• 1.

    Kloos H, David R, 2002. The paleoepidemiology of schistosomiasis in ancient Egypt. Hum Ecol Rev 9: 1425.

  • 2.

    WHO Fact Sheet on Schistosomiasis, 2010. Schistosomiasis. Available at: http://www.who.int/mediacentre/factsheets/fs115/en/index.html#. Accessed February 2, 2011.

    • Search Google Scholar
    • Export Citation
  • 3.

    Olveda RM, 2001. Disease in schistosomiasis japonica. Mahmoud A, ed. Schistosomiasis. London, UK: Imperial College Press, 361385.

  • 4.

    Zhang YY, Luo JP, Liu YM, Wang QZ, Chen JH, Xu MX, Xu JM, Wu J, Tu XM, Wu GL, Zhang ZS, Wu HW, 2009. Evaluation of Kato-Katz examination method in three areas with low-level endemicity of schistosomiasis japonica in China: a Bayesian modeling approach. Acta Trop 112: 1622.

    • Search Google Scholar
    • Export Citation
  • 5.

    Lier T, Simonsen GS, Wang T, Lu D, Haukland HH, Vennervald BJ, Johansen MV, 2009. Low sensitivity of the formol-ethyl acetate sedimentation concentration technique in low-intensity Schistosoma japonicum infections. PLoS Negl Trop Dis 3: e386.

    • Search Google Scholar
    • Export Citation
  • 6.

    Yu JM, de Vlas SJ, Jiang QW, Gryseels B, 2007. Comparison of the Kato-Katz technique, hatching test and indirect hemagglutination assay (IHA) for the diagnosis of Schistosoma japonicum infection in China. Parasitol Int 57: 4549.

    • Search Google Scholar
    • Export Citation
  • 7.

    Doenhoff MJ, Chiodini PL, Hamilton JV, 2004. Specific and sensitive diagnosis of schistosome infection: can it be done with antibodies? Trends Parasitol 20: 3539.

    • Search Google Scholar
    • Export Citation
  • 8.

    Wu G, 2002. A historical perspective on the immunodiagnosis of schistosomiasis in China. Acta Trop 82: 193198.

  • 9.

    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 DJ, Blair D, Zhong Y, Chen Z, Liu F, Wei H, Wang ZQ, Zhang QH, Song HD, Chen S, Xu X, Xu B, Ju C, Huang Y, Brindley PJ, McManus DP, Feng Z, Han ZG, Lu G, Ren S, Wang Y, Gu W, Kang H, Chen J, Chen X, Chen S, Wang L, Yan J, Wang B, Lu X, Jin L, Wang B, Pu S, Zhang X, Zhang W, Hu Q, Zhu G, Wang J, Yang H, Ning Z, Beriman M, Wei CL, Ruan Y, Zhao G, Wang S, 2009. The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 460: 345356.

    • Search Google Scholar
    • Export Citation
  • 10.

    Dzik J, 2006. Molecules released by helminth parasites involved in host colonization. Acta Biochim Pol 53: 3364.

  • 11.

    Chiumento L, Bruschi F, 2009. Enzymatic antioxidant systems in helminth parasites. Parasitol Res 105: 593603.

  • 12.

    Kang SW, Baines IC, Rhee SG, 1998. Characterization of mammalian peroxiredoxin that contains one conserved cysteine. J Biol Chem 273: 63036311.

    • Search Google Scholar
    • Export Citation
  • 13.

    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: 135143.

    • Search Google Scholar
    • Export Citation
  • 14.

    Mulvenna J, Moertel L, Jones MK, Nawaratna S, Lovas EM, Gobert GN, Colgrave M, Jones A, Loukas A, McManus DP, 2010. Exposed proteins of the Schistosoma japonicum tegument. Int J Parasitol 40: 543554.

    • Search Google Scholar
    • Export Citation
  • 15.

    Jin Y, Lu K, Zhou WF, Fu ZQ, Liu JM, Shi YJ, Li H, Lin JJ, 2010. Comparison of recombinant proteins from Schistosoma japonicum for schistosomiasis diagnosis. Clin Vaccine Immunol 17: 476480.

    • Search Google Scholar
    • Export Citation
  • 16.

    Goto Y, Carter D, Gedurian J, Inoue N, Kawazu S, Reed SG, 2010. Upregulated expression of B-cell antigen family tandem repeat proteins by Leishmania amastigotes. Infect Immun 78: 21382145.

    • Search Google Scholar
    • Export Citation
  • 17.

    Kim TY, Kang SY, Ahn IY, Cho SY, Hong SJ, 2001. Molecular cloning and characterization of an antigenic protein with a repeating region from Clonorchis sinensis. Korean J Parasitol 39: 5766.

    • Search Google Scholar
    • Export Citation
  • 18.

    Goto Y, Coler RN, Reed SG, 2007. Bioinformatic identification of tandem repeat antigens of the Leishmania donovani complex. Infect Immun 75: 846851.

    • Search Google Scholar
    • Export Citation
  • 19.

    Goto Y, Duthie MS, Kawazu S, Inoue N, Carter D, 2011. Biased cellular locations of tandem repeat antigens in African trypanosomes. Biochem Biophys Res Commun 405: 434438.

    • Search Google Scholar
    • Export Citation
  • 20.

    Goto Y, Carter D, Reed SG, 2008. Immunological dominance of Trypanosoma cruzi tandem repeat proteins. Infect Immun 76: 39673974.

  • 21.

    Kirinoki M, Hu M, Yokoi H, Chigusa Y, Matsuda H, 2003. Immunoblot analysis of Schistosoma japonicum egg antigens with sera from patients with acute and chronic schistosomiasis japonica. Southeast Asian J Trop Med Public Health 34: 702707.

    • Search Google Scholar
    • Export Citation
  • 22.

    Kirinoki M, Chigusa Y, Ohmae H, Sinuon M, Socheat D, Matsumoto J, Kitikoon V, Matsuda H, 2011. Efficacy of sodium metaperiodate (SMP)-ELISA for the serodiagnosis of schistosomiasis mekongi. Southeast Asian J Trop Med Public Health 42: 2533.

    • Search Google Scholar
    • Export Citation
  • 23.

    Nara T, Iizumi K, Ohmae H, Sy OS, Tsubota S, Inaba Y, Tsubouchi A, Tanabe M, Kojima S, Aoki T, 2007. Antibody isotype responses to paramyosin, a vaccine candidate for schistosomiasis, and their correlations with resistance and fibrosis in patients infected with Schistosoma japonicum in Leyte, The Philippines. Am J Trop Med Hyg 76: 384391.

    • Search Google Scholar
    • Export Citation
  • 24.

    Hertz-Fowler C, Peacock CS, Wood V, Aslett M, Kerhornou A, Mooney P, Tivey A, Berriman M, Hall N, Rutherford K, Parkhill J, Ivens AC, Rajandream MA, Barrell B, 2004. GeneDB: a resource for prokaryotic and eukaryotic organisms. Nucleic Acids Res 32: D339D343.

    • Search Google Scholar
    • Export Citation
  • 25.

    Benson G, 1999. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27: 573580.

  • 26.

    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 perspective on host-parasite interplay by comparative transcriptomic and proteomic analyses of Schistosoma japonicum. PLoS Pathog 2: e29.

    • Search Google Scholar
    • Export Citation
  • 27.

    Wellcome Trust Sanger Institute, Pathogen Sequencing Unit, GeneDB. http:/www.genedb.org/. Accessed July 13, 2010.

  • 28.

    Matsuda H, Tanaka H, Blas BL, Nosenas JS, Tokawa T, Ohsawa S, 1984. Evaluation of ELISA with ABTS, 2-2'-azino-di-(3-ethylbenzthiazoline sulfonic acid), as the substrate of peroxidase and its application to the diagnosis of schistosomiasis. Jpn J Exp Med 54: 131138.

    • Search Google Scholar
    • Export Citation
  • 29.

    Altman DG, 1991. Inter-rater agreement. Practical Statistics for Medical Research. London, UK: Chapman and Hall, 404.

  • 30.

    Goto Y, Coler RN, Guderian J, Mohamath R, Reed SG, 2006. Cloning, characterization, and serodiagnostic evaluation of Leishmania infantum tandem repeat proteins. Infect Immun 74: 39393945.

    • Search Google Scholar
    • Export Citation
  • 31.

    Tan JC, Tan A, Checkley L, Honsa CM, Ferdig MT, 2010. Variable numbers of tandem repeats in Plasmodium falciparum genes. J Mol Evol 71: 268278.

  • 32.

    Cheng PC, Tsaihong JC, Lee KM, 2007. Application of recombinant Sjc26GST for serodiagnosis of Schistosoma japonicum infection in water buffalo (Bos buffelus). Vet Parasitol 150: 314320.

    • Search Google Scholar
    • Export Citation
  • 33.

    Peng SY, Lee KM, Tsaihong JC, Cheng PC, Fan PC, 2008. Evaluation of recombinant fructose-1,6-biphosphate aldolase ELISA test for the diagnosis of Schistosoma japonicum in water buffaloes. Res Vet Sci 85: 527533.

    • Search Google Scholar
    • Export Citation
  • 34.

    Zhou XH, Wu JY, Huang XQ, Kunnon SP, Zhu XQ, Chen XG, 2010. Identification and characterization of Schistosoma japonicum Sjp40, a potential antigen candidate for the early diagnosis of schistosomiasis. Diagn Microbiol Infect Dis 67: 337345.

    • Search Google Scholar
    • Export Citation
  • 35.

    Boarino A, Scalone A, Gradoni L, Ferroglio E, Vitale F, Zanatta R, Giuffrida MG, Rosati S, 2005. Development of recombinant chimeric antigen expressing immunodominant B epitopes of Leishmania infantum for serodiagnosis of visceral leishmaniasis. Clin Diagn Lab Immunol 12: 647653.

    • Search Google Scholar
    • Export Citation
  • 36.

    Beghetto E, Spadoni A, Bruno L, Buffolano W, Gargano N, 2006. Chimeric antigens of Toxoplasma gondii: toward standardization of toxoplasmosis serodiagnosis using recombinant products. J Clin Microbiol 44: 21332140.

    • Search Google Scholar
    • Export Citation
  • 37.

    Goto Y, Howard RF, Bhatia A, Trigo J, Nakatani M, Netto EM, Reed SG, 2009. Distinct antigen recognition pattern during zoonotic visceral leishmaniasis in humans and dogs. Vet Parasitol 160: 215220.

    • Search Google Scholar
    • Export Citation
  • 38.

    Frank SA, 2002. Immunological variability of hosts. Immunology and Evolution of Infectious Disease. Princeton, NJ: Princeton University Press, 132135.

    • Search Google Scholar
    • Export Citation
  • 39.

    Xu J, Peeling RW, Chen JX, Wu XH, Wu ZD, Wang SP, Feng T, Chen SH, Li H, Guo JG, Zhou XN, 2011. Evaluation of immunoassays for the diagnosis of Schistosoma japonicum infection using archived sera. PLoS Negl Trop Dis 5: e949.

    • Search Google Scholar
    • Export Citation
  • 40.

    Leonardo LR, Acosta LP, Olveda RM, Aligui GDL, 2002. Difficulties and strategies in the control of schistosomiasis in the Philippines. Acta Trop 82: 295299.

    • Search Google Scholar
    • Export Citation
 
 
 

 

 

 

 

 

 

Human Antibody Response to Thioredoxin Peroxidase-1 and Tandem Repeat Proteins as Immunodiagnostic Antigen Candidates for Schistosoma japonicum Infection

View More View Less
  • National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido, Japan; Laboratory of Tropical Medicine and Parasitology, Dokkyo Medical University, Tochigi, Japan; Department of Parasitology, College of Public Health, University of the Philippines, Manila, Philippines

Schistosomiasis continues to be a public health problem in many tropical and subtropical countries. Improving the diagnostic tools for surveillance and monitoring in areas that have reached elimination level will help hasten the possible elimination of this disease. This study therefore aims to develop enzyme-linked immunosorbent assay through the use of recombinant proteins such as thioredoxin peroxidase-1 (SjTPx-1) and four tandem repeat proteins (Sj1TR, Sj2TR, Sj4TR, and Sj7TR). Cutoff values were calculated using 38 serum samples from healthy Japanese volunteers. Sera from 35 schistosomiasis-confirmed patients, four cured from the disease by chemotherapy, and 15 endemic negative controls were used to assess these antigens. SjTPx-1 and Sj7TR both had 85.71% sensitivity. Furthermore, these antigens were also tested against human sera positive for other parasitic infections and showed no or very minimal cross-reaction. These results suggest the potential defined antigens for development of an accurate diagnostic test for schistosomiasis.

Author Notes

*Address correspondence to Shin-ichiro Kawazu, National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, 2-13 Inada-cho, Obihiro, Hokkaido, 080-8555 Japan. E-mail: skawazu@obihiro.ac.jp

Financial Support: This study was supported in part by a grant from Global COE Program from the Japanese Ministry of Education, Science, Sports, Culture and Technology and by grant H23-Shinkosaiko-014 for research on emerging and re-emerging infectious diseases from the Ministry of Health, Labour and Welfare of Japan.

Authors' addresses: Jose Ma. Angeles, Yasuyuki Goto, Noboru Inoue, and Shin-ichiro Kawazu, National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido, Japan, E-mails: amoj28@yahoo.com, aygoto@mail.ecc.u-tokyo.ac.jp, ircpmi@obihiro.ac.jp, and skawazu@obihiro.ac.jp. Masashi Kirinoki and Yuichi Chigusa, Laboratory of Tropical Medicine and Parasitology, Dokkyo Medical University, Tochigi, Japan, E-mails: kirinoki@dokkyomed.ac.jp and ychigusa@dokkyomed.ac.jp. Lydia Leonardo, Pilarita Tongol-Rivera, and Elena Villacorte, Department of Parasitology, College of Public Health, University of the Philippines, Manila, Philippines, E-mails: leonardolydia7@gmail.com, ptongolrivera@yahoo.com, and eavillacorte@yahoo.com.

Save