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

Experimental Parasitology

Volumn 125, Issue 4, 2010, Pages 329-337

  Nisbet, A J ^a   Smith, S K ^a   Armstrong, S ^b   Meikle, L I ^a   Wildblood, L A ^a   Beynon, R J ^b   Matthews, J B ^a,c  

^a MOREDUN RESEARCH INSTITUTE   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Activation associated secreted proteins; IgA response; Teladorsagia circumcincta; Vaccine development

Indexed keywords

ACTIVATION ASSOCIATED SECRETED PROTEIN; COMPLEMENTARY DNA; IMMUNOGLOBULIN A; PARASITE ANTIGEN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; DNA SEQUENCE; ESCHERICHIA COLI; GENETIC TRANSCRIPTION; IMMUNE RESPONSE; IMMUNOBLOTTING; IMMUNOGENICITY; LARVAL STAGE; MUCUS; NEMATODE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTERTAGIA OSTERTAGI; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN PURIFICATION; PROTEIN SECRETION; PROTEOMICS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; SHEEP; TELADORSAGIA CIRCUMCINCTA;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, HELMINTH; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GASTRIC MUCOSA; HELMINTH PROTEINS; IMMUNOBLOTTING; IMMUNOGLOBULIN A, SECRETORY; LARVA; MASS SPECTROMETRY; PHYLOGENY; PROTEOMICS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SHEEP; SHEEP DISEASES; TRICHOSTRONGYLOIDEA; TRICHOSTRONGYLOIDIASIS;

ESCHERICHIA COLI; OSTERTAGIA OSTERTAGI; OVIS ARIES; TELADORSAGIA CIRCUMCINCTA;

EID: 77953017036     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2010.02.014     Document Type: Article

References (51)

1. Asojo O.A., Goud G., Dhar K., Loukas A., Zhan B., Deumic V., et al. X-ray structure of Na-ASP-2, a pathogenesis-related-1 protein from the nematode parasite, Necator americanus, and a vaccine antigen for human hookworm infection. Journal of Molecular Biology 2005, 346:801-814.
2. Balic A., Bowles V.M., Liu Y.S., Meeusen E.N. Local immune responses in sensitized sheep following challenge infection with Teladorsagia circumcincta. Parasite Immunology 2003, 25:371-381.
3. Bartley D.J., Jackson F., Jackson E., Sargison N. Characterisation of two triple resistant field isolates of Teladorsagia from Scottish lowland sheep farms. Veterinary Parasitology 2004, 123:189-199.
4. Bethony J., Loukas A., Smout M., Brooker S., Mendez S., Plieskatt J., et al. Antibodies against a secreted protein from hookworm larvae reduce the intensity of hookworm infection in humans and vaccinated laboratory animals. FASEB Journal 2005, 19:1743-1745.
5. Bethony J.M., Simon G., Diemert D.J., Parenti D., Desrosiers A., Schuck S., et al. Randomized, placebo-controlled, double-blind trial of the Na-ASP-2 hookworm vaccine in unexposed adults. Vaccine 2008, 26:2408-2417.
6. Busso D., Goldweic N.M., Hayashi M., Kasahara M., Cuasnicú P.S. Evidence for the involvement of testicular protein CRISP2 in mouse sperm-egg fusion. Biology of Reproduction 2007, 76:701-708.
7. Cantacessi C., Campbell B.E., Visser A., Geldhof P., Nolan M.J., Nisbet A.J., et al. A portrait of the " SCP/TAPS" proteins of eukaryotes - developing a framework for fundamental research and biotechnological outcomes. Biotechnology Advances 2009, 27:376-388.
8. Chalmers I.W., McArdle A.J., Coulson R.M., Wagner M.A., Schmid R., Hirai H., Hoffmann K.F. Developmentally regulated expression, alternative splicing and distinct sub-groupings in members of the Schistosoma mansoni venom allergen-like (SmVAL) gene family. BMC Genomics 2008, 9:89.
9. Cottee P.A., Nisbet A.J., Abs EL-Osta Y.G., Webster T.L., Gasser R.B. Construction of gender-enriched cDNA archives for adult Oesophagostomum dentatum by suppressive-subtractive hybridization and a microarray analysis of expressed sequence tags. Parasitology 2006, 132:691-708.
10. Diemert D.J., Bethony J.M., Hotez P.J. Hookworm vaccines. Clinical Infectious Diseases 2008, 46:282-288.
11. Dyrløv Bendtsen J., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides: SignalP 3.0. Journal of Molecular Biology 2004, 340:783-795.
12. Geldhof P., Claerebout E., Knox D., Vercauteren I., Looszova A., Vercruysse J. Vaccination of calves against Ostertagia ostertagi with cysteine proteinase enriched protein fractions. Parasite Immunology 2002, 24:263-270.
13. Geldhof P., Vercauteren I., Gevaert K., Staes A., Knox D.P., Vandekerckhove J., et al. Activation-associated secreted proteins are the most abundant antigens in a host protective fraction from Ostertagia ostertagi. Molecular and Biochemical Parasitology 2003, 128:111-114.
14. Geldhof P., Vercauteren I., Vercruysse J., Knox D.P., Van Den Broeck W., Claerebout E. Validation of the protective Ostertagia ostertagi ES-thiol antigens with different adjuvantia. Parasite Immunology 2004, 26:37-43.
15. Geldhof P., Meyvis Y., Vercruysse J., Claerebout E. Vaccine testing of a recombinant activation-associated secreted protein (ASP1) from Ostertagia ostertagi. Parasite Immunology 2008, 30:57-60.
16. Gibson T.E., Everett G. Effect of different levels of intake of Ostertagia circumcincta larvae on the faecal egg counts and weight gain of lambs. Journal of Comparative Pathology 1976, 86:269-274.
17. Hawdon J.M., Jones B.F., Hoffman D.R., Hotez P.J. Cloning and characterization of Ancylostoma-secreted protein. A novel protein associated with the transition to parasitism by infective hookworm larvae. Journal of Biological Chemistry 1996, 271:6672-6678.
18. Hawdon J.M., Narasimhan S., Hotez P.J. Ancylostoma secreted protein 2: cloning and characterization of a second member of a family of nematode secreted proteins from Ancylostoma caninum. Molecular and Biochemical Parasitology 1999, 99:149-165.
19. Huang X., Madan A. CAP3: a DNA sequence assembly programme. Genome Research 1999, 9:868-877.
20. Jeanmougin F., Thompson J.D., Gouy M., Higgins D.G., Gibson T.J. Multiple sequence alignment with Clustal X. Trends in Biochemical Science 1998, 23:403-405.
21. Li B.W., Rush A.C., Crosby S.D., Warren W.C., Williams S.A., Mitreva M., et al. Profiling of gender-related gene transcripts in the filarial nematode Brugia malayi by cDNA oligonucleotide array analysis. Molecular and Biochemical Parasitology 2005, 143:49-57.
22. Lu G., Villalba M., Coscia M.R., Hoffman D.R., King T.P. Sequence analysis and antigenic cross-reactivity of a venom allergen, antigen 5, from hornets, wasps, and yellow jackets. Journal of Immunology 1993, 150:2823-2830.
23. Martínez-Valladares M., Godio-Fernández R., Vara-Del Río M.P., Martín J.F., Rojo-Vázquez F.A. Expression of the recombinant protein disulphide isomerase of Teladorsagia circumcincta. Parasite Immunology 2007, 29:47-56.
24. Meyvis Y., Geldhof P., Gevaert K., Timmerman E., Vercruysse J., Claerebout E. Vaccination against Ostertagia ostertagi with subfractions of the protective ES-thiol fraction. Veterinary Parasitology 2007, 149:239-245.
25. Meyvis Y., Callewaert N., Gevaert K., Timmerman E., Van Durme J., Schymkowitz J., et al. Hybrid N-glycans on the host protective activation-associated secreted proteins of Ostertagia ostertagi and their importance in immunogenicity. Molecular and Biochemical Parasitology 2008, 161:67-71.
26. Mulvenna J., Hamilton B., Nagaraj S., Smyth D., Loukas A., Gorman J. Proteomics analysis of the excretory/secretory component of the blood-feeding stage of the hookworm, Ancylostoma caninum. Molecular and Cellular Proteomics 2008, 8:109-121.
27. Nieuwhof G.J., Bishop S.C. Costs of the major endemic diseases of sheep in Great Britain and the potential benefits of reduction in disease impact. Animal Science 2005, 81:23-29.
28. Nisbet A.J., Gasser R.B. Profiling of gender-specific gene expression for Trichostrongylus vitrinus (Nematoda: Strongylida) by microarray analysis of expressed sequence tag libraries constructed by suppressive subtractive hybridization. International Journal for Parasitology 2004, 34:633-643.
29. Nisbet A.J., Redmond D.L., Matthews J.B., Watkins C., Yaga R., Jones J.T., et al. Stage-specific gene expression in Teladorsagia circumcincta (Nematoda: Strongylida) infective larvae and early parasitic stages. International Journal for Parasitology 2008, 38:829-838.
30. Nisbet A.J., Knox D.P., McNair C.M., Meikle L.I., Smith S.K., Wildblood L.A., et al. Immune recognition of the surface associated antigen, Tc-SAA-1, from infective larvae of Teladorsagia circumcincta. Parasite Immunology 2009, 31:32-40.
31. Page R.D.M. TreeView: an application to display phylogenetic trees on personal computers. Computer Applications in the Biological Sciences 1996, 12:357-358.
32. Parkinson J., Whitton C., Schmid R., Thomson M., Blaxter M. NEMBASE: a resource for parasitic nematode ESTs. Nucleic Acids Research 2004, 32:D427-D430.
33. Perkins D.N., Pappin D.J., Creasy D.M., Cottrell J.S. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20:3551-3567.
34. Redmond D.L., Smith S.K., Halliday A., Smith W.D., Jackson F., Knox D.P., et al. An immunogenic cathepsin F secreted by the parasitic stages of Teladorsagia circumcincta. International Journal for Parasitology 2006, 36:277-286.
35. Reinke V., Gil I.S., Ward S., Kazmer K. Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Development 2004, 131:311-323.
36. Schallig H.D., van Leeuwen M.A., Verstrepen B.E., Cornelissen A.W. Molecular characterization and expression of two putative protective excretory secretory proteins of Haemonchus contortus. Molecular and Biochemical Parasitology 1997, 88:203-213.
37. Schallig H.D., van Leeuwen M.A., Cornelissen A.W. Protective immunity induced by vaccination with two Haemonchus contortus excretory secretory proteins in sheep. Parasite Immunology 1997, 19:447-453.
38. Seaton D.S., Jackson F., Smith W.D., Angus K.W. Development of immunity to incoming radiolabelled larvae in lambs continuously infected with Ostertagia circumcincta. Research in Veterinary Science 1989, 46:241-246.
39. Simpson H.V. Pathophysiology of abomasal parasitism: is the host or parasite responsible?. Veterinary Journal 2000, 160:177-191.
40. Smith S.K., Nisbet A.J., Meikle L.I., Inglis N.F., Sales J., Beynon R.J., et al. Proteomic analysis of excretory/secretory products released by Teladorsagia circumcincta larvae early post-infection. Parasite Immunology 2009, 31:10-13.
41. Smith W.D., Jackson F., Jackson E., Williams J. Age immunity to Ostertagia circumcincta: comparison of the local immune responses of 4 1/2- and 10-month-old lambs. Journal of Comparative Pathology 1985, 95:235-245.
42. Smith W.D., Jackson F., Jackson E., Graham R., Williams J., Willadsen S.M., et al. Transfer of immunity to Ostertagia circumcincta and IgA memory between identical sheep by lymphocytes collected from gastric lymph. Research in Veterinary Science 1986, 41:300-306.
43. Stear M.J., Bairden K., Innocent G.T., Mitchell S., Strain S., Bishop S.C. The relationship between IgA activity against 4th-stage larvae and density-dependent effects on the number of 4th-stage larvae of Teladorsagia circumcincta in naturally infected sheep. Parasitology 2004, 129:363-369.
44. Tawe W., Pearlman E., Unnasch T.R., Lustigman S. Angiogenic activity of Onchocerca volvulus recombinant proteins similar to vespid venom antigen 5. Molecular and Biochemical Parasitology 2000, 109:91-99.
45. Vercauteren I., Geldhof P., Peelaers I., Claerebout E., Berx G., Vercruysse J. Identification of excretory-secretory products of larval and adult Ostertagia ostertagi by immunoscreening of cDNA libraries. Molecular and Biochemical Parasitology 2003, 126:201-208.
46. Vervelde L., Van Leeuwen M.A., Kruidenier M., Kooyman F.N., Huntley J.F., Van Die I., et al. Protection studies with recombinant excretory/secretory proteins of Haemonchus contortus. Parasite Immunology 2002, 24:189-201.
47. Visser A., Van Zeveren A.M., Meyvis Y., Peelaers I., Van den Broeck W., Gevaert K., et al. Gender-enriched transcription of activation associated secreted proteins in Ostertagia ostertagi. International Journal for Parasitology 2008, 38:455-465.
48. Wang J., Kim S.K. Global analysis of dauer gene expression in Caenorhabditis elegans. Development 2003, 130:1621-1634.
49. Wrigley J., McArthur M., McKenna P.B., Mariadass B. Resistance to a triple combination of broad-spectrum anthelmintics in naturally-acquired Ostertagia circumcincta infections in sheep. New Zealand Veterinary Journal 2006, 54:47-49.
50. Yatsuda A.P., Eysker M., Vieira-Bressan M.C., De Vries E. A family of activation associated secreted protein (ASP) homologues of Cooperia punctata. Research in Veterinary Science 2002, 73:297-306.
51. Zhan B., Liu Y., Badamchian M., Williamson A., Feng J., Loukas A., et al. Molecular characterisation of the Ancylostoma-secreted protein family from the adult stage of Ancylostoma caninum. International Journal for Parasitology 2003, 33:897-899.