The amphidial neuron pair ALD controls the temperature-sensitive choice of alternative developmental pathways in the parasitic nematode, Strongyloides stercoralis

Abstract

The parasitic nematode Strongyloides stercoralis, has several alternative developmental pathways. Upon exiting the host (humans, other primates and dogs) in faeces, 1st-stage larvae (L1) can enter the direct pathway, in which they moult twice to reach the infective 3rd-stage. Alternatively, if they enter the indirect pathway, they moult 4 times and become free-living adults. The choice of route depends, in part, on environmental cues. In this investigation it was shown that at temperatures below 34 degrees C the larvae enter the indirect pathway and develop to free-living adulthood. Conversely, at temperatures approaching body temperature (34 degrees C and above), that are unfavorable for the survival of free-living stages, larvae develop directly to infectivity. The time-period within the L1's development during which temperature influenced the choice of the pathway depended on the temperature, but, at any given temperature, occurred approximately in the middle of the time-span spent in the L1 stage, which varied inversely with temperature. This critical period was associated with the time-interval in which the number of cells in the genital primordium began to increase, thus providing a morphological marker for the pathway decision in individual worms. Sensing the environment is the function of the amphidial neurons, and therefore we examined the role of individual amphidial neurons in controlling entry into the direct pathway to infectivity. The temperature-sensitive developmental switch is controlled by the neuron pair ALD (which also controls thermotaxis), as seen by the loss of control when these neurons are ablated. Thus, in S. stercoralis a single amphidial neuron pair controls both developmental and behavioural functions.

Strongyloides stercoralis: Cell- and tissue-specific transgene expression and co-transformation with vector constructs incorporating a common multifunctional 3′ UTR

“…C. elegans gpa-3 is expressed in eight pairs of chemosensory neurons in the amphidial complex (ADF, ADL, ASE, ASG, ASH, ASI, ASJ and ASK), two pairs of sensory neurons in the phasmids (PHA and PHB) and two other non-sensory cells (Jansen, et al, 1999). The amphidial neurons of S. stercoralis have been described and their homologies with amphidial neurons of C. elegans have been proposed based on morphology, position of cell bodies within the lateral ganglion and, in several cases, function inferred from microlaser ablation studies (Ashton, et al, 1995;Ashton, et al, 1998;Lopez, et al, 2000;Nolan, et al, 2004;Ashton, et al, 2007). We have not yet determined the specific identities of the GFP-expressing neurons in S. stercoralis transformed with pAJ09.…”

“…In addition, transformation constructs that are expressed in such small, defined groupings of cells in S. stercoralis may provide the basis for genetically targeted cell ablation using modified channel forming proteins as described for C. elegans (Driscoll and Chalfie, 1991;Harbinder, et al, 1997). In some instances such an approach could provide an alternative to microlaser surgical techniques currently in use for S. stercoralis (Lopez, et al, 2000;Nolan, et al, 2004;Ashton, et al, 2007).…”

The fork head transcription factor FKTF-1b from Strongyloides stercoralis restores DAF-16 developmental function to mutant Caenorhabditis elegans

“…This hypothesis has been bolstered by the discovery that dauer switching in C. elegans and the switch between homogonic and heterogonic developmental alternatives in the parasitic nematode Strongyloides stercoralis are controlled by the homologous amphidial neurons (Bargmann and Horvitz, 1991;Ashton et al, 1998;Nolan et al, 2004). Our laboratory is investigating possible parallels between molecular mechanisms regulating dauer development in C. elegans and the development of L3i in S. stercoralis.…”

Human strongyloidiasis: identifying knowledge gaps, with emphasis on environmental control

“…13,14 However, more recent research has found that in temperatures below 34°C, larvae molt four times and develop into free-living sexually mature adults, and in temperatures above 34°C, larvae molt twice and develop into infective filariform larvae. 15,16 Chemosensory factors may also influence larval differentiation. Chemosensory and thermosensory neurons are contained in the amphids in nematodes.…”