Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-18T07:33:22.466Z Has data issue: false hasContentIssue false
  • English
  • Français

Transcriptional changes in Teladorsagia circumcincta upon encountering host tissue of differing immune status

Published online by Cambridge University Press:  05 January 2012

AILEEN M. HALLIDAY ,
F. ALEX LAINSON ,
RAJA YAGA ,
NEIL F. INGLIS ,
STEPHEN BRIDGETT ,
MINTU NATH  and
DAVE P. KNOX
AILEEN M. HALLIDAY
Affiliation:
Moredun Research Institute, Bush Loan, Penicuik EH26 0PZ, UK
F. ALEX LAINSON
Affiliation:
Moredun Research Institute, Bush Loan, Penicuik EH26 0PZ, UK
RAJA YAGA
Affiliation:
Moredun Research Institute, Bush Loan, Penicuik EH26 0PZ, UK
NEIL F. INGLIS
Affiliation:
Moredun Research Institute, Bush Loan, Penicuik EH26 0PZ, UK
STEPHEN BRIDGETT
Affiliation:
The GenePool, Ashworth Laboratories, The King's Buildings, The University of Edinburgh, Edinburgh EH9 3JT, UK
MINTU NATH
Affiliation:
Biomathematics and Statistics Scotland, James Clerk Maxwell Building, The King's Buildings, Edinburgh EH9 3JZ, UK
DAVE P. KNOX*
Affiliation:
Moredun Research Institute, Bush Loan, Penicuik EH26 0PZ, UK
*
*Corresponding author: Moredun Research Institute, Bush Loan, Penicuik EH26 0PZ, UK. Tel: +44 (0)131 445 5111. Fax: +44 (0)131 445 6111. E-mail: dave.knox@moredun.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

The aim of this study was to elucidate transcriptional changes in the parasitic nematode Teladorsagia circumcincta upon encountering either naïve or immune ovine hosts. Pools of 100 000 exsheathed 3rd- stage T. circumcincta larvae were exposed in vitro to either an immune or naïve ovine abomasal environment, RNA was extracted from the larvae and sequenced using the Roche 454 platform. Each sample produced approximately 82 000 reads that assembled to give approximately 5500 Isotigs (contigs). The two sequence datasets were clustered together to give a total of 6969 clusters of which 18 were differentially expressed (P<0·001) between the two groups. Clusters with a predominance of reads in larvae exposed to the immune abomasal environment encoded homologues of peptidyl-glycine alpha-amidating monooxygenase, heat shock-protein 16-2 and IDA-1, a tyrosine phosphatase-like receptor protein. Clusters with a predominance of reads in the naïve environment encoded homologues of cytochrome b, EGg Laying defective family member 21 and NADH dehydrogenase subunit 5. Gene ontology analyses indicated that larvae exposed to the immune environment showed an increase in expression of genes involved in ‘carbon utilization’, ‘response to stimulus’ and ‘developmental process’. These data suggest that T. circumcincta modulates gene expression in response to the immune status of the host.

Keywords

Teladorsagia circumcinctagene expressionparasitic nematodessheepproteomicsimmunity
Type
Research Article
Information
Parasitology , Volume 139 , Issue 3 , March 2012 , pp. 387 - 405
Copyright
Copyright © Cambridge University Press 2012

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

Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., Harris, M. A., Hill, D. P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J. C., Richardson, J. E., Ringwald, M., Rubin, G. M. and Sherlock, G. (2000). Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nature Genetics 25, 25–29.CrossRefGoogle ScholarPubMed
Athanasiadou, S., Pemberton, A., Jackson, F., Inglis, N., Miller, H., Thevenod, F., Mackellar, A. and Huntley, J. (2008). Proteomic approach to identify candidate effector molecules during the in vitro immune exclusion of infective Teladorsagia circumcincta in the abomasum of sheep. Veterinary Research 39, 58–62.CrossRefGoogle ScholarPubMed
Baker, R. H., Buschbaum, S., Matthews, J. B., McKendrick, I. J., Schnieder, T., Strube, C. and Nisbet, A. J. (2011). GTP-Cyclohydrolase and development in Teladorsagia circumcincta and Dictyocaulus viviparus (Nematoda: Strongylida). Experimental Parasitology 128, 309–317.CrossRefGoogle ScholarPubMed
Balic, A., Bowles, V. M., Liu, Y. S. and Meeusen, E. N. T. (2003). Local immune responses in sensitized sheep following challenge infection with Teladorsagia circumcincta. Parasite Immunology 25, 375–381.CrossRefGoogle ScholarPubMed
Bellyei, S., Szigeti, A., Boronkai, A., Pozsgai, E., Gomori, E., Melegh, B., Janaky, T., Bognar, Z., Hocsak, E., Sumegi, B. and Gallyas, F. Jr. (2007). Inhibition of cell death by a novel 16 2 kD heat shock protein predominantly via Hsp90 mediated lipid rafts stabilization and Akt activation pathway. Apoptosis 12, 97–112.CrossRefGoogle ScholarPubMed
Benjamini, Y. and Hochberg, Y. (1995). Controlling the false discovery rate – a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B-Methodological 57, 289–300.Google Scholar
Benjamini, Y. and Yekutieli, D. (2005). Quantitative trait loci analysis using the false discovery rate. Genetics 171, 783–790.CrossRefGoogle ScholarPubMed
Cai, T., Fukushige, T., Notkins, A. L. and Krause, M. (2004). Insulinoma-Associated Protein IA-2, a vesicle transmembrane protein, genetically interacts with UNC-31/CAPS and affects neurosecretion in Caenorhabditis elegans. The Journal of Neuroscience 24, 3115–3124.CrossRefGoogle ScholarPubMed
Cantacessi, C., Campbell, B. E., Young, N. D., Jex, A. R., Hall, R. S., Presidente, P. J., Zawadzki, J. L., Zhong, W., Aleman, B., Loukas, A., Sternberg, P. W. and Gasser, R. B. (2010 a). Differences in transcription between free-living and CO2-activated third-stage larvae of Haemonchus contortus. BioMed Central Genomics 11, 266–279.Google ScholarPubMed
Cantacessi, Cinzia, Mitreva, Makedonka, Campbell, Bronwyn E., Hall, Ross S., Young, Neil D., Jex, Aaron R., Ranganathan, Shoba and Gasser, Robin B. (2010 b). First transcriptomic analysis of the economically important parasitic nematode, Trichostrongylus colubriformis, using a next-generation sequencing approach. Infection, Genetics and Evolution 10, 1199–1207.CrossRefGoogle ScholarPubMed
Conesa, A. and Gotz, S. (2008). Blast2GO: A comprehensive suite for functional analysis in plant genomics. International Journal of Plant Genomics 2008, 1–12.CrossRefGoogle ScholarPubMed
Conesa, A., Gotz, S., Garcia-Gomez, J. M., Terol, J., Talon, M. and Robles, M. (2005). Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674–3676.CrossRefGoogle ScholarPubMed
Dicker, Alison J., Nath, Mintu, Yaga, Raja, Nisbet, Alasdair J., Lainson, F., Alex, Gilleard, John, S. and Skuce, Philip J. (2011). Teladorsagia circumcincta: The transcriptomic response of a multi-drug-resistant isolate to ivermectin exposure in vitro. Experimental Parasitology 127, 351–356.CrossRefGoogle ScholarPubMed
Ding, L. and Candido, E. P. (2000). Association of several small heat-shock proteins with reproductive tissues in the nematode Caenorhabditis elegans. The Biochemical Journal 351, 13–17.CrossRefGoogle ScholarPubMed
Dong, D. J., He, H. J., Chai, L. Q., Jiang, X. J., Wang, J. X. and Zhao, X. F. (2007). Identification of genes differentially expressed during larval molting and metamorphosis of Helicoverpa armigera. BioMed Central Developmental Biology 7, 73–88.Google ScholarPubMed
Dunphy, J. L., Balic, A., Barcham, G. J., Horvath, A. J., Nash, A. D. and Meeusen, E. N. (2000). Isolation and characterization of a novel inducible mammalian galectin. The Journal of Biological Chemistry 275, 32106–32113.CrossRefGoogle ScholarPubMed
Duvaux-Miret, O., Stefano, G. B., Smith, E. M., Dissous, C. and Capron, A. (1992). Immunosuppression in the definitive and intermediate hosts of the human parasite Schistosoma mansoni by release of immunoactive neuropeptides. Proceedings of the National Academy of Sciences, USA 89, 778–781.CrossRefGoogle ScholarPubMed
Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461.CrossRefGoogle ScholarPubMed
Ehre, C., Rossi, A. H., Abdullah, L. H., De, Pestel K., Hill, S., Olsen, J. C. and Davis, C. W. (2005). Barrier role of actin filaments in regulated mucin secretion from airway goblet cells. American Journal for Physiology – Cell Physiology 288, C46–C56.CrossRefGoogle ScholarPubMed
Eipper, B. A., Milgram, S. L., Husten, E. J., Yun, H. Y. and Mains, R. E. (1993). Peptidylglycine alpha-amidating monooxygenase: a multifunctional protein with catalytic, processing, and routing domains. Protein Science 2, 489–497.CrossRefGoogle ScholarPubMed
French, A. T., Knight, P. A., Smith, W. D., Brown, J. K., Craig, N. M., Pate, J. A., Miller, H. R. P. and Pemberton, A. D. (2008). Up-regulation of intelectin in sheep after infection with Teladorsagia circumcincta. International Journal for Parasitology 38, 467–475.CrossRefGoogle ScholarPubMed
Gal, T. Z., Glazer, I., and Koltai, H. (2004). An LEA group 3 family member is involved in survival of C. elegans during exposure to stress. FEBS Letters 577, 21–26.CrossRefGoogle ScholarPubMed
Goldfinch, G. M., Smith, W. D., Imrie, L., McLean, K., Inglis, N. F. and Pemberton, A. D. (2008). The proteome of gastric lymph in normal and nematode infected sheep. Proteomics 8, 1909–1918.CrossRefGoogle ScholarPubMed
Gottlieb, S. and Ruvkun, G. (1994). daf-2, daf-16 and daf-23: genetically interacting genes controlling Dauer formation in Caenorhabditis elegans. Genetics 137, 107–120.CrossRefGoogle ScholarPubMed
Gotz, S., Garcia-Gomez, J. M., Terol, J., Williams, T. D., Nagaraj, S. H., Nueda, M. J., Robles, M., Talon, M., Dopazo, J. and Conesa, A. (2008). High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Research 36, 3420–3435.CrossRefGoogle ScholarPubMed
Halliday, A. M., McAllister, H. C. and Smith, W. D. (2010). Kinetics of the local immune response in the gastric lymph of lambs after primary and challenge infection with Teladorsagia circumcincta. Parasite Immunology 32, 81–90.CrossRefGoogle ScholarPubMed
Halliday, A. M., Morrison, W. I. and Smith, W. D. (2009). Kinetics of the local cellular response in the gastric lymph of immune and susceptible sheep to infection with Teladorsagia circumcincta. Parasite Immunology 31, 402–411.CrossRefGoogle ScholarPubMed
Halliday, A. M., Routledge, C. M., Smith, S. K., Matthews, J. B. and Smith, W. D. (2007). Parasite loss and inhibited development of Teladorsagia circumcincta in relation to the kinetics of the local IgA response in sheep. Parasite Immunology 29, 425–434.CrossRefGoogle Scholar
Hartwig, K., Heidler, T., Moch, J., Daniel, H. and Wenzel, U. (2009). Feeding a ROS-generator to Caenorhabditis elegans leads to increased expression of small heat shock protein HSP-16.2 and hormesis. Genes and Nutrition 4, 59–67.CrossRefGoogle ScholarPubMed
Hu, P. J. (2007). Dauer. In WormBook (ed. The C. elegans Research Community), pp. 1–19. WormBook http://www.wormbook.orgCrossRefGoogle Scholar
Hunter, S., Apweiler, R., Attwood, T. K., Bairoch, A., Bateman, A., Binns, D., Bork, P., Das, U., Daugherty, L., Duquenne, L., Finn, R. D., Gough, J., Haft, D., Hulo, N., Kahn, D., Kelly, E., Laugraud, A., Letunic, I., Lonsdale, D., Lopez, R., Madera, M., Maslen, J., McAnulla, C., McDowall, J., Mistry, J., Mitchell, A., Mulder, N., Natale, D., Orengo, C., Quinn, A. F., Selengut, J. D., Sigrist, C. J., Thimma, M., Thomas, P. D., Valentin, F., Wilson, D., Wu, C. H. and Yeats, C. (2009). InterPro: the integrative protein signature database. Nucleic Acids Research 37, D211–D215.CrossRefGoogle ScholarPubMed
Huntley, J. F., Schallig, H. D. F. H., Kooyman, F. N. J., Mackellar, A., Jackson, F. and Smith, W. D. (1998). IgE antibody during infection with the ovine abomasal nematode, Teladorsagia circumcincta: primary and secondary responses in serum and gastric lymph of sheep. Parasite Immunology 20, 565–571.CrossRefGoogle ScholarPubMed
Iriti, M. and Faoro, F. (2009). Chemical diversity and defence metabolism: how plants cope with pathogens and ozone pollution. International Journal of Molecular Sciences 10, 3371–3399.CrossRefGoogle ScholarPubMed
Jackson, F., Greer, A. W., Huntley, J., McAnulty, R. W., Bartley, D. J., Stanley, A., Stenhouse, L., Stankiewicz, M. and Sykes, A. R. (2004). Studies using Teladorsagia circumcincta in an in vitro direct challenge method using abomasal tissue explants. Veterinary Parasitology 124, 73–89.CrossRefGoogle Scholar
Jacob, T. C. and Kaplan, J. M. (2003). The EGL-21 carboxypeptidase E facilitates acetylcholine release at Caenorhabditis elegans neuromuscular junctions. The Journal of Neuroscience 23, 2122–2130.CrossRefGoogle ScholarPubMed
Jeong, P. Y., Kwon, M. S., Joo, H. J. and Paik, Y. K. (2009). Molecular time-course and the metabolic basis of entry into dauer in Caenorhabditis elegans. Public Library of Science ONE 4, e4162.Google ScholarPubMed
Kanehisa, M. and Goto, S. (2000). KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Research 28, 27–30.CrossRefGoogle ScholarPubMed
Macaldowie, C., Jackson, F., Huntley, J., Mackellar, A. and Jackson, E. (2003). A comparison of larval development and mucosal mast cell responses in worm-naive goat yearlings, kids and lambs undergoing primary and secondary challenge with Teladorsagia circumcincta. Veterinary Parasitology 114, 1–13.CrossRefGoogle ScholarPubMed
Margulies, M., Egholm, M., Altman, W. E., Attiya, S., Bader, J. S., Bemben, L. A., Berka, J., Braverman, M. S., Chen, Y. J., Chen, Z., Dewell, S. B., Du, L., Fierro, J. M., Gomes, X. V., Godwin, B. C., He, W., Helgesen, S., Ho, C. H., Irzyk, G. P., Jando, S. C., Alenquer, M. L., Jarvie, T. P., Jirage, K. B., Kim, J. B., Knight, J. R., Lanza, J. R., Leamon, J. H., Lefkowitz, S. M., Lei, M., Li, J., Lohman, K. L., Lu, H., Makhijani, V. B., McDade, K. E., McKenna, M. P., Myers, E. W., Nickerson, E., Nobile, J. R., Plant, R., Puc, B. P., Ronan, M. T., Roth, G. T., Sarkis, G. J., Simons, J. F., Simpson, J. W., Srinivasan, M., Tartaro, K. R., Tomasz, A., Vogt, K. A., Volkmer, G. A., Wang, S. H., Wang, Y., Weiner, M. P., Yu, P., Begley, R. F. and Rothberg, J. M. (2005). Genome sequencing in microfabricated high-density picolitre reactors. Nature, Lomdon 437, 376–380.CrossRefGoogle ScholarPubMed
McDowall, J. (2007). Clathrin. http://www.ebi.ac.uk/interpro/potm/2007_4/Page1.htmGoogle Scholar
McKellar, Q. A. (1993). Interactions of Ostertagia species with their bovine and ovine hosts. International Journal for Parasitology 23, 451–462.CrossRefGoogle ScholarPubMed
Miller, H. R. P. (1996). Mucosal mast cells and the allergic response against nematode parasites. Veterinary Immunology and Immunopathology 54, 331–336.CrossRefGoogle ScholarPubMed
Moredun (2011). Moredun Research Institute Proteomics Facility. http://www.moredun.org.uk/research/expertise-@-moredun/proteomics.Google Scholar
Nelson, L. S., Rosoff, M. L. and Li, C. (1998). Disruption of a neuropeptide gene, flp-1, causes multiple behavioral defects in Caenorhabditis elegans. Science 281, 1686–1690.CrossRefGoogle ScholarPubMed
Nieuhof, G. J. and Bishop, S. C. (2005). Costs of the major endemic diseases of sheep in Great Britain and the potential benefits of reduction in disease impact. Animal Science 81, 23–29.CrossRefGoogle Scholar
Nisbet, A. J., Redmond, D. L., Matthews, J. B., Watkins, C., Yaga, R., Jones, J. T., Nath, M. and Knox, D. P. (2008). Stage-specific gene expression in Teladorsagia circumcincta (Nematoda: Strongylida) infective larvae and early parasitic stages. International Journal for Parasitology 38, 829–838.CrossRefGoogle ScholarPubMed
O'Meara, H., Barber, R., Mello, L. V., Sangaralingam, A., Viney, M. E. and Paterson, S. (2010). Response of the Strongyloides ratti transcriptome to host immunological environment. International Journal for Parasitology 40, 1609–1617.CrossRefGoogle ScholarPubMed
Ogata, H., Goto, S., Sato, K., Fujibuchi, W., Bono, H. and Kanehisa, M. (1999). KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Research 27, 29–34.CrossRefGoogle ScholarPubMed
Parkinson, J., Anthony, A., Wasmuth, J., Schmid, R., Hedley, A. and Blaxter, M. (2004). PartiGene – Constructing partial genomes. Bioinformatics 20, 1398–1404.CrossRefGoogle ScholarPubMed
Pemberton, A. D., Verdon, B., Inglis, N. F. and Pearson, J. P. (2011). Sheep intelectin-2 co-purifies with the mucin Muc5ac from gastric mucus. Research in Veterinary Science. doi: 10.1016/j.rvsc.2011.03.004.CrossRefGoogle ScholarPubMed
Prigge, S. T., Mains, R. E., Eipper, B. A. and Amzel, L. M. (2000). New insights into copper monooxygenases and peptide amidation: structure, mechanism and function. Cellular and Molecular Life Sciences 57, 1236–1259.CrossRefGoogle ScholarPubMed
R Development Core Team (2010). A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Release 2.13. http://www.R-project.org.Google Scholar
Riddle, D. L. and Albert, P. S. (1997). Genetic and Environmental Regulation of Dauer Larva Development. In C. elegans II 2nd Edn. Chapter 26. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA.Google ScholarPubMed
Roche (2010). Part C – GS De Novo Assembler, GSS Reference Mapper, SFF Tools. In 454 Sequencing System Software Manual, v 2.5.3 454 Life Sciences Corp, A Roche Company. Branford CT 06405.Google Scholar
Roche (2011). Roche 454 Website. http://www.454.com.Google Scholar
Sargison, N. D. (2011). Pharmaceutical control of endoparasitic helminth infections in sheep. Veterinary Clinics of North America: Food Animal Practice 27, 139–156.Google ScholarPubMed
Scott, P. R., Sargison, N. D. and Wilson, D. J. (2007). The potential for improving welfare standards and productivity in United Kingdom sheep flocks using veterinary flock health plans. The Veterinary Journal 173, 522–531.CrossRefGoogle ScholarPubMed
Smith, S. K., Nisbet, A. J., Meikle, L. I., Inglis, N. F., Sales, J., Beynon, R. J. and Matthews, J. B. (2009). Proteomic analysis of excretory/secretory products released by Teladorsagia circumcincta larvae early post-infection. Parasite Immunology 31, 10–19.CrossRefGoogle ScholarPubMed
Smith, W. D. (2007). Some observations on immunologically mediated inhibited Teladorsagia circumcincta and their subsequent resumption of development in sheep. Veterinary Parasitology 147, 103–109.CrossRefGoogle ScholarPubMed
Smith, W. D., Jackson, F., Jackson, E., Graham, R., Williams, J., Willadsen, S. M. and Fehilly, C. B. (1986). Transfer of immunity to Ostertagia circumcincta and IgA memory between identical sheep by lymphocytes collected from gastric lymph. Research in Veterinary Science 41, 300–306.CrossRefGoogle ScholarPubMed
Smith, W. D., Jackson, F., Jackson, E. and Williams, J. (1983). Local immunity and Ostertagia circumcincta: changes in the gastric lymph of immune sheep after a challenge infection. Journal of Comparative Pathology 93, 479–488.CrossRefGoogle ScholarPubMed
Stear, M. J., Bishop, S. C., Doligalska, M., Duncan, J. L., Holmes, P. H., Irvine, J., McCririe, L., McKellar, Q. A., Sinski, E. and Murray, M. (1995). Regulation of egg production, worm burden, worm length and worm fecundity by host responses in sheep infected with Ostertagia circumcincta. Parasite Immunology 17, 643–652.CrossRefGoogle ScholarPubMed
Stear, M. J., Strain, S. and Bishop, S. C. (1999 a). How lambs control infection with Ostertagia circumcincta. Veterinary Immunology and Immunopathology 72, 213–218.CrossRefGoogle ScholarPubMed
Stear, M. J., Strain, S. and Bishop, S. C. (1999 b). Mechanisms underlying resistance to nematode infection. International Journal for Parasitology 29, 51–56.CrossRefGoogle ScholarPubMed
Sun, H. Q., Yamamoto, M., Mejillano, M. and Yin, H. L. (1999). Gelsolin, a multifunctional actin regulatory protein. Journal of Biological Chemistry 274, 33179–33182.CrossRefGoogle ScholarPubMed
Thomas, J. H., Birnby, D. A. and Vowels, J. J. (1993). Evidence for parallel processing of sensory information controlling dauer formation in Caenorhabditis elegans. Genetics 134, 1105–1117.CrossRefGoogle ScholarPubMed
Thompson, F. J., Barker, G. L., Hughes, L. and Viney, M. E. (2008). Genes important in the parasitic life of the nematode Strongyloides ratti. Molecular and Biochemical Parasitology 158, 112–119.CrossRefGoogle ScholarPubMed
Vandekerckhove, J., Bauw, G., Vancompernolle, K., Honore, B. and Celis, J. (1990). Comparative two-dimensional gel analysis and microsequencing identifies gelsolin as one of the most prominent downregulated markers of transformed human fibroblast and epithelial cells. Journal of Cell Biology 111, 95–102.CrossRefGoogle ScholarPubMed
Wormbase (2011). Wormbase website. http://www.wormbase.org. Release WS225.Google Scholar
Young, N. D., Hall, R. S., Jex, A. R., Cantacessi, C. and Gasser, R. B. (2003). Elucidating the transcriptome of Fasciola hepatica – A key to fundamental and biotechnological discoveries for a neglected parasite. Biotechnology Advances 28, 222–231.CrossRefGoogle Scholar
Zahn, T. R., Macmorris, M. A., Dong, W., Day, R. and Hutton, J. C. (2001). IDA-1, a Caenorhabditis elegans homolog of the diabetic autoantigens IA-2 and phogrin, is expressed in peptidergic neurons in the worm. The Journal of Comparative Neurology 429, 127–143.3.0.CO;2-H>CrossRefGoogle ScholarPubMed