Hostname: page-component-848d4c4894-pjpqr Total loading time: 0 Render date: 2024-06-25T14:05:01.699Z Has data issue: false hasContentIssue false

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

Published online by Cambridge University Press:  18 November 2004

T. J. NOLAN
Affiliation:
Laboratory of Parasitology, University of Pennsylvania School of Veterinary Medicine, 3800 Spruce St, Philadelphia, PA 19104, USA
M. BRENES
Affiliation:
Laboratory of Parasitology, University of Pennsylvania School of Veterinary Medicine, 3800 Spruce St, Philadelphia, PA 19104, USA
F. T. ASHTON
Affiliation:
Laboratory of Parasitology, University of Pennsylvania School of Veterinary Medicine, 3800 Spruce St, Philadelphia, PA 19104, USA
X. ZHU
Affiliation:
Laboratory of Parasitology, University of Pennsylvania School of Veterinary Medicine, 3800 Spruce St, Philadelphia, PA 19104, USA
W. M. FORBES
Affiliation:
Laboratory of Parasitology, University of Pennsylvania School of Veterinary Medicine, 3800 Spruce St, Philadelphia, PA 19104, USA
R. BOSTON
Affiliation:
Section of Animal Production Systems, University of Pennsylvania School of Veterinary Medicine, 382 West Street Road, Kennett Square, PA 19348, USA
G. A. SCHAD
Affiliation:
Laboratory of Parasitology, University of Pennsylvania School of Veterinary Medicine, 3800 Spruce St, Philadelphia, PA 19104, USA

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 °C the larvae enter the indirect pathway and develop to free-living adulthood. Conversely, at temperatures approaching body temperature (34 °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.

Type
Research Article
Copyright
© 2004 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

ALBERT, P. S., BROWN, S. J. & RIDDLE, D. L. ( 1981). Sensory control of dauer larva formation in Caenorhabditis elegans. Journal of Comparative Neurology 198, 435451.CrossRefGoogle Scholar
ASHTON, F. T., BHOPALE, V. M., FINE, A. E. & SCHAD, G. A. ( 1995). Sensory neuroanatomy of a skin-penetrating nematode parasite: Strongyloides stercoralis. I. Amphidial neurons. Journal of Comparative Neurology 357, 281295.Google Scholar
ASHTON, F. T., BHOPALE, V. M., HOLT, D., SMITH, G. & SCHAD, G. A. ( 1998). Developmental switching in the parasitic nematode Strongyloides stercoralis is controlled by the ASF and ASI amphidial neurons. Journal of Parasitology 84, 691695.CrossRefGoogle Scholar
ASHTON, F. T., LI, J. & SCHAD, G. A. ( 1999). Chemo- and thermosensory neurons: structure and function in animal parasitic nematodes. Veterinary Parasitology 84, 297316.CrossRefGoogle Scholar
BARGMANN, C. & HORVITZ, H. R. ( 1991). Control of larval development by chemosensory neurons in Caenorhabditis elegans. Science 251, 12431246.CrossRefGoogle Scholar
BARGMANN, C. & MORI, H. ( 1997). Chemotaxis and thermotaxis. In C. elegans II (ed. Riddle, D. L., Blumenthal, T., Meyer, B. J. & Preiss, J. R.), pp. 717738. Cold Spring Harbor Press, Cold Spring Harbor, USA.
FAUST, E. C. ( 1933). Experimental studies on human and primate species of Strongyloides. II. The development of Strongyloides in the experimental host. The American Journal of Hygiene 18, 114132.CrossRefGoogle Scholar
GEMMILL, A. W., VINEY, M. E. & READ, A. F. ( 1997). Host immune status determines sexuality in a parasitic nematode. Evolution 51, 393401.CrossRefGoogle Scholar
GOLDEN, J. W. & RIDDLE, D. L. ( 1984). The Caenorhabditis elegans dauer larva: developmental effects of pheromone, food, and temperature. Developmental Biology 102, 368378.CrossRefGoogle Scholar
HAMMMOND, M. P. & ROBINSON, R. D. ( 1994). Chromosome complement, gametogenesis and development of Strongyloides stercoralis. Journal of Parasitology 80, 689695.CrossRefGoogle Scholar
HOTEZ, P., HAWDON, J. & SCHAD, G. A. ( 1993). Hookworm larval infectivity, arrest and amphiparatenesis: the Caenorhabditis elegans Daf-c paradigm. Parasitology Today 9, 2326.CrossRefGoogle Scholar
KREIS, H. A. ( 1932). Studies on the genus Strongyloides (Nematodes). The American Journal of Hygiene 16, 450491.CrossRefGoogle Scholar
LOPEZ, P. M., BOSTON, R., ASHTON, F. T. & SCHAD, G. A. ( 2000 a). The neurons of class ALD mediate thermotaxis in the parasitic nematode, Strongyloides stercoralis. International Journal for Parasitology 30, 11151121.Google Scholar
LOPEZ, P. M., NOLAN, T. J. & SCHAD, G. A. ( 2000 b). Growth of the genital primordium as a marker to describe a time course for the heterogonic larval development in Strongyloides stercoralis. Journal of Parasitology 86, 882883.Google Scholar
MINEMATSU, M. M. T., TANAKA, M. & TADA, I. ( 1989). The effect of fatty acids on the developmental direction of Strongyloides ratti first-stage larvae. Journal of Helminthology 63, 102106.CrossRefGoogle Scholar
MONCOL, D. J. & TRIANTAPHYLLOU, A. C. ( 1978). Strongyloides ransomi: factors influencing the in vitro development of the free-living generation. Journal of Parasitology 64, 220225.CrossRefGoogle Scholar
MORI, I. & OHSHIMA, Y. ( 1995). Neural regulation of thermotaxis in Caenorhabditis elegans. Nature, London 376, 344347.CrossRefGoogle Scholar
NWAORGU, O. C. ( 1983). The development of the free-living stages of Strongyloides papillosus. I. Effect of temperature on the development of heterogonic and homogonic nematodes in faecal culture. Veterinary Parasitology 13, 213223.CrossRefGoogle Scholar
PREMVATI ( 1958). Studies on Strongyloides of Primates. II. Factors determining the “direct” and the “indirect” mode of life. Canadian Journal of Zoology 36, 185195.Google Scholar
RIDDLE, D. L. ( 1988). The dauer larva. In The Nematode Caenorhabditis elegans (ed. Wood, W. B.), pp. 393412. Cold Spring Harbor Laboratory Press, New York.
SCHAD, G. A., HELLMAN, M. E. & MUNCEY, D. W. ( 1984). Strongyloides stercoralis: hyperinfection in immunosuppressed dogs. Experimental Parasitology 57, 287296.CrossRefGoogle Scholar
VINEY, M. E. ( 1996). Developmental switching in the parasitic nematode Strongyloides ratti. Proceedings of the Royal Society of London, B 263, 201208.CrossRefGoogle Scholar