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BioMed Research International
Volume 2015, Article ID 416712, 8 pages
http://dx.doi.org/10.1155/2015/416712
Research Article

Iron-Binding Protein Degradation by Cysteine Proteases of Naegleria fowleri

1Department of Infectomics and Molecular Pathogenesis, Center for Research and Advanced Studies of the National Polytechnic Institute, Avenida IPN 2508, 07360 Mexico City, Mexico
2Department of Cell Biology, Center for Research and Advanced Studies of the National Polytechnic Institute, Avenida IPN 2508, 07360 Mexico City, Mexico
3Faculty of Professional Studies, Autonomous University of Mexico, Campus Cuautitlán, Km 2.5 Carretera Cuautitlán-Teoloyucan, 54714 Cuautitlán Izcalli, Mexico

Received 22 September 2014; Revised 17 December 2014; Accepted 19 December 2014

Academic Editor: Mehdi Chenik

Copyright © 2015 Moisés Martínez-Castillo 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. S. Rojas-Hernández, M. A. Rodríguez-Monroy, R. López-Revilla, A. A. Reséndiz-Albor, and L. Moreno-Fierros, “Intranasal coadministration of the Cry1Ac protoxin with amoebal lysates increases protection against Naegleria fowleri meningoencephalitis,” Infection and Immunity, vol. 72, no. 8, pp. 4368–4375, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Shibayama, J. D. J. Serrano-Luna, S. Rojas-Hernández, R. Campos-Rodríguez, 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. View at Publisher · View at Google Scholar · View at Scopus
  3. R. F. Carter, “Description of a Naegleria sp. isolated from two cases of primary amoebic meningo-encephalitis, and of the experimental pathological changes induced by it,” Journal of Pathology, vol. 100, no. 4, pp. 217–244, 1970. View at Publisher · View at Google Scholar · View at Scopus
  4. K. L. Jarolim, J. K. McCosh, and M. J. Howard, “The role of blood vessels and lungs in the dissemination of Naegleria fowleri following intranasal inoculation in mice,” Folia Parasitologica, vol. 49, no. 3, pp. 183–188, 2002. View at Publisher · View at Google Scholar · View at Scopus
  5. K. L. Jarolim, J. K. McCosh, M. J. Howard, and D. T. John, “A light microscopy study of the migration of Naegleria fowleri from the nasal submucosa to the central nervous system during the early stage of primary amebic meningoencephalitis in mice,” Journal of Parasitology, vol. 86, no. 1, pp. 50–55, 2000. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Rojas-Hernández, A. Jarillo-Luna, M. Rodríguez-Monroy, L. Moreno-Fierros, and R. Campos-Rodríguez, “Immunohistochemical characterization of the initial stages of Naegleria fowleri meningoencephalitis in mice,” Parasitology Research, vol. 94, no. 1, pp. 31–36, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. I. Cervantes-Sandoval, J. D. J. Serrano-Luna, E. García-Latorre, V. Tsutsumi, and M. Shibayama, “Characterization of brain inflammation during primary amoebic meningoencephalitis,” Parasitology International, vol. 57, no. 3, pp. 307–313, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. R. M. Hysmith and R. C. Franson, “Elevated levels of cellular and extracellular phospholipases from pathogenic Naegleria fowleri,” Biochimica et Biophysica Acta, vol. 711, no. 1, pp. 26–32, 1982. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Das, A. K. Saha, T. A. Nerad et al., “Partial purification and characterization of Naegleria fowleriβ-glucosidase,” The Journal of Protozoology, vol. 34, no. 1, pp. 68–74, 1987. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Ferrante and E. J. Bates, “Elastase in the pathogenic free-living amoebae Naegleria and Acanthamoeba spp.,” Infection and Immunity, vol. 56, no. 12, pp. 3320–3321, 1988. View at Google Scholar · View at Scopus
  11. R. Herbst, C. Ott, T. Jacobs, T. Marti, F. Marciano-Cabral, and M. Leippe, “Pore-forming polypeptides of the pathogenic protozoon Naegleria fowleri,” The Journal of Biological Chemistry, vol. 277, no. 25, pp. 22353–22360, 2002. View at Publisher · View at Google Scholar · View at Scopus
  12. J. Lee, J.-H. Kim, H.-J. Sohn et al., “Novel cathepsin B and cathepsin B-like cysteine protease of Naegleria fowleri excretory-secretory proteins and their biochemical properties,” Parasitology Research, vol. 113, no. 8, pp. 2765–2776, 2014. View at Publisher · View at Google Scholar · View at Scopus
  13. I. Cervantes-Sandoval, J. D. J. Serrano-Luna, E. García-Latorre, V. Tsutsumi, and M. Shibayama, “Mucins in the host defence against Naegleria fowleri and mucinolytic activity as a possible means of evasion,” Microbiology, vol. 154, no. 12, pp. 3895–3904, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. D. Eisen and R. C. Franson, “Acid-active neuraminidases in the growth media from cultures of pathogenic Naegleria fowleri and in sonicates of rabbit alveolar macrophages,” Biochimica et Biophysica Acta, vol. 924, no. 2, pp. 369–372, 1987. View at Publisher · View at Google Scholar · View at Scopus
  15. E. P. Skaar, “The battle for iron between bacterial pathogens and their vertebrate hosts,” PLoS Pathogens, vol. 6, no. 8, Article ID e1000949, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. A. Morgenthau, A. Pogoutse, P. Adamiak, T. F. Moraes, and A. B. Schryvers, “Bacterial receptors for host transferrin and lactoferrin: molecular mechanisms and role in host-microbe interactions,” Future Microbiology, vol. 8, no. 12, pp. 1575–1585, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. P. W. Whitby, T. M. VanWagoner, J. M. Springer, D. J. Morton, T. W. Seale, and T. L. Stull, “Burkholderia cenocepacia utilizes ferritin as an iron source,” Journal of Medical Microbiology, vol. 55, no. 6, pp. 661–668, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. G. Ortíz-Estrada, S. Luna-Castro, C. Piña-Vázquez et al., “Iron-saturated lactoferrin and pathogenic protozoa: could this protein be an iron source for their parasitic style of life?” Future Microbiology, vol. 7, no. 1, pp. 149–164, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. M. E. Wilson, R. W. Vorhies, K. A. Andersen, and B. E. Britigan, “Acquisition of iron from transferrin and lactoferrin by the protozoan Leishmania chagasi,” Infection and Immunity, vol. 62, no. 8, pp. 3262–3269, 1994. View at Google Scholar · View at Scopus
  20. N. León-Sicairos, M. Reyes-López, A. Canizalez-Román et al., “Human hololactoferrin: endocytosis and use as an iron source by the parasite Entamoeba histolytica,” Microbiology, vol. 151, no. 12, pp. 3859–3871, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Serrano-Luna, I. Cervantes-Sandoval, V. Tsutsumi, and M. Shibayama, “A biochemical comparison of proteases from pathogenic Naegleria fowleri and non-pathogenic Naegleria gruberi,” Journal of Eukaryotic Microbiology, vol. 54, no. 5, pp. 411–417, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Bradford, “A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing mthe principle of protein-dye binding,” Analytical Biochemistry, vol. 72, no. 1, pp. 248–254, 1976. View at Publisher · View at Google Scholar · View at Scopus
  23. D. E. Kyle and G. P. Noblet, “Vertical distribution of potentially pathogenic free-living amoebae in freshwater lakes,” Journal of Protozoology, vol. 32, no. 1, pp. 99–105, 1985. View at Publisher · View at Google Scholar · View at Scopus
  24. J. K. Actor, S.-A. Hwang, and M. L. Kruzel, “Lactoferrin as a natural immune modulator,” Current Pharmaceutical Design, vol. 15, no. 17, pp. 1956–1973, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. A. J. Psaltis, M. A. Bruhn, E. H. Ooi, L. W. Tan, and P.-J. Wormald, “Nasal mucosa expression of lactoferrin in patients with chronic rhinosinusitis,” The Laryngoscope, vol. 117, no. 11, pp. 2030–2035, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. A. L. Newsome and W. E. Wilhelm, “Inhibition of Naegleria fowleri by microbial iron-chelating agents: ecological implications,” Applied and Environmental Microbiology, vol. 45, no. 2, pp. 665–668, 1983. View at Google Scholar · View at Scopus
  27. S. G. Bradley, D. M. Toney, Y. Zhang, and F. Marciano-Cabral, “Dependence of growth, metabolic expression, and pathogenicity of Naegleria fowleri on exogenous porphyrins,” The Journal of Parasitology, vol. 82, no. 5, pp. 763–768, 1996. View at Publisher · View at Google Scholar · View at Scopus
  28. R. N. Band and W. Balamuth, “Hemin replaces serum as a growth requirement for Naegleria,” Journal of Applied Microbiology, vol. 28, no. 1, pp. 64–65, 1974. View at Google Scholar · View at Scopus
  29. A. L. Newsome and W. E. Wilhelm, “Effect of exogenous iron on the viability of pathogenic Naegleria fowleri in serum,” Experientia, vol. 37, no. 11, pp. 1160–1162, 1981. View at Publisher · View at Google Scholar · View at Scopus
  30. F. López-Soto, N. León-Sicairos, M. Reyes-López et al., “Use and endocytosis of iron-containing proteins by Entamoeba histolytica trophozoites,” Infection, Genetics and Evolution, vol. 9, no. 6, pp. 1038–1050, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. M. W. Rey, S. L. Woloshuk, H. A. De Boer, and F. R. Pieper, “Complete nucleotide sequence of human mammary gland lactoferrin,” Nucleic Acids Research, vol. 18, no. 17, p. 5288, 1990. View at Publisher · View at Google Scholar · View at Scopus
  32. A. Pierce, D. Colavizza, M. Benaissa et al., “Molecular cloning and sequence analysis of bovine lactotransferrin,” European Journal of Biochemistry, vol. 196, no. 1, pp. 177–184, 1991. View at Publisher · View at Google Scholar · View at Scopus
  33. H. Riechelmann, T. Deutschle, E. Friemel, H. J. Gross, and M. Bachem, “Biological markers in nasal secretions,” European Respiratory Journal, vol. 21, no. 4, pp. 600–605, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. C. Fillebeen, L. Descamps, M.-P. Dehouck et al., “Receptor-mediated transcytosis of lactoferrin through the blood-brain barrier,” The Journal of Biological Chemistry, vol. 274, no. 11, pp. 7011–7017, 1999. View at Publisher · View at Google Scholar · View at Scopus
  35. P. P. Ward, E. Paz, and O. M. Conneely, “Multifunctional roles of lactoferrin: a critical overview,” Cellular and Molecular Life Sciences, vol. 62, no. 22, pp. 2540–2548, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. J. R. Connor, S. L. Menzies, S. M. St. Martin, and E. J. Mufson, “Cellular distribution of transferrin, ferritin, and iron in normal and aged human brains,” Journal of Neuroscience Research, vol. 27, no. 4, pp. 595–611, 1990. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Fleming and J. G. Joshi, “Ferritin: isolation of aluminum-ferritin complex from brain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 84, no. 22, pp. 7866–7870, 1987. View at Publisher · View at Google Scholar · View at Scopus
  38. S. A. Benkovic and J. R. Connor, “Ferritin, transferrin, and iron in selected regions of the adult and aged rat brain,” Journal of Comparative Neurology, vol. 338, no. 1, pp. 97–113, 1993. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Jane, I. Roskams, and J. R. Connor, “Iron, transferrin, and ferritin in the rat brain during development and aging,” Journal of Neurochemistry, vol. 63, no. 2, pp. 709–716, 1994. View at Google Scholar · View at Scopus
  40. A. J. Martinez, E. C. Nelson, and R. J. Duma, “Animal model of human disease. Primary amebic meningoencephalitis, Naegleria meningoencephalitis, CNS protozoal infection,” The American Journal of Pathology, vol. 73, no. 2, pp. 545–548, 1973. View at Google Scholar · View at Scopus
  41. A. Sroka, M. Sztukowska, J. Potempa, J. Travis, and C. A. Genco, “Degradation of host heme proteins by lysine- and arginine-specific cysteine proteinases (gingipains) of Porphyromonas gingivalis,” Journal of Bacteriology, vol. 183, no. 19, pp. 5609–5616, 2001. View at Publisher · View at Google Scholar · View at Scopus
  42. A. H. T. Hissen, J. M. T. Chow, L. J. Pinto, and M. M. Moore, “Survival of Aspergillus fumigatus in serum involves removal of iron from transferrin: the role of siderophores,” Infection and Immunity, vol. 72, no. 3, pp. 1402–1408, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. J. F. Alderete, K. M. Peterson, and J. B. Baseman, “Affinities of Treponema pallidum for human lactoferrin and transferrin,” Genitourinary Medicine, vol. 64, no. 6, pp. 359–363, 1988. View at Google Scholar · View at Scopus
  44. 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 Publisher · View at Google Scholar · View at Scopus
  45. C. A. King and T. M. Preston, “Studies of anionic sites on the cell surface of the amoeba Naegleria gruberi using cationized ferritin,” Journal of Cell Science, vol. 28, pp. 133–149, 1977. View at Google Scholar · View at Scopus
  46. A. Ferrante and Y. H. Thong, “Antibody induced capping and endocytosis of surface antigens in Naegleria fowleri,” International Journal for Parasitology, vol. 9, no. 6, pp. 599–601, 1979. View at Publisher · View at Google Scholar · View at Scopus
  47. E. C. Theil, “Ferritin: structure, gene regulation, and cellular function in animals, plants, and microorganisms,” Annual Review of Biochemistry, vol. 56, pp. 289–315, 1987. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Scaglia, S. Gatti, R. Brustia, G. Chichino, and E. G. Rondanelli, “Phagocytosis of human erythrocytes by Naegleria is not related to species pathogenicity. A phase-contrast cinemicrographic study,” Microbiologica, vol. 14, no. 1, pp. 45–53, 1991. View at Google Scholar · View at Scopus
  49. P. Alonso and E. Zubiaur, “Phagocytic activity of three Naegleria strains in the presence of erythrocytes of various types,” Journal of Protozoology, vol. 32, no. 4, pp. 661–664, 1985. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Pynnonen, R. E. Stephenson, K. Schwartz, M. Hernandez, and B. R. Boles, “Hemoglobin promotes Staphylococcus aureus nasal colonization,” PLoS Pathogens, vol. 7, no. 7, Article ID e1002104, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. A. B. Vermelho, M. N. L. Meirelles, A. Lopes, S. D. G. Petinate, A. A. Chaia, and M. H. Branquinha, “Detection of extracellular proteases from microorganisms on agar plates,” Memorias do Instituto Oswaldo Cruz, vol. 91, no. 6, pp. 755–760, 1996. View at Publisher · View at Google Scholar · View at Scopus
  52. D. Talamás-Lara, B. Chávez-Munguía, A. González-Robles et al., “Erythrophagocytosis in Entamoeba histolytica and Entamoeba dispar: a comparative study,” BioMed Research International, vol. 2014, Article ID 626259, 10 pages, 2014. View at Publisher · View at Google Scholar
  53. V. Tsutsumi, A. Ramírez-Rosales, H. Lanz-Mendoza et al., “Entamoeba histolytica: erythrophagocytosis, collagenolysis, and liver abscess production as virulence markers,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 86, no. 2, pp. 170–172, 1992. View at Publisher · View at Google Scholar · View at Scopus
  54. A. J. Barrett, “Classification of peptidases,” Methods in Enzymology, vol. 244, pp. 1–15, 1994. View at Publisher · View at Google Scholar · View at Scopus
  55. H. J. Atkinson, P. C. Babbitt, and M. Sajid, “The global cysteine peptidase landscape in parasites,” Trends in Parasitology, vol. 25, no. 12, pp. 573–581, 2009. View at Publisher · View at Google Scholar · View at Scopus
  56. J. C. Mottram, M. J. Helms, G. H. Coombs, and M. Sajid, “Clan CD cysteine peptidases of parasitic protozoa,” Trends in Parasitology, vol. 19, no. 4, pp. 182–187, 2003. View at Publisher · View at Google Scholar · View at Scopus