Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
권호 표지
DOI QR코드

DOI QR Code

Contact-Independent Cell Death of Human Microglial Cells due to Pathogenic Naegleria fowleri Trophozoites

  • Kim, Jong-Hyun (Department of Microbiology, and Department of Molecular Science & Technology, Ajou University School of Medicine) ;
  • Kim, Dae-Sik (Department of Clinical Laboratory Science, Dongnam Health College) ;
  • Shin, Ho-Joon (Department of Microbiology, and Department of Molecular Science & Technology, Ajou University School of Medicine)
  • Published : 2008.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Free-living Naegleria fowleri leads to a fatal infection known as primary amebic meningoencephalitis in humans. Previously, the target cell death could be induced by phagocytic activity of N. fowleri as a contact-dependent mechanism. However, in this study we investigated the target cell death under a non-contact system using a tissue-culture insert. The human microglial cells, U87MG cells, co-cultured with N. fowleri trophozoites for 30 min in a non-contact system showed morphological changes such as the cell membrane destruction and a reduction in the number. By fluorescence-activated cell sorter (FACS) analysis, U87MG cells co-cultured with N. fowleri trophozoites in a non-contact system showed a significant increase of apoptotic cells (16%) in comparison with that of the control or N. fowleri lysate. When U87MG cells were co-cultured with N. fowleri trophozoites in a non-contact system for 30 min, 2 hr, and 4 hr, the cytotoxicity of amebae against target cells was 40.5, 44.2, and 45.6%, respectively. By contrast, the cytotoxicity of non-pathogenic N. gruberi trophozoites was 10.2, 12.4, and 13.2%, respectively. These results suggest that the molecules released from N. fowleri in a contact-independent manner as well as phagocytosis in a contact-dependent manner may induce the host cell death.

Keywords

References

  1. Carter RF. Description of a Naegleria species isolated from two cases of primary amoebic meningoencephalitis and of the experimental pathological changes induced by it. J Pathol 1970; 100:217-244 https://doi.org/10.1002/path.1711000402
  2. Schuster FL, Visvesvara GS. Free-living amebaee as opportunistic and non-opportunistic pathogens of humans and animals. Int J Parasitol 2004; 34: 1001-1027 https://doi.org/10.1016/j.ijpara.2004.06.004
  3. Carter RF. Primary amoebic meningoencephalitis: clinical, pathological and epidemiological features of six fatal cases. J Pathol Bacteriol 1968; 96: 1-25 https://doi.org/10.1002/path.1700960102
  4. Anderson K, Jamieson A. Primary amoebic meningoencephalitis. Lancet 1972; 19: 379 https://doi.org/10.1016/S0140-6736(02)95185-8
  5. Apley J, Clarke SK, Roome AP, Sandry SA, Saygi G, Silk B, Warhurst DC. Primary amoebic meningoencephalitis in Britain. Br Med J 1970; 7: 596-599
  6. Shin HJ, Im KI. Pathogenic free-living amebaee in Korea. Korean J Parasitol 2004; 42: 93-119 https://doi.org/10.3347/kjp.2004.42.3.93
  7. De Jonckheere JF. Growth characteristics, cytopathic effect in cell culture, and virulence in mice of 36 type strains belonging to 19 different Acanthamebae spp. Appl Environ Microbiol 1980; 39: 681-685
  8. Shin HJ, Cho MS, Jung SY, Kim HI, Park S, Seo JH, Yoo JC, Im KI. Cytopathic changes in rat microglial cells induced by pathogenic Acanthamebae culbertsoni: morphology and cytokine release. Clin Diagn Lab Immunol 2001; 8: 837-840
  9. Han KL, Lee HJ, Shin MH, Shin HJ, Im KI, Park SJ. The involvement of an integrin-like protein and protein kinase C in amoebic adhesion to fibronectin and amoebic cytotoxicity. Parasitol Res 2004; 94: 53-60
  10. Marciano-Cabral F, John DT. Cytopathogenicity of Naegleria fowleri for rat neuroblastoma cell cultures: scanning electron microscopy study. Infect Immun 1983; 40: 1214-1217
  11. Shin HJ, Cho MS, Jung SY, Kim HI, Park S, Kim HJ, Im KI. Molecular cloning and characterization of a gene encoding a 13.1 kDa antigenic protein of Naegleria fowleri. J Eukaryot Microbiol 2001;48: 713-717 https://doi.org/10.1111/j.1550-7408.2001.tb00211.x
  12. Kang SY, Song KJ, Jeong SR, Kim JH, Park S, Kim K, Kwon MS, Shin HJ. Role of the Nfa1 protein in pathogenic Naegleria fowleri co-cultured with CHO target cells. Clin Diagn Lab Immunol 2005; 12: 873-876
  13. Jeong SR, Kang SY, Lee SC, Song KJ, Im KI, Shin HJ. Decreasing effect of an anti-Nfa1 polyclonal antibody on the in vitro cytotoxicity of pathogenic Naegleria fowleri. Korean J Parasitol 2004; 42: 35-40 https://doi.org/10.3347/kjp.2004.42.1.35
  14. Oh YH, Jeong SR, Kim JH, Song KJ, Kim K, Park S, Sohn S, Shin HJ. Cytopathic changes and pro-inflammatory cytokines induced by Naegleria fowleri trophozoites in rat microglial cells and protective effect of an anti-Nfa1 antibody. Parasite Immunol 2005; 27: 453-459 https://doi.org/10.1111/j.1365-3024.2005.00799.x
  15. Song KJ, Song KH, Kim JH, Sohn HJ, Lee YJ, Park CE, Shin HJ. Heat shock protein 70 of Naegleria fowleri is important factor for proliferation and in vitro cytotoxicity. Parasitol Res 2008; 103: 313-317 https://doi.org/10.1007/s00436-008-0972-x
  16. Willaert E. Isolement et culture in vitro des amibes de genre Naegleria. Ann Soc Belg Med Trop 1971; 51: 701-708
  17. De Jonckheere JF. A group I intron in the SSUrDNA of some Naegleria spp. demonstrated by polymerase chain reaction amplification. J Euk Microbiol 1993; 40: 179-187 https://doi.org/10.1111/j.1550-7408.1993.tb04901.x
  18. Huston CD, Houpt ER, Mann BJ, Hahn CS, Petri WA. Caspase 3-dependent killing of host cells by the parasite Entamebae histolytica. Cell Microbiol 2000; 2: 617-625 https://doi.org/10.1046/j.1462-5822.2000.00085.x
  19. Lightowlers MW, Rickard MD. Excretory-secretory products of helminth parasites: effects on host immune responses. Parasitology 1988; 96: S123-S166 https://doi.org/10.1017/S0031182000086017
  20. Feldman MR. Naegleria fowleri: Fine structural localizaion of acid phosphatase and heme proteins. Exp Parasitol 1977; 41: 290-306 https://doi.org/10.1016/0014-4894(77)90102-3
  21. Moore MB, Ubelaker JE, Marin JH, Silvany R, Dougherty JM, Meyer DR, McCulley JP. In vitro penetration of human corneal epithelium by Acanthamebae castellanii: a scanning and transmission electron microscopy study. Cornea 1991; 10: 291-298 https://doi.org/10.1097/00003226-199107000-00003
  22. Ferrante A, Bates EJ. Elastase in the pathogenic free-living amebae Naegleria and Acanthamebae spp. Infect Immun 1988; 56: 3320-3321
  23. Khan NA, Jarrol EL, Panjwani N, Cao Z, Paget TA. Proteases as markers for differentiation of pathogenic and non-pathogenic species of Acanthamebae. J Clin Microbiol 2000; 43: 391-395

Cited by

  1. Immunodominant antigens in Naegleria fowleri excretory-secretory proteins were potential pathogenic factors vol.105, pp.6, 2009, https://doi.org/10.1007/s00436-009-1610-y
  2. Screening of Swiss hot spring resorts for potentially pathogenic free-living amoebae vol.126, pp.1, 2008, https://doi.org/10.1016/j.exppara.2009.12.008
  3. Naegleria fowleri Lysate Induces Strong Cytopathic Effects and Pro-inflammatory Cytokine Release in Rat Microglial Cells vol.49, pp.3, 2008, https://doi.org/10.3347/kjp.2011.49.3.285
  4. Novel cathepsin B and cathepsin B-like cysteine protease of Naegleria fowleri excretory-secretory proteins and their biochemical properties vol.113, pp.8, 2008, https://doi.org/10.1007/s00436-014-3936-3
  5. NLRP3 Inflammasome Activation in THP-1 Target Cells Triggered by Pathogenic Naegleria fowleri vol.84, pp.9, 2008, https://doi.org/10.1128/iai.00275-16
  6. Naegleria fowleri after 50 years: is it a neglected pathogen? vol.65, pp.9, 2016, https://doi.org/10.1099/jmm.0.000303
  7. Amphotericin B induces apoptosis-like programmed cell death in Naegleria fowleri and Naegleria gruberi vol.163, pp.7, 2017, https://doi.org/10.1099/mic.0.000500
  8. Surveillance of Acanthamoeba spp. and Naegleria fowleri in environmental water by using the duplex real-time PCR vol.54, pp.2, 2018, https://doi.org/10.7845/kjm.2018.8012
  9. Cytopathic Change and Inflammatory Response of Human Corneal Epithelial Cells Induced by Acanthamoeba castellanii Trophozoites and Cysts vol.57, pp.3, 2008, https://doi.org/10.3347/kjp.2019.57.3.217
  10. Cellular characterization of actin gene concerned with contact‐dependent mechanisms in Naegleria fowleri vol.41, pp.8, 2008, https://doi.org/10.1111/pim.12631
  11. In Vitro Activity of Statins against Naegleria fowleri vol.8, pp.3, 2008, https://doi.org/10.3390/pathogens8030122
  12. Fowlerstefin, a cysteine protease inhibitor of Naegleria fowleri , induces inflammatory responses in BV-2 microglial cells in vitro vol.13, pp.1, 2008, https://doi.org/10.1186/s13071-020-3909-6
  13. Differential Exoproteome and Biochemical Characterisation of Neoparamoeba perurans vol.9, pp.6, 2021, https://doi.org/10.3390/microorganisms9061258
  14. Naegleria fowleri Induces Jurkat T Cell Death via O-deGlcNAcylation vol.59, pp.5, 2008, https://doi.org/10.3347/kjp.2021.59.5.501