Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-17T15:26:21.021Z Has data issue: false hasContentIssue false
  • English
  • Français

The dynamics of ultrastructural changes during Entamoeba invadens encystation

Published online by Cambridge University Press:  14 July 2020

Eman Abdelazeem Abuelwafa Mousa ,
Miako Sakaguchi ,
Risa Nakamura ,
Osama Hussein Abdella ,
Hiroki Yoshida ,
Shinjiro Hamano  and
Fumika Mi-ichi Open the ORCID record for Fumika Mi-ichi [Opens in a new window]
Eman Abdelazeem Abuelwafa Mousa
Affiliation:
Department of Parasitology, Institute of Tropical Medicine (NEKKEN), Nagasaki University, 1-12-4 Sakamoto, Nagasaki852-8523, Japan Department of Medical Parasitology, Faculty of Medicine, South Valley University, Qena, Egypt
Miako Sakaguchi
Affiliation:
Central Laboratory, Institute of Tropical Medicine (NEKKEN), Nagasaki University, 1-12-4 Sakamoto, Nagasaki852-8523, Japan The Joint Usage/Research Center on Tropical Disease, Institute of Tropical Medicine (NEKKEN), Nagasaki University, 1-12-4 Sakamoto, Nagasaki852-8523, Japan
Risa Nakamura
Affiliation:
Department of Parasitology, Institute of Tropical Medicine (NEKKEN), Nagasaki University, 1-12-4 Sakamoto, Nagasaki852-8523, Japan The Joint Usage/Research Center on Tropical Disease, Institute of Tropical Medicine (NEKKEN), Nagasaki University, 1-12-4 Sakamoto, Nagasaki852-8523, Japan
Osama Hussein Abdella
Affiliation:
Department of Medical Parasitology, Faculty of Medicine, South Valley University, Qena, Egypt
Hiroki Yoshida
Affiliation:
Division of Molecular and Cellular Immunoscience, Department of Biomolecular Sciences, Faculty of Medicine, Saga University, 5-1-1 Nabeshima, Saga849-8501, Japan
Shinjiro Hamano*
Affiliation:
Department of Parasitology, Institute of Tropical Medicine (NEKKEN), Nagasaki University, 1-12-4 Sakamoto, Nagasaki852-8523, Japan The Joint Usage/Research Center on Tropical Disease, Institute of Tropical Medicine (NEKKEN), Nagasaki University, 1-12-4 Sakamoto, Nagasaki852-8523, Japan
Fumika Mi-ichi*
Affiliation:
Division of Molecular and Cellular Immunoscience, Department of Biomolecular Sciences, Faculty of Medicine, Saga University, 5-1-1 Nabeshima, Saga849-8501, Japan
*
Authors for correspondence: Fumika Mi-ichi, E-mail: [email protected], Shinjiro Hamano, E-mail: [email protected]
Authors for correspondence: Fumika Mi-ichi, E-mail: [email protected], Shinjiro Hamano, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Entamoeba histolytica infection causes amoebiasis, which is a global public health problem. The major route of infection is oral ingestion of E. histolytica cysts, cysts being the sole form responsible for host-to-host transmission. Cysts are produced by cell differentiation from proliferative trophozoites in a process termed ‘encystation’. Therefore, encystation is an important process from a medical as well as a biological perspective. Previous electron microscopy studies have shown the ultrastructure of precysts and mature cysts; however, the dynamics of ultrastructural changes during encystation were ambiguous. Here, we analysed a series of Entamoeba invadens encysting cells by transmission electron microscopy. Entamoeba invadens is a model for encystation and the cells were prepared by short interval time course sampling from in vitro encystation-inducing cultures. We related sampled cells to stage conversion, which was monitored in the overall population by flow cytometry. The present approach revealed the dynamics of ultrastructure changes during E. invadens encystation. Importantly, the results indicate a functional linkage of processes that are crucial in encystation, such as glycogen accumulation and cyst wall formation. Hence, this study provides a reference for studying sequential molecular events during Entamoeba encystation.

Keywords

Cell differentiationdormancyinfectious diseaseprotozoan parasite
Type
Research Article
Information
Parasitology , Volume 147 , Issue 12 , October 2020 , pp. 1305 - 1312
Check for updates
Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

These authors contributed equally to this work.

References

Aguilar-Díaz, H, Díaz-Gallardo, M, Laclette, JP and Carrero, JC (2010) In vitro induction of Entamoeba histolytica cyst-like structures from trophozoites. PLoS Neglected Tropical Diseases 4, e607.CrossRefGoogle ScholarPubMed
Aguilar-Díaz, H, Laclette, JP and Carrero, JC (2013) Silencing of Entamoeba histolytica glucosamine 6-phosphate isomerase by RNA interference inhibits the formation of cyst-like structures. Biomed Research International 2013, 758341.CrossRefGoogle ScholarPubMed
Baba, M, Takeshige, K, Baba, N and Ohsumi, Y (1994) Ultrastructural analysis of the autophagic process in yeast: detection of autophagosomes and their characterization. Journal of Cell Biology 124, 903–913.CrossRefGoogle ScholarPubMed
Barker, DC and Deutsch, K (1958) The chromatoid body of Entamoeba invadens. Experimental Cell Research 15, 604–610.CrossRefGoogle ScholarPubMed
Barker, DC and Svihla, G (1964) Localization of cytoplasmic nucleic acid during growth and encystment of Entamoeba invadens. Journal of Cell Biology 20, 389–398.CrossRefGoogle ScholarPubMed
Campos-Gongora, E, Viader-Salvado, JM, Martinez-Rodriguez, HG, Zuniga-Charles, MA, Galindo, JM and Said-Fernandez, S (2000) Mg, Mn, and Co ions enhance the formation of Entamoeba histolytica cyst-like structures resistant to sodium dodecyl sulfate. Archives of Medical Research 31, 162–168.CrossRefGoogle ScholarPubMed
Chatterjee, A, Ghosh, SK, Jang, K, Bullitt, E, Moore, L, Robbins, PW and Samuelson, J (2009) Evidence for a ‘wattle and daub’ model of the cyst wall of Entamoeba. PLoS Pathogens 5, e1000498.CrossRefGoogle ScholarPubMed
Chavez-Munguia, B and Martinez-Palomo, A (2011) High-resolution electron microscopical study of cyst walls of Entamoeba spp. Journal of Eukaryotic Microbiology 58, 480–486.CrossRefGoogle Scholar
Chavez-Munguia, B, Cristobal-Ramos, AR, Gonzalez-Robles, A, Tsutsumi, V and Martinez-Palomo, A (2003) Ultrastructural study of Entamoeba invadens encystation and excystation. Journal of Submicroscopic Cytology and Pathology 35, 235–243.Google ScholarPubMed
Chavez-Munguia, B, Omana-Molina, M, Gonzalez-Lazaro, M, Gonzalez-Robles, A, Cedillo-Rivera, R, Bonilla, P and Martinez-Palomo, A (2007) Ultrastructure of cyst differentiation in parasitic protozoa. Parasitology Research 100, 1169–1175.CrossRefGoogle ScholarPubMed
Deutsch, K and Zaman, V (1959) An electron microscopic study of Entamoeba invadens Rodhain 1934. Experimental Cell Research 17, 310–319.CrossRefGoogle ScholarPubMed
Eichinger, D (1997) Encystation of Entamoeba parasites. Bioessays 19, 633–639.CrossRefGoogle ScholarPubMed
Gonzalez-Salazar, F, Viader-Salvado, JM, Martinez-Rodriguez, HG, Campos-Gongora, E, Mata-Cardenas, BD and Said-Fernandez, S (2000) Identification of seven chemical factors that favor high-quality Entamoeba histolytica cyst-like structure formation under axenic conditions. Archives of Medical Research 31, S192–S193.CrossRefGoogle ScholarPubMed
Ludvik, J and Shipstone, AC (1970) The ultrastructure of Entamoeba histolytica. Bulletin of the World Health Organization 43, 301–308.Google ScholarPubMed
Manna, D and Singh, U (2019) Nuclear factor Y (NF-Y) modulates encystation in Entamoeba via stage-specific expression of the NF-YB and NF-YC subunits. mBio 10, e00737-19.CrossRefGoogle ScholarPubMed
Mi-ichi, F, Yoshida, H and Hamano, S (2016) Entamoeba encystation: new targets to prevent the transmission of amoebiasis. PLoS Pathogens 12, e1005845.CrossRefGoogle Scholar
Mi-Ichi, F, Miyake, Y, Tam, VK and Yoshida, H (2018) A flow cytometry method for dissecting the cell differentiation process of Entamoeba encystation. Frontiers in cellular and infection microbiology 8, 250.CrossRefGoogle ScholarPubMed
Mitra, BN, Pradel, G, Frevert, U and Eichinger, D (2010) Compounds of the upper gastrointestinal tract induce rapid and efficient excystation of Entamoeba invadens. International Journal for Parasitology 40, 751–760.CrossRefGoogle ScholarPubMed
Osada, M (1959) Electron-microscopic studies on protozoa I. Fine structure of Entamoeba histolytica. Keio Journal of Medicine 8, 99–103.CrossRefGoogle Scholar
Picazarri, K, Nakada-Tsukui, K and Nozaki, T (2008) Autophagy during proliferation and encystation in the protozoan parasite Entamoeba invadens. Infection and Immunity 76, 278–288.CrossRefGoogle ScholarPubMed
Picazarri, K, Nakada-Tsukui, K, Tsuboi, K, Miyamoto, E, Watanabe, N, Kawakami, E and Nozaki, T (2015) Atg8 is involved in endosomal and phagosomal acidification in the parasitic protist Entamoeba histolytica. Cellular Microbiology 17, 1510–1522.CrossRefGoogle ScholarPubMed
Proctor, EM and Gregory, MA (1972) The ultrastructure of axenically cultivated trophozoites of Entamoeba histolytica with particular reference to an observed variation in structural pattern. Annals of Tropical Medicine & Parasitology 66, 335–338.CrossRefGoogle Scholar
Proctor, EM and Gregory, MA (1973) Ultrastructure of cysts of E. histolytica. International Journal for Parasitology 3, 455–456.CrossRefGoogle ScholarPubMed
Quach, J, St-Pierre, J and Chadee, K (2014) The future for vaccine development against Entamoeba histolytica. Human Vaccines & Immunotherapeutics 10, 1514–1521.CrossRefGoogle ScholarPubMed
Ralston, KS and Petri, WA (2011) The ways of a killer: how does Entamoeba histolytica elicit host cell death? Essays in Biochemistry 51, 193–210.Google ScholarPubMed
Said-Fernandez, S, Campos-Gongora, E, Gonzalez-Salazar, F, Martinez-Rodriguez, HG, Vargas-Villarreal, J and Viader-Salvado, JM (2001) Mg2+, Mn2+, and Co2+ stimulate Entamoeba histolytica to produce chitin-like material. Journal of Parasitology 87, 919–923.Google ScholarPubMed
Saito-Nakano, Y, Yasuda, T, Nakada-Tsukui, K, Leippe, M and Nozaki, T (2004) Rab5-associated vacuoles play a unique role in phagocytosis of the enteric protozoan parasite Entamoeba histolytica. Journal of Biological Chemistry 279, 49497–49507.CrossRefGoogle ScholarPubMed
Samanta, SK and Ghosh, SK (2012) The chitin biosynthesis pathway in Entamoeba and the role of glucosamine-6-P isomerase by RNA interference. Molecular and Biochemical Parasitology 186, 60–68.CrossRefGoogle ScholarPubMed
Samuelson, J, Bushkin, GG, Chatterjee, A and Robbins, PW (2013) Strategies to discover the structural components of cyst and oocyst walls. Eukaryotic Cell 12, 1578–1587.CrossRefGoogle ScholarPubMed
Siddiqui, WA and Rudzinska, MA (1963) A helical structure in ribonucleoprotein bodies of Entamoeba invadens. Nature 200, 74–75.CrossRefGoogle ScholarPubMed
Suresh, S, Ehrenkaufer, G, Zhang, H and Singh, U (2016) Development of RNA interference trigger-mediated gene silencing in Entamoeba invadens. Infection and Immunity 84, 964–975.CrossRefGoogle ScholarPubMed
Tanyuksel, M and Petri, WA Jr (2003) Laboratory diagnosis of amoebiasis. Clinical Microbiology Reviews 16, 713–729.CrossRefGoogle Scholar
Watanabe, K and Petri, WA Jr (2015) Molecular biology research to benefit patients with Entamoeba histolytica infection. Molecular Microbiology 98, 208–217.CrossRefGoogle ScholarPubMed
Wright, R (2000) Transmission electron microscopy of yeast. Microscopy Research and Technique 51, 496–510.3.0.CO;2-9>CrossRefGoogle ScholarPubMed
Zulfiqar, H, Mathew, G and Horrall, S (2020) Amebiasis. In Horrall, S (ed.), StatPearls. Treasure Island, FL: StatPearls Publishing LLC.Google ScholarPubMed
Supplementary material: File

Mousa et al. supplementary material

Mousa et al. supplementary material 1

Download Mousa et al. supplementary material(File)
File 15.3 KB
Supplementary material: Image

Mousa et al. supplementary material

Mousa et al. supplementary material 2

Download Mousa et al. supplementary material(Image)
Image 1.3 MB