Teladorsagia circumcincta: Activation-associated secreted proteins in excretory/secretory products of fourth stage larvae are targets of early IgA responses in infected sheep

Nisbet, Alasdair J.; Smith, Simon; Armstrong, Stuart D.; Meikle, L. I.; Wildblood, L. A.; Beynon, Robert J.; Matthews, J. B.

doi:10.1016/j.exppara.2010.02.014

Cited by 29 publications

(40 citation statements)

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“…Despite the fact that the exact function of SCP/TAPS proteins remains unknown, various studies have shown that they are amongst the most abundant proteins expressed and secreted during the transition from the free-living to the parasitic life stages, suggesting an important role in the onset of parasitism [55]. Compared with the number of SCP/TAPS proteins identified in the ES material of some other species [20], [56], [57], it is surprising that only 2 were identified in the current study. However, this finding is concordant with previous evidence from genomic and transcriptomic datasets [23] indicating the presence of only 12 SCP/TAPS-encoding genes in the A. suum with relatively limited transcription levels (results not shown).…”

Section: Discussionmentioning

confidence: 99%

Proteomic Analysis of the Excretory-Secretory Products from Larval Stages of Ascaris suum Reveals High Abundance of Glycosyl Hydrolases

et al. 2013

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Background Ascaris lumbricoides and Ascaris suum are socioeconomically important and widespread parasites of humans and pigs, respectively. The excretory-secretory (ES) molecules produced and presented at the parasite-host interface during the different phases of tissue invasion and migration are likely to play critical roles in the induction and development of protective immune and other host responses.Methodology/Principal FindingsThe aim of this study was to identify the ES proteins of the different larval stages (L3-egg, L3-lung and L4) by LC-MS/MS. In total, 106 different proteins were identified, 20 in L3-egg, 45 in L3-lung stage and 58 in L4. Although most of the proteins identified were stage-specific, 15 were identified in the ES products of at least two stages. Two proteins, i.e. a 14-3-3-like protein and a serpin-like protein, were present in the ES products from the three different larval stages investigated. Interestingly, a comparison of ES products from L4 with those of L3-egg and L3-lung showed an abundance of metabolic enzymes, particularly glycosyl hydrolases. Further study indicated that most of these glycolytic enzymes were transcriptionally upregulated from L4 onwards, with a peak in the adult stage, particularly in intestinal tissue. This was also confirmed by enzymatic assays, showing the highest glycosidase activity in protein extracts from adult worms gut.Conclusions/SignificanceThe present proteomic analysis provides important information on the host-parasite interaction and the biology of the migratory stages of A. suum. In particular, the high transcriptional upregulation of glycosyl hydrolases from the L4 stage onwards reveals that the degradation of complex carbohydrates forms an essential part of the energy metabolism of this parasite once it establishes in the small intestine.

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Section: Discussionmentioning

confidence: 99%

Proteomic Analysis of the Excretory-Secretory Products from Larval Stages of Ascaris suum Reveals High Abundance of Glycosyl Hydrolases

et al. 2013

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“…Before the RNAi experiments commenced, transcripts of Tci-asp-1 and tdc00462 were sought in T. circumcincta exsheathed L3. In previous studies, the protein and transcript of Tci-asp-1 were identified in L4, but not in exsheathed L3 (Nisbet et al, 2010b), exsheathment in these former studies being stimulated using sodium hypochlorite. Here, we compared two exsheathment methods and the results showed that transcription of Tci-asp-1 and tdc00462 was activated only after exsheathing L3 with CO 2 .…”

Section: Discussionmentioning

confidence: 95%

“…Accession numbers, primer and probe sequences (orientated from 5 0 to 3 0 end) of the candidate marker genes (dcr-1, rsd-3 and ego-1) and the housekeeping genes ( pmp-3 and y45f10d.4) for the qRT-PCR in C. elegans. and the remaining 10,000 used for immunoblotting with sera to a recombinant version of Tci-ASP-1 (rTci-ASP-1) (Nisbet et al, 2010b).…”

Section: Genementioning

confidence: 99%

Marker genes for activation of the RNA interference (RNAi) pathway in the free-living nematodeCaenorhabditis elegansand RNAi development in the ovine nematodeTeladorsagia circumcincta

et al. 2013

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The nematode Teladorsagia circumcincta is a major cause of parasitic gastroenteritis in sheep in temperate regions. The development of resistance to the major anthelmintic classes used for its control is a threat to small ruminant farming sustainability. Vaccination is a potential alternative control method for this nematode. Gene datasets can be exploited to identify potential vaccine candidates and these validated further by methods such as RNA interference (RNAi) prior to vaccine trials. Previous reports indicate that RNAi in parasitic nematodes is inconsistent and, to date, there are no internal controls that indicate activation of the RNAi pathway in response to double-stranded RNA (dsRNA). The present aims were to determine whether or not the transcription levels of potential marker genes in the RNAi pathway could indicate activation of the pathway in Caenorhabditis elegans and to develop an RNAi platform in T. circumcincta. In C. elegans, transcript levels of three candidate marker genes, Ce-dcr-1 (Dicer), Ce-ego-1 (Enhancer of Glp-One family member) and Ce-rsd-3 (RNAi Spreading Defective), were analysed and results indicated that activation of the pathway had no effect on transcript levels of these genes. In T. circumcincta, two vaccine candidate genes from the Activation-associated Secreted Protein (ASP) family were targets for knockdown. RNAi experiments showed successful silencing of both targets, although inconsistencies in efficacy were observed. After testing a number of parameters that might affect variability, it was found that the length of the storage period of the larvae plays an important role in the consistency of the RNAi results.

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“…Elevated levels of antigen-specific IgG1, IgG2a, IgG2b and IgA were observed during experimental infection by Brugia malayi, and correlates with resistance to infection (Shakya et al, 2009). Nisbet et al (2010) denoted that secretory/excretory antigens of Teladorsagia circumcincta are targets of early IgA response in infected sheep. In mice infected by Vampirolepis nana, expulsion of the parasite is closely associated with the appearance of parasite-specific IgA (Matsuzawa et al, 2008).…”

Section: Discussionmentioning

confidence: 99%

Lagochilascaris minor: Specific antibodies are related with resistance to experimental infection in A/J strain of mice

et al. 2011

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SummaryLagochilascaris minor is the causative agent of human lagochilascariosis, a disease that affects the neck region causing abscesses with eggs, adult parasites and L3/L4 larvae within purulent exudates. Nowadays, mice are considered intermediary hosts for the parasite. In previous study we observed that A/J mice experimentally infected with Lagochilascaris minor showed higher survival ratios than B10.A mice. Now, we denoted that A/J mice (resistant to experimental infection) produced higher levels of IgM, IgG and IgA against the crude extract (excepted for IgM) and secreted/excreted antigens of the parasite; on the other hand, B10.A mice (susceptible to experimental infection) produced higher levels of IgE in the later period of the experimental infection than A/J infected mice.

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Teladorsagia circumcincta: Activation-associated secreted proteins in excretory/secretory products of fourth stage larvae are targets of early IgA responses in infected sheep

Cited by 29 publications

References 50 publications

Proteomic Analysis of the Excretory-Secretory Products from Larval Stages of Ascaris suum Reveals High Abundance of Glycosyl Hydrolases

Proteomic Analysis of the Excretory-Secretory Products from Larval Stages of Ascaris suum Reveals High Abundance of Glycosyl Hydrolases

Marker genes for activation of the RNA interference (RNAi) pathway in the free-living nematodeCaenorhabditis elegansand RNAi development in the ovine nematodeTeladorsagia circumcincta

Lagochilascaris minor: Specific antibodies are related with resistance to experimental infection in A/J strain of mice

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