Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-27T17:43:05.741Z Has data issue: false hasContentIssue false

Vaccines against the zoonotic trematodes Schistosoma japonicum, Fasciola hepatica and Fasciola gigantica

Published online by Cambridge University Press:  02 February 2007

D. P. McMANUS
Affiliation:
Molecular Parasitology Laboratory, Queensland Institute of Medical Research, 300 Herston Road, Brisbane, Q 4006, Australia
J. P. DALTON
Affiliation:
Institute for the Biotechnology of Infectious Diseases University of Technology Sydney (UTS), Level 6, Building 4, Harris Street & Thomas Street, Ultimo, Sydney, NSW 2007, Australia

Abstract

Schistosoma japonicum, Fasciola hepatica and F. gigantica are digenetic trematodes and, therefore, possess similar life cycles. While schistosomiasis japonica has for a long time been recognised as a major disease of both humans and animals, infection with fasciolids has only been considered of relevance to animals. However, a number of recent reports indicate that fasciolosis is becoming a serious public health problem, especially in South America, Egypt and Iran (sporadic cases are also on the increase throughout Europe). Vaccines targeted at animals could play an important role in controlling these three diseases in animals and, by blocking transmission of infection, have a concurrent beneficial effect on disease in humans. Approaches towards identifying and producing vaccines against these parasites are similar and are discussed in this reveiw.

Type
Research Article
Copyright
© 2006 Cambridge University Press

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

Acosta, D., Goni, F. and Carmona, C. ( 1998). Characterization and partial purification of a leucine aminopeptidase from Fasciola hepatica. Journal of Parasitology 84, 17.Google Scholar
Agatsuma, T., Arakawa, Y., Iwagami, M., Honzako, Y., Cahyaningsih, U., Kang, S.-Y. and Hong, S.-J. ( 2000). Molecular evidence of natural hybridisation between Fasciola hepatica and Fasciola gigantica. Parasitology International 49, 231238.CrossRefGoogle Scholar
Almeida, M. S., Torloni, H., Lee-Ho, P., Vilar, M. M., Taumayturgo, N., Simpson, A. J. and Tendler, M. ( 2003). Vaccination against Fasciola hepatica using a Schistosoma mansoni defined recombinant antigen, Sm14. Parasite Immunology 25, 135137.CrossRefGoogle Scholar
Andrews, S. ( 1999). The Life Cycle of Fasciola hepatica. In Fasciolosis ( ed. Dalton, J. P.) CAB International, Wallingford, Oxon, pp. 377410.
Bergquist, N. R., Leonardo, L. R. and Mitchell, G. F. ( 2005). Vaccine-linked chemotherapy: can schistosomiasis control benefit from an integrated approach? Trends in Parasitology 21, 112117.Google Scholar
Bernal, D., De La Rubia, J. E., Carrasco-Abad, A. M., Toledo, R., Mas-Coma, S. and Marcilla, A. ( 2004). Identification of enolase as a plasminogen-binding protein in excretory-secretory products of Fasciola hepatica. FEBS Letters 563, 203206.CrossRefGoogle Scholar
Blas, B. L., Rosales, M. I., Lipayon, I. L., Yasuraoka, K., Matsuda, H. and Hayashi, M. ( 2004). The schistosomiasis problem in the Philippines: a review. Parasitology International 53, 127134.CrossRefGoogle Scholar
Bozas, S. E. and Spithill, T. W. ( 1996). Identification of 3-hydroxyproline residues in several proteins of Fasciola hepatica. Experimental Parasitology 82, 6972.CrossRefGoogle Scholar
Bjorland, J., Bryan, R. T., Strauss, W., Hillyer, G. V. and McAuley, J. B. ( 1995). An outbreak of acute fasioliasis among Aymara Indians in the Bolivian Altiplano. Clinical Infectious Diseases 21, 12281233.CrossRefGoogle Scholar
Brady, M. T., O'Neill, S. M., Dalton, J. P. and Mills, K. H. G. ( 1999). Fasciola hepatica suppresses a protective Th1 response against Bordetella pertussis. Infection and Immunity 67, 53725378.Google Scholar
Capron, A., Riveau, G., Capron, M. and Trottein, F. ( 2005). Schistosomes: the road from host-parasite interactions to vaccines in clinical trials. Trends in Parasitology 21, 143149.CrossRefGoogle Scholar
Carmona, C. ( 2005). Fasciola hepatica recombinant leucyl aminopeptidase functionally expressed in Escherichia coli induced high levels of protection in rabbits. 20th International Conference of the World Association for the Advancement of Veterinary Parasitology (WAAVP), Christchurch, New Zealand.
Casanueva, P., Hillyer, G. V., Ramajo, V., Oleaga, A., Espinoza, E. Y. and Munro, A. ( 2001). Immunoprophylaxis against Fasciola hepatica in rabbits using a recombinant Fh15 fatty acid-binding protein. Journal of Parasitology 87, 697700.CrossRefGoogle Scholar
Chai, M., McManus, D. P., Moertel, L., Tran, M., Loukas, A., Jones, M. K. and Gobert, G. N. ( 2006). Transcriptome profiling of lung schistosomula, in vitro cultured schistosomula and adult Schistosoma japonicum. Cellular and Molecular Life Sciences 63, 919929.CrossRefGoogle Scholar
Chen, M. G. and Feng, Z. ( 1999). Schistosomiasis control in China. Parasitology International 48, 1119.Google Scholar
Chen, H. A. and Lin, D. ( 2004). The prevalence and control of schistosomiasis in Poyang Lake region, China. Parasitology International 53, 115125.CrossRefGoogle Scholar
Cheng, G. F., Lin, J. J., Feng, X. G., Fu, Z. Q., Jin, Y. M., Yuan, C. X., Zhou, Y. C. and Cai, Y. M. ( 2005). Proteomic analysis of differentially expressed proteins between the male and female worms of Schistosoma japonicum after pairing. Proteomics 5, 511521.CrossRefGoogle Scholar
Collins, P. R., Stack, C. N., O'Neill, S. M., Doyle, S., Ryan, T., Brennan, G. P., Mousley, A., Stewart, M., Maule, A. G., Dalton, J. P. and Donnelly, S. ( 2004). Cathepsin L1, the major protease involved in liver fluke (Fasciola hepatica) virulence: propeptide cleavage sites and autoactivation of the zymogen secreted from gastrodrmal cells. Journal of Biological Chemistry 279, 1703817046.CrossRefGoogle Scholar
Corbeil, L. B. ( 2002). Antibodies as effectors. Veterinary Immunology and Immunopathology 87, 169175.CrossRefGoogle Scholar
Crawley, A. and Wilkie, B. N. ( 2003). Porcine Ig isotypes: function and molecular characteristics. Vaccine 21, 29112922.CrossRefGoogle Scholar
Curtale, F., Hassanein, Y. A. and Savioli, L. ( 2005). Control of human fascioliasis by selective chemotherapy: design, cost and effect of the first public health, school-based intervention implemented in endemic areas of the Nile Delta, Egypt. Transaction of the Royal Society of Tropical Medicine and Hygiene 99, 599609.CrossRefGoogle Scholar
Curtale, F., Mas-Coma, S., Hassanein, Y. A., Barduagni, P., Pezzotti, P. and Savioli, L. ( 2003). Clinical signs and household characteristics associated with human fascioliasis among rural population in Egypt: a case-control study. Parasitologia 45, 511.Google Scholar
Curwen, R. S., Ashton, P. D., Johnston, D. A. and Wilson, R. A. ( 2004). The Schistosoma mansoni soluble proteome: a comparison across four life-cycle stages. Molecular and Biochemical Parasitology 138, 5766.CrossRefGoogle Scholar
Curwen, R. S., Ashton, P. D., Sundaralingam, S. and Wilson, R. A. ( 2006). Identification of novel proteases and immunomodulators in the secretions of schistosome cercariae that facilitate host entry. Molecular Cellular Proteomics. Feb 9 [Epub ahead of print].CrossRefGoogle Scholar
Da'Dara, A. A. and Harn, D. A. ( 2005). DNA vaccines against tropical parasitic diseases. Expert Reviews in Vaccines 4, 575589.CrossRefGoogle Scholar
Dalton, J. P., Brindley, P. J., Knox, D. P., Hotez, P. J., Brady, C., Donnelly, S., O'Neill, S. M., Mulcahy, G. and Loukas, A. C. ( 2003 a). Helminth Vaccines: from mining genomic information for vaccine targets to systems used for protein expression. International Journal for Parasitology 33, 621640.Google Scholar
Dalton, J. P., McGonigle, S., Rolph, T. and Andrews, S. ( 1996). Induction of protective immunity in cattle against infection with Fasciola hepatica by vaccination with cathepsin L proteinases and with hemoglobin. Infection and Immunity 64, 50665074.Google Scholar
Dalton, J. P. and Mulcahy, G. ( 2001). Parasite Vaccines – A Reality? Veterinary Parasitology 98, 149167.Google Scholar
Dalton, J. P., O'Neill, S. M., Stack, C., Collins, P., Walsh, A., Sekiya, M., Doyle, S., Mulcahy, G., Hoyle, D., Khaznadji, E., Moire, N., Brennan, G., Mousley, A., Kreshchenko, N., Maule, A. and Donnelly, S. ( 2003 b). Fasciola hepatica cathepsin L-like proteases: biology, function, and potential in the development of first generation liver fluke vaccines. International Journal for Parasitology 33, 11731181.Google Scholar
Dalton, J. P., Skelly, P. and Halton, D. W. ( 2004). The role of the tegument and gut in nutrient uptake by parasitic platyhelminths. Canadian Journal of Zoology 82, 211232.CrossRefGoogle Scholar
Dalton, J. P. and Spithill, T. ( 1998). Approaches towards the development of a vaccine against liver fluke disease. Parasitology Today 14, 224228.Google Scholar
De Bont, J., Claerebout, E., Riveau, G., Schacht, A. M., Smets, K., Conder, G., Brake, D. A., Capron, A. and Vercruysse, J. ( 2003). Failure of a recombinant Schistosoma bovis-derived glutathione S-transferase to protect cattle against experimental Fasciola hepatica infection. Veterinary Parasitology 113, 135144.CrossRefGoogle Scholar
De Bont, J. and Vercruysse, J. ( 1998) Schistosomiasis in cattle. Advances in Parasitology 41, 285364.CrossRefGoogle Scholar
Donnelly, S., Sekiya, M., Mulcahy, G., O'Neill, S. and Dalton, J. P. ( 2005). Thioredoxin peroxidase secreted by Fasciola hepatica induces alternative activation of macrophages. Infection and Immunity 73, 166173.CrossRefGoogle Scholar
Espino, A. M., Gil, R., Osuna, A. and Hillyer, G. V. ( 2005). Fasciola hepatica: humoral and cellular responses to a member of the saposin-like protein family following delivery as a DNA vaccine in mice. Experimental Parasitology 110, 373383.CrossRefGoogle Scholar
Espino, A. M. and Hillyer, G. V. ( 2003). Molecular cloning of a member of the Fasciola hepatica saposin-like protein family. Journal of Parasitology 89, 545552.CrossRefGoogle Scholar
Espino, A. M. and Hillyer, G. V. ( 2004). A novel Fasciola hepatica saposin-like recombinant protein with immunoprophylactic potential. Journal of Parasitology 90, 876879.CrossRefGoogle Scholar
Estes, D. M. and Brown, W. C. ( 2002). Type 1 and type 2 responses in regulation of Ig isotype expression in cattle. Veterinary Immunology and Immunopathology 90, 110.CrossRefGoogle Scholar
Esteban, J. G., Gonzalez, C., Curtale, F., Munoz-Antoli, C., Valero, M. A., Bargues, M. D., El Sayed, M., El Wakeel, A., Abdel-Wahad, Y., Montresor, A., Engels, D., Savioli, L. and Mas-Coma, S. ( 2003). Hyperendemic fascioliasis associated with schistosomiasis in villages of the Nile Delta, Egypt. American Journal of Tropical Medicine and Hygiene 69, 429437.Google Scholar
Estuningsih, S. E., Smooker, P. M., Wiedosari, E., Widjajanti, S., Vaiano, S., Partoutomo, S. and Spithill, T. W. ( 1997). Evaluation of antigens of Fasciola gigantica as vaccines against tropical fasciolosis in cattle. International Journal for Parasitology 27, 14191428.CrossRefGoogle Scholar
Fairweather, I. and Boray, J. C. ( 1999). Mechanism of fasciolicide action and drug resistance in Fasciola hepatica. In Fasciolosis ( ed. Dalton, J. P.) CAB International, Wallingford, Oxon, UK. pp. 225276.
Fan, J., Gan, X., Yang, W., Shen, L., McManus, D. P. and Brindley, P. J. ( 2003). A Schistosoma japonicum very low-density lipoprotein-binding protein. International Journal of Biochemistry and Cell Biology 35, 14361451.CrossRefGoogle Scholar
Fitzpatrick, J. M., Johansen, M. V., Johnston, D. A., Dunne, D. W. and Hoffmann, K. F. ( 2004). Gender-associated gene expression in two related strains of Schistosoma japonicum. Molecular and Biochemical Parasitology 136, 191209.CrossRefGoogle Scholar
Fitzpatrick, J. M., Johnston, D. A., Williams, G. W., Williams, D. J., Freeman, T. C., Dunne, D. W. and Hoffmann, K. F. ( 2005). An oligonucleotide microarray for transcriptome analysis of Schistosoma mansoni and its application/use to investigate gender-associated gene expression. Molecular and Biochemical Parasitology 141, 113.CrossRefGoogle Scholar
Gan, Y., Shi, Y. E., Bu, L. Y., Ning, C. X. and Zhu, H. G. ( 2005). [Vaccination of mice with recombinant nucleic acid vaccine encoding the integral membrane protein Sj23 and cytokine IL-12 elicits specific immune responses against schistosomiasis japonica.] [Article in Chinese]. Zhonghua Yi Xue Za Zhi 85, 193198.Google Scholar
Gan, X.-X., Zeng, X.-P., Wang, Y., Ding, J.-Z., Shen, H.-Y., Shen, L. Y., McManus, D. P., Brindley, P. J. and Fan, J. J. ( 2006). Recombinant tegumental protein Schistosoma japonicum very low density lipoprotein binding protein as a vaccine candidateagainst Schistosoma japonicum. Memorias do Instituto Oswaldo Cruz 101, 913.CrossRefGoogle Scholar
Gobert, G. N. and McManus, D. P. ( 2005). Update on paramyosin in parasitic worms. Parasitology International 54, 101107.CrossRefGoogle Scholar
Gobert, G. N., Moertel, L., Nelson, C., Mcinnis, R. L., Jones, M. K., Hu, W. and McManus, D. P. ( 2006). Transcriptomics tool for the human blood flukes Schistosoma using microarray gene expression profiling. Experimental Parasitology 114, 160172.CrossRefGoogle Scholar
Graczyk, T. and Fried, B. ( 1999). Development of Fasciola hepatica in the intermediate host. In Fasciolosis ( ed. Dalton, J. P.) CAB International, Wallingford, Oxon, UK. pp. 3146.
Guo, J., Li, Y., Gray, D., Ning, A., Hu, G., Chen, H., Davis, G. M., Sleigh, A. C., Feng, Z., McManus, D. P. and Williams, G. M. ( 2006). A drug-based intervention study on the importance of buffaloes for human Schistososma japonicum infection around Poyang Lake, People's Republic of China. American Journal of Tropical Medicine and Hygiene 74, 335341.Google Scholar
Hagan, P. and Sharaf, O. ( 2003). Schistosomiasis vaccines. Expert Opinion on Biological Therapy 3, 12711278.CrossRefGoogle Scholar
Harmsen, M. M., Cornelissen, J. B., Buis, H. E., Boersma, W. J., Jeurissen, S. H. and Van Milligan, F. J. ( 2004). Identification of a novel Fasciola hepatica cathepsin L protease containing protective epitopes within the propeptide. International Journal for Parasitology 34, 675682.CrossRefGoogle Scholar
He, Y. K., Liu, S. X., Zhang, X. Y., Song, G. C., Luo, X. S., Li, Y. S., Xu, Y. X., Yu, X. L., Li, Y., Hou, X. Y. and McManus, D. P. ( 2003). Field assessment of recombinant Schistosoma japonicum 26 kDa glutathione S-transferase in Chinese water buffaloes. Southeast Asian Journal of Tropical Medicine and Public Health 34, 473479.Google Scholar
Hein, W. R., Barber, T., Cole, S.-A., Morrison, L. and Pernthaner, A. ( 2004). Long-term collection and characterization of afferent lymph from the ovine small intestine. Journal of Immunological Methods 293, 153168.CrossRefGoogle Scholar
Hien, T. V., Dung, T. T. K., Chi, N. H., Dahn, P. H. and Pham, P. T. ( 2001). Fasciolosis in Vietnam. Southeast Asian Journal of Tropical Medicine and Public Health 31 (), 4850.Google Scholar
Hillyer, G. H. and Apt, W. ( 1997) Food-borne trematode infections in the Americas. Parasitology Today 13, 8788.CrossRefGoogle Scholar
Hillyer, G. H., Soler De Galanes, M., Rodriguez-Perz, J., Bjorland, J., Siva De Lagrava, M., Ramirez Guzman, S. and Bryan, R. T. ( 1992). Use of the Falcon Assay Screening Test-Enzyme-Linked Immunosorbant Assay (FAST-ELISA) and the Enzyme-Linked Immunoelectrotransfer Blot (EITB) to determine the prevalence of human fascioliasis in the Bolivian Altiplano. American Journal of Tropical Medicine and Hygiene 46, 603609.CrossRefGoogle Scholar
Hillyer, G. V. ( 2005). Fasciola antigens as vaccines against fasciolosis and schistosomiasis. Journal of Helminthology 79, 18.Google Scholar
Hopkins, D. R. ( 1992). Homing in on helminths. American Journal of Tropical Medicine and Hygiene 46, 626634.CrossRefGoogle Scholar
Hoyle, D. V., Dalton, J. P., Chase-Topping, M. and Taylor, D. W. ( 2003). Pre-exposure of cattle to drug-abbreviated Fasciola hepatica infections: the effect upon subsequent challenge infection and the early immune response. Veterinary Parasitology 111, 6582.CrossRefGoogle Scholar
Hu, W., Yan, Q., Shen, D. K., Liu, F., Zhu, Z. D., Song, H. D., Xu, X. R., Wang, Z. J., Rong, Y. P., Zeng, L. C., Wu, J., Zhang, X., Wang, J. J., Xu, X. N., Wang, S. Y., Fu, G., Zhang, X. L., Wang, Z. Q., Brindley, P. J., McManus, D. P., Xue, C. L., Feng, Z., Chen, Z. and Han, Z. G. ( 2003). Evolutionary and biomedical implications of a Schistosoma japonicum complementary DNA resource. Nature Genetics 35, 139147.CrossRefGoogle Scholar
Ishikawa, H., Ohmae, H., Pangilinan, R., Redulla, A. and Matsuda, H. ( 2006). Modeling the dynamics and control of Schistosoma japonicum transmission on Bohol island, the Philippines. Parasitology International 55, 2329.CrossRefGoogle Scholar
Itagaki, T. and Tsutsumi, K. ( 1998) Triploid form of Fasciola in Japan: genetic relationships between Fasciola hepatica and Fasciola gigantica determined by ITS-2 sequence of nuclear rDNA. International Journal for Parasitology 28, 777781.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, 11281132.3.0.CO;2-0>CrossRefGoogle Scholar
King, C. H., Dickman, K. and Tisch, D. J. ( 2005). Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365, 15611569.CrossRefGoogle Scholar
Knudsen, G. M., Medzihradszky, K. F., Lim, K. C., Hansell, E. and McKerrow, J. H. ( 2005). Proteomic analysis of Schistosoma mansoni cercarial secretions. Molecular and Cellular Proteomics 4, 18621875.CrossRefGoogle Scholar
Kofta, K. W., Mieszczanek, L., Plucienniczak, G. and Wedrychowicz, H. ( 2000). Successful DNA immunization of rats against fascioliasis. Vaccine 18, 29852990.CrossRefGoogle Scholar
Law, R. H., Smookeer, P. M., Irving, J. A., Piedrafita, D., Ponting, R., Kennedy, N. J., Whisstock, J. C., Pike, R. N. and Spithill, T. W. ( 2003). Cloning and expression of the major secreted cathepsin B-like protein from juvenile Fasciola hepatica and analysis of immunogenicity following liver fluke infection. Infection and Immunity 71, 69216932.CrossRefGoogle Scholar
Lebens, M., Sun, J. B., Czerkinsky, C. and Holmgren, J. ( 2004). Current status and future prospects for a vaccine against schistosomiasis. Expert Review of Vaccines 3, 315328.CrossRefGoogle Scholar
Leenstra, T., Acosta, L. P., Wu, H. W., Langdon, G. C., Solomon, J. S., Manalo, D. L., Su, L., Jiz, M., Jarilla, B., Pablo, A. O., Mcgarvey, S. T., Olveda, R. M., Friedman, J. F. and Kurtis, J. D. ( 2006). T-helper-2 cytokine responses to Sj97 predict resistance to reinfection with Schistosoma japonicum. Infection and Immunity, 74, 370381.CrossRefGoogle Scholar
Liu, J. M., Cai, X. Z., Lin, J. J., Fu, Z. Q., Yang, G. Z., Shi, F. H., Cai, Y. M., Shen, W., Taylor, M. G. and Wu, X. F. ( 2004). Gene cloning, expression and vaccine testing of Schistosoma japonicum SjFABP. Parasite Immunology 26, 351358.CrossRefGoogle Scholar
Lopez-Aban, J., Oleaga, A., Ramajo, V., Casanueva, P., Perez Arellano, J. L., Hillyer, G. V. and Muro, A. ( 2000). Vaccination of mice against Schistosoma bovis with a recombinant fatty acid binding protein from Fasciola hepatica. Veterinary Parasitology 91, 3342.CrossRefGoogle Scholar
Lopez-Aban, J., Ramajo, V., Perez Arellano, J. L., Oleaga, A., Hillyer, G. V. and Muro, A. ( 1999). A fatty acid binding protein from Fasciola hepatica induced protection in C57/Bl mice from challenge infection with Schistosoma bovis. Veterinary Parasitology 83, 107121.CrossRefGoogle Scholar
Macpherson, C. N. L. ( 2005). Human behaviour and the epidemiology of parasitic zoonoses. International Journal for Parasitology 35, 113.CrossRefGoogle Scholar
Maggioli, G., Piacenza, L., Carambula, B. and Carmona, C. ( 2004). Purification, characterization, and immunolocalization of a thioredoxin reductase from adult Fasciola hepatica. Journal of Parasitology 90, 205211.CrossRefGoogle Scholar
Martinez-Fernandez, A. R., Nogal-Ruiz, J. J., Lopez-Aban, J., Ramajo, V., Oleaga, A., Manga-Gonzalez, Y., Hillyer, G. V. and Muro, A. ( 2004). Vaccination of mice and sheep with Fh12FABP from Fasciola hepatica using the new adjuvant/immunomodulator system ADAD. Veterinary Parasitology 126, 287298.CrossRefGoogle Scholar
Mas-Coma, S. ( 2004). Human fasciolosis: epidemiological patterns in human endemic areas of South America, Africa and Asia. Southeast Asian Journal of Tropical Medicine 35 (), 111.Google Scholar
Mas-Coma, S., Angles, R., Esteban, J. G., Bargues, M. D., Buchon, P., Franjen, M. and Strauss, W. ( 1999 b). The Northern Bolivian Altiplano: a region highly endemic for human fasciolosis. Tropical Medicine and International Health 4, 454467.Google Scholar
Mas-Coma, S., Barques, M. D. and Valero, M. A. ( 2005). Fascioliasis and other plant-borne trematode zoonoses. International Journal for Parasitology 35, 12551278.CrossRefGoogle Scholar
Mas-Coma, S., Esteban, M. D. and Barques, M. D. ( 1999 a). Human Fasciolosis. In Fasciolosis ( ed. Dalton, J. P.) CAB International Publishing, Wallingford, Oxon, UK. pp. 411434.
McGonigle, S., Curley, J. P. and Dalton, J. P. ( 1997). Cloning of peroxidoxin, a novel antioxidant, from the helminth parasite Fasciola hepatica. Parasitology 115, 101104.CrossRefGoogle Scholar
McGonigle, S. and Dalton, J. P. ( 1995). Isolation of liver fluke haemoglobin. Parasitology 111, 209215.CrossRefGoogle Scholar
McGonigle, S., Dalton, J. P. and James, E. R. ( 1998). Peroxidoxins. Parasitology Today 14, 139145.CrossRefGoogle Scholar
McManus, D. P. ( 2005). Prospects for development of a transmission blocking vaccine against Schistosoma japonicum. Parasite Immunology 27, 297308.CrossRefGoogle Scholar
McManus, D. P. and Bartley, P. B. ( 2004). A vaccine against Asian schistosomiasis. Parasitology International 53, 163173.CrossRefGoogle Scholar
Meemon, K., Grams, R., Vichasri-Grams, S., Homan, A., Korge, G., Viyanant, V., Upatham, E. S., Habe, S. and Sobhon, P. ( 2004). Molecular cloning and analysis of stage and tissue-specific expression of cathepsin B encoding genes from Fasciola gigantica. Molecular and Biochemical Parasitology 136, 110.CrossRefGoogle Scholar
Meeusen, E. N. T. and Balic, A. ( 2000). Do eosinophils have a role in the killing of helminth parasites? Parasitology Today 16, 95101.Google Scholar
Meeusen, E. N. T. and Piedrafita, D. ( 2003). Exploiting natural immunity to helminth parasites for the development of veterinary vaccines. International Journal for Parasitology 33, 12851290.CrossRefGoogle Scholar
Moertel, L., McManus, D. P., Piva, T. J., Young, L., McInnis, R. L. and Gobert, G. N. ( 2006). Oligonucleotide microarray analysis of strain- and gender-associated gene expression in the human blood fluke, Schistosoma japonicum. Molecular and Cellular Probes 20, 280289.CrossRefGoogle Scholar
Moghaddam, A. S., Massound, J., Mahmoodi, M., Mahvi, A. H., Periago, M. V., Artigas, P., Fuentes, M. V., Bargues, M. D. and Mas-Coma, S. ( 2004). Human and animal fascioliasis in Mazandarin province, northern Iran. Parasitology Research 94, 6169.Google Scholar
Mulcahy, G., Joyce, P. and Dalton, J. P. ( 1999). The Immunology of Fasciolosis. In Fasciolosis (ed. J. P. Dalton) CAB International, Wallinford, UK. pp. 341376.
Mulcahy, G., O'Connor, F., Mcgonigle, S., Dowd, A., Clery, D. G., Andrews, S. J. and Dalton, J. P. ( 1998). Correlation of specific antibody titre and avidity with protection in cattle immunised against Fasciola hepatica. Vaccine 16, 932939.CrossRefGoogle Scholar
Muro, A., Ramajo, V., Lopez, J., Simon, F. and Hillyer, G. V. ( 1997). Fasciola hepatica: vaccination of rabbits with native and recombinant antigens related to fatty acid binding proteins. Veterinary Parasitology 69, 219229.CrossRefGoogle Scholar
O'Neill, S. M., Brady, M. T., Callanan, J. J., Mulcahy, G., Joyce, P., Mills, H. G. and Dalton, J. P. ( 1999 b). Fasciola hepatica infection downregulates Th1 responses in mice. Parasite Immunology 22, 147155.Google Scholar
O'Neill, S. M., Mills, K. H. G. and Dalton, J. P. ( 2001). Fasciola hepatica cathepsin L cysteine proteinase suppresses Bordetella pertussis-specific IFN-γ production in vitro. Parasite Immunology 23, 541547.CrossRefGoogle Scholar
O'Neill, S. M., Parkinson, M., Dowd, A. J., Strauss, W., Angles, R. and Dalton, J. P. ( 1999 a). Immunodiagnosis of human fasciolosis using recombinant Fasciola hepatica cathepsin L1 cysteine proteinase. American Journal of Tropical Medicine and Hygiene 60, 749751.Google Scholar
O'Neill, S. M., Parkinson, M., Strauss, W., Angles, R. and Dalton, J. P. ( 1998). Immunodiagnosis of Fasciola hepatica infection (fasciolosis) in a human population in the Bolivian Altiplano using purified cathepsin L cysteine proteinase. American Journal of Tropical Medicine and Hygiene 58, 417423.CrossRefGoogle Scholar
Paykari, H., Dalimi, A. and Madani, R. ( 2002). Immunization of sheep against Fasciola gigantica with glutathione S-transferase. Veterinary Parasitology 105, 153159.CrossRefGoogle Scholar
Pearce, E. J. ( 2003). Progress towards a vaccine for schistosomiasis. Acta Tropica 86, 309313.CrossRefGoogle Scholar
Pearce, E. J. and Macdonald, A. S. ( 2002). The immunobiology of schistosomiasis. Nature Reviews in Immunology 2, 499511.CrossRefGoogle Scholar
Piacenza, L., Acosta, D., Basmadjian, I., Dalton, J. P. and Carmona, C. ( 1999). Vaccination of sheep with cathepsin L proteinases and with leucine aminopeptidase induces high levels of protection against fasciolosis. Infection and Immunity 67, 19541961.Google Scholar
Piedrafita, D., Parsons, J. C., Sandeman, R. M., Wood, R. M., Estuningsih, S. E., Partoutomo, S. and Spithill, T. W. ( 2001). Antibody-dependent cell-mediate cytotoxicity to newly excysted juvenile Fasciola hepatica in vitro is mediated by reactive nitrogen intermediates. Parasite Immunology 23, 473482.CrossRefGoogle Scholar
Piedrafita, D., Spithill, T. W., Dalton, J. P., Brindley, J. P., Sandeman, M. R., Wood, P. R. and Parsons, J. C. ( 2000). Juvenile Fasciola hepatica are resistant to killing in vitro by free radicals compared with larvae of Schistosoma mansoni. Parasite Immunology 22, 287295.CrossRefGoogle Scholar
Ramajo, V., Oleaga, A., Casenueva, P., Hillyer, G. V. and Muro, A. ( 2001). Vaccination of sheep against Fasciola hepatica with homologous fatty acid binding proteins. Veterinary Parasitology 97, 3546.CrossRefGoogle Scholar
Reed, M. B., Strugnell, R. A., Pannacio, M. and Spithill, T. W. ( 2000). A novel member of the NK-lysin protein family is developmentally regulated and secreted by Fasciola hepatica. Molecular and Biochemical Parasitology 105, 297303.CrossRefGoogle Scholar
Rim, H. J., Farag, H. F., Sornmani, S. and Cross, J. H. ( 1994). Food-borne trematodes: ignored or emerging? Parasitology Today 10, 207209.Google Scholar
Rokni, M. B., Massoud, J., O'Neill, S. M., Parkinson, M. and Dalton, J. P. ( 2002). Diagnosis of human fasciolosis in the Gilan province of Northern Iran: application of cathepsin L-ELISA. Diagnosis of Microbial Infectious Diseases 44, 175179.CrossRefGoogle Scholar
Ross, A. G. P., Bartley, P. B., Sleigh, A. C., Olds, G. R., Li, Y., Williams, G. M. and McManus, D. P. ( 2002). Schistosomiasis. New England Journal of Medicine 346, 12121220.CrossRefGoogle Scholar
Ross, A. G. P., Sleigh, A. C., Li, Y., Davis, G. M., Williams, G. M., Jiang, Z., Feng, Z. and McManus, D. P. ( 2001). Schistosomiasis in the People's Republic of China: prospects and challenges for the 21st Century. Clinical Microbiology Reviews 14, 270295.CrossRefGoogle Scholar
Savioli, L., Chitsulo, L. and Montresor, A. ( 1999). New opportunities for the control of fascioliasis. Bulletin of the World Health Organisation 77, 300.Google Scholar
Shi, F., Zhang, Y., Ye, P., Zuo, X., Shen, W., Cai, Y., Ye, P., Bickle, Q. D. and Taylor, M. G. ( 2001). Laboratory and field evaluation of Schistosoma japonicum DNA vaccines in sheep and water buffalo in China. Vaccine 20, 462467.CrossRefGoogle Scholar
Shi, Y. E., Jiang, C. F., Han, J. J., Li, Y. L. and Ruppel, A. ( 1990). Schistosoma japonicum: an ultraviolet-attenuated cercarial vaccine applicable in the field for water buffaloes. Experimental Parasitology 71, 100106.CrossRefGoogle Scholar
Spithill, T. W., Smooker, P. M. and Copeman, D. B. ( 1999 a). Fasciola gigantica: epidemiology, control, immunology, and molecular biology. In Fasciolosis ( ed. Dalton, J. P.) CAB International, Wallingford, Oxon, UK. pp. 465526.Google Scholar
Spithill, T. W., Smooker, P. M., Sexton, J. L., Bozas, E., Morrison, C. A., Creaney, J. and Parsons, J. C. ( 1999 b). Development of vaccines against Fasciola hepatica. In Fasciolosis ( ed. Dalton, J. P.) CAB International, Wallingford, Oxon, UK. pp. 377410.Google Scholar
Strauss, W., O'Neill, S. M., Parkinson, M., Angles, R. and Dalton, J. P. ( 1999). Diagnosis of human fasciolosis: detection of anti-cathepsin L antibodies in blood samples collected on filter paper. American Journal of Tropical Medicine and Hygiene 60, 746748.CrossRefGoogle Scholar
Tendler, M., Brito, C. A., Vilar, M. M., Serra-Freire, N., Diogo, C. M., Almeida, M. S., Delbem, A. C., Dasilva, J. F., Savino, W., Garratt, R. C., Katz, N. and Simpson, A. S. ( 1996). A Schistosoma mansoni fatty acid-binding protein, Sm14, is the potential basis of a dual purpose anti-helminth vaccine. Proceedings of the National Academy of Sciences, USA 93, 269273.CrossRefGoogle Scholar
Todd, C. W. and Colley, D. G. ( 2002). Practical and ethical issues in the development of a vaccine against schistosomiasis mansoni. American Journal of Tropical Medicine and Hygiene 66, 348358.CrossRefGoogle Scholar
Tort, J., Brindley, P. J., Knox, D., Wolfe, K. H. and Dalton, J. P. ( 1999). Helminth proteinases and their associated genes. Advances in Parasitology 43, 162268.Google Scholar
Van Balkom, B. W., Van Gestel, R. A., Brouwers, J. F., Krijgsveld, J., Tielens, A. G., Heck, A. J. and Van Hellemond, J. J. ( 2005). Mass spectrometric analysis of the Schistosoma mansoni tegumental sub-proteome. Journal of Proteome Research 4, 958966.CrossRefGoogle Scholar
Van Der Werf, M. J., De Vlas, S. J., Brooker, S., Looman, C. W., Nagelkerke, N. J., Habbema, J. D. and Engels, D. ( 2003). Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Tropica 86, 125139.CrossRefGoogle Scholar
Verjovski-Almeida, S., Demarco, R., Martins, E. A., Guimaraes, P. E., Ojopi, E. P., Paquola, A. C., Piazza, J. P., Nishiyama, M. Y. Jr., Kitajima, J. P., Adamson, R. E., Ashton, P. D., Bonaldo, M. F., Coulson, P. S., Dillon, G. P., Farias, L. P., Gregorio, S. P., Ho, P. L., Leite, R. A., Malaquias, L. C., Marques, R. C., Miyasato, P. A., Nascimento, A. L., Ohlweiler, F. P., Reis, E. M., Ribeiro, M. A., Sa, R. G., Stukart, G. C., Soares, M. B., Gargioni, C., Kawano, T., Rodrigues, V., Madeira, A. M., Wilson, R. A., Menck, C. F., Setubal, J. C., Leite, L. C. and Dias-Neto, E. ( 2003). Transcriptome analysis of the acoelomate human parasite Schistosoma mansoni. Nature Genetics 35, 148157.CrossRefGoogle Scholar
Vermeire, J. J., Taft, A. S., Hoffmann, K. F., Fitzpatrick, J. M. and Yoshino, T. P. ( 2006). Schistosoma mansoni: DNA microarray gene expression profiling during the miracidium-to-mother sporocyst transformation. Molecular and Biochemical Parasitology 147, 3947.CrossRefGoogle Scholar
Vilar, M. M., Barrientos, F., Almeida, M., Taumaturgo, N., Simpson, A., Garrat, R. and Tendler, M. ( 2003). An experimental bivalent peptide vaccine against schistsomiasis and fascioliasis. Vaccine 22, 137144.CrossRefGoogle Scholar
Wedrychowicz, H., Lamparska, M., Kesik, M., Kotomski, G., Mieszczanek, J., Jedlina-Panasiuk, L. and Plucienniczek, A. ( 2003). The immune response of rats to vaccination with the cDNA or protein forms of the cysteine proteinase of Fasciola hepatica. Veterinary Immunology and Immunopathology 94, 8393.CrossRefGoogle Scholar
Whitfield, P. J. ( 1979). The Biology of Parasitism: An Introduction to the Study of Associating Organisms. Edward Arnold, London.
Williams, G. M., Sleigh, A. C., Li, Y., Feng, Z., Davis, G. M., Chen, H., Ross, A. G., Bergquist, R. and McManus, D. P. ( 2002). Mathematical modelling of schistosomiasis japonica: comparison of control strategies in the People's Republic of China. Acta Tropica 82, 253262.CrossRefGoogle Scholar
Wu, Z. D., Lu, Z.-Y. and Yu, X.-B. ( 2005). Development of a vaccine agianst Schistosoma japonicum in China: a review. Acta Tropica 96, 106116.CrossRefGoogle Scholar
Yan, Y., Liu, S., Song, G., Xu, Y. and Dissous, C. ( 2005). Characterization of a novel vaccine candidate and serine proteinase inhibitor from Schistosoma japonicum (Sj serpin). Veterinary Parasitology 131, 5360.CrossRefGoogle Scholar
Zhang, W. Y., Moreau, E., Hope, J. C., Howard, C. J., Huang, W. and Chauvin, A. ( 2004 b). Fasciola hepatica and Fasciola gigantica: comparison of cellular response to experimental infection in sheep. Experimental Parasitology 111, 154159.Google Scholar
Zhang, W. Y., Moreau, E., Huang, W. and Chauvin, A. ( 2004 a). Comparison of the humoral response in sheep to Fasciola hepatica and Fasciola gigantica. Parasite 11, 153159.Google Scholar
Zhang, D. M., Pan, W. Q., Qian, L., Duke, M., Shen, L. H. and McManus, D. P. ( 2006). Investigation of recombinant Schistosoma japonicum paramyosin fragments for immunogenicity and vaccine efficacy in mice. Parasite Immunology 28, 7784.CrossRefGoogle Scholar
Zhao, S., Zhu, Y. C., Harn, D. A., Si, J., Ren, J. G., Yin, X. R., He, W., Liang, Y. S., Xu, M. and Xu, Y. L. ( 2005). Enhancement of the protective effect of SjC23 DNA vaccine against Schistosoma japonicum infection by immunostimulatory sequence [Article in Chinese]. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 23, 15.Google Scholar
Zhu, X. H., Shi, Y. E., Ning, C. X. and Zhu, H. G. ( 2005). The adjuvant effect of IL-12 on protective immunity of Schistosoma japonicum fatty acid binding protein (Sj14FABP) [Article in Chinese]. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 23, 150154.Google Scholar
Zhu, Y., Ren, J., Da'dara, A., Harn, D., Xu, M., Si, J., Yu, C., Liang, Y., Ye, P., Yin, X., He, W., Xu, Y., Cao, G. and Hua, W. ( 2004). The protective effect of a Schistosoma japonicum Chinese strain 23 kDa plasmid DNA vaccine in pigs is enhanced with IL-12. Vaccine 23, 7883.CrossRefGoogle Scholar
Zhu, Y., Si, J., Harn, D. A., Xu, M., Ren, J., Yu, C., Liang, Y., Yin, X., He, W. and Cao, G. ( 2006). Schistosoma japonicum triose-phosphate isomerase plasmid DNA vaccine protects pigs against challenge infection. Parasitology 132, 6771.CrossRefGoogle Scholar