Dynamics and ultrastructure of developmental cell fusions in the Caenorhabditis elegans hypodermis

Abstract

Cell fusions produce multinucleate syncytia that are crucial to the structure of essential tissues in many organisms [1-5]. In humans the entire musculature, much of the placenta, and key cells in bones and blood are derived from cell fusion. Yet the developmental fusion of cell membranes has never been directly observed and is poorly understood. Similarity between viral fusion proteins and recently discovered cellular proteins implies that both cell-cell and virus-cell fusion may occur by a similar mechanism [6-8]. Paradoxically, however, fusion of enveloped viruses with cells involves an opening originating as a single pore [9-11], whereas electron microscopy studies of cell-cell fusion describe simultaneous breakdown of large areas of membrane [12, 13]. Here, we have shown that developmental cell fusion is indeed consistent with initiation by a virus-like, pore-forming mechanism. We examined live cell fusions in the epithelia of Caenorhabditis elegans embryos by a new method that integrates multiphoton, confocal, and electron microscopy. The fusion aperture always originated at a single point restricted to the apical adherens junction and widened slowly as a radial wavefront. The fusing membranes dispersed by vesiculation, rather than simple unfolding of the conjoined double bilayer. Thus, in these cells fusion appears to require two specialized sequential processes: formation of a unique primary pore and expansion of the opening by radial internalization of the interacting cell membranes.

Essential Roles of 3′-Phosphoadenosine 5′-Phoshosulfate Synthase in Embryonic and Larval Development of the Nematode Caenorhabditis elegans

“…This observation demonstrates that axial elongation of the intestine was normal, but elongation of the hypodermis and body wall muscles failed. Consistent with this notion, Nob animals derived from pps-1(RNAi) in jcIs1 (ajm-1::GFP) worms (45), which express GFP marker at cell junctions between the epidermal, pharyngeal, and intestinal cells, exhibited an abnormal shape of the lateral epidermis seam cells at the posterior region of the pharynx bulb (Fig. 5, C and D); however, there was no significant difference in pharynx length and seam cell shape at the anterior region of the pharynx bulb between RNAi and control animals (not shown).…”

DLG-1 Is a MAGUK Similar to SAP97 and Is Required for Adherens Junction Formation

“…The pattern of DLG-1 expression highly resembles that of the adherens junction protein AJM-1, which encodes the MH27 antigen and was previously known as JAM-1 (Kö ppen et Mohler et al, 1998;Podbilewicz and White, 1994;Priess and Hirsh, 1986;Raich et al, 1999;Wood, 1988). Indeed, DLG-1 colocalizes with AJM-1::GFP as evidenced by immunostaining (Figure 2A-F, n ϭ 18/18).…”

The Caenorhabditis elegans Distal‐less ortholog ceh‐43 is required for development of the anterior hypodermis

“…The anterior-most hypodermis consists of small cylindrical syncytial cells that join the main hypodermal body syncytia to the inner epithelia of the digestive tract. The main body hypodermis develops from a cluster of dorsal cells that undergo epiboly and enclose the blastoderm embryo ventrally and posteriorly before elongation starts (Sulston et al, 1983;Williams-Masson et al, 1997;Mohler et al, 1998). In the embryo, these hypodermal cells generate a circumferential pressure and elongate to shape the embryo into a worm (Priess and Hirsh, 1986).…”