do not express Ptc, P compartments are rendered blind to the Hh signal (Hidalgo and Ingham, 1990); hence only cells in A compartments that lie within the range of Hh will see it and respond to it.

Depending on the developmental context, the response to Hh varies. In the embryonic abdominal segments (and probably also in the thoracic segments), target cells receiving Hh in the A compartment anterior to the P compartment respond by maintaining expression of wingless (wg, Ingham and Hidalgo, 1993), whereas in the wing, the decapentaplegic gene (dpp) is induced. wg and dpp encode long-range morphogen molecules, which diffuse away from their source cells to pattern the surrounding tissue and also regulate cell division, cell size and cell survival. Hence, compartments are central to controlling organ morphogenesis, and the organisation of the final insect body plan.

Compartments in Vertebrates

It is now known that compartments are also a feature of vertebrate development, in the form of hindbrain rhombomeres (Fraser et al. 1990).

References

Crick, F. H. and Lawrence, P. A. (1975). Compartments and polyclones in insect development. Science 189, 340-7.

Lawrence, P. A. and Struhl, G. (1996). Morphogens, compartments, and pattern: lessons from drosophila? Cell 85, 951-61.

Ingham, P. W., Taylor, A. M. and Nakano, Y. (1991). Role of the Drosophila patched gene in positional signalling. Nature 353, 184-7.

Fraser, S., Keynes, R. and Lumsden, A. (1990). Segmentation in the chick embryo hindbrain is defined by cell lineage restrictions. Nature 344, 431-5.

Ingham, P. W. and Hidalgo, A. (1993). Regulation of wingless transcription in the Drosophila embryo. Development 117, 283-91.

Tabata, T., Eaton, S. and Kornberg, T. B. (1992). The Drosophila hedgehog gene is expressed specifically in posterior compartment cells and is a target of engrailed regulation. Genes Dev 6, 2635-45.

Morata, G. and Lawrence, P. A. (1975). Control of compartment development by the engrailed gene in Drosophila. Nature 255, 614-7.

Hidalgo, A. and Ingham, P. (1990). Cell patterning in the Drosophila segment: spatial regulation of the segment polarity gene patched. Development 110, 291-301.

Kornberg, T., Siden, I., O'Farrell, P. and Simon, M. (1985). The engrailed locus of Drosophila: in situ localization of transcripts reveals compartment-specific expression. Cell 40, 45-53.