Skip to main content

Advertisement

SpringerLink
Log in

Proteomic analysis of schistosomiasis japonica vaccine candidate antigens recognized by UV-attenuated cercariae-immunized porcine serum IgG2

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Many studies have showed that the radiation-attenuated cercariae (RAC) vaccine could induce the high protection of laboratory animals to resist the schistosoma infection by cellular and humoral mechanism. Here, we aimed to identify possible vaccine antigens by using specific IgG2 antibody from RAC-vaccinated pigs or vaccination and challenge pigs. The antigens from the schistosomal soluble worm antigen preparation (SWAP) recognized by the porcine IgG2 antibody were obtained using immunoprecipitation technique. These antigens were separated by 2-D electrophoresis, and 116 spots were successfully identified by MALDI-TOF MS from about 400 putative spots in gels. Among these spots, 113 spots could match to the Schistosoma japonicum. These identified proteins in four groups were classified by Gene Ontology (Go) database, and the mainly functions of these proteins were involved in binding, catalytic activity (thioredoxin peroxidase-2, et al.), signal transduction class (MAP Kinase, et al.), cell process (the heat shock 70-kDa protein 9B, et al.), and the intracellular component (tektin, et al.). Our methods suggested that it was possible to pull-down the interesting proteins recognized by specific antibodies. Our results may provide new clues for exploring the mechanism of high protection induced by RAC and shed some light on the research for anti-schistosomiasis japonica vaccine.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abdel-Hafeez EH, Kikuchi M, Watanabe K, Ito T, Yu C, Chen H, Nara T, Arakawa T, Aoki Y, Hirayama K (2009) Proteome approach for identification of schistosomiasis japonica vaccine candidate antigen. Parasitol Int 58:36–44

    Article  PubMed  CAS  Google Scholar 

  • Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25:25–29

    Article  PubMed  CAS  Google Scholar 

  • Bergquist NR, Colley DG (1998) Schistosomiasis vaccine:research to development. Parasitol Today 14:99–104

    Article  PubMed  CAS  Google Scholar 

  • Bickle QD (2009) Radiation-attenuated schistosome vaccination—a brief historical perspective. Parasitology 136:1621–1632

    Article  PubMed  CAS  Google Scholar 

  • Blanc JF, Lalanne C, Plomion C, Schmitter JM, Bathany K, Gion JM, Bioulac-Sage P, Balabaud C, Bonneu M, Rosenbaum J (2005) Proteomic analysis of differentially expressed proteins in hepatocellular carcinoma developed in patients with chronic viral hepatitis C. Proteomics 5:3778–3789

    Article  PubMed  CAS  Google Scholar 

  • Braschi S, Curwen RS, Ashton PD, Verjovski-Almeida S, Wilson A (2006) The tegument surface membranes of the human blood parasite Schistosoma mansoni: a proteomic analysis after differential extraction. Proteomics 6:1471–1482

    Article  PubMed  CAS  Google Scholar 

  • Crawley A, Wilkie BN (2003) Porcine Ig isotypes: function and molecular characteristics. Vaccine 21:2911–2922

    Article  PubMed  CAS  Google Scholar 

  • Crawley A, Raymond C, Wilkie BN (2003) Control of immunoglobulin isotype production by porcine B-cells cultured with cytokines. Vet Immunol Immunopathol 91:141–154

    Article  PubMed  CAS  Google Scholar 

  • Curwen RS, Ashton PD, Johnston DA, Wilson RA (2004) The Schistosoma mansoni soluble proteome: a comparison across four life-cycle stages. Mol Biochem Parasitol 138:57–66

    Article  PubMed  CAS  Google Scholar 

  • Curwen RS, Ashton PD, Sundaralingam S, Wilson RA (2006) Identification of novel proteases and immunomodulators in the secretions of schistosome cercariae that facilitate host entry. Mol Cell Proteomics 5:835–844

    Article  PubMed  CAS  Google Scholar 

  • De M (1995) How schistosomes profit from the stress responses they elicit in their hosts. Adv Parasitol 35:177–256

    Article  Google Scholar 

  • Foster N, Elsheikha HM (2012) The immune response to parasitic helminths of veterinary importance and its potential manipulation for future vaccine control strategies. Parasitol Res 110:1587–1599

    Article  PubMed  Google Scholar 

  • Gorg A, Obermaier C, Boguth G, Harder A, Scheibe B, Wildgruber R, Weiss W (2000) The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 21:1037–1053

    Article  PubMed  CAS  Google Scholar 

  • Harris MA, Clark J, Ireland A, Lomax J, Ashburner M et al (2004) The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res 32:D258–D261

    Article  PubMed  CAS  Google Scholar 

  • Hewitson JP, Hamblin PA, Mountford AP (2005) Immunity induced by the radiation-attenuated schistosome vaccine. Parasite Immunol 27:271–280

    Article  PubMed  CAS  Google Scholar 

  • Hide M, Ritleng AS, Brizard JP, Monte-Allegre A, Sereno D (2008) Leishmania infantum: tuning digitonin fractionation for comparative proteomic of the mitochondrial protein content. Parasitol Res 103:989–992

    Article  PubMed  CAS  Google Scholar 

  • Hong Y, Han Y, Fu Z, Han H, Qiu C, Zhang M, Yang J, Shi Y, Li X, Lin J (2013) Characterization and expression of the Schistosoma japonicum thioredoxin peroxidase-2 gene. J Parasitol 99:68–76

    Article  PubMed  CAS  Google Scholar 

  • Hou HB, Li YL (2003) Screening of protective antigen from Schistosoma japonicum cercariae attenuated by ultraviole irradiation. J Trop Med 3:149–151

    CAS  Google Scholar 

  • Huang KY, Chien KY, Lin YC, Hsu WM, Fong IK, Huang PJ, Yueh YM, Gan RR, Tang P (2009) A proteome reference map of Trichomonas vaginalis. Parasitol Res 104:927–933

    Article  PubMed  Google Scholar 

  • Kim J, Bae SS, Sung MH, Lee KH, Park SJ (2009) Comparative proteomic analysis of trophozoites versus cysts of Giardia lamblia. Parasitol Res 104:475–479

    Article  PubMed  Google Scholar 

  • Kumagai T, Osada Y, Kanazawa T (2006) 2-Cys peroxiredoxins from Schistosoma japonicum: the expression profile and localization in the life cycle. Mol Biochem Parasitol 149:135–143

    Article  PubMed  CAS  Google Scholar 

  • Kwatia MA, Botkin DJ, Williams DL (2000) Molecular and enzymatic characterization of Schistosoma mansoni thioredoxin peroxidase. J Parasitol 86:908–915

    PubMed  CAS  Google Scholar 

  • Laschuk A, Monteiro KM, Vidal NM, Pinto PM, Duran R, Cervenanski C, Zaha A, Ferreira HB (2011) Proteomic survey of the cestode Mesocestoides corti during the first 24 hours of strobilar development. Parasitol Res 108:645–656

    Google Scholar 

  • Lei ZL, Zheng H, Zhang LJ, Zhu R, Guo JG, Li SZ, Wang LY, Chen Z, Zhou XN (2011) Schistosomiasis status in People's Republic of China in 2010. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi 23:599–604

    PubMed  Google Scholar 

  • Lin D, Tian F, Wu H, Gao Y, Wu J, Zhang D, Ji M, McManus DP, Driguez P, Wu G (2011) Multiple vaccinations with UV-attenuated cercariae in pig enhance protective immunity against Schistosoma japonicum infection as compared to single vaccination. Parasit Vectors 4:103

    Article  PubMed  Google Scholar 

  • Liu F, Lu J, Hu W, Wang SY, Cui SJ, Chi M, Yan Q, Wang XR, Song HD, Xu XN, Wang JJ, Zhang XL, Zhang X, Wang ZQ, Xue CL, Brindley PJ, McManus DP, Yang PY, Feng Z, Chen Z, Han ZG (2006) New perspectives on host-parasite interplay by comparative transcriptomic and proteomic analyses of Schistosoma japonicum. PLoS Pathog 2:e29

    Article  PubMed  Google Scholar 

  • Lu ZY, Wang SP, Peng XC, Liu LP, Li WK, Xu SR, Zhou SH, Yu JL, Dai C, Jiang XX, Qin XX, Zeng SH (2005) Immune reactivity between the stage-specific antigenic components from Schistosoma japonicum and the immune sere from rabbits vaccinated with irradiated cercariae. Chin J zoonoses 21:197–201

    Google Scholar 

  • Lu ZY, Yang LL, Hu SM, Sun X et al (2009) Expression profile, localization of an 8-kDa calcium-binding protein from Schistosoma japonicum (SjCa8), and vaccine potential of recombinant SjCa8 (rSjCa8) against infections in mice. Parasitol Res 104:733–743

    Article  Google Scholar 

  • Mathieson W, Wilson RA (2010) A comparative proteomic study of the undeveloped and developed Schistosoma mansoni egg and its contents: the miracidium, hatch fluid and secretions. Int J Parasitol 40:617–628

    Article  PubMed  CAS  Google Scholar 

  • McManus DP, Loukas A (2008) Current status of vaccines for schistosomiasis. Clin Microbiol Rev 21:225–242

    Article  PubMed  CAS  Google Scholar 

  • Mortz E, Krogh TN, Vorum H, Gorg A (2001) Improved silver staining protocols for high sensitivity protein identification using matrix-assisted laser desorption/ionization-time of flight analysis. Proteomics 1:1359–1363

    Article  PubMed  CAS  Google Scholar 

  • Neumann S, Ziv E, Lantner F, Schechter I (1993) Regulation of HSP70 gene expression during the life cycle of the parasitic helminth Schistosoma mansoni. Eur J Biochem 212:589–596

    Article  PubMed  CAS  Google Scholar 

  • Pearce EJ, MacDonald AS (2002) The immunobiology of schistosomiasis. Nat Rev Immunol 2:499–511

    Article  PubMed  CAS  Google Scholar 

  • Richter D, Harn DA (1993) Candidate vaccine antigens identified by antibodies from mice vaccinated with 15- or 50-kilorad-irradiated cercariae of Schistosoma mansoni. Infect Immun 61:146–154

    PubMed  CAS  Google Scholar 

  • Ruppel A, Shi YE, Moloney NA (1990) Schistosoma mansoni and S. japonicum: comparison of levels of ultraviolet irradiation for vaccination of mice with cercariae. Parasitology 101(Pt 1):23–26

    Article  PubMed  Google Scholar 

  • Shi YE, Jiang CF, Han JJ, Li Y, Ruppel A (1990) Schistosoma japonicum: an ultraviolet-attenuated cercarial vaccine applicable in the field for water buffaloes. Exp Parasitol 71:100–106

    Article  PubMed  CAS  Google Scholar 

  • Sotillo J, Valero ML, Sanchez MM, Fried B, Esteban JG, Marcilla A, Toledo R (2010) Excretory/secretory proteome of the adult stage of Echinostoma caproni. Parasitol Res 107:691–697

    Article  PubMed  Google Scholar 

  • Srivastava P (2002) Roles of heat-shock proteins in innate and adaptive immunity. Nat Rev Immunol 2:185–194

    Article  PubMed  CAS  Google Scholar 

  • Tetsch L, Bend J, Holker U (2006) Molecular and enzymatic characterisation of extra- and intracellular laccases from the acidophilic ascomycete Hortaea acidophila. Antonie Van Leeuwenhoek 90:183–194

    Article  PubMed  CAS  Google Scholar 

  • Tian F, Lin D, Wu J, Gao Y, Zhang D, Ji M, 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

    Article  PubMed  Google Scholar 

  • Todryk SM, Melcher AA, Dalgleish AG, Vile RG (2000) Heat shock proteins refine the danger theory. Immunology 99:334–337

    Article  PubMed  CAS  Google Scholar 

  • Torben W, Hailu A (2007) Serum cytokines of the 20 Krad-irradiated S. mansoni cercariae vaccinated, primary and superinfected Cercopethicus aethiops aethiops. Exp Parasitol 115:121–126

    Article  PubMed  CAS  Google Scholar 

  • Van Hellemond JJ, Retra K, Brouwer JF, van Balkom BW, Yazdanbakhsh M, Shoemaker CB, Tielens AG (2006) Functions of the tegument of schistosomes: clues from the proteome and lipidome. Int J Parasitol 36:691–699

    Article  PubMed  Google Scholar 

  • Verjovski-Almeida S, DeMarc R (2008) Current developments on Schistosoma proteomics. Acta Trop 108:183–185

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Yang Z, Li Y, Yu F, Brindley PJ, McManus DP, Wei D, Han Z, Feng Z, Hu W (2006) Reconstruction and in silico analysis of the MAPK signaling pathways in the human blood fluke, Schistosoma japonicum. FEBS Lett 580:3677–3686

    Article  PubMed  CAS  Google Scholar 

  • Wen X, He L, Chi Y, Zhou S, Hoellwarth J, Zhang C, Zhu J, Wu C, Dhesi S, Wang X, Liu F, Su C (2011) Dynamics of Th17 cells and their role in Schistosoma japonicum infection in C57BL/6 mice. PLoS Negl Trop Dis 5:e1399

    Article  PubMed  CAS  Google Scholar 

  • WHO Expert Committee (2002) Prevention and control of schistosomiasis and soil-transmitted helminthiasis. World Health Organ Tech Rep Ser 912(i–vi):1–57

  • Wu XJ, Sabat G, Brown JF, Zhang M, Taft A, Peterson N, Harms A, Yoshino TP (2009) Proteomic analysis of Schistosoma mansoni proteins released during in vitro miracidium-to-sporocyst transformation. Mol Biochem Parasitol 164:32–44

    Article  PubMed  CAS  Google Scholar 

  • Yang LL, Lv ZY, Hu SM, He SJ, Li ZY, Zhang SM, Zheng HQ, Li MT, Yu XB, Fung MC, Wu ZD (2009) Schistosoma japonicum: proteomics analysis of differentially expressed proteins from ultraviolet-attenuated cercariae compared to normal cercariae. Parasitol Res 105:237–248

    Article  PubMed  Google Scholar 

  • Yang J, Yang L, Lv Z, Wang J, Zhang Q, Zheng H, Wu ZD (2012) Molecular cloning and characterization of a HSP70 gene from Schistosoma japonicum. Parasitol Res 110:1785–1793

    Article  PubMed  Google Scholar 

  • Zhang Y, Taylor MG, McCrossan MV, Bickle QD (1999) Molecular cloning and characterization of a novel Schistosoma japonicum "irradiated vaccine-specific" antigen, Sj14-3-3. Mol Biochem Parasitol 103:25–34

    Article  PubMed  CAS  Google Scholar 

  • Zhang M, Han Y, Zhu Z, Li D, Hong Y, Wu X, Fu Z, Lin J (2012) Cloning, expression, and characterization of Schistosoma japonicum tegument protein phosphodiesterase-5. Parasitol Res 110:775–786

    Article  PubMed  Google Scholar 

  • Zheng M, Hu K, Liu W, Li H, Chen J, Yu X (2011) Proteomic analysis of different period excretory secretory products from Clonorchis sinensis adult worms: molecular characterization, immunolocalization, and serological reactivity of two excretory secretory antigens-methionine aminopeptidase 2 and acid phosphatase. Parasitol Res 112:1287–1297

    Article  Google Scholar 

  • Zugel U, Kaufmann SH (1999) Immune response against heat shock proteins in infectious diseases. Immunobiology 201:22–35

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We appreciate Lin Wang, Fuqiang Wang from the Analysis and Test Center of Nanjing Medical University for the technical support for 2D electrophoresis and MS analysis. This work was supported by the National Natural Science Foundation of China (NSFC) (Project No.81171593, No.81101625) and Open Research Fund of Key Laboratory on Technology for Parasitic Diseases and Control, Ministry of Health, Jiangsu institute of Parasitic Diseases.

Conflict of interest

The authors declare that they have no conflicting financial interest.

Author information

Authors and Affiliations

  1. Department of Pathogen Biology& Immunology, Nanjing Medical University, Nanjing, Jiangsu, 210029, China

    Fang Tian, Min Hou, Lin Chen, Yanan Gao, Xia Zhang, Minjun Ji & Guanling Wu

  2. Jiangsu Province Key Laboratory of Modern Pathogen Biology, Nanjing, Jiangsu, 210029, China

    Min Hou, Lin Chen, Minjun Ji & Guanling Wu

  3. Department of Pathogen Biology and Immunology, Yangzhou University Medical College, Yangzhou, Jiangsu, 225001, China

    Fang Tian

Authors
  1. Fang Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Min Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yanan Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xia Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Minjun Ji
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Guanling Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Minjun Ji.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tian, F., Hou, M., Chen, L. et al. Proteomic analysis of schistosomiasis japonica vaccine candidate antigens recognized by UV-attenuated cercariae-immunized porcine serum IgG2. Parasitol Res 112, 2791–2803 (2013). https://doi.org/10.1007/s00436-013-3447-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-013-3447-7

Keywords

Search

Navigation