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A preliminary proteomic survey of the in vitro excretory/secretory products of fourth-stage larval and adult Teladorsagia circumcincta

Published online by Cambridge University Press:  03 January 2006

H. CRAIG ,
J. M. WASTLING  and
D. P. KNOX
H. CRAIG
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik, Midlothian, Scotland EH 26 0PZ, UK
J. M. WASTLING
Affiliation:
University of Liverpool, Faculty of Veterinary Science, University of Liverpool, PO Box 147, Liverpool L69 3BX, UK
D. P. KNOX
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik, Midlothian, Scotland EH 26 0PZ, UK
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Abstract

The nature of the proteins which comprise the in vitro excretory/secretory products (ES) of the fourth-stage larva (L4) and adult Teladorsagia circumcincta are largely undefined, despite the fact that this nematode induces profound changes, in part related to parasite ES, in the cellular architecture of the glands lining the abomasal surface of infected sheep and goats. In this study, the protein components of L4 and adult ES were fractionated using 1D gel electrophoresis and the major protein bands, detected by Coomassie blue staining, excised from the gel and subjected to tryptic digest and subsequent mass spectrometric analysis. The resultant peptide mass fingerprints were used to identify 15 L4 and 13 adult ES proteins. Several proteins, such as globin and some metabolic enzymes, were present in both ES. L4 ES alone contained thioredoxin peroxidase, an enzyme that can detoxify free radicals resulting from host inflammatory responses to the parasite, a cysteine proteinase which may aid penetration of the gastric mucosa and 2 different galectins which may influence cell differentiation and morphogenesis. Adult ES contained a nucleoside diphosphate kinase homologue, an enzyme which has been linked to cellular changes and can affect liquid secretion and goblet cell degranulation.

Keywords

Teladorsagiaexcretory/secretory productsproteomicsmass spectrometry
Type
Research Article
Information
Parasitology , Volume 132 , Issue 4 , April 2006 , pp. 535 - 543
Copyright
2006 Cambridge University Press

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References

REFERENCES

Bakker, N., Vervelde, l., Kanobana, K., Knox, D. P., Cornelissen, A. W., de Vries, E. and Yatsuda, A. P. ( 2004). Vaccination against the nematode Haemonchus contortus with a thiol-binding fraction from the excretory/secretory products (ES). Vaccine 22, 618–628.CrossRefGoogle Scholar
Barrett, J. ( 1981). The anaerobic end-products of helminths. Parasitology 88, 179–198.Google Scholar
Cancela, M., Carmona, C., Rossi, S., Frangione, B., Goni, F. and Berasain, P. ( 2004) Purification, characterization, and immunolocalization of paramyosin from the adult stage of Fasciola hepatica. Parasitology Research 92, 441–448.CrossRefGoogle Scholar
Claerebout, E., Smith, W. D., Pettit, D., Geldhof, P., Raes, S., Geurden, T. and Vercruysse, J. ( 2005). Protection studies with a globin-enriched protein fraction of Ostertagia ostertagi. Veterinary Parasitology 128, 299–307.CrossRefGoogle Scholar
Dalton, J. P., McGonigle, S., Rolph, T. P. and Andrews, S. J. ( 1996). Induction of protective immunity in cattle against infection with Fasciola hepatica by vaccination with cathepsin L proteinases and haemoglobin. Infection and Immunity 64, 5066–5074.Google Scholar
Donaldson, S. H., Picher, M. and Boucher, R. C. ( 2002). Secreted and cell-associated adenylate kinase and nucleoside diphosphokinase contribute to extracellular nucleotide metabolism on human airway surfaces. American Journal of Respiratory Cell and Molecular Biology 26, 209–215.CrossRefGoogle Scholar
Dougherty, M. K. and Morrison, D. K. ( 2004). Unlocking the code of 14-3-3. Journal for Cell Scientists 117, 1875–1884.CrossRefGoogle Scholar
Frenkel, M. J., Dopheide, T. A., Wagland, B. M. and Ward, C. W. ( 1992). The isolation, characterization and cloning of a globin-like, host-protective antigen from the excretory-secretory products of Trichostrongylus colubriformis. Molecular and Biochemical Parasitology 50, 27–36.CrossRefGoogle Scholar
Geldhof, P., Claerebout, E., Knox, D., Vercauteren, I., Looszova, A. and Vercruysse, J. ( 2000). Proteinases released in vitro by the parasitic stages of the bovine abomasal nematode Ostertagia ostertagi. Parasitology 121, 639–647.CrossRefGoogle Scholar
Geldhof, P., Vercauteren, I., Gevaert, K., Staes, A., Knox, D.P., Vandekerckhove, J., Vercruysse, J. and Claerebout, E. ( 2003 a). Activation-associated secreted proteins are the most abundant antigens in a host protective fraction from Ostertagia ostertagi. Molecular and Biochemical Parasitology 128, 111–114.Google Scholar
Geldhof, P., Claerebout, E., Knox, D., Vercauteren, I., Looszova, A. and Vercruysse, J. ( 2002). Vaccination of calves against Ostertagia ostertagi with cysteine proteinase enriched protein fractions. Parasite Immunology 24, 263–270.CrossRefGoogle Scholar
Geldhof, P., Vercauteren, I., Vanzeveren, A., DeMaere, V., Berx, G., Knox, D., Vercruysse, J. and Claerebout, E. ( 2003 b). Protein disulphide isomerase of Ostertagia ostertagi: an excretory-secretory product of L4 and adult worms? International Journal for Parasitology 33, 129–136.Google Scholar
Gobert, G. N. and McManus, D. P. ( 2005). Update on paramyosin in parasitic worms. Parasitology International 54, 101–107.CrossRefGoogle Scholar
Goud, G. N., Zhan, B., Ghosh, K., Loukas, A., Hawdon, J., Dobardzic, A., Deumic, V., Liu, S., Dobardzic, R., Zook, B. C., Jin, Q., Liu, Y., Hoffman, L., Chung-Debose, S., Patel, R., Mendez, S. and Hotez, P. J. ( 2004). Cloning, yeast expression, isolation, and vaccine testing of recombinant Ancylostoma-secreted protein (ASP)-1 and ASP-2 from Ancylostoma ceylanicum. Journal of Infectious Disease 189, 919–929.CrossRefGoogle Scholar
Gounaris, K., Thomas, S., Najarro, P. and Selkirk, M. E. ( 2001). Secreted variant of nucleoside diphosphate kinase from the intracellular parasitic nematode Trichinella spiralis. Infection and Immunity 69, 3658–3662.CrossRefGoogle Scholar
Hartman, D., Cottee, P. A., Savin, K. W., Bhave, M., Presidente, P. J., Fulton, L., Walkiewicz, M. and Newton, S. E. ( 2003). Haemonchus contortus: molecular characterisation of a small heat shock protein. Experimental Parasitology 104, 96–103.CrossRefGoogle Scholar
Hertzberg, H., Huwyler, U., Kohler, L., Rehbein, S. and Wanner, M. ( 2002). Kinetics of exsheathment of infective ovine and bovine strongylid larvae in vivo and in vitro. Parasitology 125, 65–70.CrossRefGoogle Scholar
Heschl, M. F. and Baillie, D. L. ( 1990). The HSP70 multigene family of Caenorhabditis elegans. Comparative Biochemistry and Physiology B 96, 633–637.CrossRefGoogle Scholar
Hsu, V., Zobel, C. L., Lambie, E. J., Schedl, T. and Kornfeld, K. ( 2002). Caenorhabditis elegans lin-45 raf is essential for larval viability, fertility and the induction of vulval cell fates. Genetics, 160, 481–492.Google Scholar
Jolodar, A., Fischer, P., Bergmann, S., Buttner, D. W., Hammerschmidt, S. and Brattig, N. W. ( 2003). Molecular cloning of an alpha-enolase from the human filarial parasite Onchocerca volvulus that binds human plasminogen. Biochimica et Biophysica Acta 1627, 111–120.CrossRefGoogle Scholar
Jefferies, J. R., Campbell, A. M., Van Rossum, A. J., Barrett, J. and Brophy, P. M. ( 2001). Proteomic analysis of Fasciola hepatica excretory-secretory products. Proteomics 1, 1128–1132.3.0.CO;2-0>CrossRefGoogle Scholar
Jenkins, R. E., Taylor, M. J., Gilvary, N. J. and Bianco, A. E. ( 1998). Tropomyosin implicated in host protective responses to microfilariae in onchocerciasis. Proceedings of the National Academy of Sciences, USA 95, 7550–7555.CrossRefGoogle Scholar
Kasai, K. and Hirabayashi, J. ( 1996). Galectins: a family of animal lectins that decipher glycocodes. Journal for Biochemistry 119, 1–8.CrossRefGoogle Scholar
Klimowski, L., Chandrashekar, R. and Tripp, C. A. ( 1997). Molecular cloning, expression and enzymatic activity of a thioredoxin peroxidase from Dirofilaria immitis. Molecular and Biochemical Parasitology 90, 297–306.CrossRefGoogle Scholar
Knox, D. P. ( 2000). Development of vaccines against gastrointestinal nematodes. Parasitology 120 (Suppl), S43–S61.CrossRefGoogle Scholar
McCarthy, J. S., Wieseman, M., Tropea, J., Kaslow, D., Abraham, D., Lustigman, S., Tuan, R., Guderian, R. H. and Nutman, T. B. ( 2002). Onchocerca volvulus glycolytic enzyme fructose-1,6-bisphosphate aldolase as a target for a protective immune response in humans. Infection and Immunity 70, 851–858.CrossRefGoogle Scholar
McGillivery, D. J., Yong, W. K., Adler, B. and Riffkin, G. G. ( 1992). A purified stage-specific 31 kDa antigen as a potential protective antigen against Ostertagia circumcincta in lambs. Vaccine 10, 607–613.CrossRefGoogle Scholar
Morton, R. E., Yong, W. K., Riffkin, G. G., Bozas, S., Spithill, T. W., Adler, B. and Parsons, J. C. ( 1995). Inability to reproduce protection against Teladorsagia circumcincta in sheep with a purified stage-specific 31 kDa antigen complex. Vaccine 13, 1482–1485.CrossRefGoogle Scholar
O'Donnell, I. J., Dineen, J. K., Wagland, B. M., Letho, S., Werkmeister, J. A. and Ward, C. W. ( 1989). A novel host protective antigen from Trichostrongylus colubriformis. International Journal for Parasitology 45, 101–108.CrossRefGoogle Scholar
Piacenza, L., Acosta, D., Basmadjan, I., Dalton, J. P. and Carmona, C. ( 1999). Vaccination with cathepsin L proteases and with leucine aminopeptidase induces high levels of protection against fascioliasis in sheep. Infection and Immunity 67, 1954–1961.Google Scholar
Pirneskoski, A., Klappa, P., Lobell, M., Williamson, R. A., Byrne, L., Alanen, H. I., Salo, K. E., Kivirikko, K. I., Freedman, R. B. and Ruddock, L. W. ( 2004). Molecular characterization of the principal substrate binding site of the ubiquitous folding catalyst protein disulfide isomerase. Journal of Biological Chemistry 279, 10374–10381.CrossRefGoogle Scholar
Rabinovich, G. A., Baum, L. G., Tinari, N., Paganelli, R., Natoli, C., Liu, F. T. and Iacobelli, S. ( 2002). Galectins and their ligands: amplifiers, silencers or tuners of the inflammatory response? Trends in Immunology 23, 313–320.Google Scholar
Rubartelli, A., Bajetto, A., Allavena, G., Wollman, E. and Sitia, R. ( 1992). Secretion of thioredoxin by normal and neoplastic cells through a leaderless secretory pathway. Journal of Biological Chemistry 267, 24161–24164.Google Scholar
Rubinstein, N., Illaregui, J. M., Toscano, M. A. and Rabinovich, G. A. ( 2004). The role of galectins in the initiation, amplification and resolution of the inflammatory response. Tissue Antigens 64, 1–12.CrossRefGoogle Scholar
Schallig, H. D. and Van Leeuwen, M. A. ( 1997). Protective immunity to the blood-feeding nematode Haemonchus contortus induced by vaccination with parasite low molecular weight antigens. Parasitology 114, 293–299.CrossRefGoogle Scholar
Skuce, P. J., Stewart, E. M., Smith, W. D. and Knox, D. P. ( 1999). Cloning and characterisation of glutamate dehydrogenase. Parasitology 118, 297–304.CrossRefGoogle Scholar
Scott, I. and McKellar, Q. A. ( 1998). The effects of excretions/secretions of Ostertagia circumcincta on ovine abomasal tissues in vitro. International Journal for Parasitology 28, 451–460.CrossRefGoogle Scholar
Tsuji, N., Suzuki, K., Kasuga-Aoki, H., Isobe, T., Arakawa, T. and Matsumoto, Y. ( 2003). Mice intranasally immunized with a recombinant 16-kilodalton antigen from roundworm Ascaris parasites are protected against larval migration of Ascaris suum. Infection and Immunity 71, 5314–5323.CrossRefGoogle Scholar
Urquhart, G. M., Armour, J., Duncan, J. L., Dunn, A. M. and Jennings, F. W. ( 1987). Veterinary Parasitology. Longman Scientific and Technical, Essex, U.K.
Van Eden, W., Hauet-Broere, F., Berlo, S., Paul, L., Van Der Zee, R., De Kleer, I., Prakken, B. and Taams, L. ( 2005). Stress proteins as inducers and targets of regulatory T cells in arthritis. International Reviews of Immunology 24, 181–197.CrossRefGoogle Scholar
Vercauteren, I., Geldhof, P., Peelaers, I., Claerebout, E., Berx, G. and Vercruysse, J. ( 2003). Identification of excretory-secretory products of larval and adult Ostertagia ostertagi by immunoscreening of cDNA libraries. Molecular and Biochemical Parasitology 126, 201–208.CrossRefGoogle Scholar
Vercauteren, I., Geldhof, P., Vercruysse, J., Peelaers, I., Van Den Broeck, W., Gevaert, K. and Claerebout, E. ( 2004). Vaccination with an Ostertagia ostertagi polyprotein allergen protects calves against homologous challenge infection. Infection and Immunity 72, 2995–3001.CrossRefGoogle Scholar
Winter, M. and Page, A. P. ( 2000). Prolyl 4-hydroxylase is an essential procollagen-modifying enzyme required for exoskeleton formation and the maintenance of body shape in the nematode Caenorhabditis elegans. Molecular and Cell Biology 20, 4084–4093.CrossRefGoogle Scholar
Wu, Y., Egerton, G., Ball, A., Tanguay, R. M. and Bianco, A. E. ( 2000). Characterization of the heat-shock protein 60 chaperonin from Onchocerca volvulus. Molecular and Biochemical Parasitology 107, 155–168.CrossRefGoogle Scholar
Yatsuda, A. P., Krijgsveld, J., Cornelissen, A. W., Heck, A. J. and De Vries, E. ( 2003). Comprehensive analysis of the secreted proteins of the parasite Haemonchus contortus reveals extensive sequence variation and differential immune recognition. Journal of Biological Chemistry 278, 16941–16951.CrossRefGoogle Scholar
Young, C., McKeand, J. and Knox, D. P. ( 1995). Proteinases released in vitro by the parasitic stages of Teladorsagia circumcincta, an ovine abomasal nematode. Parasitology 110, 465–471.CrossRefGoogle Scholar