About this Journal Submit a Manuscript Table of Contents
Journal of Biomedicine and Biotechnology
Volume 2010 (2010), Article ID 591079, 10 pages
Research Article

Progesterone Induces Scolex Evagination of the Human Parasite Taenia solium: Evolutionary Implications to the Host-Parasite Relationship

1Departamento de Biología, Facultad de Química, Universidad Nacional Autónoma de México, AP 70228, 04510 México, DF, Mexico
2Departamento de Inmunología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, AP 70228, 04510 México, DF, Mexico
3Instituto de Biología, Universidad Nacional Autónoma de México, 04510 México, DF, Mexico

Received 30 July 2009; Accepted 14 September 2009

Academic Editor: Luis I. Terrazas

Copyright © 2010 Galileo Escobedo 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. T. E. Nash, G. Singh, A. C. White, et al., “Treatment of neurocysticercosis: current status and future research needs,” Neurology, vol. 67, no. 7, pp. 1120–1127, 2006.
  2. H. H. Garcia and O. H. Del Brutto, “Neurocysticercosis: updated concepts about an old disease,” The Lancet Neurology, vol. 4, no. 10, pp. 653–661, 2005.
  3. A. Flisser, E. Sarti, M. Lightowlers, and P. Schantz, “Neurocysticercosis: regional status, epidemiology, impact and control measures in the Americas,” Acta Tropica, vol. 87, no. 1, pp. 43–51, 2003. View at Publisher · View at Google Scholar
  4. A. C. White Jr., “Neurocysticercosis: a major cause of neurological disease worldwide,” Clinical Infectious Diseases, vol. 24, no. 2, pp. 101–113, 1997.
  5. P. C. Fan and W. C. Chung, “Sociocultural factors and local customs related to taeniasis in east Asia,” The Kaohsiung Journal of Medical Sciences, vol. 13, no. 11, pp. 647–652, 1997.
  6. A. E. Gonzalez, C. Gavidia, N. Falcon, et al., “Protection of pigs with cysticercosis from further infections after treatment with oxfendazole,” The American Journal of Tropical Medicine and Hygiene, vol. 65, no. 1, pp. 15–18, 2001.
  7. Z. Pawlowski, J. Allan, and E. Sarti, “Control of Taenia solium taeniasis/cysticercosis: from research towards implementation,” International Journal for Parasitology, vol. 35, no. 11-12, pp. 1221–1232, 2005. View at Publisher · View at Google Scholar · View at PubMed
  8. C. Barton Behravesh, L. F. Mayberry, J. R. Bristol, et al., “Population-based survey of taeniasis along the United States-Mexico border,” Annals of Tropical Medicine and Parasitology, vol. 102, no. 4, pp. 325–333, 2008.
  9. A. C. Moore, L. I. Lutwick, P. M. Schantz, et al., “Seroprevalence of cysticercosis in an Orthodox Jewish community,” The American Journal of Tropical Medicine and Hygiene, vol. 53, no. 5, pp. 439–442, 1995.
  10. P. M. Schantz, A. C. Moore, J. L. Munoz, et al., “Neurocysticercosis in an Orthodox Jewish community in New York City,” The New England Journal of Medicine, vol. 327, no. 10, pp. 692–695, 1992.
  11. M. T. Rabiela, Y. Hornelas, C. Garcia-Allan, E. Rodriguez-del-Rosal, and A. Flisser, “Evagination of Taenia solium cysticerci: a histologic and electron microscopy study,” Archives of Medical Research, vol. 31, no. 6, pp. 605–607, 2000. View at Publisher · View at Google Scholar
  12. G. Escobedo, L. Lopez-Griego, and J. Morales-Montor, “Neuroimmunoendocrine modulation in the host by helminth parasites: a novel form of host-parasite coevolution?” NeuroImmunomodulation, vol. 16, no. 2, pp. 78–87, 2009. View at Publisher · View at Google Scholar · View at PubMed
  13. O. Bottasso and J. Morales-Montor, “Neuroimmunomodulation during infectious diseases: mechanisms, causes and consequences for the host,” NeuroImmunomodulation, vol. 16, no. 2, pp. 65–67, 2009. View at Publisher · View at Google Scholar · View at PubMed
  14. H. S. Thabet, S. S. Thabet, N. M. Ali, and N. S. Ahmed, “Effects of ovariectomy and thyroidectomy on course and outcome of Trichinella spiralis infection in rat,” Journal of the Egyptian Society of Parasitology, vol. 38, no. 1, pp. 29–46, 2008.
  15. Y. Osorio, D. L. Bonilla, A. G. Peniche, P. C. Melby, and B. L. Travi, “Pregnancy enhances the innate immune response in experimental cutaneous leishmaniasis through hormone-modulated nitric oxide production,” Journal of Leukocyte Biology, vol. 83, no. 6, pp. 1413–1422, 2008. View at Publisher · View at Google Scholar · View at PubMed
  16. C. D. Santos, M. P. Toldo, F. H. Santello, V. Filipin Mdel, V. Brazao, and J. C. do Prado Junior, “Dehydroepiandrosterone increases resistance to experimental infection by Trypanosoma cruzi,” Veterinary Parasitology, vol. 153, no. 3-4, pp. 238–243, 2008.
  17. J. Morales-Montor, G. Escobedo, J. A. Vargas-Villavicencio, and C. Larralde, “The neuroimmunoendocrine network in the complex host-parasite relationship during murine cysticercosis,” Current Topics in Medicinal Chemistry, vol. 8, no. 5, pp. 400–407, 2008. View at Publisher · View at Google Scholar
  18. N. Pena, J. Morales, J. Morales-Montor, et al., “Impact of naturally acquired Taenia solium cysticercosis on the hormonal levels of free ranging boars,” Veterinary Parasitology, vol. 149, no. 1-2, pp. 134–137, 2007.
  19. J. Morales, T. Velasco, V. Tovar, et al., “Castration and pregnancy of rural pigs significantly increase the prevalence of naturally acquired Taenia solium cysticercosis,” Veterinary Parasitology, vol. 108, no. 1, pp. 41–48, 2002.
  20. F. W. Bazer, R. C. Burghardt, G. A. Johnson, T. E. Spencer, and G. Wu, “Interferons and progesterone for establishment and maintenance of pregnancy: interactions among novel cell signaling pathways,” Reproductive Biology, vol. 8, no. 3, pp. 179–211, 2008.
  21. G. Escobedo, C. Larralde, A. Chavarria, M. A. Cerbon, and J. Morales-Montor, “Molecular mechanisms involved in the differential effects of sex steroids on the reproduction and infectivity of Taenia crassiceps,” Journal of Parasitology, vol. 90, no. 6, pp. 1235–1244, 2004. View at Publisher · View at Google Scholar
  22. L. I. Terrazas, R. Bojalil, T. Govezensky, and C. Larraide, “A role for 17-β-estradiol in immunoendocrine regulation of murine cysticercosis (Taenia crassiceps),” Journal of Parasitology, vol. 80, no. 4, pp. 563–568, 1994.
  23. J. Morales-Montor, S. Baig, C. Hallal-Calleros, and R. T. Damian, “Taenia crassiceps: androgen reconstitution of the host leads to protection during cysticercosis,” Experimental Parasitology, vol. 100, no. 4, pp. 209–216, 2002. View at Publisher · View at Google Scholar
  24. J. A. Vargas-Villavicencio, C. Larralde, and J. Morales-Montor, “Gonadectomy and progesterone treatment induce protection in murine cysticercosis,” Parasite Immunology, vol. 28, no. 12, pp. 667–674, 2006. View at Publisher · View at Google Scholar · View at PubMed
  25. P. Ascenzi, A. Bocedi, and M. Marino, “Structure-function relationship of estrogen receptor α and β: impact on human health,” Molecular Aspects of Medicine, vol. 27, no. 4, pp. 299–402, 2006. View at Publisher · View at Google Scholar · View at PubMed
  26. R. A. Hiipakka and S. Liao, “Molecular mechanism of androgen action,” Trends in Endocrinology and Metabolism, vol. 9, no. 8, pp. 317–324, 1998. View at Publisher · View at Google Scholar
  27. S. Gadkar-Sable, C. Shah, G. Rosario, G. Sachdeva, and C. Puri, “Progesterone receptors: various forms and functions in reproductive tissues,” Frontiers in Bioscience, vol. 10, pp. 2118–2130, 2005.
  28. C. Guerra-Araiza, A. Coyoy-Salgado, and I. Camacho-Arroyo, “Sex differences in the regulation of progesterone receptor isoforms expression in the rat brain,” Brain Research Bulletin, vol. 59, no. 2, pp. 105–109, 2002. View at Publisher · View at Google Scholar
  29. F. Remoue, J. C. Mani, M. Pugniere, A. M. Schacht, A. Capron, and G. Riveau, “Functional specific binding of testosterone to Schistosoma haematobium 28-kilodalton glutathione S-transferase,” Infection and Immunity, vol. 70, no. 2, pp. 601–605, 2002. View at Publisher · View at Google Scholar
  30. C. Konrad, A. Kroner, M. Spiliotis, R. Zavala-Gongora, and K. Brehm, “Identification and molecular characterisation of a gene encoding a member of the insulin receptor family in Echinococcus multilocularis,” International Journal for Parasitology, vol. 33, no. 3, pp. 301–312, 2003. View at Publisher · View at Google Scholar
  31. I. Bhai and A. K. Pandey, “Gonadal hormones in experimental Ancylostoma caninum infections in male Swiss albino mice,” International Journal for Parasitology, vol. 12, no. 6, pp. 589–591, 1982. View at Publisher · View at Google Scholar
  32. J. Morales-Montor, F. Mohamed, A. M. Ghaleb, S. Baig, C. Hallal-Callerost, and R. T. Damian, “In vitro effects of hypothalamic-pituitary-adrenal axis (HPA) hormones on Schistosoma mansoni,” Journal of Parasitology, vol. 87, no. 5, pp. 1132–1139, 2001.
  33. G. Escobedo, C. W. Roberts, J. C. Carrero, and J. Morales-Montor, “Parasite regulation by host hormones: an old mechanism of host exploitation?” Trends in Parasitology, vol. 21, no. 12, pp. 588–593, 2005. View at Publisher · View at Google Scholar · View at PubMed
  34. R. T. Damian, “Parasite immune evasion and exploitation: reflections and projections,” Parasitology, vol. 115, supplement, pp. S169–S175, 1997.
  35. M. Shibayama, J. Serrano-Luna Jde, S. Rojas-Hernandez, R. Campos-Rodriguez, and V. Tsutsumi, “Interaction of secretory immunoglobulin A antibodies with Naegleria fowleri trophozoites and collagen type I,” Canadian Journal of Microbiology, vol. 49, no. 3, pp. 164–170, 2003.
  36. M. Spiliotis, C. Konrad, V. Gelmedin, et al., “Characterisation of EmMPK1, an ERK-like MAP kinase from Echinococcus multilocularis which is activated in response to human epidermal growth factor,” International Journal for Parasitology, vol. 36, no. 10-11, pp. 1097–1112, 2006.
  37. K. Brehm and M. Spiliotis, “The influence of host hormones and cytokines on Echinococcus multilocuiaris signalling and development,” Parasite, vol. 15, no. 3, pp. 286–290, 2008.
  38. G. W. Esch and J. D. Smyth, “Studies on the in vitro culture of Taenia crassiceps,” International Journal for Parasitology, vol. 6, no. 2, pp. 143–149, 1976. View at Publisher · View at Google Scholar
  39. J. Morales-Montor, G. Escobedo, M. Rodriguez-Dorantes, N. Tellez-Ascencio, M. A. Cerbon, and C. Larralde, “Differential expression of AP-1 transcription factor genes c-fos and c-jun in the helminth parasites Taenia crassiceps and Taenia solium,” Parasitology, vol. 129, no. 2, pp. 233–243, 2004. View at Publisher · View at Google Scholar
  40. J. D. Thompson, D. G. Higgins, and T. J. Gibson, “CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice,” Nucleic Acids Research, vol. 22, no. 22, pp. 4673–4680, 1994.
  41. J. Felsenstein, PHYLIP (Phylogeny Inference Package), Version 3.572, University of Washington, Seattle, Wash, USA, 1999.
  42. D. L. Swofford, PAUP 4.0b10. Phylogenetic Analysis Using Parsimony (and Other Methods), Sinauer, Sunderland, Mass, USA, 2002.
  43. E. Cabrera-Munoz, A. Gonzalez-Arenas, M. Saqui-Salces, et al., “Regulation of progesterone receptor isoforms content in human astrocytoma cell lines,” The Journal of Steroid Biochemistry and Molecular Biology, vol. 113, no. 1-2, pp. 80–84, 2009.
  44. A. Gonzalez-Arenas, T. Neri-Gomez, C. Guerra-Araiza, and I. Camacho-Arroyo, “Sexual dimorphism in the content of progesterone and estrogen receptors, and their cofactors in the lung of adult rats,” Steroids, vol. 69, no. 5, pp. 351–356, 2004. View at Publisher · View at Google Scholar · View at PubMed
  45. I. Camacho-Arroyo, G. Gonzalez-Aguero, A. Gamboa-Dominguez, M. A. Cerbon, and R. Ondarza, “Progesterone receptor isoforms expression pattern in human chordomas,” Journal of Neurooncology, vol. 49, no. 1, pp. 1–7, 2000. View at Publisher · View at Google Scholar
  46. I. Camacho-Arroyo, C. Guerra-Araiza, and M. A. Cerbon, “Progesterone receptor isoforms are differentially regulated by sex steroids in the rat forebrain,” Neuroreport, vol. 9, no. 18, pp. 3993–3996, 1998.
  47. O. A. Sukocheva, Y. Yang, and J. F. Gierthy, “Estrogen and progesterone interactive effects in postconfluent MCF-7 cell culture,” Steroids, vol. 74, no. 4-5, pp. 410–418, 2009. View at Publisher · View at Google Scholar · View at PubMed
  48. C. L. Gibson, L. J. Gray, P. M. Bath, and S. P. Murphy, “Progesterone for the treatment of experimental brain injury; a systematic review,” Brain, vol. 131, no. 2, pp. 318–328, 2008. View at Publisher · View at Google Scholar · View at PubMed
  49. E. R. Norwitz, V. Snegovskikh, F. Schatz, et al., “Progestin inhibits and thrombin stimulates the plasminogen activator/inhibitor system in term decidual stromal cells: implications for parturition,” American Journal of Obstetrics and Gynecology, vol. 196, no. 4, pp. e381–e388, 2007.
  50. C. L. Butts, S. A. Shukair, K. M. Duncan, et al., “Progesterone inhibits mature rat dendritic cells in a receptor-mediated fashion,” International Immunology, vol. 19, no. 3, pp. 287–296, 2007.
  51. H. Aguilar-Diaz, R. J. Bobes, J. C. Carrero, et al., “The genome project of Taenia solium,” Parasitology International, vol. 55, supplement, pp. S127–S130, 2006.
  52. H. Loosfelt, F. Logeat, M. T. Vu Hai, and E. Milgrom, “The rabbit progesterone receptor. Evidence for a single steroid-binding subunit and characterization of receptor mRNA,” The Journal of Biological Chemistry, vol. 259, no. 22, pp. 14196–14202, 1984.
  53. I. Camacho-Arroyo, A. M. Pasapera, and M. A. Cerbon, “Regulation of progesterone receptor gene expression by sex steroid hormones in the hypothalamus and the cerebral cortex of the rabbit,” Neuroscience Letters, vol. 214, no. 1, pp. 25–28, 1996. View at Publisher · View at Google Scholar
  54. J. C. Leo and V. C. Lin, “The activities of progesterone receptor isoform A and B are differentially modulated by their ligands in a gene-selective manner,” International Journal of Cancer, vol. 122, no. 1, pp. 230–243, 2008. View at Publisher · View at Google Scholar · View at PubMed
  55. A. Shatnawi, T. Tran, and M. Ratnam, “R5020 and RU486 act as progesterone receptor agonists to enhance Sp1/Sp4-dependent gene transcription by an indirect mechanism,” Molecular Endocrinology, vol. 21, no. 3, pp. 635–650, 2007. View at Publisher · View at Google Scholar · View at PubMed