Further Development 8.7: Cell-Cell Interactions in the Early C. Elegans Embryo

Snails, Flowers, and Nematodes: Different Mechanisms for Similar Patterns of Specification

The P2 cell is also critical in giving the signal that distinguishes ABp from its sister, ABa (see Figure 2 in Further Development 8.6, Defining the role of SKN-1 and PAL-1 in early cell specification in C. Elegans). ABa gives rise to neurons, hypodermis, and the anterior pharynx cells, while ABp makes only neurons and hypodermal cells (see Figure 8.15). However, if one experimentally reverses the positions of these two cells, their fates are similarly reversed and a normal embryo forms. In other words, ABa and ABp are equivalent cells whose fates are determined by their positions in the embryo (Priess and Thomson 1987). Transplantation and genetic studies have shown that ABp becomes different from ABa through its interaction with the P2 cell. In an unperturbed embryo, both ABa and ABp contact the EMS blastomere, but only ABp contacts the P2 cell (see Figure 8.16C). If the P2 cell is killed at the early 4-cell stage, the ABp cell does not generate its normal complement of cells (Bowerman et al. 1992a,b). Contact between ABp and P2 is essential for the specification of ABp cell fates, and the ABa cell can be made into an ABp-type cell if it is forced into contact with P2 (Hutter and Schnabel 1994; Mello et al. 1994).

This interaction is mediated by the GLP-1 protein on the ABp cell and the APX-1 (anterior pharynx excess) protein on the P2 blastomere. In embryos whose mothers have mutant glp-1, ABp is transformed into an ABa cell (Hutter and Schnabel 1994; Mello et al. 1994). The GLP-1 protein is a member of the widely conserved family of Notch proteins, which serve as cell membrane receptors in many cell-cell interactions; it is seen on both the ABa and ABp cells (Evans et al. 1994).1 One of the most important ligands for Notch proteins such as GLP-1 is the cell surface protein Delta. In C. elegans, the Delta-like protein is APX-1, and it is found on the P2 cell (Mango et al. 1994a; Mello et al. 1994). This APX-1 signal breaks the symmetry between ABa and ABp, since it stimulates the GLP-1 protein solely on the AB descendant that it touches—namely, the ABp blastomere. Previously, we discussed that the dorsal-ventral axis of C. elegans is established in the division of the AB cell when one of its daughter cells, the ABp cell, takes up a dorsal position, thus defining the future dorsal side of the embryo. We now have learned that the molecular mechanisms for this lie in signaling from the P2 cell that confers a fate on the ABp blastomere that is different from that of its sister cell.

1 GLP-1 protein is localized in the ABa and ABp blastomeres, but the maternally encoded glp-1 mRNA is found throughout the embryo. Evans and colleagues (1994) have postulated that there might be some translational determinant in the AB blastomere that enables the glp-1 message to be translated in its descendants. The glp-1 gene is also active in regulating postembryonic cell-cell interactions. It is used later by the distal tip cell of the gonad to control the number of germ cells entering meiosis—hence the name GLP, for germ line proliferation.

Figure 1 Cell-cell signaling in the 4-cell embryo of C. elegans. The P2 cell produces two signals: (1) the juxtacrine protein APX-1 (a Delta homologue), which is bound by GLP-1 (Notch) on the ABp cell, and (2) the paracrine protein MOM-2 (Wnt), which is bound by the MOM-5 (Frizzled) protein on the EMS cell. (After M. Han. 1998. Cell 90: 581–584.)


Bowerman, B., B. A. Eaton and J. R. Priess. 1992a. skn-1, a maternally expressed gene required to specify the fate of ventral blastomeres in the early C. elegans embryo. Cell 68: 1061–1075.
PubMed Link

Bowerman, B., F. E. Tax, J. H. Thomas and J. R. Priess. 1992b. Cell interactions involved in the development of the bilaterally symmetrical intestinal valve cells during embryogenesis of Caenorhabditis elegansDevelopment 116: 1113–1122.
PubMed Link

Evans, T. C., S. L. Crittenden, V. Kodoyianni and J. Kimble. 1994. Translational control of maternal glp-1 mRNA establishes an asymmetry in the C. elegans embryo. Cell 77: 183–194.
PubMed Link

Hutter, H. and R. Schnabel. 1994. glp-1 and inductions establishing embryonic axes in C. elegansDevelopment 120: 2051–2064.
PubMed Link

Mello, C. C., B. W. Draper and J. R. Priess. 1994. The maternal genes apx-1 andglp-1 and establishment of dorsal-ventral polarity in the early C. elegansembryo. Cell 77: 95–106.
PubMed Link

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