Transcriptional changes in the hookworm, Ancylostoma caninum, during the transition from a free-living to a parasitic larva.

BACKGROUND: Third-stage larvae (L3) of the canine hookworm, Ancylostoma caninum, undergo arrested development preceding transmission to a host. Many of the mRNAs up-regulated at this stage are likely to encode proteins that facilitate the transition from a free-living to a parasitic larva. The initi...

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Published in:PLoS Neglected Tropical Diseases
Main Authors: Bennett J D Datu, Robin B Gasser, Shivashankar H Nagaraj, Eng K Ong, Peter O'Donoghue, Russell McInnes, Shoba Ranganathan, Alex Loukas
Format: Article in Journal/Newspaper
Language:English
Published: Public Library of Science (PLoS) 2008
Subjects:
Online Access:https://doi.org/10.1371/journal.pntd.0000130
https://doaj.org/article/3f370d885406402c9651f385b0167449
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spelling ftdoajarticles:oai:doaj.org/article:3f370d885406402c9651f385b0167449 2023-05-15T15:13:12+02:00 Transcriptional changes in the hookworm, Ancylostoma caninum, during the transition from a free-living to a parasitic larva. Bennett J D Datu Robin B Gasser Shivashankar H Nagaraj Eng K Ong Peter O'Donoghue Russell McInnes Shoba Ranganathan Alex Loukas 2008-01-01T00:00:00Z https://doi.org/10.1371/journal.pntd.0000130 https://doaj.org/article/3f370d885406402c9651f385b0167449 EN eng Public Library of Science (PLoS) http://europepmc.org/articles/PMC2217673?pdf=render https://doaj.org/toc/1935-2727 https://doaj.org/toc/1935-2735 1935-2727 1935-2735 doi:10.1371/journal.pntd.0000130 https://doaj.org/article/3f370d885406402c9651f385b0167449 PLoS Neglected Tropical Diseases, Vol 2, Iss 1, p e130 (2008) Arctic medicine. Tropical medicine RC955-962 Public aspects of medicine RA1-1270 article 2008 ftdoajarticles https://doi.org/10.1371/journal.pntd.0000130 2022-12-31T07:25:10Z BACKGROUND: Third-stage larvae (L3) of the canine hookworm, Ancylostoma caninum, undergo arrested development preceding transmission to a host. Many of the mRNAs up-regulated at this stage are likely to encode proteins that facilitate the transition from a free-living to a parasitic larva. The initial phase of mammalian host invasion by A. caninum L3 (herein termed "activation") can be mimicked in vitro by culturing L3 in serum-containing medium. METHODOLOGY/PRINCIPAL FINDINGS: The mRNAs differentially transcribed between activated and non-activated L3 were identified by suppression subtractive hybridisation (SSH). The analysis of these mRNAs on a custom oligonucleotide microarray printed with the SSH expressed sequence tags (ESTs) and publicly available A. caninum ESTs (non-subtracted) yielded 602 differentially expressed mRNAs, of which the most highly represented sequences encoded members of the pathogenesis-related protein (PRP) superfamily and proteases. Comparison of these A. caninum mRNAs with those of Caenorhabditis elegans larvae exiting from developmental (dauer) arrest demonstrated unexpectedly large differences in gene ontology profiles. C. elegans dauer exiting L3 up-regulated expression of mostly intracellular molecules involved in growth and development. Such mRNAs are virtually absent from activated hookworm larvae, and instead are over-represented by mRNAs encoding extracellular proteins with putative roles in host-parasite interactions. CONCLUSIONS/SIGNIFICANCE: Although this should not invalidate C. elegans dauer exit as a model for hookworm activation, it highlights the limitations of this free-living nematode as a model organism for the transition of nematode larvae from a free-living to a parasitic state. Article in Journal/Newspaper Arctic Directory of Open Access Journals: DOAJ Articles Arctic PLoS Neglected Tropical Diseases 2 1 e130
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
spellingShingle Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
Bennett J D Datu
Robin B Gasser
Shivashankar H Nagaraj
Eng K Ong
Peter O'Donoghue
Russell McInnes
Shoba Ranganathan
Alex Loukas
Transcriptional changes in the hookworm, Ancylostoma caninum, during the transition from a free-living to a parasitic larva.
topic_facet Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
description BACKGROUND: Third-stage larvae (L3) of the canine hookworm, Ancylostoma caninum, undergo arrested development preceding transmission to a host. Many of the mRNAs up-regulated at this stage are likely to encode proteins that facilitate the transition from a free-living to a parasitic larva. The initial phase of mammalian host invasion by A. caninum L3 (herein termed "activation") can be mimicked in vitro by culturing L3 in serum-containing medium. METHODOLOGY/PRINCIPAL FINDINGS: The mRNAs differentially transcribed between activated and non-activated L3 were identified by suppression subtractive hybridisation (SSH). The analysis of these mRNAs on a custom oligonucleotide microarray printed with the SSH expressed sequence tags (ESTs) and publicly available A. caninum ESTs (non-subtracted) yielded 602 differentially expressed mRNAs, of which the most highly represented sequences encoded members of the pathogenesis-related protein (PRP) superfamily and proteases. Comparison of these A. caninum mRNAs with those of Caenorhabditis elegans larvae exiting from developmental (dauer) arrest demonstrated unexpectedly large differences in gene ontology profiles. C. elegans dauer exiting L3 up-regulated expression of mostly intracellular molecules involved in growth and development. Such mRNAs are virtually absent from activated hookworm larvae, and instead are over-represented by mRNAs encoding extracellular proteins with putative roles in host-parasite interactions. CONCLUSIONS/SIGNIFICANCE: Although this should not invalidate C. elegans dauer exit as a model for hookworm activation, it highlights the limitations of this free-living nematode as a model organism for the transition of nematode larvae from a free-living to a parasitic state.
format Article in Journal/Newspaper
author Bennett J D Datu
Robin B Gasser
Shivashankar H Nagaraj
Eng K Ong
Peter O'Donoghue
Russell McInnes
Shoba Ranganathan
Alex Loukas
author_facet Bennett J D Datu
Robin B Gasser
Shivashankar H Nagaraj
Eng K Ong
Peter O'Donoghue
Russell McInnes
Shoba Ranganathan
Alex Loukas
author_sort Bennett J D Datu
title Transcriptional changes in the hookworm, Ancylostoma caninum, during the transition from a free-living to a parasitic larva.
title_short Transcriptional changes in the hookworm, Ancylostoma caninum, during the transition from a free-living to a parasitic larva.
title_full Transcriptional changes in the hookworm, Ancylostoma caninum, during the transition from a free-living to a parasitic larva.
title_fullStr Transcriptional changes in the hookworm, Ancylostoma caninum, during the transition from a free-living to a parasitic larva.
title_full_unstemmed Transcriptional changes in the hookworm, Ancylostoma caninum, during the transition from a free-living to a parasitic larva.
title_sort transcriptional changes in the hookworm, ancylostoma caninum, during the transition from a free-living to a parasitic larva.
publisher Public Library of Science (PLoS)
publishDate 2008
url https://doi.org/10.1371/journal.pntd.0000130
https://doaj.org/article/3f370d885406402c9651f385b0167449
geographic Arctic
geographic_facet Arctic
genre Arctic
genre_facet Arctic
op_source PLoS Neglected Tropical Diseases, Vol 2, Iss 1, p e130 (2008)
op_relation http://europepmc.org/articles/PMC2217673?pdf=render
https://doaj.org/toc/1935-2727
https://doaj.org/toc/1935-2735
1935-2727
1935-2735
doi:10.1371/journal.pntd.0000130
https://doaj.org/article/3f370d885406402c9651f385b0167449
op_doi https://doi.org/10.1371/journal.pntd.0000130
container_title PLoS Neglected Tropical Diseases
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