Rapid changes in the surface of parasitic nematodes during transition from pre- to post-parasitic forms

Abstract

All mammalian-parasitic stages of a range of nematode species investigated (Brugia pahangi, Acanthocheilonema viteae, Strongyloides ratti, Nippostrongylus brasiliensis, Trichinella spiralis and Ostertagia ostertagi) labelled in a surface-restricted manner with the fluorescent lipid analogues 5-N-(octadecanoyl)aminofluorescein (AF18) or nitrobenzoxadiazole-cholesterol (NBD-chol), but failed to bind other similar probes. In contrast, the surfaces of the 'pre-parasitic' infective stages of these species had affinity for neither AF18 nor NBD-chol. This exclusion of lipid analogues changed rapidly upon exposure of the larvae to tissue culture conditions which mimic the mammalian tissue environment (e.g. RPMI 1640/37 degrees C) such that the above probes could then insert into the surface layer of the larvae. The dauer larva of Caenorhabditis elegans also excluded the probes, but became permissive to labelling upon stimulation to emerge from the dauer state. The time taken for the surface transformation to occur ranged from less than 10 min in the vector-borne parasites to approximately 5 h in those which enter by the oral route, with direct skin-penetrators occupying an intermediate position. In all cases, the alteration proceeded too rapidly for it to have been associated with a moult. Fluorescence Recovery After Photobleaching (FRAP) studies of A. viteae larvae showed that approximately 50% of the AF18 probe was free to diffuse within the plane of the surface immediately after transformation. This is only a transitory state because AF18 was found to be highly restricted in its lateral diffusion on the surface of adult parasites. In the larvae of S. ratti, the change in affinity for AF18 was accompanied by the rapid shedding of an otherwise stable surface coat of polyanionic material, here visualized by labelling with fluorescein-conjugated cationized ferritin. Incubation of larvae in lipid-rich host serum during the induction of transformation inhibited subsequent labelling with AF18. This possibly reflects competition for insertion sites and an in vivo propensity towards the acquisition of host lipid by invading parasites.

Influence of Root Exudates and Soil on Attachment of Pasteuria penetrans to Meloidogyne arenaria

“…Nematodes can alter their surface composition in response to environmental signals, and evidence for this switching has been observed in changes in surface antigens, as well as changes in surface lipophilicity (Proudfoot et al, 1993;Olsen et al, 2007). Caenorhabditis elegans, widely studied as a model for environmental induction of surface changes, was found to switch its surface antigens based on environmental cues, and the switch involved chemosensory neurons (Grenache et al, 1996;Olsen et al, 2007).…”

Global analysis of dauer gene expression inCaenorhabditis elegans

“…3). The expression of these genes peak after change in surface lipophilicity (about 30 minutes) and commitment to exit (about 1 hour), but before many morphological and behavioral changes, such as pharyngeal pumping (about 3 hours) and increase in the diameter of the worm (Cassada and Russell, 1975;Golden and Riddle, 1984;Proudfoot et al, 1993). These genes could be an early transcriptional response that sets up the dauer recovery process.…”

“…Upon transfer to favorable conditions, the first visible change is a change in surface lipophilicity (30 minutes), and commitment to dauer recovery occurs after approximately 50-60 minutes (Golden and Riddle, 1984;Proudfoot et al, 1993). Pharyngeal pumping, movement and increased body volume occur within 3 hours at 25°C (Cassada and Russell, 1975).…”

Caenorhabditis elegans Mutants Resistant to Attachment of Yersinia Biofilms

“…The noncollagenous epicuticle is exceedingly thin, and electron microscopy reveals little of its structure. Lipid analog probes associate with the epicuticle of many nematodes, but the probes do not diffuse as they do in a cellular lipid bilayer, implying a different type of organization (Proudfoot et al 1993). A biochemical study of the C. elegans surface suggested that the epicuticle contains a heterodimeric protein complex (Blaxter 1993).…”