Caenorhabditis elegans Vulval Induction

Paul W Sternberg, California Institute of Technology, Pasadena, California, USA

Published online: January 2006

DOI: 10.1038/npg.els.0004190

Study of Caenorhabditis elegans vulval development has improved our understanding of inductive signalling and pattern formation at the single cell level, and has led to the definition of signalling cascades. Studies of signal transduction during vulval development have led to the discovery of what is considered a universal signalling pathway from growth factor receptor to RAS to MAP kinase to the nucleus, and the discovery of the LIN-12/Notch family of receptors that mediate lateral signalling.

Keywords: intercellular signalling; signal transduction; pattern formation; organogenesis; cell lineage

Figure 1. Overlapping domains of homeodomain protein gene expression. Ovals represent the ventral epidermal Pn.p cells. The yellow cells become the vulval competence group. The domains of expression of genes encoding homeodomain containing proteins genes are indicated by coloured bars.
Figure 2. Schematic of early vulval development. (a) Yellow ovals represent VPCs. Green cell is the anchor cell. (b) After induction and patterning P6.p is specified to the 1° fate (blue), P5.p and P7.p to the 2° fate (red) and the remaining three VPCs to the 3° fate (yellow). (c) All VPCs divide one round, and the 3° daughters differentiate as hyp7 syncytial epidermis (S). (d) After two rounds of division, most of the granddaughters are specified to generate mature vulval cell types (A, C, D, E and F). Two cells (Bs) divide and generate one B1 and one B2 cell each. The anchor cell attaches to the vulF cells.
Figure 3. Summary of the three VPC fates.
Figure 4. Evidence for graded response to the inductive signal LIN-3 from the anchor cell. The response of single VPCs to lin-3 is indicated by the coloured histogram. Blue, 1° fate; purple, 1°/2° hybrid fate; red, 2° fate; orange, 1°/3° or 2°/3° hybrid fate; yellow, 3° fate. Red X indicates cell ablation. Excess lin-3 is a transgenic animal overexpressing lin-3 from the anchor cell.
Figure 5. Summary of the anchor cell to VPC inductive signalling pathway.
Figure 6. Summary of cell interactions in a multivulva mutant, indicating lateral signalling. (a) Intact lin-15 animal has all 1° (blue) or 2° (red) VPCs with a 1° VPC closest to the anchor cell (green). (b) Gonad-ablated (X) animal has all 1° or 2° VPCs, but the precise pattern is somewhat variable. (c) Single VPC in the absence of the gonad is 1°. (d) With two adjacent VPCs, one is 1° while the other is 2°; the order is stochastic. (e) With an anchor cell, the closest VPC to the anchor cell is 1°.
Figure 7. Lateral signalling works in two modes. (a) Lateral signalling between VPCs can prevent adjacent VPCs from both being 1°. Blue arrows indicate lateral signalling via LIN-12. (b) Lateral signalling allows a 1° VPC to induce its neighbours to become 2° even if they are unable to receive LIN-3. Green rectangles indicate LET-23, the presumed receptor for LIN-3. Green arrow indicates LIN-3.
Figure 8. Model for antagonism between LET-23 and LIN-12 signalling. Arrows, positive regulation; Bars, negative regulation. (a) VPCs, two of which are shown here, respond to a gradient of LIN-3 from the anchor cell. Reception of LIN-3 via LET-23 promotes specification as a 1° VPC and activates transcription of DSL ligands for LIN-12. In addition, it leads to downregulation of LIN-12 protein. Reception of LIN-12 activates transcription of inhibitors of LET-23 signalling. (b) The closest VPC to the anchor cell, P6.p (shown on the left), receives a stronger LIN-3 signal and thus sends a stronger DSL signal; thereby weakening the response to LET-23 in its neighbours. (c) Eventually, the 1° VPC signals unidirectionally to the 2° VPC.
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 References
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    Horvitz HR and Sternberg PW (1991) Multiple intercellular signalling systems control the development of the C. elegans vulva. Nature 351: 535–541.
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 Further Reading
    Bersert T, Hoier EF, Battu G, Canevascini S and Hajnal A (2001) Notch inhibition of RAS singalling through MAP kinase phosphatase LIP-1 during C. elegans vulval development. Science 291: 1055–1058.
    Hill RJ and Sternberg PW (1992) The gene lin-3 encodes an inductive signal for vulval development in C. elegans. Nature 358(6386): 470–476.
    Inoue T, Wang M, Ririe TO, Fernandes JS and Sternberg PW (2005) Transcriptional network underlying Caenorhabditis elegans vulval development. Proceedings of the National Academy of Sciences of the USA 102(14): 4972–4977.
    Kimble J (1981) Alterations in cell lineage following laser ablation of cells in the somatic gonad of Caenorhabditis elegnas. Developmental Biology 87(2): 286–300.
    Sternberg PW (1988) Lateral inhibition during vulval induction in Caenorhabditis elegans. Nature 335: 551–554.
    Sternberg PW and Horvitz HR (1989) The combined action of two intercullar singalling pathways specifies three cells fates during vulval induction in C. elegans. Cell 58: 679–693.

Related Sub-Topics:

Intracellular and Extracellular Signalling | Genes, Molecules and Cellular Processes | Organogenesis
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Article Title: Caenorhabditis elegans Vulval Induction
 
How to Cite close
Sternberg, Paul W(Jan 2006) Caenorhabditis elegans Vulval Induction. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1038/npg.els.0004190]