The Plexin PLX-2 and the Ephrin EFN-4 Have Distinct Roles in MAB-20/Semaphorin 2A Signaling in <i>Caenorhabditis elegans</i> Morphogenesis

Nakao, Fumi; Hudson, Martin L.; Suzuki, Motoshi; Peckler, Zachary; Kurokawa, Rie; Liu, Zhicen; Gengyo-Ando, Keiko; Nukazuka, Akira; Fujii, Takashi; Suto, Fumikazu; Shibata, Yoshiaki; Shioi, Go; Fujisawa, Hajime; Mitani, Shohei; Chisholm, Andrew; Takagi, Shin

doi:10.1534/genetics.106.067116

Cited by 41 publications

(55 citation statements)

References 57 publications

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“…2). In agreement with mab-20 and plx-2 functioning in the same pathway (Ikegami et al, 2004;Nakao et al, 2007;Wang et al, 2008), mab-20; plx-2 animals exhibited similar levels of SDQL axon defects as mab-20 and plx-2 single mutant animals ( Fig. 2 and Wang et al, 2008).…”

Section: Efn-4 Functions In the Same Genetic Pathway As Lad-2 In Axonsupporting

confidence: 71%

“…Indeed, epidermal morphogenesis defects in efn-4 null embryos are synergistically enhanced in a vab-1 null background, consistent with each protein functioning in parallel pathways (Chin-Sang et al, 2002). EFN-4 also plays a major role in morphogenesis of the male tail, a process in which VAB-1 and the other three ephrins have not been reported to participate (Ikegami et al, 2004;Nakao et al, 2007). More recently, EFN-4 was revealed to have a role in promoting axon branching that is also partially independent of VAB-1 (Schwieterman et al, 2016).…”

Section: Introductionmentioning

confidence: 68%

“…Prior studies established EFN-4 and MAB-20/semaphorin as essential for male tail morphogenesis (Ikegami et al, 2004;Nakao et al, 2007). In these studies, shown to function in common pathways.…”

Section: Efn-4 Functions In the Same Genetic Pathway As Lad-2 In Axonmentioning

confidence: 99%

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EFN-4/Ephrin functions in LAD-2/L1CAM-mediated axon guidance in Caenorhabditis elegans

et al. 2016

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During development of the nervous system, growing axons rely on guidance molecules to direct axon pathfinding. A well-characterized family of guidance molecules are the membrane-associated ephrins, which together with their cognate Eph receptors, direct axon navigation in a contact-mediated fashion. In C. elegans, the ephrin-Eph signaling system is conserved and is best characterized for their roles in neuroblast migration during early embryogenesis. This study demonstrates a role for the C. elegans ephrin EFN-4 in axon guidance. We provide both genetic and biochemical evidence that is consistent with the C. elegans divergent L1 cell adhesion molecule LAD-2 acting as a non-canonical ephrin receptor to EFN-4 to promote axon guidance. We also show that EFN-4 probably functions as a diffusible factor because EFN-4 engineered to be soluble can promote LAD-2-mediated axon guidance. This study thus reveals a potential additional mechanism for ephrins in regulating axon guidance and expands the repertoire of receptors by which ephrins can signal.

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Section: Efn-4 Functions In the Same Genetic Pathway As Lad-2 In Axonsupporting

confidence: 71%

Section: Introductionmentioning

confidence: 68%

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EFN-4/Ephrin functions in LAD-2/L1CAM-mediated axon guidance in Caenorhabditis elegans

et al. 2016

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“…The ray 1 phenotype in plx-1 adults is remarkably rescued by driving expression of plx-1 under the lin-32 promoter (lin-32p) ( Fig. 1I; Nakao et al 2007). Since in larval males the lin-32p drives gene expressions pre-dominantly in nine R(n) cells and their descendants (Supplemental Fig.…”

Section: A Role For Semaphorin-plexin Signaling In the Epidermal Ray mentioning

confidence: 99%

Semaphorin controls epidermal morphogenesis by stimulating mRNA translation via eIF2α in Caenorhabditis elegans

Nukazuka¹,

Fujisawa²,

Inada³

et al. 2008

Genes Dev.

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Conserved semaphorin-plexin signaling systems govern various aspects of animal development, including axonal guidance in vertebrates and epidermal morphogenesis in Caenorhabditis elegans. Here we provide in vivo evidence that stimulation of mRNA translation via eukaryotic initiation factor 2␣ (eIF2␣) is an essential downstream event of semaphorin signaling in C. elegans. In semaphorin/plexin mutants, a marked elevation in the phosphorylation of eIF2␣ is observed, which causes translation repression and is causally related to the morphological epidermal phenotype in the mutants. Conversely, removal of constraints on translation by genetically reducing the eIF2␣ phosphorylation largely bypasses requirement for the semaphorin signal in epidermal morphogenesis. We also identify an actin-depolymerizing factor/cofilin, whose expression in the mutants is predominantly repressed, as a major translational target of semaphorin signaling. Thus, our results reveal a physiological significance for translation of mRNAs for cytoskeletal regulators, linking environmental cues to cytoskeletal rearrangement during cellular morphogenesis in vivo.[Keywords: C. elegans; cofilin; eIF2; epidermal morphogenesis; mRNA translation; semaphorin] Supplemental material is available at http://www.genesdev.org.

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“…Furthermore, certain Sema proteins are membrane associated and thus would be ideal candidates to mediate signaling between cells in contact (Zhou et al, 2008). Indeed, Sema6a helps organize chick cardiac development (Toyofuku et al, 2004) and Plx2 controls C. elegans epidermal morphogenesis (Nakao et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Sema6a and Plxna2 mediate spatially regulated repulsion within the developing eye to promote eye vesicle cohesion

et al. 2014

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Organs are generated from collections of cells that coalesce and remain together as they undergo a series of choreographed movements to give the organ its final shape. We know little about the cellular and molecular mechanisms that regulate tissue cohesion during morphogenesis. Extensive cell movements underlie eye development, starting with the eye field separating to form bilateral vesicles that go on to evaginate from the forebrain. What keeps eye cells together as they undergo morphogenesis and extensive proliferation is unknown. Here, we show that plexina2 (Plxna2), a member of a receptor family best known for its roles in axon and cell guidance, is required alongside the repellent semaphorin 6a (Sema6a) to keep cells integrated within the zebrafish eye vesicle epithelium. sema6a is expressed throughout the eye vesicle, whereas plxna2 is restricted to the ventral vesicle. Knockdown of Plxna2 or Sema6a results in a loss of vesicle integrity, with time-lapse microscopy showing that eye progenitors either fail to enter the evaginating vesicles or delaminate from the eye epithelium. Explant experiments, and rescue of eye vesicle integrity with simultaneous knockdown of sema6a and plxna2, point to an eye-autonomous requirement for Sema6a/Plxna2. We propose a novel, tissue-autonomous mechanism of organ cohesion, with neutralization of repulsion suggested as a means to promote interactions between cells within a tissue domain.

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The Plexin PLX-2 and the Ephrin EFN-4 Have Distinct Roles in MAB-20/Semaphorin 2A Signaling in Caenorhabditis elegans Morphogenesis

Cited by 41 publications

References 57 publications

EFN-4/Ephrin functions in LAD-2/L1CAM-mediated axon guidance in Caenorhabditis elegans

EFN-4/Ephrin functions in LAD-2/L1CAM-mediated axon guidance in Caenorhabditis elegans

Semaphorin controls epidermal morphogenesis by stimulating mRNA translation via eIF2α in Caenorhabditis elegans

Sema6a and Plxna2 mediate spatially regulated repulsion within the developing eye to promote eye vesicle cohesion

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