Parasitology Research

, Volume 106, Issue 5, pp 1225–1231 | Cite as

Immunoblot analysis of membrane antigens of Schistosoma mansoni, Schistosoma intercalatum, and Schistosoma haematobium against Schistosoma-infected patient sera

  • Italo M. Cesari
  • Diana E. Ballen
  • L. Mendoza
  • Alain Ferrer
  • Jean-Pierre Pointier
  • Maryvonne Kombila
  • Dominique Richard-Lenoble
  • Andre ThéronEmail author
Original Paper


Antigens present in aqueous n-butanolic extracts (BE) of Schistosoma mansoni (Venezuelan JL strain), Schistosoma intercalatum (Cameroon EDEA strain), and Schistosoma haematobium (Yemen strain) adult worm membranes were compared in immunoblot against sera of patients infected with S. mansoni, S. intercalatum, S. haematobium, Schistosoma japonicum, or Schistosoma mekongi looking for similarities (common antigens) and differences (species-specific antigens). About 17 S. mansoni BE polypeptides (M r ∼8 to >80 kDa) were commonly recognized by S. mansoni-infected patient sera from Venezuela, Senegal, and Ethiopia. S. intercalatum-, S. haematobium-, or S. japonicum-infected sera were almost unreactive with S. mansoni BE. Nonetheless, S. mekongi-infected sera weakly cross-reacted with a ∼10–15-kDa subset of S. mansoni BE. About 72.7% of S. intercalatum-infected patient sera reacted with a ∼19–21-kDa complex in S. intercalatum BE and cross-reacted with a similar complex in S. haematobium BE. Conversely, all S. haematobium-infected patient sera reacted with a ∼19–21-kDa complex in S. haematobium BE and cross-reacted with the ∼19–21-kDa complex in S. intercalatum BE; S. mansoni- and S. japonicum-infected patient sera did not react with S. intercalatum or S. haematobium BE. Results showed the presence of a common membrane antigen between African schistosome species and species-specific antigens in S. mansoni BE that could be useful to discriminate between species and/or to detect Schistosoma infections.


Schistosomiasis Adult Worm Schistosoma Patient Seron Schistosoma Haematobium 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank the CNRS (France)-FONACIT (Venezuela) convention for financing the travels between France and Venezuela and ECOS-Nord V06A01. We thank Cesar Matos and Anne Rognon for their contribution to maintenance of life cycles of the schistosome species.


  1. Abath FG, Xavier EM, Allen R, Gomes YM, Lucena-Silva N, Baliza M, Simpson AJ (2000) Characterization of Sm13, a tegumental antigen of Schistosoma mansoni. Parasitol Res 86:745–752CrossRefPubMedGoogle Scholar
  2. Alarcón de Noya B, Cesari IM, Losada S, Colmenares C, Balzán C, Hoebeke J, Noya O (1997) Evaluation of alkaline phosphatase immunoassay and comparison with other diagnostic methods in areas of low transmission of schistosomiasis. Acta Trop 66:69–78CrossRefPubMedGoogle Scholar
  3. Alarcón de Noya B, Gevara R, Colmenares C, Losada S, Noya O (2006) Low transmission areas of schistosomiasis in Venezuela: consequences on the diagnosis, treatment, and control. Mem Inst Oswaldo Cruz 101:29–35Google Scholar
  4. Alarcón de Noya B, Ruiz R, Losada S, Colmenares C, Contreras R, Cesari IM, Noya O (2007) Detection of schistosomiasis cases in low-transmission areas based on coprologic and serologic criteria the Venezuelan experience. Acta Trop 103:41–49CrossRefPubMedGoogle Scholar
  5. Bradford MM (1976) A rapid method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  6. Butterworth AE, Capron M, Cordingly JS, Dalton PR, Dunne DW, Kariuki HC, Kimani G, Koech D, Mugambi M, Ouma JH et al (1985) Immunity after treatment of human schistosomiasis. II. Identification of resistant individuals, and analysis of their immune responses. Trans R Soc Trop Med Hyg 79:393–408CrossRefPubMedGoogle Scholar
  7. Capron A, Pierce R, Balloul JM, Grzych JM, Dissous C, Sondermeyer P, Lecocq JP (1987) Protective antigens experimental schistosomiasis. Acta Trop 44:63–69Google Scholar
  8. Cesari IM, Simpson AJH, Evans WH (1981) Properties of a series of tegumental membrane bound phosphohydrolase activities of Schistosoma mansoni. Biochem J 198:467–473PubMedGoogle Scholar
  9. Cesari IM, Pujol FH, Rodríguez M, Alarcón de Noya B (1987) Possible use of Schistosoma mansoni enzymes as antigens for immunodiagnosis. Mem Inst Oswaldo Cruz 82(suppl IV):175–177PubMedGoogle Scholar
  10. Cesari IM, Pujol FH, Alarcón de Noya B, Noya O, Hoebeke J, Bout D (1992) Immunodiagnosis based on enzyme markers. In: Bergquist R (ed) Diagnostic Approaches in Schistosomiasis. Wiley, London, pp 83–101Google Scholar
  11. Cesari IM, Ferrer A, Kombila M, Pichard E, Decam E, Li-Shu Q, Bout D, Richard-Lenoble D (1998) Specificity of the solid phase alkaline phosphatase immunocapture assay for the diagnosis of human Schistosoma mansoni infection. Trans R Soc Trop Med Hyg 9:38–39CrossRefGoogle Scholar
  12. Cesari IM, Mendoza L, Ballen DE, Alarcón de Noya B (2002) Evaluación del “IEFA” como técnica de inmunodiagnóstico en el programa de lucha contra la bilharziosis. Bol Mal San Amb XLII:29–32Google Scholar
  13. Cesari IM, Ballen DE, Mendoza L, Matos C (2005) Detection of Schistosoma mansoni membrane antigens by immunoblot análisis of sera of patients from low-transmission areas. Clin Diag Lab Immunol 12(2):280–286Google Scholar
  14. Chitsulo L, Engels D, Montresor A, Savioli L (2000) The global status of schistosomiasis and its control. Acta Trop 77:41–51CrossRefPubMedGoogle Scholar
  15. Harn D (1987) Immunisation with schistosome membrane antigens. Acta Trop 44:46–49Google Scholar
  16. King CHH (2009) Toward the elimination of schistosomiasis. Global health. New England J Med 360(2):106–109CrossRefGoogle Scholar
  17. Kusel JR, Al-Adhami BH, Doenhoff (2007) The schistosome in the mammalian host: understanding the mechanisms of adaptation. Review Parasitol 134(11):1477–1526Google Scholar
  18. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRefPubMedGoogle Scholar
  19. Losada S, Chacón N, Colmenares C, Bermúdez H, Lorenzo A, Pointier JP, Theron A, Alarcón de Noya B, Noya O (2005) Schistosoma: cross-reactivity and antigenic community among different species. Exp Parasitol 111(3):182–190CrossRefPubMedGoogle Scholar
  20. Low MG, Zilversmit DB (1980) Role of phosphatidyl inositol in attachment of alkaline phosphatase to membranes. Biochemistry 19:3913–3918CrossRefPubMedGoogle Scholar
  21. Loukas A, Tran M, Pearson MS (2007) Schistosome membrane proteins as vaccines. Invited review. Int J Parasitol 37:257–26CrossRefPubMedGoogle Scholar
  22. Morgan JAT, DeJong RJ, Kazibwe F, Mkoji GM, Loker ES (2003) A newly-identified lineage of Schistosoma. Int J Parasitol 33:977–985CrossRefPubMedGoogle Scholar
  23. Morgan JA, Dejong RJ, Adeoye GO, Ansa EDO, Barbosa CS, Brémond P, Cesari IM, Charbonnel N, Corrêa LR, Coulibaly C, D’andrea PS, De Souza CP, Doenhoff MJ, File S, Idris MA, Incani RN, Jarne P, Karanja DM, Kazibwe F, Kpikpi J, Lwambo NJ, Mabaye A, Magalhães LA, Makundi A, Moné H, Mouahid G, Muchemi GM, Mungai BN, Séne M, Southgate V, Tchuenté LA, Théron A, Yousif F, Zanotti-Magalhães EM, Mkoji GM, Loker ES (2005) Origin and diversification of the human parasite Schistosoma mansoni. Mol Ecol 14:3889–3902CrossRefPubMedGoogle Scholar
  24. Mutapi F, Mduluza T, Gomez-Escobar N, Gregory WF, Fernandez C, Midzi N, Maizels RM (2006) Immuno-epidemiology of human Schistosoma haematobium infection: preferential IgG3 antibody responsiveness to a recombinant antigen dependent on age and parasite burden. BMC Infect Dis 6:1–11CrossRefGoogle Scholar
  25. Pujol FH, Cesari IM (1990) Antigenicity of adult Schistosoma mansoni alkaline phosphatase. Parasite Immunol 12:189–198CrossRefPubMedGoogle Scholar
  26. Pujol FH, Cesari IM (1993) Schistosoma mansoni: surface membrane isolation with lectin-coated beads. Memb Biochem 10:155–161CrossRefGoogle Scholar
  27. Pujol FH, Alarcón de Noya B, Cesari IM (1989) Immunodiagnosis of schistosomiasis mansoni with APIA (Alkaline Phosphatase). Immunol Invest 18:1071–1080CrossRefPubMedGoogle Scholar
  28. Sher A, Kusel J, Pérez H, Clegg J (1974) Partial isolation of a membrane antigen which includes formation of antibodies lethal to schistosomes cultured in vitro. Exp Immunol 18:357–369Google Scholar
  29. Simpson AJG, Hackett F, Kelly C, Knight M, Payares G, Omer-Ali P, Lillywhite J, Fleck SL, Smithers SR (1986) The recognition of Schistosoma mansoni surface antigens by antibodies from patients infected with S. mansoni and S. haematobium. Trans R Soc Trop Med Hyg 80:261–270CrossRefPubMedGoogle Scholar
  30. Simpson AJG, Knight M, Kelly C, Hackett F, Omer-Ali P, Smithers SR (1987) The cloning of schistosome antigens. Acta Trop 44:83–99Google Scholar
  31. Skelly PJ (2005) The surface of schistosomes within the vertebrate host. In: Secor WA, Colley DG (eds) Book World Class Parasites: Schistosomiasis, vol 10. Springer, New York, pp 81–100Google Scholar
  32. Smithers SR (1987) Vaccination against schistosomes and other systemic helminthes. Int J Parasitol 17:31–42CrossRefPubMedGoogle Scholar
  33. Smithers SR, Hackett F, Ali PO, Simpson AJG (1989) Protective immunization of mice against Schistosoma mansoni with purified adult worm surface membranes. Parasite Immunol 11:301–318CrossRefPubMedGoogle Scholar
  34. Smithers SR, Hackett F, Braga V, Simpson AJG (1990) Immunoblotting identifies additional antigens recognized by mice protectively vaccinated with adult Schistosoma mansoni tegumental membranes. Parasitol Res 76:454–456CrossRefPubMedGoogle Scholar
  35. Tanford C, Reynolds JA (1976) Characterisation of membrane proteins in detergent solutions. Biochim Biophys Acta 457:133–170PubMedGoogle Scholar
  36. Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Biotechnology 24:145–149Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Italo M. Cesari
    • 1
  • Diana E. Ballen
    • 1
  • L. Mendoza
    • 1
  • Alain Ferrer
    • 2
  • Jean-Pierre Pointier
    • 4
  • Maryvonne Kombila
    • 3
  • Dominique Richard-Lenoble
    • 3
  • Andre Théron
    • 4
    Email author
  1. 1.Centro de Microbiología y Biología CelularInstituto Venezolano de Investigaciones Científicas (IVIC)CaracasVenezuela
  2. 2.Laboratoire de Parasitologie, Mycologie et Médecine TropicaleU.F.R. de MédecineTours cedexFrance
  3. 3.Département de Parasitologie–Mycologie–Médecine Tropicale Faculté de Médecine et des Sciences de la SantéUniversité des Sciences de la SantéLibrevilleGabon
  4. 4.UMR 5244 CNRS-EPHE-UPVD Biologie et Ecologie Tropicale et MéditerranéenneUniversité de Perpignan Via DomitiaPerpignan CedexFrance

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