Volume 76, Issue 2
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645


We examined whether antibody isotype responses to paramyosin (PM), a vaccine candidate for schistosomiasis, are associated with age-dependent resistance and pathology in liver fibrosis using human sera collected from 139 individuals infected with in Leyte, The Philippines. We report that IgA and IgG3 responses to PM showed a positive correlation with age and that the epitopes responsible were localized predominantly within the N-terminal half of PM. In addition, the IgG3 response to PM was associated with serum level of procollagen-III-peptide (P-III-P), an indicator of progression of liver fibrosis. These results imply that IgG3 against PM may not only provoke age-dependent resistance to infection but also enhance liver fibrosis. In contrast, levels of IgE to PM and to multiple PM fragments showed a negative correlation with P-III-P level. Thus, in contrast to IgG3, increases in PM-specific IgE may contribute to suppression of liver pathogenesis in schistosomiasis.


Article metrics loading...

The graphs shown below represent data from March 2017
Loading full text...

Full text loading...



  1. Kabatereine NB, Vennervald BJ, Ouma JH, Kemijumbi J, Butterworth AE, Dunne DW, Fulford AJ, 1999. Adult resistance to schistosomiasis mansoni: age-dependence of reinfection remains constant in communities with diverse exposure patterns. Parasitology 118 : 101–105. [Google Scholar]
  2. Woolhouse ME, Taylor P, Matanhire D, Chandiwana SK, 1991. Acquired immunity and epidemiology of Schistosoma haematobium. Nature 351 : 757–759. [Google Scholar]
  3. Li YS, Sleigh AC, Ross AG, Li Y, Williams GM, Forsyth SJ, Tanner M, McManus DP, 1999. A 2-year prospective study in China provides epidemiological evidence for resistance in humans to re-infection with Schistosoma japonicum. Ann Trop Med Parasitol 93 : 629–642. [Google Scholar]
  4. Acosta LP, Aligui GD, Tiu WU, McManus DP, Olveda RM, 2002. Immune correlate study on human Schistosoma japonicum in a well-defined population in Leyte, Philippines: I. Assessment of ‘resistance’ versus ‘susceptibility’ to S. japonicum infection. Acta Trop 84 : 127–136. [Google Scholar]
  5. Hagan P, Blumenthal UJ, Dunn D, Simpson AJ, Wilkins HA, 1991. Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature 349 : 243–245. [Google Scholar]
  6. Dunne DW, Butterworth AE, Fulford AJ, Kariuki HC, Langley JG, Ouma JH, Capron A, Pierce RJ, Sturrock RF, 1992. Immunity after treatment of human schistosomiasis: association between IgE antibodies to adult worm antigens and resistance to reinfection. Eur J Immunol 22 : 1483–1494. [Google Scholar]
  7. Webster M, Libranda-Ramirez BD, Aligui GD, Olveda RM, Ouma JH, Kariuki HC, Kimani G, Olds GR, Fulford AJ, Butterworth AE, Dunne DW, 1997. The influence of sex and age on antibody isotype responses to Schistosoma mansoni and Schistosoma japonicum in human populations in Kenya and the Philippines. Parasitology 114 : 383–393. [Google Scholar]
  8. Li Y, Sleigh AC, Ross AG, Zhang X, Williams GM, Yu X, Tanner M, McManus DP, 2001. Human susceptibility to Schistosoma japonicum in China correlates with antibody isotypes to native antigens. Trans R Soc Trop Med Hyg 95 : 441–448. [Google Scholar]
  9. Hernandez MG, Hafalla JC, Acosta LP, Aligui FF, Aligui GD, Ramirez BL, Dunne DW, Santiago ML, 1999. Paramyosin is a major target of the human IgA response against Schistosoma japonicum. Parasite Immunol 21 : 641–647. [Google Scholar]
  10. Ndhlovu P, Cadman H, Vennervald BJ, Christensen NO, Chidimu M, Chandiwana SK, 1996. Age-related antibody profiles in Schistosoma haematobium infections in a rural community in Zimbabwe. Parasite Immunol 18 : 181–191. [Google Scholar]
  11. Butterworth AE, Bensted-Smith R, Capron A, Capron M, Dalton PR, Dunne DW, Grzych JM, Kariuki HC, Khalife J, Koech D, 1987. Immunity in human schistosomiasis mansoni: prevention by blocking antibodies of the expression of immunity in young children. Parasitology 94 : 281–300. [Google Scholar]
  12. Bergquist R, Colley D, 1999. Schistosome vaccines: research to development. Parasitol Today 14 : 99–104. [Google Scholar]
  13. Chen H, Nara T, Zeng X, Satoh M, Wu G, Jiang W, Yi F, Kojima S, Zhang S, Hirayama K, 2000. Vaccination of domestic pig with recombinant paramyosin. against Schistosoma japonicum in China. Vaccine 18 : 2142–2146. [Google Scholar]
  14. McManus DP, Wong JY, Zhou J, Cai C, Zeng Q, Smyth D, Li Y, Kalinna BH, Duke MJ, Yi X, 2001. Recombinant paramyosin (rec-Sj-97) tested for immunogenicity and vaccine efficacy against Schistosoma japonicum in mice and water buffaloes. Vaccine 20 : 870–878. [Google Scholar]
  15. Janecharut T, Hata H, Takahashi H, Yoshida S, Saito H, Kojima S, 1992. Effects of recombinant tumour necrosis factor on antibody-dependent eosinophil-mediated damage to Schistosoma japonicum larvae. Parasite Immunol 14 : 605–616. [Google Scholar]
  16. Nara T, Matsumoto N, Janecharut T, Matsuda H, Yamamoto K, Irimura T, Nakamura K, Aikawa M, Oswald I, Sher A, 1994. Demonstration of the target molecule of a protective IgE antibody in secretory glands of Schistosoma japonicum larvae. Int Immunol 6 : 963–971. [Google Scholar]
  17. Kojima S, Niimura M, Kanazawa T, 1987. Production and properties of a mouse monoclonal IgE antibody to Schistosoma japonicum. J Immunol 139 : 2044–2049. [Google Scholar]
  18. Li YS, Ross AG, Sleigh AC, Li Y, Waine GJ, Williams GJ, Tanner M, McManus DP, 1999. Antibody isotype responses, infection and re-infection for Schistosoma japonicum in a marshland area of China. Acta Trop 73 : 79–92. [Google Scholar]
  19. King CL, Xianli J, Malhotra I, Liu S, Mahmoud AA, Oettgen HC, 1997. Mice with a targeted deletion of the IgE gene have increased worm burdens and reduced granulomatous inflammation following primary infection with Schistosoma mansoni. J Immunol 158 : 294–300. [Google Scholar]
  20. Owhashi M, Nawa Y, Watanabe N, 1989. Granulomatous response in selective IgE-deficient SJA/9 mice infected with Schistosoma japonicum. Int Arch Allergy Appl Immunol 90 : 310–312. [Google Scholar]
  21. Silveira AM, Bethony J, Gazzinelli A, Kloos H, Fraga LA, Alvares MC, Prata A, Guerra HL, Loverde PT, Correa-Oliveira R, Gazzinelli G, 2002. High levels of IgG4 to Schistosoma mansoni egg antigens in individuals with periportal fibrosis. Am J Trop Med Hyg 66 : 542–549. [Google Scholar]
  22. Hirsch C, Zouain CS, Alves JB, Goes AM, 1997. Induction of protective immunity and modulation of granulomatous hypersensitivity in mice using PIII, an anionic fraction of Schistosoma mansoni adult worm. Parasitology 115 : 21–28. [Google Scholar]
  23. Hirsch C, Carvalho-Queiroz C, Franco GR, Pena SD, Simpson AJ, Goes AM, 1997. Evidentiation of paramyosin (Sm-97) as a modulating antigen on granulomatous hypersensitivity to Schistosoma mansoni eggs. Mem Inst Oswaldo Cruz 92 : 663– 667. [Google Scholar]
  24. Ohmae H, Tanaka M, Hayashi M, Matsuzaki Y, Kurosaki Y, Blas BL, Portillo GG, Sy OS, Irie Y, Yasuraoka K, 1992. Improvement of ultrasonographic and serologic changes in Schistosoma japonicum-infected patients after treatment with praziquantel. Am J Trop Med Hyg 46 : 99–104. [Google Scholar]
  25. Ohmae H, Tanaka M, Hayashi M, Matsuzaki Y, Kurosaki Y, Blas BL, Portillo GG, Sy OS, Irie Y, Yasuraoka K, 1992. Ultrasonographic and serologic abnormalities in Schistosoma japonicum infection in Leyte, the Philippines. Am J Trop Med Hyg 46 : 89–98. [Google Scholar]
  26. Ohmae H, Sy OS, Chigusa Y, Portillo GP, 2003. Imaging diagnosis of schistosomiasis japonica: the use in Japan and application for field study in the present endemic area. Parasitol Int 52 : 385–393. [Google Scholar]
  27. Li YS, Sleigh AC, Ross AG, Li Y, Williams GM, Tanner M, McManus DP, 2000. Two-year impact of praziquantel treatment for Schistosoma japonicum infection in China: reinfection, subclinical disease and fibrosis marker measurements. Trans R Soc Trop Med Hyg 94 : 191–197. [Google Scholar]
  28. Tsukamoto T, Yamamoto T, Ikebe T, Takemura S, Shuto T, Kubo S, Hirohashi K, Kinoshita H, 2004. Serum markers of liver fibrosis and histologic severity of fibrosis in resected liver. Hepatogastroenterology 51 : 777–780. [Google Scholar]
  29. Acosta LP, McManus DP, Aligui GD, Olveda RM, Tiu WU, 2004. Antigen-specific antibody isotype patterns to Schistosoma japonicum recombinant and native antigens in a defined population in Leyte, the Philippines. Am J Trop Med Hyg 70 : 549–555. [Google Scholar]
  30. Jankovic D, Kullberg MC, Dombrowicz D, Barbieri S, Caspar P, Wynn TA, Paul WE, Cheever AW, Kinet JP, Sher A, 1997. Fc epsilonRI-deficient mice infected with Schistosoma mansoni mount normal Th2-type responses while displaying enhanced liver pathology. J Immunol 159 : 1868–1875. [Google Scholar]
  31. Deng J, Gold D, LoVerde PT, Fishelson Z, 2003. Inhibition of the complement membrane attack complex by Schistosoma mansoni paramyosin. Infect Immun 71 : 6402–6410. [Google Scholar]
  32. Laclette JP, Shoemaker CB, Richter D, Arcos L, Pante N, Cohen C, Bing D, Nicholson-Weller A, 1992. Paramyosin inhibits complement C1. J Immunol 148 : 124–128. [Google Scholar]
  33. Parizade M, Arnon R, Lachmann PJ, Fishelson Z, 1994. Functional and antigenic similarities between a 94-kD protein of Schistosoma mansoni (SCIP-1) and human CD59. J Exp Med 179 : 1625–1636. [Google Scholar]
  34. Loukas A, Jones MK, King LT, Brindley PJ, McManus DP, 2001. Receptor for Fc on the surfaces of schistosomes. Infect Immun 69 : 3646–3651. [Google Scholar]
  35. Jankovic D, Cheever AW, Kullberg MC, Wynn TA, Yap G, Caspar P, Lewis FA, Clynes R, Ravetch JV, Sher A, 1998. CD4+ T cell-mediated granulomatous pathology in schistosomiasis is downregulated by a B cell-dependent mechanism requiring Fc receptor signaling. J Exp Med 187 : 619–629. [Google Scholar]

Data & Media loading...

  • Received : 22 Feb 2006
  • Accepted : 28 Sep 2006

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error