Do Filarid Nematodes have a Vascular System

The organization of filarid nematode anatomy has evolved for optimal acquisition of nutrients and delivery of biosynthetic products. The hypodermal cells are key factories for proteins destined for both the hypodermis and the cuticle. To optimize nutrient acquisition, the metabolically active hypodermal cells have cell bodies that bulge as four cords along the length of the worm, putting them in close apposition to the gut epithelium1xWeber, P. Tropenmed. Parasitol. 1984; 35: 221–230PubMedSee all References, 2xStrote, G. and Bonow, I. Parasitol. Res. 1991; 77: 526–535Crossref | PubMed | Scopus (13)See all References.The hypodermis comprises a syncytia, which provides one pathway by which protein synthesized in the hypodermal cell bodies can reach the worm’s surface or cuticle. We propose that a second pathway exists through a network of intercellular channels or conduits connected to the pseudocoelom in the nematodes (Fig. 1Fig. 1). Previously, these structures were referred to as basal lamina, intercellular space or pseudocoelomic membrane1xWeber, P. Tropenmed. Parasitol. 1984; 35: 221–230PubMedSee all References, 2xStrote, G. and Bonow, I. Parasitol. Res. 1991; 77: 526–535Crossref | PubMed | Scopus (13)See all References, 3xChitwood, B.G. and Chitwood, M.B. : 1–50See all References, 4xLevine, N.D. : 344–409See all References.Fig. 1Distribution of Onchocerca proteins in proposed channel network. Aldolase (a): Note grains of immunogold labeling of aldolase in L3, contiguous to cord cell (HC), between muscle cells (M), in cuticle (C), the channel network (arrowheads) and the connections to pseudocoelomic space (arrow). Ov-Alt-1 (b): Note labeling of Ov-Alt-1 in the disintegrating granules (G) of L3, Day 1 in culture, the channels (arrowheads) connecting the esophagus to the cuticle (C), and throughout all layers of the cuticle of L3 by Day 1 in culture. Scale bars = 500 nm.View Large Image | Download PowerPoint SlideThese structures form a network, which may in fact be akin to vascular channels, filled with pseudocoelomic fluid, and capable of efficiently transporting proteins to dispersed regions of the nematode body. Muscular contraction during worm movement could provide the hydrostatic pressure required to circulate fluid through the network. Fig. 1Fig. 1 shows the localization of the Onchocerca volvulus aldolase (encoded by clone Ov-S104, accession no. U96178), a protein synthesized in the hypodermal cell bodies (cords), but then dispersed along the channel network. In a previous study, synthesis of the Onchocerca cysteine protease LOVCP was also traced to hypodermal cells and the glandular esophagus. It, too, appeared to be secreted into the channel network and then transported to the hypodermal–cuticular interface5xLustigman, S. et al. J. Biol. Chem. 1996; 271: 30181–30189Crossref | PubMed | Scopus (82)See all References5. Another protein, Ov-Alt-1, encoded by the cDNA clone Ov-alt-1 [accession no U96176, and homologous to Di 20/22 and Bm-alt-1 (6xFrank, G.R., Tripp, C.A., and Grieve, R.B. Mol. Biochem. Parasitol. 1996; 75: 231–240Crossref | PubMed | Scopus (32)See all References, 7xGregory, W.F., Blaxter, M.L., and Maizels, R.M. Mol. Biochem. Parasitol. 1997; 87: 85–95Crossref | PubMed | Scopus (67)See all References)] was found to be present only in the granules of the glandular esophagus in the vector derived L3 stage (G.T. Joseph, T. Huima and S. Lustigman, unpublished). However, when the larvae initiated the molting process (L3, Day 1 in culture), the protein appeared to be transported from degranulating esophageal cells to the cuticle via channels (Fig. 1bFig. 1b).Electron micrographs of filarids provide only a static vision of the proposed channel network. Proof of its existence must come from further physiologic studies. We encourage investigators working with different parasitic nematodes to evaluate techniques for introducing tracer material that could be followed by dynamic microscopy in living worms. Membrane networks similar to those we have seen in Onchocerca are also found in Wuchereria1xWeber, P. Tropenmed. Parasitol. 1984; 35: 221–230PubMedSee all References1 and Brugia (J.H. McKerrow, T. Huima and S. Lustigman, unpublished).