A deep exploration of the transcriptome and "excretory/secretory" proteome of adult Fascioloides magna

Molecular and Cellular Proteomics

Volumn 11, Issue 11, 2012, Pages 1340-1353

  Cantacessi, Cinzia ^a,b   Mulvenna, Jason ^c   Young, Neil D ^a   Kasny, Martin ^d   Horak, Petr ^d   Aziz, Ammar ^b   Hofmann, Andreas ^e   Loukas, Alex ^b   Gasser, Robin B ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b JAMES COOK UNIVERSITY   (Australia)

^c QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^d CHARLES UNIVERSITY   (Czech Republic)

^e GRIFFITH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

40S RIBOSOMAL PROTEIN; 60S RIBOSOMAL PROTEIN; CALMODULIN; CATHEPSIN B; CATHEPSIN L; CHAPERONIN 60; CYTOCHROME C OXIDASE; INITIATION FACTOR 4B; NADH UBIQUINONE OXIDOREDUCTASE CHAIN 5; NIEMANN PICK C1 PROTEIN; PEPTIDES AND PROTEINS; PROTEOME; RETINAL SPECIFIC ATP BINDING CASSETTE TRANSPORTER; SPECTRIN ALPHA CHAIN; TRANSCRIPTOME; TUBULIN ALPHA 3 CHAIN; UNCLASSIFIED DRUG;

ARTICLE; BIOINFORMATICS; FASCIOLOIDES MAGNA; FASCIOLOIDIASIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OFFGEL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ELECTROPHORESIS; PROTEIN MOTIF; PROTEOMICS; SEQUENCE HOMOLOGY; TREMATODE;

AMINO ACID SEQUENCE; ANIMALS; CATHEPSIN L; DEER; FASCIOLIDAE; GENE EXPRESSION PROFILING; HELMINTH PROTEINS; HUMANS; ISOENZYMES; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; PROTEOME; PROTEOMICS; RNA, MESSENGER; SEQUENCE ALIGNMENT; TRANSCRIPTOME;

FASCIOLA HEPATICA; FASCIOLIDAE; FASCIOLOIDES MAGNA;

EID: 84869230563     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.019844     Document Type: Article

References (89)

1. Boray, J. C. (1997) Chemotherapy of infections with Fasciolidae. In Immunology,Pathobiology and Control of Fasciolosis (Boray, J. C., ed.), pp. 83-97, MSD AGVET, Rahway, NJ
2. Kaplan, R. M. (2001) Fasciola hepatica: a review of the economic impact in cattle and considerations for control. Vet. Ther. 2, 40-50
3. Young, N. D., Hall, R. S., Jex, A. R., Cantacessi, C., and Gasser, R. B. (2010) Elucidating the transcriptome of Fasciola hepatica - a key to fundamental and biotechnological discoveries for a neglected parasite. Biotechnol.Adv. 28, 222-231
4. Pybus, M. J. (2001). Liver flukes. In Parasitic Diseases in Wild Mammals (Samuel, W. M., Pybus, M. J., and Kocan, A. A., eds.), pp. 121-149, Iowa State Press, Iowa City, IA
5. Coil, W. H. (1977) The penetration of Fascioloides magna miracidia into the snail host Fossaria bulimoides. A scanning electron microscope study. Zeitschrift für Parasitenkunde 52, 53-59
6. Fairweather, I. (2005) Triclabendazole: new skills to unravel an old(ish) enigma. J. Helminthol. 79, 227-234
7. Maes, L., Vanparijs, O., Lauwers, H., and Deckers, W. (1990) Comparative efficacy of closantel and triclabendazole against Fasciola hepatica in experimentally infected sheep. Vet. Rec. 127, 450-452 (Pubitemid 20371374)
8. Keiser, J., and Utzinger, J. (2004) Chemotherapy for major food-borne trematodes: a review. Expert Opin. Pharmacother. 5, 1711-1726 (Pubitemid 39117714)
9. Flynn, R. J., Mulcahy, G., and Elsheikha, H. M. (2010) Coordinating innate and adaptive immunity in Fasciola hepatica infection: implications for control. Vet. Parasitol. 169, 235-240
10. Overend, D. J., and Bowen, F. L. (1995) Resistance of Fasciola hepatica to triclabendazole. Aust. Vet. J. 72, 275-276
11. Coles, G. C., Rhodes, A. C., and Stafford, K. A. (2000) Activity of closantel against adult triclabendazole-resistant Fasciola hepatica. Vet. Rec. 146, 504 (Pubitemid 30232514)
12. Moll, L., Gaasenbeek, C. P. H., Vellema, P., and Borgsteede, F. H. M. (2000) Resistance of Fasciola hepatica against triclabendazole in cattle and sheep in the Netherlands. Vet. Parasitol. 91, 153-158 (Pubitemid 30411964)
13. Thomas, I., Coles, G. C., and Duffus, K. (2000) Triclabendazole-resistant Fasciola hepatica in southwest Wales. Vet. Rec. 146, 200 (Pubitemid 30102785)
14. Fairweather, I. (2009) Triclabendazole progress report, 2005-2009: an advancement of learning? J. Helminthol. 83, 139-150
15. Gaasenbeek, C. P. H., Moll, L., Cornelissen, J., Vellema, P., and Borgsteede, F. H. M. (2001) An experimental study on triclabendazole resistance of Fasciola hepatica in sheep. Vet. Parasitol. 95, 37-43 (Pubitemid 32332747)
16. Spithill, T. W., and Dalton, J. P. (1998) Progress in development of liver fluke vaccines. Parasitol. Today 14, 224-228 (Pubitemid 28240078)
17. Piacenza, L., Acosta, D., Basmadjian, I., Dalton, J. P., and Carmona, C. (1999) Vaccination with cathepsin L proteinases and with leucine aminopeptidase induces high levels of protection against fascioliasis in sheep. Infect. Immun. 67, 1954-1961 (Pubitemid 29144421)
18. Dalton, J. P., and Mulcahy, G. (2001) Parasite vaccines - a reality? Vet.Parasitol. 98, 149-167 (Pubitemid 32539274)
19. Dalton, J. P., Brindley, P. J., Knox, D. P., Brady, C. P., Hotez, P. J., Donnelly, S., O'Neill, S. M., Mulcahy, G., and Loukas, A. (2003) Helminth vaccines: from mining genomic information for vaccine targets to systems used for protein expression. Int. J. Parasitol. 33, 621-640 (Pubitemid 36638541)
20. Dalton, J. P., O'Neill, S., Stack, C., Collins, P., Walshe, A., Sekiya, M., Doyle, S., Mulcahy, G., Hoyle, D., Khaznadji, E., Moire, N., Brennan, G., Mousley, A., Kreshchenko, N., Maule, A. G., and Donnelly, S. M. (2003) Fasciola hepatica cathepsin L-like proteases: biology, function, and potential in the development of first generation liver fluke vaccines. Int. J.Parasitol. 33, 1173-1181 (Pubitemid 37107373)
21. McManus, D. P., and Dalton, J. P. (2006) Vaccines against the zoonotic trematodes Schistosoma japonicum, Fasciola hepatica and Fasciola gigantica.Parasitology 133, S43-S61 (Pubitemid 46208030)
22. Acosta, D., Cancela, M., Piacenza, L., Roche, L., Carmona, C., and Tort, J. F. (2008) Fasciola hepatica leucine aminopeptidase, a promising candidate for vaccination against ruminant fasciolosis. Mol. Biochem. Parasitol.158, 52-64 (Pubitemid 351172463)
23. Jayaraj, R., Piedrafita, D., Dynon, K., Grams, R., Spithill, T. W., and Smooker, P. M. (2009) Vaccination against fasciolosis by a multivalent vaccine of stage-specific antigens. Vet. Parasitol. 160, 230-236
24. Robinson, M. W., Menon, R., Donnelly, S. M., Dalton, J. P., and Ranganathan, S. (2009) An integrated transcriptomics and proteomics analysis of the secretome of the helminth pathogen Fasciola hepatica: proteins associated with invasion and infection of the mammalian host. Mol. Cell.Proteomics 8, 1891-1907
25. Young, N. D., Jex, A. R., Cantacessi, C., Hall, R. S., Campbell, B. E., Spithill, T. W., Tangkawattana, S., Tangkawattana, P., Laha, T., and Gasser, R. B. (2011) A portrait of the transcriptome of the neglected trematode, Fasciolagigantica - biological and biotechnological implications. PLoSNegl. Trop. Dis. 5, e1004
26. Kasny, M., Mikes, L., Hampl, V., Dvorak, J., Caffrey, C. R., Dalton, J. P., and Horak, P. (2009) Chapter 4. Peptidases of trematodes. Adv. Parasitol. 69, 205-297
27. DeMarco, R., and Verjovski-Almeida, S. (2009) Schistosomes - proteomics studies for potential novel vaccines and drug targets. Drug Discov. Today14, 472-478
28. Chuan, J., Feng, Z., Brindley, P. J., McManus, D. P., Han, Z., Jianxin, P., and Hu, W. (2010) Our wormy world: genomics, proteomics and transcriptomics in East and southeast Asia. Adv. Parasitol. 73, 327-371
29. Cantacessi, C., Campbell, B. E., and Gasser, R. B. (2012) Key strongylid nematodes of animals - impact of next-generation transcriptomics on systems biology and biotechnology. Biotechnol. Adv. 30, 469-488
30. Verjovski-Almeida, S., and DeMarco, R. (2008) Current developments in Schistosoma proteomics. Acta Trop. 108, 183-185
31. Mulvenna, J., Hamilton, B., Nagaraj, S. H., Smyth, D., Loukas, A., and Gorman, J. J. (2009) Proteomics analysis of the excretory/secretory component of the blood-feeding stage of the hookworm, Ancylostomacaninum. Mol. Cell. Proteomics 8, 109-121
32. Young, N. D., Campbell, B. E., Hall, R. S., Jex, A. R., Cantacessi, C., Laha, T., Sohn, W. M., Sripa, B., Loukas, A., Brindley, P. J., and Gasser, R. B. (2010) Unlocking the transcriptomes of two carcinogenic parasites, Clonorchis sinensis and Opisthorchis viverrini. PLoS Negl. Trop. Dis. 4, e719
33. Bentley, D. R., Balasubramanian, S., Swerdlow, H. P., George, D., Gietzen, K. J., Goddard, C. P., Golda, G. S., Granieri, P. A., Green, D. E., Gustafson, D. L., Hansen, N. F., Harnish, K., Haudenschild, C. D., Heyer, N. I., Hims, M. M., Ho, J. T., Horgan, A. M., Hoschler, K., Hurwitz, S., Ivanov, D. V., Johnson, M. Q., James, T., Huw Jones, T. A., Kang, G. D., Kerelska, T. H., Kersey, A. D., Khrebtukova, I., Kindwall, A. P., Kingsbury, Z., Kokko-Gonzales, P. I., Kumar, A., Laurent, M. A., Lawley, C. T., Lee, S. E., Lee, X., Liao, A. K., Loch, J. A., Lok, M., Luo, S., Mammen, R. M., Martin, J. W., McCauley, P. G., McNitt, P., Mehta, P., Moon, K. W., Mullens, J.W., Newington, T., Ning, Z., Ling Ng, B., Novo, S. M., O'Neill, M. J., Osborne, M. A., Osnowski, A., Ostadan, O., Paraschos, L. L., Pickering, L., Pike, A. C., Pike, A. C., Chris Pinkard, D., Pliskin, D. P., Podhasky, J., Quijano, V. J., Raczy, C., Rae, V. H., Rawlings, S. R., Chiva Rodriguez, A., Roe, P. M., Rogers, J., Rogert Bacigalupo, M. C., Romanov, N., Romieu, A., Roth, R. K., Rourke, N. J., Ruediger, S. T., Rusman, E., Sanches-Kuiper, R. M., Schenker, M. R., Seoane, J. M., Shaw, R. J., Shiver, M. K., Short, S. W., Sizto, N. L., Sluis, J. P., Smith, M. A., Ernest Sohna Sohna, J., Spence, E. J., Stevens, K., Sutton, N., Szajkowski, L., Tregidgo, C. L., Turcatti, G., Vandevondele, S., Verhovsky, Y., Virk, S. M., Wakelin, S., Walcott, G. C., Wang, J., Worsley, G. J., Yan, J., Yau, L., Zuerlein, M., Rogers, J., Mullikin, J. C., Hurles, M. E., McCooke, N. J., West, J. S., Oaks, F. L., Lundberg, P. L., Klenerman, D., Durbin, R., and Smith, A. J. (2008) Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456, 53-59
34. Schulz, M. H., Zerbino, D. R., Vingron, M., and Birney, E. (2012) Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics 28, 1086-1092
35. Li, R., Yu, C., Li, Y., Lam, T. W., Yiu, S. M., Kristiansen, K., and Wang, J. (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics25, 1966-1967
36. Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L., and Wold, B. (2008) Mapping and quantifying mammalian transcriptomes by RNA-seq. Nat.Methods 5, 621-628 (Pubitemid 351911867)
37. Cantacessi, C., Jex, A. R., Hall, R. S., Young, N. D., Campbell, B. E., Joachim, A., Nolan, M. J., Abubucker, S., Sternberg, P. W., Ranganathan, S., Mitreva, M., and Gasser, R. B. (2010) A practical, bioinformatic workflow system for large data sets generated by next-generation sequencing. Nucleic Acids Res. 38, e171
38. Young, N. D., Jex, A. R., Li, B., Liu, S., Yang, L., Xiong, Z., Li, Y., Cantacessi, C., Hall, R. S., Xu, X., Chen, F., Wu, X., Zerlotini, A., Oliveira, G., Hofmann, A., Zhang, G., Fang, X., Kang, Y., Campbell, B. E., Loukas, A., Ranganathan, S., Rollinson, D., Rinaldi, G., Brindley, P. J., Yang, H., Wang, J., Wang, J., and Gasser, R. B. (2012) Whole-genome sequence of Schistosoma haematobium. Nat. Genet. 44, 221-225
39. The Schistosoma japonicum Genome Sequencing and Functional Analysis Consortium (2009) The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 460, 345-351
40. Berriman, M., Haas, B. J., LoVerde, P. T., Wilson, R. A., Dillon, G. P., Cerqueira, G. C., Mashiyama, S. T., Al-Lazikani, B., Andrade, L. F., Ashton, P. D., Aslett, M. A., Bartholomeu, D. C., Blandin, G., Caffrey, C. R., Coghlan, A., Coulson, R., Day, T. A., Delcher, A., DeMarco, R., Djikeng, A., Eyre, T., Gamble, J. A., Ghedin, E., Gu, Y., Hertz-Fowler, C., Hirai, H., Hirai, Y., Houston, R., Ivens, A., Johnston, D. A., Lacerda, D., Macedo, C. D., McVeigh, P., Ning, Z., Oliveira, G., Overington, J. P., Parkhill, J., Pertea, M., Pierce, R. J., Protasio, A. V., Quail, M. A., Rajandream, M. A., Rogers, J., Sajid, M., Salzberg, S. L., Stanke, M., Tivey, A. R., White, O., Williams, D. L., Wortman, J., Wu, W., Zamanian, M., Zerlotini, A., Fraser-Liggett, C. M., Barrell, B. G., and El-Sayed, N. M. (2009) The genome of the blood fluke Schistosoma mansoni. Nature 460, 352-358
41. 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 Res. 37, D211-D215
42. 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. Nat.Genet. 25, 25-29 (Pubitemid 30257031)
43. Ye, J., Fang, L., Zheng, H., Zhang, Y., Chen, J., Zhang, Z., Wang, J., Li, S., Li, R., Bolund, L., and Wang, J. (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res. 34, W293-W297 (Pubitemid 44529781)
44. Xie, C., Mao, X., Huang, J., Ding, Y., Wu, J., Dong, S., Kong, L., Gao, G., Li, C. Y., and Wei, L. (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res. 39, W316-W322
45. Bendtsen, J. D., Nielsen, H., von Heijne, G., and Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340, 783-795 (Pubitemid 38829638)
46. Sonnhammer, E. L. L., von Heijne, G., and Krogh, A. (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. In Proceedings of the Sixth International Conference on IntelligentSystems for Molecular Biology, pp. 175-182, AAAI, Menlo Park, CA
47. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E. L. (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567-580 (Pubitemid 33032862)
48. Moller, S., Croning, M. D. R., and Apweiler, R. (2001) Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 17, 646-653 (Pubitemid 32707587)
49. Chen, Y., Zhang, Y., Yin, Y., Gao, G., Li, S., Jiang, Y., Gu, X., and Luo, J. (2005) SPD - a web based secreted protein database. Nucleic AcidsRes. 33, D169-D173 (Pubitemid 40207853)
50. Choo, K. H., Tan, T. W., and Ranganathan, S. (2005) SPdb - a signal peptide database. BMC Bioinformatics 6, 249
51. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-907
52. Searle, B. C. (2010) Scaffold: a bioinformatics tool for validating MS/MS-based proteomics studies. Proteomics 10, 1265-1269
53. Keller, A., Nesvizhskii, A. I., Kolker, E., and Aebersold, R. (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74, 5383-5392 (Pubitemid 35215372)
54. Nesvizhsii, A. I., Keller, A., Kolker, E., and Aebersold, R. (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal.Chem. 75, 4646-4658 (Pubitemid 37082259)
55. Emanuelsson, O., Brunak, S., von Heijne, G., and Nielsen, H. (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat.Protoc. 2, 953-971 (Pubitemid 46745592)
56. Blom, N., Sicheritz-Pontén, T., Gupta, R., Gammeltoft, S., and Brunak, S. (2004) Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4, 1633-1649 (Pubitemid 38738322)
57. Cho, P. Y., Lee, M. J., Kim, T. I., Kang, S. Y., and Hong, S. J. (2006) Expressed sequence tag analysis of adult Clonorchis sinensis, the Chinese liver fluke. Parasitol. Res. 99, 602-608 (Pubitemid 44337951)
58. Cho, P. Y., Kim, T. I., Whang, S. M., and Hong, S. J. (2008) Gene expression profile of Clonorchis sinensis metacercariae. Parasitol. Res. 102, 277-282 (Pubitemid 350215798)
59. Kang, J. M., Bahk, Y. Y., Cho, P. Y., Hong, S. J., Kim, T. S., Sohn, W. M., and Na, B. K. (2010) A family of cathepsin F cysteine proteases of Clonorchis sinensis is the major secreted proteins that are expressed in the intestine of the parasite. Mol. Biochem. Parasitol. 170, 7-16
60. Yoo, W. G., Kim, D. W., Ju, J. W., Cho, P. Y., Kim, T. I., Cho, S. H., Choi, S. H., Park, H. S., Kim, T. S., and Hong, S. J. (2011) Developmental transcriptomic features of the carcinogenic liver fluke, Clonorchis sinensis.PLoS Negl. Trop. Dis. 5, e1208
61. Kim, T. S., de Guzman, J. V., Kong, H. H., and Chung, D. I. (2006) Comparison of gene representation between diploid and triploid Paragonimuswestermani by expressed sequence tags analyses. J. Parasitol. 92, 803-816
62. Horton, P., Park, K., Obayashi, T., Fujita, N., Harada, H., Adams-Collier, C. J., and Nakai, K. (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res. 35, W585-W587
63. Jefferies, J. R., Campbell, A. M., vanRossum, A. J., Barrett, J., and Brophy, P. M. (2001) Proteomic analysis of Fasciola hepatica excretory-secretory products. Proteomics 1, 1128-1132 (Pubitemid 33696478)
64. Morphew, R. M., Wright, H. A., LaCourse, E. J., Porter, J., Barrett, J., Woods, D. J., and Brophy, P. M. (2011) Towards delineating functions within the Fasciola secreted cathepsin I protease family by integrating in vivo based sub-proteomics and phylogenetics. PLoS Negl. Trop. Dis. 5, e937
65. Robinson, M. W., Tort, J. F., Lowther, J., Donnelly, S. M., Wong, E., Xu, W., Stack, C. M., Padula, M., Herbert, B., and Dalton, J. P. (2008) Proteomics and phylogenetic analysis of the cathepsin L protease family of the helminth pathogen Fasciola hepatica: expansion of a repertoire of virulence-associated factors. Mol. Cell. Proteomics 7, 1111-1123 (Pubitemid 351943958)
66. Wilson, R. A., Wright, J. M., de Castro-Borges, W., Parker-Manuel, S. J., Dowle, A. A., Ashton, P. D., Young, N. D., Gasser, R. B., and Spithill, T. W. (2011) Exploring the Fasciola hepatica tegument proteome. Int. J.Parasitol. 41, 1347-1359
67. Zheng, M., Hu, K., Liu, W., Hu, X., Hu, F., Huang, L., Wang, P., Hu, Y., Huang, Y., Li, W., Liang, C., Yin, X., He, Q., and Yu, X. (2011) Proteomic analysis of excretory secretory products from Clonorchis sinensis adult worms: molecular characterization and serological reactivity of excretory-secretory antigen-fructose-1,6-bisphosphatase. Parasitol. Res. 1, 1-8
68. Mulvenna, J., Sripa, B., Brindley, P. J., Gorman, J., Jones, M. K., Colgrave, M. L., Jones, A., Nawaratna, S., Laha, T., Suttiprapa, S., Smout, M. J., and Loukas, A. (2010) The secreted and surface proteomes of the adult stage of the carcinogenic human liver fluke Opisthorchis viverrini. Proteomics10, 1063-1078
69. Robinson, M. W., Corvo, I., Jones, P. M., George, A. M., Padula, M. P., To, J., Cancela, M., Rinaldi, G., Tort, J. F., Roche, L., and Dalton, J. P. (2011) Collagenolytic activities of the major secreted cathepsin L peptidases involved in the virulence of the helminth pathogen, Fasciola hepatica.PLoS Negl. Trop. Dis. 4, e1012
70. Nickel, W. (2003) The mystery of nonclassical protein secretion. A current view on cargo proteins and potential export routes. Eur. J. Biochem. 270, 2109-2119
71. Robinson, M. W., Colhoun, L. M., Fairweather, I., Brennan, G. P., and Waite, J. H. (2001) Development of the vitellaria of the liver fluke, Fasciolahepatica, in the rat host. Parasitology 123, 509-518 (Pubitemid 33043612)
72. Chen, J. M., Dando, P. M., Stevens, R. A., Fortunato, M., and Barrett, A. J. (1998) Cloning and expression of mouse legumain, a lysosomal endopeptidase. Biochem. J. 335, 111-117 (Pubitemid 28477056)
73. Turk, D., and Guncar, G. (2003) Lysosomal cysteine proteases (cathepsins): promising drug targets. Acta Crystallogr. D Biol. Crystallogr. 59, 203-213 (Pubitemid 36224841)
74. Robinson, M. W., Dalton, J. P., and Donnelly, S. (2008) Helminth pathogen cathepsin proteases: it's a family affair. Trends Biochem. 33, 601-608
75. Irving, J. A., Spithill, T. W., Pike, R. N., Whisstock, J. C., and Smooker, P. M. (2003) The evolution of enzyme specificity in Fasciola spp. J. Mol. Evol.57, 1-15 (Pubitemid 36920445)
76. Tort, J., Brindley, P. J., Knox, D., Wolfe, K. H., and Dalton, J. P. (1999) Proteinases and associated genes of parasitic helminths. Adv. Parasitol.43, 161-266 (Pubitemid 29184935)
77. Dalton, J. P., Brindley, P. J., Donnelly, S., and Robinson, M. W. (2009) The enigmatic asparaginyl endopeptidase of helminth parasites. TrendsParasitol. 25, 59-61
78. Hall, S. L., Braschi, S., Truscott, M., Mathieson, W., Cesari, I. M., and Wilson, R. A. (2011) Insights into blood feeding by schistosomes from a proteomic analysis of worm vomitus. Mol. Biochem. Parasitol. 179, 18-29
79. Liu, F., Cui, S. J., Hu, W., Feng, Z., Wang, Z. Q., and Han, Z. G. (2008) Excretory/secretory proteome of the adult developmental stage of human blood fluke, Schistosoma japonicum. Mol. Cell. Proteomics 8, 1236-1251
80. Dalton, J. P., Skelly, P., and Halton, D. W. (2004) Role of the tegument and gut in nutrient uptake by parasitic platyhelminths. Can. J. Zool. 24, 211-232 (Pubitemid 38908436)
81. MacKenzie, A., Wilson, H. L., Kiss-Toth, E., Dower, S. K., North, R. A., and Surprenant, A. (2001) Rapid secretion of interleukin-1β by microvescicle shedding. Immunity 15, 825-835 (Pubitemid 34008509)
82. McGonigle, L., Mousley, A., Marks, N. J., Brennan, G. P., Dalton, J. P., Spithill, T. W., Day, T. A., and Maule, A. G. (2008) The silencing of cysteine proteases in Fasciola hepatica newly excysted juveniles using RNA interference reduces gut penetration. Int. J. Parasitol. 38, 149-155 (Pubitemid 350266652)
83. Salazar-Calderón, M., Martin-Alonso, J. M., Ruiz de Eguino, A. D., and Parra, F. (2001) Heterologous expression and functional characterization of thioredoxin from Fasciola hepatica. Parasitol. Res. 87, 390-395 (Pubitemid 32391441)
84. Salazar-Calderón, M., Martin Alonso, J. M., Castro, A. M., and Parra, F. (2003) Cloning, heterologous expression in Escherichia coli and characterization of a protein disulfide isomerase from Fasciola hepatica. Mol.Biochem. Parasitol. 126, 15-23 (Pubitemid 36120601)
85. Sekiya, M., Mulcahy, G., Irwin, J. A., Stack, C. M., Donnelly, S. M., Xu, W., Collins, P., and Dalton, J. P. (2006) Biochemical characterisation of the recombinant peroxiredoxin (FhePrx) of the liver fluke, Fasciola hepatica.FEBS Lett. 580, 5016-5022 (Pubitemid 44404083)
86. Cervi, L., Rossi, G., and Masih, D. T. (1999) Potential role for excretory-secretory forms of glutathione-S-transferase (GST) in Fasciola hepatica.Parasitology 119, 627-633
87. Donnelly, S., O'Neill, S. M., Sekiya, M., Mulcahy, G., and Dalton, J. P. (2005) Thioredoxin peroxidase secreted by Fasciola hepatica induces the alternative activation of macrophages. Infect. Immun. 73, 166-173 (Pubitemid 40041106)
88. Donnelly, S., Stack, C. M., O'Neill, S. M., Sayed, A. A., Williams, D. L., and Dalton, J. P. (2008) Helminth 2-Cys peroxiredoxin drives Th2 responses through a mechanism involving alternatively activated macrophages. FASEB J. 22, 4022-4032
89. Wang, X., Chen, W., Huang, Y., Sun, J., Men, J., Liu, H., Luo, F., Guo, L., Lv, Z., Deng, C., Zhou, C., Fan, Y., Li, X., Huang, L., Hu, Y., Liang, C., Hu, X., Xum, J., and Yum, X. (2011) The draft genome of the carcinogenic human liver fluke Clonorchis sinensis. Genome Biol. 12, R107