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Journal of Parasitology Research
Volume 2012, Article ID 541268, 8 pages
http://dx.doi.org/10.1155/2012/541268
Review Article

Schistosoma Tegument Proteins in Vaccine and Diagnosis Development: An Update

1Laboratório de Esquistossomose, Centro de Pesquisas René Rachou, Fundação Oswaldo Cruz, Avenida Augusto de Lima 1715, Belo Horizonte,MG 30190-002, Brazil
2Instituto Nacional de Ciências e Tecnologia em Doenças Tropicais (INCT-DT), Avenida Augusto de Lima 1715, Belo Horizonte, MG 30190-002, Brazil

Received 27 July 2012; Accepted 24 September 2012

Academic Editor: Andrea Teixeira-Carvalho

Copyright © 2012 Cristina Toscano Fonseca et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. N. R. Bergquist, L. R. Leonardo, and G. F. Mitchell, “Vaccine-linked chemotherapy: can schistosomiasis control benefit from an integrated approach?” Trends in Parasitology, vol. 21, no. 3, pp. 112–117, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. N. Berhe, G. Medhin, B. Erko et al., “Variations in helminth faecal egg counts in Kato-Katz thick smears and their implications in assessing infection status with Schistosoma mansoni,” Acta Tropica, vol. 92, no. 3, pp. 205–212, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Berriman, B. J. Haas, P. T. Loverde et al., “The genome of the blood fluke Schistosoma mansoni,” Nature, vol. 460, no. 7253, pp. 352–358, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. Y. Zhou, H. Zheng, Y. Chen et al., “The Schistosoma japonicum genome reveals features of host-parasite interplay,” Nature, vol. 460, no. 7253, pp. 345–351, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. A. V. Protasio, I. J. Tsai, A. Babbage et al., “A systematically improved high quality genome and transcriptome of the human blood fluke Schistosoma mansoni,” PLoS Neglected Tropical Diseases, vol. 6, no. 1, Article ID e1455, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. N. D. Young, A. R. Jex, B. Li et al., “Whole-genome sequence of Schistosoma haematobium,” Nature Genetics, vol. 44, no. 2, pp. 221–225, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Zerlotini, M. Heiges, H. Wang et al., “SchistoDB: a Schistosoma mansoni genome resource,” Nucleic Acids Research, vol. 37, no. 1, pp. D579–D582, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. A. R. C. Harris, R. J. Russell, and A. D. Charters, “A review of schistosomiasis in immigrants in Western Australia, demonstrating the unusual longevity of Schistosoma mansoni,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 78, no. 3, pp. 385–388, 1984. View at Google Scholar · View at Scopus
  9. S. J. Davies, J. L. Grogan, R. B. Blank, K. C. Lim, R. M. Locksley, and J. H. McKerrow, “Modulation of blood fluke development in the liver by hepatic CD4+ lymphocytes,” Science, vol. 294, no. 5545, pp. 1358–1361, 2001. View at Publisher · View at Google Scholar · View at Scopus
  10. R. L. De Mendonça, H. Escrivá, D. Bouton, V. Laudet, and R. J. Pierce, “Hormones and nuclear receptors in schistosome development,” Parasitology Today, vol. 16, no. 6, pp. 233–240, 2000. View at Publisher · View at Google Scholar · View at Scopus
  11. P. Saule, E. Adriaenssens, M. Delacre et al., “Early variations of host thyroxine and interleukin-7 favor Schistosoma mansoni development,” Journal of Parasitology, vol. 88, no. 5, pp. 849–855, 2002. View at Google Scholar · View at Scopus
  12. P. Amiri, R. M. Locksley, T. G. Parslow et al., “Tumour necrosis factor α restores granulomas and induces parasite egg-laying in schistosome-infected SCID mice,” Nature, vol. 356, no. 6370, pp. 604–607, 1992. View at Publisher · View at Google Scholar · View at Scopus
  13. P. T. LoVerde, A. Osman, and A. Hinck, “Schistosoma mansoni: TGF-β signaling pathways,” Experimental Parasitology, vol. 117, no. 3, pp. 304–317, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. I. Wolowczuk, S. Nutten, O. Roye et al., “Infection of mice lacking interleukin-7 (IL-7) reveals an unexpected role for IL-7 in the development of the parasite Schistosoma mansoni,” Infection and Immunity, vol. 67, no. 8, pp. 4183–4190, 1999. View at Google Scholar · View at Scopus
  15. R. B. Blank, E. W. Lamb, A. S. Tocheva et al., “The common γ chain cytokines interleukin (IL)-2 and IL-7 indirectly modulate blood fluke development via effects on CD4+ T cells,” Journal of Infectious Diseases, vol. 194, no. 11, pp. 1609–1616, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. D. A. A. Vignali, P. Crocker, Q. D. Bickle, S. Cobbold, H. Waldmann, and M. G. Taylor, “A role for CD4+ but not CD8+ T cells in immunity to Schistosoma mansoni induced by 20 krad-irradiated and Ro 11-3128-terminated infections,” Immunology, vol. 67, no. 4, pp. 466–472, 1989. View at Google Scholar · View at Scopus
  17. D. Jankovic, T. A. Wynn, M. C. Kullberg et al., “Optimal vaccination against Schistosoma mansoni requires the induction of both B cell- and IFN-γ-dependent effector mechanisms,” Journal of Immunology, vol. 162, no. 1, pp. 345–351, 1999. View at Google Scholar · View at Scopus
  18. M. Street, P. S. Coulson, C. Sadler et al., “TNF is essential for the cell-mediated protective immunity induced by the radiation-attenuated schistosome vaccine,” Journal of Immunology, vol. 163, no. 8, pp. 4489–4494, 1999. View at Google Scholar · View at Scopus
  19. F. G. C. Abath and R. C. Werkhauser, “The tegument of Schistosoma mansoni: functional and immunological features,” Parasite Immunology, vol. 18, no. 1, pp. 15–20, 1996. View at Google Scholar · View at Scopus
  20. Z. G. Han, P. J. Brindley, S. Y. Wang, and C. Zhu, “Schistosoma genomics: new perspectives on schistosome biology and host-parasite interaction,” Annual Review of Genomics and Human Genetics, vol. 10, pp. 211–240, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. M. K. Jones, G. N. Gobert, L. Zhang, P. Sunderland, and D. P. McManus, “The cytoskeleton and motor proteins of human schistosomes and their roles in surface maintenance and host-parasite interactions,” BioEssays, vol. 26, no. 7, pp. 752–765, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. D. J. Hockley and D. J. McLaren, “Schistosoma mansoni: changes in the outer membrane of the tegument during development from cercaria to adult worm,” International Journal for Parasitology, vol. 3, no. 1, pp. 13–20, 1973. View at Google Scholar · View at Scopus
  23. M. Salzet, A. Capron, and G. B. Stefano, “Molecular crosstalk in host-parasite relationships: Schistosome- and leech-host interactions,” Parasitology Today, vol. 16, no. 12, pp. 536–540, 2000. View at Publisher · View at Google Scholar · View at Scopus
  24. R. T. Damian, “Molecular mimicry revisited,” Parasitology Today, vol. 3, no. 9, pp. 263–266, 1987. View at Google Scholar · View at Scopus
  25. S. R. Smithers, D. J. McLaren, and F. J. Rahalho-Pinto, “Immunity to schistosomes: the target,” American Journal of Tropical Medicine and Hygiene, vol. 26, no. 6, pp. 11–19, 1977. View at Google Scholar · View at Scopus
  26. F. Santoro, P. J. Lachmann, A. Capron, and M. Capron, “Activation of complement by Schistosoma mansoni schistosomula: killing of parasites by the alternative pathway and requirement of IgG for classical pathway activation,” Journal of Immunology, vol. 123, no. 4, pp. 1551–1557, 1979. View at Google Scholar · View at Scopus
  27. D. A. Dean, “Decreased binding of cytotoxic antibody by developing Schistosoma mansoni. Evidence for a surface change independent of host antigen adsorption and membrane turnover,” Journal of Parasitology, vol. 63, no. 3, pp. 418–426, 1977. View at Google Scholar · View at Scopus
  28. A. Dessein, J. C. Samuelson, and A. E. Butterworth, “Immune evasion by Schistosoma mansoni: loss of susceptibility to antibody or complement-dependent eosinophil attack by schistosomula cultured in medium free of macromolecules,” Parasitology, vol. 82, no. 3, pp. 357–374, 1981. View at Google Scholar · View at Scopus
  29. E. L. Racoosin, S. J. Davies, and E. J. Pearce, “Caveolae-like structures in the surface membrane of Schistosoma mansoni,” Molecular and Biochemical Parasitology, vol. 104, no. 2, pp. 285–297, 1999. View at Publisher · View at Google Scholar · View at Scopus
  30. R. El Ridi, S. H. Mohamed, and H. Tallima, “Incubation of Schistosoma mansoni lung-stage schistosomula in corn oil exposes their surface membrane antigenic specificities,” Journal of Parasitology, vol. 89, no. 5, pp. 1064–1067, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. D. J. McLaren, “Will the real target of immunity to schistosomiasis please stand up,” Parasitology Today, vol. 5, no. 9, pp. 279–282, 1989. View at Google Scholar · View at Scopus
  32. G. N. Gobert, M. Chai, and D. P. McManus, “Biology of the schistosome lung-stage schistosomulum,” Parasitology, vol. 134, no. 4, pp. 453–460, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. F. V. Durães, N. B. Carvalho, T. T. Melo, S. C. Oliveira, and C. T. Fonseca, “IL-12 and TNF-α production by dendritic cells stimulated with Schistosoma mansoni schistosomula tegument is TLR4- and MyD88-dependent,” Immunology Letters, vol. 125, no. 1, pp. 72–77, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. B. W. M. Van Balkom, R. A. Van Gestel, J. F. H. M. Brouwers et al., “Mass spectrometric analysis of the Schistosoma mansoni tegumental sub-proteome,” Journal of Proteome Research, vol. 4, no. 3, pp. 958–966, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Braschi, W. C. Borges, and R. A. Wilson, “Proteomic analysis of the shistosome tegument and its surface membranes,” Memorias do Instituto Oswaldo Cruz, vol. 101, supplement 1, pp. 205–212, 2006. View at Google Scholar · View at Scopus
  36. S. Braschi and R. A. Wilson, “Proteins exposed at the adult schistosome surface revealed by biotinylation,” Molecular and Cellular Proteomics, vol. 5, no. 2, pp. 347–356, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Loukas, S. Gaze, J. P. Mulvenna et al., “Vaccinomics for the major blood feeding helminths of humans,” OMICS A Journal of Integrative Biology, vol. 15, no. 9, pp. 567–577, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. T. Teixeira De Melo, J. Michel De Araujo, F. Do Valle Durães et al., “Immunization with newly transformed Schistosoma mansoni schistosomula tegument elicits tegument damage, reduction in egg and parasite burden,” Parasite Immunology, vol. 32, no. 11-12, pp. 749–759, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. G. P. Dillon, T. Feltwell, J. P. Skelton et al., “Microarray analysis identifies genes preferentially expressed in the lung schistosomulum of Schistosoma mansoni,” International Journal for Parasitology, vol. 36, no. 1, pp. 1–8, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. G. N. Gobert, M. H. Tran, L. Moertel et al., “Transcriptional changes in Schistosoma mansoni during early schistosomula development and in the presence of erythrocytes,” PLoS Neglected Tropical Diseases, vol. 4, no. 2, article e600, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. J. M. Correnti, P. J. Brindley, and E. J. Pearce, “Long-term suppression of cathepsin B levels by RNA interference retards schistosome growth,” Molecular and Biochemical Parasitology, vol. 143, no. 2, pp. 209–215, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. M. E. Morales, G. Rinaldi, G. N. Gobert, K. J. Kines, J. F. Tort, and P. J. Brindley, “RNA interference of Schistosoma mansoni cathepsin D, the apical enzyme of the hemoglobin proteolysis cascade,” Molecular and Biochemical Parasitology, vol. 157, no. 2, pp. 160–168, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. M. H. Tran, T. C. Freitas, L. Cooper et al., “Suppression of mRNAs encoding tegument tetraspanins from Schistosoma mansoni results in impaired tegument turnover,” PLoS pathogens, vol. 6, no. 4, Article ID e1000840, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. F. Liu, S. J. Cui, W. Hu, Z. Feng, Z. Q. Wang, and Z. G. Han, “Excretory/secretory proteome of the adult developmental stage of human blood fluke, Schistosoma japonicum,” Molecular and Cellular Proteomics, vol. 8, no. 6, pp. 1236–1251, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Verjovski-Almeida, R. DeMarco, E. A. L. Martins et al., “Transcriptome analysis of the acoelomate human parasite Schistosoma mansoni,” Nature Genetics, vol. 35, no. 2, pp. 148–157, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. C. D. Criscione, C. L. L. Valentim, H. Hirai, P. T. LoVerde, and T. J. C. Anderson, “Genomic linkage map of the human blood fluke Schistosoma mansoni,” Genome Biology, vol. 10, no. 6, article R71, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. W. Castro-Borges, A. Dowle, R. S. Curwen, J. Thomas-Oates, and R. A. Wilson, “Enzymatic shaving of the tegument surface of live schistosomes for proteomic analysis: a rational approach to select vaccine candidates,” PLoS Neglected Tropical Diseases, vol. 5, no. 3, article e993, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. W. Castro-Borges, D. M. Simpson, A. Dowle et al., “Abundance of tegument surface proteins in the human blood fluke Schistosoma mansoni determined by QconCAT proteomics,” Journal of Proteomics, vol. 74, pp. 1519–1533, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. F. C. Cardoso, J. M. R. Pinho, V. Azevedo, and S. C. Oliveira, “Identification of a new Schistosoma mansoni membrane-bound protein through bioinformatic analysis,” Genetics and Molecular Research, vol. 5, no. 4, pp. 609–618, 2006. View at Google Scholar · View at Scopus
  50. F. C. Cardoso, G. C. Macedo, E. Gava et al., “Schistosoma mansoni tegument protein Sm29 is able to induce a Th1-type of immune response and protection against parasite infection,” PLoS Neglected Tropical Diseases, vol. 2, no. 10, article e308, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. D. W. Dunne, M. Webster, P. Smith et al., “The isolation of a 22 kDa band after SDS-PAGE of Schistosoma mansoni adult worms and its use to demonstrate the IgE responses against the antigen(s) it contains are associated with human resistance to reinfection,” Parasite Immunology, vol. 19, no. 2, pp. 79–89, 1997. View at Google Scholar · View at Scopus
  52. M. L. Santiago, J. C. R. Hafalla, J. D. Kurtis et al., “Identification of the Schistosoma japonicum 22.6-kDa antigen as a major target of the human IgE response: similarity of IgE-binding epitopes to allergen peptides,” International Archives of Allergy and Immunology, vol. 117, no. 2, pp. 94–104, 1998. View at Publisher · View at Google Scholar · View at Scopus
  53. L. G. G. Pacífico, C. T. Fonseca, L. Chiari, and S. C. Oliveira, “Immunization with Schistosoma mansoni 22.6 kDa antigen induces partial protection against experimental infection in a recombinant protein form but not as DNA vaccine,” Immunobiology, vol. 211, no. 1-2, pp. 97–104, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. L. G. G. Pacífico, C. T. Fonseca, M. M. Barsante, L. S. Cardoso, M. I. Araújo, and S. C. Oliveira, “Aluminum hydroxide associated to Schistosoma mansoni 22.6 kDa protein abrogates partial protection against experimental infection but not alter interleukin-10 production,” Memorias do Instituto Oswaldo Cruz, vol. 101, supplement 1, pp. 365–368, 2006. View at Google Scholar · View at Scopus
  55. L. S. Cardoso, S. C. Oliveira, A. M. Góes et al., “Schistosoma mansoni antigens modulate the allergic response in a murine model of ovalbumin-induced airway inflammation,” Clinical and Experimental Immunology, vol. 160, no. 2, pp. 266–274, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. D. Smyth, D. P. McManus, M. J. Smout, T. Laha, W. Zhang, and A. Loukas, “Isolation of cDNAS encoding secreted and transmembrane proteins from Schistosoma mansoni by a signal sequence trap method,” Infection and Immunity, vol. 71, no. 5, pp. 2548–2554, 2003. View at Publisher · View at Google Scholar · View at Scopus
  57. M. H. Tran, M. S. Pearson, J. M. Bethony et al., “Tetraspanins on the surface of Schistosoma mansoni are protective antigens against schistosomiasis,” Nature Medicine, vol. 12, no. 7, pp. 835–840, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. W. Zhang, J. Li, M. Duke et al., “Inconsistent protective efficacy and marked polymorphism limits the value of Schistosoma japonicum tetraspanin-2 as a vaccine target,” PLoS Neglected Tropical Diseases, vol. 5, no. 5, Article ID e1166, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. S. Y. Sauma and M. Strand, “Identification and characterization of glycosylphosphatidylinositol-linked Schistosoma mansoni adult worm immunogens,” Molecular and Biochemical Parasitology, vol. 38, no. 2, pp. 199–210, 1990. View at Publisher · View at Google Scholar · View at Scopus
  60. P. J. Brindley, M. Strand, A. P. Norden, and A. Sher, “Role of host antibody in the chemotherapeutic action of praziquantel against Schistosoma mansoni: identification of target antigens,” Molecular and Biochemical Parasitology, vol. 34, no. 2, pp. 99–108, 1989. View at Google Scholar · View at Scopus
  61. E. J. M. Nascimento, R. V. Amorim, A. Cavalcanti et al., “Assessment of a DNA vaccine encoding an anchored- glycosylphosphatidylinositol tegumental antigen complexed to protamine sulphate on immunoprotection against murine schistosomiasis,” Memorias do Instituto Oswaldo Cruz, vol. 102, no. 1, pp. 21–27, 2007. View at Google Scholar · View at Scopus
  62. V. P. Martins, C. S. Pinheiro, B. C. P. Figueiredo et al., “Vaccination with enzymatically cleaved GPI-anchored proteins from schistosoma mansoni induces protection against challenge infection,” Clinical and Developmental Immunology, vol. 2012, Article ID 962538, 11 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  63. H. M. Ahmed and M. H Romeih, “Protection against Schistosoma mansoni infection with recombinant schistosomula 21.7 kDa protein,” Arab Journal of Biotechnology, vol. 24, pp. 229–249, 2001. View at Google Scholar
  64. H. M. Ahmed, M. H. Romeih, and T. S. Abou-Shousha, “DNA immunization with the gene encoding Sm21.7 protects mice against S. mansoni infections,” American Journal of Science, vol. 2, pp. 59–69, 2006. View at Google Scholar
  65. K. A. Shalaby, L. Yin, A. Thakur, L. Christen, E. G. Niles, and P. T. LoVerde, “Protection against Schistosoma mansoni utilizing DNA vaccination with genes encoding Cu/Zn cytosolic superoxide dismutase, signal peptide-containing superoxide dismutase and glutathione peroxidase enzymes,” Vaccine, vol. 22, no. 1, pp. 130–136, 2003. View at Publisher · View at Google Scholar · View at Scopus
  66. Z. Hong, D. J. Kosman, A. Thakur, D. Rekosh, and P. T. LoVerde, “Identification and purification of a second form of Cu/Zn superoxide dismutase from Schistosoma mansoni,” Infection and Immunity, vol. 60, no. 9, pp. 3641–3651, 1992. View at Google Scholar · View at Scopus
  67. H. Mei and P. T. LoVerde, “Schistosoma mansoni: the developmental regulation and immunolocalization of antioxidant enzymes,” Experimental Parasitology, vol. 86, no. 1, pp. 69–78, 1997. View at Publisher · View at Google Scholar · View at Scopus
  68. H. Mei, A. Thakur, J. Schwartz, and P. T. Lo Verde, “Expression and characterization of glutathione peroxidase activity in the human blood fluke Schistosoma mansoni,” Infection and Immunity, vol. 64, no. 10, pp. 4299–4306, 1996. View at Google Scholar · View at Scopus
  69. M. D. M. Mourão, N. Dinguirard, G. R. Franco, and T. P. Yoshino, “Role of the endogenous antioxidant system in the protection of Schistosoma mansoni primary sporocysts against exogenous oxidative stress,” PLoS Neglected Tropical Diseases, vol. 3, no. 11, article e550, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. J. V. Hamilton, M. Klinkert, and M. J. Doenhoff, “Diagnosis of schistosomiasis: antibody detection, with notes on parasitological and antigen detection methods,” Parasitology, vol. 117, pp. S41–S57, 1998. View at Google Scholar · View at Scopus
  71. M. J. Doenhoff, P. L. Chiodini, and J. V. Hamilton, “Specific and sensitive diagnosis of schistosome infection: can it be done with antibodies?” Trends in Parasitology, vol. 20, no. 1, pp. 35–39, 2004. View at Publisher · View at Google Scholar · View at Scopus
  72. G. B. F. Carvalho, R. A. da Silva-Pereira, L. G. G. Pacífico, and C. T. Fonseca, “Identification of Schistosoma mansoni candidate antigens for diagnosis of schistosomiasis,” Memorias do Instituto Oswaldo Cruz, vol. 106, no. 7, pp. 837–843, 2011. View at Google Scholar · View at Scopus
  73. C. M. Xia, R. Rong, Z. X. Lu et al., “Schistosoma japonicum: a PCR assay for the early detection and evaluation of treatment in a rabbit model,” Experimental Parasitology, vol. 121, no. 2, pp. 175–179, 2009. View at Publisher · View at Google Scholar · View at Scopus
  74. J.-J. Guo, H.-J. Zheng, J. Xu, X.-Q. Zhu, S.-Y. Wang, and C.-M. Xia, “Sensitive and specific target sequences selected from retrotransposons of Schistosoma japonicum for the diagnosis of schistosomiasis,” PLoS Neglected Tropical Diseases, vol. 6, no. 3, Article ID e1579, 2012. View at Publisher · View at Google Scholar · View at Scopus
  75. Z. R. Zhong, H. B. Zhou, X. Y. Li et al., “Serological proteome-oriented screening and application of antigens for the diagnosis of Schistosomiasis japonica,” Acta Tropica, vol. 116, no. 1, pp. 1–8, 2010. View at Publisher · View at Google Scholar · View at Scopus
  76. A. S. Verkman, “Physiological importance of aquaporin water channels,” Annals of Medicine, vol. 34, no. 3, pp. 192–200, 2002. View at Google Scholar · View at Scopus
  77. J. Song and Q.-F. He, “Bioinformatics analysis of the structure and linear B-cell epitopes of aquaporin-3 from Schistosoma japonicum,” Asian Pacific Journal of Tropical Medicine, vol. 5, no. 2, pp. 107–109, 2012. View at Publisher · View at Google Scholar · View at Scopus
  78. E. G. Vasconcelos, P. S. Nascimento, M. N. L. Meirelles, S. Verjovski-Almeida, and S. T. Ferreira, “Characterization and localization of an ATP-diphosphohydrolase on the external surface of the tegument of Schistosoma mansoni,” Molecular and Biochemical Parasitology, vol. 58, no. 2, pp. 205–214, 1993. View at Publisher · View at Google Scholar · View at Scopus
  79. R. Bhardwaj and P. J. Skelly, “Purinergic signaling and immune modulation at the schistosome surface?” Trends in Parasitology, vol. 25, no. 6, pp. 256–260, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. R. DeMarco, A. T. Kowaltowski, R. A. Mortara, and S. Verjovski-Almeida, “Molecular characterization and immunolocalization of Schistosoma mansoni ATP-diphosphohydrolase,” Biochemical and Biophysical Research Communications, vol. 307, no. 4, pp. 831–838, 2003. View at Publisher · View at Google Scholar · View at Scopus
  81. J. Levano-Garcia, R. A. Mortara, S. Verjovski-Almeida, and R. DeMarco, “Characterization of Schistosoma mansoni ATPDase2 gene, a novel apyrase family member,” Biochemical and Biophysical Research Communications, vol. 352, no. 2, pp. 384–389, 2007. View at Publisher · View at Google Scholar · View at Scopus
  82. R. G. P. R. Mendes, M. A. N. Gusmão, A. C. R. G. Maia et al., “Immunostimulatory property of a synthetic peptide belonging to the soluble ATP diphosphohydrolase isoform (SmATPDase 2) and immunolocalisation of this protein in the schistosoma mansoni egg,” Memorias do Instituto Oswaldo Cruz, vol. 106, no. 7, pp. 808–813, 2011. View at Google Scholar · View at Scopus
  83. M. E. Hemler, “Specific tetraspanin functions,” Journal of Cell Biology, vol. 155, no. 7, pp. 1103–1107, 2001. View at Publisher · View at Google Scholar · View at Scopus