Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-27T03:06:44.049Z Has data issue: false hasContentIssue false

Vaccines and diagnostics for zoonotic schistosomiasis japonica

Published online by Cambridge University Press:  31 October 2014

HONG YOU
Affiliation:
Molecular Parasitology Laboratory, Infectious Diseases Division, QIMR Berghofer Medical Research Institute, 300 Herston Road, Herston, Brisbane, QLD 4006, Australia
DONALD P. MCMANUS*
Affiliation:
Molecular Parasitology Laboratory, Infectious Diseases Division, QIMR Berghofer Medical Research Institute, 300 Herston Road, Herston, Brisbane, QLD 4006, Australia
*
* Corresponding author: Molecular Parasitology Laboratory, Infectious Diseases Division, QIMR Berghofer Medical Research Institute, 300 Herston Road, Herston, Brisbane, QLD 4006, Australia. E-mail: Don.McManus@qimrberghofer.edu.au

Summary

Schistosomiasis is one of the most prevalent, insidious and serious of the tropical parasitic diseases. Although the effective anthelmintic drug, praziquantel, is widely available and cheap, it does not protect against re-infection, drug-resistant schistosome may evolve and mass drug administration programmes based around praziquantel are probably unsustainable long term. Whereas protective anti-schistosome vaccines are not yet available, the zoonotic nature of Schistosoma japonicum provides a novel approach for developing a transmission-blocking veterinary vaccine in domestic animals, especially bovines, which are major reservoir hosts, being responsible for up to 90% of environmental egg contamination in China and the Philippines. However, a greater knowledge of schistosome immunology is required to understand the processes associated with anti-schistosome protective immunity and to reinforce the rationale for vaccine development against schistosomiasis japonica. Importantly as well, improved diagnostic tests, with high specificity and sensitivity, which are simple, rapid and able to diagnose light S. japonicum infections, are required to determine the extent of transmission interruption and the complete elimination of schistosomiasis following control efforts. This article discusses aspects of the host immune response in schistosomiasis, the current status of vaccine development against S. japonicum and reviews approaches for diagnosing and detecting schistosome infections in mammalian hosts.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2014 

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

Angeles, J. M., Goto, Y., Kirinoki, M., Leonardo, L., Tongol-Rivera, P., Villacorte, E., Inoue, N., Chigusa, Y. and Kawazu, S. (2011). Human antibody response to thioredoxin peroxidase-1 and tandem repeat proteins as immunodiagnostic antigen candidates for Schistosoma japonicum infection. American Journal of Tropical Medicine and Hygiene 85, 674679.Google Scholar
Angeles, J. M., Goto, Y., Kirinoki, M., Asada, M., Leonardo, L. R., Rivera, P. T., Villacorte, E. A., Inoue, N., Chigusa, Y. and Kawazu, S. (2012). Utilization of ELISA using thioredoxin peroxidase-1 and tandem repeat proteins for diagnosis of Schistosoma japonicum infection among water buffaloes. PLoS Neglected Tropical Diseases 6, e1800.Google Scholar
Hoy, A. M., Lundie, R. J., Ivens, A., Quintana, J. F., Nausch, N., Forster, T., Jones, F., Kabatereine, N. B., Dunne, D. W., Mutapi, F., MacDonald, A. S. and Buck, A. H. (2014). Parasite-derived microRNAs in host serum as novel biomarkers of Helminth infection. PLoS Neglected Tropical Diseases 8, e2701.Google Scholar
Berhe, N., Medhin, G., Erko, B., Smith, T., Gedamu, S., Bereded, D., Moore, R., Habte, E., Redda, A., Gebre-Michael, T. and Gundersen, S. G. (2004). Variations in helminth faecal egg counts in Kato-Katz thick smears and their implications in assessing infection status with Schistosoma mansoni . Acta Tropica 92, 205212.Google Scholar
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., et al. (2009). The genome of the blood fluke Schistosoma mansoni . Nature 460, 352358.Google Scholar
Boulanger, D., Reid, G. D., Sturrock, R. F., Wolowczuk, I., Balloul, J. M., Grezel, D., Pierce, R. J., Otieno, M. F., Guerret, S., Grimaud, J. A., Butterworth, A. E. and Capron, A. (1991). Immunization of mice and baboons with the recombinant Sm28GST affects both worm viability and fecundity after experimental infection with Schistosoma mansoni . Parasite Immunology 13, 473490.Google Scholar
Bueding, E. (1950). Carbohydrate metabolism of schistosoma mansoni . Journal of General Physiology 33, 475495.Google Scholar
Cai, S. F., Li, W. G. and Wang, M. (2011). Diagnosis of chronic schistosomiasis japonicum with the recombinant Sj26GST-Sj32 fusion protein by ELISA. Sichuan Da Xue Xue Bao. Yi Xue Ban (Journal of Sichuan University. Medical Science Edition) 42, 331334.Google Scholar
Cao, Y., Zhao, B., Han, Y., Zhang, J., Li, X., Qiu, C., Wu, X., Hong, Y., Ai, D., Lin, J. and Fu, Z. (2013). Gene gun bombardment with DNA-coated golden particles enhanced the protective effect of a DNA vaccine based on thioredoxin glutathione reductase of Schistosoma japonicum . Biomed Research International 2013, 952416.Google Scholar
Chand, M. A., Chiodini, P. L. and Doenhoff, M. J. (2010). Development of a new assay for the diagnosis of schistosomiasis, using cercarial antigens. Transactions of the Royal Society of Tropical Medicine and Hygiene 104, 255258.Google Scholar
Chen, D., Luo, X., Xie, H., Gao, Z., Fang, H. and Huang, J. (2013 a). Characteristics of IL-17 induction by Schistosoma japonicum infection in C57BL/6 mouse liver. Immunology 139, 523532.Google Scholar
Chen, H., Nara, T., Zeng, X., Satoh, M., Wu, G., Jiang, W., Yi, F., Kojima, S., Zhang, S. and Hirayama, K. (2000). Vaccination of domestic pig with recombinant paramyosin against Schistosoma japonicum in China. Vaccine 18, 21422146.Google Scholar
Chen, D., Xie, H., Luo, X., Yu, X., Fu, X., Gu, H., Wu, C., Tang, X. and Huang, J. (2013 b). Roles of Th17 cells in pulmonary granulomas induced by Schistosoma japonicum in C57BL/6 mice. Cellular Immunology 285, 149157.Google Scholar
Chen, H. and Lin, D. (2004). The prevalence and control of schistosomiasis in Poyang Lake region, China. Parasitology International 53, 115125.Google Scholar
Cheng, G., Luo, R., Hu, C., Cao, J. and Jin, Y. (2013). Deep sequencing-based identification of pathogen-specific microRNAs in the plasma of rabbits infected with Schistosoma japonicum . Parasitology 140, 17511761.Google Scholar
Colley, D. G., Bustinduy, A. L., Secor, W. E. and King, C. H. (2014). Human schistosomiasis. The Lancet 383, 22532264.Google Scholar
Da'dara, A. A., Li, Y. S., Xiong, T., Zhou, J., Williams, G. M., McManus, D. P., Feng, Z., Yu, X. L., Gray, D. J. and Harn, D. A. (2008). DNA-based vaccines protect against zoonotic schistosomiasis in water buffalo. Vaccine 26, 36173625.Google Scholar
Deelder, A. M., Klappe, H. T., van den Aardweg, G. J. and van Meerbeke, E. H. (1976). Schistosoma mansoni: demonstration of two circulating antigens in infected hamsters. Experimental Parasitology, 40, 189197.Google Scholar
de Jong, E. C., Vieira, P. L., Kalinski, P., Schuitemaker, J. H., Tanaka, Y., Wierenga, E. A., Yazdanbakhsh, M. and Kapsenberg, M. L. (2002). Microbial compounds selectively induce Th1 cell-promoting or Th2 cell-promoting dendritic cells in vitro with diverse Th cell-polarizing signals. Journal of Immunology 168, 17041709.Google Scholar
Deng, W., Xu, B., Hu, H., Li, J., Hu, W., Song, S., Feng, Z. and Fan, C. (2013). Diagnosis of schistosomiasis japonica with interfacial co-assembly-based multi-channel electrochemical immunosensor arrays. Scientific Reports 3, 1789.Google Scholar
de Oliveira, E. J., Kanamura, H. Y., Takei, K., Hirata, R. D., Valli, L. C., Nguyen, N. Y., de Carvalho Rodrigues, I., de Jesus, A. R. and Hirata, M. H. (2008). Synthetic peptides as an antigenic base in an ELISA for laboratory diagnosis of Schistosomiasis mansoni . Transactions of the Royal Society of Tropical Medicine and Hygiene 102, 360366.Google Scholar
de Oliveira Fraga, L. A., Lamb, E. W., Moreno, E. C., Chatterjee, M., Dvorak, J., Delcroix, M., Sajid, M., Caffrey, C. R. and Davies, S. J. (2010). Rapid induction of IgE responses to a worm cysteine protease during murine pre-patent schistosome infection. BMC Immunology 11, 56.Google Scholar
Diallo, T. O., Remoue, F., Schacht, A. M., Charrier, N., Dompnier, J. P., Pillet, S., Garraud, O., N'Diaye A, A., Capron, A., Capron, M. and Riveau, G. (2004). Schistosomiasis co-infection in humans influences inflammatory markers in uncomplicated Plasmodium falciparum malaria. Parasite Immunology 26, 365369.Google Scholar
Doenhoff, M. J., Chiodini, P. L. and Hamilton, J. V. (2004). Specific and sensitive diagnosis of schistosome infection: can it be done with antibodies? Trends in Parasitology, 20, 3539.Google Scholar
Du, X., Wu, J., Zhang, M., Gao, Y., Zhang, D., Hou, M., Ji, M. and Wu, G. (2011). Upregulated expression of cytotoxicity-related genes in IFN-gamma knockout mice with Schistosoma japonicum infection. Journal of Biomedicine and Biotechnology 2011, 864945.Google Scholar
Elias, D., Akuffo, H., Pawlowski, A., Haile, M., Schon, T. and Britton, S. (2005). Schistosoma mansoni infection reduces the protective efficacy of BCG vaccination against virulent Mycobacterium tuberculosis . Vaccine 23, 13261334.Google Scholar
El Ridi, R., Tallima, H., Mahana, N. and Dalton, J. P. (2010). Innate immunogenicity and in vitro protective potential of Schistosoma mansoni lung schistosomula excretory–secretory candidate vaccine antigens. Microbes and Infection 12, 700709.Google Scholar
Fagundes Teixeira, C., Neuhauss, E., Ben, R., Romanzini, J. and Graeff-Teixeira, C. (2007). Detection of Schistosoma mansoni eggs in feces through their interaction with paramagnetic beads in a magnetic field. PLoS Neglected Tropical Diseases 1, e73.Google Scholar
Fallon, P. G., Richardson, E. J., McKenzie, G. J. and McKenzie, A. N. (2000). Schistosome infection of transgenic mice defines distinct and contrasting pathogenic roles for IL-4 and IL-13: IL-13 is a profibrotic agent. Journal of Immunology 164, 25852591.Google Scholar
Fung, M. S., Xiao, N., Wang, S. and Carlton, E. J. (2012). Field evaluation of a PCR test for Schistosoma japonicum egg detection in low-prevalence regions of China. American Journal of Tropical Medicine and Hygiene 87, 10531058.Google 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 Schistosoma japonica . Zhonghua Yi Xue Za Zhi 85, 193198.Google Scholar
Gan, Y., Shi, Y. E., Bu, L. Y., Zhu, X. H., Ning, C. X. and Zhu, H. G. (2004). Immune responses against Schistosoma japonicum after vaccinating mice with a multivalent DNA vaccine encoding integrated membrane protein Sj23 and cytokine interleukin-12. Chinese Medical Journal 117, 18421846.Google Scholar
Gobert, G. N. and McManus, D. P. (2005). Update on paramyosin in parasitic worms. Parasitology International 54, 101107.Google Scholar
Gobert, G. N., Stenzel, D. J., Jones, M. K. and McManus, D. P. (1997). Immunolocalization of the fatty acid-binding protein Sj-FABPc within adult Schistosoma japonicum . Parasitology 115 (Pt 1), 3339.Google Scholar
Gonnert, R. and Andrews, P. (1977). Praziquantel, a new board-spectrum antischistosomal agent. Zeitschrift fur Parasitenkunde 52, 129150.Google Scholar
Gordon, C. A., Acosta, L. P., Gray, D. J., Olveda, R. M., Jarilla, B., Gobert, G. N., Ross, A. G. and McManus, D. P. (2012). High prevalence of Schistosoma japonicum infection in Carabao from Samar Province, the Philippines: implications for transmission and control. PLoS Neglected Tropical Diseases 6, e1778.Google Scholar
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 Schistosoma japonicum infection around Poyang Lake, People's Republic of China. American Journal of Tropical Medicine and Hygiene 74, 335341.Google Scholar
Guo, D., Wang, H., Zeng, D., Li, X., Fan, X. and Li, Y. (2011). Vaccine potential of hemocyanin from Oncomelania hupensis against Schistosoma japonicum . Parasitology International 60, 242246.CrossRefGoogle ScholarPubMed
Guo, J. J., Zheng, H. J., Xu, J., Zhu, X. Q., Wang, S. Y. and Xia, C. M. (2012). Sensitive and specific target sequences selected from retrotransposons of Schistosoma japonicum for the diagnosis of schistosomiasis. PLoS Neglected Tropical Diseases 6, e1579.Google Scholar
Han, H., Peng, J., Hong, Y., Zhang, M., Han, Y., Liu, D., Fu, Z., Shi, Y., Xu, J., Tao, J. and Lin, J. (2013). MicroRNA expression profile in different tissues of BALB/c mice in the early phase of Schistosoma japonicum infection. Molecular and Biochemical Parasitology 188, 19.Google Scholar
Han, Y., Zhang, M., Hong, Y., Zhu, Z., Li, D., Li, X., Fu, Z. and Lin, J. (2012). Characterization of thioredoxin glutathione reductase in Schiotosoma japonicum . Parasitology International 61, 475480.Google Scholar
He, X., Sai, X., Chen, C., Zhang, Y., Xu, X., Zhang, D. and Pan, W. (2013). Host serum miR-223 is a potential new biomarker for Schistosoma japonicum infection and the response to chemotherapy. Parasites and Vectors 6, 272.Google Scholar
He, S., Yang, L., Lv, Z., Hu, W., Cao, J., Wei, J., Sun, X., Yang, J., Zheng, H. and Wu, Z. (2010). Molecular and functional characterization of a mortalin-like protein from Schistosoma japonicum (SjMLP/hsp70) as a member of the HSP70 family. Parasitology Research 107, 955966.Google Scholar
Hesse, M., Cheever, A. W., Jankovic, D. and Wynn, T. A. (2000). NOS-2 mediates the protective anti-inflammatory and antifibrotic effects of the Th1-inducing adjuvant, IL-12, in a Th2 model of granulomatous disease. American Journal of Pathology 157, 945955.Google Scholar
Hesse, M., Modolell, M., La Flamme, A. C., Schito, M., Fuentes, J. M., Cheever, A. W., Pearce, E. J. and Wynn, T. A. (2001). Differential regulation of nitric oxide synthase-2 and arginase-1 by type 1/type 2 cytokines in vivo: granulomatous pathology is shaped by the pattern of L-arginine metabolism. Journal of Immunology 167, 65336544.Google Scholar
Hong, Y., Han, Y., Fu, Z., Han, H., Qiu, C., Zhang, M., Yang, J., Shi, Y., Li, X. and Lin, J. (2013). Characterization and expression of the Schistosoma japonicum thioredoxin peroxidase-2 gene. Journal of Parasitology 99, 6876.Google Scholar
Hong, Y., Han, H., Peng, J., Li, Y., Shi, Y., Fu, Z., Liu, J., Lin, J. and Li, X. (2010). Schistosoma japonicum: cloning, expression and characterization of a gene encoding the alpha5-subunit of the proteasome. Experimental Parasitology 126, 517525.Google Scholar
Horsnell, W. G. and Brombacher, F. (2010). Genes associated with alternatively activated macrophages discretely regulate helminth infection and pathogenesis in experimental mouse models. Immunobiology 215, 704708.Google Scholar
Hou, X., Yu, F., Man, S., Huang, D., Zhang, Y., Liu, M., Ren, C. and Shen, J. (2012). Negative regulation of Schistosoma japonicum egg-induced liver fibrosis by natural killer cells. PLoS Neglected Tropical Diseases 6, e1456.Google Scholar
Hsu, S. Y., Xu, S. T., He, Y. X., Shi, F. H., Shen, W., Hsu, H. F., Osborne, J. W. and Clarke, W. R. (1984). Vaccination of bovines against schistosomiasis japonica with highly irradiated schistosomula in China. American Journal of Tropical Medicine and Hygiene 33, 891898.Google 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.Google Scholar
Hu, Y., Lu, W., Shen, Y., Xu, Y., Yuan, Z., Zhang, C., Wu, J., Ni, Y., Liu, S. and Cao, J. (2012). Immune changes of Schistosoma japonicum infections in various rodent disease models. Experimental Parasitology 131, 180189.Google Scholar
Hua, W. Q., Yu, C. X., Yin, X. R. and Qian, C. Y. (2011). Application of F-ELISA for immunodiagnosis of schistosomiasis japonica. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi 23, 158162.Google Scholar
Huang, H., Liu, F., Huang, S., Yuan, S., Liao, B., Yi, S., Zeng, Y. and Chu, P. K. (2012). Sensitive and simultaneous detection of different disease markers using multiplexed gold nanorods. Analytica Chimica Acta 755, 108114.Google Scholar
Kallestrup, P., Zinyama, R., Gomo, E., Butterworth, A. E., van Dam, G. J., Gerstoft, J., Erikstrup, C. and Ullum, H. (2006). Schistosomiasis and HIV in rural Zimbabwe: efficacy of treatment of schistosomiasis in individuals with HIV coinfection. Clinical Infectious Diseases 42, 17811789.Google Scholar
Kanamura, H. Y., Hancock, K., Rodrigues, V. and Damian, R. T. (2002). Schistosoma mansoni heat shock protein 70 elicits an early humoral immune response in S. mansoni infected baboons. Memorias do Instituto Oswaldo Cruz 97, 711716.Google Scholar
Kane, C. M., Cervi, L., Sun, J., McKee, A. S., Masek, K. S., Shapira, S., Hunter, C. A. and Pearce, E. J. (2004). Helminth antigens modulate TLR-initiated dendritic cell activation. Journal of Immunology 173, 74547461.Google Scholar
Kariuki, T. M., Van Dam, G. J., Deelder, A. M., Farah, I. O., Yole, D. S., Wilson, R. A. and Coulson, P. S. (2006). Previous or ongoing schistosome infections do not compromise the efficacy of the attenuated cercaria vaccine. Infection and Immunity 74, 39793986.Google Scholar
Karl, S., Gutierrez, L., Lucyk-Maurer, R., Kerr, R., Candido, R. R., Toh, S. Q., Saunders, M., Shaw, J. A., Suvorova, A., Hofmann, A., House, M. J., Woodward, R. C., Graeff-Teixera, C., St Pierre, T. G. and Jones, M. K. (2013). The iron distribution and magnetic properties of schistosome eggshells: implications for improved diagnostics. PLoS Neglected Tropical Diseases 7, e2219.Google Scholar
Karmakar, S., Zhang, W., Ahmad, G., Torben, W., Alam, M. U., Le, L., Damian, R. T., Wolf, R. F., White, G. L., Carey, D. W., Carter, D., Reed, S. G. and Siddiqui, A. A. (2014). Use of an Sm-p80-based therapeutic vaccine to kill established adult Schistosome parasites in chronically infected baboons. Journal of Infectious Diseases 209, 19291940.Google 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.Google Scholar
Kosinski, K. C., Adjei, M. N., Bosompem, K. M., Crocker, J. J., Durant, J. L., Osabutey, D., Plummer, J. D., Stadecker, M. J., Wagner, A. D., Woodin, M. and Gute, D. M. (2012). Effective control of Schistosoma haematobium infection in a Ghanaian community following installation of a water recreation area. PLoS Neglected Tropical Diseases 6, e1709.Google 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.Google Scholar
Lei, J. H., Su, B. T., Xu, H., Shen, J. L., Guan, X. H., Feng, Z. Q., Li, Y. L., Xu, M. X. and Liu, W. Q. (2011). Evaluation of an IgY-based immunomagnetic enzyme-linked immunosorbent assay system for detection of circulating Schistosoma japonicum antigen in serum samples from patients in China. American Journal of Tropical Medicine and Hygiene 85, 10541059.Google Scholar
Lei, J. H., Guan, F., Xu, H., Chen, L., Su, B. T., Zhou, Y., Wang, T., Li, Y. L. and Liu, W. Q. (2012). Application of an immunomagnetic bead ELISA based on IgY for detection of circulating antigen in urine of mice infected with Schistosoma japonicum . Veterinary Parasitology 187, 196202.Google Scholar
Li, G. F., Wang, Y., Zhang, Z. S., Wang, X. J., Ji, M. J., Zhu, X., Liu, F., Cai, X. P., Wu, H. W. and Wu, G. L. (2005). Identification of immunodominant Th1-type T cell epitopes from Schistosoma japonicum 28 kDa glutathione-S-transferase, a vaccine candidate. Acta Biochimca et Biophysica Sinica (Shanghai) 37, 751758.Google Scholar
Li, Y. S., McManus, D. P., Lin, D. D., Williams, G. M., Harn, D. A., Ross, A. G., Feng, Z. and Gray, D. J. (2014 a). The Schistosoma japonicum self-cure phenomenon in water buffaloes: potential impact on the control and elimination of schistosomiasis in China. International Journal for Parasitology 44, 167171.Google Scholar
Li, Y. S., McManus, D. P., Lin, D. D., Williams, G. M., Harn, D. A., Ross, A. G., Feng, Z. and Gray, D. J. (2014 b). The Schistosoma japonicum self-cure phenomenon in water buffaloes: potential impact on the control and elimination of schistosomiasis in China. International Journal for Parasitology 44, 167171.Google Scholar
Liang, Y. J., Luo, J., Lu, Q., Zhou, Y., Wu, H. W., Zheng, D., Ren, Y. Y., Sun, K. Y., Wang, Y. and Zhang, Z. S. (2012). Gene profile of chemokines on hepatic stellate cells of schistosome-infected mice and antifibrotic roles of CXCL9/10 on liver non-parenchymal cells. PLoS ONE 7, e42490.Google Scholar
Lier, T., Johansen, M. V., Hjelmevoll, S. O., Vennervald, B. J. and Simonsen, G. S. (2008). Real-time PCR for detection of low intensity Schistosoma japonicum infections in a pig model. Acta Tropica 105, 7480.Google Scholar
Lin, D., Tian, F., Wu, H., Gao, Y., Wu, J., Zhang, D., Ji, M., McManus, D. P., Driguez, P. and Wu, G. (2011 a). Multiple vaccinations with UV-attenuated cercariae in pig enhance protective immunity against Schistosoma japonicum infection as compared to single vaccination. Parasites and Vectors 4, 103.Google Scholar
Lin, D. D., Liu, Y. M., Hu, F., Li, Y. F., Tao, B., Yuan, M., Xie, S. Y., Huang, M. J., Jiang, Q. L., Li, J. Y., Gao, Z. L. and Wang, J. M. (2011 b). Evaluation on application of common diagnosis methods for schistosomiasis japonica in endemic areas of China. III. Analysis and evaluation of underestimation of prevalence of Schistosoma japonicum infection by routine Kato-Katz technique. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi 23, 642647.Google 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.Google Scholar
Liu, J. L., Fontaine, J., Capron, A. and Grzych, J. M. (1996). Ultrastructural localization of Sm28 GST protective antigen in Schistosoma mansoni adult worms. Parasitology 113 (Pt 4), 377391.Google Scholar
Liu, P., Shi, Y., Yang, Y., Cao, Y., Shi, Y., Li, H., Liu, J., Lin, J. and Jin, Y. (2012). Schistosoma japonicum UDP-glucose 4-epimerase protein is located on the tegument and induces moderate protection against challenge infection. PLoS One 7, e42050.Google Scholar
Liu, S., Song, G., Xu, Y., Yang, W. and McManus, D. P. (1995). Immunization of mice with recombinant Sjc26GST induces a pronounced anti-fecundity effect after experimental infection with Chinese Schistosoma japonicum . Vaccine 13, 603607.Google Scholar
Liu, J., Wang, J., Wang, S., Xu, B., Liu, X., Wang, X. and Hu, W. (2013). Molecular cloning and characterization of Schistosoma japonicum aldose reductase. Parasitology Research 112, 549558.Google Scholar
Loukas, A., Jones, M. K., King, L. T., Brindley, P. J. and McManus, D. P. (2001). Receptor for Fc on the surfaces of schistosomes. Infection and Immunity 69, 36463651.Google Scholar
Loukas, A., Tran, M. and Pearson, M. S. (2007). Schistosome membrane proteins as vaccines. International Journal for Parasitology 37, 257263.Google Scholar
Lu, Y., Xu, B., Ju, C., Mo, X., Chen, S., Feng, Z., Wang, X. and Hu, W. (2012 a). Identification and profiling of circulating antigens by screening with the sera from schistosomiasis japonica patients. Parasites and Vectors 5, 115.Google Scholar
Lu, Y., Xu, B., Ju, C., Mo, X. J., Chen, S. B., Feng, Z., Wang, X. N. and Hu, W. (2012 b). Cloning, expression and immunodiagnostic analysis of Schistosoma japonicum calcium-binding EF-hand domain containing protein. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi (Chinese Journal of Parasitology and Parasitic Diseases) 30, 165169.Google Scholar
Luo, X., Xie, H., Chen, D., Yu, X., Wu, F., Li, L., Wu, C. and Huang, J. (2014). Changes in NK and NKT cells in mesenteric lymph nodes after a Schistosoma japonicum infection. Parasitology Research 113, 10011009.Google Scholar
Luo, X. P., Chen, D. H., Xie, H. Y., Gao, Z. Y., Fang, H. L. and Huang, J. (2012). Immune response of Th17 cells in mesenteric lymph node of mice infected by Schistosoma japonicum . Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi (Chinese Journal of Parasitology and Parasitic Diseases), 30, 258261, 267.Google Scholar
McKee, A. S. and Pearce, E. J. (2004). CD25+CD4+ cells contribute to Th2 polarization during helminth infection by suppressing Th1 response development. Journal of Immunology 173, 12241231.Google Scholar
McManus, D. P. and Dalton, J. P. (2006). Vaccines against the zoonotic trematodes Schistosoma japonicum, Fasciola hepatica and Fasciola gigantica. Parasitology 133(Suppl), S43S61.Google Scholar
McManus, D. P. and Loukas, A. (2008). Current status of vaccines for schistosomiasis. Clinical Microbiology Reviews 21, 225242.Google Scholar
McManus, D. P., Gray, D. J., Li, Y., Feng, Z., Williams, G. M., Stewart, D., Rey-Ladino, J. and Ross, A. G. (2010). Schistosomiasis in the People's Republic of China: the era of the Three Gorges Dam. Clinical Microbiology Reviews 23, 442466.Google Scholar
McManus, D. P., Wong, J. Y., Zhou, J., Cai, C., Zeng, Q., Smyth, D., Li, Y., Kalinna, B. H., Duke, M. J. and Yi, X. (2001). Recombinant paramyosin (rec-Sj-97) tested for immunogenicity and vaccine efficacy against Schistosoma japonicum in mice and water buffaloes. Vaccine 20, 870878.Google Scholar
McWilliam, H. E., Piedrafita, D., Li, Y., Zheng, M., He, Y., Yu, X., McManus, D. P. and Meeusen, E. N. (2013). Local immune responses of the Chinese water buffalo, Bubalus bubalis, against Schistosoma japonicum larvae: crucial insights for vaccine design. PLoS Neglected Tropical Diseases 7, e2460.Google Scholar
Mentink-Kane, M. M. and Wynn, T. A. (2004). Opposing roles for IL-13 and IL-13 receptor alpha 2 in health and disease. Immunological Reviews 202, 191202.Google Scholar
Mo, A. X., Agosti, J. M., Walson, J. L., Hall, B. F. and Gordon, L. (2014). Schistosomiasis elimination strategies and potential role of a vaccine in achieving global health goals. American Journal of Tropical Medicine and Hygiene 90, 5460.Google Scholar
Modolell, M., Corraliza, I. M., Link, F., Soler, G. and Eichmann, K. (1995). Reciprocal regulation of the nitric oxide synthase/arginase balance in mouse bone marrow-derived macrophages by TH1 and TH2 cytokines. European Journal of Immunology 25, 11011104.Google Scholar
Murray, C. J., Vos, T., Lozano, R., Naghavi, M., Flaxman, A. D., Michaud, C., Ezzati, M., Shibuya, K., Salomon, J. A., Abdalla, S., Aboyans, V., Abraham, J., Ackerman, I., Aggarwal, R., Ahn, S. Y., Ali, M. K., Alvarado, M., Anderson, H. R., Anderson, L. M., Andrews, K. G., Atkinson, C., Baddour, L. M., Bahalim, A. N., Barker-Collo, S., Barrero, L. H., Bartels, D. H., Basanez, M. G., Baxter, A., Bell, M. L., Benjamin, E. J., et al. (2012). Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380, 21972223.Google Scholar
Obeng, B. B., Aryeetey, Y. A., de Dood, C. J., Amoah, A. S., Larbi, I. A., Deelder, A. M., Yazdanbakhsh, M., Hartgers, F. C., Boakye, D. A., Verweij, J. J., van Dam, G. J. and van Lieshout, L. (2008). Application of a circulating-cathodic-antigen (CCA) strip test and real-time PCR, in comparison with microscopy, for the detection of Schistosoma haematobium in urine samples from Ghana. Annals of Tropical Medicine and Parasitology 102, 625633.Google Scholar
Ohta, N., Kumagai, T., Maruyama, H., Yoshida, A., He, Y. and Zhang, R. (2004). Research on calpain of Schistosoma japonicum as a vaccine candidate. Parasitology International 53, 175181.Google Scholar
Pearce, E. J. and MacDonald, A. S. (2002). The immunobiology of schistosomiasis. Nature Reviews: Immunology 2, 499511.Google Scholar
Peng, J., Han, H., Hong, Y., Wang, Y., Guo, F., Shi, Y., Fu, Z., Liu, J., Cheng, G. and Lin, J. (2010). Cloning and expressing of cyclophilin B gene from Schistosoma japonicum and the analysis of immunoprotective effect. Sheng Wu Gong Cheng Xue Bao 26, 317323.Google Scholar
Qian, C. Y., Huang, B., Yu, C. X., Zhang, J., Yin, X. R., Wang, J., Song, L. J., Zhang, W. and Ke, X. D. (2011). Detection of the circulating antigen 14-3-3 protein of Schistosoma japonicum by time-resolved fluoroimmunoassay in rabbits. Parasites and Vectors 4, 95.Google Scholar
Qiu, C., Liu, S., Hong, Y., Fu, Z., Wei, M., Ai, D. and Lin, J. (2012). Molecular characterization of thyroid hormone receptor beta from Schistosoma japonicum and assessment of its potential as a vaccine candidate antigen against schistosomiasis in BALB/c mice. Parasites and Vectors 5, 172.Google Scholar
Rabello, A. and Enk, M. (2006). Progress towards the detection of schistosomiasis. In Report of the Scientific Working Group Meeting on Schistosomiasis for the Special Programme for Research and Training in Tropical Diseases (ed. WHO), pp. 6771. WHO, Geneva.Google Scholar
Reid, G. D., Sturrock, R. F., Harrison, R. A. and Tarara, R. P. (1995). Schistosoma haematobium in the baboon (Papio anubis): assessment of protection levels against either a single mass challenge or repeated trickle challenges after vaccination with irradiated schistosomula. Journal of Helminthology, 69, 139147.Google Scholar
Riner, D. K., Ferragine, C. E., Maynard, S. K. and Davies, S. J. (2013). Regulation of innate responses during pre-patent schistosome infection provides an immune environment permissive for parasite development. PLoS Pathogens 9, e1003708.Google Scholar
Ross, A. G., 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.Google Scholar
Sabin, E. A., Kopf, M. A. and Pearce, E. J. (1996). Schistosoma mansoni egg-induced early IL-4 production is dependent upon IL-5 and eosinophils. Journal of Experimental Medicine, 184, 18711878.Google Scholar
Schramm, G., Falcone, F. H., Gronow, A., Haisch, K., Mamat, U., Doenhoff, M. J., Oliveira, G., Galle, J., Dahinden, C. A. and Haas, H. (2003). Molecular characterization of an interleukin-4-inducing factor from Schistosoma mansoni eggs. Journal of Biological Chemistry 278, 1838418392.Google Scholar
Seto, E. Y., Remais, J. V., Carlton, E. J., Wang, S., Liang, S., Brindley, P. J., Qiu, D., Spear, R. C., Wang, L. D., Wang, T. P., Chen, H. G., Dong, X. Q., Wang, L. Y., Hao, Y., Bergquist, R. and Zhou, X. N. (2011). Toward sustainable and comprehensive control of schistosomiasis in China: lessons from Sichuan. PLoS Neglected Tropical Diseases 5, e1372.Google 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.Google Scholar
Shi, F., Zhang, Y., Ye, P., Lin, J., Cai, Y., Shen, W., 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.Google Scholar
Shuxian, L., Yongkang, H., Guangchen, S., Xing-song, L., Yuxin, X. and McManus, D. P. (1997). Anti-fecundity immunity to Schistosoma japonicum induced in Chinese water buffaloes (Bos buffelus) after vaccination with recombinant 26 kDa glutathione-S-transferase (reSjc26GST). Veterinary Parasitology 69, 3947.Google Scholar
Siddiqui, A. A., Pinkston, J. R., Quinlin, M. L., Saeed, Q., White, G. L., Shearer, M. H. and Kennedy, R. C. (2005). Characterization of the immune response to DNA vaccination strategies for schistosomiasis candidate antigen, Sm-p80 in the baboon. Vaccine 23, 14511456.Google Scholar
Siddiqui, A. A., Siddiqui, B. A. and Ganley-Leal, L. (2011). Schistosomiasis vaccines. Human Vaccines 7, 11921197.Google Scholar
Sun, L. P., Wang, W., Liang, Y. S., Tian, Z. X., Hong, Q. B., Yang, K., Yang, G. J., Dai, J. R. and Gao, Y. (2011). Effect of an integrated control strategy for schistosomiasis japonica in the lower reaches of the Yangtze River, China: an evaluation from 2005 to 2008. Parasites and Vectors 4, 243.Google Scholar
Tallima, H., Salah, M., Guirguis, F. R. and El Ridi, R. (2009). Transforming growth factor-beta and Th17 responses in resistance to primary murine Schistosomiasis mansoni . Cytokine 48, 239245.Google Scholar
Tang, H., Ming, Z., Liu, R., Xiong, T., Grevelding, C. G., Dong, H. and Jiang, M. (2013). Development of adult worms and granulomatous pathology are collectively regulated by T- and B-cells in mice infected with Schistosoma japonicum . PLoS ONE 8, e54432.Google Scholar
Taylor, M. G., Huggins, M. C., Shi, F., Lin, J., Tian, E., Ye, P., Shen, W., Qian, C. G., Lin, B. F. and Bickle, Q. D. (1998). Production and testing of Schistosoma japonicum candidate vaccine antigens in the natural ovine host. Vaccine 16, 12901298.Google Scholar
Tian, F., Lin, D., Wu, J., Gao, Y., Zhang, D., Ji, M. and Wu, G. (2010). Immune events associated with high level protection against Schistosoma japonicum infection in pigs immunized with UV-attenuated cercariae. PLoS ONE 5, e13408.Google Scholar
Vercruysse, J., Schetters, T. P., Knox, D. P., Willadsen, P. and Claerebout, E. (2007). Control of parasitic disease using vaccines: an answer to drug resistance? Revue Scientifique et Technique, Office International des Epizooties 26, 105115.Google Scholar
Wang, C., Chen, L., Yin, X., Hua, W., Hou, M., Ji, M., Yu, C. and Wu, G. (2011 a). Application of DNA-based diagnostics in detection of schistosomal DNA in early infection and after drug treatment. Parasites and Vectors 4, 164.Google Scholar
Wang, J., Yu, C. X., Yin, X. R., Zhang, W., Qian, C. Y., Song, L. J., Ke, X. D., Xu, Y. L., He, W. and Cao, G. Q. (2011 b). Monitoring specific antibody responses against the hydrophilic domain of the 23 kDa membrane protein of Schistosoma japonicum for early detection of infection in sentinel mice. Parasites and Vectors 4, 172.Google Scholar
Wang, S. P., Chen, X. C. and Gao, D. M. (2009). Research progress on schistosome vaccine and prospect of its application in China. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi (Chinese Journal of Parasitology and Parasitic Diseases) 27, 402411.Google Scholar
Wang, L., Liu, W., Yang, M., Peng, D. and Chen, L. (2013). Development of a Streptococcus gordonii vaccine strain expressing Schistosoma japonicum Sj-F1 and evaluation of using this strain for intranasal immunization in mice. Parasitology Research 112, 17011708.Google Scholar
Wang, J., Song, L. J., He, W., Yin, X. R., Qian, C. Y., Zhang, W., Xu, Y. L., Cao, G. Q., Ke, X. D. and Yu, C. X. (2012). Identification of early diagnostic molecules in soluble egg antigen of Schistosoma japonicum by MASS. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi 24, 132136.Google Scholar
Wang, T., Zhang, S., Wu, W., Zhang, G., Lu, D., Ornbjerg, N. and Johansen, M. V. (2006 a). Treatment and reinfection of water buffaloes and cattle infected with Schistosoma japonicum in Yangtze River Valley, Anhui province, China. Journal of Parasitology 92, 10881091.Google Scholar
Wang, X. H., Wu, X. H. and Zhou, X. N. (2006 b). Bayesian estimation of community prevalences of Schistosoma japonicum infection in China. International Journal for Parasitology 36, 895902.Google Scholar
Wen, X., He, L., Chi, Y., Zhou, S., Hoellwarth, J., Zhang, C., Zhu, J., Wu, C., Dhesi, S., Wang, X., Liu, F. and Su, C. (2011). Dynamics of Th17 cells and their role in Schistosoma japonicum infection in C57BL/6 mice. PLoS Neglected Tropical Diseases 5, e1399.Google Scholar
Wichmann, D., Panning, M., Quack, T., Kramme, S., Burchard, G. D., Grevelding, C. and Drosten, C. (2009). Diagnosing schistosomiasis by detection of cell-free parasite DNA in human plasma. PLoS Neglected Tropical Diseases 3, e422.Google Scholar
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.Google Scholar
Wilson, M. S., Mentink-Kane, M. M., Pesce, J. T., Ramalingam, T. R., Thompson, R. and Wynn, T. A. (2007). Immunopathology of schistosomiasis. Immunology and Cell Biology 85, 148154.Google Scholar
Wu, Z., Liu, S., Zhang, S., Tong, H., Gao, Z., Liu, Y., Lin, D., Liu, Z., Wu, G., Yi, H., Song, G. and Xu, Y. (2004). Persistence of the protective immunity to Schistosoma japonicum in Chinese yellow cattle induced by recombinant 26 kDa glutathione-S-transferase (reSjc26GST). Veterinary Parasitology 123, 167177.Google Scholar
Wu, Z. D., Lu, Z. Y. and Yu, X. B. (2005). Development of a vaccine against Schistosoma japonicum in China: a review. Acta Tropica 96, 106116.Google Scholar
Wu, X., Zhao, B., Hong, Y., Li, X., Peng, J., Zhang, J., Wang, F., Shi, Y., Fu, Z. and Lin, J. (2012). Characterization of Schistosoma japonicum estrogen-related receptor beta like 1 and immunogenicity analysis of the recombinant protein. Experimental Parasitology, 131, 383392.Google Scholar
Xiong, Y., Zhang, M., Hong, Y., Wei, M., Ai, D., Meng, P., Han, Y., Fu, Z., Shi, Y., Yang, J. and Lin, J. (2013). Characterization analysis of plasma membrane repair relative gene myoferlin. PLoS One, 8, e66396.Google Scholar
Xu, J., Feng, T., Lin, D. D., Wang, Q. Z., Tang, L., Wu, X. H., Guo, J. G., Peeling, R. W. and Zhou, X. N. (2011 a). Performance of a dipstick dye immunoassay for rapid screening of Schistosoma japonicum infection in areas of low endemicity. Parasites and Vectors 4, 87.Google Scholar
Xu, B., Ju, C., Lu, Y., Mo, X. J., Feng, Z., Xu, X. N. and Hu, W. (2011 b). Cloning and expression of metalloprotease gene from Schistosoma japonicum and its immunoprotective efficiency. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi (Chinese Journal of Parasitology and Parasitic Diseases) 29, 8186.Google Scholar
Xu, B., Gordon, C. A., Hu, W., McManus, D. P., Chen, H. G., Gray, D. J., Ju, C., Zeng, X. J., Gobert, G. N., Ge, J., Lan, W. M., Xie, S. Y., Jiang, W. S., Ross, A. G., Acosta, L. P., Olveda, R. and Feng, Z. (2012). A novel procedure for precise quantification of Schistosoma japonicum eggs in bovine feces. PLoS Neglected Tropical Diseases 6, e1885.Google Scholar
Xu, J., Rong, R., Zhang, H. Q., Shi, C. J., Zhu, X. Q. and Xia, C. M. (2010). Sensitive and rapid detection of Schistosoma japonicum DNA by loop-mediated isothermal amplification (LAMP). International Journal for Parasitology 40, 327331.Google Scholar
Xu, J., Liu, A. P., Guo, J. J., Wang, B., Qiu, S. J., Sun, H., Guan, W., Zhu, X. Q., Xia, C. M. and Wu, Z. D. (2013). The sources and metabolic dynamics of Schistosoma japonicum DNA in serum of the host. Parasitology Research 112, 129133.Google Scholar
Xu, X., Zhang, Y., Lin, D., Zhang, J., Xu, J., Liu, Y. M., Hu, F., Qing, X., Xia, C. and Pan, W. (2014). Serodiagnosis of Schistosoma japonicum infection: genome-wide identification of a protein marker, and assessment of its diagnostic validity in a field study in China. Lancet Infectious Diseases 14, 489497.Google Scholar
Yang, J., Fu, Z., Feng, X., Shi, Y., Yuan, C., Liu, J., Hong, Y., Li, H., Lu, K. and Lin, J. (2012). Comparison of worm development and host immune responses in natural hosts of Schistosoma japonicum, yellow cattle and water buffalo. BMC Veterinary Research 8, 25.Google Scholar
You, H., Zhang, W., Moertel, L., McManus, D. P. and Gobert, G. N. (2009). Transcriptional profiles of adult male and female Schistosoma japonicum in response to insulin reveal increased expression of genes involved in growth and development. International Journal for Parasitology 39, 15511559.Google Scholar
You, H., Gobert, G. N., Duke, M. G., Zhang, W., Li, Y., Jones, M. K. and McManus, D. P. (2012). The insulin receptor is a transmission blocking veterinary vaccine target for zoonotic Schistosoma japonicum . International Journal for Parasitology 42, 801807.Google Scholar
You, H., Stephenson, R. J., Gobert, G. N. and McManus, D. P. (2014). Revisiting glucose uptake and metabolism in schistosomes: new molecular insights for improved schistosomiasis therapies. Frontiers in Genetics 5, 176.Google Scholar
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 . Nature Genetics 44, 221225.Google Scholar
Yu, L. L., Ding, J. Z., Wen, L. Y., Lou, D., Yan, X. L., Lin, L. J., Lu, S. H., Lin, D. D. and Zhou, X. N. (2011). Development of a rapid dipstick with latex immunochromatographic assay (DLIA) for diagnosis of schistosomiasis japonica. Parasites and Vectors 4, 157.Google Scholar
Yu, X. L., He, Y. K., Xiong, T., Zhao, Y. Q., Shi, M. Z., Zhou, J., Liu, Z. C., Luo, X. S., Fu, X., He, H. B., Harn, D. A. and Li, Y. S. (2006). Protective effects of co-immunization with SjCTPI-Hsp70 and interleukin-12 DNA vaccines against Schistosoma japonicum challenge infection in water buffalo. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi (Chinese Journal of Parasitology and Parasitic Diseases) 24, 433436.Google Scholar
Yu, Q., Yang, H., Feng, Y., Yang, X. and Zhu, Y. (2012 a). Magnetic affinity enzyme-linked immunoassay based on recombinant 26 kDa glutathione-S-transferase for serological diagnosis of schistosomiasis japonica. Acta Tropica 124, 199202.Google Scholar
Yu, Q., Yang, H., Feng, Y., Zhu, Y. and Yang, X. (2012 b). Magnetic affinity enzyme-linked immunoassay for diagnosis of Schistosomiasis japonicum in persons with low-intensity infection. American Journal of Tropical Medicine and Hygiene 87, 689693.Google Scholar
Yu, Q., Yang, H., Guan, F., Feng, Y., Yang, X. and Zhu, Y. (2014). Detection of IgG in sera of patients with schistosomiasis japonica by developing magnetic affinity enzyme-linked immunoassay based on recombinant 14-3-3 protein. Transactions of the Royal Society of Tropical Medicine and Hygiene 108, 3741.CrossRefGoogle ScholarPubMed
Zaccone, P., Fehervari, Z., Jones, F. M., Sidobre, S., Kronenberg, M., Dunne, D. W. and Cooke, A. (2003). Schistosoma mansoni antigens modulate the activity of the innate immune response and prevent onset of type 1 diabetes. European Journal of Immunology, 33, 14391449.Google Scholar
Zhang, X., Gao, Y. N., Hou, M., Chen, L., Ji, M. J. and Wu, G. L. (2011). Antibody responses to leucine aminopeptidase in Schistosoma japonicum infection. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi 23, 163167.Google Scholar
Zhang, X. B., Hu, F., Xie, S. Y., Tao, B., Yuan, M., Liu, Y. M., Li, J. Y., Li, Z. J. and Lin, D. D. (2012 a). Field application of antibody detection in a low transmission area of Schistosoma japonicum . Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi (Chinese Journal of Parasitology and Parasitic Diseases) 30, 468473.Google Scholar
Zhang, Y., Chen, L., Gao, W., Hou, X., Gu, Y., Gui, L., Huang, D., Liu, M., Ren, C., Wang, S. and Shen, J. (2012 b). IL-17 neutralization significantly ameliorates hepatic granulomatous inflammation and liver damage in Schistosoma japonicum infected mice. European Journal of Immunology 42, 15231535.Google Scholar
Zhang, Z., Xu, H., Gan, W., Zeng, S. and Hu, X. (2012 c). Schistosoma japonicum calcium-binding tegumental protein SjTP22.4 immunization confers praziquantel schistosomulumicide and antifecundity effect in mice. Vaccine 30, 51415150.Google Scholar
Zhang, M., Han, Y., Zhu, Z., Li, D., Hong, Y., Wu, X., Fu, Z. and Lin, J. (2012 d). Cloning, expression, and characterization of Schistosoma japonicum tegument protein phosphodiesterase-5. Parasitology Research 110, 775786.Google Scholar
Zhang, R., Yoshida, A., Kumagai, T., Kawaguchi, H., Maruyama, H., Suzuki, T., Itoh, M., El-Malky, M. and Ohta, N. (2001). Vaccination with calpain induces a Th1-biased protective immune response against Schistosoma japonicum . Infection and Immunity 69, 386391.Google Scholar
Zhou, X. H., Wu, J. Y., Huang, X. Q., Kunnon, S. P., Zhu, X. Q. and Chen, X. G. (2010). Identification and characterization of Schistosoma japonicum Sjp40, a potential antigen candidate for the early diagnosis of schistosomiasis. Diagnostic Microbiology and Infectious Disease 67, 337345.Google Scholar
Zhou, Y. B., Yang, M. X., Wang, Q. Z., Zhao, G. M., Wei, J. G., Peng, W. X. and Jiang, Q. W. (2007). Field comparison of immunodiagnostic and parasitological techniques for the detection of Schistosomiasis japonica in the People's Republic of China. American Journal of Tropical Medicine and Hygiene 76, 11381143.Google Scholar
Zhou, Y., Zheng, H., Chen, Y., Zhang, L., Wang, K., Guo, J., Huang, Z., Zhang, B., Huang, W., Jin, K., Dou, T., Hasegawa, M., Wang, L., Zhang, Y., Zhou, J., Tao, L., Cao, Z., Li, Y., Vinar, T., Brejova, B., Brown, D., Li, M., Miller, D. J., Blair, D., Zhong, Y., Chen, Z., Liu, F., Hu, W., Wang, Z. Q., Zhang, Q. H., et al. (2009). The Schistosoma japonicum genome reveals features of host–parasite interplay. Nature 460, 345351.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.Google Scholar
Zhu, Y., Si, J., Ham, D. A., Yu, C., He, W., Hua, W., Yin, X., Liang, Y., Xu, M. and Xu, R. (2002). The protective immunity produced in infected C57BL/6 mice of a DNA vaccine encoding Schistosoma japonicum Chinese strain triose-phosphate isomerase. Southeast Asian Journal of Tropical Medicine and Public Health 33, 207213.Google 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.Google Scholar
Zhu, Y. C. (2005). Immunodiagnosis and its role in schistosomiasis control in China: a review. Acta Tropica 96, 130136.Google Scholar
Zhu, Z., Fu, Z., Zhang, M., Han, Y., Hong, Y., Li, D., Zhao, Z., Shi, Y., Li, X. and Lin, J. (2012). Protective efficacy evaluation induced by recombinant protein LHD-Sj23-GST of Schistosoma japonicum emulsified with three different adjuvants. Parasite Immunology 34, 341344.Google Scholar