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International Journal of Inflammation
Volume 2012, Article ID 512097, 6 pages
http://dx.doi.org/10.1155/2012/512097
Review Article

Interface Molecules of Angiostrongylus cantonensis: Their Role in Parasite Survival and Modulation of Host Defenses

Laboratório de Biologia Parasitária Faculdade de Biociências e Laboratório de Parasitologia Molecular Instituto de Pesquisas Biomédicas Pontifícia Universidade do Rio Grande do Sul (PUCRS), 90690-900 Porto Alegre, RS, Brazil

Received 3 November 2011; Accepted 23 January 2012

Academic Editor: Kittisak Sawanyawisuth

Copyright © 2012 Alessandra L. Morassutti and Carlos Graeff-Teixeira. 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. R. M. Maizels, D. A. P. Bundy, M. E. Selkirk, D. F. Smith, and R. M. Anderson, “Immunological modulation and evasion by helminth parasites in human populations,” Nature, vol. 365, no. 6449, pp. 797–805, 1993. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. K. Henkle-Dührsen and A. Kampkötter, “Antioxidant enzyme families in parasitic nematodes,” Molecular and Biochemical Parasitology, vol. 114, no. 2, pp. 129–142, 2001. View at Publisher · View at Google Scholar · View at Scopus
  3. J. M. Dzik, “Molecules released by helminth parasites involved in host colonization,” Acta Biochimica Polonica, vol. 53, no. 1, pp. 33–64, 2006. View at Google Scholar · View at Scopus
  4. J. P. Hewitson, J. R. Grainger, and R. M. Maizels, “Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity,” Molecular and Biochemical Parasitology, vol. 167, no. 1, pp. 1–11, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  5. C. Graeff-Teixeira, A. C. A. Da Silva, and K. Yoshimura, “Update on eosinophilic meningoencephalitis and its clinical relevance,” Clinical Microbiology Reviews, vol. 22, no. 2, pp. 322–348, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  6. Q. P. Wang, D. H. Lai, X. Q. Zhu, X. G. Chen, and Z. R. Lun, “Human angiostrongyliasis,” The Lancet Infectious Diseases, vol. 8, no. 10, pp. 621–630, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. R. L. Caldeira, C. L. G. F. Mendonça, C. O. Goveia et al., “First record of molluscs naturally infected with Angiostrongylus cantonensis (Chen, 1935) (Nematoda: Metastrongylidae) in Brazil,” Memorias do Instituto Oswaldo Cruz, vol. 102, no. 7, pp. 887–889, 2007. View at Google Scholar · View at Scopus
  8. J. H. Diaz, “Helminthic eosinophilic meningitis: emerging zoonotic diseases in the South,” The Journal of the Louisiana State Medical Society, vol. 160, no. 6, pp. 333–342, 2008. View at Google Scholar · View at Scopus
  9. T. Pincay, L. García, E. Narváez, O. Decker, L. Martini, and J. M. Moreira, “Angiostrongyliasis due to Parastrongylus (Angiostrongylus) cantonensis in Ecuador. First report in South America,” Tropical Medicine & International Health, vol. 14, no. 2, p. 37, 2009. View at Google Scholar
  10. A. Maldonado Jr., R. O. Simões, A. P. M. Oliveira et al., “First report of Angiostrongylus cantonensis (Nematoda: Metastrongylidae) in Achatina fulica (Mollusca: Gastropoda) from Southeast and South Brazil,” Memorias do Instituto Oswaldo Cruz, vol. 105, no. 7, pp. 938–941, 2010. View at Google Scholar · View at Scopus
  11. C. A. Behm and K. S. Ovington, “The role of eosinophils in parasitic helminth infections: insights from genetically modified mice,” Parasitology Today, vol. 16, no. 5, pp. 202–209, 2000. View at Publisher · View at Google Scholar · View at Scopus
  12. M. E. Rothenberg and S. P. Hogan, “The eosinophil,” Annual Review of Immunology, vol. 24, pp. 147–174, 2006. View at Google Scholar
  13. S. J. Ackerman and B. S. Bochner, “Mechanisms of eosinophilia in the pathogenesis of hypereosinophilic disorders,” Immunology and Allergy Clinics of North America, vol. 27, no. 3, pp. 357–375, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  14. K. Yoshimura, K. Uchida, K. Sato, and H. Oya, “Ultrastructural evidence for eosinophil-mediated destruction of Angiostrongylus cantonensis transferred into the pulmonary artery of non-permissive hosts,” Parasite Immunology, vol. 6, no. 2, pp. 105–118, 1984. View at Google Scholar · View at Scopus
  15. O. Sasaki, H. Sugaya, K. Ishida, and K. Yoshimura, “Ablation of eosinophils with anti-IL-5 antibody enhances the survival of intracranial worms of Angiostrongylus cantonensis in the mouse,” Parasite Immunology, vol. 15, no. 6, pp. 349–354, 1993. View at Google Scholar · View at Scopus
  16. H. Sugaya, M. Aoki, T. Yoshida, K. Takatsu, and K. Yoshimura, “Eosinophilia and intracranial worm recovery in interleukin-5 transgenic and interleukin-5 receptor α chain-knockout mice infected with Angiostrongylus cantonensis,” Parasitology Research, vol. 83, no. 6, pp. 583–590, 1997. View at Publisher · View at Google Scholar · View at Scopus
  17. H. Sugaya, C. Graeff-Teixeira, K. Ishida, S. Matsuda, K. Katahira, and K. Yoshimura, “Interleukin-5 transgenic mice show augmented resistance to Angiostrongylus costaricensis infection,” Parasitology Research, vol. 88, no. 4, pp. 350–355, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. P. M. Intapan, S. Kittimongkolma, K. Niwattayakul, K. Sawanyawisuth, and W. Maleewong, “Cerebrospinal fluid cytokine responses in human eosinophilic meningitis associated with angiostrongyliasis,” Journal of the Neurological Sciences, vol. 267, no. 1-2, pp. 17–21, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  19. Z. Diao, X. Chen, C. Yin, J. Wang, H. Qi, and A. Ji, “Angiostrongylus cantonensis: effect of combination therapy with albendazole and dexamethasone on Th cytokine gene expression in PBMC from patients with eosinophilic meningitis,” Experimental Parasitology, vol. 123, no. 1, pp. 1–5, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. K. M. Chen and S. C. Lai, “Biochemical and pathological evaluation of albendazole/thalidomide co-therapy against eosinophilic meningitis or meningoencephalitis induced by Angiostrongylus cantonensis,” Journal of Antimicrobial Chemotherapy, vol. 59, no. 2, pp. 264–276, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  21. W. Y. Du, J. W. Liao, C. K. Fan, and K. E. Su, “Combined treatment with interleukin-12 and mebendazole lessens the severity of experimental eosinophilic meningitis caused by Angiostrongylus cantonensis in ICR mice,” Infection and Immunity, vol. 71, no. 7, pp. 3947–3953, 2003. View at Publisher · View at Google Scholar · View at Scopus
  22. C. C. Chuang, K. E. Su, C. W. Chen et al., “Anti-CCR3 monoclonal antibody inhibits eosinophil infiltration in Angiostrongylus cantonensis-infected ICR mice,” Acta Tropica, vol. 113, no. 3, pp. 209–213, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  23. K. Ishida and K. Yoshimura, “Differences in responses of rat- and guinea-pig-eosinophils to eosinophil chemotactic factors derived from Angiostrongylus cantonensis,” Parasite Immunology, vol. 12, no. 3, pp. 269–283, 1990. View at Google Scholar · View at Scopus
  24. S. Reinhardt, I. Scott, and H. V. Simpson, “Neutrophil and eosinophil chemotactic factors in the excretory/secretory products of sheep abomasal nematode parasites: NCF and ECF in abomasal nematodes,” Parasitology Research, vol. 109, no. 3, pp. 627–635, 2011. View at Publisher · View at Google Scholar · View at PubMed
  25. J. D. Lee and C. M. Yen, “Protease secreted by the infective larvae of Angiostrongylus cantonensis and its role in the penetration of mouse intestine,” American Journal of Tropical Medicine and Hygiene, vol. 72, no. 6, pp. 831–836, 2005. View at Google Scholar · View at Scopus
  26. A. L. Morassutti, P. M. Pinto, B. K. Dutra, G. T. Oliveira, H. B. Ferreira, and C. Graeff-Teixeira, “Detection of anti-oxidant enzymatic activities and purification of glutathione transferases from Angiostrongylus cantonensis,” Experimental Parasitology, vol. 127, no. 2, pp. 365–369, 2011. View at Publisher · View at Google Scholar · View at PubMed
  27. A. L. Morassutti, K. Levert, P. M. Pinto, A. J. da Silva, P. Wilkins, and C. Graeff-Teixeira, “Characterization of Angiostrongylus cantonensis excretory-secretory proteins as potential diagnostic targets,” Experimental Parasitology, vol. 130, no. 1, pp. 26–31, 2012. View at Publisher · View at Google Scholar · View at PubMed
  28. S. Donnelly, S. M. O'Neill, M. Sekiya, G. Mulcahy, and J. P. Dalton, “Thioredoxin peroxidase secreted by Fasciola hepatica induces the alternative activation of macrophages,” Infection and Immunity, vol. 73, no. 1, pp. 166–173, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  29. S. Donnelly, C. M. Stack, S. M. O'Neill, A. A. Sayed, D. L. Williams, and J. P. Dalton, “Helminth 2-Cys peroxiredoxin drives Th2 responses through a mechanism involving alternatively activated macrophages,” FASEB Journal, vol. 22, no. 11, pp. 4022–4032, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  30. A. A. Sayed, S. K. Cook, and D. L. Williams, “Redox balance mechanisms in Schistosoma mansoni rely on peroxiredoxins and albumin and implicate peroxiredoxins as novel drug targets,” Journal of Biological Chemistry, vol. 281, no. 25, pp. 17001–17010, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  31. F. U. Hartl and M. Hayer-Hartl, “Molecular chaperones in the cytosol: from nascent chain to folded protein,” Science, vol. 295, no. 5561, pp. 1852–1858, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  32. A. Zocevic, P. Mace, I. Vallee et al., “Identification of Trichinella spiralis early antigens at the pre-adult and adult stages,” Parasitology, pp. 1–9, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  33. B. Vergnes, B. Gourbal, I. Girard, S. Sundar, J. Drummelsmith, and M. Ouellette, “A proteomics screen implicates HSP83 and a small kinetoplastid calpain-related protein in drug resistance in Leishmania donovani clinical field isolates by modulating drug-induced programmed cell death,” Molecular and Cellular Proteomics, vol. 6, no. 1, pp. 88–101, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  34. F. Piano, A. J. Schetter, M. Mangone, L. Stein, and K. J. Kemphues, “RNAi analysis of genes expressed in the ovary of Caenorhabditis elegans,” Current Biology, vol. 10, no. 24, pp. 1619–1622, 2000. View at Publisher · View at Google Scholar · View at Scopus
  35. T. Inoue, K. Hirata, Y. Kuwana et al., “Cell cycle control by daf-21/Hsp90 at the first meiotic prophase/metaphase boundary during oogenesis in Caenorhabditis elegans,” Development Growth and Differentiation, vol. 48, no. 1, pp. 25–32, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  36. A. Lígia Bender, R. Lucyk Maurer, M. C. Fernandes da Silva et al., “Eggs and reproductive organs of female Angiostrongylus costaricensis are more intensely recognized by human sera from acute phase in abdominal anglostrongyliasis,” Revista da Sociedade Brasileira de Medicina Tropical, vol. 36, no. 4, pp. 449–454, 2003. View at Google Scholar · View at Scopus
  37. A. Oladiran and M. Belosevic, “Trypanosoma carassii hsp70 increases expression of inflammatory cytokines and chemokines in macrophages of the goldfish (Carassius auratus L.),” Developmental and Comparative Immunology, vol. 33, no. 10, pp. 1128–1136, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  38. F. Hauet-Broere, L. Wieten, T. Guichelaar, S. Berlo, R. Van Der Zee, and W. Van Eden, “Heat shock proteins induce T cell regulation of chronic inflammation,” Annals of the Rheumatic Diseases, vol. 65, no. 3, pp. iii65–iii68, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  39. D. R. Schultz and P. I. Arnold, “Heat shock (stress) proteins and autoimmunity in rheumatic diseases,” Seminars in Arthritis and Rheumatism, vol. 22, no. 6, pp. 357–374, 1993. View at Google Scholar · View at Scopus
  40. M. A. Toscano, A. G. Commodaro, J. M. Ilarregui et al., “Galectin-1 suppresses autoimmune retinal disease by promoting concomitant Th2- and T regulatory-mediated anti-inflammatory responses,” Journal of Immunology, vol. 176, no. 10, pp. 6323–6332, 2006. View at Google Scholar · View at Scopus
  41. S. Katoh, N. Ishii, A. Nobumoto et al., “Galectin-9 inhibits CD44-hyaluronan interaction and suppresses a murine model of allergic asthma,” American Journal of Respiratory and Critical Care Medicine, vol. 176, no. 1, pp. 27–35, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  42. J. P. Hewitson, Y. M. Harcus, R. S. Curwen et al., “The secretome of the filarial parasite, Brugia malayi: proteomic profile of adult excretory-secretory products,” Molecular and Biochemical Parasitology, vol. 160, no. 1, pp. 8–21, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. A. D. Klion and J. E. Donelson, “OvGa1BP, a filarial antigen with homology to vertebrate galactoside- binding proteins,” Molecular and Biochemical Parasitology, vol. 65, no. 2, pp. 305–315, 1994. View at Publisher · View at Google Scholar · View at Scopus
  44. C. H. Hokke and M. Yazdanbakhsh, “Schistosome glycans and innate immunity,” Parasite Immunology, vol. 27, no. 7-8, pp. 257–264, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  45. I. van Die and R. D. Cummings, “Glycan gimmickry by parasitic helminths: a strategy for modulating the host immune response?” Glycobiology, vol. 20, no. 1, pp. 2–12, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  46. E. van Liempt, S. J. van Vliet, A. Engering et al., “Schistosoma mansoni soluble egg antigens are internalized by human dendritic cells through multiple C-type lectins and suppress TLR-induced dendritic cell activation,” Molecular Immunology, vol. 44, no. 10, pp. 2605–2615, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  47. M. Kiel, P. Josh, A. Jones, R. Windon, P. Hunt, and K. Kongsuwan, “Identification of immuno-reactive proteins from a sheep gastrointestinal nematode, Trichostrongylus colubriformis, using two-dimensional electrophoresis and mass spectrometry,” International Journal for Parasitology, vol. 37, no. 13, pp. 1419–1429, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  48. M. S. Pearson, J. M. Bethony, D. A. Pickering et al., “An enzymatically inactivated hemoglobinase from Necator americanus induces neutralizing antibodies against multiple hookworm species and protects dogs against heterologous hookworm infection,” FASEB Journal, vol. 23, no. 9, pp. 3007–3019, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  49. P. S. Sijwali, J. Koo, N. Singh, and P. J. Rosenthal, “Gene disruptions demonstrate independent roles for the four falcipain cysteine proteases of Plasmodium falciparum,” Molecular and Biochemical Parasitology, vol. 150, no. 1, pp. 96–106, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  50. 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 PubMed · View at Scopus
  51. M. Sajid and J. H. McKerrow, “Cysteine proteases of parasitic organisms,” Molecular and Biochemical Parasitology, vol. 120, no. 1, pp. 1–21, 2002. View at Google Scholar · View at Scopus
  52. M. H. Shin, Y. B. Chung, and H. Kita, “Degranulation of human eosinophils induced by Paragonimus westermani-secreted protease,” The Korean Journal of Parasitology, vol. 43, no. 1, pp. 33–37, 2005. View at Google Scholar · View at Scopus
  53. Y. H. Liu, Y. P. Han, Z. Y. Li et al., “Molecular cloning and characterization of cystatin, a cysteine protease inhibitor, from Angiostrongylus cantonensis,” Parasitology Research, vol. 107, no. 4, pp. 915–922, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  54. S. Hartmann and R. Lucius, “Modulation of host immune responses by nematode cystatins,” International Journal for Parasitology, vol. 33, no. 11, pp. 1291–1302, 2003. View at Publisher · View at Google Scholar · View at Scopus
  55. T. Zavasnik-Bergant, “Cystatin protease inhibitors and immune functions,” Frontiers in Bioscience, vol. 13, no. 12, pp. 4625–4637, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. C. Schnoeller, S. Rausch, S. Pillai et al., “A helminth immunomodulator reduces allergic and inflammatory responses by induction of IL-10-producing macrophages,” Journal of Immunology, vol. 180, no. 6, pp. 4265–4272, 2008. View at Google Scholar · View at Scopus
  57. A. Delaney, A. Williamson, A. Brand et al., “Cloning and characterisation of an aspartyl protease inhibitor (API-1) from Ancylostoma hookworms,” International Journal for Parasitology, vol. 35, no. 3, pp. 303–313, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  58. W. Fang, S. Xu, Y. Wang et al., “ES proteins analysis of Angiostrongylus cantonensis: products of the potential parasitism genes?” Parasitology Research, vol. 106, no. 5, pp. 1027–1032, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus