1887

Abstract

is an amoeboflagellate responsible for the fatal central nervous system (CNS) disease primary amoebic meningoencephalitis (PAM). This amoeba gains access to the CNS by invading the olfactory mucosa and crossing the cribriform plate. Studies using a mouse model of infection have shown that the host secretes mucus during the very early stages of infection, and this event is followed by an infiltration of neutrophils into the nasal cavity. In this study, we investigated the role of trophozoites in inducing the expression and secretion of airway mucin and pro-inflammatory mediators. Using the human mucoepidermal cell line NCI-H292, we demonstrated that induced the expression of the MUC5AC gene and protein and the pro-inflammatory mediators interleukin-8 (IL-8) and interleukin-1 (IL-1), but not tumour necrosis factor- or chemokine c-c motif ligand 11 (eotaxin). Since the production of reactive oxygen species (ROS) is a common phenomenon involved in the signalling pathways of these molecules, we analysed if trophozoites were capable of causing ROS production in NCI-H292 cells by detecting oxidation of the fluorescent probe 2,7-dichlorofluorescein diacetate. NCI-H292 cells generated ROS after 15–30 min of trophozoite stimulation. Furthermore, the expression of MUC5AC, IL-8 and IL-1 was inhibited in the presence of the ROS scavenger DMSO. In addition, the use of an epidermal growth factor receptor inhibitor decreased the expression of MUC5AC and IL-8, but not IL-1. We conclude that induces the expression of some host innate defence mechanisms, such as mucin secretion (MUC5AC) and local inflammation (IL-8 and IL-1) in respiratory epithelial cells via ROS production and suggest that these innate immune mechanisms probably prevent most PAM infections.

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2009-11-01
2019-10-16
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References

  1. Carter, R. F. ( 1970; ). Description of a Naegleria sp. isolated from two cases of primary amoebic meningo-encephalitis, and of the experimental pathological changes induced by it. J Pathol 100, 217–244.[CrossRef]
    [Google Scholar]
  2. Cervantes-Sandoval, I., Serrano-Luna, J. J., García-Latorre, E., Tsutsumi, V. & Shibayama, M. ( 2008a; ). Characterization of brain inflammation during primary amoebic meningoencephalitis. Parasitol Int 57, 307–313.[CrossRef]
    [Google Scholar]
  3. Cervantes-Sandoval, I., Serrano Luna, J. J., García-Latorre, E., Tsutsumi, V. & Shibayama, M. ( 2008b; ). Mucins in host defence against Naegleria fowleri and mucinolytic activity as a possible means of evasion. Microbiology 154, 3895–3904.[CrossRef]
    [Google Scholar]
  4. Cursons, R. T., Brown, T. J., Keys, E. A., Moriarty, K. M. & Till, D. ( 1980; ). Immunity to pathogenic free-living amoebae: role of cell-mediated immunity. Infect Immun 29, 408–410.
    [Google Scholar]
  5. Edwards, J. H., Griffiths, A. J. & Mullins, J. ( 1976; ). Protozoa as sources of antigen in ‘humidifier fever’. Nature 264, 438–439.[CrossRef]
    [Google Scholar]
  6. Ferrante, A. ( 1989; ). Augmentation of the neutrophil response to the Naegleria fowleri by tumor necrosis factor alpha. Infect Immun 57, 3110–3115.
    [Google Scholar]
  7. Ferrante, A. & Mocatta, T. J. ( 1984; ). Human neutrophils require activation by mononuclear leucocytes conditioned medium to kill the pathogenic free-living amoeba, Naegleria fowleri. Clin Exp Immunol 56, 559–566.
    [Google Scholar]
  8. Ferrante, A., Carter, R. F., Lopez, A. F., Rowan-Kelly, B., Hill, N. L. & Vadas, M. A. ( 1988; ). Depression of immunity to Naegleria fowleri in mice by selective depletion of neutrophils with a monoclonal antibody. Infect Immun 56, 2286–2291.
    [Google Scholar]
  9. Ferrante, A., Hill, N. L., Goh, D. H. & Kumaritilake, L. ( 1989; ). Altered neutrophils in mice immune to experimental Naegleria amoebic meningoencephalitis. Immunol Lett 22, 301–305.[CrossRef]
    [Google Scholar]
  10. Hsu, H. Y. & Wen, M. H. ( 2002; ). Lipopolysaccharide-mediated reactive oxygen species and signal transduction in the regulation of interleukin-1 gene expression. J Biol Chem 277, 22131–22139.[CrossRef]
    [Google Scholar]
  11. Ibelgaufts, H. ( 1995; ). Cytokines Dictionary. Wenheim, Germany: Wiley-VCH.
  12. Jarolim, K. L., McCosh, J. K., Howard, M. J. & John, D. T. ( 2000; ). A light microscopy study of the migration of N. fowleri from the nasal submucosa to the central nervous system during the early stage of primary amebic meningoencephalitis in mice. J Parasitol 86, 50–55.[CrossRef]
    [Google Scholar]
  13. Jarolim, K. L., McCosh, J. K. & Howard, M. J. ( 2002; ). The role of blood vessels and lungs in the dissemination of Naegleria fowleri following intranasal inoculation in mice. Folia Parasitol (Praha) 49, 183–188.[CrossRef]
    [Google Scholar]
  14. John, D. T. & Nussbaum, S. L. ( 1983; ). Naegleria fowleri infection acquired by mice through swimming in amebae-contaminated water. J Parasitol 69, 871–874.[CrossRef]
    [Google Scholar]
  15. Kim, S. H., Smith, C. J. & Van Eldik, L. J. ( 2004; ). Importance of MAPK pathways for microglial proinflammatory cytokine IL-1β production. Neurobiol Aging 25, 431–439.[CrossRef]
    [Google Scholar]
  16. Kim, S., Schein, A. J. & Nadel, J. A. ( 2005; ). E-cadherin promotes EGFR-mediated cell differentiation and MUC5AC mucin expression in cultured human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 289, L1049–L1060.[CrossRef]
    [Google Scholar]
  17. Marciano-Cabral, F. & Cabral, G. A. ( 2007; ). The immune response to Naegleria fowleri amoeba and pathogenesis of infection. FEMS Immunol Med Microbiol 51, 243–259.
    [Google Scholar]
  18. Nakanaga, T., Nadel, J. A., Ueki, I. F., Koff, J. L. & Shao, M. X. ( 2007; ). Regulation of interleukin 8 via an airway epithelial signaling cascade. Am J Physiol Lung Cell Mol Physiol 292, L1289–L1296.[CrossRef]
    [Google Scholar]
  19. Rojas-Hernández, S., Jarillo-Luna, A., Rodríguez-Monroy, M., Moreno-Fierros, L. & Campos-Rodríguez, R. ( 2004; ). Immunohistochemical characterization of the initial stages of Naegleria fowleri meningoencephalitis in mice. Parasitol Res 94, 31–36.
    [Google Scholar]
  20. Rose, M. C., Nickola, T. J. & Voynow, J. A. ( 2001; ). Airway mucus obstruction: mucin glycoproteins, MUC gene regulation and goblet cell hyperplasia. Am J Respir Cell Mol Biol 25, 533–537.[CrossRef]
    [Google Scholar]
  21. Rowan-Kelly, B., Ferrante, A. & Thong, Y. H. ( 1980; ). Activation of complement by Naegleria. Trans R Soc Trop Med Hyg 74, 333–336.[CrossRef]
    [Google Scholar]
  22. Schuster, F. L. & Visvesvara, G. S. ( 2004; ). Free-living amoeba as opportunistic and non-opportunistic pathogens of humans and animals. Int J Parasitol 34, 1001–1027.[CrossRef]
    [Google Scholar]
  23. Serrano-Luna, J., Cervantes-Sandoval, I., Tsutsumi, V. & Shibayama, M. ( 2007; ). Biochemical comparison of proteases from pathogenic Naegleria fowleri and non-pathogenic Naegleria gruberi. J Eukaryot Microbiol 54, 411–417.[CrossRef]
    [Google Scholar]
  24. Shao, M. X. & Nadel, J. A. ( 2005; ). Neutrophil elastase induces MUC5AC mucin production in human airway epithelial cells via a cascade involving protein kinase C, reactive oxygen species, and TNF-α-converting enzyme. J Immunol 175, 4009–4016.[CrossRef]
    [Google Scholar]
  25. Shao, M. X., Ueki, I. F. & Nadel, J. A. ( 2003; ). Tumor necrosis factor α-converting enzyme mediates MUC5AC mucin expression in cultured human airway epithelial cells. Proc Natl Acad Sci U S A 100, 11618–11623.[CrossRef]
    [Google Scholar]
  26. Shimizu, T., Shimizu, S., Hattori, R. & Majima, Y. ( 2003; ). A mechanism of antigen-induced goblet cell degranulation in the nasal epithelium of sensitized rats. J Allergy Clin Immunol 112, 119–125.[CrossRef]
    [Google Scholar]
  27. Smirnova, M. G., Guo, L., Birchall, J. P. & Pearson, J. P. ( 2003; ). LPS up-regulates mucin and cytokine mRNA expression and stimulates mucin and cytokine secretion in goblet cells. Cell Immunol 221, 42–49.[CrossRef]
    [Google Scholar]
  28. Takeyama, K., Dabbagh, K., Lee, H. M., Agustí, C., Lausier, J. A., Ueki, I. F., Grattan, K. M. & Nadel, J. A. ( 1999; ). Epidermal growth factor system regulates mucin production in airways. Proc Natl Acad Sci U S A 96, 3081–3086.[CrossRef]
    [Google Scholar]
  29. Takeyama, K., Dabbagh, K., Shim, J. J., Dao-Pick, T., Ueki, I. F. & Nadel, J. A. ( 2000; ). Oxidative stress causes mucin synthesis via transcription of epidermal growth factor receptor: role of neutrophils. J Immunol 164, 1546–1552.[CrossRef]
    [Google Scholar]
  30. Teruya, H., Higa, F., Akamine, M., Ishikawa, C., Okudaira, T., Tomimori, K., Mukaida, N., Tateyama, M., Heuner, K. & other authors ( 2007; ). Mechanisms of Legionella pneumophila-induced interleukin-8 expression in human lung epithelial cells. BMC Microbiol 7, 102 [CrossRef]
    [Google Scholar]
  31. Thong, Y. H., Carter, R. F., Ferrante, A. & Kowan-Kelly, B. ( 1983; ). Site of expression of immunity to Naegleria fowleri in immunized mice. Parasite Immunol 5, 67–76.[CrossRef]
    [Google Scholar]
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