Parasites, Hosts and Diseases

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

DOI QR Code

Phagocytosis-associated genes in Acanthamoeba castellanii feeding on Escherichia coli

  • Min-Jeong Kim (Department of Biomedical Science, Graduate School, Kyung Hee University) ;
  • Eun-Kyung Moon (Department of Medical Zoology, Kyung Hee University School of Medicine) ;
  • Hye-Jeong Jo (Department of Biomedical Science, Graduate School, Kyung Hee University) ;
  • Fu-Shi Quan (Department of Medical Zoology, Kyung Hee University School of Medicine) ;
  • Hyun-Hee Kong (Department of Parasitology, Dong-A University College of Medicine)
  • Received : 2023.08.17
  • Accepted : 2023.10.09
  • Published : 2023.11.30
Download PDF
⟨ Previous Next ⟩

Abstract

Acanthamoeba species are free-living amoebae those are widely distributed in the environment. They feed on various microorganisms, including bacteria, fungi, and algae. Although majority of the microbes phagocytosed by Acanthamoeba spp. are digested, some pathogenic bacteria thrive within them. Here, we identified the roles of 3 phagocytosis-associated genes (ACA1_077100, ACA1_175060, and AFD36229.1) in A. castellanii. These 3 genes were upregulated after the ingestion of Escherichia coli. However, after the ingestion of Legionella pneumophila, the expression of these 3 genes was not altered after the consumption of L. pneumophila. Furthermore, A. castellanii transfected with small interfering RNS (siRNA) targeting the 3 phagocytosis-associated genes failed to digest phagocytized E. coli. Silencing of ACA1_077100 disabled phagosome formation in the E. coli-ingesting A. castellanii. Alternatively, silencing of ACA1_175060 enabled phagosome formation; however, phagolysosome formation was inhibited. Moreover, suppression of AFD36229.1 expression prevented E. coli digestion and consequently led to the rupturing of A. castellanii. Our results demonstrated that the ACA1_077100, ACA1_175060, and AFD36229.1 genes of Acanthamoeba played crucial roles not only in the formation of phagosome and phagolysosome but also in the digestion of E. coli.

Keywords

Acknowledgement

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No. 2020R1F1A1068719).

References

  1. Siddiqui R, Khan NA. Biology and pathogenesis of Acanthamoeba. Parasit Vectors 2012;5:6. https://doi.org/10.1186/1756-3305-5-6 
  2. Diehl MLN, Paes J, Rott MB. Genotype distribution of Acanthamoeba in keratitis: a systematic review. Parasitol Res 2021;120(9):3051-3063. https://doi.org/10.1007/s00436-021-07261-1 
  3. Iovieno A, Ledee DR, Miller D, Alfonso EC. Detection of bacterial endosymbionts in clinical acanthamoeba isolates. Ophthalmology 2010;117(3):445-452. https://doi.org/10.1016/j.ophtha.2009.08.033 
  4. Scheikl U, Sommer R, Kirschner A, Rameder A, Schrammel B, et al. Free-living amoebae (FLA) co-occurring with legionellae in industrial waters. Eur J Protistol 2014;50(4):422-429. https://doi.org/10.1016/j.ejop.2014.04.002 
  5. Greub G, Raoult D. Microorganisms resistant to free-living amoebae. Clin Microbiol Rev 2004;17(2):413-433. https://doi.org/10.1128/CMR.17.2.413-433.2004 
  6. Nora T, Lomma M, Gomez-Valero L, Buchrieser C. Molecular mimicry: an important virulence strategy employed by Legionella pneumophila to subvert host functions. Future Microbiol 2009;4(6):691-701. https://doi.org/10.2217/fmb.09.47 
  7. Segal G, Feldman M, Zusman T. The Icm/Dot type-IV secretion systems of Legionella pneumophila and Coxiella burnetii. FEMS Microbiol Rev 2005;29(1):65-81. https://doi.org/10.1016/j.femsre.2004.07.001 
  8. Qiu J, Luo ZQ. Effector translocation by the Legionella Dot/Icm type IV secretion system. Curr Top Microbiol Immunol 2013;376:103-115. https://doi.org/10.1007/82_2013_345 
  9. Moon EK, Kim MJ, Lee HA, Quan FS, Kong HH. Comparative analysis of differentially expressed genes in Acanthamoeba after ingestion of Legionella pneumophila and Escherichia coli. Exp Parasitol 2022;232:108188. https://doi.org/10.1016/j.exppara.2021.108188 
  10. Kim MJ, Moon EK, Jo HJ, Quan FS, Kong HH. Identifying the function of genes involved in excreted vesicle formation in Acanthamoeba castellanii containing Legionella pneumophila. Parasit Vectors 2023;16(1):215. https://doi.org/10.1186/s13071-023-05824-y 
  11. Mou Q, Leung PHM. Differential expression of virulence genes in Legionella pneumophila growing in Acanthamoeba and human monocytes. Virulence 2018;9(1):185-196. https://doi.org/10.1080/21505594.2017.1373925 
  12. Harding CR, Schroeder GN, Reynolds S, Kosta A, Collins JW, et al. Legionella pneumophila pathogenesis in the Galleria mellonella infection model. Infect Immun 2012;80(8):2780-2790. https://doi.org/10.1128/IAI.00510-12 
  13. Moon EK, Kim MJ, Lee HA, Quan FS, Kong HH. Comparative analysis of differentially expressed genes in Acanthamoeba after ingestion of Legionella pneumophila and Escherichia coli. Exp Parasitol 2022;232:108188. https://doi.org/10.1016/j.exppara.2021.108188 
  14. Lycett G. The role of Rab GTPases in cell wall metabolism. J Exp Bot 2008;59(15):4061-4074. https://doi.org/10.1093/jxb/ern255 
  15. Barr FA. Review series: Rab GTPases and membrane identity: causal or inconsequential? J Cell Biol 2013;202(2):191-199. https://doi.org/10.1083/jcb.201306010 
  16. Pamarthy S, Kulshrestha A, Katara GK, Beaman KD. The curious case of vacuolar ATPase: regulation of signaling pathways. Mol Cancer 2018;17(1):41. https://doi.org/10.1186/s12943-018-0811-3 
  17. Moon EK, Hong Y, Chung DI, Kong HH. Cysteine protease involving in autophagosomal degradation of mitochondria during encystation of Acanthamoeba. Mol Biochem Parasitol 2012;185(2):121-126. https://doi.org/10.1016/j.molbiopara.2012.07.008 
  18. Corbett Y, Parapini S, Perego F, Messina V, Delbue S, et al. Phagocytosis and activation of bone marrow-derived macrophages by Plasmodium falciparum gametocytes. Malar J 2021;20(1):81. https://doi.org/10.1186/s12936-021-03589-2