Polarization of the anterior–posterior axis of C. elegans is a microtubule-directed process

Abstract

In Caenorhabditis elegans, polarity along the anterior-posterior (A/P) axis is established shortly after fertilization and is determined by the sperm, whose position specifies the posterior end of the embryo'. Although many factors required for the establishment of A/P polarity have been described, the nature of the spatial cue provided by the sperm remains unknown. Here we show that a microtubule-organizing centre is necessary and sufficient to establish several aspects of A/P polarity. In wildtype embryos, appearance of the first molecular asymmetries along the A/P axis correlates with and requires nucleation of microtubules by the sperm-derived centrosomes (sperm asters). In mutant embryos arrested in meiosis, sperm asters fail to form, and posterior is defined by the position of the persistent meiotic spindle rather than by the position of the sperm. Together, our data indicate that the primary spatial cue for A/P polarity in C. elegans derives from microtubules emanating from the sperm asters. Our findings support a parallel between C. elegans zygotes and other cells, such as Drosophila oocytes, which rely on microtubules to regulate polarity.

Multiple Functions and Dynamic Activation of MPK-1 Extracellular Signal-Regulated Kinase Signaling inCaenorhabditis elegansGermline Development

“…Additionally, it has been proposed that active ERK inhibits sperm centrosome function in a variety of vertebrates and invertebrates (Stephano and Gould 2000). In C. elegans, the sperm centrosome may trigger the completion of female meiosis and appears to function in anterior/posterior axis formation at the one-cell stage (Sadler and Shakes 2000;Wallenfang and Seydoux 2000;Cowan and Hyman 2004;McNally and McNally 2005). The removal of active MPK-1 during maturation may be important to ensure that subsequent processes mediated by the sperm centrosome are not inhibited.…”

Polarization of theC. eleganszygote proceeds via distinct establishment and maintenance phases

“…Transient localization in the anterior cortex was also described for endogenous PAR-2 in immunofluorescence experiments . The significance of this localization is not known, but may be due to the transient influence of the meiotic spindle in this area of the cortex (Wallenfang and Seydoux, 2000).…”

“…The GFP fusions are all aminoterminal GFP fusions under the control of the pie-1 promoter and 3′UTR, with the exception of PIE-1:GFP, which is a carboxy-terminal GFP fusion. GFP:PAR-2, PIE-1:GFP and GFP:tubulin were described previously (Wallenfang and Seydoux, 2000;Reese et al, 2000;Strome et al, 2001). Initially, four independent lines were generated for GFP:PAR-6, four for GFP:PAR-2, two for PIE-1:GFP, one for GFP:MEX-5 and one for GFP:MEX-6.…”

“…To analyze polarization dynamics in live embryos, we used GFP fusions to PAR-2, PAR-6, PIE-1, MEX-5 and MEX-6 (see Materials and Methods) (Wallenfang and Seydoux, 2000;Reese et al, 2000;Strome et al, 2001). The GFP:ORF fusions were driven under the control of the pie-1 promoter and 3′UTR.…”

Advances in Cytokinesis Research. Cytokinesis in the C. elegans Embryo: Regulating Contractile Forces and a Late Role for the Central Spindle.

“…The posterior pole, towards which internal cytoplasm moves, is specified after fertilization by the position of the sperm pronucleus and its associated asters (Goldstein and Hird, 1996). Signals from the sperm-donated centrosome, possibly involving astral microtubule contact with the cell cortex, appear to initiate the microfilament-dependent flux and thereby specify the anterior-posterior body axis (O'Connell et al, 2000;Wallenfang and Seydoux, 2000). Thus cortical microfilaments fulfill multiple functions in the one cell embryo, with different spatial regulation occurring at different times to mediate distinct processes that include polar body extrusion, axis formation and cytokinesis during mitosis.…”