Caenorhabditis elegansPlexinA, PLX-1, interacts with transmembrane semaphorins and regulates epidermal morphogenesis

Abstract

The plexin family transmembrane proteins are putative receptors for semaphorins, which are implicated in the morphogenesis of animal embryos, including axonal guidance. We have generated and characterized putative null mutants of the C. elegans plexinA gene, plx-1. plx-1 mutants exhibited morphological defects: displacement of ray 1 and discontinuous alae. The epidermal precursors for the affected organs were aberrantly arranged in the mutants, and a plx-1::gfp transgene was expressed in these epidermal precursor cells as they underwent dynamic morphological changes. Suppression of C. elegans transmembrane semaphorins, Ce-Sema-1a and Ce-Sema-1b, by RNA interference caused a displacement of ray 1 similar to that of plx-1 mutants, whereas mutants for the Ce-Sema-2a/mab-20 gene, which encodes a secreted-type semaphorin, exhibited phenotypes distinct from those of plx-1 mutants. A heterologous expression system showed that Ce-Sema-1a, but not Ce-Sema-2a, physically bound to PLX-1. Our results indicate that PLX-1 functions as a receptor for transmembrane-type semaphorins, and, though Ce-Sema-2a and PLX-1 both play roles in the regulation of cellular morphology during epidermal morphogenesis, they function rather independently.

ztf-16 is a novel heterochronic modulator that opposes adult cell fate in dauer and continuous life histories in Caenorhabditis elegans

“…S5). These breaks appeared smaller than similar breaks that were previously described in mutants with defects in epidermal morphogenesis or seam cell fate (Fujii et al 2002;Smith et al 2005;Brabin et al 2011). The basis for this phenotype is unclear and was not explored further.…”

Mosaic gene expression analysis of semaphorin–plexin interactions in Caenorhabditis elegans using the IR‐LEGO single‐cell gene induction system

“…NW1358 smp‐1(ev715) and SU93 ( jcIs1(ajm‐1::gfp; rol‐6(su1006)) ) were provided by Joe Culotti (Ginzburg et al, 2002) and Jeff Simske (Mohler, Simske, Williams‐Masson, Hardin, & White, 1998), respectively. The plx‐1(nc37), ncIs13(ajm‐1::gfp), ncIs15 (ajm‐1::gfp) (Fujii et al, 2002; Liu et al, 2005), and ncIs17(hsp::gfp) (Kamei et al, 2009) strains were generated as previously described. The generation of ncEx2005(hsp::Cre ; eft‐3p < C < gfp) was described previously (Suzuki et al, 2014).…”

“…(ajm-1::gfp) (Fujii et al, 2002;Liu et al, 2005), and ncIs17(hsp::gfp) (Kamei et al, 2009) strains were generated as previously described.…”

“…In C. elegans , a type I transmembrane semaphorin, SMP‐1, binds to the plexin A subfamily member PLX‐1, and regulates the morphogenesis of organs of epidermal origin, which include rays in the male tail (Fujii et al, 2002; Ginzburg, Roy, & Culotti, 2002) and the vulva in hermaphrodites (Dalpé, Brown, & Culotti, 2005; Liu et al, 2005). The vulva, a passage for eggs and sperm localized at the ventral midline of adult hermaphrodites, originates from epithelial cells known as vulval precursor cells (VPCs) (Sharma‐Kishore, White, Southgate, & Podbilewicz, 1999; Sulston & Horvitz, 1977).…”

Molecular basis of the silkworm mutant rel causing red egg color and embryonic death

“…The results of in situ hybridization showed that the spatial expression positions of BmSema1a gene were the head and thorax, which is consistent with the position where the thoracic swelling appeared in some mosaic individuals. The semaphorin-1a gene of Caenorhabditis elegans not only regulates the correct localization of rays, but also monitors epidermis morphogenesis (Fujii et al, 2002;Ginzburg et al, 2002). Fas2 and Integrin proteins are critical for the forward and reverse signal transduction of semaphorins, respectively, which can regulate cell movement and morphology in vertebrates and invertebrates (Kruger et al, 2005;Tran et al, 2007;Battistini & Tamagnone, 2016).…”